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ANIMAL BEHAVIOUR, 2008, 76, 1305e1317doi:10.1016/j.anbehav.2008.06.015

The use of self-motion cues and landmarks by Clark’s nutcrackers

(Nucifraga columbiana) during a small-scale search task

BRETT GIBSON & TYLER WILKS

University of New Hampshire, Durham

(Received 15 January 2008; initial acceptance 20 February 2008;

final acceptance 2 June 2008; published online 8 August 2008; MS. number: A08-00026)

Past research has indicated that the Clark’s nutcracker encodes information about landmarks into memoryto return to a hidden goal during small-scale navigation tasks. However, the ability to navigate using self-motion cues has been largely unexplored in avian species, including the nutcracker. In the current study,we trained four birds to move from a position near the perimeter of a 12-sided arena into a square enclo-sure where a hidden goal was located. Both self-motion cues and landmarks were available to locate thegoal during training. The nutcrackers were able to locate the goal accurately using only self-motion cueswhen landmarks near the goal were removed during testing in Experiment 1. However, the results fromExperiment 2 indicated that nutcrackers weighed local landmarks more heavily than self-motion cueswhen both sets of cues were placed in conflict.

� 2008 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Keywords: Clark’s nutcracker; dead reckoning; frame of refe

CorrespoHampshbgibson@

0003e3

rence; landmark; memory; navigation; Nucifraga columbiana;self-motion

Many animals need to navigate in their environmentaccurately to locate a home, return to hidden food, or findother resources for survival. Animals use frames of refer-ence, coordinate systems based on one or more cues (forreviews see Gallistel 1990; Gallistel & Cramer 1996;Golledge 1999; Kelly & Gibson 2007; Shettleworth1998), to help establish their position in the world duringnavigation. Animals use a frame of reference to self-orientin an environment and discriminate the spatial relation-ship between two or more locations (e.g. Cheng 1986;Biegler & Morris 1996; Wiltschko & Wiltschko 1998; Boles& Lohman 2003). There are several sources of information(cues) that an animal can use to establish a frame of refer-ence for navigation.

A body-centred frame of reference is generated by self-motion cues, via a mechanism of navigation known asdead reckoning or path integration (Wehner & Srinivasan1981; Mittelstaedt & Mittelstaedt 1982; von Saint Paul1982; Etienne et al. 1986, 1992; Loomis et al. 1993; Segui-not et al. 1993, 1998; Alyan & Jander 1994; Benhamou1997; Collett et al. 1999; Biegler 2000). An animal

ndence: B. Gibson, Psychology Department, University of Newire, 10 Conant Hall, Durham, NH 03867, U.S.A. (email:cisunix.unh.edu).

1305472/08/$34.00/0 � 2008 The Association for the Stu

determines its position and the positions of other objectsin the environment (see Gallistel 1990; Gallistel & Cramer1996) when dead-reckoning by integrating the distanceand angle travelled during a journey. Distance and direc-tion information may be obtained from a variety of sour-ces, including proprioceptive cues, vestibular cues, opticflow and solar and magnetic cues, that help indicate theanimal’s movements (see Shettleworth 1998).

In a well-cited example of dead reckoning, Mittelstaedt& Mittelstaedt (1982) placed a female gerbil and her litterin a nest on the perimeter of a round arena. The experi-menters then placed a pup from the litter in a cup in anunpredictable location in the area. The mother then wasallowed to depart the nest and search for the pup. Mittel-staedt & Mittelstaedt conducted the tests in the dark sothat the gerbils could not use visual cues during thesearch. The gerbil set a heading that typically returnedher directly to the nest after finding the pup, even whenthe outward journey had been indirect. Mittelstaedt &Mittelstaedt rotated the cup while the gerbil was retrievingthe pup during some test conditions. When the experi-menters rotated the cup slowly, the gerbil returned toa point on the perimeter of the arena that was propor-tional to the amount of rotation. When the experimentersrotated the cup quickly, the gerbil could detect thechange, compensate for the rotation and return to the

dy of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

ANIMAL BEHAVIOUR, 76, 41306

starting point of her journey (the nest). Thus, the gerbil’smovements provided a frame of reference that indicatedher position and the position of important objects relativeto her starting location.

Few researchers have examined the use of self-motioncues during navigation by birds. Wiltschko & Wiltschko(1998) report that young pigeons may use self-motioninformation (referred to as ‘‘route reversal’’) when initiallylearning about their environment. After the third monthof development, however, the use of self-motion cuesdiminishes as the pigeons rely more upon local land-marks, celestial cues, and magnetic information to estab-lish a geometric framework (see below) for navigation.Other work has indicated that adult birds can use deadreckoning. von Saint Paul (1982) transported adult geese1 km in an open cart along a winding path and releasedthem. The birds tended to depart in a direction that wouldhave returned them to their starting position. One limita-tion of a frame of reference based on self-motion cues isthat errors in the estimation of position may accumulatewhen the animal estimates the distance and angle trav-elled (Etienne et al. 1988; Muller & Wehner 1988; Loomiset al. 1993; Merkle et al. 2006). In these cases it may beuseful to use familiar objects in an environment to estab-lish or correct position.

An earth-centred frame of reference is established byusing objects (e.g. landmarks) or cues aligned with theearth to determine one’s heading and location. Landmarkscan also be used to establish a vector, including thedistance and direction, between one or more landmarksand a goal. Numerous studies have indicated that animalsare able to encode both the distance and the directionbetween one or more landmarks and a goal (for reviewssee Gallistel 1990; Redish & Touretzky 1997; Healy 1998;Shettleworth 1998; Golledge 1999). For example, Spetchet al. (1997) trained people and pigeons to search for a hid-den goal that was positioned in the centre of an array offour identical landmarks. The distance between theobjects was doubled during a probe test. The pigeonstended to search in the same distance and direction inwhich the goal had been during training and appliedthe vector to one of the four landmarks, while generallyignoring the others. People, in contrast, tended to con-tinue to search in the centre of the expanded array, indi-cating that they had encoded the location as being inthe ‘middle’. This report and others (Cheng 1988, 1989,1994; Gould-Beierle & Kamil 1998; Kamil & Jones 2000;Kamil & Cheng 2001; Cheng et al. 2006) indicate that an-imals can encode vectors, the perceived distance anddirection between one or more objects, to determine theposition of a goal.

Frames of reference established by both self-motion cuesand landmarks may work together to provide an animalwith a flexible system of determining direction andencoding positions in space (Gallistel 1990; Etienne1992; McNaughton et al. 1996; Etienne & Jeffery 2004).Information supplied by dead reckoning may combinewith references to landmarks to create a representationof an environment. In this view, dead reckoning providesa metric coordinate system onto which relevant land-marks can be encoded. Dead reckoning may then be

used to update and keep track of position with respect tothe frame. One animal that may rely heavily upon bothself-motion cues and landmarks is the Clark’s nutcracker.

The Clark’s nutcracker collects up to 30,000 pine seedsand buries them in the ground in thousands of hiddencaches in its environment during a 3-week period in theautumn (see Balda & Kamil 1998 for a review). The nut-cracker makes its caches up to 22 km from the collectionsite and several seeds are generally placed in a single cache(Balda 1987). Nutcrackers rely upon the accurate recoveryof pine seeds from their caches to survive the harsh winterconditions of their alpine environment and also as an en-ergy resource for reproduction in the spring (VanderWall& Balda 1981). A large body of work has shown thatnutcrackers rely upon their spatial memory to return tohidden caches (e.g. Kamil & Balda 1985; Balda & Kamil1992). Several studies have indicated that nutcrackersuse landmarks to establish a frame for returning to hiddengoals (VanderWall 1982; Kamil & Jones 1997, 2000;Gould-Beierle & Kamil 1998; see Kamil & Cheng 2001for a review). Whereas much work has investigated hownutcrackers use landmarks to return to a hidden goal (Ka-mil & Cheng 2001), to our knowledge no study has exam-ined whether nutcrackers are able to use self-motion foraccurate navigation.

Examining the use of self-motion cues in nutcrackers isimportant for several reasons. Dead reckoning has primar-ily been investigated in arthropods and mammals, asreviewed above. Our knowledge of the use of self-motioncues in reptiles, including avian species, is extremelylimited. It remains to be seen whether dead reckoning isa conserved trait or has evolved independently severaltimes. Thus, examining how birds may use self-motioncues is an important start in filling in this knowledge gap.Likewise, given that the use of self-motion cues may beubiquitous across various groups, understanding howdifferent animals use self-motion cues may provide thebasis for understanding how different brains solve a similarproblem. Finally, investigating whether nutcrackers caneffectively use self-motion cues is important, becausethese cues may combine with landmark information toprovide a rich and flexible frame of reference for accu-rately returning to thousands of cache sites during thecourse of a winter. Therefore, in the current study, weinvestigated the extent to which nutcrackers use self-motion cues to locate a goal.

EXPERIMENT 1

We used a procedure similar to that developed by Etienneet al. (1998) to investigate the use of self-motion cues bynutcrackers. We released the nutcrackers into a uniform12-sided arena and trained them to return to food thatwas hidden in one of four quadrants inside a square enclo-sure in the centre of the arena. The square enclosure hadfour guillotine doors, one on each side. We positionedthree unique landmarks inside the enclosure. Duringtraining, we opened either the door of the enclosurethat was in front of the start position (0�) or the doorthat was 180� from the start position. The corner of the

Startbox

Startposition

Tube

N

GIBSON & TYLER: USE OF SELF-MOTION INFORMATION BY NUTCRACKERS 1307

enclosure in which the food was placed remained fixedrelative to the three landmarks inside of the enclosureand the bird’s start location in the arena. Therefore, duringtraining, a bird could use self-motion cues, landmarks orboth types of cues to learn the location of the hiddenfood. We administered test trials in which the landmarkswere removed to see if the birds were capable of usingself-motion cues to return to the location where thefood was during training.

Method

x

270º 90º

0º

180º

Figure 1. An overhead view of the 12-sided arena, start box withconnecting tube and square enclosure. The start box was attached

to one of the tubes that allowed entry into the interior of the 12-

sided arena (see text). The point at which the bird entered intothe apparatus is defined as the start position. Different sides of the

arena were used as the start location across trials (see text). The other

start tubes are not shown. The square enclosure with the three

unique landmarks was centred in the interior of the apparatus. Thefour guillotine doors of the enclosure (hashed boxes) are labelled

0�, 90�, 180� and 270�. The door located 180� from the start loca-

tion is open in this example. The goal location (X) was always in

the same position relative to the start location.

AnimalsWe used four wild-caught Clark’s nutcrackers in this

study. We housed the birds individually in54 � 54 � 90 cm cages and maintained them on a naturallight/dark cycle. All of the birds had previous experienceusing landmarks to locate hidden food buried in cellulosesubstrate. We fed the nutcrackers a mixed diet of pinenuts, peanuts, sunflower seeds, turkey starter, parrotpellets and mealworms. The birds had free access to gritand water. We maintained the birds at 88% of their adlibitum weight during the study.

ApparatusWe conducted training and testing in a radially sym-

metrical 12-sided arena that was 1.8 m in diameter and1.8 m tall (Fig. 1). We positioned the arena in a large rect-angular room in a laboratory. We took special care toensure that each of the 12 interior walls of the arenawas identical, so that an animal inside could not orient in-side the apparatus. We constructed the walls and ceiling ofthe interior of the arena from white melamine andcovered the floor with granular substrate (Bed O’ Cobs,Maumee, Ohio, U.S.A.) to a depth of 6 cm. We couldopen one of two removable walls of the arena to walkinto the interior and set up the experimental trials. Weilluminated the interior of the arena using 12.20-W halo-gen house lights that were mounted to the ceiling andcentred 60 cm from the adjacent wall. We measured theluminance of each wall in the arena using a photometer(LiteMate/SpotMate III Photometer, Photo Research,Burbank, California, U.S.A.) and detected a difference ofno more than 0.1 log units between the walls. We alsomounted 12 square pieces of one-way glass (3 � 3 cm) tothe ceiling 8 cm from each light and hid a wide-anglecamera (Model WV-BP330, Panasonic, New Jersey,U.S.A.) behind one of these one-way mirrors to view thefloor of the arena.

We insulated the walls and ceiling of the arena with 23-cm-thick fibreglass insulation to help reduce uncontrolledauditory cues that might emanate from outside the arena.To this end, we also projected white noise into the roomusing eight symmetrically arranged speakers mounteddirectly above the arena.

TrainingWe started a training trial by transporting a bird from its

home cage to the experimental room in a 30 � 30 � 30 cm

opaque sound-attenuating transport box. We then placedthe transport box on a swivel platform and slowly rotatedthe box for 15 s. We moved the position of the swivel plat-form in the room across trials to disrupt the ability of thebirds to orient with respect to the outside world. After dis-orientation, we attached the transport box to one of fourpossible 10.80-cm-diameter PVC entrance tubes that werepositioned through the north, south, east and west wallsof the arena. We also created eight ‘dummy’ entrancetubes in each of the remaining walls of the apparatus sothat from the interior of the arena each wall appearedvisually identical. We changed the tube that served asthe entrance tube for each trial according to a block ran-domized schedule (thus the absolute position of the startlocation changed from trial to trial). We then allowedthe bird to acclimate for 30 s in the transport box. Next,we turned the lights in the arena on and opened byremote control a guillotine door that blocked the birdfrom entering the tube. The bird then travelled from thetransport box through the tube and into the interior ofthe arena. We then immediately closed the guillotine

ANIMAL BEHAVIOUR, 76, 41308

door between the transport box and the start tube. Werefer herein to the position of the bird after entering theinterior of the arena as the start position (Fig. 1).

We positioned a square enclosure (60 � 60 � 40 cm) inthe centre of the arena (Fig. 1) prior to the start of the trial.We constructed the walls and ceiling of the enclosure fromwhite melamine so that they would also be uniform. Weallowed the nutcracker to enter into the interior of theenclosure through one of four 20 � 30 cm guillotine-styledoors centred on the four walls of the enclosure. Eachdoor of the enclosure was aligned with the north, south,east or west wall of the arena (the potential start tubes).We opened only one of the four doors to provide entranceinto the interior of the apparatus during each trial. Duringtraining, we opened either the door that was directly infront of the starting position (0� condition) or the doorthat was 180� from the starting position (180� condition).We never used the other two doors (90 and 270� from thestarting position) as an entrance during training. The floorof the enclosure was covered with 6 cm of granular sub-strate that was swept level with a broom. We placed a cam-era (Model WV-BP330, Panasonic) in the ceiling of theenclosure for viewing the interior. We positioned four12-V lights evenly around the camera to illuminate theinterior of the enclosure.

We also positioned three visually distinct uprightlandmarks made of 10.80-cm-diameter PVC pipe insidethe square enclosure (Figs 1, 2). One landmark was centredin the square enclosure and the other two landmarks werepositioned in the left and right corners relative to the doorthat was 0� from the starting position. The centre land-mark was bright orange with a black-chequered patternand was 20 cm high. The landmark in the left corner ofthe box (from the point of view of a bird entering the0� door) was white, 30 cm tall, and positioned 40 cmfrom the centre landmark. The landmark in the right

0º

180º

270º60 c

m

90º

QIIIQIV

QII

Goal

QI

Figure 2. An overhead view of the square enclosure that shows the

location of the goal in Quadrant I and the three virtual locations

(small circles in Quadrants IIeIV) of the goal (see text). The three

unique landmarks (large circle in centre and two large circles inQuadrants I and II) are also shown. The four guillotine doors of the

enclosure (hashed boxes) are labelled 0�, 90�, 180� and 270�.

corner of the box was black and 40 cm tall and also posi-tioned 40 cm from the centre landmark. We divided theinterior of the enclosure into four virtual quadrants (seeAnalyses below), one for each of the four corners of theapparatus (Fig. 2). For half of the birds, we buried twopine nuts a few centimetres below the substrate, halfwaybetween the centre and the black landmark (Fig. 2, Quad-rant I); for the other half of the birds, we placed the seedshalfway between the centre landmark and the white land-mark. Note that, although we counterbalanced the posi-tion of the goal across birds, we refer to the goalquadrant as Quadrant I for the remainder of the paper.

We allowed the birds to make up to 30 digs whilesearching for the hidden goal. We ended the trial whena bird found the seeds or had made 30 digs or when 5 minhad passed since the start of the trial. After the conclusionof a trial, we turned off the lights in the arena and turnedon a light in the transport box. We opened the guillotinedoor to the start tube and the bird returned to the startbox. We conducted four trials of training per day.

Although we used different start tubes across trials (thatis, the absolute direction of the start location in the roomchanged), the configuration of the landmarks, the posi-tions of the doors, and the location of the hidden goalremained fixed relative to the starting location. We rotatedthe enclosure between trials to ensure that any unforeseencues inside the enclosure could not be used to determinethe location of the goal.

During the first eight training trials, we opened the doorthat was 0� from the start position and placed two seedson the surface of the substrate at the goal location. Wegradually buried the seeds over the course of the nexteight trials until the seeds were completely hidden 4 cmbelow the surface of the substrate. We continued trainingwith the buried seeds for eight additional trials and mea-sured the birds’ search accuracy by recording the absolutedistance (cm) from the location of the hidden food of thefirst five digs the birds made inside the box. We defineda dig as the bird placing its beak in the substrate. Duringthe next stage of training, we opened the door 180�

from the starting location for two trials and the door0� from the starting location for the other two trials ina daily session. We varied randomly the order in whichthe birds experienced the two open entrances across thefour trials of a session. We continued training until a bird’smean search accuracy for the goal was less than 10 cm foreight consecutive trials. All of the birds reached this crite-rion within eight sessions.

Probe testsFamiliar and novel doors. Each of the four birds partici-

pated in eight test trials. The procedures for the test trialswere similar to the procedures used during the trainingtrials except that we removed the pine seeds and the blackand white landmarks (the orange central landmark insidethe enclosure could not be used to orient). On each day oftesting, we administered one test and three training trialsidentical to those described previously. We randomlydetermined the order of the test and the three trainingtrials with the constraint that the test could not be

GIBSON & TYLER: USE OF SELF-MOTION INFORMATION BY NUTCRACKERS 1309

conducted during the first trial. After each day of testingwe required that the birds complete 2 days of training(eight trials) before the next test. We also required that thebirds maintain an average search accuracy of 10 cm or lessduring these days; otherwise they continued training untilthey met the criterion. We presented the birds with fourfamiliar-door tests: two test trials in which the familiar0� entrance was opened (0� condition) and two trials inwhich the familiar 180� entrance was opened (180� condi-tion). We also presented the birds with four tests in whichthe novel doors were used: two trials in which the novel90� entrance was opened (90� condition) and two trialsin which the novel 270� entrance was opened (270� con-dition). Note that we refer to the last two doors as noveldoors even though the birds encountered each door onfour occasions during Experiment 1. Because the birds in-frequently encountered these doors and because food wasnever used during these tests, we are confident that thesedoors could not be used as landmarks to learn the locationof the goal.

Because the birds repeatedly entered the apparatusthrough either the 0 or the 180� door during training, itis difficult to distinguish whether the birds would haveused either self-motion cues or cues provided by thegeometric relationship between the doors and the loca-tion of the goal during the 0 or 180� test conditions (seeFig. 3, Familiar door conditions). Specifically, the birdsmay have learned a vector (distance and direction)between the opening of the door and the goal duringthe 0� condition and a separate vector between the doorand the goal during the 180� condition. We subsequentlyrefer to these cues as door-to-goal vectors. Figure 3 showstwo such vectors, one each for the 0 and 180� conditions.We administered the tests with the novel doors to

Familiar door conditions

Goal

QIV

QI

QIII

QII

180º

0º

Figure 3. The distribution of the nutcrackers’ pecks during probe testin

pecks made by individual birds during the familiar (0 and 180�) and noupper left, as in Fig. 2, and the remaining three quadrants are labelled c

doors being open in each graphic, but we opened only one door during

a different marker and individual markers indicate a single peck for each b

bird for each test. The dashed arrows indicate door-to-goal vectors (onelearned during training. During testing with the familiar doors these vect

ing. The application of these vectors with respect to the novel doors wo

distinguish between the use of self-motion informationand that from other types of landmark cues like door-to-goal vectors. If the birds were capable of using self-motioncues, then they should search in the same quadrant(Quadrant I) that contained the seeds during training inthe tests with the novel doors (Fig. 3, Novel door condi-tion). If, in contrast, the birds were using familiar-doorcues, then during the tests with the novel doors, theymight be expected to search in a corner of the enclosuredefined by the door-to-goal vector learned during the0 or 180� training condition (Fig. 3, Novel door condi-tions). The use of such vectors would lead the birds tosearch in Quadrants II and IV, respectively.

Control tests. The control tests were similar to the testtrials except that we released the birds from an entranceabove and in the centre of the arena, rather than throughone of the start tubes in the sides of the arena. We placeda bird on a perch in a 30 � 30 � 30 cm sound-attenuatingchamber that was centred above the arena. The bottomfloor of this chamber had a sliding door that allowedentrance into the 12-sided arena below and that couldbe opened remotely. We changed the orientation of thechamber from trial to trial to eliminate potential direc-tional cuing. After we opened the door of the chamber,the bird flew down (1.8 m) to the floor of the arena andentered the square enclosure through one of the openguillotine doors, as during the other training and testtrials.

We presented the birds with two control test trials inwhich we opened the 0� entrance to the enclosure(familiar door), two trials in which we opened the 180�

entrance (familiar door), two trials in which we openedthe 90� entrance (novel door), and two trials in which we

Goal

QIV QIII

QI QII

270º

90º

Novel door conditions

g with the familiar (left) and novel (right) doors. The markers show

vel (90 and 270�) door conditions. Quadrant I (QI) is located in thelockwise from this position. We show both of the familiar and novel

an actual probe test (see text). Each bird’s responses are indicated by

ird. Each graphic shows the distribution of the first five pecks for each

from the 0� door and one from the 180� door) that may have beenors would have led the birds to search in Quadrant I, as during train-

uld have directed the birds to search in Quadrants II and IV.

ANIMAL BEHAVIOUR, 76, 41310

opened the 270� entrance (novel door). We changed theorientation of the box inside the arena across trials asdescribed previously. We dispersed the test trials through-out the training trials as described previously.

During the control tests we reasoned that if the birdswere using potentially uncontrolled cues during trainingto locate the goal (see Discussion), they should be able touse this information during the control tests and search inthe corner that contained the seeds during testing. At theother extreme, if the birds were not oriented, then theyshould search randomly in the four quadrants of theenclosure across tests. Another likely possibility is thatthe birds would use familiar door-to-goal vectors poten-tially learned during training.

AnalysesWe conducted a set of analyses in which we used the

quadrant in which the birds made each of their first fivedigs as a dependent measure. We calculated the pro-portion of total responses in each quadrant during eachtest condition (familiar versus novel door). We then usedFreidman’s tests to compare the proportion of choicesduring each test condition, as well as the proportion ofchoices during each test condition versus the proportionof choices that would be expected by chance. We thenperformed a second identical analysis using the data fromthe control tests. We controlled for a inflation using theBonferroni procedure.

We used search accuracy as a dependent measure fora second analysis. We calculated the distance of the birds’first five digs during each test trial from the Cartesianposition of the goal (Quadrant I). The first five digs appearto reflect most accurately the nutcrackers’ search behav-iour (Gibson & Kamil 2001).We also calculated the dis-tance of these same five digs from the Cartesian positionin which the goal would have appeared to be relative tothe three remaining quadrants (three apparent locationsof the goal; Fig. 2). Each of the four quadrants of the inte-rior of the enclosure would have appeared identical whenthe landmarks were removed. Our expectation was that, ifthe birds were using self-motion cues, search accuracyshould be less when determined relative to the goal quad-rant (Quadrant I) than to the other three quadrants(Quadrants IIeIV). We used the four distance measuresin a repeated-measures multivariate analysis of variance(MANOVA) that used test condition (probe versus con-trol), door condition (familiar versus novel) and the pecksthe birds made as repeated measures.

PredictionsThe nutcrackers should search in the quadrant where

the goal was during training (Quadrant I) during thefamiliar-door probe tests, because both familiar door-to-goal vectors and self-motion cues predict search at thislocation (Fig. 3, Familiar door conditions). If nutcrackerscan use self-motion cues alone, they should continue tosearch in the quadrant where the goal was during training(Quadrant I) when tested with the novel doors (Fig. 3,Novel door conditions). Alternatively, the birds mightuse familiar door-to-goal vectors learned during training

and search in Quadrants II and IV during the tests withthe novel doors (Fig. 3, Novel door conditions).

When self-motion cues are uninformative during thecontrol tests, the birds should rely upon familiar door-to-goal vectors and search in Quadrants I and III during thefamiliar door conditions and Quadrants II and IV duringthe novel door control tests (see Fig. 3). Each of thesequadrants is consistent with the same distance and direc-tion of the goal relative to the 0 or 180� door during train-ing. Another possibility is that the birds will searchrandomly among the four corners during the control tests.

Results

Nutcrackers tended to search in the quadrant wherethey had previously found the goal during the familiar-door (0 and 180�) probe conditions (Fig. 3). The propor-tion of digs in the goal quadrant was high for the famil-iar-door conditions (Fig. 4a) and significantly differentfrom that expected by chance (c2

80 ¼ 40.32, P < 0.0001).It is difficult to distinguish if the nutcrackers were usingself-motion cues, familiar door-to-goal vectors, or somecombination of both cues to locate the goal during the fa-miliar-door tests, because the same cues were availableduring training and testing. Importantly, during the probetests with the novel doors the nutcrackers also searchedprimarily in the quadrant (Quadrant I) where the goalwas located during training (c2

80 ¼ 33.38, P < 0.0001).Thus, the nutcrackers were probably using self-motioncues to locate the goal during the novel-door tests, asfamiliar door-to-goal vectors would have directed themto search in other corners of the apparatus (Fig. 3, Noveldoor conditions).

Whereas the nutcrackers tended to search in the goalquadrant during the probe tests, choices were somewhatmore dispersed between the four quadrants during thetests with the novel doors compared to the tests with thefamiliar doors. The distribution of the birds’ choicesduring the familiar-door conditions was significantlydifferent from that observed during the novel-door con-ditions (c2

80 ¼ 5.00, P ¼ 0.03). Further analysis indicatedthat the distribution of the birds’ choices during the270� condition (0.65 of responses in Quadrant I; datanot shown) was significantly different from that observedduring the 90� condition (0.98 of responses in Quadrant I;data not shown; c2

80 ¼ 8.33, P < 0.002), but that choicesduring the 90� condition did not differ from either ofthe familiar-door (0 and 180�) conditions (all P < 0.05).

We predicted that the nutcrackers might search inquadrants defined by familiar door-to-goal vectors duringthe control tests, because self-motion cues were uninfor-mative about the location of the goal. Specifically, thebirds should have searched in Quadrants I and III duringthe control tests with the familiar doors if using door-to-goal vectors learned during training (Fig. 5). Indeed, theproportion of digs delivered to Quadrants I and III washigh during the familiar door condition (Fig. 4) and signif-icantly different from chance (c2

80 ¼ 34.11, P < 0.0001),indicating the use of door-to-goal vectors. We predictedthat the birds would also use familiar door-to-goal vectors

(a)

(b)

1

0.9

0.8

0.7

0.6

0.5

0.4

0.3

0.2

0.1

0

40

35

30

25

20

15

10

5

0

Prop

orti

on o

f d

igs

Acc

ura

cy (

cm)

Q2 Q3 Q4Q1Quadrant

Probe_familiar

Probe_novel

Control_familiar

Control_novel

Figure 4. (a) The proportion of total pecks delivered to each quad-

rant during the probe and control conditions in Experiment 1

when either the familiar or the novel doors were opened. (b) The

mean accuracy scores calculated relative to each of the four quad-rants for each of the same conditions as in (a).

GIBSON & TYLER: USE OF SELF-MOTION INFORMATION BY NUTCRACKERS 1311

during the control test with the novel doors and this wasthe case. The nutcrackers primarily searched in QuadrantsII and IV using familiar door-to-goal vectors, and the pro-portion of responses in these quadrants was different fromchance (c2

80 ¼ 22.22, P < 0.0001). The distributions ofchoices during the familiar and novel door conditionswere significantly different from each other (c2

80 ¼ 48.33,P < 0.0001).

The analyses that we performed using the MANOVAand accuracy as a dependent measure revealed a similarpattern of results. Within-subject contrasts revealed a sig-nificant interaction between test and door conditionswhen the accuracy scores were calculated from thequadrant where the goal was during training (QuadrantI; F1,3 ¼ 13.85, P ¼ 0.03), but not when the accuracy scoreswere calculated from any of the other three quadrants(Q2: F1,3 ¼ 0.00, P ¼ 0.96; Q3: F1,3 ¼ 6.16, P ¼ 0.09; Q4:F1,3 ¼ 4.77, P ¼ 0.12). We subsequently performed pair-wise comparisons that indicated the birds were moreaccurate (Fig. 4) during the familiar-door conditionwhen accuracy scores were calculated from Quadrant I(X� SE ¼ 9:45� 1:78) than when calculated with respectto the apparent location of the goal in Quadrant II

(29.48 � 2.47), Quadrant III (32.24 � 1.00), or QuadrantIV (26.69 � 1.32; all P < 0.05). We also found a similar pat-tern for the novel door tests (Fig. 4). The birds were moreaccurate when scores were calculated from Quadrant I(X� SE ¼ 10:59� 0:84) than when calculated withrespect to the apparent location of the goal in QuadrantII (24.82 � 1.80), Quadrant III (32.75 � 0.64), or QuadrantIV (23.62 � 2.12; all P < 0.05). Thus, the findings from thenovel door condition strongly indicated that the birdswere using self-motion cues to search in the quadrantwhere they had previously found food during training(Quadrant I).

A different pattern emerged during the control condi-tion (Fig. 4). We conducted pairwise comparisons thatindicated that accuracy was better for Quadrants I(X� SE ¼ 24:05� 0:74) and III (23.71 � 1.07) than forQuadrants II (28.48 � 1.71) and IV (29.51 � 0.50; allP < 0.05). In contrast, during the novel-door tests, accu-racy was better when measured from Quadrants II(X� SE ¼ 23:66� 1:02) and IV (21.99 � 1.28) than whenmeasured from Quadrants I (29.54 � 0.45) and III(27.75 � 0.71; all P > 0.05). Thus, during the control tests,the birds were using door-to-goal vectors learned duringtraining that directed them to search a fixed distanceand direction from the door that was open (Fig. 5). Thebirds searched in different quadrants as the door thatwas opened changed.

The results from the MANOVA failed to indicate aninteraction between test condition and door condition(F3,9 ¼ 3.61, P ¼ 0.37). The main effects of test condition(F3,1 ¼ 109.83, P ¼ 0.07) and door condition (F3,1 ¼ 5.86,P ¼ 0.29) were also not significant.

Discussion

The nutcrackers may have used at least five types of cuesto locate the goal during the training condition. Specifi-cally, they may have learned to use landmarks inside thesquare enclosure to locate the hidden goal. The birds mayalso have learned to use two door-to-goal vectors, onefrom each of the open doors during the 0 and 180�

conditions. That is, the birds may have learned that thegoal was located at a fixed distance and direction from the0� door and the 180� door. It is also possible that the birdsmay have learned two motor routes, one from the startlocation through the 0� door and ending at the goal, theother through the 180� door and ending at the goal.Another possibility is that the birds may have learned toencode the location of the goal using self-motion cuesrelative to their starting position in the arena. In contrastto a motor route, this type of representation would allowthe birds to locate the goal from a number of differententry points into the square enclosure. Finally, the birdsmay have attempted to use a variety of uncontrolled cues(e.g. odour of the pine nuts, auditory cues or magneticcues that were outside of the arena, markings on the walls)to identify the location of the goal.

The birds were able to locate the goal accurately duringthe 0 and 180� test conditions when the same doors thathad been encountered during training were open. The

Familiar door conditions

Goal Goal

QIVQIV

QI

QIII QIII

QII QI QII

180º

0º

270º

90º

Novel door conditions

Figure 5. The distribution of the nutcrackers’ pecks during the control test in Experiment 1 when a familiar (left) or a novel (right) door was

open. The dashed arrows indicate door-to-goal vectors (one from the 0� door and one from the 180� door) that may have been learned duringtraining. During testing with the familiar doors these vectors would have led the birds to search in Quadrants I and III (as in training). Note that

this pattern is somewhat different from that in Fig. 3, because the birds were disoriented and presumably had no way to distinguish between

the doors. The application of the learned door-to-goal vectors with respect to the novel doors would have directed the birds to search in Quad-rants II and IV.

ANIMAL BEHAVIOUR, 76, 41312

nutcrackers were not relying on learned landmark-to-goalvectors to locate the goal during these tests because weremoved the informative landmarks inside the enclosure.Likewise, because we removed the pine nuts and mixedthe bedding between trials, we can be equally confidentthat the birds were not relying upon odour information.However, because the 0 and 180� entrances into thesquare enclosure had been used during training, the birdsmay have, nevertheless, relied upon familiar motor pro-grams, door-to-goal vectors, or self-motion cues to locatethe goal accurately. The tests with the novel doors wereinformative in examining these possibilities.

During the novel-door probe conditions, the birds werejust as accurate in searching for the goal as when thefamiliar doors were used. Likewise, the birds made a largeproportion of their responses in Quadrant I when search-ing for the hidden goal. Both sets of information suggestthat the nutcrackers can effectively use a representationbased on a sense of self-direction to locate a hidden goal.The birds should have primarily searched in Quadrants IIand IV if they had relied upon remembered door-to-goalvectors during the novel door tests. That is, the birdswould have applied one of the two door-to-goal vectorsencoded during the 0 and 180� training conditions duringthe novel-door condition. The birds also appeared toweigh self-motion cues more heavily than familiar door-to-goal vectors, given their tendency to search in Quad-rant I rather than Quadrant II or IV. Note that if thenutcrackers had used familiar door-to-goal vectors, theywould have ignored self-motion cues encoded from theirstart point that indicated conflict between the positions ofthe familiar 0 and 180� doors and the positions of thenovel doors. Finally, it is unlikely that the nutcrackersrelied upon motor programs to locate the goal becausethey were forced to travel a new route during the noveldoor conditions.

Whereas the proportion of responses in Quadrant I wasstatistically indistinguishable during the familiar- andnovel-door conditions, the overall proportion of responsesduring the novel-door condition was different from thatobserved during the familiar-door condition. The differ-ence appears to be due to an increase in search variabilityduring the 270� novel door tests. During the second of thetwo tests, some birds searched in Quadrants II and IV,consistent with the use of door-to-goal vectors that hadbeen encoded during training. The increase in variabilitymay be explained by the fact that the second test with the270� door was the last of the series of probe tests and twoof the birds appeared to have started searching in otherareas (and relied upon different sets of cues) after repeatedunrewarded tests had been administered.

During the control tests, the birds were released fromthe top of the arena and allowed to enter a single doorinto the inside of the square enclosure. Because the startposition was unfamiliar and the square enclosure wasrotated from trial to trial, the birds should not have beenable to distinguish which door was opened (0, 90, 180 or270� condition). Nor could the birds rely upon past self-motion cues to locate the goal because the start positionwas unfamiliar. The nutcrackers may have also attemptedto use auditory or magnetic cues outside the arena tolocate the goal. Because the goal was changing unpredict-ably among one of four absolute locations in the arena itwould have been difficult to use such cues reliably.Nevertheless, we conducted control tests to be confidentthat the nutcrackers were not using uncontrolled cuesinside or outside of the arena to locate the goal during thetests with the novel doors.

The birds searched primarily in Quadrants I and IIduring the control tests with the familiar doors (0 and180� conditions). Such a pattern could indicate the use ofuncontrolled cues or the familiar door-to-goal vector that

0º

270º60 c

m

90º

QIV

QII

Goal

QI

GIBSON & TYLER: USE OF SELF-MOTION INFORMATION BY NUTCRACKERS 1313

had been encoded during training. The birds searched inQuadrants II and IV during the control tests with thenovel doors (90 and 270� conditions), a pattern consistentwith the use of door-to-goal vectors encoded relative tothe 0 and 180� doors during training. Thus, the resultsfrom the control tests indicated that the nutcrackers werenot using uncontrolled sources of information to directtheir search; rather the birds searched in locations basedon familiar door-to-goal vectors when self-motion cueswere unavailable. Moreover, the birds appeared to favourthe door-to-goal vector associated with the 0� door, thedoor/condition the birds had the most experience withduring training.

180º

Figure 6. An overhead view of the square enclosure that shows the

location of the goal and the three virtual locations (small circles in

Quadrants IIeIV) of the goal during Experiment 2. Note that thetwo informative landmarks were rotated 180� from their position

in Experiment 1 (Fig. 2).

EXPERIMENT 2

During training in Experiment 1, both self-motion andlandmark cues were available to direct the search fora hidden goal during training. The results from our testsin Experiment 1 indicated that the birds could use self-motion cues in the absence of landmarks to search fora hidden goal. In Experiment 2, we conducted tests inwhich both the self-motion cues and the landmarks wereavailable, but each gave conflicting information about thelocation of the goal. During these conflict tests, if self-motion cues were controlling navigation, birds would beexpected to search in one corner of the enclosure (Quad-rant I). In contrast, if bird were weighing cues from thelandmarks in the enclosure more heavily, they would beexpected to concentrate their digs in Quadrant III, next tothe upright landmark that had been near the goal duringtraining.

Methods

AnimalsWe examined the same four birds that were tested in

Experiment 1 during Experiment 2.

TrainingAfter Experiment 1, we returned the nutcrackers back to

training. We conducted the training trials in the samemanner as in Experiment 1. We started testing after thebirds met the criterion as indicated in Experiment 1.

TestingWe conducted the test trials in the same way as the

training trials except that we removed the pine seeds androtated the informative landmarks inside the enclosure180� from their normal position during training (Fig. 6).That is, the two informative landmarks (the white andblack landmarks) were on opposite sides of the enclosurerelative to their positions during training. We conductedtwo tests for each of the 0, 90, 180 and 270� conditions,for a total of eight tests. After each day of testing, werequired that the birds complete 2 days (eight trials) oftraining, during which time they were required to main-tain an average search accuracy of less than 10 cm beforeanother test was administered.

AnalysisWe analysed the choice data and accuracy data using

models similar to those described for Experiment 1. Incontrast to Experiment 1, we performed a log transforma-tion on the accuracy data to establish normality. Wereport the untransformed data in the figures for Experi-ment 2 (Figs 7, 8), however.

PredictionsIf the birds use self-motion or familiar door-to-goal cues,

they should search in Quadrant I during the conflict testswith the familiar doors (Fig. 7). In contrast, if the birds usethe landmarks inside the square enclosure, they shouldsearch in Quadrant III. The tests with the novel doorswere again the most informative about how the nut-crackers weigh different types of spatial cues. We designedthese tests to distinguish between the use of the threetypes of cues: self-motion cues, familiar door-to-goal vec-tors, and the landmarks inside the square enclosure(Fig. 7). Specifically, if the birds were using self-motioncues they should search in the same corner in which thegoal had been located during training (Quadrant I,Fig. 7). If the birds were using familiar door-to goal vec-tors, then they should search in Quadrants II and IV(Fig. 7). Finally, if the birds weighed landmarks insidethe square enclosure more heavily than these other twosources of information, then they should search in Quad-rant III (Fig. 5).

Results and Discussion

Two birds searched primarily in Quadrant I during theconflict tests with the familiar doors (Fig. 7). This patternis consistent with the use of either familiar door-to-goalvectors or self-motion cues. One bird appeared to weigh

Familiar door conditions

Goal Goal

QIVQIV

QI

QIII QIII

QII QI QII

180º

0º

270º

90º

Novel door conditions

Figure 7. The distribution of the nutcrackers’ pecks during the familiar- (left) and novel- (right) door conditions during conflict testing in Ex-

periment 2. During the conflict tests with the novel doors, the birds should search in Quadrant I if using self-motion cues, Quadrant III if usingthe landmarks inside the enclosure, and Quadrants II and IV if using learned door-to-goal vectors.

ANIMAL BEHAVIOUR, 76, 41314

the landmarks inside the square enclosure more heavilythan the other cues and searched predominantly in Quad-rant III during the familiar door tests. The fourth birdtended to distribute its choices between Quadrants I and

0.60

0.50

0.40

0.30

0.20

0.10

0

Prop

orti

on o

f d

igs

Acc

ura

cy (

cm)

FamiliarNovel

45

40

35

30

25

20

15

10

5

0Q2 Q3 Q4Q1

Quadrant

(a)

(b)

Figure 8. (a) The proportion of the total pecks delivered to each

quadrant during Experiment 2 when either the familiar or the noveldoors were opened. (b) The mean accuracy scores when calculated

relative to each of the four quadrants for these same conditions.

III, which is consistent with the use of all three types ofcues. The proportion of digs (Fig. 8) made in each quad-rant during the familiar door conditions was significantlydifferent from chance (P < 0.05). Thus, choices were dis-tributed about equally between Quadrants I and III duringthese tests. The search pattern observed during the famil-iar door condition in Experiment 2 was different from thatobserved during Experiment 1, when the birds predomi-nantly searched in Quadrant I (Fig. 3). Thus, for somebirds, the pattern of search appeared to be influenced bythe appearance of the informative landmarks inside theenclosure.

We observed a very different pattern of search duringthe tests with the novel doors. As mentioned above, weused the tests with the novel doors to discriminate whichof the three types of cues the birds may have been using.During these tests, all four nutcrackers searched primarilyin Quadrant III (Fig. 7), which is consistent with the use ofthe landmarks inside the square enclosure. The proportionof digs (Fig. 8) made during the tests with the novel doorswas significantly different from chance (Z80 ¼ 7.23,P ¼ 0.007). In addition, the distributions of choicesmade during the familiar and novel door conditionswere significantly different from each other (Z80 ¼ 35.77,P < 0.0001).

The results from the MANOVA using accuracy asa dependent measure failed to indicate a significant effectof door condition (F2,1 ¼ 1.30, P ¼ 0.53). We subsequentlyperformed an ANOVA in which we measured the distanceof the birds’ pecks from the virtual location of the goal ineach of the four quadrants and used quadrant as a repeatedvariable. We failed to find a main effect of quadrant(F3,9 ¼ 1.13, P ¼ 0.39) in this analysis across the familiar-door conditions. We also performed a second identicalANOVA using the data from the novel-door conditions.We did find a main effect of quadrant (F3,9 ¼ 39.84,P ¼ 0.01) when considering the tests with the novel doors.Follow-up comparisons indicated that the birds were more

GIBSON & TYLER: USE OF SELF-MOTION INFORMATION BY NUTCRACKERS 1315

accurate compared to Quadrant III than any of the otherquadrants (all P < 0.05). Thus, the results from this setof analyses show that the nutcrackers were weighing land-marks inside the enclosure more heavily than other cuesto search for the hidden goal.

Combined, the results from Experiments 1 and 2 in-dicate that the birds relied more heavily upon landmarksinside the enclosure and self-motion information thanupon door-to-goal vectors (which would have directed tothe birds to Quadrant II or IV during the novel-door testsin both experiments). Thus, nutcrackers appeared to relymore heavily upon proximal landmark information thanupon self-motion information, and both of these cuetypes were weighed more heavily than door-to-goalvectors. The findings are discussed in more detail in theGeneral Discussion.

GENERAL DISCUSSION

Many animals appear capable of accurately using land-mark cues to determine their position in an environment(Wehner & Srinivasan 1981; Mittelstaedt & Mittelstaedt1982; von Saint Paul 1982; Etienne 1992; Loomis et al.1993; Seguinot et al. 1993, 1998; Alyan & Jander 1994;Benhamou 1997; Biegler 2000). The use of self-motion in-formation has been relatively less well studied, particu-larly for avian species (e.g. von Saint Paul 1982;Wiltschko & Wiltschko 1998; Sutton & Shettleworth2005). Here we examined the ability of Clark’s nutcrackersto use self-motion cues during a small-scale navigationtask. Much empirical work has investigated how nut-crackers use allocentric information in small-scale searchtasks to return to hidden goals (VanderWall 1982; Kamil& Jones 1997, 2000; Gould-Beierle & Kamil 1998; Gibson& Kamil 2001; see Kamil & Cheng 2001 for a review). Toour knowledge, no study has addressed the extent towhich nutcrackers can use self-motion information duringnavigation (small or large scale).

The results from the current study are consistent withother work indicating that animals can accurately use self-motion frames of reference. In Experiment 1 of thecurrent study, we hid a goal inside a square enclosure ata fixed position relative to the bird’s entry point into thearena. The birds entered the interior of the squareenclosure through a door that was either 0 or 180� fromthe start location during training. The 0 and 180� testconditions were identical to the training conditionsexcept that we removed the seeds during the test condi-tions. During these tests, the birds continued to locate thegoal. However, these tests were unable to distinguish theuse of self-motion cues from a number of allocentric cuessuch as familiar door-to-goal vectors. The 90 and 270�

novel-door conditions were important because wedesigned them to distinguish between the use of self-motion and landmark cues during search. During the testwith the novel doors, the proportion of digs made inQuadrant I, the quadrant defined by the self-motion cues,was not statistically different from that observed duringthe tests with the familiar doors. Likewise, search accuracywas higher when calculated from Quadrant I than when

calculated from any of the other three quadrants for boththe 90 and the 270� novel-door conditions. Thus, nut-crackers were able to establish a frame of reference usingself-motion cues to determine the location of a hiddengoal. The results from the control tests indicated that theperformance during testing in Experiment 1 could not beaccounted for by uncontrolled cues.

Whereas the results from Experiment 1 indicated thatnutcrackers are capable of using self-motion cues to locatea hidden goal, the results from the second experimentsuggest that nutcrackers may weigh landmark informationmore heavily than self-motion information. During con-flict tests, the local landmarks were rotated and indicatedthat the birds should search in one corner of theenclosure, whereas self-motion information indicatedthe birds should search in another corner. The nutcrackerstended to search in the corner specified by the rotatedlandmarks. The results are comparable to past workindicating that animals use a variety of cues duringnavigation, but may organize the use of these cueshierarchically (Etienne 1992; Winston 1994; Maaswinkel& Wishaw 1999). The relatively close proximity of thelandmarks to the goal may have biased the animals touse allocentric cues that conflicted with self-motion infor-mation. Past work has indicated that landmarks posi-tioned close to a goal (but not so close as to bea beacon) are highly favoured sources of information dur-ing search (see Kamil & Cheng 2001 for a review).

The results of the current study are similar to thosereported by Sutton & Shettleworth (2005) using similarprocedures with pigeons. In Experiment 3 of their study,they removed informative local landmarks (as in Experi-ment 1 of our study) and the pigeons tended to searchin the quadrant consistent with the use of self-motioninformation. Likewise, when the informative landmarksin the testing environment were rotated, both nutcrackersand pigeons weighed local landmark information moreheavily than self-motion cues. One difference was thatthe pigeons examined by Sutton & Shettleworth wereless accurate than nutcrackers using both self-motionand landmark cues. Pigeons were considerably less accu-rate than nutcrackers when using self-motion cues duringthe landmark removal tests (pigeons in Experiment 3,opaque transport group: X� SDw28:00� 12:00; nut-crackers in Experiment 1: X ¼ 10:02; CI ¼ 6:32� 13:71)and when using landmark information during the conflicttests (pigeons in Experiment 2, opaque transport group:X� SDw28:00�w10:00; nutcrackers in Experiment 2:X ¼ 9:74, CI ¼ 1.60 � 17.87). One possibility is that thecomparatively worse accuracy of pigeons was a result ofbeing tested in a square arena that was approximatelydouble the size of the one used with nutcrackers. Duringthe tests in which the landmarks were rotated, if a pigeonsearched in the location defined by self-motion cues dur-ing some proportion of the time, it would reduce the accu-racy scores. Such errors would not have such an egregiouseffect in reducing accuracy for nutcrackers because thetesting environment was smaller. Pigeons were also pas-sively transported to the testing environment, whereasthe nutcrackers were able to move freely from the startlocation to the goal. The difference in the availability of

ANIMAL BEHAVIOUR, 76, 41316

self-motion cues was likely to have affected the pigeons’ability to use self-motion information. Another possibilityis that, although nutcrackers and pigeons show qualita-tively similar patterns of performance, the better accuracyof nutcrackers reflects a real difference in their ability touse both self-motion and allocentric information. Pastwork has indicated that nutcrackers are more accuratethan pigeons when using allocentric information whenboth species are given comparable tasks (Jones et al.2002). The nutcrackers and pigeons did show a qualita-tively similar pattern of performance, as both speciestended to make a similar proportion of responses in thequadrant defined by self-motion cues during the land-mark-removal tests, as well as making a similar proportionof responses in the quadrant defined by local landmarksduring the conflict tests. Future work more directly explor-ing comparative differences in the use of self-motioninformation would be of considerable interest.

The approach used to investigate the use of self-motioninformation in the current study is somewhat differentfrom that used in past work with small-scale navigationtasks (Mittelstaedt & Mittelstaedt 1982; Etienne et al.1986; Etienne 1992; Sequinot et al. 1993). Many of thesestudies used animals that leave a nest to forage for a re-source in the environment before returning home. Theability of the animal to determine the location of homeaccurately after making the excursion (the homeward vec-tor) is taken as evidence for dead reckoning. In contrast, inthe current study, the birds were using self-motion infor-mation to identify the position of a goal in an environ-ment. Whereas the examination of how animals mayuse self-motion cues to determine goal location in anenvironment is not unique (e.g. Etienne et al. 1992;Etienne 1998), the approach is less common than thestudy of how self-motion cues contribute to homewardvectors.

We used a relatively small number of birds in thecurrent study. In Experiment 1, individual differences insearch were apparent during the tests with the novel door(particularly during the second of the 270� novel-doortests), as the pattern of search was somewhat moredistributed. If we had used more birds the pattern ofsearch may have been more focused during these tests.Likewise, during Experiment 2 we expected that differentbirds might favour different types of cues during theconflict tests. Some birds appeared to use self-motion cues,whereas others appeared to favour landmarks during thetests with the novel doors. Importantly, during the testswith the novel doors in Experiment 2 all the birdsfavoured the use of landmarks over other cues, indicatingthe importance of landmarks in directing behaviour.

Note that we have been hesitant in this report toindicate that the nutcrackers were using dead reckoningto locate the position of the goal in the square enclosure.The use of the term ‘dead reckoning’ assumes that ananimal is making a determination of the distance anddirection of the position of the goal (in the current study)relative to home. Nutcrackers were clearly using self-motion directional information generated by self-motioncues relative to their start location to determine which offour corners to search in the square enclosure. Nutcrackers

may have not used distance information potentiallygenerated by self-motion cues (and part of the dead-reckoning system) because the goal was always a fixeddistance from the corner of the box (an allocentric cue).The assessment of the distance component of deadreckoning has been somewhat limited in other studiesthat have used small-scale navigation tasks. Because theanimals in these tasks typically encounter the edge of anarena before encountering the nest, the role of actuallydetermining the home position and the distance requiredto return home is limited (e.g. Mittelstaedt & Mittelstaedt1982; Etienne et al. 1986). Certainly, the fact that nut-crackers can use directional information during thissmall-scale navigational task suggests that directionalinformation can be determined, presumably using deadreckoning.

Nutcrackers may use familiar routes, landmarks, andeven celestial cues to return to a site in which they havemade several caches (long-distance navigation). Once ata cache site (small-scale navigation task), nutcrackersappear capable of using beacons, single landmarks, con-figurations of landmarks, and celestial cues to recover theirhidden caches accurately. The results from Experiment 2are consistent with this past work and indicate thatproximal allocentric cues provide strong sources ofinformation for finding hidden goals. The results fromExperiment 1 extend the past work with nutcrackers andindicate that they may also be able to use self-motioninformation to locate hidden goals. Specifically, nut-crackers may use their entry position into a cache locationas a starting point to engage a self-motion representationof the cache locations in the area to direct search.Alternatively, some researchers have suggested thata self-motion frame may be used to establish and updatean allocentric frame of reference. An animal that is dead-reckoning in its environment can use the estimation of itscurrent position to encode the locations of landmarks thatit encounters relative to the starting position. Later, ananimal may learn to associate these landmarks with otherlocations in the environment (allocentric relationships).The animal’s position on the allocentric frame as it movesthrough the environment may then be updated using self-motion cues. The extent to which self-motion informa-tion may be used to establish or update allocentric frameswas not directly examined in this study, but would be ofconsiderable interest for future work.

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