Recaching of Jeffrey pine (Pinus jeffreyi) seeds

by yellow pine chipmunks (Tamias amoenus):

potential effects on plant reproductive success

Stephen B. Vander Wall and Jamie W. Joyner

Abstract: Animals that scatter-hoard seeds frequently dig up and recache them at new locations. The effect of the recachingof seeds on plant reproductive success was studied in the Sierra Nevada of western Nevada. The fate of 1000 individuallymarked Jeffrey pine (Pinus jeffreyi) seeds initially placed in 100 primary caches in a 10 × 10 array was monitored duringautumn 1995 and spring 1996. Yellow pine chipmunks (Tamias amoenus) quickly removed nearly all of the seeds andrecached many of them in 377 secondary caches containing 727 seeds. Later, rodents dug up most of these caches andtransferred them to 213 tertiary caches (283 seeds), 75 quaternary caches (92 seeds), and 13 quintic (fifth order) caches (13 seeds).Overall, rodents ate 15.3% of the seeds they took from primary through quintic caches, and an additional 71.1% of the seedsdisappeared, probably to underground runways and larders. During our spring survey of the study site, 133 seeds (13.6%)from 84 caches had germinated or were about to germinate. As rodents moved seeds from cache site to cache site, severalchanges occurred that potentially influenced the distribution and survival of Jeffrey pine seedlings. First, the number of seedsper cache decreased. Second, cached seeds were gradually moved farther from the source area. Third, the dispersal distancebetween successive cache sites decreased. Fourth, the distribution of cached seeds became more even. Lastly, more seeds werecached beneath shrubs, which serve as nurse plants for Jeffrey pine seedlings. Consequently, the movement of seeds betweencache sites by chipmunks may increase the probability that Jeffrey pine seedlings will establish from rodent caches.

Résumé: Souvent, les animaux qui dispersent leurs graines de réserve les déterrent pour les recacher ailleurs. Les effets de cetexercice sur le succès reproducteur des plantes a été étudié dans la Sierra Nevada, dans l’ouest du Nevada. Le sort de 1000graines de pins de Jeffrey (Pinus jeffreyi) d’abord enfouies dans 100 caches primaires disposées selon un arrangement 10 × 10a été suivi au cours de l’automne 1995 et du printemps 1996. Les Tamias amènes (Tamias amoenus) ont eu tôt fait derecueillir presque toutes les graines et en ont recaché un grand nombre dans 377 caches secondaires contenant 727 graines. Parla suite, ils ont refouillé la plupart de ces caches et transféré leur butin dans 213 caches tertiaires (283 graines), 75 cachesquaternaires (92 graines) et 13 caches quinaires (13 graines). Dans l’ensemble, les tamias ont mangé 15,3% des graines qu’ilsont manipulées entre les caches primaires et les caches quinaires et 71,1% du reste des graines sont disparues, probablementemportées dans des tunnels souterrains ou des garde-manger. À l’inventaire du printemps, 133 graines (13,6%) trouvées dans84 caches avaient germé ou étaient sur le point de le faire. Lors du transport des graines d’une cache à une autre, plusieurschangements se sont produits qui ont pu influencer la répartition et la survie des graines de pin. D’abord, le nombre de grainespar cache a diminué. Deuxièmement, les graines cachées ont été déménagées de plus en plus loin de leur point d’origine.Troisièmement, la distance de dispersion entre les caches successives a diminué. Quatrièmement, la répartition des graines estdevenue graduellement plus uniforme. Enfin, les tamias ont caché un plus grand nombre de graines sous les buissons qui sontainsi devenus des plantes protectrices pour les pousses du pin. Il semble que le déplacement des graines d’une cache à uneautre par les tamias augmente la probabilité d’établissement des pousses du pin de Jeffrey à partir des caches de rongeurs.[Traduit par la Rédaction]

Introduction

Burial of seeds, fruits, nuts, and other food items in shallowsurface excavations (i.e., scatter-hoarding) is a common meansof food storage for several groups of birds and rodents. Thispattern of food hoarding is thought to provide an importantmeans of protecting stored food from other animals (Stapanianand Smith 1978; Clarkson et al. 1986; review in Vander Wall1990), and is most frequently observed in species that are un-able to protect a stockpile of food (i.e., a larder) from com-

petitors. In general, the purpose of these food stores is to serveas an energy source during periods of food scarcity. Not allscatter-hoarded seeds and nuts are retrieved, and neglectedpropagules often germinate in the spring. The certainty of ger-mination of seeds in animal caches is sufficient that many plantspecies appear to be adapted to use seed-caching animals astheir primary agent of seed dispersal (Vander Wall and Balda1977; Bossema 1979; Lanner 1982; Tomback 1983; Van-der Wall 1994b).

A growing body of evidence indicates that animals movescatter-hoarded seeds around after the initial caching (DeGangeet al. 1989; Jenkins and Peters 1992; Clarke and Kramer 1994;Jenkins et al. 1995; Vander Wall 1995a). These movementsinclude the transfer of seeds from one cache site to another.Hereafter, we refer to this activity as recaching. Understandingrecaching is important from two perspectives. First, it is

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Received May 7, 1997. Accepted August 28, 1997.

S.B. Vander Wall and J.W. Joyner.Department of Biologyand the Ecology, Evolution, and Conservation BiologyProgram, University of Nevada, Reno, NV 89557, U.S.A.

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important to understand who is moving the seeds, the hoarderor another individual, and how these movements influence thehoarder’s long-term food supply. Do the movements indicatethat an individual is actively managing its food supply, or dothey represent the theft of cached seeds by another individual(i.e., a hoarder–thief interaction)? Second, it is important tounderstand how the movement of seeds influences the prob-ability that new plants will be established, and how the distri-bution of these plants might be altered. Does repeated movingof cached seeds influence the dynamics of hoarder–plant interac-tions in any way?

This study addresses the second perspective: the impact ofrecaching on plant reproductive success. We determined thisby tracing the history of a population of Jeffrey pine (Pinusjeffreyi) seeds moved from primary cache sites to subsequentcache sites. By doing so, we hoped to determine how the dis-tribution of caches changes over time, what proportion of theseeds are eaten as animals repeatedly handle them, and thepotential benefits of recaching to the pine. The fate of seedsbetween initial dispersal and seed germination months or yearslater is often complicated (for a review see Chambers andMacMahon 1994). Determining what happens to seeds duringthis period is crucial in understanding how natural selectionacts on seeds and in determining patterns of plant establishmentin communities. This study, by documenting the movementsof seeds and how these movements influence plant reproduc-tion, may provide insights into these important processes.

We used Jeffrey pine seeds in this study because they arethe preferred food of chipmunks and other rodents at our SierraNevada study site (Vander Wall 1995c), and because previousstudies have revealed that chipmunks and corvids are impor-tant dispersers of these seeds (Tomback 1978; Vander Wall1992a, 1992b, 1993, 1995b, 1995c). Jeffrey pine cones ripenand shed seeds in September. These wind-dispersed seeds areavailable to foragers either on the ground surface or in surfacecaches for 2–3 months until winter snow accumulates. In thespring, the surviving seeds break dormancy and produce aseedling. Long-term dormancy (>1 year) is rare. Considerableevidence gathered here and during previous studies at this site(Vander Wall 1992b, 1993, 1995b) indicates that yellow pinechipmunks (Tamias amoenus) were responsible for most of therecaching of seeds that we observed. Clark’s nutcrackers(Nucifraga columbiana), Steller’s jays (Cyanocitta stelleri),and other birds, although common at the study site, probablyhad little impact on recaching because birds are not very ef-fective at locating seed caches that they did not prepare (Sherryet al. 1981; Vander Wall 1982; Kamil and Balda 1985). Never-theless, it was not our objective to determine who was movingthe seeds or to assess the consequences of recaching on thehoarder’s stored food supply; we will address these questionsin future studies.

Study area

We conducted this study between 1 September 1995 and 19 May1996 at the University of Nevada’s Whittell Forest and Wildlife Areain Little Valley, Washoe County, Nevada (39°15′10"N,119°52′35"W, elevation 1975 m). The research area is located on theeast slope of the Carson Range, 30 km south of Reno and 5 km north-east of Lake Tahoe. Little Valley is ≈8 km long and 2 km wide; theelevation ranges from 1960 to 2680 m. The plot we chose for thisstudy was on level ground and contained numerous antelope bitter-

brush (Purshia tridentata) shrubs and a few Jeffrey and lodgepolepine (Pinus contorta) saplings. Soils consisted of decomposed granitewith little plant litter except for pine needles beneath trees. Immedi-ately surrounding the plot are mature Jeffrey pines, which produced asmall crop of cones in the autumn of 1995. Few bitterbrush seeds,another important food source for chipmunks, were produced in thisarea in the summer of 1995. For more details regarding the study sitesee Vander Wall (1994b).

Materials and methods

We selected 1000 medium-sized, filled Jeffrey pine seeds and dividedthese into 100 groups of 10. We numbered each group of seeds from1 to 100 with indelible black ink. We numbered the opposite side ofeach seed from 1 to 10 within each group, using indelible red ink. Thisnumbering scheme served to uniquely identify all seeds. We alsolabeled all seeds with scandium-46, a gamma emitter with a half-lifeof 84.5 d. Labeling methods are described in Vander Wall (1994b).Each seed coat absorbed ≈1 µCi (1 Ci = 37 GBq) of radioisotope. Wecould detect single seeds from a distance of ≈30 cm.

On 1 September 1995, we established 100 caches of labeled seedsin a 10 × 10 array with 2-m spacing. Each cache contained 10 seedswith the same black cache number on one side and a red seed numberon the other. We buried the seeds in clumps ≈1 cm deep (a depthtypical of yellow pine chipmunk caches), taking care to groom thesurface of the soil to eliminate, as far as possible, signs of disturbance.We inconspicuously marked cache sites with small (3 cm) pieces ofcolored and numbered flagging in the foliage of shrubs and saplingsas high as possible above the cache site (usually 50–100 cm).Hereafter we refer to these caches as primary caches.

On 8 September 1995, we surveyed the grid of primary cachesusing portable Eberline ASP-1 counters with SPA-3 probes (Eberline,Santa Fe, New Mexico) to determine whether caches had been re-moved. We also searched the surrounding area for new caches. Wesearched outwards in all directions from the original caching grid toa distance of at least 10 m beyond the most distant cache found in anyparticular direction. When we discovered new caches, we carefullyexposed the seeds (taking care not to touch the seeds, to avoid leavingour scent), counted them (including unlabeled indigenous seeds), re-corded their cache and seed numbers, determined the cache locationusing Cartesian coordinates with respect to the southwest corner ofthe original caching grid, and collected information on cache micro-habitat. Microhabitat data included distance to the edge of the nearestshrub or sapling, distance to the center of that shrub or sapling, andsubstrate type (mineral soil, light litter (<5 mm deep), or heavy litter(>5 mm deep)). We then reburied the seeds at the cache site andattempted to remove any evidence of our visit. We also located andidentified, if possible, seeds that rodents had eaten and left on theground surface. During our searches, we found 26 seeds with blurredor otherwise illegible numbers, and did not include these seeds in thedata presented here. Consequently, the number of seeds providinguseful data in the study was 974.

We surveyed the area 3 times during the autumn, the final searchencompassing an area of >12 000 m2. Because of the large spatialscale, we were not able to survey the entire area in 1 d, as we wouldhave preferred, but had to spread each survey over a 3- to 4-weekperiod. We conducted a check of all extant cache sites on 2 December1995 to determine the presence or absence of caches just before wintersnow accumulated at the study site. On 19 May 1996, approximately2 weeks after snowmelt, we surveyed all cache sites to determinewhich contained seeds that had germinated or were about to germinate.

Results

Of the original 100 primary caches that we established on the10 × 10 caching grid on 1 September, rodents removed 91within 1 week. Eight other primary caches disappeared later in

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the fall or during the winter, leaving only one of the originalcaches intact at the end of the experiment. Rodents ate some ofthe seeds they took from these primary caches (7.1%), andsome other seeds disappeared (17.2%), but most of the seeds(74.7%) served as the source for 722 new caches made byrodents (Fig. 1). Repeated surveys of the area revealed thatmany rodent caches were ephemeral, and that the history ofseeds was often dynamic (Fig. 2). We found 377 secondarycaches containing 727 seeds. Later we found that rodents haddug up 283 of these seeds and moved them to 213 tertiarycaches. Later still, rodents reburied 92 of these seeds at 75 quater-nary caches. Finally, rodents removed 13 seeds from quaternarycaches and deposited them in 13 quintic (fifth order) caches.

When rodents dug up secondary or subsequent caches, theyseldom ate the seeds at the cache sites. Overall, we foundevidence that rodents ate 8.2% of the seeds they took fromsecondary through quintic caches (Fig. 2). We found the hullsof most of these seeds with the identifying numbers still legiblenear cache sites. A larger portion of the seeds (53.9%) disap-peared. We suspect that rodents ate most of these in under-ground runways or stored the seeds in their undergroundlarders, where we could not detect them. Rodents may haverecached some of these seeds outside the surveyed area, butthis number is probably small because random searches out-side the main search area failed to reveal any.

Our spring survey of the area on 19 May revealed that 133seeds from 84 caches had germinated or were about to germi-nate. This is equivalent to 13.6% of all seeds put out and 10.2%of all caches recorded (including the 100 caches that we estab-lished). Most of the surviving seeds were from secondary andtertiary caches (Fig. 2), but the greatest proportion came fromquintic caches (4 of 13 seeds, or 30.8%).

It was difficult to determine the amount of time that seedsremained at a particular cache site because we never knew howmuch time had elapsed between a chipmunk making a cacheand our finding it, and because we did not know preciselywhen chipmunks removed seeds from a known cache site. Toestimate cache longevity, we took a subset of 160 secondarycaches that we discovered and mapped during a relatively shortperiod (8–11 September) and determined how many were stillpresent on 30 September, a day on which we checked thestatus of all caches located up to that time. Thirty-three cacheswere still present at the end of this 23-d period. Using a for-mula (Vander Wall 1994a) for determining the half-life of apopulation of seeds being removed by foragers, we calculateda cache half-life of 10.1 d. This is equivalent to a mean cacheremoval rate of 6.6% of extant caches per day. The rate ofcache removal appeared to diminish sharply later in the autumn.

The fate of one especially well-documented primary cacheillustrates the ephemeral nature of most caches (Fig. 3). When

Fig. 1. The square shows the location of the 10 × 10 array of 100 primary caches, each containing 10 Jeffrey pine seeds. The circles indicatethe location of 722 secondary through quintic caches made by the yellow pine chipmunks using seeds from the primary caches. Solid circlesindicate sites where animals removed seeds; open circles represent sites where seeds survived to the time of germination in the spring.

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we surveyed the array of primary caches on 8 September 1995,one seed from cache 90 had been eaten and the other nine seedswere gone. We found two of these missing seeds in secondarycache 196 and six seeds in secondary cache 212 on 9 September.

By 10 September, cache 212 had been removed and we foundfive of the six seeds in tertiary cache 250. On 11 September,we found the sixth seed in tertiary cache 359. Also on that daywe found the ninth seed from cache 90 in secondary cache 261

Fig. 2. The fate of 974 seeds from 100 primary caches. The width of the arrows is proportional to the number of seeds following a particularpathway.

Fig. 3. The history of 10 seeds from primary cache 90. The square represents the array of 100 primary caches. Numbered circles representcache sites. Lines show the minimum distance traveled between successive caches. See the text for further details.

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along with one seed from primary cache 76. Sometime before30 September, cache 261 disappeared, and the single seedwas never seen again. On 21 October, we found the single seedfrom cache 359 eaten at the cache site. About 2 weeks later (3and 4 November), we found a cluster of four quaternary caches≈65 m to the southeast made from the five seeds in cache 250.The single seeds in caches 744 and 767 later disappeared andwere never seen again. The two seeds in cache 768 disappeareda few days after we discovered the cache. One of these seedswas never seen again, but the other was found on 18 Novemberin quintic cache 815 along with a seed from primary cache 67(which was in its fourth cache site). The single seed in cache748 was eaten during the winter. On 19 May 1996, we foundtwo seedlings in secondary cache 196 (9 m from the sourcecache) and two seedlings emerging from quintic cache 815(82 m from the source cache). In summary, we discovered the10 seeds from primary cache 90 in a total of 10 cache sites: 3seeds were eaten, 4 were followed for part of their history buteventually disappeared and were presumed eaten, and 3 ger-minated.

We observed changes in three characteristics of caches asseeds were moved from low to higher order cache sites. First,the number of seeds per cache decreased. Primary caches madeby yellow pine chipmunks during other experiments in thesame study area (Vander Wall 1992b, 1993, 1995b) contained3.73 ± 1.90 (mean ± 1 SD) Jeffrey pine seeds (n = 945caches). Secondary caches in this experiment containedroughly half that number (1.93 ± 1.13 seeds/cache, n = 377),and tertiary and quaternary caches contained even fewer (1.33 ±0.66 seeds/cache, n = 213, and 1.39 ± 0.68 seeds/cache, n = 75,respectively). There was a slight increase in the number of seedsin quintic caches (1.62 ± 0.65 seeds/cache), but the sample sizewas small (13). The combined sample of tertiary, quaternary,and quintic caches contained significantly fewer seeds percache than did secondary caches (unpaired t test, t = 8.174,df = 676, P < 0.001).

Second, the median (and mean) distance from cache sitesto their original source (primary) cache gradually increased asrodents recached seeds (Fig. 4). The median distance from theprimary cache of origin was 27.8 m for secondary caches,30.2 m for tertiary caches, 31.5 m for quaternary caches, and28.2 m for quintic caches. Mean values for the same set ofcomparisons are 29.7, 33.2, 36.8, and 38.0 m. The distributionof primary- to secondary-cache distances (Fig. 4a) was nearlysignificantly different from the distribution of primary- totertiary-cache distances (Fig. 4b) (χ2 = 32.723, df = 22, P = 0.07).The distribution of primary- to secondary-cache distances(Fig. 4a) was significantly different from the combined distri-bution of primary- to quaternary- and quintic-cache distances(Figs. 4c and 4d) (χ2 = 32.416, df = 12, P < 0.005).

Third, the median (and mean) distance between subsequentcache sites gradually decreased as rodents recached seeds(Fig. 5). The median distance from primary- to secondary-cache sites was 27.8 m, from secondary- to tertiary-cache sites12.5 m, from tertiary- to quaternary-cache sites 8.8 m, andfrom quaternary- to quintic-cache sites 5.0 m. Mean values forthe same set of comparisons were 29.7, 19.2, 16.6, and 18.0 m.The distribution of primary- to secondary-cache distances(Fig. 5a) was significantly different from the distribution ofsecondary- to tertiary-cache distances (Fig. 5b) (χ2 = 122.072,df = 14, P < 0.001). The distribution of secondary- to tertiary-

cache distances (Fig. 5b) was significantly different from thecombined distribution of tertiary- to quaternary- and quaternary-to quintic-cache distances (Figs. 5c and 5d) (χ2 = 16.134,df = 7, P < 0.025).

The microhabitat distribution of cache sites changed onlyslightly during this experiment. Overall, yellow pine chip-munks made 65% of caches in mineral soil, 31% in light plantlitter, and 4% in heavy plant litter. The proportion of cachesmade in mineral soil versus light and heavy plant litter did notdiffer significantly with cache order (χ2 = 3.255, df = 3, P >0.05). Chipmunks placed 28.2% of caches under the canopyof shrubs, 29.2% at the canopy edge, and 42.5% in the open.In this case, however, the distribution of caches graduallychanged with cache order: 48.2% of secondary caches wereunder or at the edge of a shrub canopy, whereas 64.6% oftertiary through quintic caches were under or at the edge of ashrub canopy (χ2 = 17.053, df = 3, P < 0.001).

Discussion

These data indicate that caches made by yellow pine chip-munks are dynamic: most seeds remain at a given cache sitefor only a fraction of the total storage period. Recovered seedswere not all consumed, but met one of three fates. First, rodentsate some seeds immediately at or near the cache site. This fatewas uncommon, accounting for only 15.3% of all seeds. Sec-ond, rodents carried seeds away, apparently to undergroundburrows, where they either ate them or added them to theirwinter larders. Some of these larder-hoarded seeds might ger-minate, but seedlings cannot establish. We suspect that most ofthe seeds that disappeared in this study (71.1%) met this fate.The percentage of seeds that we did not relocate during thestudy increased with cache order: 17.2% from primary caches,43.7% from secondary caches, 50.2% from tertiary caches,62.0% from quaternary caches, and 61.5% from quinticcaches. The general increase in the percentage of seeds thatdisappeared with increasing cache order has two possible ex-planations: (1) we relocated seeds from caches made earlier inthe cache sequence at a higher rate because we had more timeto look for them, and (2) the probability of rodents taking seedsto a below-ground larder may have increased as winter ap-proached. We suspect that both factors contributed to the ob-served pattern. Third, chipmunks often recovered seeds andrecached them at another site. The percentage of recachedseeds was 74.6% from primary caches, 38.9% from secondarycaches, 32.5% from tertiary caches, and 14.1% from quater-nary caches (mean = 40.0%). The general decline in these per-centages suggests that the probability of rodents recachingseeds on the ground surface may decrease as winter approaches.

Several methodological and sampling biases may have in-fluenced our ability to precisely measure the amount of secon-dary caching exhibited by yellow pine chipmunks. It ispossible that our presence in the study area led to an overesti-mate of the amount of recaching that typically occurs. Ourexcavation of caches may have been perceived by rodents, andthey may have reacted by later moving seeds to new cachesites.The small pieces of flagging we used to mark cache sites,although relatively inconspicuous and placed as high above thecache site as possible, may have helped foragers find cachedseeds, which they then moved to new sites. And our use ofrelatively large and closely spaced primary caches, a design

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Fig. 4. Frequency distributions of the distances between primary caches and secondary caches (a), tertiary caches (b), quaternary caches (c),and quintic caches (d). The solid arrows indicate the median distance for each distribution and the open arrows the mean distance for eachdistribution.

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Fig. 5. Frequency distributions of the distances between primary and secondary caches (a), secondary and tertiary caches (b), tertiary andquaternary caches (c), and quaternary and quintic caches (d). The solid arrows indicate the median distance for each distribution and the openarrows the mean distance for each distribution.

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that we adopted to minimize the handling of radioactive seeds,may have stimulated more secondary caching than would haveoccurred if chipmunks had made the primary caches. On theother hand, it seems likely that we found only a portion of thecaches made by the chipmunks. We do not know the historyof the seeds between their disappearance from one cache siteand our discovery of them elsewhere weeks later, but giventhe amount of recaching observed, it seems likely that manyseeds resided at cache sites which we never discovered. Seedsthat we know to have been in two cache sites may well havebeen in several other sites that we did not know about. Themagnitude of these two types of error may never be known,but the fact that they have opposite effects on the amount of recach-ing which we detected helps to reduce their overall impact.

The amount of recaching observed in this study was con-siderably greater than that seen at the same site in an earlierstudy using antelope bitterbrush seeds (Vander Wall 1995a).In that study, not only was the amount of recaching muchreduced (110 primary caches, 12 secondary caches, and 2 ter-tiary caches from 1000 seeds monitored over 83 d), but seed-transport distances were also much shorter (maximum = 15.9 m,mean = 6.2 m). There are at least two reasons for these dra-matic differences. First, chipmunks are sensitive to the char-acteristics of the seeds they handle. Yellow pine chipmunksappear to value Jeffrey pine seeds much more highly thanbitterbrush seeds, perhaps because the pine seeds provide 3.8times more energy per unit handling time and contain more fatthan bitterbrush seeds (Vander Wall 1995c). As a consequenceof this greater perceived value, the chipmunks appear to pro-tect Jeffrey pine seeds by transporting them farther and puttingfewer seeds in each cache than bitterbrush seeds. Second,differences in the availability of alternative foods, of which wehave little quantitative knowledge, may have caused the chip-munks to treat the seeds differently in the 2 years. The resultsof this study and the earlier study on bitterbrush (Vander Wall1995a) are compatible with the notion that chipmunks managecaches more intensively, and (or) search for and steal thecaches of other individuals more diligently, when the cachesare of greater value.

Why these rodents recached Jeffrey pine seeds so exten-sively is not yet clear. Several possibilities exist, including thechecking of cache contents and seed quality by the cacher asa component of cache management (DeGange et al. 1989), therefreshing of cache-site memories by the cacher (Grubb andPravosudov 1994), and raiding of the caches of other individu-als and recaching to obtain control of the cached food supply(Daly et al. 1992). Future studies will determine who is mov-ing the seeds, and we hope this will help us understand whysome seeds are moved so frequently.

All of the five different classes of caches (primary throughquintic) contained some germinating seeds. Figure 2 indicatesthat most germinating seeds came from secondary caches andthat few were contributed by primary caches. However, thepaucity of germinating seeds from primary caches may be anartifact of the experimental design. Since we made the primarycaches fairly large (10 seeds compared with a mean of 3.7seeds in primary caches made by chipmunks) and spaced themrather closely (2 m), we probably increased the removal rateof primary caches above that typical in unmanipulated situ-ations. If this is true, it would have led to an underestimationof the amount of germination expected from primary caches.

The decline in the percentage of seeds that germinated fromsecondary through quintic caches (Fig. 2) is probably the typi-cal pattern, although the actual percentages probably varygreatly from year to year.

The repeated moving of seeds from one site to another hassome potentially important consequences for seed dispersaland plant establishment. First, as seeds were recached, cachestended to become smaller. This is because a portion of therecovered seeds were eaten and the remaining seeds were oftenrecached at two or more sites. Occasionally seeds from twocaches were combined to make a larger cache, but the prevail-ing pattern was that large caches became fragmented overtime, resulting in a preponderance (92%) of one- and two-seedcaches at the time of seed germination in the spring. The frag-menting of caches creates more potential plant-establishmentsites. Note that the number of seeds in the study was reducedfrom 974 in primary caches to 133 that eventually germinated(a reduction of 86%), but the number of caches decreased from100 primary caches to 84 sites that eventually produced seed-lings (a reduction of 16%). Despite a large reduction in surviv-ing seeds, there was only a small reduction in establishmentsites compared with the number of primary-cache sites. Fur-thermore, the smaller number of seedlings per clump shouldhave reduced seedling competition, which has a small but sig-nificant influence on seedling survivorship in the first summer(Vander Wall 1992a).

Second, rodents gradually moved seeds away from the seedsource as they recached them (Fig. 4). The initial movementof seeds to primary-cache sites is highly directional, away fromthe seed source (Vander Wall 1992b). Yellow pine chipmunksappear to be sensitive to concentrations of food and respondby dispersing the food to scattered cache sites. Recaching ofthese items occurs after the concentrated food patch has beendepleted, and appears to be in random directions. But the effectof these random movements is still that most of the seeds aremoved away from the original seed source, because for anygiven dispersal movement, more than half of the potentialcache sites lie away from the original seed source. The generaldecline in distance between successive cache sites (Fig. 5) maybe related to the local abundance of food at the time of recach-ing. When food was concentrated in primary caches (Fig. 5a),chipmunks carried the seeds for relatively long distances, butafter the primary caches had been depleted and as subsequentcaches became increasingly dispersed, the perceived abun-dance of the food supply gradually declined (Figs. 4b–4d). Un-der the latter conditions, chipmunks transport most seeds forrelatively short distances.

The potential benefit of these cache movements to the pinemay be that its seeds are dispersed more evenly throughout thehabitat. Initial wind dispersal of relatively heavy seeds, suchas those of the Jeffrey pine, leaves most of the seeds clumpedunder or near the canopy of the source tree (Augspurger andFranson 1987; Greene and Johnson 1989) (Fig. 6). Relativelyfew seeds are likely to be transported long distances by wind.The initial (primary) caching of these wind-dispersed seeds byyellow pine chipmunks moves them away from the source tree(Vander Wall 1992b). These chipmunks seldom cache seedsunder the source trees where they gathered them, and typicallymove them 5–40 m away. Furthermore, chipmunks cachemost seeds in shrubby habitats, where the chipmunks havecover and nest sites and where pine saplings are more likely

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to establish (Vander Wall 1993). Subsequent recaching of theseeds serves to redistribute the caches more uniformly aroundthe source plant, resulting in a longer, flatter distribution ofcaches (Fig. 4). Whether this type of distribution actuallybenefits the pine is not yet certain, but the more widespreadand even distribution of seeds likely increases the probabilityof some seeds being deposited in habitats and microhabitatssuitable for seedling establishment.

Acknowledgements

We thank Janine Auger, Liza Bitton, Allison Jones, KimObermeyer, Kathie Vander Wall, and Joe Veech for theirassistance. The Whittell Board of Control generously grantedpermission for us to conduct the study. The research wasfunded in part by National Science Foundation GrantDEB–9306369 to S.B.V. and an Ecology, Evolution, and Con-servation Biology Program fellowship to J.W.J.

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Fig. 6. Generalized distributions of Jeffrey pine seeds at differentstages of seed dispersal. The left end of the x axis represents thebase of a source tree. The “wind” dispersal curve is the initial phaseof seed dispersal. The curve labeled “primary caches” representscaching of the wind-dispersed seeds by rodents; the curve labeled“secondary+ caches” represents secondary through quintic cachesthat animals have created from seeds taken from primary caches.Note that the median distance from the source tree and the generalevenness of the distributions increase with subsequent recaching.

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