WHAT RESOURCES ARE AVAILABLE TO DESERT GRANIVORES:SEED RAIN OR SOIL SEED BANK?

764

Ecology, 78(3), 1997, pp. 764–773q 1997 by the Ecological Society of America

WHAT RESOURCES ARE AVAILABLE TO DESERT GRANIVORES:SEED RAIN OR SOIL SEED BANK?

MARY V. PRICE AND JAMIE W. JOYNER1

Department of Biology, University of California, Riverside, California 92521 USA

Abstract. Patterns of resource availability mold many ecological processes, but weknow little about the availability of resources to consumers in nature, even for well-studiedsystems such as the granivorous animals of North American deserts. What we do knowabout seed resources in deserts is based primarily on seeds extracted from soil samples,but this might present a distorted view of resource availability if animals mostly harvestnewly produced seeds before they enter the soil seed bank. In order to assess how largethe distortion might be, we simultaneously monitored the seed bank and ‘‘seed rain’’ overa 19-mo period in the eastern Mojave Desert of California. The seed bank averagedø106 000 seeds/m2 and 38 g/m2, much higher than values reported for other North Americandesert sites. This corresponds roughly to the seed production of a single year, since dailyseed rain averaged 262 seeds/m2 and 0.26 g/m2. However, input from the seed rain did notaccumulate in the soil. Instead, the seed bank decreased by a daily average of 114 seeds/m2 and 0.007 g/m2 during our study. This suggests that virtually all seeds germinate, die,or are harvested by granivores soon after being dispersed. Large seeds comprised a greaterfraction of the seed rain than of the seed bank, suggesting that such seeds are differentiallydepleted, probably by granivores, before they enter the soil. Because seed drop was seasonal,temporal variation comprised a significant component of among-sample variance in theseed rain. Temporal variance in the seed bank was much smaller, presumably becausegranivores harvested most of the seed rain. Conversely, spatial variance was a significantcomponent for the seed bank, but not the seed rain, perhaps as a result of spatial patternsof seed harvest or seed caching by granivores. By virtue of these variance patterns, as wellas other attributes, seeds in the soil present different challenges to granivores than do newlyproduced seeds. Our understanding of desert granivore foraging and community ecology,and of granivore–seed interactions, depends critically on choosing the appropriate measureof seed availability to granivores.

Key words: food storage; granivory; heteromyid rodents; Mojave Desert; resource availability;resource dynamics; seed bank; seed caching; seed rain.

INTRODUCTION

Spatial and temporal heterogeneity in the availabilityof resources molds ecological processes at many levels,from the behavior and morphology of individuals tothe dynamics of populations, coexistence of species,and functioning of ecosystems. Despite the central im-portance of resources, however, we can only rarelymeasure resource availability precisely or understandthoroughly the processes that determine it. This ig-norance constrains our ability to answer many ecolog-ical questions.

It is not that ecologists have been lazy; several dif-ficulties confront those who try to measure the avail-ability of resources to consumers in nature. First, someforms of a resource may be unavailable because theyare toxic, of poor quality, or difficult for consumerswith particular morphologies or sensory abilities to de-

Manuscript received 30 January 1996; revised 20 May1996; accepted 21 May 1996; final version received 9 July1996.

1 Present address: Department of Biology, University ofNevada, Reno, Nevada 89557 USA.

tect or process; we need to account for this and measureonly usable resources. Second, what we record, gen-erally with random sampling, is likely to underestimatethe resources actually encountered by the consumer.The animal may use a nonrandom search strategy thatyields higher encounter rates than does random search,it may respond to cues we do not detect, or it may beknowledgeable about the recent history of exploitationwithin a particular foraging area and avoid searchingin depleted areas (Possingham 1989). Finally, and mostimportantly, we often characterize resource availabilityin terms of the standing crop, the abundance at oneplace and time, rather than in terms of cumulative re-source input and consumption. Whereas such a ‘‘snap-shot’’ of resources may yield an accurate picture ofresource availability at a moment in time, it is unlikelyto give an accurate measure of availability over longertime periods because resources are dynamic. Equalstanding crops can result from high rates of productionbalanced by high rates of consumption, or from lowproduction balanced by low consumption, but cumu-lative resource availability to consumers is higher in

April 1997 765SEED RAIN AND SOIL SEED BANK IN DESERTS

the first case. In assessing resource availability overany substantial period of time, therefore, it is insuffi-cient to measure the standing crop; one also shouldmeasure turnover (Wiens 1984).

Assemblages of specialized granivores that inhabitNorth American deserts are well-studied by ecologists,and our knowledge of them illustrates several of thepoints just raised. On the one hand, we now understanda good deal about properties of seeds and of seed patch-es that affect the ability of these animals to find, har-vest, and ingest resources (Brown et al. 1979, Priceand Jenkins 1986, Kotler and Brown 1988, Vander Wall1991, 1993, Crist and MacMahon 1992, Randall 1993,Reichman and Price 1993). We know that changes inthe size of granivore populations closely reflect pre-cipitation-related changes in seed production (e.g.,Brown et al. 1979, Brown and Harney 1993). We alsoknow that the structure of granivore communities iscorrelated with average productivity (Brown et al.1979, Brown and Harney 1993) and with spatial andtemporal heterogeneity in factors that affect the costsand benefits of foraging (Price and Brown 1983, Kotlerand Brown 1988, Brown and Harney 1993, Reichmanand Price 1993). We know much less about the dy-namics of seed input and consumption. With consid-erable effort, workers have extracted seeds from sam-ples of the top few centimeters of desert soils, underthe assumption that this measures at least the standingcrop of resources available to granivores (e.g., Frenchet al. 1974, Nelson and Chew 1977, Mehlhop and Scott1983, Reichman 1984, Hassan and West 1986, Priceand Reichman 1987, Kemp 1989, Crist and MacMahon1992). A handful of studies has gone further to estimateseed production by plants, or input to the soil surfacevia the ‘‘seed rain’’ falling into seed traps (Tevis 1958,Soholt 1973, French et al. 1974, Pulliam and Brand1975, Whitford 1978). We are aware of only two studies(French et al. 1974, Pulliam and Brand 1975) that haveattempted to compare patterns of standing crop in thesoil seed bank with the seed rain and seed consumption,and thus to more completely characterize resource dy-namics.

Our purpose in this paper is to add to the sparseknowledge of resource dynamics in desert granivoresystems by reporting on patterns of temporal and spa-tial variation in the soil seed bank and seed rain in theMojave Desert. From discrepancies between patternsfor the standing crop and input, we conclude that gran-ivores at this site may make little use of the soil seedbank, contrary to what previous workers have assumed(ourselves included, e.g., Price and Reichman 1987).Instead, the animals appear to rely mostly on newlyproduced seeds. This possibility has major implicationsfor our understanding of the community ecology ofdesert granivores, some of which we discuss.

THE STUDY SITE

We worked at 1250 m elevation in the eastern MojaveDesert, 135 km east of Barstow, California, USA

(Flynn 159 USGS quadrangle, T8N R12E S18; 348479N, 1158399 W), in Granite Cove, a portion of the Uni-versity of California’s Sweeney Granite MountainsDesert Research Center. Cattle were removed from theCenter when it was established in the early 1980s. Thestudy site is on a gently sloping piedmont, with soilsof coarse sands derived from weathered granite. Thesite supports a diverse desert shrubland vegetation withelements from the Sonoran, Mojave, and Great BasinDeserts (Thorne et al. 1981). Common shrubs includeAcacia greggii, Yucca schidigera, Larrea tridentata,Hymenoclea salsola, Coleogyne ramosissima, Salaza-ria mexicana, and Acamptopappus sphaerocephalus.Most precipitation results from winter frontal storms,but summer convective storms bring significant rainfallin some years. Yearly totals from 1986 through 1994averaged 23.8 cm, with 63% falling in cool months(November–April) and 37% in warm months (May–October).

Dominant granivores at the site are heteromyid ro-dents (M. V. Price, personal observation). Two kan-garoo rat species, Dipodomys merriami and D. pana-mintinus, are abundant and active all year, whereas thesingle pocket mouse species, Perognathus longimem-bris, is active from April to October only. Several moreomnivorous Peromyscus species that also eat seeds areless abundant than heteromyids in most years (M. V.Price, unpublished data). Granivorous ants are rare atthis site, perhaps because of its high elevation. Gra-nivorous birds are most abundant in fall and winter.

METHODS

The seed rain

We established 12 sampling stations spaced 10 mapart along a 110-m transect through a gently slopingarea of homogeneous vegetation and topography. Ateach station, two seed traps were placed 50–75 cmapart in an open space $1 m from a shrub canopy(hereafter ‘‘Open’’ microhabitat), and two traps wereplaced under the canopy of the nearest shrub of $1.5m canopy diameter, one to the northeast and one to thesoutheast (hereafter ‘‘Bush’’ microhabitat). Prevailingwinds are from the northwest and can gust to $100km/h.

Seed traps consisted of a 6.3 cm diameter plasticfunnel inserted into a 100 mL plastic specimen cup ofthe same diameter (Fig. 1). The trap was buried withits rim 0.5 cm above the soil surface. Insects enteringthe funnel could not find their way out again, and thestem of the funnel (1.2 cm diameter) was too narrowto admit rodents. We initially installed traps on 24 April1992 and collected and replaced them on 15 August1992, 8 November 1992, 15 February 1993, 2 May1993, 24 June 1993, and 22 September 1993. The finalcollection was on 26 November 1993. Samples col-lected on 15 February 1993 were discarded because wehad neglected to put drainage holes in those cups, and

766 Ecology, Vol. 78, No. 3MARY V. PRICE AND JAMIE W. JOYNER

FIG. 1. Design of traps used to sample the seed rain. Therim of the funnel was seated onto the rim of the cup with abead of silicon sealant. Small holes in the bottom of the cupprovided drainage.

seeds became moldy. Samples also were discardedfrom seed traps that had been unearthed by wind, water,or animal disturbance.

We examined the material that fell into seed trapsunder a dissecting microscope, and recorded numbersof apparently viable seeds (those that did not crumblewhen probed with forceps) of each species as an es-timate of the total seed rain during each sampling pe-riod. The cumulative seed rain was divided by the num-ber of days in the sampling period to estimate dailyseed rain. This may be an underestimate for specieswhose seeds are dispersed in structures with linear di-mensions much larger than 1.2 cm. Such seeds mightaccumulate in the funnel, where they could be har-vested by granivores, rather than falling into the spec-imen cup. On the other hand, traps in the Open micro-habitat may have overestimated the seed rain. Somecontained sand, an indication that they accumulatedwind- or water-borne material (including seeds) froman area larger than the 31.2-cm2 area directly above thecup.

Seed rain is an accurate estimate of the total resourceinput to the system only if granivores do not harvestseeds directly from plants before seed dispersal. Bothrodents and ants do clip fruits directly from low-grow-ing herbaceous plants, but they also harvest dispersedseeds on the ground, as do many granivorous birds(Reichman and Price 1993; M. V. Price, personal ob-servation). We assume here that ground-foraging is thedominant foraging mode: Crist and MacMahon (1992)reported that only 5% of foraging harvester ants re-moved seeds directly from plants; the granivorous ro-dents common to Granite Cove rarely climb (Lemenand Freeman 1986, Reichman and Price 1993); andground-feeding bird species dominate the avian gran-ivores common to the study site (M. V. Price, personalobservation).

The soil seed bank

We collected a soil sample from within 2 m of eachseed trap, and from the same microhabitat, whenevertraps were installed or replaced. The only exceptionwas that soil samples were not taken on 15 August1992. Samples were taken with a circular corer, 6.3 cmin diameter, to a depth of 2 cm, and were stored inpaper bags. We were careful not to disturb vegetationnear seed traps or to resample previously cored points.

Soil samples were air-dried for $1 mo in the labo-ratory, and then weighed. Fine silt was first removedby passing each sample through a sieve with a meshsize (0.25 mm) that retained the smallest seeds. Thecoarse fraction was then mixed with a saturated solu-tion of K2CO3, and the organic material was decantedonto a preweighed disk of coarse filter paper in a Buch-ner funnel and then rinsed with tap water to removethe salt. The filter paper was removed, oven-dried at608C, and reweighed to estimate the mass of the organicmaterial. In most cases, we searched only a represen-tative subsample of the organic fraction for seeds. Theseed number in the entire sample was estimated bydividing the number recorded in the subsample by thefraction (by mass) of the original organic material thatwas subsampled (see Price and Reichman 1987 for fur-ther details).

Seed masses were obtained from voucher specimensof all species encountered in samples, and the totalmass of seeds in soil or trap samples was estimated asa product of seed number and per-seed mass. We ver-ified species identifications by comparing voucherswith specimens in the herbarium of the University ofCalifornia, Riverside. Our nomenclature follows Hick-man (1993).

STATISTICAL ANALYSIS

To compare spatial and temporal heterogeneity in theseed bank vs. the seed rain, and to conduct significancetests, we partitioned total variance among samples into‘‘variance components’’ that were calculated from ex-pected mean squares for a three-factor, mixed-modelANOVA. We used the Scheffe model, which treats ran-dom-factor main effects as the variance, among levelsof the random factor, in marginal means taken overlevels of a fixed factor (Ayres and Thomas 1990, Fry1992). Main effects were sample Date (a temporal com-ponent of variance, treated as a random effect), Station(a spatial component, treated as a random effect), andMicrohabitat (a spatial component, treated as a fixedeffect). The variance among individual samples nestedwithin Date–Station–Microhabitat combinations wasused as the Error variance. We used the GLM Procedureof SAS (SAS Institute 1990) to derive variance com-ponents and to perform approximate significance tests.Most variance components were derived and testedwith the full three-factor model, using the RANDOMstatement and the TEST option. Scheffe variance com-


FIG. 2. Relative abundances of the 22 most numerousseed species recorded in Granite Cove. Values indicate theproportional representation of each species in the pooled seedbank or seed rain sample. Bou ari, Bouteloua aristidoides;Ast sp2, Unknown Asteraceae; Vul oct, Vulpia octoflora; Pecpen, Pectocarya penicillata; Sch bar, Schismus barbatus; Brorub, Bromus madritensis rubens; Cry mic, Cryptantha mi-crantha; Eri wal, Eriophyllum wallacei; Ast sp1, UnknownAsteraceae; Cry cir, Cryptantha circumcissa; Cry uta, Cryp-tantha utahensis; Bou bar, Bouteloua barbata; Lar tri, Larreatridentata; Ama fim, Amaranthus fimbriatus; Fer cyl, Fero-cactus cylindraceus; Aca sph, Acamptopappus sphaeroce-phalus; Hym sal, Hymenoclea salsola; Ero cic, Erodium ci-cutarium; Col ram, Coleogyne ramosissima; Amb dum, Am-brosia dumosa; Cry pte, Cryptantha pterocarya; Ams tes,Amsinckia tesselata.

FIG. 3. Size distribution of seeds taken from soil samples(seed bank) or from seed traps (seed rain).

ponents were calculated from a reduced model thatincluded only Date, Station, Microhabitat, and Date 3Station effects, and were tested over an appropriateerror mean square using the TEST statement. We sub-stituted the error variance from the full factorial modelin calculations of variance components for random fac-tors. Ayres and Thomas (1990) compare SAS vs. Schef-fe treatments of mixed-model ANOVA and provide anexample of a three-factor model that is directly anal-ogous to ours.

F tests were used to test the significance of eachvariance component, using synthetic denominatormean squares and Satterthwaite’s approximation (Sokaland Rohlf 1995) for denominator degrees of freedomas appropriate. The relative magnitude of each com-ponent was expressed as a percentage of the error vari-ance. Negative expected mean squares were set to zero.Patterns of heterogeneity in abundance of seeds in theseed bank and seed rain were compared in terms of therelative magnitudes of variance components, and theirstatistical significance.

RESULTS

The array of seed species observed in traps over-lapped considerably with that observed in the soil. Werecorded totals of 33 and 32 species, respectively, in

soil and trap samples, 23 species of which were com-mon to both. The relative abundances of seed speciesdiffered considerably between soil and trap samples,however (Fig. 2). A primary difference was that large-seeded species (seeds . 1.0 mg) such as Acamptopap-pus sphaerocephalus, Ambrosia dumosa, Amsinckiatessellata, Bromus madritensis rubens, Coleogyne ra-mosissima, Erodium cicutarium, Hymenoclea salsola,and Larrea tridentata, were underrepresented in thesoil relative to trap samples, leading to significant dif-ferences in the size distribution of seeds in the seedrain and the soil seed bank (Fig. 3; G test of hetero-geneity: G 5 8732; df 5 4; P , 0.0001).

Seeds generally were more abundant in soil than intrap samples, whether abundances were expressed interms of density (means of 105 794 vs. 16 479 seeds/m2, respectively) or mass (means of 38.4 vs. 16.7 g/m2,respectively).

In both years of the study, the seed rain was pulsedin time (Fig. 4). When expressed as numbers of seedsdropped per day, input from the seed rain was highestin May when seeds of spring ephemerals were beingdispersed. When expressed as grams per day, however,peaks occurred later because shrubs, which tend to haveheavy seeds, dropped their seeds in summer (Fig. 4).

There was a suggestion that the cumulative seed rainover a sampling period varied with precipitation (Fig.4). 57 767 seeds/m2 were dropped between 1 April 1992and 15 August 1992, in response to 42.4 cm of pre-cipitation during the previous 6 mo (October 1991–March 1992). This was 1.74 times the number in theseed rain between May 1993 and September 1993, aftera drier winter with only 30.0 cm precipitation. Simi-larly, the 4.1 cm of summer precipitation in 1992 (Julythrough September; precipitation in May and June rare-ly stimulates seed germination) was less than that forsummer 1993 (4.8 cm), and fewer seeds were inputbetween August and November 1992 (2820 seeds/m2)than between September and November 1993 (11 996seeds/m2).


FIG. 4. Temporal patterns of precipitation, seed bank, andseed rain. Seed banks (closed circles) represent mean mass(or number) of seeds per square meter. Seed rain values (openbars) represent mean mass (or number) of seeds accumulatingin seed traps per day per square meter. Error bars indicate 1standard error of the mean.

The soil seed bank did not closely reflect inputs fromthe seed rain. In fact, over the five sampling periodsfor which we obtained information both on the changein the seed bank and on input from the seed rain, theseed bank tended to decrease (seed number per squaremeter) or stay approximately stable (seed mass persquare meter), despite input from the seed rain (Fig. 4,Table 1). Only in the spring or early summer of 1993did inputs exceed losses (Table 1), and that temporaryaccumulation was eliminated by fall 1993 (Fig. 4). Ifwe assume that the change in the seed bank over asampling period equals the total input from the seedrain minus the total losses to granivores, germination,and decomposition, then lost input from the seed rainrepresented a large fraction of the estimated totallosses: 69% when expressed as seeds per square meterand 95% when expressed as grams per square meter(Table 1). If we further assume that granivore harvest

is a large component of the total seed loss, then itappears as though newly produced seeds in the seedrain comprise the bulk of their harvest.

Seed abundance in the soil seed bank was signifi-cantly greater in the Bush microhabitat than the Openmicrohabitat, whether abundance was expressed asnumbers or mass per square meter (Fig. 5, Tables 2 and3). In contrast, the Open microhabitat had significantlygreater input from the seed rain than did the Bush mi-crohabitat, when expressed as numbers per square me-ter, and there was no significant microhabitat effectwhen the seed rain was expressed as grams per squaremeter (Fig. 5, Tables 2 and 3). This discrepancy be-tween microhabitat distributions in the seed bank andseed rain could perhaps be an artifact of Open trapssampling material from a larger area than did Bushtraps, which were sheltered by grass stems. However,the discrepancy between microhabitat patterns in theseed bank and seed rain held true for plant specieswhose seeds vary considerably in size and potential forwind dispersal. The six species whose seeds were moreabundant under shrubs, in both the soil and in the seedrain, either were shrub species under which Bush trapswere placed (Larrea tridentata, Coleogyne ramosissi-ma), or were herbaceous species that were closely as-sociated with shrubs in Granite Cove (Schismus bar-batus, Bromus madritensis rubens, Amsinckia tesse-lata, Cryptantha pterocarya).

The magnitude of temporal and spatial heterogeneityin the soil seed bank can be compared quantitativelywith that for the seed rain by partitioning overall vari-ance into components due to Date (a temporal factor)on the one hand, and to Microhabitat and Station (spa-tial factors) on the other. We can also examine inter-actions among these factors. For the seed rain ex-pressed as seed mass per square meter, no variancecomponent was statistically significant (Table 2). Thetwo largest components (Date, and Date 3 Station 3Microhabitat) were only 5% of the error variance, andthe Microhabitat effect was negative, and hence as-sumed to be zero. In contrast, Microhabitat, Station 3Microhabitat, and Date 3 Station 3 Microhabitat weresignificant (P , 0.05) for the seed bank (Table 2).Microhabitat variance was large (110% of Error vari-ance), and Date variance was relatively small (,3% ofError variance).

Variance patterns for the seed bank and seed rainalso were divergent when expressed as numbers persquare meter (Table 3). In this case, three componentsof overall variance in the seed rain were significant(Date, Microhabitat, and Date 3 Microhabitat). Thelargest component was Date (50% of Error variance),Microhabitat was the second largest component (19%of Error variance), and Station variance was relativelysmall. For the seed bank, Station, Date 3 Station, Mi-crohabitat, and Date 3 Microhabitat components weresignificant. The largest component was Microhabitat


TABLE 1. Estimates of inputs and losses to the soil seed bank in the Mojave Desert studyarea, expressed as total number or mass of seeds per square meter during a sampling period.The change in the seed bank is assumed to equal the input minus the cumulative loss, arelationship used to estimate total losses from observed values for the seed bank and seedrain.

Time periodChange†

(seed bank)Input‡

(seed rain) Loss§

A. No. seeds/m2

24 Apr 1992–8 Nov 1992 224 098 60 587 84 68514 Feb 1993–2 May 1993 9605 3680 259252 May 1993–24 June 1993 215 289 17 466 32 755

24 Jun 1993–22 Sep 1993 26020 16 032 22 05222 Sep 1993–26 Nov 1993 214 275 11 996 26 271Total no. seeds/m2\ 250 077 109 761 159,838

B. Seed mass, g/m2

24 Apr 1992–8 Nov 1992 25.38 55.57 60.9514 Feb 1993–2 May 1993 23.44 1.75 5.192 May 1993–24 Jun 1993 15.83 21.25 5.42

24 Jun 1993–22 Sep 1993 29.79 35.14 43.9322 Sep 1993–26 Nov 1993 25.45 14.90 20.35Total seed mass, g/m2\ 28.23 128.61 135.84

† ‘‘Change’’ indicates the seed bank at the end of a time period minus the seed bank at thestart of that time period.

‡ ‘‘Input’’ indicates the input from the seed rain.§ ‘‘Loss’’ indicates the cumulative losses from granivore harvest, germination, and decom-

position of the seed bank.\ Totals are summed values across time periods.

FIG. 5. Mean number (top) or mass (bottom) of seeds persquare meter taken from soil samples (seed bank) or fromseed traps (seed rain) located in Bush and Open microhabitats.Error bars indicate 1 standard error of the mean.

(46% of Error variance), and Date variance was rela-tively small (1% of Error variance).

DISCUSSION

During the 19 months of this study, seed banks atthe Granite Mountains were considerably larger thanthose reported for other desert sites. Kemp (1989) re-ported averages of 8000 to 30 000 seeds/m2, whereasour values were closer to 106 000 seeds/m2, or 38 g/m2.We have no reason to believe that our study occurredduring a period of unusually high seed production andunusually low granivore densities. Perhaps the rarityof harvester ants at our site allows more small seedsto accumulate in the seed bank. The coarse soils alsocould make seeds more difficult for granivores to ex-tract (see Price and Heinz 1984, Price and Podolsky1989), causing them to stop foraging at seed densitiesthat would be profitable under other circumstances(Brown 1988).

Soil and trap samples gave qualitatively similar pic-tures of species composition of the seed resource. Inquantitative terms, however, there were differences thatmay provide insights into the granivore–seed interac-tion. One difference is that large-seeded species wereunderrepresented in the seed bank, relative to accu-mulation in seed traps. This could occur if large seedspersist for shorter periods in the soil, either because ofhigh mortality or high germination rates. Seeds of des-ert perennials, which tend to be large, do frequentlylack the prolonged dormancy characteristic of ephem-erals (Kemp 1989), but large seeds also appear to berelatively immune to mortality from pathogens (Crist


TABLE 2. Variance components for the soil seed bank and seed rain, expressed as mass of seeds per square meter.

Source

Seed rain

s2† %‡ df§ P\

Seed bank

s2† %‡ df§ P\

Date 62.39 4.8 6 0.177 22.48 2.7 6 0.140Station 15.92 1.2 11 0.279 95.60 11.6 11 0.274Date 3 Station 234.52 0.0 62 0.761 204.78 24.7 64 0.189Microhabitat 28.61 0.0 1 0.874 906.95 109.5 1 0.0002Date 3 Microhabitat 1.52 0.1 6 0.421 222.96 0.0 6 0.722Station 3 Microhabitat 232.47 0.0 11 0.685 99.80 12.0 11 0.044Date 3 Station 3 Microhabitat 63.34 4.9 56 0.341 242.08 29.2 63 0.013Error 1287.56 828.05

† Variance.‡ The variance component expressed as a percentage of the error variance (variance components with negative estimates

are set to zero).§ The numerator degrees of freedom for F tests of each variance component. When synthetic mean squares were needed,

denominator degrees of freedom were estimated from Sattherthwaite’s approximation.\ The probability that F . 1.0.

TABLE 3. Variance components for soil seed bank and seed rain, expressed as number of seeds per square meter. Degreesof freedom and conventions are as in Table 2.

Source

Seed rain

s2 % P

Seed bank crop

s2 % P

Date 128 910 098 50.4 0.0001 53 397 863 1.1 0.341Station 1 326 231 0.5 0.371 795 488 148 15.9 0.006Date 3 Station 212 571 452 0.0 0.861 1 846 260 932 36.9 0.0001Microhabitat 48 809 926 19.1 0.019 2 279 861 143 45.5 0.003Date 3 Microhabitat 22 269 039 8.7 0.018 482 658 296 9.6 0.010Station 3 Microhabitat 23 654 939 0.0 0.614 77 860 278 1.6 0.307Date 3 Station 3 Microhabitat 216 009 443 0.0 0.691 94 219 124 1.9 0.420Error 255 929 801 5 009 080 000

and Friese 1993), making it unclear whether or not toexpect a relationship between seed size and persistencein the soil seed bank. Alternatively, granivores maypreferentially harvest large seeds before they enter theseed bank. This seems a plausible explanation for thedeficit of large seeds in the soil at Granite Cove, be-cause heteromyid rodents do prefer large over smallseeds (cf. Randall 1993, Reichman and Price 1993),and because the moist conditions conducive both togermination and to pathogen-induced mortality oc-curred during a minority of sampling periods.

In general, desert granivores act as a ‘‘sieve’’ (sensuHarper 1977) that determines which newly producedseeds enter the seed bank, and this sieve appears to bean important one. Soholt (1973), for example, esti-mated that a stable population of Merriam’s kangaroorats in the Mojave Desert utilized 95% of the annualseed production of Erodium cicutarium, a staple food.Similarly, Chew and Chew (1970) estimated that a Chi-huahuan Desert population of Dipodomys merriamiconsumed 85% of all seeds produced. Whitford (1978)and Tevis (1958) estimated that harvester ants con-sumed large fractions of the annual seed production forpreferred species. Our observations also suggest thatgranivores divert a large proportion of annual seed pro-duction: seed losses exceeded input from the seed rainover the study period, and the ‘‘lost’’ seed rain con-

stituted 69% and 95% of the total losses for seed num-bers and mass, respectively.

If granivores indeed consume most of each year’sseed crop, then they are likely to be limited by newlyproduced seeds, rather than by the seed bank. Severalobservations indicate that the soil seed bank may belargely unavailable to them. First, there is a mismatchbetween observed granivore densities and those den-sities that could be supported over the short term bythe seed bank. For example, individual Merriam’s kan-garoo rats consume ø1 kg seeds/yr (Soholt 1973, Nagyand Gruchacz 1994), so that the 38 g/m2 in the seedbank at Granite Cove could support several hundredindividuals per hectare for a year if the bank were fullyavailable. In fact, Merriam’s kangaroo rats rarely reachdensities .20/ha, and they do seem to be strongly foodlimited (Soholt 1973, Zeng and Brown 1987, Brownand Heske 1990, Nagy and Gruchacz 1994). Second,population densities of granivorous desert rodents re-spond quickly to annual changes in the seed crop, withlittle carryover to subsequent years (O’Farrell et al.1975, Nelson and Chew 1977, Brown and Heske 1990,Price and Kelly 1994). This suggests that each year’sseed production, rather than the more stable seed bank,determines fecundity and mortality. Finally, direct ob-servations of diets indicate that granivorous ants androdents primarily harvest recently produced seeds. Har-


vester ant diets generally track temporal patterns in theavailability of fresh seeds for preferred species (Tevis1958, Rissing and Wheeler 1976, Whitford 1978,Mehlhop and Scott 1983, Crist and MacMahon 1992),avoiding the partially decomposed seeds that haveoverwintered from the previous season’s production(Crist and Friese 1993). Westoby et al. (1982) reportedthat seed banks for several grass species in Australiaremained constant throughout a drought that sup-pressed seed production, whereas ants continued to for-age actively for newly produced seeds of the few plantspecies that managed to reproduce during the drought.Rodents also appear to harvest seeds as they are beingdispersed. M’Closkey (1983) observed that rodent for-aging was concentrated under shrubs that were drop-ping seeds; McAuliffe (1990) observed that rodentsharvested 97% of the seed pods of paloverde trees with-in 1 wk of seed drop; and McAdoo et al. (1983) notedthat Ord’s kangaroo rats shifted from Russian thistleto Indian rice grass as soon as the latter, a preferredfood, began to drop seeds.

If current seed production indeed is critical for desertgranivores, then temporal variation in seed resourcesmay be more ecologically important, and spatial vari-ation less important, than hitherto appreciated. Ourstudy suggests that patterns in the seed rain are char-acterized primarily by temporal variance, in markedcontrast to the spatial variance that characterizes theseed bank: temporal and temporal 3 spatial compo-nents of variance (Date, Date 3 Microhabitat, Date 3Microhabitat 3 Station) were large for the seed rainbut small for standing crop, whereas the reverse wastrue for spatial components (Station, Microhabitat, andtheir interactions). Our interpretation of this pattern isas follows. The seed rain is temporally pulsed becauseof seasonality, and Date 3 Microhabitat interactionsreflect variation among plant species in timing of seeddrop. This temporal variation is not strongly reflectedin the seed bank, because granivores quickly harvestmost of the new production. The pronounced spatialvariance in the seed bank, in turn, could arise at leastpartly from microhabitat preferences or microhabitat-specific variation in granivore harvest efficiency (e.g.,Price and Heinz 1984, Price and Waser 1985, Price andReichman 1987, Price and Podolsky 1989), and fromspatial patterns of seed caching by kangaroo rats (e.g.,Reichman 1984, Daly et al. 1992, Jenkins and Peters1992, Jenkins et al. 1995). It does not appear, from oursamples, that the seed rain is as spatially heterogeneousas is the soil seed bank.

Patterns of heterogeneity in available seed resourcesmay be central to an understanding of granivore com-munity structure, because such heterogeneity can pro-mote coexistence of competing species that specializeon different portions of the resource spectrum (Tilman1982, Chesson 1986, 1991, Kotler and Brown 1988,Brown 1989). The pronounced spatial variance in theseed bank has, therefore, stimulated much interest in

the microhabitat specificity of foraging by coexistingheteromyid rodents (e.g., Price and Brown 1983, Priceand Waser 1985, Price 1986, Reichman and Price 1993)and in the consequences of seed patchiness for relativeforaging efficiency of species that differ in size andmorphology (e.g., Reichman and Obserstein 1977,Reichman 1981, Price 1983, Morgan and Price 1992,Reichman and Roberts 1994) or behavior (e.g., Bern-stein 1975, Davidson 1977). Temporal variance has re-ceived less attention, except in the context of seasonaldistribution of activity (Kotler and Brown 1988, Brown1989). However, if the standing crop represents thelargely unavailable, leftover seed resource, then vari-ance in overall density among microhabitats, degree ofpatchiness, or species composition of the soil seed bankmay be relatively unimportant. Of more importancemay be the ability of animals to persist through tem-poral fluctuations in the abundance of easily harvestedfresh seeds. Many vagile species like birds cope withalternating ‘‘fat’’ and ‘‘lean’’ periods by migration orregional movement (Levey and Stiles 1992). In con-trast, many more sedentary species, including graniv-orous desert ants and rodents, integrate over such pe-riods by storing seeds (Vander Wall 1990). For theseseed-storing species, success may well depend on theability to sequester newly produced seeds before othergranivores do so, and to store them securely againsttheft or spoilage (Reichman et al. 1986, Jenkins andPeters 1992, Jenkins et al. 1995).

In many deserts, temporal variation in seed produc-tion of the sort we document here could, therefore,promote a ‘‘cache economy’’ that shapes granivore–granivore and granivore–plant interactions and opensup hitherto-unappreciated mechanisms for coexistenceof competitors. To evaluate this possibility, we need toknow much more about what resources granivores ac-tually use. We also need to know much more aboutcaching and its consequences: the variation in cachingbehaviors within and among species; the costs and ben-efits of alternative caching strategies (e.g., larderhoard-ing vs. scatterhoarding, Vander Wall 1990, Jenkins etal. 1995); the extent to which caches made by oneindividual are available to others of the same and dif-ferent species (e.g., Daly et al. 1992, Jacobs 1992, Van-der Wall 1991, 1993); the possibility that different spe-cies are specialized as resource concentrators vs. pil-ferers; and the effects of caching on seedling recruit-ment of the plants themselves (e.g., Price and Jenkins1986, Vander Wall 1992, 1994, Heske et al. 1993).

ACKNOWLEDGMENTS

We thank Andy Sanders for help with seed identification;Philippe Cohen and Cindy Stead for encouragement and per-mission to work in Granite Cove; Claudia Luke and Jim Andrefor precipitation records; Nick Waser for critical input, edi-torial suggestions, and encouragement throughout; Ernie Tay-lor and Shannan Szychowski for field assistance; Steve Jen-kins and two anonymous reviewers for helpful comments onthe manuscript; and the University of California, Riverside,Academic Senate for financial support.


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WHAT RESOURCES ARE AVAILABLE TO DESERT GRANIVORES:SEED RAIN OR SOIL SEED BANK?

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