Grey squirrels remember the locations of buried nuts

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1 Anim. Behav., 1991,41, 103 ll0 Grey squirrels remember the lcatins f buried nuts LUCIA F. JACOBS+ & EMILY R. LIMANT Deprtnrent f Bilgv, Princetn University, Princetn, NJ 08544, U.S.A. ( Received 2 January 1990; initial acceptance l2 March 1990: fnal acceptance I9 June 1990, MS. number: e5344) Abstract. It has previusly been assumed that grey squirrels, Sciurus cqrlinensis, cannt remember the lcatins f nuts they have buried, and hence must relcate nuts by their dur. This assumptin was tested by measuring the accuracy f cache retrieval f captive squirrels. Each squirrel was released alne intanutdrarena,whereitcached l0hazelnuts.afteradelay f 2,4 r l2days,eachsquirrel was returned t the arena and tested fr its ability t retrieve nuts frm its wn cache sites and frm l0 cache sites used by ther squirrels. Althugh each squirrel's wn caches were clse t the caches f ther squirrels, the squirrels retrieved significantly mre nuts frm their wn sites than frm sites used by ther squirrels, after all delays. The retrieval accuracy f the squirrels under these cnditins indicates that while grey squirrels can lcate buried nuts by their dur, they can als remember the individual lcatins f nuts they have buried. 'Squirrels have been criticized fr hiding nuts in 1986). Remembering the lcatin f fd surces, varius places fr future use and then frgetting the hwever, may be easier than remembering cache places. Well, Squirrels d nt bther with minr lcatins. The fd-strer must nt nly learn the details like that. They have ther things n their lcatin f many mre cache sites than fd s.urce mind, such as hiding mre nuts where they can't sites, but it must learn them in ne trial, when the find them'(cuppy 1949). fd item.is hidden, and it may have little pprtunity t rehearse its memry. In this study we That fd-string birds can remernber the lcatins f their fd caches is nw firmly established (marph tits, Parus palustrr: Sherry et al. by a fd-string mammal. examine the rle fspatial memry in cache retrieval l98l; Shettlewrth & Krebs 1982; black-capped Whether grey squirrels remember where they chickadees, P. atricapillus: Sherry 1984; Clark's have buried their nuts has lng been debated nutcrackers, Nucifraga clumbiana: Vandpr Wall (Merriam 1884; Stapanian & Smith 1984;Gurnell 1982; Kamil & Balda 1985). Surprisingly, there is 1987). Like the seed-eating birds mentined earlier, nly limited evidence that a mammal can remember grey squirrels scatter-hard (Mrris 1962), placing the lcatins f its caches (Macdnald 1976), individual seeds, such as acrns (Fagaceae) r desirite the wide ccurrence f fd-string in hickry nuts (Juglandaceae), in separatd cache sites mammals (Smith& Reichman 1984; Sherry 1985); and retrieving them mnths later (fhmpsn & instead, mammals are assumed t find a cache Thmpsn 1980). Grey squirrels frequently cache by the dur f its cntents (Cahalane 1942; nuts in areas adjacent t r verlapping the caching Tinbergen 1965; Hward et al: 1968; Murie 1977)- areas f ther squirrels (Jacbs 1987) and are One type f spatial memry has been studied in capable f detecting caches by their dur detail in fd-stbring mammals: memry fr the (Ihmpsn & Thmpsn 1980). Thus, under lcatin'f fd (labratry rat, Rattus natural cnditins, grey squirrels may search fr nrvegicis: Oltn & Samuelsn 1976; Mnglian buried seeds they have cached and thse cached by gerbil, Mirines unguiculatus: Cllett et al. 1986; ther squirrels. Ifa squinel remembers the lcatins grey suirrel, Sciurus carlinensis: McQuade et al. f its caches, it shuld be mre likely t find its wn caches than t find anther squirrel's caches. We *Present tested this hypthesis by bserving captive grey address: Department f Psychlgy, University f utah, Salt Lake city, ut 84112, u.s.a. squirrels retrieving nuts frm tw types'f cache tpresent address: Department f Neurbilgy, Harvard sites: sites they had chsen and sites ther squirrels Medical Schl, Bstn, MA 02t 15, U.S.A. had chsen U0 I 0 I l99l The Assciatin fr thc Studv f Animal Bchaviur 103

2 r04 Animal Behaviur,4l, I f. \ Experimental Design M ETHO DS T measure the accuracy f cache retrieval, captive grey squirrels were individually released int a large utdr arena and allwed t cache hazelnuts. After a delay f 2-12 days, fresh nuts were buried in the squirrel's cache sites and in an equal number f additinal sites that had previusly been chsen by ther squirrels. If squirrels remember the sites f individual caches, they shuld retrieve a greater prprtin f their wn caches than thse f ther squirrels. The rws and clumns f cncrcte blcks were painted with black numbers and letters measuring apprximately 25x l5cm t facilitate descriptin f the squirrels' mvements. Six cinder blcks, painted either yellw, blue r red, were placed at regular intervals arund the arena, t serve as prminent visual landmarks. Squirrels were released int the arena thrugh a small dr at ne end f the arena; the bserver sat n a small raised platfrm n ne side f the arena. Prcedure Caching phase The squirrel was first released int the arena and Subjects given I O-l 5 shelled hazelnuts t eat, since squirrels Eight hand-raised male grey squirrels, between d nt cache until satiated; shelling the nuts the ages f7 mnths and 2 years, served as subjects. reduced the squirrel's eating time. Squirrels spent Squirrels were kept in individual wire cages an average (+sn) f 23*2 min eating hazelnuts. measuring 6 I x 6l x 122 cm, which cntained Once a squirrel appeared satiated, which we heavy wden nestbxes filled with straw. The assessed by criteria such as a decrease in feeding cages std under a tarpaulin next t the utdr rate, it was given unshelled hazelnuts, ne at a time, experimental arena; the squirrels were expsed t frm the frnt f the arena. It usually ate sme f natural light and temperature cnditins during the these hazelnuts and then began caching them. perid f the study (Octber t December 1984). Squirrels wuld ften cache several nuts, then eat Squirrels were fed cmmercial hamster chw and ne r tw nuts befre cntinuing t cache the rest. given water ad libitum. They were als ccasinally We cntinued this prcedure until the squirrel had fed apples, unshelled peanuts, hazelnuts and black cadhed I 0 hazelnuts; n average, the squirrels spent walnuts; squirrels ften cached nuts and hamster 2.3+0'3 min caching each nut, and cached 9-ll chw in their cages. nuts in 22'l+ l:3min. Squirrels generally cached I'r l0 nuts (10'010'l);9 r ll cached nuts ccurred --, Apparatus when a squirrel either refused t cache mre than nine nuts r ate a nut previusly cached r was The experimental arena was situated in an pen inadvertantly given an extra nut. The bserver field belnging t Stny Frd Bilgical Statin f described the squirrel's mvements n a prtable Princetn University. The arena was a greenhuse tape-recrder; cache lcatins were marked n a skeletn cvered with 2.5-cm wire mesh and a cmmercial shade-clth; since the cvering was nt caching, it was returned t its hme c4ge. map f the arena. When the squirrel had finished waterprf, trials were nt generally run during heavy rain. The surface area f the caching arena measured P reparatin 4'6 x 9.8 m and was cvered with a fr re tieval matrix f cncrete blcks measuring 20x40cm, The buried nuts were remved by the bserver, which frmed a grid, 19 blcks wide by 23 blcks and the hle left by the remval was filled in and lng. The blcks were separated by grass-cvered smthed ver. Latex glves were wrn during this interstices abut 4 cm wide. Partway thrugh the prcedure t minimize the additin f dur cues study, hwever, the grass was cvered with a layer t the cache sites and all effrts were made t minimize disturbance f the sites. Extensive digging, f small pebbles, as it had becme sparse in areas where the squirrels had cached repeatedly. Data hwever, was ccasinally required t find a nut. frm each f these arena substrate cnditins were The exact lcatin f a buried nut was marked n a first analysed separately, but because the results map and als a distinctive mark was placed n the frm the tw arena cnditins were similar (as clsest cncrete blck with a waterprf ink described later), these data were cmbined. marker. This mark ensured that the replacement -l -l ii I

3 nut wuld be placed in the same site as the riginal nut. Because several squirrels were tested each day and cache sites were rarely reused, many such marks accumulated ver the curse f the trials. These small marks culd nt have served as landmarks lr retrieval f a squirrel's wn caches, since all nuts were buried next t such marks. Retrieval phase The retrieval phase ccurred 2,4 r I 2 days after thecaching phase. During the intervening perid the squirrels were fed sparingly; they were given n fd fr 24 h prir t the retrieval phase. Immediately preceding the retrieval trial, fresh nuts (nt handled previusly by squirrel r bserver) were buried in the lcatins previusly chsen by the squirrel. An equal number f fresh nuts were buried in 'ther' lcatins. The sites fr these ther caches were chsen randmly frm a list f caches made that week by squirrels ther than the subject. Ifa chsen site was less than l0 cm frm the subject'site r frm a previusly chsen ther site, it was disqualified and a new ther site was chsen. The nuts were hahdled with latex glves and were buried abut 2 cm beneath the surface, a depth similar t that f the riginal caches. Refilling f cache sites was dne blind: the experimenter burying the nuts did nt knw whichfthe caches belnged t the subject and which t.bther squirrels. The squirrel was allwed t retrieve the same number f nutp{hat it had buried. Once again, the squirrel's mvements and the time at which a nut was retrieved ivere nted n a prtable taperecrder. The squirrels spent a similar length f time retrieving and eating a nut as they had spent caching it:- 2.5*0.1min. The squirrel rvas then f 'returned t its hme cage and nt used in anther r trial fr at least 24 h. - We tested squirrels after three delay perids (2,4 and 12 days). Because the arena was utside, bad weather frced us t cancel several trials and thus equal numbers f trials per delay were nt btained. We cmpleted the fllwing trials: 2-day delay, 2.4 trials/squirrel (N:7); 4-day delay, 1.0 trial/squirrel (il:5); l2-day delay, l.l trials/ squirrel (/V:6). Because f the small sample size, we decided t cmbine the 4- and l2-day delays int ne categry, '4 r mre' days. As discussed belw, there were n significant differences between data frm trials with 4- and l2-day delays. Satiatin appeared t affect retrieval behaviur in several trials: after sme squirrels had retrieved Jacbs & Liman: Grey squirrel memry 105 and eaten a number f nuts, they re-cached subsequently retrieved nuts. Because their retrieval scres might have been affected by their search fr new cache sites, such retrievals culd nt be used t calculate retrieval accuracy, and several such retrievals were excluded frm a few trials. Thus, althugh in each trial the squirrel was allwed t retrieve as many nuts as it had previusly cached (mean l0'0f 0'l nuts; range 9-l I nuts), the mean number f retrievals per trial that cntributed t the analysis was 9' I * 0'3 (range l- I 0) nuts. RESULTS Figure I shws a representative trial by ne squirrel (Alvin; 2-day delay); the subject retrieved caches with a typical degree f accuracy in this trial. Cache Placement An imprtant assumptin f ur experimental design was that all squirrels distributed theircaches abut the arena in a similar manner. If this had nt been the case. we wuld nt have been able t distinguish between the squirrel's preference fr a particular part fthe arena and its memry findividual cache sites. T cmpare cache distributins between squirrels, the arena was divided int six equal-sized areas. The mean number f caches each squirrel placed in each f the six areas, cmbining all delay pe:irrds is shwn in Fig. 2. By cmparing the inset schematic representatin f the arena t the cache distributin data, it can be seen that the squirrels cached mre nuts in sme areas than thers. Overall, the pattern may be described as a strng preference fr caching near the back and side walls f the arena. This was nt a simple preference fr edges, because the squirrels did nt cache nuts near the frnt edge. Instead, the squirrels were prbably placing caches far frm the fd surce. They als culd have been aviding the bserver wh sat at the fd surce. Hwever, as the squirrels were tame, having been hand-raised by ne f us (L.F.J.), this seems unlikely. In pilt trials, when the bserver wa$ in the enclsure, squirrels cached nuts arund the bserver's feet. Hwever, preferences fr certain caching areas varied little between individuals; there was n significant difference between individuals in the percentage f caches placed in each arca (7,2:l'403, df:j, P:0'946, Friedman's methd fr randmized blcks).

4 106 Animal Behaviur,4l, l ( ) r5 r3 t8 a2 T a7 (b) t \ \2 d" \ r **",-i;" (2day delay). l: Alvin's cachegfl: caches f ther squirrels. Numbers refer t the sequence in which nuts were cached r retrieved, the arrw indicatgs the lcatin f the bserver and the surce f hazclnuts, and the rectangle in lwer left indicates the squirels'. place fentry int the arena. The plygn in (b) defines thse caches cnsidered, fr the analysis, t be available during retrieval. 40 = 3s *20 c dr l?3456 Subre Figure 2. Summary f cache placement in the experimental arena by all squirrels (. y':8), cmbining all delay perids. Pints indicate the mean (*se) pcrcentagef allcaches placed in each subarea byeach squinel. Inset diagram shws the relative psitins f the subareas; the arrw indicates the bserver's p<isitin, which wai als the surie f the nuts t be cached.

5 Jacbs & Lintan: Gre1, tquirrel menrry t07! a a^ AI E l z. 2 Dys 4 r l2 Dys Dely Figure 3. Number f caches retrieved after delays f 2 days and 4 r 12 days. Bar heights indicate the mean (*se) number f caches retrieved;!: wn caches, l: ther caches. Despite repeated use f the same areas, squirrels rarely cached mre than nce in the same cache site. When 'same site' is defined as tw sites less than I 0 cm apart, nly 45 f266 cache sites chsen ver a 4-mnth perid (including caches made in abrted trials) were ever used mre than nce; in nly nine f these cases was a site reused by the same squirrel. Memry fr Cache Lcatins A greater.number f a squirrel's wn caches ('wn') retriel il than caches f ther squirrels ('ther') relative t the numbers f each cache type available, was taken as psitive evidence fr memry f cache lcatin. Frclarity, we first present the mean number feach type f cache retrieved a after delays f 2 and 4 r 12 days (Fig. 3). Overall, * squirrels retrieved mre f their wn caches i than ther caches, regardless f the length f delay (2- day delay: P<0.009; 4- r l2-day delay: p<0.006, Wilcxn's signed-ranks test). A mre precise cmparisn, hwever, is that f the number f each type retrieved t the number f each type available. The number f available caches f each type was determined by cunting nly thse caches that lay within the area searched by the squirrel, rather than cunting all caches in the arena. This was dne such that an individual squirrel's preference fr a particular part f the arena wuld nt bias the analysis twards a higher recvery f wn caches. The search area fr each trial was defined as the minimum plygn that encmpassed all the retrieved caches, as seen in Fie. l. Within this area, the numbers f wn caches rctrieved. ther caches retrieved. wn caches available and ther caches available rvere cunted. Fr cach trial, the rati f rvn cachcs rctricvcd t ther caches retrieved was cmpared with the rati f wn caches available t ther caches available. Fr example Alvin's retrieval, illustrated in Fig. l, was analysed as fllws: he retrieved seven f his wn caches and three ther caches, yielding a rati f 7: 3, r 2'3:l in caches retrieved. This rati is greater than the rati f cache types that were available in the plygnal area defined abve as the search area; which, in this case, was 9:6 r l'5:1. Data were analysed separately lr trials with a 2-day delay and flr thse with a 4- r l2-day delay. In the majrity f the 2-day delay trials ( l5 f l7), the rati f wn t ther retrieved was greater than the rati f wn t ther available; n average, 2'7 +0'7 wn:ther were retrieved, cmpared with l'3 + 0'l wn:ther available. In l2 f l3 trials at a lnger delay (4 r l2 days) the same was true; n average, 2'3 +0'3 wn t ther were retrieved, cmpared with wn:theravailable. These differences were statistically significant (2-day delay: P < 0'009; 4- r I 2-day delay: P < 0.013, Wilcxn's signed-ranks test). Furthermre, there was n difference between the scres after 4- and after l2-d,ay delays (P:0'186, Mann-Whitney U-test), justifying their being cmbined fr the previus analysis. There was als n difference in the scres btained fr 2-day trials irr,.the grass-cvered arena and the gravel-cvered arena; these trials were als cmbined in the previus analysis. T exdtnine the strength f the squirrels' preferential retrieval f their wn caches in mre detail, we reanalysed sme f the data using transcripts f the squirrels' behaviur during cache retrieval (10 trials, frm all delays). The lcatin where a squirrel ate each retrieved nut was ascertained frm the transcripts. Assuming that this lcatin was als the starting pint f the squirrel's next search, we then measured the distanc frm this lcatin t the tw clsest caches. [n sme cases, the tw clsest caches were ne wn cache and ne ther cache; mrever, ne f these caches was clser t the squirrel than the ther. A squirrel, facing such a chice between tw clse caches, culd simply retrieve the clsest cache, regardless f whether it was its wn cache r that f anther squirrel, r it culd preferentially retrieve its wn cache, even if the ther cache was clser, r it culd disregard bth clsest caches and retrieve a mre distant

6 108 Animal Behaviur, 4l, I Own cche clser Other cche clser ( ) I ' I Squirre I Squirrel (b) Clse cche nt retrieved 36 (, tl Or '/ il*t Figure 4. Retrieval fcache types (wn r ther) under different retrievat cnditins. O: wn caches; O : ther caches. The arrw frm the squirrel t the cache represents the squirrel's retrieval decisin; the thickness fthe line indicates the frequency at which squirrels chse t retrieve their wn caches r ther caches. (a) An adjacent cache was retrieved, and either the squirrel's wn cache was clser r the ther cache was clser (N:45). (b) A distant cache, nt ne f the tw clsest caches, is retrieved (N:47). cache, either ne fits wn r that fanther squirrel. $u:fu cases where a chice was presented were then gnalysed further. Ifthe difference in distance frm ihe squirrel t each f the tw clsest caches was less than 0.5 m, the retrieval was put int the 'wn cache clser'categry. In the sample analysed, retrievals f distant caches were as frequently bserved (N:47) as retrievals f clsest caches (nf:45). The number f wn caches retrieved was cmpared with the number f ther caches retrieved fr each f the three types f retrieval: ( I ) wn cache is clser and a clse cache is taken, (2) ther cache is clser and a clse cache is taken. and (3) a clse cache is nt taken. The bserved number f retrievals was then cmpared with the expected number f retrievals f each type. The expected number f clse retrievals was estimated as twthirds, because f the bservatin that when ne f the tw clsest caches were taken, 30 f the 45 caches retrieved were clser than the cache nt retrieved. Thus, it appears that the verall prbability fa clse cache being retrieved (regardless f cache type) is 30/45 r tw-thirds. When squirrels chse t retrieve caches frm further away, we expected them t retrieve equal numbers f wn and ther. t.l Regardless f the psitin f the cache relative t the squirrel, squirrels always retrieved mre f their wn caches than ther caches, as shwn in Fig. 4. The bias twards retrieving wn is significant under bthcnditins: wncacheclser(12 : l5'7, df: l, P < 0'00 I ) and ther cache clser (X,2: 6' I 8, df -- l, P<0'05). Even when retrieving further caches, squirrels retrieved mre nuts frm their wn cache sites than frm ther sites (12: 13'30, df:, P<0.001). DISCUSSION Althugh squirrels buried nuts in areas where ther squirrels had als buried nuts, they retrieved significantly mre nuts frm their wn cache sites than frm the cache sites f ther squirrels, even after delays f 4 r l2 days. This retrieval accuracy culd nt be explained by the squirrels' habitual use fthe

7 Jacbs & Linnn: Grey sauirrel memry r09 r : same areas: the rati f wn caches t ther caches hundred times as large as the experimental arena retrieved was greater than expected based n the used here (Jacbs 1987). The maximum length f availability f caches in the area searcheduring time between caching and retrieval in the field has retrieval. A squirrel was als mre likely t retrieve nt been determined, but it is prbably 8-9 mnths its wn cache even when anther squirrel's cache (Cahalane 1942; Thmpsn & Thmpsn 1980). was clser t it r when a squirrel neglected t Finally, such factrs as the number f caches, the retrieve the cache clsest itself and instead dus size f the caching area and the length f time up a mre distant nut. befre retrieval may interact and thereby increase These results supprt ur hypthesis that grey the difficulty f the squirrel's task. squirrels can remember where they bury nuts. Regardless f its capacity, a grey squirrel's Clearly, hwever, squirrels use ther methds, in memry fr cache lcatins may have significant additin t their memry f specific lcatins, t adaptive value. When caches are cvered witlt find buried nuts. Because the squirrel always snw, as is the case fr much f this species' range retrieved at least ne nut frm anther squirrel's and fr much f the retrieval seasn, a squirrel's cache, ur results cnfirm earlier bservatins that survival may depend n its accurate memry f grey squirrels can lcate a cache by the dur fits sme cache lcatins. Even in the absence f snw cntents (Thmpsn& Thmpsn 1980). cver, the use f memry may be critical t a fdstrer's survival. Fx squirrels, Sciuraniger,prefer That squirrels find caches using dur cues has been well-established; that they are als capable f t cache in pen fields. This behaviur has been remembering cache lcatins is a nvel result. An hypthesized t decrease cache pilfering by increasing the predatin risk faced by wuld-be cache pil- interesting implicatin f these results is that the squirrels emplyed tw methds t find caches: ferers, wh must frage mre slwly than wners, they returned t sites where they had buried nuts wh can mve efficiently t and frm remembered and they searched fr the dur f buried nuts. sites in expsed areas (Stapanian& Smith 1986). Under the cnditins f this experiment, either the Memry f cache lcatins, even in the absence first methd was used mre ften than the secnd, f cmpetitrs r predatrs, may have additinal r it succeeded mre ften. Perhaps these methds adaptive value if it increases a squirrel's retrieval are used simultaneusly: squirrels might sniff the efficiency. The squirrels in this study appeared t grund fr dur cues while they are rienting t minimize their retrieval searcli paths by running the lcatins f remembered caches. Evidence frm directly frm ne patch ftrv r three caches t the a study fgreysquirrels searching fr hidden seeds next, harvesting the caches r"ith little ;e-tracing f suggests that squirrels place different weights upn their path; this can be seen in the sequence f the cues assciated with a remembered fd surce retrievals illustrated in Fig. l. If s, this wuld indicate that grey squirrels, like chimpanzees Pan (McQuade et al. 1986). Captive grey squimels were trained t lk fr seeds in cvered dishes, which trgldytes (Menzel, 1973), can remember a series differed in their lcatin. their clur and their f lcatins in relatin t each ther and use this dur. The cues were then disassciated, and the infrmatin t frm a cgnitive map, where infrmatin abut cache sites may be encded. analysis f the squirrel's rientatin errrs led t the cnclusin that the mst imprtant cue was the Such cgnitive prcessing wuld be adapfive in lcatin f the fd dish, fllwed by its clur and an animal that manages an inventry f thusands dur. If squirrels use the same methds t find f items, ver many mnths. Grey squirrels are their caches as t find fd surces, then the mst active all winter, even at the nrthern limit f their imprtant feature remembered abut a cache may range (Thmpsn 1977), and during this perid be its lcatin as well. Grey squirrels, like blackcapped chickadees, may als remember the type f searching fr caches and ccasinally digging up they spend much time n the grund, apparently seed in a cache (Sherry 1984); their memry f the and reburying a nut r acrn (Jacbs, unpublished clur and dur f fd dishes, in the abve bservatins). In the present study, squirrels als study, suggests that they can. dug up and reburied nuts, thugh nt until they had Our experiment, hwever, des nt address the first eaten several nuts. These bservatinsuggest questin f the capacity f a squirrel's memry fr that grey squirrels may redistribute their caches. cache lcatins. Under natural cnditins, grey Such behaviur culd be advantageus: squirrels squirrels may cache thusands f nuts, ver areas a culd rearrange caches that were hastily laid ut

8 il0 Animul Behaviur.4l.l f \, during the autumn harvest, and thus maintain an Kanril, A. C. & Balda, R. C Cachc recvery and ptimum dispersin f caches, which has been spatial memry in Clark's nutcrackers (Nucifraga clunrbiarm). J. exp. Psych.. Anim. Behav. shwn Prc., t reduce ll, lss t pilferers (Stapanian& 95 ilr. Smith 1984). As the year prgressed and they Macdnald. D Fd caching by red fxes and sme emptied mre caches, the remaining caches culd ther carnivres. Z. Tierpsychl., 42, again be rearranged. Such husbandry f caches McQuade, D. 8., Willians, E. H. & Eichenbaum, H. B. wuld als relresh their memry fcache I 986. lcatins, Cues used fr lcalizing fd by the grey squirrel (Sciurns ca r I ine ns is). E t h I gy, 72, and thus reduce the length f time they must Menzel, E. W Chimpanzee spatial memry remember the lcatins. Mre infrmatin n the rganizatin. S c ie nce, 182, natural histry fcache retrieval by grey squirrels is Merriam, C. H The vertebrates f the Adirndack needed befre the capacity and adaptive value f regin, nrtheastern New Yrk: Mammalia. Irans Linn. their Sc. N.Y..2, 126. spatial memry fr cache lcatins can be Mrris, D The behaviur f the green acuchi fully estimated. (Myprcta pratti) with special referenc t scatter harding. P r c. z l. S c. Lnd., 139, 70 l Murie, J. O Cues used frcache-finding by agutis (D asy prc t a punc Mta). J. M ammal., 5E, ACKNOWLEDGMENTS Oltn. D. S. & Samuelsn. R. J Remembrance f places passed: spatial memry in rats. J- exp. Psychl.: We thank Daniel Rubenstein and Henry Hrn fr Anim. Behav. Prc.,2,97-l 16. advice and encuragement; Martin Daly and an Sherry, D. F Fd strage by black-capped chickadees: memry fr the lcatin and cntents f caches. annymus referee fr suggesting helpful new analyses f data; David Sherry, Luc-Alain Anim. Behav., 32, Sherry, D. F Fd strage by birds and mammals. Giraldeau, Rachel Herz, Jan Murie, Steven Gaulin - Adv. Srud. Behav.,15, and Steven Jenkins fr cmments n earlier drafts. Sherry, D. F., Krebs, J. R. & Cwie, R. J Memry Sme baby squirrels were prvided by PAWS, and fr the lcatin f stred fd in marsh tits. lnirz. hazelnuts were dnated by Hazelnut Grwers f Behav.,29,126{u_ Oregn. This Shettlewrth, S. J. & Krebs, J. R Hw marsh tits study was funded by Grants-in-Aid find their hards: the rles fsite preference and spatial frm the Natinal Academy f Sciences and frm memry. J. exp. Psychl.: Anim. Behav. Prc., 8, the Sigma Xi Sciety, and by the Department f 35+37s. Bilgy, Princetn University. Smith, C. C. & Reichmann, O. J The evlutin f fd caching in birds and rnammals. l. Rev. Ecl. Syst., 15, t' Stapanian, M. A. & Smith, C. C Den.':ity-dependent : REFERENCES survival f scatterharded nuts: an experimental' apprach. Eclgy,65, I Cahalane, V. H Caching and recvery f fd by Stapanian, M. A. & Smith, C. C Hw fx squirrels western fx squirrel. J. Wildl. Mgmt,6; influence the invasin fprairies by nut-bearing trees. Cllett, T. S., Cartwright, B. A. & Smith, B. A J. M atnmal., 67, l,andmark learning and visu-spatial memries in Thmpsn, D. C Diurnal and seasnal activity f gerbils. J. cmp. Physil., lse, the grey squirrel (Scr'urra carlinensb). Can. J. Zl., Cuppy, W Hw t Auract the Wmbat. Chicag: 55, I University f Chicag Press. Thmpsn, D. C. & Thmpsn, P. S Fd habits Gurnell, J The Natural Histry f Squirrels. and caching bchaviur f urban grey squirrels. Can. J. Lndn: Christpher Helm. Zl.,S,70l-710. Hward, W. E., Marsh, R. E. & Cle, R. E Fd Tinbergen, N Vn den Vrratskammern des detectin by deer mice using lfactry rather than Rtfuchses (Yulpes vulpes L.). Z. Tierpsychl., 22, visual cues. Anim. Behav.,16, l3-l?. I l Jacbs, L. F Fd-string decisins in the grey Vander Wall, S. B An experimental analysis f squirrel (Sciurus carlinensis). Ph.D. thesis, Princetn cachb recvery in Clark's nutcrackcr. Anim. Behau.,30, University c'! u t

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