ADAPTATION TO LIFE IN THE DESERT IN THE
BROWN HARE (LEPUS CAPENSIS)
NOGA KRONFELD AND AMIRAM SHKOLNIK
Department of Zoology, Tel Aviv University, Ramat Aviv, Tel Aviv 69978, Israel
Adaptations to life in the desert were studied in brown hares (Lepus capensis) from the
Negev Desert of Israel. For comparison, brown hares from a temperate region in southern
France were included in the study. All animals sustained themselves on dry alfalfa hay.
The desert hares, however, required, on the basis of their specific metabolic weight, only
75% of the amount of food consumed by the European hares, and their digestive capacity
was superior. Resting metabolic rate of the desert hares was 61 % of the value recorded in
the European hares, and their lower critical temperature was higher. Rate of water turnover
was 124 ml kgo.82 day-I in the desert hares, only one-half of the value recorded for the
European hares. The desert hares were able to drink salt (NaCI) solutions up to a concentration of 6%. Their maximal urine concentration was 4,470 mosmol kg-I. The maximal
concentration of the salt solution consumed by the European hares was 2.5% and their
maximal urine concentration was 2,500 mosmol kg-I.
Key words:
Lepus capensis, food, digestibility, energy, urine osmolality, succulent plants
Brown hares, Lepus capensis, are distributed over a wide geographic range in Africa, Asia, and southern Europe (Corbert
and Hill, 1991; Harrison and Bates, 1991;
Myers and MacInnes, 1981; Yom-tov,
1967). Within this range, they inhabit a variety of bioclimatic regions, temperate and
humid, as well as hot and dry, including the
barren terrain of the Negev Desert of Israel,
and the Arava Valley. This stretch of extreme arid desert extends between the Dead
Sea and the Red Sea and forms part of the
Big Rift Valley. Favorable climatic conditions, with abundant green forage, prevail
in this area only during the short period that
follows the sparse and erratic winter rains;
average annual rainfall is <50 mm. In the
dry season of 8-9 months, high temperatures cause the annual vegetation to wilt
and water sources to dry up. In this season,
daily air temperature may be >40°C, relative humidity < 10%, and mean solar radiation 3,553 kJ cm- 2 day-I. Average daily
evaporation is 14 mm, twice that recorded
in the Mediterranean zone (Stem et aI.,
1986). At the end of the summer, diet of the
Journal of Mammalogy, 77(1):171-178, 1996
brown hare consists mainly of emaciated
desert shrubs, high in plant cell-wall constituents, or xerophylic succulent plants,
high in salt content.
Unlike des'ert rodents, who retreat to the
favorable conditions of their burrows during the heat of the day (Schmidt Nielsen,
1964), brown hares rest during the day in
shallow depressions only poorly shaded by
desert shrubs. Although the hares are relatively abundant in this harsh environment,
the ways this species copes with desert conditions, balances its water metabolism, and
exploits the meager low-quality forage have
hardly been studied. The present study is
aimed at exploring the brown hare's adaptation to life in the desert. For comparison,
hares from southern France, a temperate
Mediterranean area, also were studied. Although the genus Lepus is confusing taxonomically, it is widely accepted that the
species europeus and capensis are synonyms (Corbet and Hill, 1991: Corbet and
Southern; 1977: Petter, 1961). Consequently, brown hares from southern France and
the hares once called Cape hares are now
171
172
Vol. 77, No. 1
JOURNAL OF MAMMALOGY
considered to belong the same species,
Lepus capensis.
MATERIALS AND METHODS
Eleven mature brown hares (four males, seven
females) with body mass of 1.4 ± 0.1 kg (mean
± 1 SD), were captured in live traps during summer in the Arava Depression, ca. 50 km S of the
Dead Sea. Five hares (two males, three females)
were imported from southern France; they had
a body mass of 2.8 ± 0.2 kg. The hares were
housed in individual cages at 25-29°C and 4060% relative humidity, and a photoperiod of
12L: 12D. They were maintained on dry alfalfa
hay, a high-quality roughage (with 37% neutral
detergent fiber, 15.8% protein, and an energy
value of 20.37 kJ/g). Food and water were offered ad lib.
Food offered, uneaten food, and feces were
measured and sampled daily for 6 consecutive
days. The samples were dried at 90°C to constant weight and analyzed for energy content using a Gulleokamp ballistic bomb calorimeter.
Neutral detergent fiber and crude protein were
determined in Miloda Laboratories (Akko, Israel) according to the method of Goering and Van
Soest (1970).
One dose of alfalfa hay, labeled by chromium
mordant according to the method of Uden et al.
(1982), was fed to the hares before a regular
meal. Feces were collected over the 72 h that
followed the ingestion of the labeled food, at 34-h intervals. The chromium in the fecal samples was determined by atomic-absorption spectophotometry according to Williams et ai.
(1962). Mean retention time of particulate matter
in the digestive tract was calculated according
to the equation of Faichney (1975).
Oxygen consumption was measured in an
open-circuit system (Hill, 1972) at ambient
temperaturs of 12-35°C. Oxygen concentrations in the air flowing (at a rate of 6-8 1
min-I) through the metabolic chamber (30 by
45 by 50 cm) were determined by a paramagnetic Servomax Taylor O 2 analyzer. The system
was calibrated by the one-step, N 2-dilution
technique (Fedak et aI., 1981). Prior to the l-h
recording time, 2 h were allowed for the equilibration of the system and for the animals to
relax in the chamber.
Rates of water turnover were calculated from
the disappearance rates of tritiated water injected intramuscularly into the animals (0.5
mCi in 0.5 ml saline). Total body water was
calculated from the dilution of the marker.
Blood plasma was sampled 5 h after the injection of the marker (when, according to preliminary measurements, the distribution of the
marker is complete) and again every 2nd day
for the next 6 days. Tritium activity in the plasma samples was determined in a Packard
PriCard 4530 scintillation counter.
The capacity to use salt solution for drinking
was studied by offering hares NaCI solutions at
progressively increasing concentrations (starting
with 0.5%) in place of drinking water. To increase the animal's demand for drinking, the
regular diet was supplemented by soybean cakes
(50% protein). The maintenance of constant
body mass was the criterion for the animal's
ability to balance its water metabolism while
drinking NaCI solutions. Five urine samples
were collected from each hare during the period
of maximal electrolyte loading. Osmotic concentration of urine was determined by a Vescor
(5500) vapor-pressure osmometer.
Relative medullary thickness (RMT) was assessed according to Sperber (1944); RMT =
medullary thickness/(product of the three dimensions of the kidney)113 in kidneys of animals that
had died in the field or accidentally during the
experiments (n = 3 for European hares, n = 6
for desert hares).
Results are presented as mean ± 1 SD. A (test was used to assess the differences between
the two groups of animals. Critical points and
slopes of regression lines were determined according to Nickerson et al. (1989).
RESULTS
On a diet consisting solely of roughage
(dry alfalfa hay), with water ad lib., hares
from both the desert and the temperate region maintained a constant body mass. Desert hares consumed significantly less food
than European hares (Fig. O. On the basis
of specific metabolic body mass, desert
hares consumed 75% the amount consumed
by the European hares. Digestibility of dry
matter in desert hares was 80% and in European hares 72% (Fig. 1). Digestibility of
plant fiber was 51 % in desert hares and
43% in European hares. The mean retention
time of the digesta was similar in the two
popUlations (15.5 :!:: 3.5 in desert hares and
February 1996
KRONFELD AND SHKOLNIK-BROWN HARES IN A DESERT ENVIRONMENT
173
100.-------------------------------------~
o
o
digested
infeces
80-
60
40-
720/0
20
O~--~--------._I------~--------~-------r-I-------L--~
Desert hares
European hares
FIG. l.-Weight-specific amounts of food eaten, showing portion digested and portion remaining
in the feces, in desert hares and European hares fed alfalfa hay. Amounts are expressed as weightspecific amounts of dry matter. Percentage figures in the bars indicate the level of digestibility of
dry matter.
14.1 ± 1.2 in European hares) in spite of a
two-fold difference in their body mass.
The rate of oxygen consumption at rest
under thermoneutral conditions was 0.375 ±
0.048 ml g-l h- 1 in desert hares and 0.54 ±
0.071 ml g-l h- 1 in European hares (Fig. 2).
On the basis of specific metabolic mass, the
thermoneutral resting metabolic rate calculated from the rates of oxygen consumption
was 39% lower in desert hares than in European hares. The lower critical point in desert hares was 24°C ambient, but in European
hares no increase in oxygen consumption
was detected, even when ambient temperature was lowered to 12°C (Fig. 2).
The rate of water turnover of desert hares
was significantly lower (P < 0.01) than the
rate of water turnover of European hares
(124.7 ± 7.9 and 336.8 ± 22.9 ml day-l
Bm- O•82 respectively, where Bm = body
mass). The biological half-life of tritium in
desert hares was 5.15 days, twice the value
found in hares from the temperate zone
(Fig. 3).
On a diet of dry alfalfa hay supplemented
by soy cake, desert hares maintained their
body mass constant even when drinking 6%
NaCl. Hares from the temperate region lost
body mass when the concentration of their
drinking solution was increased to 2.5%
NaCI (Table 1). Maximum urine concentration and average maximal concentration in
desert hares (n = 6) were both significantly
higher than in European hares (n = 3; Table
1). The average relative medullary thickness in the desert popUlation also was significantly higher than that of European
hares (Table 1).
JOURNAL OF MAMMALOGY
174
1.2
1.0
0 ....•
Desert hares
o-
European hares
Vol. 77, No.1
00 [J
0.8
o
"0.. •••••
0
EI
0.6
o
o
o
0
'o"S
0
00 0
'"
'.
o
0.4
o
·s·····. ··••••.••
o
0
0
0
'.
0
,l
oog/oO
~
······l:!t;!.. e ... 'O' .......
o
0.2
12
14
16
18
20
22
24
26
28
30
32
34
36
Air temperature (oC)
FIG. 2.-Oxygen consumption of resting hares exposed to a range of air temperatures.
DISCUSSION
Compatible with data presented for other
desert herbivorous mammals (Shkolnik,
1988), the maintenance requirement of food
of the desert brown hare is frugal, and food
is digested efficiently (Fig. 1). The efficiency at which roughage, high in plant cellwall constituents, is digested often is related
to the time digesta is retained in the alimentary tract (mean retention time) and
subjected to bacterial degradation. Based on
allometric considerations (ratio of capacity
of alimentary tract to consumption of food).
Demment and Van Soest (1985) have argued that mean retention time is expected
to be shorter, and consequently digestibility
of food inferior, in a small herbivore than
in one of a larger body mass. They have
further argued that by being limited in their
digestive capacities, herbivores of small
body size are, as a rule, restricted in their
food preferences to forages high in readily
digested constituents. In the present study,
hares from both population were nonetheless capable of sustaining themselves on a
high-fiber diet (alfalfa hay). A spacious
hind gut, as well as cecotropy, apparently
lend this capacity to lagomorphs in general
(Stevens, 1988). Despite the body mass of
the desert hare being one-half that of the
European one, the mean retention time of
the digesta in its alimentary tract was equal
to that recorded in the European hare. Furthermore, the desert hare digested the highfiber plant material more efficiently and, on
both a mass-specific basis and a metabolic
one, it required less food. Presumably, factors other than body size therefore, are, involved in determining the time digesta are
retained in the alimentary tract of a desert
herbivore. The low intake of food (dry matter) demonstrated in the desert hare is one
February 1996
KRONFELD AND SHKOLNIK-BROWN HARES IN A DESERT ENVIRONMENT
175
115
/""'.
~
110
D Desert hares
105
o European hares
'-"
~
0
'.0
100
C\l
.J:j
95
53
90
u
~
0
U
[)
~
~
'1:j
WTO=124 ml kg 0.82 d- 1
85
80
75
Q)
~
'.0
.....
~
70
65
60
55
50
0
100
150
200
Time (h)
FrG. 3.-Rate of water turnover (WTO), based on rate of disappearance of tritiated water in desert
hares and European hares.
explanation for the extended time the digesta are retained in these animals. It has
been suggested (Brosh et aI., 1986) that an
economic water metabolism is also a factor
improving digestibility. A reduced flow of
fluid in the alimentary tract is likely to slow
down the rate at which the small particulate
matter is carried out with the flow, thus,
resulting in an extended retention time.
Digestive capacities found in hares from
the Negev Desert exceed not only the capacities found in their relatives from southern Europe, but also those reported for the
black-tailed jackrabbit (L. califomicus) that
dwells in the Mojave Desert (Shoemaker et
aI., 1976). It is suggested that the capacity
to digest roughages efficiently helps the
desert hares of the Negev to economize
TABLE I.-Relative medullary thickness, urine osmolality (maximal value in each population, and
average (±1 SE) of the maximal values of all individuals) and maximal concentration of NaCI
solutions tolerated by desert hares and European hares.
Population
Desert
Temperate
P
Relative medullary
thickness
Maximal urine
concentration
(mosmol kg-I)
Average urine
concentration
mosmol kg- I
Maximal
concentration of
NaCI drinking
solution (%)
7.8 ± 0.3
5.5 ± 0.3
<0.01
4,470
2,500
<0.01
3,415 ± 450
2,230 ± 250
<0.01
6
<2.5
<0.01
176
JOURNAL OF MAMMALOGY
their food requirements and extend their
forage preferences.
In addition to an efficient digestive capacity, a low rate of energy expenditure
also may contribute to a reduction in the
amount of food an animal requires for
maintenance. The resting metabolic rate of
the European hares measured at thermoneutrality was compatible to the value expected
from its body mass according to Kleiber's
equation (1961). On the basis of metabolic
body mass, the rate of oxygen consumption
measured in desert hares was, however,
only 61 % the value measured in the European ones and 60% the value expected from
their body mass. It also was lower (by 25%)
than comparable values reported for the
jackrabbit (Hinds, 1977). Low values for
resting metabolic rate at thermoneutrality
are reported for many desert mammals
(Shkolnik, 1988), and it is suggested that
this helps these animal to conserve both energy and water.
The lower critical temperature found in
desert hares is similar to the value reported
for jackrabbits in the Sonoran Desert
(Hinds, 1977) and is far higher than in European hares. It appears that this profound
difference in the lower critical temperature
indicates that desert hares also differ greatly
in their thermal conductance from hares
that live in a temperate climate, that of desert hares being far greater than that of European ones. The significance of a high
core-to-environment thermal conductance
has been extensively highlighted as an adaptation to a hot climate (Dawson and
Schmidt-Nielsen, 1966: Scholander et aI.,
1950).
Allometric equations for rates of water
flux are given by Richmond et aI. (1962)
and Nicol (1978). The value found in desert
hares was only one-half that expected from
their body mass and similar to the rate of
water turnover reported for the jackrabbit
(Nagy, 1988). The value found for European hares was as expected from their body
mass, according to these equations. In the
arid Negev Desert, where drinking water is
Vol. 77, No.1
virtually unavailable, the ability to balance
such a frugal water economy to the extent
found in the hare population is still enigmatic.
The only source of appreciable amounts
of water during the prolonged dry Negev
summer are the succulent plants that contain sap with high concentrations of electrolytes. Field observation indicates that,
during the dry season, hares in the Negev
clearly prefer such plants.
The ability to use the sap of succulent
desert plants as a water source depends primarily on the power of the kidney to excrete the excessive electrolytes dissolved in
the sap. In many mammals, a correlation
has been demonstrated between the ability
to concentrate urine and the relative length
of their renal medulla (Sperber, 1944). The
relative medullary thickness found in Negev hares is close to that of other highly
adapted desert mammals (Shkolnik, 1988),
while the relative medullary thickness measured in the European population is within
the range reported for cats, dogs, and rats;
animals that cannot survive in the desert if
denied drinking water (Schmidt-Nielsen
and O'Dell, 1961).
Desert hares in the laboratory could use
salt solutions almost twice the osmotic concentration of sea water. The capacity to use
highly concentrated salt solution as a water
source and the ability to excrete excessive
solutes in a concentrated urine are not
shared by European hares. It is suggested
that these capacities provide desert hares
with an important source for both water and
readily available energy.
It is concluded that economic energy expenditure and frugal water metabolism
combine with physiological aptitudes, enabling the desert hare to meet its food and
water, requirement by efficiently exploiting
desert resources. These characteristics are
neither shared by hares from the temperate
region, nor are they apparently shared by
the jackrabbits from the American deserts
"that when vegetation dries out during the
summer draught ... die of dehydration, but
February 1996
KRONFELD AND SHKOLNIK-BROWN HARES IN A DESERT ENVIRONMENT
populations are replenished by explosive reproduction by survivors.. after winter
rains" (Nagy, 1993:220). No seasonal
changes were observed in the size of desert
hare populations. Furthermore, Stavy
(1976, 1987) reports that reproductive cycles in populations of the desert hare are
carried on year round, presumably unaffected by the harsh summer conditions.
While Nagy concludes that adaptation of
jackrabbits to life in the desert is related to
"opportunistic exploitation of seasonally
and spatially favorable conditions" (Nagy,
1993:220), it appears that physiological adaptations provide desert brown hares with
the capacity to cope successfully with desert conditions year round.
ACKNOWLEDGMENTS
The study was supported by the Israel Cohen
Chair in Environmental Physiology. We thank Z.
Zook-Rimon and G. Ben-Nun for their valuable
help in the field.
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Submitted 25 March 1994. Accepted 26 April 1995.
Associate Editor was Barbara H. Blake.