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The Ecology of Spatial

CHAPTER · DECEMBER 1994 DOI: 10.1007/978-94-011-0091-5_16

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64. Scltcnk.F(l9tl9)Ahottringptrrcutlurcfi)rsludyingsputillrnorrroryinirrrrurlurcanrlarlulltrdcnts,J Neuntst:i. M cth.2(>, 249-258. 6.5.Scht:nk,lr.,Cotttltrtt,l|.,irnrl(ilolfly,M.C,(1990)Alglc;rnrldircctiorlrlitylrlltctrirl'sorganizirtiorr6l visit scqucnccsand spatial lcarning in rrrodularnraz.cs, Leurn. Motiv. Zl,164-189. 6(r. Schcnk,F.,Contant,ll.,andWcrffcli,l'.(1990)lntrahippocarnpalcholincrgicgraftsinagcdratsconrpcns:rlc impairmcntsin a radialrnazc and in a placelcarning task., Exp. Bnin Res.E2, 64 l -650. THD ECOLOGYOF SPATIALCOGNITION 67. Schenk,F. and Gafner,M. (1992) Spatiallearning under limited accessto visual landmarks,Z)r ./. Neurosci.,Suppl. 5, 23 15. Adaptivepatterns of spaceuse and hippocantpal size in wild rodents 68. Schenk,F.andCafner,M.(1993)Placelearningintheabsenceofvisualcues,Ear.J.Neurosci.,Supp!.6, 69. Schenk,F.andMorris,R.C.M.(1985)Dissociationbetwcencomponentsofspatialmemoryinr^rsafrcr rccoveryfrom theeffects ofretrohippocampal lesions, Exp. Brain Res.58 I l-2g, 70. Sharp,P.E.,Kubie,J.L.,andMuller,R.U.(1990)Firingpropertiesofhippocampalneuronsinavisually L.F. JACOBS symmetricalenvironment: contributions ofmultiple sensory cucs and mnemonic processe s,J. Neurosci.ld, 3093-3105. Dept. of Psychology,Universitl- of California ?l' SindenJ.D.,Hodges,H.,andGray,J.A.(inpress)Neuraltransplantandrecoveryofcognitivefunction, Berkeley,Califurnia 94720, USA Behav.Brain Sci. 72.Squire,L.R. ( 1992) Memory and the hippocampus: a synthesis from findingswith ratsand humans, P.ryclal, Ilev.99, 195-231. Strijkstra,A.M. and Bolhuis,J.J. (1987) Mernory persislancc of ratsin a radialrnazc varies wirh rrainins procedure,Behav. Neural Biol. 47, 158-166. humanbody represents a whole museum of organs,each with a longevolutionary 1A "Justas the Sutherland,R.J. and Dyck, R.H.( I 983)Hippocampal and neocortical contributions to spatiallearning and history,so we should expect to findthat the mind is organizedin a similarway. It canno more memory,Neurosci. Abstract I 13 89.9. bca productwithout history than is the body in whichit exists". 75.Suzuki,S.w, Augcrinos, C., and Black, A.H. ( t980)Stinrulus control of spatialbchavior on rhe cight-arrn mazein rats,Izarn, Motiv. ll. l-18. CarlJung, Man artd HisSymbols (1964) 76.Thinus-Blanc,C. (1987) Cognitive Processes ond Spatial Orientation in Animaland Man, NATO Scienrific Affairs Division,Dordrecht. 't't . Thinus-Blanc,C. (in press)A modelof animalsparial cognition, in H. Roitblatand J. A. Meycr (cds.), 1, Introduction ComparotiveApproach to CognitiveScience, MIT Press, (Mass.). Cambridge To understandthe brain and its function,it will benecessary to understandits evolutionary 78.Wilkie, D.M. andPalfrey, R. ( 1987)A computersimulation modei of rats'place navigation in the Morris watermaze, Behav. Res. Meth. lnstr.Conp.19,4ffi-403. history.It isthus not surprising that one of mostexciting developments in Whishaw,l.Q. ( I99l) Localeor taxonsy.stems: no placefor neophrcnology?Hippocompus l,272-274. isthe interface between cognitive and evolutionary biology. Certain areas of intersectionmay be more profitable than others, and in thepresent chapter, I will arguethat one of the most importantquestions is the ecologicaland evolutionarysignificance of spatialcognition. Spatialcognition is a majorfocus of cognitiveneuroscience. Yet in therush to understand spatialcognition in humans,more fundamental questions have often been left behind.For cxample,howdid spatial cognition evolve?Why did spatial cognitionevolve?Whatcurrent ccologicalvariables prcdict specializations in spatialcognition and its neuralbasis? A complereunderstanding of this ability will rcquiremultidisciplinary studies of theecology' mechanismand function of spatialcognition. Whatis the ecology of spatialcognition? Ironically, an animal's knowledge of thespatial distributionsofresources isthe cornerstone ofbehavioral ecology, the study ofthe "survival valucof behavior"[40]. Oneof its basictenets is thatthe spatial and temporal distribution of criticalresources, such as food, refuge or mates,will determinethe spatial dispersion and hencesocial organization behavior of animalscJnrpeting for suchresources [42]' This theoryhas predicted complex social and competitiveinteractions in a varietyof animal species,both vertebrateand invertebrate,terrestrial and aquatic [40]. ln short,an animal'sknowledge of spatialdistributions is criticalto its survivaland reproduction.To studythe evolution of thiscognitive trait requiresknowledge both of its phylogenetichistory and comparative studies of itscurrent function. Comparative studies iemanda diversityof speciesro bepowerful and it is a happycoincidence that we have clctailcclknowlcdgc ol'spatial cognition in a laboratoryspecies, the Norwegian rat, which, 301 E. Allevoet al.(eds.), Behavioural Brain Researchin Naturalisticand Semi-NaluralisticSettings,30l-322. @ 1995Kluwer AcademicPublishers. Printed in rheNetherlands. 303

asa rodcnt,bclongs to thc rnost divcrsc orderof mammals, thc ordcr Rodcntia. Iio

Addingto thcunprcdictability of thisrcsourcc is thctcrnporal distribution ol sccds.Oak Caching andhickory trcc spccicsarc "masting"spccics: individual trces producc a largecrop at r14 r5 --* * **r rg\ I \ irregularintcrvals [521. Thus a squirrclcannot prcdict thc cxact spatial distribution of foocl "\-*1.1.", '\----rd withtlutcarcl'ully sarrrpling thc quality and dcnsity ol'nuts on a lurgcrnurnbcr ol'trccs. Anr.l ( \ i:6 I sincethis distribution changes daily, depending on the nuntbcr ol'compctitors, this task /\ 7d. e\i may \r 1,-''.l requirca largcspatial ntcmory capacity. \ I '{/,1.-'-/r'r Manytree squirrcl species lacc an evcn nrorc challenging task: thcy scattcr-hoard. Birds \?, and mammalsthat scattcr-hoard storc all ---i thcir lbod in small,undel'cndcd caches [46], i*:-".""" a7 thoughscatter-hoarding isbest defined as the single deposition offood to a storagesite [83]. t Thisdistinguishes it from themore familiar type of hoardingin rodents,larder hoarding, or multipledepositions to the samesite. Thus scatter-hoarded,but not larderhoarded, food cachesmust be rclocated at thetimc of consumption,which may bc hours,days or months Retrieval routes afterthey werefirst cached.Thus scatter-hoarders must find their food twice:first. when lS'o*^ ..- r -dJ s it is harvestedand second, when the cache is retricvcd. .} o.- This doublechallenge has resulted in specializedspatial memory abilities in scatter- t"*-'\ hoardingbirds (see chapters by clayton andKrebs, and shettlcworth, present volume). dr. Early work on marshtits andblack-capped chickadees additionally demonstrated that the o\ birdswere not findingcaches by theirodor [70]. In contrast,mammalian scatter-hoardcrs f*-***"..1 havelong been assumed to relyexclusively on odorcues to relocatctheir caches, and to eschewthc use of mcmory[75], dcspite the famcd ability of laboratoryrats in remembcring I dat thelocations of scattcredfood items [54]. Graysquirrels are obligate food-storers, depending completely on theircached seeds for Figure 2. Schematicrepresentation ofcaching and retrieval routesby the squirrel Alvin, aftera delay ofwo winter survival [78]. In addition,gray squinelsbreed in mid-winter,and this fact may days. Solid squaresare Alvin's caches,open squarcsar€ the cachesof other squirrels,Numbers refer to the sequencein which nutswerecached orretrieved, thearrow indicatesthe locationofthe observerandthe source explainthe strong correlation betwcen adult fcmale fecundity and the size of thehickory nut of hazelnuts(adapted from [30]). cropshown [5 | ]. Thusa graysquirrcl's ability to rctricvcits cachcs, wecks or monthsalicr caching,not only dictatesits survivalbut also its reproduction. Graysquirrels frequently cache nuts in areasthat adjoin or overlapwith thecaching areas week.Thus, the retrieval condition mimicked the situation faced by wild graysquinels of of othersquinels [26]. Field studies have shown that tree squirrels can locate experimentally looking for their own cachesamongst a backgroundof6ther squirrels'caches. buriedseeds by theirodor [4, 14,15,78).If they can also remernbcr cache locarions, gray Althoughsquirrels buried nuts in areaswhere other squirrels had also buried nuts, they squirrelswould have a rninimumrcpertoirc of tworctricval stratcgics: trial-and-error scarch retrievedsignificantly more nutsfrom their own cachesites than from thecache sites of for cacheodor, whcther of theirown or of othersquirrcls' cachcs, and nrcmoryfor the other squirrels,even after delaysof 4 or 12 days.This retrievalaccuracy could not be locationsof theirown caches. explainedby thesquinels' habitual use of thesame areas: the ratio of own cachesto other cacheswas greater than expected based on the availabilityofcaches in thearea searched 2.2.THEROLE OF MEMORY IN CACHERETRIEVAL duringretrieval. A squinelwas also more likely to retrieveits own cache even when another To fi ndout whcthcr gray squ irrcls can rcnrcnrbcr cachclocations, I rncasurcd cachc rctricval squirrel'scache was closer to it or whena squirrelneglected to retrievethe cache closest accuracyin captivcgray squirrcls, by comparing theirsuccess in retrieving nuts liom caches to itself and insteaddug up a moredistant nut. Thus the results of thisexperiment clearly that they had made,and cachesother squirrelshad made.Il a squirrelremembers the showeda biasof about2:l in favorofown caches.In addition,the path taken and the order locationsof itscaches, then it couldretrieve moreof itsown caches than another squirrel's in which cacheswere taken suggested the useof a cognitivemap of thecaches. Figure 2 caches. showsthe routes taken in onetrial after a two daydelay. Such an extreme difference in these This propositionwas testedon eight hand-rearedmale gray squirrels,caching and routessuggest the use of a predeterminedroute based on acognitive map of thecaches. With retrievingnuts in a large(5x l0 m) outdoorarena. Squirrels wcre allowed to cachehazelnuts sucha map,a squirrel,having maximized cache dispersion and hence maximized the length andthen several days later, were re-released into thearena to find themagain. During the of routestravelled during caching, could then minimize travel distance during retrieval [30] . delays,the original nuts wcre unearthed and, for theretrieval phasc, new nuts wcre buricd It is anadvantage ofstudying a walkingscatter-hoarder, such as a squirrel,that these travel in theirplace. In addition,the number of cacheswas doubled, by addingl0 morecaches to routescan be moreeasily measured than the routes followed by a scatter-hoardercaching theoriginal number; the locations ofthese caches had been chosen by othersquirrels that in threedimensions, such as a bird. 306 307 Thiscxperiment dcntonstrated thata graysquirrcl coulcl use two simultancousretricval stratcgics:olfactory trial and crrorscarch and mcnrory of spccil'iclocations. Ilr somc ways, thisis not surprising,given thc naturar historyof thegray squirrer. First, vision prays an importantrolc in thcirbchavior, 1)80 Graysquirrcli arc

)| ! A. r'o I x 4. a *-*-*l*r-" .-.*^-*-,-.- at a ".r.""*, ;r" I x a t xX o lo )o tt 2. to 5. T O

u. -*"*o-o** aa tom o-"o"o-,..^.""o I o. I . o 3. aa oo I aaa ao o t.. oI al o I 1m ? i oo I $ in sixconsecutive trials by onekangaroo rat (male 6 I 3). Open oo o I Figure5. Thedistributions of cachesprod uced I ? squaresi ndicate plares that contained a rcgulararray of I 6 sand-filledcups for cachinglsolid squares indicate o oo a arcasof thc arcnawithout santl cups for caching.Frlled circlcs indicatc cache locations (adapted fronr [27]). I o****'**-o --*'o*.*'**6 tttl,scus)yielded the following results. First, a kangaroorat's caches can be pilfered by up Figure4.The cachedistribution and subsequent pilfering of cachesin onefocal individual, Female HL l. A) in additionto predationsby otherkangaroo rats' Second, Thesolid circle indicates her current day bunow, t he fi |led square indicate provisioning sitcs, to threeof four otherspecies, andX's indicatc pilfcred cachcs.Light hatchcdareas indicate her nlovelnentsprior to provisioning.B) Circlcsindicares rrap srtes. pilieringkangaroo rats are olien ncighbors, and finatly, caches are morc likely to be Filled circlesindicate that the trappedanimal showed evidence ofdye in its bolus.Solid circle the tiap site in o."o, whereanimals are at a high density.Thus in ourstudy site, evidence from thedyed of theprovisioned kangaroo rat, femaleHLI ; the hatchedcircle indicates the trap sites of orherin

In addition,kangaroo rats may havcto kccptrack of theplace of risk.our long-tcrnr monitoringof kangaroorats show that prcdation events are not independent; a cluster of prcdltionsby accrtain typc of prcdator,such as Crcat Horned Owl, suggestspredators move throughdesertconccntrating onlocal areas. Although this raises interesting questions about thespatial cognitive ability of owls asthey search for kangaroorats (especially as owls on (D oursitc olicn scattcr-hoardkangaroo rats alicr theyhave bcen killed !), it alsosuggests such l)lltcnl.sarc l)r'cdictablc, und tltus can lrc lcllncd by lcsidcntkirnguroo rnts. Cuncnt rcscirrch Q in my laboratoryis addressingthese questions. Thus, it is clearthat the risk of predationmust continually act to reduceaboveground activity.Our evidencefor thiscomes from theradiotracking records of animalsthat were subsequentlytaken by predators.Our standarddata on movementsconsists of hourlyradio- fixes,which yieldsmean movement between fixes. Records collected between 1980 and FE8E3Rftgss8sEE 1990on 50 predationevents, allowed us to comparethe movements of 44 recentpredation victimswith other kangaroorats trackedsimultaneously but escapingpredation. The comparisonsupports the hypothesis that activity is costly:victims had moved significantly Timeof Night greaterdistancesbetween radio fixes than their contemporaries atthe time of theirdeath [8]. 3.3.SEX DIFFERENCESIN SPACEUSE Figure 6' AbovegroundactivilY as-revealed by. kangaroo rats' rneandistance from their day burrow ar scheduledhourly radiotransmitterfixes' If activityincreases the risk predation,why o".o.ding ti moon phase.Data are pooi"; ;;;179 individuals of aresome kangaroo rats more active? One of trackedbetween I 980 and 1990.on thedeep CanyJnsite, and arefrom dateswithin 3 weeksof the wintcr themain predictors of activityis reproductivecondition. Both males and females increase solstice;sunset occurred within the hour before the I 700radio fix andsunrise w ithinthe hour after 0600 radio fix (adaptedfrorn [6]). the ratesof movementin their home rangeduring the breedingseason [2], and this is corrclatedwith incrcasedprcdation. Howevcr, thcrc is alsoa sexdifference in thechange 3.2.PREDATION AND SPACEUSE of activitylevel and hence in therisk of predation.Males show significant increases in the Among rateof movementrelative to females,and this is correlatedwith a correspondinglyhigh rate themost conspicous adaptation of kangaroorats to their nicheare their anti-predator of predation.Why do malesincur higher risk? In kangaroorats, it appearsthat familiarity adaptations,i.e., fast locomotion and abirityio detect predators g4]. by sound[79, Thus breedsnot receptivityto kangaroorats specialize in foraging contemptbut mate.Male kangaroorats increasevisitation to underthe constraints ofconstani predation risk, further shapingthe spatialcognitive neighboringfemales and such increased visitation appears to positivelyinfluence female taskthey face.They must not only rememberwhere their cachesare, whcre thcir pilfering matechoicc [62,63). ncighborsarc and cvcn whcrc thc cachcs of thcirpilfcring ncighborsarc, but whcrc anclwhcn it is sal'cto rbragc,cachc and to rctricvecachcs. 3.4.SEX DIFFERENCESIN SPATIALLEARNING on our study site in s,outhcrn carifornia(Dccp CanyonDcscrl RescarchStation), Suchsex differences in spaceuse are typical in polygynousmammalian species. Females Merriam'skangaroo rats facc a panopry of predators.wc havcdocumented predation by gencrallyhave small, localized ranges, while rangeexpansion is an importanttactic used coyote(Canis latrans), grcat horncd owl (Bubo virginianus),northcrn shrikc (I_a,la.s by polygamousmales to maximizethe numberof potentialmates [82]. Thus,in these ludovicianus)and four spccicsofsnakes (3 rattrcsnakcs,l gopher snake) [g]. we havc systems,mobility confersgreater reproductive benefits on malesthan on females.This docuntcntcdonc rcsponsc irr tlctail:lhc ilvoidancc ol';rctiviry urrclcr bright rnoonlight. This lcadsto inequalityof spaccuse during thc brcedingseason and thus under polygamy, the is a wcll describedphcnonlcnon: nocturnaldescrt rodent.s arc lessacti-vc undcr high Iight two sexesexperience divergent selective pressures for spatialability. Underpolygyny, conditionsof the full moon (rll. [43, Howcvcr,.ur rcsults,based on datafrom 156 malesshould profit more than females from anyincrease in spatialskills thatcould facilitate radiotaggcdkangaroo rars trackcdbctwcen l9g0 and 1992ontheDccp Canyon sitc, show rnobility.The processof acquiringmates might include:locating and remembering the thatkangaroo rats are exquisitely sensitiveto time of risk. We foundthat avoidance of burrowsof females,monitoring their state of receptivityby olfactoryinvestigation, leaving activityis modulatedhour by hour,that the pattern reverses underdark moon conditions [6] scentmarks at regularintervals such that familiarity is increased- all of thesetasks could andthat changes in activity influencenot only theirrisk ofpredation but also their risk to requirea significantcommitment to spatiallearning. certainspecies of predator As t8]. seenin Fig.6, duringthe full moon,Kangaroo rats However,such sex differencesin spaceuse are absentin specieswith monogamous concentratetheir aboveground activity during the crepuscularperiods. Theoppositepattern matingsystems [57]. In monogamousspecies, the sexesexhibit convergent reproductive is seenduring the new moon, the darkest period ofihe lunarcycle: kangaioo rat activity strategies.They exploit the environment in similarways and thus express similar patterns peaksat midnight[6]. ofspaceuse (Fig. 7). Gaulin and FitzGerald [20,22) predicted that such differences in space 3t2 313

Polygamy Monogamy in rnalcslionr scvcralpolygamous spccics 112,22,861 similar pattcrn has bccn obscrvcd in ourown spccics[38]. In contrast,polygamous females show differentspecializations in spatiallearning. Femalesappear to attendinstead to more fine-grainedspatial details of an environment, Jg such as the appearanceand locationof visual landmarks.In laboratoryrats, if such Fe Itndnrarksarc altcrcd,lbtnalc pcrfonnancc shows rnuch greatcr disruption than nralc pcrlbrmance[86]. :*{"E Suchspecialization in femalespatial learning has also been demonstrated in humans[72] Jg anddesert kangaroo rats. Kangaroo rats were trained to locatea hiddenplastic token which, fe. if found,resulted in a food reward.Using similar methods to studiesof laboratoryrats, the arenawas rotatedto disruptperformance; as predictedfemale performance was more disruptedthan that of malesby suchrotations [42,. Figure 7' Schematicdiagrarn of spaceusc in rnatnrnalianspccics with tjiffcrcnt nratingsyslclrs. un(lcr and the Hippocampus polygamy, malc honlc-rangcs 4. Brain Allocation cncotnpassscvcral smallcr I'cnralcrlngcs; undcr rrxrnolarny,lrralcs nnd femalesshare ajoint homc-rangeor territory. Othercontributors to thisvolumc will haveaddrcsscd questions of hippocampalstructure, function,genetics and development in detail(see chapters by Claytonand Krebs,and Shettleworth,present volume). Thus I will passlightly over these topics and concentrate usewould resu lt inthc prcscncc ol'scx d if'fcrcnccs in spatiallcarn ing in polygamous spccrcs, instcadon simplcpattcrns of hippocampalsiz-e in wild rodentsand their ecological and andthc absencc ol'such dil'l'crcnccs in monogamousspccics. They tcstJthis hypothcsis evolutionarysignificance. with severalspecies of volcs,rodents in thegcnus Microtus,a gcnus which displaysnearly with natural theentire range of marnmalian The first suggestionthat the sizeof the hippocampuscould be correlated matingsystems, from promiscuity to monogamy [55]. Thus in polygamous patternsof spatialbehavior came from studiesof passerinebirds [5,41,7l]. The spccics,such as thc mcadow vorc (M. pennsylvanicu.s), brcccting rralcs may range cxtraorclinaryrcsult that food-storingspccics havc proportionatelylarger hippocampal over areaslbur to livc timesgreatcr than thoseol' brcedingfemalcs. This sex formationsthan speciesthat do not storefood openedup a new field: neuroethological differencein rangesize is absentamong immature meadow voles and among adults outside studiesof spatialcognition. Yet our knowledgeof hippocampalfunction was still limited thebreeding season, indicating that range expansion is a sexuallyselected inate rcproduc- (actic. to studiesof laboratoryrodents, raised and tested under simple laboratory conditions. The tivc Monogatntlusvttlc spccics, suclr as pinc (M. pirtctot:uttt) and prliric v1;lcs(M. lollowingstuclics arc a lirst attcrnptto trridgcthis gap bctwccn thc ncurophysiologyol' ochrogaster),lack such scx difl'crcnces in rangingbchavior, rcgardlcss ofage orrcprocluc- spatialcognition in thelab rodent and the role of spatialcognition in thebehavior of wild tivecondition. As prcdicted,volcs of polygamousspccics exhibitcd strong scx dil'l'crcnces rodents. in spatialability; in contrast,monogamous volc species, testccl undcr iclentical conclitions, lackcd Siz.c,of coursc,is a crudemcasure of brainallocation. However, it is a basicprinciple of strchscx dil'l'crcnccs (rcviowcd in llgl). Thchypothcsis thnt scxual sclcctiorr clrr braincvglution that incrcascd function is rcflcctcdin incrcascdcomplexity of its ncural predictpatterns ol' spatiallcarning ability, also ofTcrcdan cxplanationlbr prcvious basis.Although this has rccently been questioned [66,671, it isstill aconservative and useful obscrvationsof scx clil'l'crcnccsin spatiallcarning in laboratoryrats, a dorncsticateol' pointwith whichto thinkabout brain evolution. Thus, given the caveat that the polygynousanccsrry I l4]. starting 1ptio6ol'"biggcr is bcttcr" is always an assunrption tobc tcstcd (scc itlso chaptcr by Dcitcon, 3.5.SEX-SPECIFIC SPATIALABILITIES presentvolume), we canask questions about the relative allocation ofbrain to functional Thc dif'f'crcncchctwccn ntalcs antl f'crnalcsilppcars to rcsult lionr two scx-spccil'ic subunits.In thccase of thehippocampal formation, we assume that certain species will need spccializ.ationsin spatial learning: navigational ability ancl mcmory lbr objcctlocation. morcdctailed cognitive maps or a greaterstorage capacity for spatialdata or evena faster Navigationalability has bccn conccptualizcd as thc ability to lbrm cognitivcnraps, from codingand/or rctrieval of spatialinformation. All of theseconditions might be sufficient whichan animal may construct novelroutes to Iocations, or constructroutes based on partial selectivepressure to changethe allocationof brainspace to incrdasedinvestment in the arraysof landmarks[81]. This is an oversimplification, of course, of animportanr concept hippocampalformation (or, as I will referto theAmmon's horn and dentate gyrus in therest which hasbccn and conrinucs to bc discusscdat manylcvcls ofanalysis Ilg, 53,60] (scc of this chapter,the hippocampus). As discussedelsewhere in this volume,the sizeof the chapterby Schenket al., presentvolume). However, for presentpurposes it is this typeof hippocampalformation in songbirdsis correlatedwith food-storingbehavior. spatialability that is requiredfor locatingand rememberingthe locationsof ephemeral Thus,one would predict that differences in spaceuse predict differenc.es in hippocampal resources,such as receptive females. In thelaboratory, such navigational abilities have been size;i.e., rodentsthat must track unpredictablespatial distributions of critical resources assayedby performanceon mazes,such as the symmetrical maze I I 2]; theradial arm maze shouldhave proportionately larger hippocampi (see chapter by Claytonand Krebs,and [54]' andthe water maze [47]. Superioracquisition of thesetasks have bcen demonstratecl Shettleworth,present volume). 314 3r5

4.I. HIPPOCAMPALSIZE IN FOOD-STORINCRODENTS Thc l'irstqucstion onc rnight ask is whcthcr, likc birds,ftxxl-sloring rodcnts huvc rclativcly q) 0.80 largcrhippocampi than rodcnt spccics that do not storc lood. Howcvcr, bccausc most rodcnt .N food-storersuse only a singlelarder [83], such a "cognitiveniche" would not demand a adaptivcspecializations orcven the use of spatialmemory. Thus spccics using thc colnlnon 6 o- stratcgyof lardcrhoarding should bc prcdictcd to havcless allocation to hippocampusthan E closelyrelated species using a memory-intcnsivcstratcgy such as scattcr-hoarding. (d 0.70 () In collaborationwith WayneSpencer, I testedthis hypothesisby cornparingrelativc o hippocampalvolume in Merriam'skangaroo rats and bannertail kangaroo rats ( D. spectabi- o_ lis).These species are sympatric throughout much of theirrange and although their diets and .+ matingsystems are similar,they differ dramaticallyin their methodof food-storage.As c 0.60 q) discussedearlier, Meriam's kangaroorats store seeds in scatteredlocations and uso spatial .z memoryto relocatethese caches [27] whereasbannertail kangaroo rats return food to one o centralcache, which they defend. Bannertails are larger than Meniam's anddefend small, o productivetenitories from which they harvest seeds, using a scriesof trailswhich emanatc tr 0.50 from a centrallylocated burrow [36,64). Meriam's, in contrast,lbragc over largerarcas anddo not maintaina permanenthome burrow [3]. Together,these differences in behavior suggestthat Merriam's kangaroo rats experience greater selection pressure on theability to Merriam's Ord's Bannertail mapspatial relationships among new food sourcesor to rememberthe precise locations of food caches. kangaroo kangaroo kangaroo We trappedwild adultmale kangaroo rats from thescspccies during thc breeding season r€[ Ert Ert on sitesnear Portal, Arizona: Meriam's, bannertailsand Ord's (D. ordii). Much lessis knownof theecology of Ord'skangaroo rats, despite a widegeographical distribution [64]. Figure 8. Relative hippocampalsize in three speciesof kangaroorats: Merriam's (n = 5 males,4 females), Ord's (n = 4 males)and Bannertail (n = 5 males,4females). Relative range in hippocampalsize was calculated from However,Schroder [69] measuredhome utilization all threePortal species of the ratio ofobservedhippocampal volume to expectedhippocampal volume in a small mammalofequivalent kangaroorat, and found that Ord's home range was intermediate in sizebetween Merriam's brainvolume (formore details see [3 I ]). Box plotsrepresent the 25%,50% and?5% quantiles foreach species; andbannertails. Thus we also measured hippocampal volume in Ord'skangaroo rats, with horizontallines indicate the l07oand 9070 quantiles (adapted from [31]). theprediction that it mightalso be intermediate in size.Finally, although thcse species differ in foragingtactics, they all havethe samemating system. Thus, bannertails are also kangaroorat thanin bannertails.Adding our sampleof Ord's kangaroorats to theanalysis polygynous,and males increase their space use dramatically during the breeding season lent furthersupport to thehypothesis that hippocampal size is relatedto patternsof natural [62].This predicts that in additionto thespecies differences in hippocampalsizc, predictcd spaceuso. Ord's kangaroorats appearedto be intermediateto the other speciesin by homerangc sizc and food-storing bchavior, wc wouldalso scc dif'fcrcnccs in hippocarn- hippocampalsizc (Fig. 8). Howcvcr, bccause we hadno data on femaleOrd's, we limited pal sizebetwccn malcs and fcrnalcs. our statisticalcomparisons to pairwisecomparisons of relativehippocampal size among Hippocampalvolumc was rncasurcd using standard histological tcchniqucs: pcrfusion rnalcs.Therc wcre no significantdill'erences between male Ord's kangaroorats and male with buffercdformalin, scctioning of frozcntissuc and staining for Nisslsuhstancc with banncrtailkangaroo rat in relativehippocampal size, however Ord's kangaroo rats did have crcsylviolct. Hippocampalarcas wcrc thcn digitizedfrom projectedimagcs of scrial significantlysmaller hippocampi than Merriam'', kangaroo rat [31]. scctions,and uscd to calculatc volume of hippocampus.Whole brain volume was estimatcd Theseresults suggest that it is notjust thespatial distribution offood cachespersethat from brainweight to producea measureof relativehippocampal size. Because of species conelateswith hippocampalsize. Scatter-hoarding species do not usuallydefend territo- diffcrencesin brainwcight, a ratioof obscrvedhippocampal size to cxpectedhippocampal ries, but roam more widely and thus havelarger home ranges [83]. Mean home ranges size was calculatcdbased on the relationshipbetween hippocampal volunte and brain (weightedJennrich-Turner areas [35]) for Dipodomys,published in [69] are:Merriam's, volumefrom a largesample of smallmammals [?6]; details of thismethod can be foundin I .79ha; Ord's, l 28ha; and Bannertails, 0. l3 ha.Thus, species ranking by homerange size [31]. Sexdifferences in hippocampalvolume, however, were analyzed using an analysis of roughlycorrelates with speciesranking by relativehippocampal size (Fig. 8). Homerange covariance,as recommendedby [57]. sizeitself is only a roughmeasure of spaceuse; moreprecise measures of spaceuse pattems, As predicted,patterns of naturalspace use conelated with hippocampalsize within and such as the numberof new foragingsites visited in a foragingbout, may yield better betweenspecies. Relative hippocampal volume was significantlygreater in Merriam's conelationswith hippocampalsize [73]. 316 3t'l

A. Merriam'sKangaroo Rat A a 800

E "- 1.975 600 a ^.-] T c ; I g 6 . E $ eoo ; o e E E :1.92s g 2oo .: I ffi 6 ,::"::^:JW @--l Effi-_-l E of n Moadow Pinc E $ r.ezs o FigureI 0. A andB) Sexdifferences in spatialabilities, and C) relativehippocampal size (in proponionto the 5 volumeof the entirebrain) in breedingadult voles. Sarnple sizes were l0 individualsof eachsex in each species. - 1.825 3.10 3.12 3.14 3.16 3.18 4.3.SEASONAL MODULATION OF SEX DIFFERENCES log(brain volume) (r#l In addition,sex differences in patternsofspace use are seasonal. Polygamous meadow voles showmarked seasonal changes in socialsystem and space use [2 ], 44]. Male homeranges B.EBannertailKangaroo Rat in thewinterdecrease to a sizesimilar to thatof nonbreedingmales or females,accompanied cf- andthe fonnation sexand lineage groups E by an increasein socialtolerance ofmixed [44]. Thc.scbchaviclral changes arc corrclatcd with changcsin brainstructurc. Under natural o E conditions,volcs show largc scasonal l'luctuations in cranialvolume and brain wcight [ 13, 6 88, 901.These nreasures reach a maximumduring the summerbreeding season and a > 2.05 (! minimumin winter.The structuralchanges appear to be triggeredby photoperiod,i.e. the E hours.In the laboratory,meadow voles males reared under summer G numberof daylight o ---rnn photoperiod( l4 h daylight)had heavier brains than males reared under winter photoperiod .so c (10 h daylight)t9, 101.Rearing photoperiod had no effecton normalfemales, although o fcrnalcsmasculinizcd with nconataltcstostcronc injcctions also showed this effectof I r.gs proximate 3.31 3.32 3.33 3.34 3.3s 3.36 photopcriodon adult brain size [85]. Photoperiodthus appears to be the cue triggeringchanges in brain mass,and the responscappears to be sexuallydimorphic. log(brain volume) (r#l Suchdrastic changes in spatialand social ecology, accompanied by grosschanges in brain volume,might be expectedto effectchanges in spatiallearning ability. With my collabo- Figure differcnccs 9. Sex in hippocarnpalsizc in kangaroorats. Points rcprcscnt individual rnales (lilled rators,I haveevidcncc that such changcs occur in two speciesof polygamousvoles, the circle)and fernalcs (opcn circle). Sanrplc sizes wcrc 5 males,4fclnalcs for cachspccics (adaptcd irom [3 I ]). rncadowvolc andthc montanc vole (M. nontanus),a speciesthat shows sex differences in naturalspacc use [32,33,341.Thc idea that scx diflerences in spatiallcarning are modulatcd 4.2.SEX DIFFERENCESIN HIPPOCAMPAL SIZE by photopcriodwcrc tcstcdin two ways.First, montanc volcs wcrc raisedon winteror As expected,males havc largcr hippocampi than lemalcs in bothMerriam's kangaroo rat summerphotoperiods and testedon the Morris water maze147), a task which yields andbanncrtails [3 | | (Fig.9).Thcsc pattcrns suggcst that, as in passcrincbirds, hippocarnpal consistcntscx diffcrcnces in laboratory-rcarcdmcadow voles [37], and in wild montane sizcis partially dctclrtt ittcd by thccognitivc dcrnlnds ol'lirraging, and as in volcs,is partially volcs(Jacobs, unpublishcd data). Howcvcr, thc malcadvantagc in spatialnavigation to a determinedby thecognitive demands imposed by themating system. hiddengoal was only presentin animalsreared under the long photoperiod, simulating the Sincemost mammalian spccics are polygynous, like thc kangaroo rats, and are thus summerbreeding season [28]. This has also been shown in deer mice (Peromyscus scxuallydimorphic in thcir uscof spacc,hippocampal size should be dimorphicin nnniculatus):only micereared under long (i.e., summer) day lengths show sex differences mostspecies. Moreover, hippocampal size should be sexually dimorphic in polygy- in spatiallearning, with a maleadvantage. However such differences were absent in mice nous speciesand monomorphicin monogamousspecies. This, in fact, is the case. rearedand tested in short(i.e., winter) day lengths [17]. Polygynousmale meadow voles, trapped as adults during the breedingseason, have Becausethere is noevidence of seasonalchanges in learningunder natural conditions or significantlylarger hippocampi, relative to thesize of thewhole brain, than conspe- in wild voles,my collaboratorsand I also reexaminedexisting data on spatiallearning cific fernalcs.Therc is, in contrast,no scxualdimorphisrn in hippocampalsizc in abilityin wild-caughtmcadow volcs.In this previously published study [22], meadow voles monogamouspine voles [29] (Fig. l0). were capturedduring naturalshort days (early December)and were then housedin the 3lu 3r9 laboratoryunder long day conditions(14 h daylight).Volcs wcrcrhcn tcstcd at rcgular suchvariation in traitexprcssion could bc precisclyadapted to meetsuch challenges. The intcrvalsovcr a pcriodol'scvcral ntonths on a scricsol'scvcn syrnrnctrical rnaz-cs [ | 2 J. S uch next step is to apply the methodsthat havc beenso successfulin the geneticstudy of an exposurcto incrcasedphotopcriod produccs prcdictablc incrcascs in brainand bocly hippocampalstructure (visualization of themossy fiber tract with theTimm's stainand wcightsin thisspccics, and this rcsponsc isrnorc pronouncod in rnalcs[10j. As prcclictcd, quantificationof thevolume of hippocampalcomponents using stereology; see chapter by thesewinter-caught voles showed no sex differcnce initially, however a malesupcriority in Madeiraand Andrade, present volume) to studiesof wild rodents.I havecurrently begun taskacquisition did developaftcr scveral wceks in theartificially lengthcncd photopcriod suchstudies to examinespecies and sex differences in thevolume of themossy fiber tracts 128j. andhippocampal subcomponents. Thusdespitc diffcrcnces in speciesand mcthodology, therc is incrcasingevi

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