Download Comparative ecology of desert small mammals: a

Journal of Mammalogy, 92(6):1158–1178, 2011
Comparative ecology of desert small mammals: a selective review of
the past 30 years
DOUGLAS A. KELT*
Department of Wildlife, Fish, & Conservation Biology, University of California, One Shields Avenue, Davis, CA 95616,
USA
* Correspondent: [email protected]
Rooted in the conceptual revolutions of the 1960s and 1970s, contemporary research on the ecology of desert
small mammals has progressed markedly in recent decades. Areas of particular emphasis include the role of
extrinsic (e.g., climate) compared with intrinsic (e.g., density-dependence) factors on population growth and
associated metrics, the role of competition compared with predation in influencing foraging decisions and
habitat selection, the influence of small mammals on community structure and composition via consumption
and redistribution of plant materials, and as ecological engineers and keystone species (or guilds). Recent
emphasis on the energetic basis of assemblage composition is intriguing and warrants further work, and the
generality of zero-sum dynamics requires further assessment. Desert systems continue to be the focus of much
ecological research, and small mammals remain central figures in understanding the interplay between biotic
and abiotic factors and between intrinsic and extrinsic drivers. Small mammals in deserts worldwide exemplify
the importance of diverse approaches to ecological research, including local manipulative field experiments,
long-term demographic monitoring, and both laboratory and field-based studies on behavioral and foraging
ecology.
Key words: Africa, competition, ecological engineers, foraging, keystone species, North America, Palearctic, predation,
South America
E 2011 American Society of Mammalogists
DOI: 10.1644/10-MAMM-S-238.1
Desert small mammals have figured prominently in both the
development of ecological thought and the empirical assessment of theory. This development has not been distributed
evenly across the deserts of different continents, and
consequently paradigms based on 1 regional or continental
fauna have been found wanting when sufficient data were
available from other deserts or regions. This is typical of the
growth of scientific thought, however, and has spurred a
number of intercontinental comparisons of desert small
mammals (Kelt et al. 1996, 1999; Morton et al. 1994;
Shenbrot et al. 1994, 1999; Stapp 2010).
Deserts occur on all continents (Fig. 1) and can be classified
into 5 general types based on the geoclimatic factors that led
to their development (Cloudsley-Thompson 1975; Laity
2008). Subtropical high-pressure belts at roughly 30u latitude
are a product of atmospheric circulation; dry air descending
in the Hadley circulation cells leads to desiccation that is
accentuated by compressional warming of this descending air.
The resulting subtropical deserts cover about 20% of Earth’s
surface and include the Sahara, Karoo, and Kalahari in Africa,
deserts of the Arabian Peninsula, the Sonoran, Mojave, and
Chihuahuan deserts of North America, and much of Australia.
Interior continental deserts are far from the ocean and receive
air that has been depleted of moisture. The Gobi and Karakum
regions of Asia and the Great Basin of North America
exemplify this type of desert, and interior Australia’s dry
climate is accentuated by this influence. Cold ocean currents
can dry air sufficiently to lead to coastal deserts. The
Humboldt Current is a major cause of the Atacama and
Sechura deserts of western South America, the Benguela
Current a cause of southern Africa’s Namib Desert, and the
California Current a cause of coastal portions of the Sonoran
Desert in Baja California. Rain-shadow deserts occur on the
lee side of major mountain ranges. Patagonia, the Great Basin,
and some of Australia’s desert regions are caused or
accentuated by rain-shadow effects. As indicated above, these
factors can reinforce each other, as is the case for the Great
Basin (continental and rain-shadow effects) and much of
Australia (subtropical, continental, and rain-shadow effects),
or parts of the Sahara, the Arabian Peninsula, and the Horn of
www.mammalogy.org
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SPECIAL FEATURE—DESERT SMALL MAMMAL ECOLOGY
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FIG. 1.—Satellite view of Earth depicting the general locations of major deserts (see Laity [2008] for details of desert regions). Subtropical
deserts include the Sahara and deserts of the Iranian (Dasht-e Kavir and Dasht-e Lut) and Arabian peninsulas, the Kalahari and Karoo in Africa,
much of Australia, and the Mojave, Sonoran, and Chihuahuan deserts of North America. Coastal deserts resulting from cold oceanic currents
include the Sechura and Atacama of South America, the Namib of southern Africa, and sections of several other deserts (see text). Continental
interior deserts include the Gobi and Karakum regions of Asia and the Great Basin of North America. Rain-shadow deserts include the Puna,
Monte, and Patagonian regions of South America, although the Great Basin, Gobi, and parts of Australia’s deserts all are influenced by
continental and rain-shadow effects as well. Source of satellite photo: National Aeronautics and Space Administration, Goddard Space Flight
Center (Blue Marble Next Generation collection, August: http://visibleearth.nasa.gov/view_rec.php?id57119; accessed 24 January 2011).
Africa (subtropical deserts with cold coastal waters). The
Puna Desert of South America is a very high-elevation
(.3,500 m) desert that is caused in part by the drying
influence of the Humboldt Current and in part by rainshadow effects of the Andes. Finally, polar deserts occur
where water is present but in the form of ice and snow. Polar
deserts are qualitatively distinct from the other 4 categories
and will not be considered here.
Much of our contemporary understanding of desert ecology
developed through the International Biological Program in
the 1960s and 1970s. At this time community ecology was
undergoing a renaissance, applying ecological insights rooted
in works by G. Evelyn Hutchinson and Robert MacArthur to
biotic assemblages in diverse systems. Perhaps because many
of the authors of this scientific renaissance came from North
America, the fauna of North American deserts rapidly
assumed center stage in ecological research on deserts
(although see Prakash and Ghosh 1975), and heteromyid
rodents became particularly well known for their adaptations
to desert life. Their diversity and various means of coping with
the extremes of desert life were illustrated in a number of
papers in the 1950s and 1960s; adaptations included expansion
of auditory bullae, production of highly concentrated urine,
retrieval of a high proportion of respiratory water, nocturnal
and subterranean habits, and a granivorous diet combined with
extensive caching behavior. These adaptations were particu-
larly well developed in the bipedal kangaroo rats (Dipodomys), and these gradually became conflated, with bipedality
assumed to be associated with water independence and a
granivorous diet. In the 3rd published product of the
International Biological Program Mares et al. (1977; see also
Mares 1976) compared small mammals of the Sonoran and
Monte deserts (physiographically similar deserts in North and
South America, respectively; Fig. 1) and documented high
morphological convergence at the community level, and
particularly so for rodents (e.g., Ctenomys and Thomomys;
Neotoma, Phyllotis, and Octomys; and Eligmodontia, Paralomys, and Peromyscus). Mares attributed the greater species
richness in the Sonoran Desert to finer subdivision of niche
space relative to that in the Monte Desert. A subsequent paper
supported these observations but noted very different levels of
granivory in the 2 deserts and concluded that a granivorous
trophic strategy was not highly convergent (Mares and
Rosenzweig 1978). Further assessments integrating diverse
global deserts further emphasized morphological convergence
(Mares 1993a), but a comprehensive pandesertic analysis
(Mares 1993b) conclusively refuted the connection between
bipedality and granivory (see also Kelt et al. 1996; Kerley and
Whitford 1994), and a review of trophic strategies in desert
small mammals highlighted both temporal and spatial
variation in diets, even within species, and emphasized the
important role of abiotic influences on the ecology of small
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FIG. 2.—Number of publications on ecology of desert small
mammals in the ISI Web of Knowledge database (http://wokinfo.com/;
accessed 10 May 2010). Results based on the following search criteria:
subject (ecology or foraging or demography or biogeography or
competition or predation or assembly rules or keystone species or
ecological engineer) and subject (desert) and taxa (Rodentia or
Insectivora or Soricomorpha or Lagomorpha or Marsupialia) and either
subject or geographic region (North America or South America or Africa
or Australia or Palearctic or Europe or Asia). Although this omits a
number of publications and includes some that do not pertain clearly to
ecology, it provides an objective index of relative activity in these
regions, thereby allowing for direct comparisons.
Vol. 92, No. 6
application of this to and within theoretical constructs remains
much deeper for Nearctic and Palearctic species. Thus, this
review inevitably is dominated by northern examples. I have
excluded entirely Australia from my review, because this has a
large literature of its own and is the subject of papers by 2
contributors to this Special Feature (Dickman et al. 2011;
Letnic et al. 2011).
What follows is by necessity a selective survey of themes
that I believe have greatly improved our understanding of
desert small mammal ecology and of ecology in general. Thus,
other than tangential consideration as they pertain to the topics
I have selected, I will not address in depth several themes that
many find exciting and topical, such as physiological or
behavioral ecology of desert small mammals, both of which
have been the subject of much interesting work in recent
years. To make this review as generally informative as
possible, and to provide structure to the wealth of available
literature, I focus my efforts on 4 themes: competition
compared with predation; the influence of biotic and abiotic
factors; assemblage structure and composition; and food
hoarding and the role that small mammals have in regulating
vegetative ecology and habitat structure.
Increased understanding of desert systems can have
particular importance to managers and both conservation and
restoration ecologists in the face of global climate change and
concerns over desertification in many regions (Geist 2005).
Deserts have long been leading field laboratories for
developing and testing hypotheses for ecological structure
and function, in part because they are relatively simple
systems in terms of vegetative structure and the nature of
abiotic influences. However, structural simplicity by no means
implies ecological transparency. Decades of research have
underscored the complex nature of desert ecology.
COMPETITION COMPARED WITH PREDATION
mammal communities in arid regions (Fox 2011). Walsberg
(2000) and Tracy and Walsberg (2002) clarified additional
features of the ecology and physiology of these animals that
suggest they are not the pinnacle of desert adaptation as they
had been depicted.
In spite of the global distribution of deserts, our understanding of desert systems and the ecology of desert small
mammals has matured more rapidly in some regions than
others (Fig. 2). Publications on North American and Middle
Eastern deserts have been much more numerous than those on
South American or African arid regions, but studies on the
latter have been making substantial headway in recent
decades. One objective of this paper is to clarify what is and
is not known from desert regions in these 4 main continental
areas. The dramatic growth in literature on desert small
mammals in recent decades (Fig. 2) precludes any attempt to
distill this in a brief synopsis. This work continues to be
dominated by research on Northern Hemisphere systems,
however, and although research elsewhere is rapidly increasing, our understanding of small mammal ecology and
Tremendous effort has been exerted in quantifying the
ecological importance and relative role of competition and
predation in ecological communities, including for small
mammals. Whereas this topic is much less controversial—
both factors have strong and pervasive impacts on ecological
structure and function—what is less clear is when and under
what conditions either of these general factors assumes
precedence over the other. Several fundamentally different
approaches have been used to explore this subject.
Assembly rules.—Static approaches to assessing the role of
competitive interactions include the application of assembly
rules (Brown et al. 2000, 2002; Fox and Brown 1993; Kelt
et al. 1999) and geographic assessment of local composition
relative to that of species pools (Brown and Kurzius 1987;
Kelt et al. 1996, 1999; Morton et al. 1994), all of which have
documented overwhelmingly that small mammal assemblages
in North American deserts are structured in ways consistent
with predictions of a competition paradigm. Limited efforts
elsewhere generally have supported this conclusion (Kelt et al.
1995). These results might not hold up against alternative
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SPECIAL FEATURE—DESERT SMALL MAMMAL ECOLOGY
approaches, however. Although comparison of local to
regional species composition strongly supports a role of
competition in the Negev Desert (Kelt et al. 1996), subsequent
analysis of small mammal assemblage composition at 24
permanent 1-ha grids and use of 2 approaches based on
regression models yielded significant negative associations in
only 6 of 45 species pairs and 1–4 of 16 seasons studied
(Shenbrot and Krasnov 2002). The general paucity of evidence
for pairwise competition in this system was upheld with
16 years of data (Shenbrot et al. 2010).
Long-term field manipulations.—Some investigators have
tracked the demography of focal species or the structure of
targeted assemblages after manipulating the numbers of a
putative competitor. Likely the best-known study applying this
approach to small mammals is the long-term program of
J. H. Brown at Portal, Arizona, on the northern edge of
the Chihuahuan Desert (Brown 1998). Experimental exclusion
of Dipodomys there clearly has shown competitive release
by pocket mice (Chaetodipus and Perognathus—Brown and
Munger 1985; Munger and Brown 1981), with qualitatively
identical responses to exclusions in 1977 and to a 2nd set of
exclusions initiated in 1988 (Heske et al. 1994).
In contrast, evidence for the role of competition at Parque
Nacional Bosque Fray Jorge in northern Chile (Fray Jorge
hereafter) has been much less apparent, even after 20 years of
experimental manipulations (Gutiérrez et al. 2010; Meserve
et al. 2003, 2009, 2011). Experimental exclusion of degus
(Octodon degus) from a series of grids yielded no meaningful
changes in any other species. A longer time series, however,
and sophisticated demographic modeling (Previtali et al. 2009)
extracted clear signals of intraspecific competition among O.
degus, as have foraging studies (see below).
Short-term experiments with giving-up densities.—Longterm field studies such as those in Portal, Arizona, and Fray
Jorge in Chile do not directly assess the mechanisms
underlying competitive suppression, however. An alternative
means of assessing the importance of competitive interactions
is to pursue manipulative studies over shorter periods,
commonly (but not always) in experimental enclosures. This
approach requires a metric for assessing the magnitude of
competition under different experimental conditions and to
this end J. S. Brown (1988, 1989b) developed the concept of
giving-up densities (GUDs), the density of food resources in a
patch at which an animal would cease foraging, presumably
because the costs (e.g., competition or predation) exceeded the
benefits (e.g., the rate of finding additional food). Measurement of GUDs has become extremely common in foraging
studies, but they have been used most extensively in studies on
desert small mammals. In Arizona Brown (1989b) compared 4
mechanisms of species coexistence in a diverse (13 species)
assemblage. Coexistence of 3 of these species (Perognathus
amplus, Dipodomys merriami, and Xerospermophilus tereticaudus) is explained best by seasonal variation in foraging
efficiency, with each species exhibiting maximal foraging
efficiency in a different season. Coexistence of the 4th species
(Ammospermophilus harrisii) is explained best by spatial
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variation in resource abundance; this species forages widely
but skims fairly superficially. Brown (1989b) noted, however,
that his study site was atypical in having only 2 nocturnal
granivores and relatively high activity of diurnal sciurids and
also in the unexpected lack of a role for microhabitat as a
mechanism of species coexistence. Given this, it is unclear
how more diverse assemblages elsewhere in North America
might have been formed by the 2 mechanisms of coexistence
documented at his site, or whether additional mechanisms
would be needed to explain the composition of more speciesrich assemblages. Unfortunately, little subsequent work has
been pursued on this issue in North America.
In the Negev Desert researchers have gradually teased apart
a variety of predictions from foraging theory by focusing on
habitat selection by gerbils (Gerbillus). Assuming 2 species
have distinct (but overlapping) habitat preferences, researchers
experimentally vary the density of each species to yield a 2dimensional graph defined by the densities of the 2 species.
Such a graph will include regions in which one or the other
species uses habitats opportunistically and a region where
both species will select habitats in the face of presumed
competition with the other species. These regions are
separated by lines called isolegs, corresponding to lines of
equal competitive abilities.
Using sand trays to quantify activity by individual species
in experimental enclosures and foraging trays to quantify their
foraging, researchers have assessed habitat preferences of
species both in isolation and in the presence of competitors.
Much of their work has focused on Gerbillus andersoni
allenbyi and G. pyramidum, both of which favor semistabilized sand dunes over stabilized sand dunes. In the absence
of the larger and dominant G. pyramidum (about 40 g) the
smaller and subordinate G. a. allenbyi (about 24 g) uses
stabilized sand only at very high population densities
(Abramsky et al. 1990, 1991, 1992, 1994). In the presence
of the competitive dominant, however, G. a. allenbyi is
relegated largely to stabilized sand dunes, except at low
densities of G. pyramidum. An important contribution of these
studies was the experimental assessment of isolegs for both
species and documentation that isolegs frequently are not
linear. Abramsky et al. (2001) quantified that an additional
1.8–3 g of millet seed per day is required for G. a. allenbyi to
overcome the competitive influence of the larger G.
pyramidum.
A 3rd and much smaller species (Gerbillus henleyi, about
10 g) occurs on a variety of substrates in the Negev Desert but
at least in Israel is rare on all of them (Mendelssohn and YomTov 1999). Shenbrot and Krasnov (2002) argue that this
reflected competitive suppression by larger gerbils; in their
study this included Gerbillus gerbillus and Dipodillus
dasyurus, both of which are more effective in exploiting
seeds buried in deep soil layers (Krasnov et al. 2000).
Abramsky et al. (2005) studied G. henleyi in association with
2 other larger Gerbillus (G. a. allenbyi and G. pyramidum) and
tested the hypothesis that the rarity of the smaller gerbil
reflected competitive interactions with the larger taxa. Their
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alternative hypothesis was that the naked hind feet of G. henleyi
put it at a disadvantage to the hairy-soled G. a. allenbyi and G.
pyramidum in moving about and maneuvering on sandy
substrates. The ratio of body mass to hind-foot area was
allometrically similar among all 3 Gerbillus, however, and in 2
species of Meriones (M. crassus, about 90 g, and M. sacramenti,
about 110 g). G. henleyi lay slightly above the allometric curve,
suggesting that its relative hind-foot surface area was at least as
large as for other species of Gerbillus. Assessments of activity
under manipulated densities of G. henleyi and either G. a.
allenbyi, G. pyramidum, or both, indicated that interspecific
competition was sufficient to explain the reduced abundance of
the smaller species wherever either of the larger species existed.
One intriguing result was that interaction strengths (aGH,GX,
where GH 5 G. henleyi and GX 5 either G. a. allenbyi or G.
pyramidum) were strongly negative at low levels of activity of
the larger competitor species but were weak (G. a. allenbyi) or
mildly positive (G. pyramidum) at moderate to higher levels of
activity, suggesting a facilitation effect at least by the largest
species. Abramsky et al. (2005) explained this in terms of
apparent competition, although this might be incomplete
because they excluded predators from their enclosures.
Nonetheless, they estimated that competitive interactions likely
are responsible for just over 90% of the reduction of G. henleyi
from the productive sand dune habitat in the Negev Desert.
Habitat selection using isodars and paraisodars.—Elsewhere in Israel Shenbrot and Krasnov (2000) modified the
Morris’s (1987, 1988) isodar theory to quantify habitat
selection by an assemblage of small mammals across an
ecological gradient. Whereas isolegs represent lines of equal
competitive abilities in co-occurring species, isodars (after
Darwin) represent lines of equal fitness within a single species
across habitats. And because isodars have been used by Morris
and others to reflect temporal replicates within sampling plots,
Shenbrot and Krasnov (2000) analyzed spatial replicates and
so referred to their equal-fitness contours as paraisodars to
distinguish these from true isodars. Results of Shenbrot and
Krasnov (2000) largely mirrored earlier reports (Abramsky
et al. 1985a, 1985b; Rosenzweig and Abramsky 1985), with
some informative exceptions. Most notably, Shenbrot and
Krasnov (2000) reported density-independent habitat selection
in both D. dasyurus and G. gerbillus; Abramsky et al. (1985a,
1985b) and Rosenzweig and Abramsky (1985) had reported
these species to exhibit density-dependent habitat selection.
Shenbrot and Krasnov (2000) explained this discrepancy as a
function of the larger spatial scale of their efforts. In the case
of D. dasyurus Abramsky et al. (1985a, 1985b) studied this
species within a single habitat type, whereas Shenbrot and
Krasnov (2000) studied a much broader array of habitats.
Rosenzweig and Abramsky (1985) studied G. gerbillus where
it coexisted with potential competitors (G. a. allenbyi and G.
pyramidum). In contrast, Shenbrot and Krasnov (2000:277)
studied G. gerbillus in ‘‘a small peripheral isolate … in the
absence of any potential congeneric competitor.’’ Shenbrot
et al. (2006) further pursued the question of densityindependent habitat distribution and constant niche breadth
Vol. 92, No. 6
in D. dasyurus, arguing that this was a counterintuitive result
of density-dependent processes of habitat selection. Further
work in this area would be enlightening.
Intraspecific competition.—Whereas most studies on the
role of competition have emphasized interactions between
species, the role of intraspecific competition has received
much less attention (Keddy 2001). Modeling of long-term
demographic data both in Chile (Lima and Jaksic 1999a; Lima
et al. 2002, 2003; Previtali et al. 2009, 2010) and North
America (Lima et al. 2008) has underscored the role of
density-dependent regulation of small mammal populations
even in the face of strong fluctuation in abiotic drivers.
Hughes et al. (1994) manipulated densities of Gerbillurus
tytonis to assess the role of intraspecific competition (see
‘‘Predation’’ below), and Kotler et al. (2005) capitalized on a
year with very low densities of the behaviorally dominant G.
pyramidum to assess foraging and interference among sexes of
G. a. allenbyi. Using GUDs to measure activity, Kotler et al.
(2005) provided either pulsed or temporally renewed resources
through the night by presenting multiple foraging trays per
field station and adjusting the number of trays that contained
seed. Male G. a. allenbyi are active earlier than females and
remain active later, and this is more pronounced when
resources are pulsed (6 trays provided at the beginning of
the night) than when they are renewed throughout the night (a
single tray provided at 6 evenly spaced intervals). Additionally, females use stabilized sand dunes more than do males,
although the species is known to favor semistabilized dunes.
Kotler et al. (2005) argued that when these observations were
integrated they suggest that male G. a. allenbyi interfere with
foraging females, resulting in spatial and temporal adjustments
in foraging activities. Predictably, G. pyramidum reduces the
time that G. a. allenbyi spend in seed trays (Ovadia et al. 2005;
see also Ovadia and zu Dohna 2003), but this influences male
G. a. allenbyi more than females. This results in reduced
aggression by male G. a. allenbyi on females and indirectly
leads to reduced body mass in males and increased survival in
females. Hence, intraspecific competitive interactions are mediated by gender-focused interspecific interactions. Such integration of behavioral and community ecology in other regions
would be helpful in shedding light on the role of behavioral
interactions in mediating or facilitating coexistence.
The role of agonistic interactions in habitat partitioning has
been well documented for a number of small mammals in the
Namib and Kalahari deserts (Dempster and Perrin 1989, 1990;
Perrin and Boyer 1996, 2000). Perrin and Kotler (2005) built
on this to test 5 mechanisms underlying coexistence of
Gerbilliscus leucogaster and Rhabdomys pumilio in a Kalahari
savanna. Their results failed to support any of these
mechanisms, leading them to suggest a 6th mechanism,
seasonal variation in resources and a trade-off of maintenance
efficiency and foraging efficiency (Brown 1989a), although
their study was too brief (June–July) to assess this thoroughly.
Whereas most work on the ecology of desert small
mammals and both patterns and mechanisms of coexistence
has focused on sandy desert habitats, rocky habitats also are
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SPECIAL FEATURE—DESERT SMALL MAMMAL ECOLOGY
common in deserts worldwide. Using foraging trays and
GUDs, Jones et al. (2000) investigated coexistence between 2
species of spiny mice (Acomys cahirinus and A. russatus). The
former species is nocturnal whereas the latter generally is
diurnal but can be nocturnal as well (Kronfeld-Schor and
Dayan 2003). Jones et al. (2000) reported the nocturnal A.
cahirinus to be a habitat generalist and to skim resources only
superficially, similar to Ammospermophilus in the Sonoran
Desert (Brown 1989b). A. russatus is more specialized in
habitat and forages more extensively within trays. Subsequent
work with experimental exclosures confirmed that both
species have similar foraging preferences, but the nocturnal
A. cahirinus exploits more patches and with greater efficiency,
possibly explaining the diurnal habit of A. russatus when in
sympatry (Gutman and Dayan 2005).
Predation.—In contrast to competition, predation is a clear
and immediate influence on small mammals, but its
importance in structuring small mammal assemblages has
been somewhat more challenging to document. Two decades
of comprehensive demographic monitoring at Fray Jorge,
Chile, has demonstrated an important role of predation on
some species of small mammals (Lagos et al. 1995; Meserve
et al. 1993, 1996), but this is much less important than the
abiotic influence of El Niño–associated rainfall (Gutiérrez
et al. 2010; Meserve et al. 2003, 2009; Previtali et al. 2009,
2010). In contrast, experimental field studies have provided
compelling evidence of a trenchant role of predation in habitat
selection and foraging ecology.
Two behavioral patterns are presumed to reflect perception
of predation risk. First, many small mammals reduce foraging
activities under conditions of high ambient light (Alkon and
Saltz 1988; Brown and Peinke 2007; Kotler 1984, 1985;
Kotler et al. 1993a, 1993b; Price et al. 1984; but see Prugh and
Brashares 2010). Second, many species forage more extensively in covered habitats (such as under shrubs) than in open
habitats (Hughes et al. 1994; Kelt et al. 2004; Kotler et al.
1991; Longland and Price 1991; Wondolleck 1978). In North
America bipedal Dipodomys and Microdipodops are more
active in open areas than quadrupedal Chaetodipus and
Perognathus (Price 1986; Reichman and Price 1993), but the
inflated auditory bullae of Dipodomys and Microdipodops
presumably increase their auditory sensitivity to approaching
predators (Webster and Webster 1971, 1975), and their bipedal
locomotion has been shown to facilitate escape from owls
(Longland and Price 1991).
In the presence of owl predation G. a. allenbyi moves to
areas of reduced predator pressure when possible, rather than
simply reducing foraging (Abramsky et al. 1997). To assess
the relative influence of predation and competition (with G.
pyramidum) Abramsky et al. (1998) used paired experimental
subplots with similar distributions of habitats separated by
fences; small holes in the fencing allowed free movement by
the smaller, subordinate G. a. allenbyi but not the larger and
dominant G. pyramidum. After documenting that the subordinate species consistently shifts its activity to the subplot
lacking the competitive dominant, researchers flew an aerial
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predator (barn owls [Tyto alba]) in either the subplot with the
dominant gerbil species or the one without the competitor
species. Results were compelling and unambiguous. Regardless of the presence or absence of the dominant gerbil, the
subordinate species shifts activity to the subplot lacking owls.
When confronted with potential owl predation, G. a. allenbyi
evidently ignores interspecific competition, distributing its
foraging activities as if G. pyramidum were not present
(Abramsky et al. 1998). Further supporting the overwhelming
influence of predation, Rosenzweig et al. (1997) documented
that at low population densities G. a. allenbyi forages
exclusively in a subplot lacking predation threat (barn owls).
Only at moderate to high densities does intraspecific
competition result in some foraging activity in a subplot
subjected to owl flights. They characterized the zero isocline
for the gerbil, or the victim isocline. An isocline is a line in
bivariate space defined by predator and prey population
density (y and x, respectively) below which population size
increases and above which it decreases. Theory predicts that
at low victim densities and in part because processing prey
takes time, the isocline should be positive (e.g., prey should
coalesce spatially in the face of a fixed predator density), but
this should become negative at higher densities. Rosenzweig
et al. (1997) confirmed this for G. a. allenbyi, stressing that
this was distinct from collaborative foraging because these
gerbils are not social foragers, and the only benefit they
appeared to gain was increased vigilance through the presence
of additional potential victims.
Gerbillus a. allenbyi modifies foraging activity as a
function of the hunger state of owls (Berger-Tal and Kotler
2010). Hungry owls are more active than recently fed owls,
making more swoops and more dives. In response, G. a.
allenbyi limits its foraging activities to areas closer to its
burrows, visits and forages in fewer foraging patches, and
harvests less food from these patches. These behavioral
responses are qualitatively similar to those comparing nights
without owls and nights with fed owls, leading the authors to
suggest that predator risk was additive. Berger-Tal et al.
(2010) extended this by simultaneously manipulating the
hunger state of both owls and G. a. allenbyi. In the presence of
fed owls, hungry and fed gerbils have similar GUDs. In
contrast, when confronted with hungry owls, fed gerbils forage
much less than hungry gerbils. Overall, however, hungry
gerbils consume much less (have higher GUDs) in the
presence of hungry owls than when confronted with fed owls.
Pygmy rock mice (Petromyscus collinus) in a South African
kopje (5 inselberg—a small hill rising above the surrounding
veld) evidently are highly constrained to foraging in or very
close to the kopje (Brown et al. 1998), presumably reflecting
increased predation threat away from the rock cover. This
threat is so pervasive that these authors speculated that pygmy
rock mice at their site survive by foraging for seeds in feces of
hyraxes (Procavia capensis) rather than exposing themselves
through other foraging activities.
In the Namib Desert of southern Africa Hughes et al. (1994)
applied GUDs to assess the relative strength of competition
1164
JOURNAL OF MAMMALOGY
and predation for G. tytonis across 3 habitats, 2 lunar phases,
and various levels of both intraspecific (via removal of 25% of
coexisting conspecifics) and interspecific (via removal of all
coexisting individuals of R. pumilio) competition. Both of
these species favor similar microhabitat, but G. tytonis also
occupies a 2nd microhabitat that presents higher predation
risk. Hughes et al. (1994) assessed foraging activity (via sand
tracking) and foraging efficiency (using GUDs) in 3 habitats in
and around an isolated island of vegetation surrounded by
dunes. Gerbillurus activity and foraging efficiency are both
lower under a full moon than under a new moon in all 3
habitats (Hughes and Ward 1993; Hughes et al. 1995).
Reduction of both intraspecific and interspecific competition
results in increased foraging activity and efficiency (when R.
pumilio was reintroduced this effect reversed). Threat of
predation in open habitats limits foraging activity by both
species to more protected habitat, where competition is
consequently greater. Hence, the threat of predation drives
these species to elevated competition.
In northern Chile Yunger et al. (2002) and Kelt et al. (2004)
documented that nocturnal small mammals (Abrothrix olivaceus and Phyllotis darwini) foraged more in plots from which
diurnal O. degus had been excluded. Where O. degus had not
been excluded, Phyllotis foraged more away from shrubs than
under shrub cover. Additionally, the role of predation can vary
temporally; Yunger et al. (2002) reported a much stronger
response to predator removal (using experimental exclosures)
than did Kelt et al. (2004), although differences in field
protocols could be partially responsible.
Risk also is associated with foraging under bushes, and a
few studies have demonstrated that small mammals adjust
their foraging microhabitat depending on the presence or
absence of snakes (Bouskila 1995; Kotler et al. 1992, 1993a,
1993b). Paradoxically, D. merriami in the Mojave Desert
forages more at trays with snakes (Bouskila 1995). This was
inferred to reflect avoidance of the larger Dipodomys deserti,
which avoids these trays and therefore forages in open habitats
away from trays with snakes. Because snakes are more active
in summer, aversion to shrub habitats by D. merriami
generally is greater in summer than winter (Bouskila 1995).
However, at another site in the Mojave D. merriami responded
to the scent of snakes only in winter (Herman and Valone
2000). These authors suggested that the low density of snake
predators at their site might have led to reduced aversion to
shrubs in summer. Using experimental arenas in a laboratory
setting, Pierce et al. (1992) found that Great Basin rattlesnakes
(Crotalus oreganus lutosus) are not differentially successful at
capturing quadrupedal (Perognathus parvus and Peromyscus
maniculatus) over bipedal (D. merriami and Microdipodops
megacephalus) rodents but that certain species (M. megacephalus and P. parvus) are more prone to capture than others
(D. merriami and P. maniculatus), presumably reflecting
behavioral differences. Two Israeli species of Acomys shift
their foraging activities to more open habitats during summer
when snakes are active. This occurs both for the nocturnal A.
cahirinus and the diurnal A. russatus, presumably increasing
Vol. 92, No. 6
risk of predation by diurnal hawks and nocturnal owls, and
increasing thermoregulatory costs for the diurnal species
(Jones et al. 2000, 2001). It is not surprising that rodent
responses to sit-and-wait predators such as snakes are very
different from those to aerial predators such as owls (Bouskila
1995; Kotler et al. 1993b). Although the relative and opposing
effects of raptorial and reptilian predation on foraging
activities warrant further investigation (Jones et al. 2001),
this inherently requires controlled experiments.
Balancing foraging with predation risk requires decisions
concerning allocation of time to apprehensive behaviors in
which an animal diverts attention away from foraging and
toward detection of predators (Kotler et al. 2002). Kotler et al.
(2002, 2004a) used GUDs to assess the role of apprehension
and time allocation in foraging decisions by G. pyramidum
and G. a. allenbyi under different energetic states and levels of
predation risk. Although both species prefer to forage early in
the night (Ziv et al. 1993), where they co-occur G. pyramidum
is active earlier in the night when resources are richer but
predation risk greater, whereas the smaller G. a. allenbyi
forages later, when resources are sparser but both competition
(with G. pyramidum) and predation risk (owls and foxes) are
lower (Kotler et al. 1993c; Ziv et al. 1993). Kotler et al. (2002,
2004a) quantified this by presenting gerbils with paired
foraging trays in which seeds were either evenly distributed
within a sandy matrix or were distributed only in the lower
half of the sandy matrix. Increased apprehension should
manifest as greater selection of the former tray because
resources were more readily accessible there. In summer
apprehension was greater early in the night than later, under
full moon than new moon conditions, and in open microhabitats than under shrubs, consistent with a hypothesis that
apprehension is greater under the threat of predation (Kotler
et al. 2002). In winter, however, gerbils face a more thermally
stressful and more spatially homogeneous environment
(moister soils are less susceptible to redistribution by daily
winds—Kotler et al. 2004b), and GUDs are higher (in
response to thermal stress) and more consistent across time
and space. Given this, Kotler et al. (2004b) argued that
apprehension is relatively more important in winter, underscoring the role of seasonality in understanding factors driving
evolution of foraging behaviors.
Abramsky et al. (2002) used sand tracking to quantify
foraging activity in open and shrub microhabitats in paired
plots differing in predation risk. Their results indicate that 4–
8 g of additional seed availability is needed to offset predation
threat for G. a. allenbyi and that this species allocates 25%
of its foraging time to vigilance. Somewhat surprisingly, they
found that preference for shrub microhabitat was not much
greater in the presence of predation risk than in control plots.
This contrasts with results by Kotler and Blaustein (1995),
who reported that in the presence of predation threat seed
density needed to be 4–8 times richer in open microhabitats
for these to be perceived by this species to be equally as
valuable as shrub microhabitat. Abramsky et al. (2002)
suggested that the estimate of Kotler and Blaustein (1995)
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SPECIAL FEATURE—DESERT SMALL MAMMAL ECOLOGY
for the cost of predation might be too large but that differences
in estimates likely reflect different experimental approaches.
Whereas Abramsky et al. (2002) conducted 6–8 owl flights
over large (1-ha) enclosures over a 2-h period, Kotler and
Blaustein (1995) conducted their study in an aviary (0.09 ha)
and left 2 barn owls in the aviary for the entire night. These
studies also measured different response variables. Kotler and
Blaustein (1995) quantified seed removal with GUDs, whereas
Abramsky et al. (2002) quantified foraging activity with
tracking plates; these could record different components of
foraging activity.
In southern Africa Cape ground squirrels (Xerus inauris)
exhibit a behavioral repertoire that reflects a high predation
threat that is habitat-dependent (Unck et al. 2009). van der
Merwe and Brown (2008) quantified the variation in foraging
cost in this species attributed to predation as the landscape of
fear (Brown et al. 1999; Laundré et al. 2001), noting that less
than one-fourth of the space used by the colonies studied
presented low foraging costs (in estimated joules/min),
whereas up to 92% represented very high foraging costs.
The increasing body of information on behavioral ecology of
this species makes this an attractive candidate for further work
on the integration of behavior, habitat, and predation threat.
That both competition and predation alter activity and
habitat selection by small mammals is not a novel observation
(Abramsky et al. 1998; Brown 1988; Kotler et al. 1988), and
an either–or paradigm emphasizing the importance and role of
only 1 of these factors is no longer productive. Efforts should
continue to focus on quantifying and characterizing the
relative importance of each of these, the context in which
one is more or less influential than the other, and the
mitigating role of contingencies such as microhabitat, resource
availability, and assemblage composition.
THE INFLUENCE OF BIOTIC COMPARED WITH
ABIOTIC FACTORS
By definition, deserts are influenced strongly and clearly by
abiotic factors (Cloudsley-Thompson 1975; Laity 2008; Ward
2009; Whitford 2002), but the magnitude, frequency, and
predictability of these can vary greatly such that their relative
roles can differ markedly from region to region. Research on
ecological structure and function throughout the 1970s and 1980s
emphasized the role of biotic factors, but in the past
10–20 years the importance of abiotic factors and their role
in establishing the context for biotic influences has gained
attention. Fox (2011) addresses this issue from a different
perspective. Deeper insight into the role of extrinsic drivers such
as episodic rainfall events and the relative importance of density
dependence compared with density independence generally
require longer time series or good fortune, or both, and as a result
few studies have been able to dissect the role of biotic compared
with abiotic factors, which may influence local systems over very
different temporal windows and have very different magnitudes.
In arid environments most species are well adapted to
limited availability of water, and small mammals in most
1165
deserts respond positively to rainfall (Previtali et al. 2009;
Shenbrot et al. 2010; Thibault et al. 2010b). The role of
precipitation can be far from simple or linear, however, and
long-term biotic responses to rainfall can be confounded with
changes in shrub cover and in small mammal species
composition (Thibault et al. 2010b). Of course, too much
water can negatively influence ecosystem functions. At Portal,
Arizona, only by tracking small mammals monthly were
researchers able to document the community-wide consequences of extreme rainfall events. In September 1983 heavy
rains were implicated in a catastrophic decline of Dipodomys
spectabilis (Valone and Brown 1995). A single storm dropped
about 130 mm of rain in the vicinity of this site within 1 week.
The subsequent decline in numbers of D. spectabilis was
attributed cautiously to destruction of underground food
stores, although other options could not be eliminated.
In a 2nd event at the same site monsoonal rains dropped
approximately 30 mm of rain in less than 2 h, causing sheet
flooding about 35 cm deep. Thibault and Brown (2008)
documented short-term, assemblage-wide responses. Two
kangaroo rat species (D. merriami and D. ordii) were affected
disproportionately by the flooding associated with this rainfall,
with reduced population sizes and reduced survival. In
contrast, numbers of pocket mice (Chaetodipus baileyi and
C. penicillatus) increased immediately after the flood, and
these species exhibited increased survival. Thibault and
Brown (2008) argued that this event effectively reset longterm demographic trends (see also Lima et al. 2008).
As noted above, Kotler et al. (2005) and Ovadia et al.
(2005) studied intraspecific interactions in G. a. allenbyi in
a year when the dominant G. pyramidum was at very low
numbers. This occurred in the winter of 1994–1995 when
rainfall was .250% of normal, leading to extensive
development of soil crusts that stabilized most sand dunes
and to greatly reduced population densities of the dominant
competitor, G. pyramidum.
In northern Chile we have observed a similar resetting of
community dynamics following periodic heavy rains, most
associated with El Niño periods (Gutiérrez et al. 2010;
Meserve et al. 2003, 2009). These remarkable demographic
responses to El Niño–associated rainfall have promoted a
general consensus that small mammal dynamics in northern
Chile are governed primarily by extrinsic factors and that
density-dependent intrinsic feedback loops are only secondary
influences on survival and reproductive rates. Over the past
decade, however, numerous studies on P. darwini from a
separate site in north-central Chile (Aucó, about 80 km
southeast of Fray Jorge) have demonstrated conclusively that
intrinsic feedback on such parameters as population density
(Lima and Jaksic 1998b), population growth rate (Lima and
Jaksic 1999b; Lima et al. 2002), survival (Lima and Jaksic
1999c; Lima et al. 2001), recruitment (Lima and Jaksic 1999c;
Lima et al. 2001), maturation rate (Lima et al. 2001), and
reproduction (Lima and Jaksic 1998a) interact with both
predation and climate to determine the population rate of
change at any given period. These studies also have shown
1166
JOURNAL OF MAMMALOGY
variation in the influence of different factors on the rate of
population growth over spatial scales as small as north- and
south-facing slopes on either side of a single creek (Lima and
Jaksic 1998a; Lima et al. 1996).
Recent analyses from Fray Jorge further quantified the
relative role of intrinsic compared with extrinsic factors on the
dynamics of 2 species of small mammals (Previtali et al.
2009). Using 17 years of monthly small mammal censuses,
indirect surveys of both terrestrial and aerial predator activity,
and weather data recorded at an on-site weather station,
Previtali et al. (2009) placed small mammal dynamics in the
context of food resources, predator activity, and climatic
drivers such as rainfall (see also Gutiérrez et al. 2010; Meserve
et al. 2009, 2011). In spite of enormous population
fluctuations in response to rainfall, the dynamics of the most
common and consistently present species at this site (O. degus
and P. darwini) are dominated by direct density dependence,
especially intraspecific competition. Thus, data from both
Aucó and Fray Jorge in Chile clarify that biotic interactions
can play key roles even in systems that appear largely
structured by abiotic drivers. Somewhat surprisingly, however,
Previtali et al. (2009) extracted no evidence of an important
role of predation on either species at Fray Jorge. We know that
this is not true in the strict sense—O. degus there has increased
survival (Meserve et al. 1993) and decreased vigilance
behavior (Lagos et al. 1995) where predators have been
excluded. However, the importance of predation evidently is
subordinate to abiotic influences, and further work should
strive to assess when and under what conditions predation
plays a role in the dynamics of prey species.
Finally, a recent analysis of a 13-year data stream on D.
merriami and D. ordii at Portal, Arizona, has emphasized the
interaction of multiple extrinsic factors (Lima et al. 2008).
Population density of D. merriami is explained best by the
interaction of summer rainfall and numbers of the larger (and
competitively dominant) D. spectabilis. Density of D. ordii is
explained best by summer rainfall alone. The Sonoran and
Chihuahuan deserts receive both summer and winter rains, and
earlier work had shown that Dipodomys influences the winter
annual plant assemblage but not the summer annual
assemblage (Guo and Brown 1996), leading to speculation
that winter rains were more influential in the dynamics of
these rodents. The application of logistic modeling helped to
clarify that a combination of intra- and interspecific
interactions and summer precipitation best explains the
dynamics of these kangaroo rat species.
It should not be surprising that the clearest examples of the
relative roles of biotic and abiotic drivers come from longterm field studies. The unpredictability of extreme abiotic
events greatly reduces the probability of their being documented in the 1- to 3-year field projects favored by graduate
education and typical funding periods (Cody and Smallwood
1996; Hobbie et al. 2003). Replicate sites in the desert regions
already under study would be useful to assess the extent to
which existing studies are representative of the broader desert
areas in which they occur.
Vol. 92, No. 6
ASSEMBLAGE STRUCTURE AND COMPOSITION
Understanding of the factors governing the structure and
composition of desert small mammal assemblages has
increased over the past several decades. Local species
composition clearly is a function of the pool of species
available to colonize a site and the resources available at a site
(Brown et al. 2000, 2002; Brown and Kurzius 1987; Fox and
Brown 1993; Kelt 1999; Kelt et al. 1996, 1999; Morton et al.
1994). Apart from such ‘‘snapshot’’ studies over large spatial
scales (see ‘‘Competition Compared with Predation’’ above),
it has been long-term research with experimental exclusions
that have been key to understanding organismal and
community responses to both artificial and natural biotic
perturbations. Unfortunately, such studies are rare and very
difficult to maintain for extended periods. The longest-running
such study in arid regions is J. H. Brown’s program near
Portal, in southeastern Arizona, and much of this section
emphasizes work done there (see also Brown 1998; Thibault
et al. 2010b). Given the general lack of comparison sites,
however, the extent to which this site characterizes other aridzone small mammal faunas is not entirely clear, as I allude to
at the end of this section.
When research at Portal was initiated in 1977, Dipodomys
was removed experimentally from a series of replicate sites.
No other species of seed-eating small mammals increased
their use of energetic resources and thereby compensated for
the energetic resources made available by the exclusion of
Dipodomys (Brown 1998; Brown et al. 1986) until Bailey’s
pocket mice (C. baileyi) immigrated to this site in 1996.
Within only a few years energetic consumption by this species
had compensated for 90% of the missing Dipodomys (Ernest
and Brown 2001a), and its influence was complementary
rather than redundant to that of Dipodomys (Thibault et al.
2010a). This delayed response reflected the time required for 1
or more C. baileyi to reach this site and underscores the
importance of large-scale spatial dynamics in local ecological
interactions (Peterson and Parker 1998; Ricklefs and Schluter
1993; Wiens 1989), although smaller-scale dynamics also can
influence community assembly and dynamics (Milstead et al.
2007).
Over 25 years gradual changes in vegetative structure in
southeastern Arizona resulted in substantial changes in small
mammal species composition at the Portal site. Although
species richness remained roughly constant at this site, largebodied species such as D. spectabilis declined in abundance
and smaller species (Chaetodipus and Perognathus) increased.
Mean body mass at this site dropped by about one-half and
was paralleled by near doubling in mean abundances. In spite
of these changes, net energy consumption remained essentially
constant (White et al. 2004), supporting the hypothesis that
total resource availability at this site has remained fairly
constant, with consumption of these resources being gradually
redistributed among the constituent species present.
Ernest and colleagues (Ernest and Brown 2001b; Ernest
et al. 2008) have treated the Portal data set as an example of
zero-sum, or compensatory, dynamics in which the available
December 2011
SPECIAL FEATURE—DESERT SMALL MAMMAL ECOLOGY
resources are sufficient to support a given biomass allocated
across constituent species, and changes in the abundance of
any of these species is compensated by reciprocal changes in 1
or more other species. The energetics of community assembly,
structure, and resilience is a field that is just beginning to be
investigated, and further efforts in other arid systems would be
helpful in resolving whether the Portal data set is typical or
anomalous. The energetic compensation that occurred at their
site with the immigration of C. baileyi is perhaps the best
example of this dynamic, although the stability of energy
consumption in the face of changes in relative abundance of
large and small rodents outlined above supports this as well.
The underlying assumptions of zero-sum dynamics have yet to
be tested on small mammal communities elsewhere, and the
extent to which the diversity of granivorous species at Portal
allows for this is not clear.
Goheen et al. (2005) applied a random-walk simulation to
a 23-year data stream from Portal to quantify the extent
of compensation as species immigrate or become locally
extirpated. In their simulation they allowed for species
colonization or local extinction within biologically reasonable
parameters, and for comparison with the observed species
richness at the Portal site they calculated 2 metrics (the
coefficient of variation in simulated species richness and the
range in local species richness) for each 23-year simulation.
Not surprisingly, the observed trajectory in richness was much
less variable than simulated trajectories, underscoring that
observed richness is not a consequence of random extinctions
and immigrations. When they dissected this pattern to the 3
trophic groups of small mammals at this site, however, only
the relatively speciose granivore guild (15 species) exhibited
patterns significantly less variable than predicted with a
random walk. The more depauperate herbivore and insectivore
guilds (4 and 2 species, respectively) did not vary more or less
than in the random-walk simulations. Although Goheen et al.
(2005) rightly argued that small mammals comprise only
subsets of the latter 2 guilds in the Portal area (other
herbivores include rabbits, peccaries, and deer; other insectivores include 2 genera of lizards), the richness of the granivore
guild at this site might have increased the probability of this
trophic group exhibiting compensatory dynamics. Of course,
Goheen et al. (2005) studied compensation in terms of species
richness, whereas Ernest and colleagues emphasized energetic
compensation, so these studies are not contradictory. How
readily either pattern (taxonomic or energetic compensation)
can be extended to other sites or regions remains to be
assessed. Negev Desert rodent assemblages include a number
of species that differentially occupy distinct habitats; those
found in more than 1 habitat appear to be strongly influenced
by density-dependent habitat selection (Shenbrot et al. 2010),
and taxonomic compensatory responses might be expected
here. In northern Chile, by contrast, it seems highly unlikely
that experimental exclusion of any species in Fray Jorge
would result in replacement by ecologically similar species
that are not already present there—the regional pool simply is
not large enough. What is not clear is whether Fray Jorge is
1167
more or less representative of global conditions than the Portal
data set and whether energetic compensation is as likely in
systems of lower species richness.
FOOD HOARDING AND INFLUENCES ON VEGETATIVE
ECOLOGY AND HABITAT STRUCTURE
Despite granivory as a trophic specialization being relatively
uncommon outside of North American deserts (Fox 2011; Kelt
et al. 1996; Kerley and Whitford 1994; Morton et al. 1994), seed
consumption—seasonally or as part of an omnivorous diet—
remains common in desert small mammals. Consequently,
assessment of seed availability and consumption, and the
influence of the latter on vegetative and community ecology,
remains important for understanding desert ecology. Many
small mammals also play important roles as folivores,
consuming photosynthetically active tissues and reducing
survival of germinating seeds. At 1 extreme rodents in the
Namib Desert of southern Africa consumed 100% of green
plant material locally available (Perrin and Boyer 1994). Much
less work has been done on the ecological role of folivorous
small mammals (e.g., smaller than lagomorphs) than on the role
of granivores (or graminivores—Kerley et al. 1997), however,
so I will focus my attention here on granivory.
Many rodents store seeds either in scatterhoards or
larderhoards. Whereas scatterhoards generally are placed
superficially in the soil and yield moderate to high numbers
of germinating plants (Brodin 2010), larderhoards (used also
by ants) are deep under the surface, resulting in low
germination (Longland et al. 2001). Not all small mammal
species cache the same way, of course, and some species are
more prone to cache seeds in microhabitats with greater
probability of seedling establishment (Hollander and Vander
Wall 2004). Consequently, some plants appear to have
developed a mutualistic association between heteromyid
rodents that use scatterhoarding (Longland et al. 2001), and
Vander Wall (2010) argued that plants have manipulated
animals to be effective seed dispersers. Some seed dispersal
associations reflect obligate mutualisms for the plants
(Vander Wall et al. 2006). In contrast, heteromyid foraging
and hoarding reduces the density of seeds in the seed bank,
and germinating seedlings, of the introduced annual weed
Salsola paulsenii (Longland 2007), and differential hoarding
by heteromyid rodents in sandy rather than rocky habitats
appears to influence the spatial distribution of Indian
ricegrass (Achnatherum hymenoides—Breck and Jenkins
1997).
The structure of the relationship between consumer and
prey is highly contextual, and additional subtleties are certain
to be uncovered with further work. A laboratory study of 6
heteromyid rodents from the Great Basin (Jenkins and Breck
1998) documented a positive association between body size
and larderhoarding activity, whereas a separate study on 8
heteromyid rodents from the Mojave and Sonoran deserts
(Price et al. 2000b) found that scatterhoarding increases in
prevalence with body size and that Mojave rodents tend to
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JOURNAL OF MAMMALOGY
scatterhoard more than similar-sized Sonoran taxa. Price et al.
(2000b) argued that caching behavior can facilitate coexistence among granivorous species (see also Price and Mittler
2006) and that differences between their study and that of
Jenkins and Breck (1998) might reflect different laboratory
structure and protocols. Further work to resolve the role of
behavior, community composition, and environmental influences on caching behavior would be productive.
Recent studies have emphasized how rodents smell buried
seeds (Vander Wall 2003; Vander Wall et al. 2003), the
relative effectiveness of different species in dispersing seeds
of focal plants (Hollander and Vander Wall 2004), and the role
of seed preference in caching strategies (Breck and Jenkins
1997; Leaver and Daly 2001). In the Monte Desert Taraborelli
et al. (2009) compared the ability of 4 murid rodents to detect
buried seeds of millet, sunflower, and creosote bush presented
singly or in groups of 6 seeds. They noted dramatic differences
between species in their ability to detect buried seeds. Not
surprisingly, all 4 species found grouped seeds more readily
than single seeds, and even more so when placed in moist
substrate. The benefit associated with moist substrate has been
noted previously (Johnson and Jorgensen 1981; Vander Wall
1995, 1998). The reduced ability to detect smaller caches
likely underlies field observations that very small caches (5
seeds) were unlikely to be removed by D. ordii regardless of
soil moisture or cache depth (Geluso 2005).
Additionally, individuals redistribute caches (Jenkins et al.
1995), presumably allowing for rapid caching near food
sources and subsequent redistribution to reduce the probability
of pilferage by other foragers. The role of pilferage or
secondary dispersal from hoards (Leaver and Daly 2001;
Preston and Jacobs 2001; Price and Joyner 1997; Price et al.
2000a; Roth and Vander Wall 2005) can be substantial—as
high as 30% per day (Vander Wall and Jenkins 2003). Likely
in response to this, Dipodomys adjust their hoarding strategies
depending on the composition of the small mammal
assemblage, shifting from larderhoarding to scatterhoarding
when conditions preclude them from protecting centralized
food stores (Daly et al. 1992). In the Great Basin pilferage of
scatterhoards deposited by D. merriami is greater by
conspecifics than by pocket mice (primarily Perognathus
longimembris), and they scatterhoard more when potential
competitors are mainly conspecifics rather than P. longimembris (Murray et al. 2006). In the Sonoran Desert pocket
mice (Chaetodipus) tend to larderhoard and D. merriami
scatterhoard, and whereas the former pilfer from each other
and from Dipodomys, the latter rarely pilfer other scatterhoards (Leaver and Daly 2001). In the laboratory G. a.
allenbyi shifted from larderhoarding to scatterhoarding as the
distance to a food source increased. In contrast, G. pyramidum
larderhoards at all distances, but as travel time increases, it
places larderhoards closer to food sources (Tsurim and
Abramsky 2004). Also in a laboratory setting D. merriami
adjusted caching behavior depending on the value of available
food (Leaver and Daly 1998). In Chile O. degus from a
montane population (about 2,600 m elevation) uses both
Vol. 92, No. 6
larder- and scatterhoarding, whereas those from a lowelevation population (about 450 m elevation) use only
scatterhoarding (Quispe et al. 2009); the authors speculated
that larderhoarding is favored under harsher environmental
conditions.
Most studies on hoarding strategies and their influence on
plants have been done in North America. Although a number
of studies have addressed caching behavior in the Palearctic,
very few have emphasized desert regions, and most date from
the 1970s or earlier (Vander Wall 1990). Jerboas (Dipodidae)
generally do not store food, whereas gerbils (e.g., Meriones,
Rhombomys, and Tatera) do, but the ecological implications
of this have received little study. Although hamsters (such
as Cricetulus, Cricetus, Mesocricetus, and Phodopus) are
prodigious hoarders, most work on hoarding by these animals
continues to be conducted on domesticated strains (Vander
Wall 1990).
Relatively little work has been done on hoarding by small
mammals in South American arid regions (although see
Quispe et al. [2009] outlined above). In the Monte Desert
Graomys griseoflavus and Eligmodontia typus scatterhoard,
preferentially under shrubs and at distances up to 580 cm from
the food source (Giannoni et al. 2001). Rodents at Ñacuñán
Reserve (Mendoza, Argentina) scatterhoard the large seeds of
Prosopis flexuosa, but only at 200 cm from the source
(Campos et al. 2007).
The influence of hoarding strategies and associated roles in
seed dispersal remains an arena with abundant opportunities.
Research on how foraging activities by small mammals, and
birds and ants, affect ecological structure and function would
be helpful in understanding how patterns in North America
reflect or contrast with those in other global deserts.
Ecological engineers and keystone species.—Some mammals disproportionately influence the ecology of arid systems
by modifying nutrient cycling, vegetative structure, and the
distribution and survival of seeds, and by physical disturbance
or biopedturbation. Many mammals serve as keystone species,
and a subset of these physically modify their environment
(keystone modifiers in Mills et al. [1993]) and serve as
ecological engineers. North American woodrats (Neotoma)
build large nests (middens) that ameliorate microclimatic
conditions, indirectly favoring a number of invertebrate
species, and soils associated with these middens have higher
organic matter and nitrogen mineralization than reference soils
(Whitford and Steinberger 2010). Physical effects via soil
disturbance and movement are most apparent for those species
that burrow, either fully fossorial species (such as pocket
gophers [Geomyidae], tuco-tucos [Ctenomys], coruros [Spalacopus], and mole-rats [Spalacidae and Bathyergidae]) or
those that reside in subterranean burrow systems for safety and
food storage but forage on the surface (e.g., Dipodomys,
prairie dogs [Cynomys], plains vizcachas [Lagostomus],
springhares [Pedetes], cavies [Caviidae], and great gerbils
[Rhombomys opimus]).
Some Dipodomys in North American deserts build mounds
that can be 1 m tall and 3–5 m in diameter and last decades
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SPECIAL FEATURE—DESERT SMALL MAMMAL ECOLOGY
(Compton and Hedges 1943). D. spectabilis has dramatic
effects on plant community structure (Guo 1996), with its
mounds supporting unique plant assemblages and species
otherwise rare in surrounding areas, although this could be
due partially to the preference of D. spectabilis for areas with
high forb and grass abundance and that are relatively open
and disturbed (Andersen and Kay 1999). Whatever the cause,
burrowing activities of this species increase local habitat
heterogeneity and result in higher soil nitrogen and higher
nitrogen mineralization rates, increased microbial activity,
higher infiltration rates, higher plant biomass, and different
plant species composition than surrounding areas (Ayarbe
and Kieft 2000; Guo 1996; Hawkins 1996; Hawkins and
Nicoletto 1992; Moorhead et al. 1988; Mun and Whitford
1990). Their burrows provide key habitat for a number of
vertebrates and invertebrates (Hawkins and Nicoletto 1992)
and comprise hot spots for soil fungi (Hawkins 1996). Guo
(1996) studied spatial distribution of ephemeral plants on and
adjacent to mounds of D. spectabilis, treating them as an
example of the middomain effect, where species richness was
greatest at the ecotone between mounds and surrounding
terrain. Additionally, patterns in biomass of both annual and
perennial species indicate clear influences of mound
structure. Similar differences occur at larger spatial scales,
because the exclusion of Dipodomys from experimental plots
results in significant increases in some plant species and
significant declines in others (Brown and Heske 1990; Heske
et al. 1993). The giant kangaroo rat (Dipodomys ingens)
appears to have a similar role where it occurs (Schiffman
1994; Williams et al. 1993), whereas the other large kangaroo
rat, D. deserti, might have a less pervasive influence on plant
assemblages, perhaps reflecting its use of much sandier
substrates that do not retain the signature of its burrowing and
foraging activities and the more stable substrates favored by
D. spectabilis and D. ingens.
The systemic and pervasive influence of Dipodomys spp.
has led to their characterization as keystone species or as a
keystone guild (Brock and Kelt 2004; Brown and Heske 1990;
Fields et al. 1999; Goldingay et al. 1997). Dipodomys is not
unique in this regard, because many other desert small
mammals engineer their environments. Cynomys frequently
are considered to function as ecosystem engineers (Ceballos et
al. 1999; Davidson and Lightfoot 2006, 2008; Davidson et al.
2008; Van Nimwegen et al. 2008) or as keystone species
(Bangert and Slobodchikoff 2000; Ceballos et al. 1999; Cully
et al. 2010; Davidson and Lightfoot 2006, 2007, 2008;
Davidson et al. 2008; Kotliar et al. 1999; Miller et al. 1994,
2007). Both black-tailed (C. ludovicianus) and Gunnison’s (C.
gunnisoni) prairie dogs increase landscape heterogeneity
within desert grasslands and provide subterranean refuge for
numerous species.
A recent series of papers has assessed individual and
combined keystone effects of D. spectabilis and either C.
ludovicianus or C. gunnisoni on arthropod and lizard
abundance and on patterns of landscape heterogeneity. These
papers demonstrated clearly that these species operate in
1169
a complementary fashion such that neither replaces the
ecological role of the other. In northern Mexico the structure
of plant communities on mounds of both C. ludovicianus and
D. spectabilis differed significantly from nonmound sites
(Davidson and Lightfoot 2006). At a larger spatial scale the
combined influence of both rodent species was associated with
significantly higher species richness than occurred with either
species alone. At both spatial scales, however, multivariate
ordination on plant species clearly separated all treatments,
underscoring the complementary and nonredundant role of
each keystone species. Similar complementary responses to
Dipodomys and Cynomys activities were reported for arthropods (Davidson and Lightfoot 2007), lizards (Davidson et al.
2008) for abiotic parameters such as soil disturbance, organic
material, and forb cover, and for activity by other animals
(Davidson and Lightfoot 2008). Davidson et al. (2010)
documented similar synergistic effects of C. ludovicianus
and cattle (Bos taurus).
Most desert regions have small and fully fossorial species
of mammals, but the effect of these relative to other
burrowing species has not been well quantified (in contrast,
much work has been pursued in nondesert regions—
Cameron 2000; Reichman and Seabloom 2002). In North
America Kerley et al. (2004) argued that the shorter temporal
duration of pocket gopher (Geomys and Thomomys) burrows
relative to those of Dipodomys should result in lesser
consequences for the physical or chemical properties of soils
and on the vegetation found on mound soils. Supporting this,
the only consistent response to pocket gopher activity at their
sites in the Chihuahuan and Sonoran deserts is reduced bulk
density of soils, which should increase infiltration of rainfall.
Moreover, this difference was significant at only 2 of their 3
study sites; no other parameter measured was significant at
more than 1 site, and most showed no patterns at all. The age
of these burrow systems was both varied and difficult to
quantify, however, such that the limited results documented
could reflect advanced age of the burrows studied.
Surprisingly little work has been done to assess the roles of
keystone or engineering species in Palearctic deserts. The
engineering role of Indian crested porcupines (Hystrix indica)
has been well documented (Alkon 1999; Boeken et al. 1998;
Gutterman 2003; Shachak et al. 1991; Wilby et al. 2001), but
these qualify only marginally as small mammals. A large body
of literature exists on the role of R. opimus as both a keystone
species and ecological engineer, although most of this is in
Russian (see Bondar’ et al. 1981) and not readily accessible to
western readers. However, at least 1 lucid review in English
distills much of this information (Naumov and Lobachev
1975). R. opimus is highly social and diurnal. It develops
complex burrow systems and stores large quantities of food
(to 30–40 kg). C14 dating methods have indicated that these
burrows can be occupied by ‘‘many generations of these
animals over many hundreds or even thousands of years’’
(Naumov and Lobachev 1975:555). Burrow systems are
sufficiently extensive that they alter the temperature and the
humidity of the ground. Vegetation at the center of the colony
1170
JOURNAL OF MAMMALOGY
is completely destroyed, and activities of R. opimus (bringing
cut plant parts into burrows, defecation, and urination) enrich
the soils, leading to growth of new plants especially along the
periphery of the colony and making these structures physically
distinct from surrounding areas and quite visible. Accentuating this, the transport of deeper soils to the surface and edge of
a colony leads to a depression that becomes broader and
deeper with time. As is the case for Cynomys and Dipodomys,
Rhombomys burrows provide refuge for many invertebrates
and other vertebrates and often represent the only escape from
an otherwise harsh climate. Naumov and Lobachev (1975)
summarized studies that list .200 invertebrate species found
in burrows of R. opimus (in contrast to only 38 species on the
surface at 1 site) and .60 species of vertebrates at some areas.
In the Aral Karakum 87% of mammals, 20% of birds, and
81% of reptiles and amphibians use the burrows of R. opimus
to various extents, including as ‘‘regular burrow-mates’’
(those that permanently live and reproduce in these burrows—
11 species of mammals, 6 birds, 3 reptiles, and 1 amphibian)
and ‘‘lodgers’’ (those that use these burrows frequently but
have their own refuges—4 mammals, 3 birds, and 3 reptiles).
In northern Egypt fat sand rats (Psammomys obesus)
influence vegetation dynamics both directly and indirectly,
and over both short and long terms. Reflecting the herbivorous
habits of Psammomys, however, their impacts are qualitatively
different from those of Dipodomys, although the underlying
mechanism for both genera includes both foraging and
burrowing activities (Brown and Heske 1990; El-Bana 2009).
South American drylands host their own suite of keystone
and engineering small mammals. Spalacopus cyanus (Contreras and Gutiérrez 1991; Contreras et al. 1993), Ctenomys
(Campos et al. 2001; Lara et al. 2007; Tort et al. 2004), cavies
(Galea and Microcavia—Borruel et al. 1998; Tognelli et al.
1999), and Lagostomus maximus (Branch et al. 1996, 1999;
Villarreal et al. 2008) alter their environments, in some cases
dramatically. Whether these species have keystone roles or are
merely engineering their environment with less pervasive
influences is fodder for ample further research.
One South American species for which data are compelling
is L. maximus, a social, herbivorous caviomorph rodent that
builds large underground dens—vizcacheras. L. maximus, like
H. indica, qualifies only marginally as a small mammal, but its
influence is substantial and lasting. It is a central-place
forager, and as such its influence on vegetation declines with
distance from the vizcachera (Branch et al. 1996, 1999). After
drought-induced local extinction of a colony, the signature of
the vizcachera remains a structural habitat feature for years,
with dramatically altered vegetation presumably in response to
the foraging and digging activities of the now-extirpated
vizcachas. In addition to central-place reduction of grasses,
forbs, and both small shrubs and all shrubs combined, L.
maximus collects coarse woody debris to cover its burrows,
leading to a redistribution of litter and litter carbon : nitrogen
ratios (Villarreal et al. 2008). Additionally, transport of caliche
to the surface results in significantly greater concentrations of
phosphorus in surface soils than occurs away from burrow
Vol. 92, No. 6
areas. Hence, L. maximus affects not only the spatial
distribution of vegetation but also the vertical distribution of
resources, and this influence persists long after the local
abandonment of vizcacheras.
Ctenomys spp. have heterogeneous influences on plants. In
the Monte Desert cover by herbs and by Larrea divaricata
were lower at 1 site disturbed by Ctenomys mendocinus but
not at another, whereas Larrea cuneifolia was significantly
lower at both sites (Campos et al. 2001). Although cavies
(both Galea and Microcavia) and Ctenomys are important
herbivores in the Monte Desert (Borruel et al. 1998; Tognelli
et al. 1999), the latter appear to have more pervasive effects,
leading Tort et al. (2004) to argue that herbivory by Ctenomys
might be the single most important plant–animal interaction
in the Monte Desert. At a high-elevation Puna Desert site
total plant cover is much lower in areas disturbed by C.
mendocinus. Although soil nutrients do not differ between
disturbed and undisturbed sites, plant species diversity
(Shannon–Wiener index) and species density (number of
species per unit area) are greater at undisturbed sites, and both
species richness and mean species richness are higher in
disturbed sites (Lara et al. 2007). Given the varied responses
to Ctenomys activity, further work to clarify under what
conditions they have positive as opposed to negative effects
should be a focus of further study.
Perhaps surprisingly, no work has been pursued on the
keystone role of small, social, semifossorial mammals such as
O. degus, a likely analog to Cynomys and Rhombomys, albeit
operating at different spatial scales. Fuentes et al. (1983) noted
that O. degus reduces seedling survival up to about 5 m from
shelter (rock walls that provide protection) but that introduced
European rabbits (Oryctolagus cuniculus) forage more widely
and consequently are a much more pervasive influence on
successional processes. Surprisingly, the prediction of Fuentes
et al. (1983) that this might shift the composition of Chilean
matorral to less palatable species has not spawned further
work. Comparable work in more arid regions of Chile only
recently has begun (Gutiérrez et al. 2010; Madrigal et al. 2011;
Meserve et al. 2009, 2011). Because European rabbits likely
function as keystone species (Delibes-Mateos et al. 2007) the
consequences of their introduction to arid ecosystems globally
are potentially serious.
CONCLUSIONS
The ecology of small mammals in desert systems
continues to be an exciting and dynamic field. However, even
this brief review raises more questions than answers. One
reason is that methods and questions pursued in different
deserts are a function of the interests of individual scientists,
and drawing comparisons between results from different
desert regions is complicated by the pursuit of different
questions and the use of different approaches. In some cases
replication of studies is politically difficult, financially
challenging, or both. It would be useful to establish additional
projects comparable to the one in Portal, Arizona, in other
December 2011
SPECIAL FEATURE—DESERT SMALL MAMMAL ECOLOGY
North American deserts, or even elsewhere in the Chihuahuan
Desert, to assess the generality of this study even within North
America, but such luxury seems unlikely. Some conclusions,
however, do emerge.
First, each desert is a unique product of its distinct
evolutionary history, with different lineages that have
responded to different constraints and been confronted by
different opportunities over time. Moreover, these deserts all
differ in both contemporary and historic abiotic influences,
leading to differing resource availability and differing forms
of seasonality. Brown (1995:189–191) referred to these as the
‘‘history of lineage’’ and the ‘‘history of place.’’ Ecological
processes likely function similarly in different desert faunas,
but the patterns observed in different regions are functions of
both historic and contemporary biotic and abiotic influences
and as such are likely to differ. Although Dipodomys spp. have
been ‘‘considered paragons of desert adaptation and a general
adaptive model for small mammals in deserts’’ (Mares
1993a:378), they are uniquely North American, and the
teleological process by which this adaptive model was
developed through regional research on a fascinating fauna
and gradually clarified by appropriate comparative work
elsewhere is a valuable lesson in scientific progress. This
makes Dipodomys no less impressive in their response to the
challenges of desert life.
Second, our understanding of the role of competition and
predation in assemblage structure and composition and
foraging behavior has increased greatly, but many questions
remain unanswered. Competition clearly influences small
mammal foraging ecology and even patterns of assemblage
composition, but its role relative to other factors appears to
differ from one desert region to another. Predation is a
terminal event for victims, and thus the selective pressure to
avoid participation is very strong. The threat of predation
clearly modifies small mammal behavior and demography, but
at least at Fray Jorge it appears to be subsumed beneath a
broader abiotic influence of rainfall (Previtali et al. 2009).
Although both competition and predation have been well
studied individually, surprisingly little work has compared
them directly. Manipulative experiments in the Negev Desert
indicate that threat of predation overwhelms competitive
pressure, and numerous studies have documented shifts in
habitat selection in response to real or perceived predation
threat. Further work to assess responses to different types of
predators—such as snakes, canids, and raptors—would be
particularly interesting. In many deserts snakes are seasonally
active, leading to seasonal shifts in foraging activities and
habitat selection by small mammals. Many raptors are
migratory, and where appropriate, further work on behavioral
responses to predation threats should aim to integrate such
temporal variability in both aerial and terrestrial threats.
Third, the role that mammalian seed consumption plays in
plant evolutionary ecology and ecosystem processes deserves
continued attention. This is particularly true for nonspecialist granivores and their influence on seed dispersal, plant
reproductive strategies, and plant evolutionary ecology,
1171
especially integrating nonmammalian granivores such as ants
and birds (Garb et al. 2000; Longland et al. 2001; Thompson
et al. 1991).
Fourth, the relative importance of biotic and abiotic factors
varies regionally. For example, whereas summer rainfall
mediates intrinsic dynamics among Dipodomys in Arizona
(Lima et al. 2008), it is the El Niño–associated rains every 4–
7 years that reset ecological conditions for small mammals in
northern Chile (Gutiérrez et al. 2010; Meserve et al. 2009,
2011). The relative importance of intrinsic and extrinsic
influences on demographic parameters remains an important
area of study, especially in the face of global climate change
(Meserve et al. 2009; Previtali et al. 2010). Related to this,
zero-sum ecological structure (Ernest et al. 2008) is an
exciting general principle and appears to hold true in some
systems (such as Arizona small mammals or tropical trees),
but its generality remains unclear and untested.
Fifth, further work is warranted on the role of small
mammals as keystone species and ecological engineers, and
in particular on when and where these have positive compared
with negative influence on ecological structure or dynamics.
The effects of D. spectabilis, for example, can vary regionally.
Annual plant species richness is greater on mounds of D.
spectabilis (and especially at mound edges) than between
mounds in Arizona (Guo 1996), but the reverse is the case in
northern Mexico (Davidson and Lightfoot 2006). Similarly,
the effect of Ctenomys on shrubs varies across sites (Campos
et al. 2001; Lara et al. 2007; Tort et al. 2004). Clarification of
how, when, and why extrinsic factors facilitate or inhibit these
roles has particular importance for ecological function.
Deserts have been important natural laboratories for the
continued development and testing of ecological theory. They
continue to provide dynamic venues for both observational
and manipulative field experiments, and small mammals
generally are sufficiently abundant to yield statistically and
ecologically meaningful results. Further developments are
limited only by the enthusiasm and creativity of the scientific
community, and every indication is that the intellectual
trajectory of the past few decades will continue into the
foreseeable future.
RESUMEN
Originándose en las revoluciones conceptuales de los años
sesentas y setentas, la investigación en ecologı́a de pequeños
mamı́feros de zonas desérticas ha progresado notablemente en
las dos últimas décadas. Las áreas con mayor énfasis incluyen
el rol de influencias extrı́nsecas (p. ej., clima) en contraste con
las influencias intrı́nsecas (p. ej., denso-dependencia) en el
crecimiento de la población y en las métricas asociadas, el rol
de la competencia y de la depredación al influir en las
decisiones de forrajeo y selección de hábitat, la influencia de
pequeños mamı́feros en la estructura y la composición de la
comunidad a través de su consumo y redistribución de
los materiales vegetales y sus mayores influencias como
ingenieros ecológicos y como especies (o gremios) claves. Es
1172
JOURNAL OF MAMMALOGY
curioso el reciente énfasis sobre la base energética de la
composición de ensambles y por ende merece mayores
esfuerzos, como ası́ también, la generalidad de la dinámica
de suma cero requiere una mayor evaluación. Los sistemas
desérticos siguen siendo el foco de mucha investigación
ecológica y los pequeños mamı́feros continúan siendo figuras
centrales en el entendimiento de la interacción entre factores
bióticos y abióticos y entre elementos intrı́nsecos y extrı́nsecos. Los pequeños mamı́feros de desiertos en todo el mundo
ejemplifican la importancia de diversos enfoques de investigación ecológica, incluyendo experimentos locales con manipulaciones ecológicas, monitoreo demográfico a largo plazo y
estudios tanto en el laboratorio como en el campo sobre
ecologı́a de forrajeo y de comportamiento.
ACKNOWLEDGMENTS
I thank P. L. Meserve and C. R. Dickman for inviting me to
participate in the symposium on which this paper is based. For
comments that greatly improved the manuscript and its global
coverage I thank P. L. Meserve, B. Fox, and especially G. Shenbrot
and 1 anonymous reviewer for guiding me to literature that eluded
my initial review. A. Previtali and C. Iudica improved the Spanish
summary greatly. Credit is due to the many students of small
mammal ecology whose efforts have made this synthesis possible.
This work was partially funded by the National Science Foundation
(most recently DEB-0947224 to P. L. Meserve and DEB-0948583 to
DAK) and the University of California, Davis.
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Special Feature Editor was Barbara H. Blake.