How Desert Rodents Overcome
Halophytic Plant Defenses
Morphologieal, behavioral, and physiological adaptations allow
certain rodents to consume saline vegetation
Michael A. Mares, Ricardo A. Ojeda, Carlos E. Borghi, Stella M. Giannoni,
Gabriela B. Diaz, and Janet K. Braun
C
onvergent evolution among
desert rodents has received a
great deal of attention in recent years, with research centering
on the question of how phylogenetically unrelated species evolving on
different continents have developed
similar morphological, behavioral,
ecological, or physiological characteristics in response to similar selective pressures posed by the desert
environment (Mares 1975, 1993a,
1993b, Schluter and Ricklefs 1993).
The he at and aridity of deserts pose
severe challenges for both plants and
animals. Deserts gene rally support
reduced levels of plant biomass compared with more mesic habitats
(Hadley and Szarek 1981, Rosenzweig
Michael A. Mares (e-mail: mamares@
ou.edu), a mammalian ecologist, taxonomist, and biogeographer, is the director of
the Oklahoma Museum of Natural History and a professor in the Department of
Zoology, University of Oklahoma,
Norman, OK 73019-0606. He studies the
ecology and distribution of mammals in
South America and the evolution of mammals in deserts around the world. Ricardo
A. Ojeda is a research biologist with the
Biodiversity Research Group at the
Instituto Argentino de Investigaciones de
las Zonas Aridas (IADIZA), Parque General San Martin, 5500, Mendoza, Argentina. He studies desert mammal ecology in
Argentina. Carlos E. Borghi, Stella M.
Giannoni, and Gabriela B. Diaz are mammal research biologists with the Biodiversity Research Group at IADIZA. Janet K.
Braun is a curator of mammals at the
Oklahoma Museum of Natural History
and studies the systematics of South American rodents. © 1997 American Institute of
Biological Sciences.
November 1997
Mammalian hair-Iong
known for its plasticity
in evolving to serve
functions as diverse
as thermoregulation,
defense, and crypsiscan function in
place of teeth
1968), and those plants that inhabit
the desert often have special adaptations for coping with aridity, heat,
and desert soils. For example, some
plants, such as cacti, store water in
their sterns to weather extended
droughts; others, such as desert
ephemerals, spend only a short period oE the year as a green plant
(perhaps only a few weeks during the
rainy season), and the rest of their
life as a seed.
Most deserts have areas where subsurface water is available throughout
much of the year or for extended periods during the rainy season (Cooke
et al. 1993, Walter and Stadelmann
1974). In deserts with enclosed basins, for example, low-Iying areas
accumulate runoff water containing
dissolved salts, especially chlorides
and sulfates. In these areas, high
insolation and evaporation have led
to the formation of soils with high
salt content (e.g., sodium chloride
and potassium chloride). As the wa-
ter evaporates, the salts remain to
form salt flats, or salinas (Figure 1),
areas that are largely devoid of vegetation (Cooke et al. 1993). Although
desert basins may have a high water
table that can be reached easily by
plant roots, the water is salty. Salt
content is highest in the soils that are
at the centers of the salinas (almost
pure salt) and decreases toward the
periphery. However, soils at the periphery also contain large amounts
of salt, and these areas pose special
challenges for plant growth. To maintain their hydric balance, plants must
overcome the negative water pressure of the salts in the soil and in the
ground water. If a plant cannot maintain a positive pressure against this
gradient, the plant will lose water to
the soil through its roots and die.
One group of plants that has been
successful worldwide in colonizing
areas of high salt concentrations is
the family Chenopodiaceae (Branson
et al. 1976, Walter and Stadelmann
1974). These halophytic (salt-Ioving) plants are able to concentrate
salt, moving it from the soil into (and
through) the plant. By increasing the
osmotic pressure in the tissues
through the accumulation of salts,
these plants are able to obtain water
from the salty soil (Branson et al.
1976, WalterandStadelmann 1974).
This mechanism allows these plants
to maintain a positive water balance
and to inhabit areas that are hostile
to most other plants.
Several genera of chenopodes are
widespread in the world's deserts.
Saltbush (Atriplex), which is among
the most salt tolerant of the halo699
Figure 1. A salt flat
(salina) in the Monte
Desert of Mendoza
Province, Argentina.
The center of the salt
flat is tao salty to support vegetation, although various plants,
especially chenopodiaceous halophytic
shrubs, grow along the
periphery.
phytes (Branson et al.
1976), is abundant in
North and South
American deserts,
Australia, and Africa
(Orians and Solbrig 1977, Smith
1977, WalterandStadelmann 1974).
A trip lex concentrates salts, especially
sodium chloride, in cells of the outer
tissues of the leaves (Ashby and
Beadle 1957, Kenagy 1972, 1973,
Mozafar et al. 1970, Wallace et al.
1973). As these cells accumulate salt,
they eventually burst, depositing
crystalline salt on the leaf surface
(Figure 2a). The salt helps to protect
the plant in several ways, including
providing a reflective coating that
shades the leaf from direct sunlight
and decreasing the palatability of
these evergreen plants to herbivores;
the sharp salt crystals may also function as a mechanical deterrent to
herbivores (Figure 2b).
Challenges of foraging
on halophytes
Desert mammals face a difficult task
in obtaining food and water in arid
habitats that are almost devoid of
vegetation. Because the water table
under salt flats is high, Atriplex maintains green, succulent leaves throughout the year (e.g., West 1983). This
halophyte, therefore, would appear
to be an ideal source of both nutrients and water for mammals. However, high salt loads are toxic to
mammals. If a mammal were to feed
on Atriplex, the increased salt intake
would overcome any water gained
from the food. T 0 maintain osmotic
balance, additional water would be
required to remove the salts through
urine or through perspiration
(Kenagy 1972, 1973, SchmidtNielsen 1964). This is why people
adrift at sea often die of thirst even
700
though they are surrounded by water. If sea water is consumed, its high
salt content (which is, however, lower
than the salt content of the fluids
contained in halophytic plants;
Schmidt-Nielsen 1964) simply places
a person in negative water balance,
requiring additional water to remove
salts from the body.
For a mammal to feed on Atriplex
it would, therefore, have to have
adaptations that allow it to cope
with the high salt content. Although
many rodents and animals throughout the world encounter Atriplex,
few have been reported to have such
adaptations. Nevertheless, so me
mammals are able to forage on
Atriplex (e.g., North American
pronghorns [Antilocapra americana],
Van Wormer 1969; pygmy rabbits
[Brachylagus idahoensis], Orr 1940).
Saline habitats generally do not have
a high diversity of mammals. If a
species could forage on Atriplex or
other halophytes, it could then colo- Figure 2. Salt deposits on the leaves of
nize these areas.
Atriplex. (a) The outer cells ofthe Atriplex
Despite the unpalatability of leaves store salt, eventually bursting and
Atriplex and other halophytes, and depositing a salt covering on the leaf surthe difficult, hot desert habitat, three face. (b) The salt crystals can grow to
species of phylogenetically unrelated impressive sizes, perhaps functioning as a
rodents (from three different families) mechanical defense against herbivory.
that are found in widely separated
deserts have managed to overcome the North Africa; and the red vizcacha
challenges of feeding on Atriplex. They rat (Tympanoctomys barrerae, famdo this by using strategies that in- ily Octodontidae) of the Monte Desert
volve morphological, behavioral, and of Argentina. In this article, we comphysiological adaptations. These spe- pare the adaptive strategies of these
cies are the chisel-toothed kangaroo three rodents, noting for the first time
rat (Dipodomys microps, family the unique combination of traits of the
Heteromyidae) of the Great Basin red vizcacha rat of Argentina.
Desert of North America; the fat
sand rat (Psammomys obesus, fam- The North American species. Among
ily Muridae) of the Sahara Desert of the most abundant, speciose mamBioScience Vol. 47 No. 10
mals in North America's deserts are
members of the rode nt family Heteromyidae (Genoways and Brown
1993), including kangaroo rats
(Dipodomys), kangaroo mice (Microdipodops), and pocket mice
(Perognathus and Chaetodipus).
Heteromyid rodents are among the
most desert specialized mammals in
the world and have managed to live
in the desert by becoming waterindependent seed specialists. They
store seeds for extended periods in
underground burrows, where the
anima I is sheltered from the vicissitudes of life in the arid desert. All
Dipodomys have highly specialized
kidneys that are able to produce very
concentrated urine, and they obtain
water from the seeds they eat (French
1993). Unlike its granivorous relatives, however, one species of kangaroo rat, Dipodomys microps, is not
water independent and is not a seed
specialist. Rather, it possesses
uniquely shaped (chisel-like) lower
incisors (Figure 3a) that allow it to
exploit a diet that, in contrast to that
of most kangaroo rats, consists
largely of Atriplex leaves. They use
their specialized lower incisors to
strip away the hypersaline outer leaf
tissues of Atriplex before eating the
inner portion of the leaf, which contains less salt (Kenagy 1972, 1973).
The chisel-toothed kangaroo rat
is a widespread species (its range
extends from southeast Oregon to
western Utah to southern California), and in some parts of its range it
exists despite an absence of Atriplex
(Csuti 1979). In areas where other
foods are available, D. microps eats
seeds and green plants. However,
when animals from these areas are
offered Atriplex leaves in the laboratory, they soon begin to feed on
them, stripping away the outer layers using their lower incisors. They
do not do this with plants other than
Atriplex. This behavior indicates
both a plasticity to the diet of the
species and a phylogenetically based
suite of adaptations that are related
to the consumption of Atriplex leaves
(Csuti 1979).
The North African species. The fat
sand rat, Psammomys obesus, of
North Africa also forages on Atriplex
(Degen 1988, Frankel et al. 1972)
and other halophytic chenopodes
November 1997
(e.g., Suaeda and Salsola; Daly and
Daly 1973). The kidneys of P. obesus
remove high salt loads from the blood
by producing an extremely concentrated urine (Abdallah and Tawfik
1969, Schmidt-Nielsen 1964). P.
obesus does not inhabit areas having
free water for drinking. It manages
to maintain hydric balance by processing the water contained in the
leaves of the halophytic plants it eats.
Like North American D. microps,
P. obesus also scrapes the salty layers of tissues from the leaves before
consuming them (Degen 1988), especially if the water content of the
leaves is reduced, as might occur
during drier times of the year. AIthough Psammomys have not been
studied extensively, it appears that
they are able to inhabit saline deserts
through a combination of specialized
renal capabilities and behavioral
mechanisms, a broadly similar strategy to that employed by Dipodomys.
The South American species. South
America was isolated from the Cretaceous (90 million years ago) until
the Plio-Pleistocene boundary (3
million years ago), when the Central
American land bridge connected the
continents of the Western Hemisphere (Mares 1985), leading to a
great interchange of fauna between
the two land masses. Before then,
South America was a huge island
where great faunal differentiation
had occurred. Among the unusual
groups of mammals that evolved were
the octodontid rodents, an endemie
family that was present as early as
the Oligocene, 24-38 million years
aga (Anderson and Jones 1984).
Today, nine species in six genera
remain. Most octodontids inhabit
the arid steppes and mountains of
southernmost South America.
In the Monte Desert (Mendoza
Province) in west-central Argentina,
the red vizcacha rat (Tympanoctomys
barrerae), arare, unusual, and monotypic octodontid, inhabits the narrow band of halophytic vegetation
that surrounds salt flats. This species
maintains elaborate mounds that rise
above the surrounding desert and
provide microhabitats that are conducive to the growth of chenopodes,
particularly Atriplex lampa, its primary food and the most abundant
plant in the area. Suaeda, a cheno-
Figure 3. Anterior view of the mandibles
and lower incisors of six species of desert
rodents. In all figures, the Atriplex specialist is on the left and the closely related nonAtriplex specialist is on the right. (a)
Dipodomys microps (Atriplex consumer)
and Dipodomys merriami (seed eater) of
North American deserts. (b) Tympanoctomys barrerae (Atriplex consumer)
and Octomys mimax (cactus and shrub
forager) of the Argentine Monte Desert.
(c) Psammomys obesus (Atriplex consumer) and Meriones unguiculatus (seed
eater) of Old World deserts. Note that the
lower incisors of each of the Atriplex
specialists are broad and/or chisel-shaped;
they function to remove the salty tissues
from the leaves before they are eaten, thus
reducing the amount of salt ingested. The
tips of the lower incisors of each of the
Atriplex specialists also appear chisel-like
when viewed laterally.
pode found in Africa and eaten by
Psammomys, also is abundant in the
area and is consumed by T. barrerae
(Ojeda et al. 1996). Rains and runoff
keep the area between the mounds
largely free of vegetation; consequently, deep soil is present only
adjacent to the mounds, and shrubs
are restricted to this location as well.
To investigate how T. barrerae
eats halophytes, we collected rats
from Mendoza Province, Argentina,
from mounds in a saline area supporting abundant Atriplex. Captive
rodents were offered sampies of
plants to determine food preferences.
When rats were fed Atriplex, tiny
pieces of the outer leaf tissues flew in
all directions, some sticking to the
glass sides of the aquarium. The
rodent's facial region vibrated as the
sterns were brought to the mouth,
which consists of a small round opening in the skin surrounding the buc701
Figure 4. Specialized hair bundles of
Tympanoctomys barrerae. (a) The mouth
of T. barrerae is a small round opening
with an incisor-like bristle bundle (arrow) located on each side, just posterior
to the upper incisors, wh ich occlude with
the lower incisors and vibrate to strip
the Atriplex leaves of their salt-filled
exterior tissues. (b) The bundles are composed of stiff hairs. (c) The hairs are
sharpened to an acute angle, most likely
by honing them against the tips of the
lower incisors.
cal cavity (Figure 4a). The movement of the facial muscles is associated with several adaptations for
stripping the leaves of their hypersaline tissues. T. barrerae has lower
incisors that are remarkably similar
to those of D. microps (Figure 3b)chisel-shaped teeth that remove the
hypersaline covering from the
702
Atriplex leaves. However, T. barrerae
possesses an additional and unique
adaptation: two "bristle brushes" of
stiff hairs that are located on either
side of the mouth just posterior to the
upper incisors and that resemble a
second pair of upper incisors (Figures
4a, 4b). These hairs occlude with the
lower incisors and act like bark strippers in a saw mill. The bundles of
sharp, stiff bristles (Figure 4c) quickly
strip the salt-filled exterior layer of
the leaves, thus permitting the animal
to ingest the green inner portions.
The bristles make T. barrerae a
more efficient consumer of Atriplex
leaves than D. microps. The process
by which D. microps scrapes away
the epidermal vesicles in preparation
for eating the leaf -running one side
of the leaf over the lower incisors up
to ten times, then turning the leaf
over and repeating the procedure on
the other side of the leaf-takes 1520 seconds (Kenagy 1973). By contrast, we found that T. barrerae
needed no more than one or two
seconds to strip each leaf and is able
to consume many leaves within 20
seconds. Clearly, the addition of a
specialized leaf tissue stripper that
complements the lower incisors results in a more efficient mechanism
for removal of the leaf's protective
salt layer.
We also examined the gross kidney morphology of T. barrerae, comparing it with that of a related genus
of desert octodontid (Octomys
mimax) that also is endemie to Monte
Desert but does not forage on halophytes. The kidney of T. barrerae is
similar to that of African P. obesus
(Abdallah and Tawfik 1969), especially in the long renal papilla (Figure 5); it is more similar to the African species in this regard than to its
own relative, O. mimax. A long renal papilla is a structural adaptation
that permits salts to be removed
through countercurrent filtration
(Abdallah and Tawfik 1969). In addition to its behavioral and morphological adaptations, T. barrerae also
has developed specialized kidneys for
processing electrolytes that it obtains when foraging on chenopodes
such as Atriplex.
Comparing adaptations
The lower incisors of T. barrerae are
morphologically convergent with
those of the unrelated North American heteromyid species D. microps.
A com paris on of the teeth of P. obesus
with those of D. microps and T.
barrerae shows that P. obesus has
evolved lower incisors that are similar in shape to those of its New
World counterparts and may be used
for the same purpose (Figure 3c).
Indeed, although Degen (1988) did
not discuss the mechanics of salt
tissue removal from Atriplex leaves
by P. obesus, the structure of the
lower incisors suggests that they provide a morphological adaptation for
the removal of such tissues. P. obesus,
therefore, would appear to be at least
as specialized as D. microps to the
Atriplex resource and, with its specialized kidneys, may be even more
adapted to a halophyte diet, although
the kidneys of D. microps have not
yet been examined. The combined
adaptations of T. barrerae to the
Atriplex food source are, however,
more unusual and complex than either the dental specializations of D.
microps or the dental and renal specializations of P. obesus.
The specialized bundles of hairs
of T. barrerae are functionally similar to a second set of lower incisors,
even though the hairs appear to be
an additional pair of upper incisors.
The upper incisors in all of these
taxa are used to crop leaves, whereas
the lower incisors are designed to
scrape the leaves and remove their
salty covering. By evolving bristle
bundles, T. barrerae has managed to
add a second pair of "incisors" that
are functionally similar to the saltremoving lower teeth but are placed
behind the upper incisors. This specialization permits the upper incisors to remain free to crop leaves and
serve other functions without becoming so highly specialized that they
BioScience Vol. 47 No. 10
are unable to serve any purpose but
salt removal.
The bristle bundles are anatomical structures that have not been
described in any other mamma I and
appear to be a unique evolutionary
adaptation to the Atriplex diet. Our
observations provide the first evidence that mammalian hair-Iong
known for its plastieity in evolving
to serve functions as diverse as
thermoregulation, defense, and
crypsis-can also function in place
of teeth. (Curiously, in at least one
respect, the desert rodent T. barrerae
is similar to baleen whales, which
also use keratinized material to aid
in foraging, in this case as a filter for
plankton.) With this adaptation in
addition to its unusual teeth and
specialized kidney, T. barrerae has
surpassed its ecological equivalents
in other deserts in its degree of specialization to forage on Atriplex.
Thus, T. barrerae of the Monte Desert
would appear to be the most highly
specialized halophytic plant consumer known. This high degree of
specialization could relate to its long
association with Atriplex in the
deserts and scrublands of South
America, a major center for chenopode radiation (Smith 1977).
Condusions
Given that salt flats develop on every
continent, it is interesting that only a
few mammals have been able to specialize on the abundant, succulent
vegetation associated with these habitats. Clearly, overcoming the defenses
of halophytic plants is not a simple
matter. Inereased salt loads require
additional water consumption if the
salts are to be eliminated from the
body, and water is precisely the substanee whose scarcity defines a desert.
Mammals are thus faced with the
formidable task of consuming salts
in order to take advantage of the
perennial green vegetation surrounding the salt flats. If a mamma I eats
green vegetation with high salt levels, it has to process the salt in some
way or reduce the salt content of the
plant tissues before they are eaten. In
at least three different families of
rodents occurring on different continents, one species has become a specialist on halophytes and has found a
way both to reduce the amount of
November 1997
remove salty tissues before they are
eaten. The solution is unique, but the
adaptive challenge it overcomes is
the same. Whether through specialized teeth or toothlike hair bundles,
the levels of convergence manifested
in the solution to the problem of
foraging on halophytic plants are
pronounced. There are only so many
ways to overcome an evolutionary
challenge, and although individual
solutions may vary, the types of solutions te nd to fall within similar
adaptive genres.
Acknowledgments
Figure 5. Cross-section of the kidneys of
Tympanoctomys barrerae (top) and Octomys mimax (bottom). Note that the renal
papilla (arrow) ofT. barrerae, theAtriplex
special ist, is longer and better developed
than that of o. mimax, which does not
feed on halophytes. In cross-section, the
kidneys of T. barrerae are alm ost identical
with those of the African sand rat,
Psammomys obesus, which also specializes on Atriplex (Abdallah and Tawfik
1969). A 2 cm scale is shown at right.
salts that are consumed and to eliminate from the body those salts that
are ingested. Each has developed specialized lower incisors to scrape away
salt-filled plant tissues, while also
developing kidneys that produce concentrated urine, thereby eliminating
salts from the body and maintaining
a positive water balance. Using the
specialized teeth and associated behavior of the forefeet in handling the
salty leaves, these rodents manage to
survive on halophytes in areas that
other mammals find intolerable.
Morphology, physiology, and behavior are thus interlinked to permit
each species to exploit this challenging habitat. This convergence in
morphology, behavior, and physiology is pronounced, but not perfect,
however. The development of the
bristle bundles of T. barrerae is the
most unusual adaptation of all to
plant tissues, but it is still an extension of the morphological adaptations shown by the other species to
reduce the salt content of the vegetation before it is ingested. The specialized denticulate hairs are, in effect, a second set of ineisors that
We thank Steve Adams and Rob
Channell for assistance in the field.
Various technical and editorial assistance was provided by J analee P.
Caldwell, Riehard L. Cifelli, Thomas E. Lacher Jr., and LaurieJ. Vitt.
Field work in Argentina was funded
by grants from the National Science
Foundation (BSR-8906665) andthe
National Geographie Soeiety (482092) to M. A. Mares, a grant from the
University of Oklahoma Research
Council to M. A. Mares and J. K.
Braun, and support from the Oklahoma Museum of Natural History.
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