Visual environment and delay affect cache - Semantic Scholar

Animal Learning & Behavior 199 82, 6 ( 4 ) , 4 3 9 - 4 4 7

Visual environmentand delay affect cache retrieval accuracy in a food-storing rodent CYNTHIA L. BARKLEY and LUCIA F. JACOBS Uniuersity oJ CaliJotnia, Berkeleg, California Many scatter-hoarding species use spatial memory to relocate their food caches. Two factors can affect spatial memory: the availability of landmarks in the environment, and the latency between learning and recall. Using a2 x 2 factorial design, we determined the effect of these factors on cache retrieval accuracy in Merriam's kangaroo rats (Dipodomys merrinmi). Kangaroo rats cached seeds in an arena under conditions that varied by retrieval interu'al (1 or 10 days) and by number of landmarks (0 or 16 landmarks). After I day, they recovered equal proportions ofcaches in both landmark conditions. After 10 days, they recovered more caches in the 16-landmark condition than in the bare condition. This is the first study to show that landmarks are necessary for accurate cache recovery after long delays. This result is consistent with maze studies that have shown that landmarks reduce proactive interference and that delay increases proactive interference.

Scatter-hoarding animalsstore food by hiding small amountsof food in many scatteredlocationsor caches (Morris, 1962;VanderWall, 1990),eachof which is createdwith a singledepositionof food.Cachesarelaterretrievedby the hoarder;in the caseofthe Clark'snutcracker (Nucifragacolumbiana)or the gray squirrel(Sciuruscarolinensis),the retrieval episodemay occur 8-l I months after the cachingevent(Thompson& Thompson,1980; VanderWall & Hutchins,1983).Many sitesareusedonly once,to reducethe risk of cachepilferageby competitors (Andersson & Krebs,1978;Daly,Jacobs, & Wilson,1992; Hampton& Sherry,1994),and when cachesitesarevlrtually unlimited,scatterhoardersrarelyreusesites(Jacobs & Liman, 199l). Each cachingevent can thereforebe uniquelycharacterized by its locationrelativeto nearby landmarks. Laboratory experimentshave provided evidencethat scatter-hoarding birds,suchastheblack-capped chickadee (Parusatricapillus) and the Clark's nutcrackerand mammals, suchas the gray squirrel and the Merriam's kangaroo rat (Dipodoml,smetiami), can rememberthe precise locationsoftheir scattered caches(Jacobs,I 995; Shettleworth, 1995).Evidencethatmemoryfor cachesitesis an evolvedadaptationcomesboth from comparativestudies of cacheretrieval(Balda& Kamil, 1989;Clayton,1995)

We thank JacquiGaswayand Vince Gifford for technicalassistancet Jan Randall for donating kangaroorats to us from her colonyt Martin Daly for trapsand other field equipment;Al Muth, Mark Fisher,and the Boyd Deep CanyonDesertResearchStationfor assistance and accommodationsduring trapping: and lrv Zucker, Pierre Lavenex.William Timberlake.and the two anonymousreviewersfor comments on the manuscript.This researchwas supportedby a National ScienceFoundation GraduateFellowshipto C.L.B., and funded by grants from the Nati o n a lS c i e n c eF o u nd a tio n( NSF IBN- 9 3 0 7 3 1 7 )a n d th e Un i versi tl , of C a l i f o r n i at o L . F . i . C o r r e so o n d e n ce sh o u ldb e a d d r e sse d to C . L. Barkley.Departmentof Psychology,Universityof California,Berkeley. CA 9 4 7 2 0( e - m a i l :c b ar kle y( ru clin k.b e r ke le y.e d u ) .

and from artificial testsof spatialmemory such as the memorytask(Brodbeck,Burack,& one-trialassociative Shettleworth.1992\.In both naturaland artificial tests animals of spatialmemory,it is clearthat scatter-hoarding havea remarkableability to relocateplacesin space. A first step to understandinghow this precise spatial memory works is to determinewhat factorscan influence theaccuracyofthe scatterhoarder'sretrievalperformance. Two factorsthat havebeenshownseparatelyto influence spatialmemory in artificial taskssuchas the radial arm maze arethe latency betweenlearning and testing,with retrieval intervals leading to reducedaccuracy(Roberts & Dale, 1981),and visual landmarksin the learningenvironment,with presenceof landmarksleadingto better accuracy(Cohen,Reid,& Chew 1994).We areincluding distinctobjectsin the enas landmarksall conspicuous, vironment.both distaland near.Thesefactorsmay also influenceaccuracyofcache retrieval.It is alreadyclear that many scatterhoarderscharacterizeeachcacheby the spatialrelationsbetweenthe cacheand landmarks;for example,the retrievalaccuracyof Clark'snutcrackersis lou'er u,hen landmarkspresentduring caching are removedbeforeretrieval(Balda & Turek, 1984).Shifting landmarksnearcachesalso causesboth birds and mammalsto shift their searchfor cachesto siteslocatedat the samerelativedistanceto the shiftedlandmarks(Bennett, I 993;VanderWall, I 982, I 99 I ). In a recentstudy,Clark's nutcrackerswere found to characterize the site ofa hidden food item by the relationships betweennearbylandmarks in the arena(Kamil & Jones.1997).Thus, when landmarkcuesareavailable.scatterhoardersusethesecues the completo locatecaches.Yet no studyhasaddressed mentaryquestion:Can scatterhoardersaccuratelyrecover cachesifconspicuousand salientlandmarksarenot presentduringcaching'? Althoughretrievalintervalby rtselfhasbeenshownto affect cacheretrieval accuracvin Clark's nutcrackers

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(Balda & Kamil, 1992), and black-cappedchickadees (Parusutricapil/as)(Hitchcock& Sherry,1990),no study hasexaminedthe way in which the lengthof the retrieval intervalandthepresence o1'conspicuous landmarkscombine to affectmemoryfor cachelocations.In the present study,we examinethe possibleinteractionof thesefactors in the Merriam'skangaroorat, a nocturnal,scatterhoardingrodent.Merriam'skangarooratsaresmall(35 g), primarily (thoughnot exclusively)scatter-hoarding, rod ent s( J enk ins& P e te rs1 9 9 2 ;R e y n o l d s ,1 9 5 8 ).I n the laboratory,they can rely solelyon spatialmemoryto retrievetheir caches(Jacobs,1992). Using a 2 x 2 factorial design,we testedthe effect of distinctlandmarkarraysand retrievalintervalon cache retrievalaccuracyin Merriam'skangaroorats.To manipulatevisualenvironment.we testedkangarooratseither in a bareenvironmentor in an environmentwith an array of l6 trial-uniquelandmarks.We choseto manipulate landmarksby using objectsplaced on the floor bf the arena.Most of the previousexperimentsshowingthat scatterhoardersalso rely on landmarksto orient themselvesto cacheshave beendone with within-apparatus o b jec t s( B ennet t ,1 9 9 3 ;Va n d e rW a l l , 1 9 8 2 . l 9 9 l ). To manipulate delay,we testedthe kangaroo rats after retrievalintervalsof I or l0 days.We predictedthatthe effectsof landmarkconditionwould vary as a functionof delay,with recoveryaccuracydecliningmore after long delaysif cacheshad beenmade in a bare environment than after the samedelay in an environmentwith an assortmentof uniquevisual landmarkspresent.

METHOD Kangaroo rats were tested in lu,o cache retrieval interval conditions ( I dal and l0 days, hereafter l D and 10D) and trvo .r,isualenvironment conditions (0 and I 6 trial-unique landmarks,or 0LM and l6LM ) . T h e s h o r t i n t er va l wa s th e m in im u m te sr a b ler e tr ieval i nt erv a l f o r w h i c h w e c o uld e n su r eth a t in a ll co n d itio n s.a n im al shad restricted accessto food for the same period of time and would be hungry at the start of testing. The long retrieval interval selected was s i m r l a rt o t h e l o n g e str e tr ie va lin te r va lo f 1 2 d a ysth a t h as been obse r v e du n d e r n a t u r al co n d itio n s { Da ly e t a l.. 1 9 9 2 ) . In o rder to pro" ' i d ea n a r r a y o f l a n dm a r ks th a t wo u ld b e sa lie n tto th e a ni nral s. t nal - u n i q u e a r r a n g e me n tsn ' e r e u se d . Anim a l s T h e a n i m a l sc o m p l e tin gth e cxp cr im e n ta lp r o ce d u r ewe r e 6 w i l dc au g h t M c r r i a m ' s k a n g a r o o r a ts ( 4 fe m a le s.2 m a le s) . T h e se ani m al s w e r c s e l e c t e df r o m a g r o u p o f 2 0 o n th e b a siso f th e r r wi l l i ngnessto cacheliequently in the expenmentalsituation.Three kangaroo rat s 1 3 t e m a l e s ) h a d bccn tr a p p e d in Po r r a l. Ar izo n a . in i991 or 199 2a n d m a i n t a r n e di n ca p tivity a t Sa n F r a n ciscoSta teUn iversi ty. T he o t h e r a n i m a l s( 2 m a le s, I te m a le )we r e tr a p p e da s a d u ltsi n D ec em b e r 1 9 9 5n e a rP a l m De se n .Ca lifo r n ia .All a n im a lswe r e housed on sand and were observed to cache food in their home cages. The kangaroo rats were housedsingly in 46 x 24 cm plastic cages on s a n d w i t h c o t t o n b e d d in g a n d a sm a ll co n ta in e r( a ca p p e dpl asj a r , o r a m e ta l ca n ) a s a n e st ch a m b e r Pr io rto the t ic p i p e , a -elass startof the experiment.all animals were placed into a reversedI 2: I 2-h ligh t : d a r k c y c l e . t h e l i gh ts b e in g e xtin g u ish e da t 0 8 0 0 h . Al l ani mals w e r e g i v e n a d - l i b a cce ssto a d ie t o f m ixe d b ir d se e dand rodent c h o w . L e t t u c e $ , asp r o lid e d a s a \\' a te rso u r ce .Du r in o r l reex-

periment, subjects u'ere lood restricted to l.-5-2 g of oats 2.1h prior to a cachi ng or retri eval sessi on. B ody w ei ght w as moni tored throughout the experi ment, and they w ere not permi tted to fall belorv 96% oftheir free-feeding baseline. Apparatus Thearenaforcachi ngw asa l l 8 X 179 x 4Tcmopenboxmade oiblack acrylic plastrc.enclosedby white plastic curlains suspended from the ceiling and draped inside the arena ivalls (see Figure I ). A wood collar supporteda raisedfloor in the arena.This floor consisted of eight galvanizedsteelplates(45 x 45 cm). divided into two parallel rows of four each,and the rows were separatedby a wood divider (29 x 179 cm). Each plate contained a 4 \ 4 array of 4-cm drilled hol es. E ach hol e w as fi tted w i th a cup (4-cm rnteri or di ameter; 3.25 cm deep) that hung snugl y from the cup\ ri rn. These cups, fi l l ed r.ri th sand,consti tutedI 28 potenti alcachesi tes.A pl asti cdi s h i n the centerofthe di vi der actedas a l eederduri ng cachesessi on s . Landmarks were used in the arena during the pretesttrial, habituati on tri al s. and each l 6LM test tri al . We chose obj ectsw i th nat ural shapesand texturessuch as rocks, artificial cloth flowers. sticks. and pi ne conesas w el l as short (10-cm) l engthsof 7.5-cm-di ameter black plastic pipe sawed in half. The landmarks u,ereplaced on the plates betrveencups. around the edgesofthe plates. and on the center di vi der. The l ai rdmarks w ere randoml y chosen for each tri al from a pool ofapproxrmatel y 100 obj ects.

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KANGAROORAT MEMORY There were some extra-apparatus visual cues that the animals could use to orient themselves in the arena. Holes were cut in the curtains on the two long sides ofthe arena in order to videotape tri_ als: On one side. a round hole was cut slightly larger than the lens ofthe camera, and on the other, a large rectangular hole was cut so that a mirror could be suspendedat an angle above the arena. This was done becausethe video camera could not record activity in the entire arenaunless it recorded from rhe mirror. A light also provided an e x t e r n a lv i s u a l c u e. L ig h tin g co n siste do fa sin g le 6 0 - W bul b on t he o u t s i d e o f t h e c ur ta in b e n e a th th e vid e o ca m e r a . T h i s l i sht source created a diffi.rseuneven lieht in the arena. Procedure The experiment consisted of three phases: pretest, habituation, and t e s t . A t r i a l a t e a ch p h a se o fth e e xp e r im e n tco n siste doftw o sesslons:a cache sessionand a recovery session.During cache ses_ sions, the feeder in the center ofthe arena was stocked with 60 sunflower seeds; it was empty during recovery sessions.Eight land_ marks were used for trials in the pretestand habituation phases,and either 0 or l6 landmarks were used in the test phase.For each trial, the landmarks were placed in trial-unique configurations, wrth no landmark occupying a place where one had been in the immediately pre c e d i n g t r i a l o r a p l a ce it h a d e ve r o ccu p ie d b e fo r e . T h e l and_ marks were always in the same place in a recovery session as they had b e e n i n t h e p r e c e din gca ch ese ssio n . In the pretest and habituation phases,the animals were checked af t e r 2 h , w h e r e a s i n th e te st tr ia ls, a n im a ls we r e ch e cke d after 20 min. We determined whether the animal had cached by counting the number ofseeds left in the feeder, the size ofthe kangaroo rat's cheek pouches, and whether cups appearedto contain seeds.Two signs indicated rhat caching had occurred at a site: the presenceof sand excavatedfrom a cup and the visible presenceof ieeds in the cup. Animals were removed from the arena ifthey had cached seeds ln a t l e a s tt w o c u p s . After the cache sessions,all cups were emptied and the number of seeds cached was recorded. The plates and center divider were wiped with disposable.detergent-impregnatedcleaning towels (i.e., "baby wipes") in order to clean or mask odor trails left by the animals. The cups were returned to the plates in new locations. Before retrieval sessions,each cache was replaced.ln the pretestphases,all seedsthat the animals had cached were returned. In the habituation and tesl phases,two seeds were returned to each cache. to reduce t he l i k e l i h o o d t h a t t h e an im a lswo u ld b e co m esa tia te da fte r r etri eving one or two caches,and to ensurethat all cachesemitted the same amount of odor from the seeds.E.achcup was covered with a blue plas t i cp o k e r c h i p ( d i a m e te r = 3 .7 5 cm ) , wh ich f' it sn u g ly o ver the sand surface.The chips made searchesin cups more obvious and presumably reduced odor cues from the seeds.Once removal w.asmast ere db y t h e a n i m a l , t h e p o ke r ch ip s d id n o t a p p e a rto in te r fe rew i th cache retrieval. All trials were separatedby an intertrial interval of at le a s t I I d a y s .w i t h n o m o r e th a n l5 d a ys e la p sin gb e twe e ntri al s. Pretest Phase A n i m a l s w e r e l e f t i n th e a r e n a with 6 0 su n flo we r se e d sin the feeder lbr 2-h blocks unril they cached seedsin the sand-filled cups. or un t i l 6 h h a d e l a p s e d.F a ilu r eto ca ch eo n Da y I r e su lte din a sec_ ond c a c h i n g s e s s i o nt h e n e xt d a y fo r u p to 6 h in d u r a tio n .T he animals that cached were returned to the arena 24 h later wrth their c ac h e si n c u p s i n t a c r , bu t with a ll o th e r se e d s( e .g .. in th e feeder. c ac h e d o n t h e p l a t e s o r o n th e d ivid e r ) r e m o ve d b y th e e xperi _ menter. The kangaroo rats remained in the arena until they had ret riev e dt h e i r c a c h e s .o r u n til 6 h h a d e la p se d .Ofth e 2 0 a n im a l spre_ t es t e d ,l 2 a n i m a l s c a c he da n d r e co ve r e dsu n flo we rse e d sa n d w ere ret ai n e df o r t h e n e x t p a r t o fth e e xp e r im e n t.Eig h t la n d m a r ksw ere us ed d u r i n g t h e p r e t e s rph a se .

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Habituation Phase E ach of the remai ni ng l 2 anrmal sw as gi ven habi tuati ontri al s t o ensure that it would reliably cache in the cups. The cache sessions ofthe habituation trials lasted 2 h. A retrieval sessionoccurred on the following day. The retrieval sessionslasted for 80 min or until the ani mal had recoveredat l east60% ofi ts caches.H abi tuati ontri als continued until the animal had made two cachesper session in at l east tw o sessi ons.The mi ni mum number of habi tuati on tri al s given to any animal was four. Animals that lailed to make tw.ocaches rn two sessionswithin seven habituation trials were not used in the remainder of the experiment. Six animals were moved on to the test phase. Of the 6 animals that passed through habituation, 3 had no prror experience.The 3 San Francisco Stateanimals had four to five additional habituation trials in the experimental apparatus3 months prior to the start of the experiment. Because of the break in training, they were habituated to the arena again. Test Phase The test phase consisted ofa 2 X 2 lactorial w-ithin-subjectsdesign. Each animal was tested once in each condition. and the order ofconditions was randomly assigned for each subject. The manipul ati ons w ere del ay betw eencache and recovery(l D or l 0D ) and the avai l abi l i ty of vi sual cues or l andmarks (0LM or l 6LM). A ll test trials were videotaped. In each cache session,the kangaroo rat was placed in the arena and left for 20 min. The experimenter reenteredthe room and evaluated w hether or not the ani mal had cached anv seeds.The tri al ended if the animal had made at least two cachis. Otherwise. the tri al conti nued w i th checks by the experi menter at 35 mi n and 50 mi n. A t that poi nt, i f the ani mal had not made tw o caches.i t w a s returned to its home cage with a ration ofoats and the cache session was continued the next day. Ifthe animal made one cache during the Ist day, that cache was capped with a rightly fining lid on the 2nd day.Thi s happenedone ti me for 2 ani mal s. R ecovery sessi ons occurred ei ther I or l 0 days after cache sessions.To avoid confusion. the sites used as caches in the orevious sessi onw i l l be cal l ed target caches.In addi ti on to the i areet caches,which were each replaced with nvo seeds,equal numbers of bai ted control si tes.each contai ni ngtw o seeds,rverepl aced i n the arena. \!'e chose these sites from those used bv the animals thcmselves as cache sites so that the controls reproduced any site preferencesfor that i ndi vi dual .The functi on ofthe control cachesw as to ensurethat the recovery oftarget cacheswas not based solely on searchfor the odor ofseeds.Ifodor i s the excl usi veor even the D rimary cue, kangaroorats shoul d be equal l y i i kel v ro di scoverei i he r controls or targets.Control sites were chosen from cups that the ani mal had usedto storeseedsi n the earl i esttri al s rn the arena.On the average,88 days had elapsedbetween the animal usins the sire as a cacheand the experi menterchoosi ng i t as a control . fue esti mate d the distancebetweentarget cache sites and control sites by using the number ofcups tei ther l i nearl yor di agonal l y)betteen eachconrro l and the cl osesttargetand countedthe centerdi vi der as equi val entto a 2-cup distance.The averagedrstanceberueen each conirol and the nearesttarget cache w as 8 + 0.9 cups. R ecovery sessi onsl asted 20 mi n. A l l cups i n the arenaw ere empti ed.and the numberof seedsl eft i n each targetsi te or control si te w ere counted.A targetcl r control w as consi deredretri evedi fat l eastone seedhad been removed by the ani mai . The order of si tes searchedw as evai uated fi om the vi deotapesofeach sessi on.A si te w as consi deredsearchedi fan ani mal had ei ther removed the poker chi p and dug i n the cup or arremptedto remove the poker chi p for more than 1.5 sec. S earche s w ere categori zedas: ( I ) targets;(2) control sl(3 ) nei ghbors.defi ned as anv cup adj acentto a cachesi te: and (4) uncategori zedsearches . defi ned as al l other cups i n the arena.

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Analysis Two measures were devised to analyze the data. First, the perc en t a g eo l t a r g e t c a c he sa n d co n tr o l ca ch e sr e tr ie ve d wa s cal culated. This measureshowed the animal\ recovery accuracy over the entire sesslon. The second measure. hit percentage,was based on t he o r d e r o f s e a r c h e s .It wa s d e sig n e dto b e a m o r e p r e cisemeasure of cache memory by limiting the analysis to the cups first searched by the animal. We analyzed the four categoriesofsearch types de, ich we d e fin e d a s the pers c r i b e d a b o v e u s i n g h it p e r ce n ta g e wh c en t a g eo f s e a r c h e si n ea chca te g o r yo fth e fir st se a r ch e so fthe sess ion ,u p t o t h e t o t a l n u m b e r o fo r ig in a l ca ch e sm a d e in th a t tr ial . For example. ifa kangaroo rat made four caches,and ifit then, during the searchofthe first four sites, would choose two target sires,one control site and one uncategorrzedsite. the hit percentagesrvould be 5 0 0 . 6t a r g e t . 2 5 7 oc o n tr o l. a n d 2 5 9 /ou n ca te g o r ize dsite s.

R.ESULTS Kangarooratsmadean averageof 2.1 + 0.2 cachesin eachof the four erperimentalconditions,placing I 1.4+ 0.9 sunflowerseedsin eachcache.Therewereno significant diflerencesin the numberof seedsplacedin each cacheper condition.Therewasa significanteffectofvisualenvironment on thenumberof cachesmade[F( I.5) : 10.0,p = .025]; the kangarooratsmadeon averageone morecachein the l6LM conditions.Because controlsites werechosenfrom thosethe animalhad previouslychosen as cachesites,their historyas cachescould havepotentially affectedtheir probabilityof retrievalas a control. Eighty-five percent(54164)ofcontrols $'erechosenfrom siteswherethe cachehad beenretrieved;ofthese, 51% (28154)were retrievedas controls.Of controlschosen from cachesthat had not beenretrieved,60% ( 6/ I 0 ) were retrievedas controls. Becausethepercentageoftargetsor controlsrecovered could havereflecteddifferencesin overallactivity level in the arena.the total numberof searchesthat animals madein eachconditionwas calculated.Therewere 13.3 per session,on the average. cupssearched Therewereno in totalnumberof cups statistically significantdiflerences persession[effectofretrievalinterval,F( 1.5): searched 3 .7 3,p: . 111;ef fe c to f l a n d m a rk F . (1 ,5 ) : 0 .9 6.p: : : .312'.interaction,F( I,5; I .192.p .3251.Therewas considerable variability betweensessions, however(mean n u m berof c upss ea rc h epde rc o n d i ti o n :l D , 0 L M. l9 7 + 7 .2 c ups ; lD, l6LM . 1 3 .2+ 5 .2 c u p s ; l 0 D , 0 L M, 9.3 r 4 .4 c ups ;l0D, l6L M. I I .2 + 2 .7 c u p s ). The animalsretrieveda greaterpercentageof target cachesthanofcontrol cachesunderall conditions.ascan b e s eenin F igur e2 . A th re e -w ' aay n a l y s i so f v a r i ance (ANOVA) of the effectsof retrievalintervaland visual environmenton the percentage oftargetsversuscontrols retrievedrevealedno effect of interval [f( I,5) : 4.21, p : . 0951or v is ua l e n v i ro n m e n t[f(1 ,5 ) : 5 .8 8 .p : .0 6 01.only an ef f e c to f ty p e o f s i te s e a rc h e d[F (1.5): 1 7 . 19,t r t: . 0091. The percentageof targetsretrievedwas affectedby . -- .0 1 6 ] and b o t h r et ent ionint e rv a l[F (1 ,5 ) : 1 2 .6 3 p vi s ualenv ir onm e n[F t (1 .5 1: 1 2 2 t, p : .0 1 7 ].w ith no si gnif ic antint er ac ti o nb e tw e e nth e s ee ffe c tsl ft t. St :

1.19,p : .2241.Plannedcomparisonsof percentof targets retrievedat the two retrievalintervalsrevealedno differencesbetweenthe0LM and l6LM conditionsafter a l D retenti oni nterval[f(1,5) = 0.004,p : .95].A fter the l0D retentioninterval.the differencebetweenretrievalin the OLM and l6LM conditionsapproached signi fi cance[F(1,5) : 6.162,p = .056].The retri evalof control sw as not affectedby ei ther retenti oni nterval [F( 1,5): 0.52,p = .501]or visualenvironment [F( 1,5): : 0.40,p .5551,nor did thesefactorsinteract[F( 1,5) : 0.23.p : .65ll. Comparisons of landmarkconditioneffectsat the two retentionintervallevelsalso showedno si gni fi canteffectsI D compari son, F(1,5) : 0.001.p : = .979;l 0D compari son, F(1,51 0.501,p : .51l l . We then analyzedthe initial searchesof animals,using hit percentages. Figure3 showsthe proportionof hits directedat eachsitetypeby condition.To establish whether initial searcheswere randomor directed.we first comparedsearches in cupsfor the combinedcategories oftargets, neighbors,and controls and comparedthat with searches of uncategorized sites.Of the 63 searches that constituted hits,pooledacrossall animalsandconditions, 6l rverein the combinedcategoryof targets,neighbors, and controls.Two searchesoccurredin uncategorized sites:One of thesewas a cup next to a control site; the otherwas isolated.On the average.of the 128cupsin the arena,30ofthem rveresitesconsistingoftargets,neighbors, and controls,and 98 cups were uncategorized. A chi-squaretestof the probabilityof the outcome of 2163 searches occurri ngi n the cupsthat consi stedof98/128 of the cups in the arenashowsthat this result was unl i kel y to occurby chance(X 2 = 67.145,p < .0001). An overalltwo-wayANOVA of the percentof target hits in initial searches did not revealany significanteffects [effectof retenti oni nterval ,F(1,5) : 0.430,p: .54l ; effect of l andmarks,f(1,5) :3.567, p: .l l 8; i nter acti on.f( I,5) : 4.217,p : .09511 seeFi gure4. P l anned comparisonsat the two retentionintervalsshowedthat therewasno differencein hits oftargetsat the I D retenti on i nterval[F(1.5): 0.013,p : .913].H ow ever, at the l0D retentioninterval.a significanteffectof landmarks w as found [f(1,5): 10.554.p: .0231.N o stati sti cally significanteffectsu,erefound in hit percentages ofcontrol s[retenti oni ntervalF( , 1,5) : 0.401, p = .550;l and marks.F(1,5) : 0.145,p: .530;i nteracti on, f(1,5) : 3.776,p: .l l 0]. C ompari sons at the tw o retenti oni n terr"alsalsorevealedno significanteffects! D. f( 1.5) : .302.p: .606; l 0D . F(1.-5): 2.893.7r: .l -s0l D IS C U S S ION The overallretrievalofmore targetcachesthancontrol cachesindicatesthat the kangaroorats rememberedthe locationof theircachesand usedthis memorl,to relocate them. It is unlikely that controlswere locatedby using menlory.because an averageof3 monthshadelapsedbetweentheuseofa siteasa cacheandits reuseasa control. In addition.the data stronglysuggestthat the kangaroo

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110 CacheRetrievalInterval (days) Figure 2. Percent retrieval ofcaches recovered during the cache retrieval session(N: 6). Open circles represent the average (+SE) performance in the 0-landmark condition and the filled circles represent the average(+SE ) performance in the l6-landmark condition. (A) Percentage of targets retrieved. (B) Percentage of controls retrieved,

rats treatedtargetsand controls differently.Note that all cupsadjacentto control siteswere classifiedas uncategorizedsitesin the hit analyses. Thesesiteswerealmost never searchedby kangaroorats: The percentageof initial searches ofuncategorizedsitesper conditionwasonly 0.8. By comparison,the percentage of initial searches of neighbors(sitesadjacentto targetcaches)per condition was 18.4.Finallv.initial searches ofneishborsoccurred

ofuncategorizedsitesocin all conditions,but searches curred only in the most demandingof the four conditi ons,the 10D ,OLMcondi ti on(Fi gure3). Fewercacheswere madein the OLM conditionsthan in the l6LM conditions.This might have affectedretrievalaccuracy;accuracyin the I D, OLM conditionwas not affectedby this difference,however.In addition, equalnumbersofseedswere storedacrossconditionsand

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100 90

ID -I6 L M

ID-O LM

r0D-r6LM

IOD,OLM

Figure 3. Distribution ofhits during a retrieval sessiondirected at site types. Hit percentage is defined as the proportion ofsites ofa certain type searched in the beginning ofa retrieval session,up to the total number ofcaches available at the beginning ofthat session,Open bars are proportion ofsearches in target caches,filled bars are proportion ofsearches in controls, hatched bars are searchesofneighboring sites to targets, and gray bar is searchesin all other uncategorized cups in the arena.

the hungerlevelof animalsacrossconditionsshouldhave beenthe same;thus,motivationto searchfor cachesshould also havebeenequalacrossconditions. The accuracyof cacherecallwas rnanipulated via the two parameters thatwe predictedwould interactto affect ca c her et r iev alac c u ra c y :a n i n c re a s e dd e l a y b e tw een cachingandretrieval.andthepresence ofa uniquevisual array of landmarks.We usedtrvo differentmethodsto analyzecacheretrievalaccuracy:hit percentageof targetsand percentrecoveryof targets.The percentage of targetshit was not differentin the two landmarkconditi o ns in t he lD r ete n ti o ni n te rv a l .l n th e l 0 D i n terval . however.the percentage of targetshit was higherin the l 6 LM c ondit iont ha ni n th e 0 L M c o n d i ti o nT . h e re sul ts o f t he analy s esusi n g p e rc e n tre c o v e ryo f ta rg e tsw as similar to the hit analyses.rvith the differencebetween th e l6LM andO LM c o n d i ti o n si n th e l 0 D c o n d i ti o nsapp roac hings ignif ica n c e . There were no statisticallysi,unificanteffectsof the manipulationson recoveryof control caches.However, the percentageof controlsrecoveredin the I 0D. OLM conditionwas lowerthanin the otherconditions.Perhaos failing to find or remembertheir own cachesled to a decreaseddrive to searchfor caches.This is supportedby

the decreasein overallnumberof sitessearchedin this condition.The drop in activitylevelandcontrolsearches in this conditiondoesnot invalidatethe overallresults. however.In the hit analysis,while percentage of targets hit waslowerin the l0D. 0LM thanin the l0D. l6LM condition.the percentage of controlhits washigher.andthis shou,sthe oppositeeffect(Figure4). The animalsusedfor the testphaseof the experiment werethosemostlikely to cachereliably.Our elimination procedureproduceda mix of one-thirdmaleandtwo-thirds femalesubjectsin this experiment.A previousstudy of cacheretrievalin Merriam\ kangarooratsshowedno sex di fferencesi n retri evalaccuracy(Jacobs.1992).H ow ever.in a studyofsex differencesin the desertkangaroo rat (DiTtotlonn's deserti\. Langley fbund that t'emalekangarooratswereableto useintra-apparatus landmarkcues to l ocatea goal ,w hereasmal e kangarooratsdi d not l ocatethegoalby usingthesecues( Langley,I 994).In addition. Williams. Barnett.and Meck ( 1990)found that femaleNorwayratsreliedmoreheavilyon visuallandmarks to food locationsthandid males(alto orientthemselves thoughin that studythe landmarks\\,ereextra-apparatus). Thus. if femaleMerriam'skangarooratsparticularlyatl andmarksthat w e tend to the ki nd of i ntra-apparatus

KANGAROORAT MEMORY

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A) Targets 100

90 q)

(.)

80 70

h

60 50 40 o

N

30 20 l0 110 Cache Retrieval Interval (days)

B) Controls 100 90 a

80 70 60 50 40 q

s

30 20 10

CacheRetrievalInterval (days) Figure 4. Searchesduring retrieval sessionsdirected toward target and control sites. Hit percentag€ is defined as the proportion ofsites ofa certain (vpe dug in the beginning of a retrieval session, up to the total number of caches available at the beginning of that session.Open circles represent the average (+SE) performance in the O{andmark condition, and the filled circles represent the average(+SE) performance in the l6-landmark condition. (A) Hit percentage of targets. (B) Hit percentage of controls.

choseto manipulatein our experiment,the sizeof our effect could havebeen influencedby the high proportion of femalesubjects.Futurestudiesdonewith artificial tasks may be able to test the effectsof landmarkmanipulations withoutthenecessifyof subjectelimination,andwith equal proportionsof malesand females. We choseto manipulateintra-apparatus cues ln our experiment.In other studies.intra-apparatus cueshave

beenmoresalientthanextra-apparatus cuesin a discrimi nati ontask(e.g.,C hami zo,S teri o,& Macki ntosh,198 5; March,Chamizo,& Mackintosh,1992).Langley'sfoodfinding study,with desertkangaroorats.yieldedthe oppositeeffect:animalsdid not rely primarilyon intra-apparatuscues,but i nsteadori entedthemsel vestow ar d goalsby usingextra-apparatus cues(Langley,1994).Such differencesin cue saliencvmav derivefrom the tvpe of

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cueratherthanits positionrelativeto the maze,however. In the presentexperiment,we choseour landmarksfrom a large pool of uniquely shapedobjects,such as rocks and flowers.In contrast,the intra-apparatus objectsin Langley'sexperimentwere symmetricallyplaced and identicallyshapedobjects(four wood blocks).Perhaps eitherthe varietyofobjects, and/ortheir trial-uniquespatial configurations,increasedthe saliencyof our intraapparatuscuesand hencetheir utility for predictingthe locationof caches.In additionto the type of landmarks, our useof trial-uniquelandmarksin habituationandpretest trials may have affected how the kangaroorats respondedto thetestingconditions.For example,theymay havebecomemore attentiveto the landmarksonce they learnedthat the landmarkswere trial unique and hence useful in predictingthe locationof cachesfor retrieval. Thus spatialmemory for cachescould be influencedboth by the kind of landmarksavailableand by the training procedures. How l6 landmarkshelpedmaintainmemoryfor cache sitesover many daysremainsto be determined.On the onehand,kangarooratscould uselandmarksto enhance their recall ofcachesthroughan increasedprecisionof encodingcachelocation.If, for example,they uselandmarksto encodelocationsby calculatingvectorsbetween cacheand landmarksites(Collett,Cartwright,& Smith, 1 9 86) ac , c ur ac ywo u l dd e c re a sien th e 1 0 D ,OL Mc ondi tion becausethe arenais bareand precisecodingis thus difficult. This would not be surprising,given that many scatterhoardersusenearbylandmarksto calculatelocationsof cachesor goal sites(Balda& Turek,1984;Kamil & J ones 1997; , V an d e rW a l l , 1 9 8 2 ,1 9 9 1). Si m i l a rl y,l aboratory rats swimming in the Morris water maze concentratetheir searchmore preciselyaroundthe hidden platform when there are more spatialcues in the environment(seethe comparisonof datafrom Pellymounter, Smith,& Gallagher,1987,and Rapp,Rosenberg, & Gall a g her ,1987,in Le o n a rd& M c N a u g h to n ,1 9 9 0 ).Thi s hypothesisofprecision,however,doesnot explainwhy the value of landmarksfor retrieval accuracywould increas ewit h lim e s in c ec a c h i n g . A n alt er nat iv eh y p o th e s i si s th a t tri a l -u n i q u elandmarksenhancememoryaftera long intervalby reducing proactiveinterference from previoustrials.Reducinginterferenceby changingcontextualcues,such as maze color or floor texturebetweentrials.reducesor eliminates forgettingin laboratoryrats, even 40 days after training (Zentall.l970).Althoughthis studyonly showeda reduction in retroactiveinterference,changingthe spatialarray ofobjectsshouldalsoreduceproactiveinterference. This hasbeenfound in radialarm mazeexperimentsin which proactiveinterference is reducedwhenintra-or extra-maze cueswerechangedbetweentrials(Cohenet al.. 1994).In addition, food-storingbirds testedin food-finding tasks cannotrememberthe baitedlocationunlessthey areprovi d edwit h t r ial- un i q u ec u e s(B ro d b e c ke t a l ., 1 9 9 2\.l n our experiment,aswell as Brodbeck's,thesetrial-unique

spatialcuesmay havebeenactingto reduceproactiveinterferencebetweenrepeatedrecall testsin the sameenvironment.Without uniquespatialcues,interferencemay blur the distinctionbetweeneventsin the sameor similar environments, making it difficult to distinguishbetween theseeventsover long time periods. Retrievalintervalshavealso been found to be important in proactiveinterferencein Norway rats,with longer retrievalintervalsproducingmore interference(Roberts & Dale, 1981).Althoughwe did not find retrievalinterval by itself to causedeteriorationin recall,we did find that the retrievalintervalactedwith the absenceoflandmarks to reducecacherecoveryaccuracy.Our failure to find a reduction in accuracywith the retrieval interval manipulationalone may have stemmedfrom our choice of l0 daysasour longestinterval.Previoustestsofcache memory in the black-capped chickadeeshowedno deteriorationof memory before28 days(Hitchcock& Sherry, 1990).This is the shortestretrievalintervalafter which a reductionin cacherecoveryaccuracyhasbeenobserved in the laboratory.And althoughwe cannotdirectlycompare our resultsfrom a mammalianspeciescachingin two dimensionsto thosefrom an avian speciescaching i n threedi mensi ons,i t i s nonethel ess stri ki ngthat w e could producea reductionin accuracyin as shortan interval as l0 daysby forcing animalsto cachein a bare environment.This suggeststhat a profitable approach for future researchmay be to manipulatethe visual environmentof the cachingsession,ratherthanthe length of the retrievalinterval,to measurethe memory capacity of scatterhoarders. Landmarksclearlyplay a role in memoryfor cachelocationssincescatter-hoarding animalsappearto rely on the relationshipbetweentheir cachesand nearbylandmarksto returnto specificlocations(Balda& Turek,1984; Bennett,1993;VanderWall, 1982, l99l). Yet what has not beenunderstoodis whetherlandmarksarenecessary for rememberingcachelocations.Although our results show that landmarksare not necessaryover short retention intervals.they appearto play a crucial role in sustainingthe memory overlongerintervals.In our experiment,we manipulatedthepresenceof landmarksandthe trial-uniquearrangementtogether,however;future researchshouldexplorehow thesefactorscanbe separated so thattheirindependent rolesin influencingmemoryfor cacheslocationscan be evaluated. Finally,our finding that trial-uniquelandmarksare lmportantfor sustai ni ng spatj almemoryoverti me i s si mi lar to findings from testsof spatialmemory in laboratory rats(Cohenet al., 1994;Zentall,1970).However,scatterhoardingspeciescanrememberlocationsin spacelonger thanotherspecies(Hilton & Krebs, 1990;Krebs,Healy, 1990),andcanrely on a differenthierar& Shettleworth, chy ofcuesto relocatespatiallocationsfrom thatusedby nonstoringspecies(Brodbeck,1994;Clayton& Krebs, 1993).Thus it is not yet clearwhetherthereis a qualitative differencein the effect of landmarksand test latencv

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on recall accuracyin scatter-hoarding speciesofrodents Htrcucocr, C. L., & Suennv,D. F.( I 990).Long{erm memoryfor cache si tesi n the bl ack-capped chi ckadee. A ni mal B ehavi our,40.70l -7 12. and larder-hoardingspeciessuch as the laboratory rat. In conclusion,this study showsthat intra-apparatus JAcoBs,L. F. ( 1992).Memory for cachelocationsin Merriam'skangaroo ral s.A ni mal B ehat'i orr.43.585-593. landmarksplay a significantrole in the memoryfor caches JAcoBs.L. F ( I 995 The ecologyofspatralcognition:Adaptivepatlerns ). of kangaroorats u'illing to cachefrequentlywhen there ofhi ppocampal si ze and spaceuse i n w i l d rodents.In E . A Ii ev a, A. Fasolo,H.-P Lipp, & L. Nadel (Eds.),Studiasql the brain in natis a lengthy delay betweencachingand recovery.These uralisticsettings(NATO AdvancedStudiesInstituteSeriesD, Vol. 82, landmarksmay be important in memory either because pp. 301-322).D ordrecht:K l uw er. they allow the animal to calculatethe preciselocation of Jncoes,L. F, & LIvnN , E . R . (1991).Grey squi rrel srememberthel oeachcache,or becausetheyprovidea uniquespatialarray cati onsofburi ed n)ts. A ni mal B ehavi our,41,103-l10. that the animal can use to discriminatebetweencaches JeNrrr.rs,S. H., & PErEns,R. A. ( 1992).Spatialpatternsof food storage by Merriam's kangaroorats.BehavioralEcology.3, 60-65. madeoverrepeatedtrialsin the samearena,reducinginter(1997).The seed-stori ng corvi d C l ark ' s ferencefrom previoustrials.Futureexperiments arising K rvrr,, A . C ., & JoN rs, J. E . nutcrackerlearnsgeometricrelationshipsamonglandmarks.,\alure. from the presentstudywill help determinewhat informa390,276-279. tion scatter-hoarding animalsarestoringin memoryabout K ness.J. R ., H enl y. S . D .. & S sE rrr-E w onrs, S . J. (1990). S pati al memoryofParidae:Compansonofa stonnganda non-storingspecies. the visual scenesaroundtheir cachesand further our unthe coal tit, Parusater, and the greattit, P. major. 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