This file was created by scanning the printed publication. Errors identified by the software have been corrected; however, some errors may remain. 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 in­ Three western Great Basin study areas that have under­ sects during much of this time, while ants are relatively gone extensive disturbance were monitored for species com­ inactive above ground when temperatures are cold. By position ofgranivorous rodents. Disturbed habitats at two contrast, nonhibernating rodent species are active forag­ of these sites (Red Rock and Flanigan) recovered with na­ ers for seeds all year. Furthermore, birds and ants glean tive or introduced perennial plants and were dominated seeds largely from the soil surface; rodents dig for buried by heteromyid rodent species, which are important seed­ seeds as well (Johnson and Jorgensen 1981). Thus, rodents dispersal agents for many desert plants. At one of these are often the main consumers of desert plant seeds. In sites, Indian ricegrass-a native perennial grass-rapidly addition to consuming seeds, though, large numbers of dominated the disturbed area, perhaps because of strong seeds are cached by desert rodent species in three families interactions between this grass and local heteromyid rodents. (Heteromyidae-the kangaroo rats, kangaroo mice, and The third site (Noble), which lacks heteromyids, has become pocket mice; Muridae-the New World mice, voles, and infested with an introduced annual weed (medusahead). The woodrats; and Sciuridae-the ground squirrels and chip­ seed dispersal activities ofheteromyids may be important munks). The heteromyids are a diverse group that is well in obtaining desirable responses to disturbance on desert represented in most desert localities. rangelands. Heteromyids and other arid-land rodents can harvest substantial fractions of a given plant species' seed produc­ INTRODUCTION tion. The degree of granivory probably depends both on seed density and on desirability of particular seed types. Granivorous, or seed-eating, animals are the most abun­ Thus, seeds of some plant species are greatly reduced dant and diverse herbivores in North American deserts. by rodents, while others may be barely touched (table 1). This high abundance and diversity is probably due to the From a plant's perspective, it is what the rodent does with generally greater availability and suitability of seeds as the harvested seed that is important. food compared to other types of plant materials in deserts. After seeds are harvested, rodents may consume them Desert plants produce large seasonal flushes of seeds, or cache them in one of two ways (Price and Jenkins 1986). which remain dormant and retain their nutritional quality "Larderhoarding" -practiced by most desert rodents­ for substantially longer periods than other aboveground refers to placing large caches in a centrally located burrow plant parts (Janzen 1971). Even with the seasonal nature or nest. "Scatterhoarding"-practiced mainly by hetero­ of desert seed production, seeds are available to desert myids and to a lesser degree by sciurids-refers instead granivores in the soil seed pool year-round; this is well to placing numerous smaller caches in shallow depres­ illustrated by occasional spring flushes of annual plants sions on the ground surface and covering them with soil. from seeds lying dormant in the soil over one or more win­ ters. These properties of desert plant seeds (seasonal pro­ duction in massive quantities and nutritional retention over time) also make them an ideal food for storing for fu­ Table 1-Previous studies documenting percentages of plant seed ture use. As a consequence, granivorous diets have been production harvested by rodents adopted by various groups of desert animals, and desert plants, having coevolved with these granivores, often ex­ Plant type Seeds hibit adaptations that either reduce levels of seed preda­ (site) harvested Source tion or allow them to capitalize on granivore activities for Percent dispersing their seeds. Here, I concentrate on the latter Annual grasses 93 Pearson 1964 coevolutionary relationship-seed dispersal. (California Central Valley) Various groups of rodents, birds, and seed-harvester Annual grasses 30-65 Borchert and Jain 1978 ants comprise the granivore guild in North American (Southern California) deserts (Brown and others 1979). Birds and ants are to Erodium cicutarium 95 Soholt 1973 a large extent seasonal granivores, especially in northern (Mojave Desert) Larrea tridentata 87 Chew and Chew 1970 (Chihuahuan Desert) Oryzopsis hymenoides 46 McAdoo and others 1983 (Great Basin Desert) Desert plants 30-80 Nelson and Chew 19n Paper presented at the Symposium on Ecology, Management, and Res­ toration of Intermountain Annual Rangelands, Boise, ID, May 18-22, 1992. (Mojave Desert, NV) William S. Longland is Research Ecologist, U.S. Department of Agricul­ Forbs <1 Pulliam and Brand 1975 ture, Agricultural Research Service, Conservation Biology of Rangelands, (Arizona grassland) Reno, NV 89512.

233 It is through scatterhoarding activities that desert rodents heteromyid species, while at the third site, which is domi­ are most likely to have a positive effect on seedling recruit­ nated by an introduced annual weed species, heteromyids ment; larderhoards are generally placed too deep under­ and other scatterhoarders are rare. I also discuss data ground for seedlings to successfully emerge if they germi­ from two experiments: (1) a field study illustrating strong nate. Thus, the net effect of rodents on seedling recruitment interactions between heteromyids and a native animal­ of a particular plant species is largely determined by num­ dispersed grass species, and (2) laboratory seed preference bers of seeds that are removed from the germinable seed tests with captive heteromyids showing that these rodents pool by consumption and larderhoarding versus numbers prefer seeds of this native grass to those of two introduced that persist in scatterhoards for later germination (Price annual grasses. My aim is to illustrate the potential im­ and Jenkins 1986). Scatterhoards that are not recovered portance of scatterhoarding granivores for desert range­ for future consumption may benefit seeds in three different lands by showing examples of desirable successional re­ ways: (1) buried seeds may have a higher probability of sponses to disturbance where these animals are common germination and establishment than unburied seeds and undesirable responses where they are lacking. Cer­ (Vander Wall1990), (2) buried seeds are not vulnerable to tainly, numerous ecological and historical factors combine consumption by nonscatterhoarding granivores (birds and to determine such responses, but plant/animal interactions ants) that harvest seeds only from the soil surface (Price involving native granivores are one such factor that has and JenkinS 1986), and (3) seeds of certain desert plant spe­ received little attention. cies may have enhanced germinability when they have been handled by scatterhoarding rodents (La Tourette and others METHODS 1971; McAdoo and others 1983; Reynolds and Glendening 1949). In this regard, heteromyid rodents, being very com­ Field studies were conducted at two northwestern mon and avid scatterhoarders in North American deserts, Nevada sites (Red Rock, Washoe Co., Reno NW Quad.: are very important components of arid rangeland commu­ T21N.R18E.S14; and Flanigan, Washoe Co., Flanigan nities. Although heteromyids have been known to have Quad. T27N.R18E.S2) and a northeastern California site important effects on range vegetation for some time (for (Noble, Lassen Co., Shaffer Mtn. Quad. T30N.R15E.S27). example, Reynolds 1950), results oflong-term experiments The Red Rock and Flanigan sites were burned in 1985 in the Chihuahuan Desert have recently highlighted the and 1988, respectively, while the Noble site was disturbed ecological significance of these "keystone" granivores; ro­ by extensive grazing of sheep over several decades preced­ dent exclusion experiments have shown that heteromyids ing this study. Prefire vegetation at Red Rock consisted of directly affect the species composition and physiognomy big sagebrush (Artemisia tridentata), Mormon tea (Ephe­ of the local plant community (Brown and Heske 1990). dra viridis ), desert peach (Prunus andersonii), and various Table 2 lists a sample of plant species that have been herbaceous species seeded after a previous fire, especially found germinating from rodent scatterhoards; this list in­ crested wheatgrass (Agropyron desertorum), which domi­ cludes grasses, shrubs, and trees and both native and intro­ nates the postfire vegetation. Prefire vegetation at Flanigan duced species. The native species listed appear to be depen­ consisted largely of big sagebrush, scattered shrubs of other dent on harvesting by animals for dispersal since their seeds native species, and infrequent bunches of Indian ricegrass lack external appendages that could facilitate dispersal by (Oryzopsis hymenoides); Indian ricegrass dominates the other means (for example, wind or adhesion to fur), while postfire community at Flanigan. The Noble site was domi­ the introduced species (cheatgrass) has such appendages nated by low sagebrush Taeniatherum caput-medusae) but that do not need to rely for dispersal on a granivore guild also has squirreltail (Sitanion hystrix) and rare Indian that is unfamiliar with them. ricegrass bunches. Medusahead and cheatgrass (Bromus In this paper, I present data on the species composition tectorum) have invaded undisturbed areas at Noble as well, of granivorous rodent communities at three disturbed study but to a lesser extent. Soils are sand at Flanigan, heavy sites in the western Great Basin Desert. I show that for loam at Red Rock, and clay at Noble. two of these sites, where native plants have recovered well I censused rodent populations by livetrapping twice from disturbance, rodents include mainly scatterhoarding monthly at Red Rock since the 1988 fire, and at irregular intervals at Flanigan and Noble since 1988 and 1991, re­ spectively. I trapped in the disturbed areas and in adja­ Table 2-Previous studies documenting germination of desert plant cent undisturbed (or less disturbed) areas at all three sites. seeds from rodent scatterhoards At Flanigan, I conducted experiments from 1989 to 1991 to quantify numbers of Indian ricegrass seeds harvested Plant species Location Source and cached by heteromyids. Seed harvest was quantified Velvet mesquite Arizona Reynolds and Glendening 1949 by planting single seeds and groups of 2, 10, and 100 seeds Indian ricegrass Nevada McAdoo and others 1983 at various depths (0, 1, 2, 4, or 6 em) in randomly deter­ Antelope bitterbrush California Hormay 1943 mined locations, which were checked after 7 days to deter­ Oregon West 1968 mine if they had been removed by rodents. Seed caching Nevada Vander Wall1990 was quantified by placing petri dishes with 40 g of Indian Palo Verde Arizona McAuliffe 1990 ricegrass seeds labeled with fluorescent dye on the ground Cheatgrass Nevada La Tourrette and others 1971 and locating dye spots left at scatterhoards under UV light the following night. 234 I tested for rodent preferences for Indian ricegrass, kangaroo rat-D. deserti-and little pocket mouse-P. long­ cheatgrass, and medusahead by offering food-deprived imembris) were present as well (table 3). captive rodents from Noble 1.0 g of each seed type in sepa­ Heteromyids were equally or more abundant in disturbed rate petri dishes. Trials were videotaped in the labora­ habitats during early stages of plant succession as in un­ tory. The seed types chosen first and eaten in the largest disturbed habitats at Red Rock and Flanigan, and at the quantities were determined by replaying videos and used latter site there was actually a pronounced increase in as criteria to assess potential preferences. heteromyid species diversity during this recovery. By con­ trast, the only heteromyid species occurring at Noble was RESULTS AND DISCUSSION less common in disturbed than in undisturbed habitat. Al­ though a cause-and-effect relationship cannot be inferred Proportions of various rodent species captured at the from these data, it is interesting to note that the disturbed three study sites are shown in table 3. Four rodent spe­ habitat at Noble, where native perennial plants have been cies were captured at both the Red Rock and Noble study mostly replaced by a medusahead monoculture, is also sites. Only one of the species occurring at Noble is a heter­ depauperate in the scatterhoarding rodents that disperse omyid (Great Basin pocket mouse--Perognathus parous), the seeds of many native plant species. Heteromyids are and this species was rare in the disturbed (medusahead) generally able colonizers of disturbed areas, as indicated habitat. By contrast, a nonheteromyid species (deer by the Flanigan and Red Rock data (table 3) and by an mouse--Peromyscus maniculatus) was caught signifi­ ongoing field experiment at Red Rock (USDA-ARS, unpub­ cantly (P < 0.05) more frequently in the medusahead than lished data). In this experiment, I first demonstrated that in the sagebrush habitat at Noble. Heteromyids occurred three plots in the burned habitat had similar densities of in similar proportions in disturbed and undisturbed habi­ three rodent species (Great Basin pocket mouse, Panamint tats at Red Rock, and were represented by two species kangaroo rat, and deer mouse), after which I removed veg­ (Great Basin pocket mouse and Panamint kangaroo rat­ etation on two of these plots by mowing. Heteromyids re­ Dipoclomys panamintinus) in both habitats. These two mained on the control and mowed plots in similar densi­ species were the earliest colonizers of the burned area af­ ties, but on the latter plots the nonheteromyid species ter the 1988 fire at Red Rock. Six rodent species occurred (deer mouse) disappeared after vegetation removal. This at Flanigan, and all but one of them (white-tailed ante­ suggests that the lack ofheteromyids at Noble is not sim­ lope ground squirrel-Ammospermophilus leucurus) were ply attributable to past disturbance. heteromyids. While only one of the heteromyid species The impressive abundance and diversity ofheteromyid (Merriam's kangaroo rat-D. merriami) was common in rodents in the burned habitat at Flanigan is probably due unburned sagebrush habitat at Flanigan, three were to the dominance of Indian ricegrass in this area. This pe­ quite common in the burned (Indian ricegrass) habitat rennial grass species appears to have evolved a very close (Merriam's kangaroo rat, Panamint kangaroo rat, and interaction with heteromyids. Its seed is highly preferred Ord's kangaroo rat-D. ordii) and two others (desert by these rodents; seeds of other plant species have been

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 domes­ tic sheep disturbed the Noble site. Heteromyid rodents, the primary scatter­ hoarding species at these sites, include species in the genera Dipodomys and Perognathus

Percentage of captures Undisturbed Disturbed Study sHe Rodent species habitat habitat Flanigan: Sagebrush Indian rlcegrass Dipodomys merriami 89 54 Dipodomys ordil 2 27 Dipodomys panamintinus 1 12 Dipodomys desert/ 0 3 Perognathus longimembris 1 3 Ammospermophilus leucurus 7 1 Red Rock: Agropyron/shrub Agropyron Dlpodomys panamintinus 2 16 Perognathus parvus 55 67 Peromyscus maniculatus 14 17 Reithrodontomys mega/otis 29 0 Noble: Sagebrush Medusa head Perognathus parvus 23 2 Peromyscus maniculatus 50 95 Reithrodontomys mega/otis 23 2 Spemophilus latera/Is 4 0

235 found to drop out of heteromyid diets in nature when In­ fur, is more common in the medusahead habitat at Noble dian ricegrass produces seeds (McAdoo and others 1983). than other native plants dependent on animal dispersal Indian ricegrass has a classical animal-dispersed seed mor­ vectors. phology, and seedlings appear to come mainly from hetero­ In conclusion, I suggest that a stronger understanding myid scatterhoards, which generally persist longer after of granivores' effects on native and introduced plant spe­ germination than single seedlings (personal observation). cies may be an important element in understanding suc­ Seeds in these scatterhoards often have 100 percent germi­ cessional processes in desert rangeland plant communi­ nation, partly because heteromyids discriminate against ties. Such information may simply allow prediction of empty and nonviable seeds when harvesting Indian rice­ plant species responses following disturbance based on grass (McAdoo and others 1983). Finally, the germinabil­ knowledge of granivore species composition in a given area. ity of Indian ricegrass is enhanced when the seeds have Eventually though, arid-land restoration efforts may in­ been handled by heteromyids; this may be due in part to clude active management for granivores that play impor­ breaking mechanical dormancy of the seed by removal of tant roles in maintaining native plant communities. Al­ its coat by rodents, but even unshelled seeds that have though range restoration efforts involving active human been handled by heteromyids have improved germinabil­ intervention, such as artificial seeding, may produce more ity (McAdoo and others 1983). rapid results than "natural restoration" by native fauna, Results of field experiments at Flanigan indicated that the latter carries the advantages of reduced financial ex­ up to 50 percent of Indian ricegrass seeds were harvested penditure, of not being logistically restricted by spatial by heteromyids over a 7 -day period. Depth of seeds in the scale, and of ultimately resulting in more "pristine" plant sand had a significant effect on harvest rate (P < 0.05); communities. seeds on or near the surface were harvested in the greatest quantities. Seed density, however, had no effect on harvest ACKNOWLEDGMENTS rate. Single seeds or pairs were harvested at rates similar to groups of 10 or 100, illustrating the efficiency of hetero­ I thank Steve Jenkins, Steve Vander Wall, and Jim myids at locating even low-density soil seed reserves. By Young for thoughtful comments that improved the locating caches containing seeds labeled with fluorescent manuscript. This study is a contribution of the USDA­ dyes, I found that up to 25-35 percent of Indian ricegrass Agricultural Research Service, Conservation Biology seeds harvested by heteromyids were initially cached in of Rangelands Unit, Reno, NV. 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 REFERENCES at Flanigan are fairly high, it was also apparent from dye Borchert, M. I.; Jain, S. K. 1978. The effect of rodent seed traces around rodent burrows and from large amounts of predation on four species of California annual grasses. dyed seeds that I could not locate that many seeds were Oecologia. 33: 101-113. being larderhoarded or consumed. While it is not yet pos­ Brown, J. H.; Heske, E. J. 1990. Control of a desert­ sible to determine net effects of heteromyids at this site on grassland transition by a keystone rodent guild. Sci­ the Indian ricegrass population, it is clear from the rapid ence.250:1705-1707. domination of Indian ricegrass in response to removal of Brown, J. H.; Reichman, 0. J.; Davidson, D. W. 1979. shrubs by fire that a large soil seed reserve was in place Granivory in desert ecosystems. Annual Review of even though this grass was uncommon in the prefire plant Ecology and Systematics. 10: 210-227. community. Because most of the Indian ricegrass popula­ Chew, R. M.; Chew, A E. 1970. Energy relationships of tion at Flanigan consists of clumps of two or more same­ mammals of a desert shrub (Larrea tridentata) commu­ aged individuals, it is likely that this rapid postfire re­ nity. Ecological Monographs. 40: 1-21. sponse was due to rodent scatterhoards providing this seed reserve. Hormay, A L. 1943. Bitterbrush in California. For. Res. Note 34. Washington, DC: U.S. Department of Agricul­ In laboratory seed preference experiments, the only ture, Forest Service. 13 p. rodent species that was common in medusahead habitat at Noble (deer mouse) exhibited a significant (P < 0.05) Janzen, D. H. 1971. Seed predation by animals. Annual preference for medusahead and Indian ricegrass over Review of Ecology and Systematics. 2: 465-492. cheatgrass. Great Basin pocket mice, the only heteromyid Johnson, T. K.; Jorgensen, C. D. 1981. Ability of desert species at Noble, also preferred Indian ricegrass, but rodents to find buried seeds. Journal of Range Manage­ ment. 34: 312-314. avoided medusahead seed. At Noble, established Indian ricegrass plants thrive quite well, but new recruits are La Tourrette, J. E.; Young, J. A; Evans, R. A 1971. Seed seldom found. Although Indian ricegrass may show some dispersal in relation to rodent activities in seral big promise for being established in areas vulnerable to medu­ sagebrush communities. Journal of Range Manage­ sahead infestation, the heteromyids which prefer Indian ment. 24: 118-120. ricegrass seeds and act as its dispersal agents may be lack­ McAdoo, J. K.; Evans, C. C.; Roundy, B. A.; Young, J. A.; ing, th~ limiting the persistence of an Indian ricegrass Evans, R. A 1983. Influence ofheteromyid rodents on population. Other rodents, such as deer mice, may occur Oryzopsis hymenoides germination. Journal of Range commonly in medusahead habitats, but their activities will Management. 36:61-64. not promote the establishment of native, animal-dispersed McAuliffe, J. R. 1990. Paloverdes, pocket mice, and bruchid plant species. This may explain why squirreltail, which beetles: interrelationships of seeds, dispersers, and seed has seed appendages for dispersal by wind or adhesion to predators. Southwestern Naturalist. 35: ·329-337.

236 Nelson, J. F.; Chew, R. M. 1977. Factors affecting seed Reynolds, H. G.; Glendening, G. E. 1949. Merriam kanga­ reserves in the soil of a Mojave Desert ecosystem, Rock roo rat, a factor in mesquite propagation on southern Valley, Nye County, Nevada. American Midland Natu­ Arizona rangelands. Journal of Range Management. ralist. 97: 300-320. 2:193-197. Pearson, 0. P. 1964. Carnivore-mouse predation: an ex­ Soholt, L. F.1973. Consumption of primary production ample of its intensity and bioenergetics. Journal of by a population of kangaroo rats Wipodomys merriami) Mammalogy. 45:177-188. in the Mojave Desert. Ecological Monographs. 43: Price, M. V.; Jenkins, S. H. 1986. Rodents as seed con­ 357-376. sumers and dispersers. In: Murray, D. R., ed. Seed dis­ Vander Wall, S. B. 1990. Food hoarding in animals. persal. Sydney, Australia: Academic Press: 191-235. Chicago: University of Chicago Press. 445 p. Pulliam, H. R.; Brand, M. R. 1975. The production and West, N. E. 1968. Rodent-influenced establishment of utilization of seeds in plains grassland of southeastern ponderosa pine and bitterbrush seedlings in central Arizona. Ecology. 56: 1158-1166. Oregon. Ecology. 49: 1009-1011. Reynolds, H. G. 1950. Relation of Merriam kangaroo rats to range vegetation in southern Arizona. Ecology. 31: 456-463.

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