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SEED USE BY DESERT GRANIVORES
William S. Longland
ABSTRACT
and high-elevation deserts, because most bird species are
resident only from spring through fall, and they eat insects during much of this time, while ants are relatively
inactive above ground when temperatures are cold. By
contrast, nonhibernating rodent species are active foragers for seeds all year. Furthermore, birds and ants glean
seeds largely from the soil surface; rodents dig for buried
seeds as well (Johnson and Jorgensen 1981). Thus, rodents
are often the main consumers of desert plant seeds. In
addition to consuming seeds, though, large numbers of
seeds are cached by desert rodent species in three families
(Heteromyidae-the kangaroo rats, kangaroo mice, and
pocket mice; Muridae-the New World mice, voles, and
woodrats; and Sciuridae-the ground squirrels and chipmunks). The heteromyids are a diverse group that is well
represented in most desert localities.
Heteromyids and other arid-land rodents can harvest
substantial fractions of a given plant species' seed production. The degree of granivory probably depends both on
seed density and on desirability of particular seed types.
Thus, seeds of some plant species are greatly reduced
by rodents, while others may be barely touched (table 1).
From a plant's perspective, it is what the rodent does with
the harvested seed that is important.
After seeds are harvested, rodents may consume them
or cache them in one of two ways (Price and Jenkins 1986).
"Larderhoarding"-practiced by most desert rodentsrefers to placing large caches in a centrally located burrow
or nest. "Scatterhoarding"-practiced mainly by heteromyids and to a lesser degree by sciurids-refers instead
to placing numerous smaller caches in shallow depressions on the ground surface and covering them with soil.
Three western Great Basin study areas that have undergone extensive disturbance were monitored for species composition ofgranivorous rodents. Disturbed habitats at two
of these sites (Red Rock and Flanigan) recovered with native or introduced perennial plants and were dominated
by heteromyid rodent species, which are important seeddispersal agents for many desert plants. At one of these
sites, Indian ricegrass-a native perennial grass-rapidly
dominated the disturbed area, perhaps because of strong
interactions between this grass and local heteromyid rodents.
The third site (Noble), which lacks heteromyids, has become
infested with an introduced annual weed (medusahead). The
seed dispersal activities of heteromyids may be important
in obtaining desirable responses to disturbance on desert
rangelands.
INTRODUCTION
Granivorous, or seed-eating, animals are the most abundant and diverse herbivores in North American deserts.
This high abundance and diversity is probably due to the
generally greater availability and suitability of seeds as
food compared to other types of plant materials in deserts.
Desert plants produce large seasonal flushes of seeds,
which remain dormant and retain their nutritional quality
for substantially longer periods than other aboveground
plant parts (Janzen 1971). Even with the seasonal nature
of desert seed production, seeds are available to desert
granivores in the soil seed pool year-round; this is well
illustrated by occasional spring flushes of annual plants
from seeds lying dormant in the soil over one or more winters. These properties of desert plant seeds (seasonal production in massive quantities and nutritional retention
over time) also make them an ideal food for storing for future use. As a consequence, granivorous diets have been
adopted by various groups of desert animals, and desert
plants, having coevolved with these granivores, often exhibit adaptations that either reduce levels of seed predation or allow them to capitalize on granivore activities for
dispersing their seeds. Here, I concentrate on the latter
coevolutionary relationship-seed dispersal.
Various groups of rodents, birds, and seed-harvester
ants comprise the granivore guild in North American
deserts (Brown and others 1979). Birds and ants are to
a large extent seasonal granivores, especially in northern
Table 1-Previous studies documenting percentages of plant seed
production harvested by rodents
Plant type
(site)
Seeds
harvested
Source
Percent
Annual grasses
(California Central Valley)
Annual grasses
(Southern California)
Erodium cicutarium
(Mojave Desert)
Larrea tridentata
(Chihuahuan Desert)
Oryzopsis hymenoides
(Great Basin Desert)
Desert plants
(Mojave Desert, NV)
Forbs
(Arizona grassland)
Paper presented at the Symposium on Ecology, Management, and Restoration of Intermountain Annual Rangelands, Boise, ID, May 18-22, 1992.
William S. Longland is Research Ecologist, U.S. Department of Agriculture, Agricultural Research Service, Conservation Biology of Rangelands,
Reno, NV 89512.
233
93
Pearson 1964
30-65
Borchert and Jain 1978
95
Soholt 1973
87
Chew and Chew 1970
46
McAdoo and others 1983
30-80
Nelson and Chew 19n
<1
Pulliam and Brand 1975
It is through scatterhoarding activities that desert rodents
are most likely to have a positive effect on seedling recruitment; larderhoards are generally placed too deep underground for seedlings to successfully emerge if they germinate. Thus, the net effect of rodents on seedling recruitment
of a particular plant species is largely determined by numbers of seeds that are removed from the germinable seed
pool by consumption and larderhoarding versus numbers
that persist in scatterhoards for later germination (Price
and Jenkins 1986). Scatterhoards that are not recovered
for future consumption may benefit seeds in three different
ways: (1) buried seeds may have a higher probability of
germination and establishment than unburied seeds
(Vander Wall1990), (2) buried seeds are not vulnerable to
consumption by nonscatterhoarding granivores (birds and
ants) that harvest seeds only from the soil surface (Price
and JenkinS 1986), and (3) seeds of certain desert plant species may have enhanced germinability when they have been
handled by scatterhoarding rodents (La Tourette and others
1971; McAdoo and others 1983; Reynolds and Glendening
1949). In this regard, heteromyid rodents, being very common and avid scatterhoarders in North American deserts,
are very important components of arid rangeland communities. Although heteromyids have been known to have
important effects on range vegetation for some time (for
example, Reynolds 1950), results oflong-term experiments
in the Chihuahuan Desert have recently highlighted the
ecological significance of these "keystone" granivores; rodent exclusion experiments have shown that heteromyids
directly affect the species composition and physiognomy
of the local plant community (Brown and Heske 1990).
Table 2 lists a sample of plant species that have been
found germinating from rodent scatterhoards; this list includes grasses, shrubs, and trees and both native and introduced species. The native species listed appear to be dependent on harvesting by animals for dispersal since their seeds
lack external appendages that could facilitate dispersal by
other means (for example, wind or adhesion to fur), while
the introduced species (cheatgrass) has such appendages
to facilitate dispersal. This is to be expected, since native
plant species have coevolved with local granivores, while
successful invasions of exotics are most likely with species
that do not need to rely for dispersal on a granivore guild
that is unfamiliar with them.
In this paper, I present data on the species composition
of granivorous rodent communities at three disturbed study
sites in the western Great Basin Desert. I show that for
two of these sites, where native plants have recovered well
from disturbance, rodents include mainly scatterhoarding
Table 2-Previous studies documenting germination of desert plant
seeds from rodent scatterhoards
Plant species
Velvet mesquite
Indian ricegrass
Antelope bitterbrush
Palo Verde
Cheatgrass
Location
Source
Arizona
Nevada
California
Oregon
Nevada
Arizona
Nevada
Reynolds and Glendening 1949
McAdoo and others 1983
Hormay 1943
West 1968
Vander Wall1990
McAuliffe 1990
La Tourrette and others 1971
234
heteromyid species, while at the third site, which is dominated by an introduced annual weed species, heteromyids
and other scatterhoarders are rare. I also discuss data
from two experiments: (1) a field study illustrating strong
interactions between heteromyids and a native animaldispersed grass species, and (2) laboratory seed preference
tests with captive heteromyids showing that these rodents
prefer seeds of this native grass to those of two introduced
annual grasses. My aim is to illustrate the potential importance of scatterhoarding granivores for desert rangelands by showing examples of desirable successional responses to disturbance where these animals are common
and undesirable responses where they are lacking. Certainly, numerous ecological and historical factors combine
to determine such responses, but plant/animal interactions
involving native granivores are one such factor that has
received little attention.
METHODS
Field studies were conducted at two northwestern
Nevada sites (Red Rock, Washoe Co., Reno NW Quad.:
T21N.R18E.S14; and Flanigan, Washoe Co., Flanigan
Quad. T27N.R18E.S2) and a northeastern California site
(Noble, Lassen Co., Shaffer Mtn. Quad. T30N.R15E.S27).
The Red Rock and Flanigan sites were burned in 1985
and 1988, respectively, while the Noble site was disturbed
by extensive grazing of sheep over several decades preceding this study. Prefire vegetation at Red Rock consisted of
big sagebrush (Artemisia tridentata), Mormon tea (Ephedra viridis ), desert peach (Prunus andersonii), and various
herbaceous species seeded after a previous fire, especially
crested wheatgrass (Agropyron desertorum), which dominates the postfire vegetation. Prefire vegetation at Flanigan
consisted largely of big sagebrush, scattered shrubs of other
native species, and infrequent bunches of Indian ricegrass
(Oryzopsis hymenoides); Indian ricegrass dominates the
postfire community at Flanigan. The Noble site was dominated by low sagebrush <Artemisia arbuscula) before disturbance and remains so in adjacent undisturbed areas;
the disturbed site has been dominated by an invasion of
medusahead wildrye (Taeniatherum caput-medusae) but
also has squirreltail (Sitanion hystrix) and rare Indian
ricegrass bunches. Medusahead and cheatgrass (Bromus
tectorum) have invaded undisturbed areas at Noble as well,
but to a lesser extent. Soils are sand at Flanigan, heavy
loam at Red Rock, and clay at Noble.
I censused rodent populations by livetrapping twice
monthly at Red Rock since the 1988 fire, and at irregular
intervals at Flanigan and Noble since 1988 and 1991, respectively. I trapped in the disturbed areas and in adjacent undisturbed (or less disturbed) areas at all three sites.
At Flanigan, I conducted experiments from 1989 to 1991
to quantify numbers of Indian ricegrass seeds harvested
and cached by heteromyids. Seed harvest was quantified
by planting single seeds and groups of 2, 10, and 100 seeds
at various depths (0, 1, 2, 4, or 6 em) in randomly determined locations, which were checked after 7 days to determine if they had been removed by rodents. Seed caching
was quantified by placing petri dishes with 40 g of Indian
ricegrass seeds labeled with fluorescent dye on the ground
and locating dye spots left at scatterhoards under UV light
the following night.
I tested for rodent preferences for Indian ricegrass,
cheatgrass, and medusahead by offering food-deprived
captive rodents from Noble 1.0 g of each seed type in separate petri dishes. Trials were videotaped in the laboratory. The seed types chosen first and eaten in the largest
quantities were determined by replaying videos and used
as criteria to assess potential preferences.
kangaroo rat-D. deserti-and little pocket mouse-P. longimembris) were present as well (table 3).
Heteromyids were equally or more abundant in disturbed
habitats during early stages of plant succession as in undisturbed habitats at Red Rock and Flanigan, and at the
latter site there was actually a pronounced increase in
heteromyid species diversity during this recovery. By contrast, the only heteromyid species occurring at Noble was
less common in disturbed than in undisturbed habitat. Although a cause-and-effect relationship cannot be inferred
from these data, it is interesting to note that the disturbed
habitat at Noble, where native perennial plants have been
mostly replaced by a medusahead monoculture, is also
depauperate in the scatterhoarding rodents that disperse
the seeds of many native plant species. Heteromyids are
generally able colonizers of disturbed areas, as indicated
by the Flanigan and Red Rock data (table 3) and by an
ongoing field experiment at Red Rock (USDA-ARS, unpublished data). In this experiment, I first demonstrated that
three plots in the burned habitat had similar densities of
three rodent species (Great Basin pocket mouse, Panamint
kangaroo rat, and deer mouse), after which I removed vegetation on two of these plots by mowing. Heteromyids remained on the control and mowed plots in similar densities, but on the latter plots the nonheteromyid species
(deer mouse) disappeared after vegetation removal. This
suggests that the lack ofheteromyids at Noble is not simply attributable to past disturbance.
The impressive abundance and diversity ofheteromyid
rodents in the burned habitat at Flanigan is probably due
to the dominance of Indian ricegrass in this area. This perennial grass species appears to have evolved a very close
interaction with heteromyids. Its seed is highly preferred
by these rodents; seeds of other plant species have been
RESULTS AND DISCUSSION
Proportions of various rodent species captured at the
three study sites are shown in table 3. Four rodent species were captured at both the Red Rock and Noble study
sites. Only one of the species occurring at Noble is a heteromyid (Great Basin pocket mouse--Perognathus parous),
and this species was rare in the disturbed (medusahead)
habitat. By contrast, a nonheteromyid species (deer
mouse--Peromyscus maniculatus) was caught significantly (P < 0.05) more frequently in the medusahead than
in the sagebrush habitat at Noble. Heteromyids occurred
in similar proportions in disturbed and undisturbed habitats at Red Rock, and were represented by two species
(Great Basin pocket mouse and Panamint kangaroo ratDipoclomys panamintinus) in both habitats. These two
species were the earliest colonizers of the burned area after the 1988 fire at Red Rock. Six rodent species occurred
at Flanigan, and all but one of them (white-tailed antelope ground squirrel-Ammospermophilus leucurus) were
heteromyids. While only one of the heteromyid species
(Merriam's kangaroo rat-D. merriami) was common in
unburned sagebrush habitat at Flanigan, three were
quite common in the burned (Indian ricegrass) habitat
(Merriam's kangaroo rat, Panamint kangaroo rat, and
Ord's kangaroo rat-D. ordii) and two others (desert
Table 3-Relative abundances (percent) of various rodent species occurring in disturbed
and undisturbed habitats at three western Great Basin study sites. Fire caused
the disturbance at the Red Rock and Ranigan sites; extensive use by domestic sheep disturbed the Noble site. Heteromyid rodents, the primary scatterhoarding species at these sites, include species in the genera Dipodomys and
Perognathus
Percentage of captures
Undisturbed
Study sHe
Rodent species
Flanigan:
Dipodomys merriami
Dipodomys ordil
Dipodomys panamintinus
Dipodomys desert/
Perognathus longimembris
Ammospermophilus leucurus
Red Rock:
Dlpodomys panamintinus
Perognathus parvus
Peromyscus maniculatus
Reithrodontomys mega/otis
habitat
Sagebrush
Indian rlcegrass
54
27
12
3
3
89
2
1
0
1
7
Agropyron/shrub
2
55
14
29
Sagebrush
Noble:
Perognathus parvus
Peromyscus maniculatus
Reithrodontomys mega/otis
Spemophilus latera/Is
235
Disturbed
habitat
23
50
23
4
1
Agropyron
16
67
17
0
Medusahead
2
95
2
0
found to drop out of heteromyid diets in nature when Indian ricegrass produces seeds (McAdoo and others 1983).
Indian ricegrass has a classical animal-dispersed seed morphology, and seedlings appear to come mainly from heteromyid scatterhoards, which generally persist longer after
germination than single seedlings (personal observation).
Seeds in these scatterhoards often have 100 percent germination, partly because heteromyids discriminate against
empty and nonviable seeds when harvesting Indian ricegrass (McAdoo and others 1983). Finally, the germinability of Indian ricegrass is enhanced when the seeds have
been handled by heteromyids; this may be due in part to
breaking mechanical dormancy of the seed by removal of
its coat by rodents, but even unshelled seeds that have
been handled by heteromyids have improved germinability (McAdoo and others 1983).
Results of field experiments at Flanigan indicated that
up to 50 percent of Indian ricegrass seeds were harvested
by heteromyids over a 7-day period. Depth of seeds in the
sand had a significant effect on harvest rate (P < 0.05);
seeds on or near the surface were harvested in the greatest
quantities. Seed density, however, had no effect on harvest
rate. Single seeds or pairs were harvested at rates similar
to groups of 10 or 100, illustrating the efficiency of heteromyids at locating even low-density soil seed reserves. By
locating caches containing seeds labeled with fluorescent
dyes, I found that up to 25-35 percent of Indian ricegrass
seeds harvested by heteromyids were initially cached in
scatterhoards, and that scatterhoards contained about 250
seeds on average. The largest scatterhoard found had 1,427
seeds. Although the scatterhoarding rates I have found
at Flanigan are fairly high, it was also apparent from dye
traces around rodent burrows and from large amounts of
dyed seeds that I could not locate that many seeds were
being larderhoarded or consumed. While it is not yet possible to determine net effects of heteromyids at this site on
the Indian ricegrass population, it is clear from the rapid
domination of Indian ricegrass in response to removal of
shrubs by fire that a large soil seed reserve was in place
even though this grass was uncommon in the prefire plant
community. Because most of the Indian ricegrass population at Flanigan consists of clumps of two or more sameaged individuals, it is likely that this rapid postfire response was due to rodent scatterhoards providing this
seed reserve.
In laboratory seed preference experiments, the only
rodent species that was common in medusahead habitat
at Noble (deer mouse) exhibited a significant (P < 0.05)
preference for medusahead and Indian ricegrass over
cheatgrass. Great Basin pocket mice, the only heteromyid
species at Noble, also preferred Indian ricegrass, but
avoided medusahead seed. At Noble, established Indian
ricegrass plants thrive quite well, but new recruits are
seldom found. Although Indian ricegrass may show some
promise for being established in areas vulnerable to medusahead infestation, the heteromyids which prefer Indian
ricegrass seeds and act as its dispersal agents may be lacking, th~ limiting the persistence of an Indian ricegrass
population. Other rodents, such as deer mice, may occur
commonly in medusahead habitats, but their activities will
not promote the establishment of native, animal-dispersed
plant species. This may explain why squirreltail, which
has seed appendages for dispersal by wind or adhesion to
236
fur, is more common in the medusahead habitat at Noble
than other native plants dependent on animal dispersal
vectors.
In conclusion, I suggest that a stronger understanding
of granivores' effects on native and introduced plant species may be an important element in understanding successional processes in desert rangeland plant communities. Such information may simply allow prediction of
plant species responses following disturbance based on
knowledge of granivore species composition in a given area.
Eventually though, arid-land restoration efforts may include active management for granivores that play important roles in maintaining native plant communities. Although range restoration efforts involving active human
intervention, such as artificial seeding, may produce more
rapid results than "natural restoration" by native fauna,
the latter carries the advantages of reduced financial expenditure, of not being logistically restricted by spatial
scale, and of ultimately resulting in more "pristine" plant
communities.
ACKNOWLEDGMENTS
I thank Steve Jenkins, Steve Vander Wall, and Jim
Young for thoughtful comments that improved the
manuscript. This study is a contribution of the USDAAgricultural Research Service, Conservation Biology
of Rangelands Unit, Reno, NV.
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