Site Attachment and Site Fidelity in Mi$atory Birds:

Experimental Evidencefrom the Field and Analogres

from Neurobiology
E-D. KrrrrnsoN and V. Nor-,txJn.'

I Introduction

In thischapterwe reviewbrieflywhat fieldexperiments haverevealedaboutthe

formationof sitebondsby avianmigrantsand.in sodoing.considerwhetherit is
fruitful to continuethe practiceof attributingsiteattachmenrro an imprinring-
like process.We then refer briefry to recent findings in the neurobiology of
recognitionof objectsand sitesin three areasof investigation:fitial impriniing.
relocationof food by food-cachingbirds.and homingby pigeons.we suggesrthit
analogiesbetweenthesefindings and site recognitionin migratory biids may
indicatenew directionsfor research.Thesesuggestionsare speculativebecausl
currentknowledgeis slim: we hopethe speculations may haveheuristicvalue.

2 Site Attachment end Site Fidelity

2.1 Natlrrd Hbtary of Siu Atuchtncn

understandingof the developmentof siteattachmenrin the migrarorybird is

incompleteandderivesprimarilyfrom bandingstudies.supplemented by limited
experimentalwork(seeBaker1978forsummary:sokolov1976.1992.19g4.19g6.
I988).Newly independentbirdsare thoughtto disperselocally.to exploretheir
surroundings..and perhapsto selectpotentialbreedingsiresfor the following
spring.The distancedispersedprior ro this choice.regardlessof wherherthi
choiceis made in the bird's finr aurumnor in spring.is thoughtby many (e.g..
Shields1982:Greenwood1987)to be dererminedby naturalieleciionso thaiir
balancesthe disadvantages of matingwith closerelativesand the advantages of
matins with individuals whosegeneticmakeup has been molded by similar
selectivepressures.
In general.the distanceis greaterfor femalebirdJ than for
males(e.9..Gauthreaux1978:Greenwoodl9E0).
The individual then makesis first autumn migration.sertlesin a suitable
wintersite.becomesfamiliar with is surroundings. and.in many species. forms
a bondrhatwill causeit ro rerurnin succeedingwinters(e.g..Ralphand Mewaldt
1975:Kettersonand Nolan t982: Terrill. this vol.). From this rime on rhe

'Depanmcntof Biologv.Jordan
Hall. Indianauniversity.Bloomingron.lndiana4740s.usA

E. Gwinncr(Ed.) Bird Migration

C Springer-VcrlasBcrlin Hcidelbcrg1990
I lt E.D. Kctrcrsonand V ' Nolan Jr'

migrations of site-faithful individuals are betweenknown breeding and non-

breedingareas.Additionally.in somespeciesindividualsarecaughtat the same
stopoverlocationsin successive migrations.indicatingfamiliaritywith migratory
pathwaysand fidelity to sitesalongthe way (Nolan and Ketterson-in prepara-
tion). The detailsof the developmentof bondsto seasonally occupiedlocations
surely vary widely among migratory species. just aslife historytraitsand ecology
vary widely.

2.2 Terminologt

We usethe termsiteattachmentfor the Processesleadingto formationof a bird's

preferencefor a location.TheseProcesses.which involvelearningand memory
(e.g..Lohrl 1959:Serventy1967:Wiltschkoand Wiltschko l97E: Berndt and
Winkel 1979).resultin the tendencyto confineactivitiesto a restrictedlocation.
andtheyoccurinbothsedenlaryand migratoryspecies.ltseems useful.therefore.
to use a separateterm for the expressionof the preferenceby the free-living
migrant.andwe definesitefidelityastheactofa migrantin returningtoa location
occupiedin an earlierseasonor year.

2.3 Comporcnt of SiteAttaclnentlSite FifuEty

Sitefidelityimpliesnot only thatthemigranthaslearnedtheattributesof thesite:

it alsorequiresthe motivationand the ability to return.includingthe abilitiesto
orientand to recognize thesiteuponarrival.Theseabilitiesmayexistin sedentary
species aswell (Wiltschkoand WiltschkoI 978:Nolanet al. 1986).but rarelyhave
causefor expression. In anycase.in migrans.recognitionof thesiteto whichthere
is a bond apparentlyinteractswith the migratoryphysiological stateand leadsto
the terminationof that state(Kettersonand Nolan 1987a).
While theorientationalcomponenthasreceivedmuchproductiveattention.
almostnothing is known of the recognitionstage.i.e..what the relevantlearned
attributesof the sitemay be or how PercePtionof them influencesphysiology.
Some have proposedthat animalsdevelopan integrativecognitivemap and
possessthe capacityto comparecurrenl environmentalinput to that internal
iepresentation-(O'Keefe and Nadel 1978:Bingman 1990).In that view.recog-
nition of the site upon arrival theremight consistof matchingthe perceptionof
spatial distributionof the landmarkswith the memorizedcognitivemap. Al'
ternatively.the animal might simply respondto one or two key stimuli as
indicatorsof home. What the landmarksor stimuli might be is not known.
althoughthey are often tacitly assumedto be visualand thereare someexPer'
imentaldata to supportlhat view (Schmidt-Koenigand Walcott 1978).
 I 19
Sire Attactmcar end Sitc Fidelity ia Migntory Birds

2.1 Fie&aad l^onoaory Expabturt hnati1a/.ary Siu Anadna

ondSiE FidebY
of site
we are aware of two experimental approachesto the investigation
which we term staged release. is to
atuchment and thus site noetty. The first.
displacebirdsatdifferentstagesofdevelopment(ages)and.determinethe
#il;;rween theirageorlxperiencet"hendisplaced".ng9::i. towhich
ii"y ,"*-. .ither in theyea-rof displacem.eil or later(e.g..Lohrl 1959:Ralphand
Me'waldt1975.1976:Binvenuti and Ioale 1980: Sokolovl98zl)'This approach
hasso far contributed little to identifying the cues necessaryfor recognitionbut
il;; L""; quite usefulfor identifying-thJtime or age at which attachmenttakes
place.
t'--ifr.
secondmethodis to exposebirds to a locationthat wastheir destination
their current
in a previous migration and toobsewe how this exPosure"qtT
1978:
season,smigratory state (stimmelmayr 1932: Gwinner and czeschlik
KertersonandNolan 19E3.198?a.b. t9d8:NolanandKetterson.inpress)'Ifbirds
released or held at their migratory destination fail to migratewhen it istime to do
that they
so. or to fatten and sho*Zugunruhe. this can be taken as evidence
birds-. might ultimately
i".og"ir.A the site.This apprJach.undertakenon caged
only one
prouZ "..nable to "u. rnunipulatioll' As yet' however'Y.t kno* of
the cuEs available
l,t..pt (Gwinner and Czeschlikl9?8) to altersystematically
and we are
durini the phasein which migrans learn a site(acquisitionstage).
stage.-The.results of the lone
aruare"ofno manipulationsduing the recognition
bCcaused caged birds cannot learnthe
experimentwerenegative.quite iossibly
recognition (L6hrl 1959: Berndt and
.uL, ,r.""rr"ry for iit. "tt""h.int and
Winkel 1979:Sokolov1984:Nolan and Ketterson' in press)'
A seriesofexperimens in which.prior toautumn.weexposedbothcagedand
free-living (released) dark-eyedjuntos-(Junco hyemalis\to their autumn mi-
go,ory d-estination has been rwiewed by us (Keuersonand Nolan l9EE)'
on indigo
ih.r"ior.. we pres€nthere only the resuls of a more recent study
buntings(passirinac.yanea\. Sniegowskiet al. (1988)and Sniegowski(unpub-
them until
lished iata) caught male buntings-ontheir breedingterritgrie.s.held
at a date when
ihe following rpi-ing.and then rJleasedthem on their territories
wintering far to.th.e
,oigi"tion *ir jort Seginningamongfree-living conspecifics
km to the south' If the birds
south. Controlswer. ir"nrpitt"d arid releaseaIOOO
if recognition is sufficieht to
releasedon territory recognized the site. and
rerminate migration. the eiperimentals would be expected to delete migration
h-oqe'
from that ye#s cycle.wherias the controlswould be expectedto migrate
did not remain thcre. then it mighr be
iittr" Uutttings rlleased on territory
recognize the site or that recognition could not
concludedeither that they did not
overridethe seasonalphysiologyof migration.The resuls (Table I ) areequiv,ocal
(cf' the
but suggestive.Someof thebuiiings releasedon their territoriesremained
bluethroat.
similarresultin an earlyexperimentby Stimmelmayrl932.withone
"ni on. chiffchaff. Ph.ylloscopus collybita\. Furthermore.
Erithacus sveccica.
treatment
somereleasedto thesouthreturned.However.mostindividualsin both
lm ED' Kcncrroo eod V' Nolan Jr'

Tebb t. Bchavior of indigo buatiags rchascd Prior ro ilililtiol of nigratioa'

at and esay fron thcir nitntotl dcsrinarionf

Relcasc Nurnbcr Rcrnaincd Migratcd Una"'counrcd

sitc relcascd at home horne for

Homc-lndiana 20 7 t3
Awav-Florida 20 t r2
. combined darafor t9t5. 19t6.from snicgowskiet al. ( 1988)and unpublishcd
dao by Snicgowski.

groupswere unaccountedfor. and it is possiblethat thosereleasedon territory

may- have migratednorthward.
We concludefrom rcsultsof the sccondexperimentalapproach thaUwhen
migrantsareexposcdto thcir peremial migratorydestinationat-thebeginningof
thi migration season.at least somc individuals recosnize the site and this
recognitionoverridcsmigration.However.further progressprobablywill require
a sys-temthat can be brought under laboratory control. although we havejust
aclinowledgedthe difficulty of controlling in the laboratory a phenomenon
expectedonty in free-livingbirds[but seethe laboratorysrudiesof Gliick ( l9t4)
and Robertsand Wiegl (1984)on habitat preferenceand of Hess (1973)on
environmentalimprintingl.

3 Tining of Site Attrchment rnd ttc lnFrnting Mod€l

Site atUchmentappearsin cerrainways to be analogousto imprinting. and

imprintingis sometimcsinvokedin accountingfor sile attachment-(L0hrl1959:
Sauer196?:Serventyt967: Ralphand Mcwaldt 1975:Berndtand Winkel 1979:
Sokolovl9t4). Imprinting is usuallydescribed(e.g..Bateson1979)as a special
kind of learningin whicli (l) rhe information that is acquiredrestrictsfuture
preferenceanOi2) acquisitionoccursrapidly during a crirical or sensitiveperiod
or phase.Somedefinitionsrequirethat the learningbe accomPlishedwithout
rcinforcementand that the preferencebe irreversibleor be retained'fora long
time without interveningPractice.
Mosrresearch on siteattachmentthat hasdrawn inspirationfrom imprinting
models has focusedon the timing of attachment.with at least an implicit
expectarionoffindinga scnsitivcperiod.Existenceofsucha period istraditionally
demonstratedwith data graphcdasan inverted U- or V-shapedcurve (Fig. I A)-
SubjecSare exposedto a stimulus over a range of times and later tested to
detirmine whethqrthey establishcda prefercncefor the stimulus. If exposureis
before or after the sensitiveperiod. no preferenceis exhibited. Only exPosure
duringthesensitiveperiodesrablishes whichis graphedasthepcak
a preference.
ofthe curve.
Sitc Attachmcot and Sirc Fidclity iD Migratory Birds
12r

A
Hirh
E
z=
3
E=
b(,
(rF
L al,
uJ
EF
Hc
<o
J L

Ea'V Ldr
DEVELOPMETTAL STAGEAT
INTTIALDGOSURE

c
o o
Fut
Ful
2a
>u)
l-s gs
F F
ixA
c5 E5
a It

Eafi l5!a EaiV Late H

OA1EOF OISPIJCEMEiTT DATEOF CAFTURE
AND REI.EASE ANO COI{FINEHENT

Fb. fA.D. Expcctcd resultsof stagcd-relcasc expcrimcntsundcr various hypothesesand exper'

im-cnUl designsto invcstigate timhg of lcaming. A Classicalevidenccfor a scnsitivcphasc in
imprinting. i Expccrcd re-sultsin aiuged-rclcasc cxpcrimcnt such as L6hrl's. So/rd tne shows
dashed/ine rhc rcsul[ nccess:rryto dcmonstratc a scnsitive phasc.C Expcctcd
obscrvabli rcsr,tl.u,..
rcturnslo capturesitcwhcn displacemcntsarc al variousdatcsandsubjcctsarcrclcascdimmcdiately'
it
ln left-hand'cune.a bricf imprintingJikc Processoccurscarly in fic scason:-inright-handcune
lt ientral cune. lcarning is by a gradual.individually varying proccss or
occun latc in the scason.
whoscdatJ varicsamong individuals.Sectext. D Expcocd
f*iUfy by an imprinting-likc proccss
L,urnJroLppre sirc iria sugeddclaycd-rcleasc experiment.Capturesarc.at variousdatcs.and
at thc
subjcctsarc displaced and hild unrif hte in the scason.then rclcascd simultancously
disilaccmcnt site.Left-hond risint curveshon'srelurns to thc capturc sitc if a bricf imprinting-likc,
sitc ifa brief
pro.a$ o""ur, .arly in the scasoniEouom hori:ontolcutte sho'ttsrclurns to thc caPlurc
rcturns lo thc
imprindng-like Proccssoccurslarc in thc scason.Thc right'hond risinSt'.tn:.tl:*:
.ri,ut. ril if lcarning is gradualand datc of its complction varicsamong individuals

3.1 Atuchtttcnt to ttu Natal Siu

In field experimentsto determinethe timing of attachmentto the naral site.

individualbirdsare releasedat variousagesand their latertendenc,v to returnis
monirored.The problem with this however.
method. is that the expected resultis
notan inveftedU. The reasonisthatbirdsreleased priorto the startofthe putative
sensiriveperiodwill. if theydo notdisperse.still bepresentat thebeginningof the
sensitiveperiod and therifore shouldteturn at the samerate as birds released
when the period begins.Only individualsreleasedafter the sensitiveperiod is
 ED. Kenc'rroo ead V. Noho lr.

complete would be expected to form no preference(Fig. lB). Thls. this sort of

cxperiment cannot reveal the existenct of a sensitivepcriod.-althoughit can
producedataconsistentwith the concept.ln a ficld study.to producethc invertcd
U required for a rigorous demonstrationof imprinting. birds would have to be
releaiedat a first siie at a rangeof devclopmentalstages.be recapturedand held
after a period in which they lived free. and finally disPlacedand releasedat a
sccondiite so that thosewith a Prcferenccfor the fint site could be observedto
expressit. This experimentis so difficult that we do not exPectil to be madc.
The cunyein Fig. I B is very similar to a curve of the resuls in the classic
experimentof Lohd al959).whoseyoungcollaredfrycatchen(Ficedula albicollis\
werereleasedat different agcsat a location90 km distant from their rearingsile
(whichwasnotthenatalsite).Individualsreleased priortoorearlyin post-juvenal
molt returned to the displacementsite.whereasthosethat were releasedlate in
molt or after molt was completed(the stageat which autumn migration begins)
did not return(Fig.2). Thc few similarstudiessinceL$hrl's(e.9..Serventy1967:
Berndtand Winkit l9?9) havcconfirmedhis finding that attachmenlto the natal
and/or rearingsite involveslearning: birds Uansportedwhen sufficientlyyoung
return to thedisplacementsite.But with thepossibtecxcePtionof Serventy'swork
( 1967).we arc awareof no further demonstrationof the tcrmination of a phasein
which learningoccurs.We thereforesuggestthat thereis little evidenceto justify
the generalconclusionthat natal site attachmentis an imprinting'like process.
ThJdata seemlo point just as consistentlyto a Processof gradual learning.
including explbrationand expansionof a familiar arca (Baker 1978).that
culminatesin attachment.

3.2 Attacluunt to tlu Winur Siu

Investigaton have also consideredwhether an imprinting'like processmay

accounifor attachmentto the wintcring site(Ralph and Mewaldt 1975.1976).ln
thesesuged-releaseexperimentsmarkedbirds are displacedat variousdatesin

o
Fg

2E
3ut
5?
EH G
f,

23 JUNEEJULY 24 JULY 1 ATJGUST 10 ATGUST

DAIE OF RETEASE
F[. 2" Rcturnsof collared f,ycarchershand-rearcdaway from natal sitc. displacedat variousstages
of devclopment.and relcascdat a distanct from rearingsitc (Aftcr Lohrl 1959:cf. Fig. I B)
 Birds 123
Sitc Attachmedt and Sirc Fidclity in Mignory

theirfirstwinterandthcPercentagesreturningnextw.intertgthe.homesiteare
Ideally for sucha study.all birds
analyzedin relation to date of disiplacemenr.
in spring(i'e" would
would remainat tne reteasesiteun'tilmigratingnorthward
irisome unknown place)-and the
neither home to tt,e.aliure sire nor seitle they
winter'ssite.whether
survivorswouldindicateiy theirchoiceof thefollowing Figure
site. IC
the dilplacement
hadbecomeattachedto tttir""piote-homesiteor occurs
thatsite attachment
i.pi"i, ,rr. .xpecredresulrs.first.underthehypothesis
winter(left-handcurve.Benvenuti
rapidlyduringa sens,t;;;iioa .ittte, ."rly in
(right-hand curve. Schwartz1963)and' second'
and loal6 1980)or t"t. ln'*int.r
thatiearning is gradual and varieswith individual
underthealternatef,ypoitresis
(middle tlruel. In all three possiUitities. birds displacedprior to
.-p*i."".
"uptor.-hottte site and thosedisplacedafter
atrachmenrfail to ,"*-* io ttre
we emphasize. however. that the middlecurvein
artachmentreturnto rt "i ,it..
Iflearningis rapid-
Fie. I C couldalsou. g;n.i"rcA by an imprinting-likePtTt::'
;? ;ffi;;;;-dil;s; ,.niitiu. piriod in-eachlndividual.but the dateof
of the populationmight be best
tearningvariesamonjinATuiau"ts.thebehavior
peak in mid-winter: the curve
,.fr.r."n,.o by a noinal distriburion with the
variabie'.This kind of
would look the sameas if learning*ere gradual a-nd
of the populationdifferedin
individualvariation.ouia u. produiedif mimben
the preceding
;;;i.;y.t monthsaccordingto wherherthey harchedduring
brobds.or late broods. Onepoint of
breedingsearon,n ."rty Uroods]mid-season experi-
to distinguish
iig. f6-.it that theseiifferent possibilitiesare difficult
mentally.
.---nn.*p.rimentlikethardepictedin.Fig.lCwascarriedStbyRalphand
sparrows(Zonotrichiaspp')
Mewaldt (1975.197;). *ho transportedcr6wned
The rate of return nextyearby young
variousdistancesfrom their wintei sites.
according to date of displacement:those
,f".ro*, to the capturesite varied
were_less likelyio return. and siteattachmentwas
displacedpnor to ,o,J-J"nuury
believedtohaveoccurredbymid.January.Astheauthonpo intedout.birds
periodbeforerheirreturncan
alpiu."a earlyin wintermustsunive for alonger
in theintervalbetween
be observedn.*, y."i, that is.the probabilityof mortality
would -be positivelycor-
displacementand the following winrer piesumably
relatedwirh the lengthof that interval'
The experimeniJepicted in Fig. lD is a variationon Fig. lC and wasde-
do not necessarily remain
signedro overcomethe factsthat tiansportedbirds
variation in length of the interval
ar rhe releasesite uniii tt ey migrateand that
that can be expectedto re'
L.t*."n releaseand return may affectrhe numbers
birds are captured-over a rangeof
rurn. In this staged-deluy"d-r.i"ut"design.
and released simultaneously at the
dates.displacedto uia n.ra at a seconds-ite.
to migrate. This treatment Prevents
Ji.fio"...nt sire late in winter. in time
whareverthe date
;;;i;g and alsoeliminaresvariablemortaliryafter capture.
Next winrer. return is monitored ar both the caprure site and the
;i;il;";..
occurs rapidly either. early in winter or late in
alpii".r.nt site. If artachment
caPturesiteor the
winrer (Schwartzf SOil."tt returnsshouldbe to one site.the
oirft"".ln.nt_releasesite.respectively..lf learningoccursgradually.the percent-
amongindividuals
"gJ"rbirds returningto the capturesiteshouldbe grearest
 121 ED. Kctrcrroa ud V. Notaa Jr.

captured latest. and some individuals might bc expccted to return to thc

displacement-releasc site.
Resuls of such an cxperiment appear in Fig. 3 (Nolan and Kettcrson. in
press).Dark-eyedjuncos caught throughourDecimber and Januarywere dis,
placed to an outdoor aviary surroundedby suitablejunco habirat: they were
releasedtherein latewinter. Intensiveeffortsin the following autumn and winter.
both at'the original capturesiteand at the aviary releasesite.yielded few returns
of birdscaughtat any date.but thereweretwo nobble resuls. First.juncoscaught
late in winter tendedto return at a greaterrate than thosecaught carlier. when
the data are analyzedwith the capturepcriod divided into thirds. chi square :
4.72.df = 2. 0.10>p> 0.05.Second.a few individualscaughtduring all thirds
returnedtothedisplacementsite. indicatingthatthctimingofsiteattachmentwas
highly variable.Thus. whereasan individual caughr as early as 12 December
exhibited fidelity to thecapruresite.anothcrcaughtaslateas24Januaryreturned
to the displac€ment-release site.(A youngjunco not included in this experimenr
was capturedon 5 Fcbruary. displacedto the aviary. and releasedthere on 2l
February: it returnednext winter to thc aviary.)
To summarize.it seemsappropriatcto askwhcther the tradition of usingthe
languageof imprinting to describesireattachmcntshould be continued.To be
sure. information stored during site attachmentcan be retrieved afier a long
interval of no practice.but it seemsto us that the evidencefor a sensitiveperiod
- the mostimportantcriterionfor imprinting: is slim ar best.In orderro srudy
further the questionof the relationshipbetweenimprintingand siteatrachmenr
we need a study systemwith greaterresolvingpower.

sf ToFd6eSit
.lTocetmSitc

r-20 21DG tt€t n |ca.

Dtc lOJan J|'r DO

DATEWITHDRAWN
FROi' NAruRE
F[.3. Rcturnsof youngjtncos in a winterlageddclayed-rclcaseexpcrinenr. Birdswcrc caughtat
various&tes in wintcr. displacedand hcld until late wintcr. thcn rclcascdsimulrancouslvir the
disolaccrnenrsitc (cf. Fig. I D)
Sitc AttachBcDr ead Sitc Fi.tclity in Migraory Birds 125

4 Neunl Besesof Behrvion Somerhrt Anrlogous to Site Fidelity

Recentadvancesin understandingof the neural basesof three kinds of avian

behaviorshouldintereststudentsof sitefidelity: filial imprinting (summarizedin
Horn 1985).food-cabhing(SherV and Vaccarino1989;Krebset al. 1989).and
pigeonhoming (summarizedin Bingmanet al. 1984.1985.1988.1990).Each
Lehavior involves recognition and thus has a component that is at least
superficially analogous to a comPonentof site attachment and site fidelity.
Further. thus far at least.the behaviorshaveproved amenableto study. Space
limitation permitsonly brief referenceto this work and necessarilyrequiresthat
we oversimplify. but we point out that two themes emerge.First. particular
regionsof the brain have cometo be associated with a bird's ability to learn the
atiributes of. and later to recognize.significantplacesor objecS. Second.this
neurally localizedabilily to recognizecan be uncoupled from other abilities.
including the ability to learntasksthat requirethevery behaviors(motorPatterns.-
visual discriminations)ordinarily associatedwith recognition.

4.1 Filial Imprinting

Filial imprinting occurswhen young birds(e.g.Gallus gallus)follow their mother

or someartificial substitute.with thc well-knownresult that an attachmentis
formed to the object followed (this subsectionis drawn from Horn 1985).
Imprintingis demonstrated whenthe chicksubsequently showsapreference for
the followid objectover someother Potential imprinting stimulus. This prefer-
encerequiresthat the chick recognizethe stimuluson which it trained.
During imprinting a neural representationof the imprinting stimulus is
storedin thebrain.andautoradiographyand lesioningimplicatetheintermediate
and medial part of the hyperstrialum venlrale (IMHV) of the forebrainas the
regionin whlch storagetakesplace.When the IMHV is missing.a chickcannot
acquirea preference. Further.whenthisregionis lesionedin chicksthat already
haveacquireda preferencethrough imprinting. under somecircumstances they
can no longerrecognizethe imprintedstimulus-
OneofHorn ana nisassociates'most interestingfindingsis that it is possible
rodissociate (uncouple)recognitionofa stimulusfrom associative learningofthat
samestimulus.Chicks respondto Potentialimprinting stimuli as reinforcers.A
chick placedin a cagewith two foot pedals. only one of which will activate a view
of an imprinting stimulus. will quickly learn to press the pedal that activates the
view if it finds the view rewarding. The capacity to learn this task is unaffected by
lesionsto the IMHV. However. when these same lesioned chicks are compared to
controls intheir preference forthevery stimulus they just worked to see.only the
controls exhibit the preference.In other words. the IMHV is not necessaryto
learninga taskthat permitsa chickto look at a stimulusit findsrewarding.but it
is necesiaryro rhechick'slaterability to recognizethat thing.This dissociability
of recognition from task learning is the kind of observation that is leading
neurobiologists to invoketheexistence of multiplememorysystems (Sherryand
Schacter1987).
IN ED. Kcnc|soD rad V. Nolea Jr.

a.2 Uierg

In the last decadcmany studieshave documentedthe memory capabiliticsof

food-cachingbirds.someof which can retrievetheir cachesafter severalmonths
(e.g..Kamil and Balda t9E5: Balda ct al. 1987).Two recentinvestigationshave
linked thesecapacitiesto a specificregion of the,brain.the avian hippocampus
(HP). In comparisonswithin families.specieswirlr,the greatertendencyto store
and recoverfood havelarger hippocampalrcgions(Sherry et al. 1988:Krebs et
al. l9t9). and investigationof the impact of HP aspirationon cacherecoveryin
chickadees (Pants atricapillus\ shows that suqecs lose their capacity to
remember(recognizevisually) the locationofcachesitesafteraspiration(Sherry
and Vaccarino igES).Thesechickadeesarc stiU motivated to searchand they
rctain all the motor and visual discriminatoryabilitics to do so after aspiration.
bur theyapparentlylack theabilityto recallthc spatialrelationshipbetweenfired
feedingsites.
Whetherthescfindingswill provc relevantto siteattachmentis problematic.
On thc one hand. the Usk facing a bird anemPtingto recoverstoredfood might
bc secnas involving comPonentssimilar to thosein the Usk confronting a bird
about to migrate toa previouslylcarned site: motivation to return. orientation.
and recognitionofthesiteupon anival. On theotherhand.atleast twodiffcrences
bctwecn food retrieval and site fidcliry suggestunderlying differencesin thc
neuralprocessesinvolved.In usingfood-storingmemory.the bird makesonlyone
visit to ihe cacheand may learn only a singlccueby which to recognizeit. whereas
site attachment is almost surcly not based on one brief cpisode and. corre'
spondingly.the memory is probably a compositeof cueslearnedduring various
experiences.Further. for cfficient food rctrieval cache sites must either be
foigottcn oncea secdhasbeenretrievcdor. if memorycontinues.lhecachcmust
be ivoided unlessor until it is usedagain(Sherryand Schacter1987).Sitefidelity
"programmcd forgetting."
rs unlikely to involve such

1.3 Orbnaiott ottd Hottrittg

Resuls of studiesby Bingmam and associates (19&4summarizedin Bingmanet

al. 1990) are consistentwith thc view that thc avian hippocampus plays a
necessaryrolc in spatialrecognition by homing pigeons(Columbalfvea).Whcn
HP-ablaiedpigeonsarc released50 km from home.thcir ability to orient aswell
ascontrob d;pends upon the modc of orientationthat they usc.and they exhibit
rnarkedly reduced ability to rtach home. When they havc previously been
familiar with landmarks at the relcasc site and arc forced to rely on visual
recognitionasthcir homing mcchanism.homing is muchimpaired. Furthermore.
whcn releascdnearerhomc. they evidcntly fail to rccognizcthcir homeloft when
in iS vicinity. Aftcr postopcrativc retraining. however. many of the normal
orientational and recognitionabilities are restored.
Accordingto Bingman(personalcommunication).a speculativcapplication
of theseresulGto a migratory. potentially site-faithful bird would be asfollows:
 127
Sirc Anschncatand Site Fidelity in Mignrory Birds

An individual that wascaughtin winter. subjectedto hippocampalablation.and

releasedwould havethe opportunity to relearnits winter siteafter releasebut not
to relearn iS breedingsiti.if it migiated and succeededin reachingits breeding
site (and the pigeonrisults suggesithat it might succeed).it probably would not
recognizettresite and somighi not Passout of the migratory state.However.the
fo[&ing autumn it would b?expeciedto recognizeis winter site.againassuming
that it reachedthat destination:
' i

5 Summary end Further SPeculation

There seemslittle reasonto expecta priori that the relevant characteristicsof a

breedingor winter sitewould be storedfor the long term in the samelocationin
the braii asthe quickly learnedrePresentationof a followed object' Rather'it is
intuitively more-app€;fing to describethe process_ofrecognizinghome after
migration as one oimatctring curent environmentalinput to a storedcognitive
."'p. rn. implication of th1 hippocampusin recalling or recognizing food
locationsisprovocative.but we havepointedout apparentdissimilaritiesbetween
what is involved in the processof rememberingthe locationsof a food cacheand
a homerange.Further.iheindicationthatthehippocampusisnot-necessarytothe
reacquisitidn of many sPatial abilities in pigeons considerably obscuresthe
impo'rtanceof that structure.Whateverthe relevanceof theseneural studiesfor
sltendeUty.it seemsclearthat we needto find a tractablestudysysremthat will
permit usio dismantlethe neuraland behavioralcomponents-of this fascinating
animai ability. preferablyfirst in the laboratoryand then in the field.

Acknowledgmenls. For Lind assistanccin the prcpararionof thc manurript we thank S'B' Robbins
V.P'
and L. Wo]f. For gencrouslysharing thcir wbrk prior to publication wc thank D.F. Shcrry.
Bingman.and l.D.-Sniegowsti.Forsiimularingdiscussionand hclpfulsuggestionss'cthankG. Ball.
W. iirnberlakc.n. Kamit. R. Wiltschkoand R. Suthcn. nspccBofourown rescarchrcportcdhcrcin
werc supponcd by NSF DEB-il-t0457 and 8NS-E3-15348and by Indiana Univcrsity'sOfficeof
Rcsearchand Graduatc Devclopment.

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