Did tool-use evolve with enhanced physical cognitive abilities?

2013·0.54 MB·English

by  Teschke, I.

Did tool-use evolve with enhanced
physical cognitive abilities?
I. Teschke1, C. A. F. Wascher2, M. F. Scriba1,3, A. M. P. von Bayern4,1, V. Huml1,
B. Siemers1,† and S. Tebbich5
rstb.royalsocietypublishing.org 1MaxPlanck Institute for Ornithology, Seewiesen,Germany
2Konrad LorenzForschungsstelle,Corefacility,UniversityofVienna, Gruenau, Austria
3DepartmentofEcologyand Evolution,UniversityofLausanne, Lausanne, Switzerland
4DepartmentofZoology, UniversityofOxford, Oxford, UK
5DepartmentofBehavioural Biology,UniversityofVienna, Vienna, Austria
Research
The use and manufacture of tools have been considered to be cognitively
demandingandthusapossibledrivingfactorintheevolutionofintelligence.
Cite this article: Teschke I, Wascher CAF, Inthisstudy,wetestedthehypothesisthatenhancedphysicalcognitiveabilities
Scriba MF, von Bayern AMP, Huml V, Siemers evolvedinconjunctionwiththeuseoftools,bycomparingtheperformanceof
naturallytool-usingandnon-tool-usingspeciesinasuiteofphysicalandgen-
B, Tebbich S. 2013 Did tool-use evolve with
eral learningtasks. Wepredictedthatthehabituallytool-using species, New
enhanced physical cognitive abilities? Phil
Caledonian crows and Gala´pagos woodpecker finches, should outperform
Trans R Soc B 368: 20120418.
theirnon-tool-usingrelatives,thesmalltreefinchesandthecarrioncrowsina
http://dx.doi.org/10.1098/rstb.2012.0418 physicalproblembutnotingenerallearningtasks.Weonlyfoundadivergence
inthepredicteddirectionforcorvids.Thatonlyoneofourcomparisonssup-
portsthepredictionsunderthishypothesismightbeattributabletodifferent
One contribution of 15 to a Theme Issue
complexitiesoftool-useinthetwotool-usingspecies.Acriticalevaluationis
‘Tool use as adaptation’.
offeredoftheconceptualandmethodologicalproblemsinherentincomparative
studiesontool-relatedcognitiveabilities.
Subject Areas:
behaviour, cognition, evolution
1. Introduction
Keywords:
Animal tool-use has inspired researchers of comparative cognition for decades.
tool-use, comparative cognition, corvids, Muchofthisintereststemsfromtheputativeroleoftool-useintheevolutionof
Darwin’s finches humanintelligence.Theideaisthatastoolsgainedimportanceintheecologyof
early hominids, selection acted upon cognitive abilities to improve their tool-
usingproficiency[1].Inthisscenario,information-processingwashonedinthecon-
Author for correspondence:
textoftoolmanufactureanduse,butgraduallyledtomorecomplexandgeneral
S. Tebbich
cognitiveabilities.Alternately,humantool-usemayhaveevolvedasaby-product
e-mail: [email protected] ofgeneralizedintelligenceevolvedinanothercontext(e.g.[2]).Thus,itisnotsur-
prisingthatmuchcomparativeresearchontool-usetraditionallyrevolvedaround
anthropocentric questions, mainly that of whether and to what extent animal
tool-useindicatescontinuityinthementalabilitiesofanimalsandhumans.
Today,reportsoftool-useinanimalsabound,rangingfrominsectstobirds
[3].Animaltool-usevariestremendouslyinitscomplexityandneuronalunder-
pinningsandthus,afundamentalrevisionoftheoriginalnotionthattool-useis
perseareflectionofintelligencehasbecomenecessary.Nevertheless,thereare
stillreasonsnottodiscardtheideaofapotentiallinkbetweenintelligenceand
tool-useentirely.Oneistheexistenceofanimaltool-usebearingthehallmarks
of ‘sophisticated’ and potentially complex information-processing abilities,
†Deceased 23 May 2012. e.g. those instances involving use of multiple tools, sequential tool-use and/
or complex tool modification in the wild. The rarity of sophisticated forms of
We dedicate this paper to the memoryof our animaltool-usefurthermoresuggeststhatthereareconstraintsforitsevolution,
possibly cognitive abilities and/or neural substrate. Another reason is the
friend and colleague, Bjo¨rn Siemers.
existence of supporting correlational evidence: for birds, there is a strong
relationshipbetweentool-useandbrainsize[4]andtool-useandbrainstructure
Electronic supplementary material is available
[5],andtool-useandbrainsizearerelatedinprimates[6].Itisthereforeimpor-
at http://dx.doi.org/10.1098/rstb.2012.0418 or tant to investigate the relationship between tool-use and enhanced cognition,
via http://rstb.royalsocietypublishing.org.
&
2013TheAuthors.PublishedbytheRoyalSocietyunderthetermsoftheCreativeCommonsAttribution
License http://creativecommons.org/licenses/by/3.0/, which permits unrestricted use, provided the original
authorandsourcearecredited.
but with a focus on identifying the kinds of cognitive tool- have also investigated the tool- related cognitive abilities of 2
related adaptations to expect, and with clear predictions non-tool-using primates[25–27].
ofwheretolookforthem.Twoapproachescouldbeparticu- Adeviationfromthefocusonprimatesoccurredwiththe rstb
larlyusefulinguidingustoanswers.Thefirstiscost–benefit discoveryofhighlysophisticatedtool-useinNCCs,involving .ro
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analysis:tool-relatedcognitiveadaptationsareexpectedonly use of multiple tools to extract arthropods from various sub- als
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wheretool-useisunderstrongselection.Furthermore,itmay strates and complex tool manufacture in the wild (reviewed c
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helptogeneratehypothesesthatcanexplainwhyaparticular in [28,29]). In the laboratory, they appropriately select and ty
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species evolved tool-use, whereas a closely related species modifytoolsforagiventask[30,31],displayelementsofplan- b
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did not. Second, once hypotheses about the relationship of ning in meta-tool tasks [32,33] and are able to develop h
in
tool-use and cognitive traits have been formulated, compar- spontaneous solutions to novel technical problems using g.o
ing cognitive performance between closely and distantly novelmaterialsinnovelways[34,35].Untilrecently,thetool- rg
related species is essential to test them. In elaborating related cognition of NCCs was considered unique among
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upon the significance of each of these approaches, we will corvids. However in 2009, rooks (Corvus frugilegus), a non- il
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be focusing on the context in which most tool-use occurs, tool-using corvid species, were found to perform similarlyto ra
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namelyforaging. NCCsinseveralcognitivetool-relatedtasks[36].Thissuggests R
thatthespecialcognitiveabilitiesofNCCsmayhaveevolved So
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inanothercontextprecedingtheevolutionoftool-use[2]. B
3
(a) The cost and benefits of tool-use and their The findings of Emery & Bird [36] remind us of the 6
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:
importance of a rigorous comparative programme to deter- 2
link to evolution 0
1
mine whether there is a general pattern of association 2
0
Themainbenefitoftool-useinforagingmaybeanincreasein between an adaptive cognitive specialization and tool-use. 41
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quantityorqualityofpreythatisinaccessiblewithouttools[7]. This should not only entail comparisons between distantly
Unfortunately, quantitative data on the nutritional benefit of related tool-users, but also between closely related tool-
tool-use are scarce [7–12]. At least for some species, it has users and non-tool-users. Thereby, repeated appearance of
been shown that tool-use is more costly than conventional thecognitivetraitinquestiononlyintool-usersinphylogen-
foragingtechniquesintermsoftime[8,9].Thecostsoflearning etically independent species pairs would be strong evidence
andtheexpenditureofcognitiveresourcesinvolvedintool-use foracognitiveadaptation[37].
anditsdevelopmentaremoredifficulttopindown.Learning
tousetoolsduringontogenyhasbeenshowntobeasubstan-
tial investment at least for chimpanzees (Pan troglodytes,
[13,14]) and New Caledonian crows (NCCs; Corvus mondelu- 2. Our study: test of tool-related physical
doides: [15–17]). Other factors and constraints that could
cognition in corvids
influence the evolution of tool-use are for instance the avail-
ability of tool-materials, morphology, behavioural and
Over the past 5 years, we have applied the comparative
cognitive traits such as sociality and motivation to play and
method, as described earlier, to two species pairsto investi-
interact with objects, neural substrate and related energetic
gate the question of whether the use of tools evolved in
costs [18,19]. Such limiting factors could operate to constrain
conjunction with enhanced and specialized physical cogni-
or enable the evolution of tool-use at various stages, such as
tive abilities. Previously, we compared general learning and
during its invention, its diffusion through the population
physical cognitive abilities in the WPF and a closely related
anditsmaintenanceinapopulation.
non-tool-using species, the STF. WPFs habitually use twigs
The interplay between costs, benefits and limiting factors
or cactus spines to extract arthropods from crevices and
can be exemplified by a comparison of the tool-using wood-
showsimplemodificationofthesetoolssuchtoolshortening
pecker finches (WPFs Cactospiza pallida) and the small tree
or breaking of sidetwigs [8].
finch(STF;Camarhynchusparvulus),asympatricnon-tool-using
We predicted that if tool-use evolved with enhanced
speciesthatiscloselyrelatedtotheWPF.Thoughtheyareboth
specialized cognitive abilities, WPFs should outperform STFs
extractiveforagers,theWPFismorespecializedonextracting
in physical tasks but not necessarily in the general learning
concealed prey from a substrate. Its straight beak is not only
tasks. Contrary to expectation, the STFs performed similarly
ideal for pecking at the substrate, but also well-suited for
or better than WPFs in one of the general learning tasks and
manipulating tools and may allow better vision at the beak
most of the physical tasks [38,39]. Thus, the study yielded
tip [20]. Similarly, other characteristics related to extractive
noevidencethatWPFshaveenhancedphysicalcognition.
foraging such as perseverance and high levels of neophilia
The aim of this study was to provide highly comparable
might have increasedthelikelihood for the evolution oftool-
data from a new tool-using/non-tool-using species pair from
useinthisspecies.Tosummarize,slightdifferencesinecology
a distantly related group using the methods which had been
and morphology can significantly influence the cost–benefit
applied in the preceding Darwin’s finch study. This allows a
ratio and the effect of constraining factors, thus indirectly
more complete assessment of the hypothesis that tool-use
influencingtheevolutionarytrajectoryoftool-use.
mightgenerallybeassociatedwithadaptivecognitivespecializ-
ationsinthephysicaldomain.Usingtheparadigmspreviously
establishedwithDarwin’sfinches,wetestedphysicalcognition
(b) The comparative approach
and general learning abilities in tool-using NCCs and a non-
Traditionally,therehasbeenastrongfocusoftool-usestudies tool-using species, the carrion crow (Corvus corone). To our
on comparing tool-related complex cognition (e.g. causal knowledge, ours is the only study to rigorously apply the
understanding) between humans and various primates comparative method to interspecific comparisons of closely
(reviewed in [21–24]) though a small number of studies relatedtool-using/non-tool-usingspeciespairsintwodistantly
related groups and using identical learning paradigms to test 3
(a)
allthespeciesinvolved.
rstb
(a) Methods .ro
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(i) Study locations, subjects and housing o
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AllNCCsandonehoodedcrow(Corvuscornix)weretestedat ty
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the Avian Cognition Research Station (ACRS) hosted by the b
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Max Planck Institute for Ornithology (MPIO), Seewiesen, h
in
Germany from March to November 2011. All carrion and g.o
the remaining hooded crows were tested at the Konrad rg
(b) (c) (d) (e)
Lorenz Research Station (KLF) in Gru¨nau, Austria from
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June to August 2011 and at the MPIO in June 2009 and il
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November 2009–May 2010. The test for neophilia (see ra
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below) was conducted in 2012 at the ACRS and KLF, and R
the NCCs were not the same as the ones tested in the other So
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tasks(see theelectronic supplementary material, table S1). B
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Thedatafromtwohoodedcrowswereincludedinthecar- 6
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:
rion crow dataset as these closely related species have been 2
10cm 01
onlyrecentlysplitintotwoseparatespeciesandsharesimilar 2
0
ecology and morphology [40]. Although the hooded crows Figure1.(a)Thecanetaskapparatuswithcanesandrewardsarrangedasinthe 41
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are treated as carrion crows for the statistical analysis, these initialtestcondition.Panels(b)–(e)transfertasks1–4.Adaptedfrom[38,39].
individuals have been made distinguishable from the carrion
crows in the graphs. Furthermore, some WPFs do not use subject met criterion (see general experimental procedure),
tools (detailed explanation in the methods of the electronic the colour-reward contingency was reversed in the reversal
supplementary material, see also [38]). The WPF dataset is phase. Subjects were given a maximum of 140 trials in each
thereforecomprisedtool-usingandnon-tool-usingindividuals, phase. Eight NCCs, seven carrion crows, one hooded crow
andthisdistinctionistakenintoaccountintheanalysis.Asum- and16WPFsweretestedinthisexperiment.
mary clarifying the orderof experiments, theparticipation of
each bird in each experiment as well as rearing history is (iv) Experiment 3: the novel box-opening task
giveninthemethodssectionandtheelectronicsupplementary
Theapparatuswasaboxmadeofopaque,whitePerspexwith
material,tableS1.Furtherdetailsconcerningrearingexperience
a transparent lid (box: width¼15(cid:2)depth¼12(cid:2)height¼
and housing are also in the methods section of the electronic
12cm; lid overlaps edge at front by 3cm). The lid was
supplementarymaterial.
hinged to the backedge of the box and overlapped the front
edgeofthebox.Theboxcouldbeopenedbypushingthepro-
(ii) Experiment 1: the cane task
truding lip of the lid upwards. Before testing, birds were
Thisexperimentinvolvedfoodretrievalcontingentonmaking habituated to the box by feeding from it once while it was
achoicebetweentwocanes,onlyoneofwhichcouldretrieve open. Subjects were given six sessions of 25min, receiving
thereward.Ineachcondition,onefoodrewardwasinsidethe uptothreesessionsperday.Abirdwassuccessfulandtesting
hooked portion of the cane and one outside of it (with the was ended when it opened the box and ate the reward. If a
exception of transfer task 4 in which both rewards were birddidnotmakephysicalcontactwiththeboxduringases-
inside the hooked portion of both canes; figure 1). Eight sion, it was re-habituated to the box as described above and
NCCs, five carrion crows, two hooded crows and 12 WPFs thesessionwasrepeated.Abirdwasgivenuptotwoextrases-
participatedinthisexperiment. sions upon failing to make contact with the box in any one
Transfertasks.Thosesubjectsthatsolvedtheinitialversion session. Eight NCCs, seven carrion crows and two hooded
of the task by reaching the set learning criterion (see below) crows were tested in this study. Additionally, we compare
withinamaximumof180trialswerethentestedinfourfurther theNCCdatatothatof18WPFswhichweretestedforapre-
variationsoftheinitialtask(transfertasks,figure1b–e),where viousstudy[38].The‘totallengthoftesting’(s)and‘success’
theyreceivedamaximumof20trialsineach. (opening box and gaining access to the food reward) were
themeasurementstakenforcomparison.
(iii) Experiment 2: the reversal task
(v) General experimental procedure
Theapparatusconsistedoftwofeederscoveredwithcoloured
lids (orange and blue) that were mounted 30cm apart on a Experiments were conducted in the home aviaries of the
grey Perspex base (50(cid:2)50cm). In each trial, a reward was birds, and food was removed from their aviaries approxi-
placedinoneofthefeeders,thelidswereplacedonthefeeders mately 2h before testing. The apparatus was baited out of
and birds were then allowed to remove one of the two lids. sight of the subject, and for each trial, placed onto the
A transparent Perspex divider prevented the birds from experimental table or experimental area within the home
removing the lid of both feeders. The experiment consisted aviary. The experimenter then left and observed the trial
of two phases: an initial ‘acquisition phase’ and a ‘reversal viacamcorder.
phase’. In the acquisition phase, only one colour was the Experiments 1–2 were two-choice learning experiments
rewarded (Sþ) stimulus. Half of the birds started with involving the same basic procedure. These tasks were con-
orange as Sþ and the other half with blue as Sþ. Once a ducted in blocks of 10 trials. In each trial, the subject was
given 5min to choose between two options for which the Second, we measured the latency to approach the cane 4
correct side was pseudorandomized and counterbalanced apparatus and also to touch the cane averaged over the first
rightandleft.Someslightmodificationstotheoriginaltesting 50 trials for each individual (details in the electronic sup- rstb
conditionsandtestingregimewithWPFsweremadewiththe plementary material). While strictly speaking, these do not .ro
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corvids(seetheelectronicsupplementarymaterial,methods). provide measures of novelty reaction, they do however pro- als
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Learningcriterion.Tomeetthesuccesscriterion,abirdhad vide a way of comparing the motivation with which these c
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to make 15 or more correct choices within two consecutive animals interacted with the cane apparatus. We deemed this ty
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blocksof10trials.Specifically,thenumberofcorrectresponses important as carrion crows are known to be neophobic, b
lis
inoneofthetwoblockshadtobeatleastsevenconsecutively when approaching novel food [44] and differences in motiv- h
in
correct and in the other at least eight or in one block all ation could potentially explain differences in cane task g.o
10 correct. This criterion was derived using a Monte Carlo performance. These measures were scored from videos by rg
simulation (details in [41]). Some subjects developed a pos- M.F.S.Intrialswherethebirdsdidnotapproachtheapparatus
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itional bias, which we defined as six consecutive choices of at all in 5min, birds were given a ceiling value, which was il
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one side, probably owing to intermittent reinforcement. derived byadding 1 to the maximum time in each category. ra
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When this happened, we applied a side bias correction pro- The Mann–Whitney U-test was used to compare apparatus R
cedure (‘correction trials’, see the electronic supplementary approachandcanetouchlatenciesbetweenthespecies. So
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material,methodsfordetails). B
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(b) Results 68
:
(vi) Statistical analysis (i) Experiment 1: the cane task 201
2
Fisher’s exact test was used to test for species differences in 0
Neither the five carrion crows nor the two hooded crows 4
1
the proportion of individuals to meet the success criterion. 8
were able to solve the initial task, while five of the eight
We also compared learning speed and success probabi-
NCCs and eight of the 12 WPFs met the learning criterion
lity between NCCs and carrion crows/hooded crows and
inthisphase.TheproportionofNCCsandWPFstoreachcri-
between NCCs and WPFs in the initial phases of the cane
terion in the initial task did not differ significantly (Fisher’s
task and for both phases of the reversal task using general-
exact test: p¼1). However, proportionally more NCCs than
ized linear mixed models, specifying logistic regression
carrion crows solved the initial task (Fisher’s exact test, p¼
withbinomialerrors(GLMM,[42]).Foreachspeciescompari-
0.026). The disparity in learning performance in the initial
son,aseparatemodelwasconstructedfortheinitialphaseof
task between NCCs and carrion crows was further reflected
thecanetaskandforbothphasesofthereversaltask.Priorto
in the significant difference in the speed with which they
fittingthemodel,wez-transformedtrialnumbertoameanof improved in this task (corvid model: species(cid:2)trial: x2¼
1
0andastandarddeviationof1,andsidebiascorrectiontrials
4.13,p¼0.042;figure2).
wereremovedfromalldatasets.Fulldetailsofthemodelling
NCCs and WPFs did not differ significantly in their
process and the full model results can be found in the
learning speed of the initial task (tool-user model: species(cid:2)
methods and results sections, electronic supplementary trial: x2¼0.001, p¼0.973; figure 2) nor did they differ in
1
material, tables S2–S4.
their overall success probability (tool-user model: species:
Each statistical comparison between NCCs and WPFs x2¼2.21, p¼0.137; figure 2). Nevertheless, they generally
1
was conducted once only with tool-using WPFs and once
learnedoverthecourseoftrials(tool-usermodel:trial:z¼4.98,
withallWPFspooled(detailsintheelectronicsupplementary
p,0.001;figure2).
material,methods).Sincetheconclusionsalwaysremainedthe
Transferperformance.The fiveNCCsand eightWPFsthat
sameregardlessofwhichWPFgroupingwasused,wereport
successfully solved the initial task were subsequently tested
onlyresultsforthecomparisonofNCCswithpooledWPFs.
in four transfer tasks. Only one WPF and no NCCs met
Allstatisticswere conductedwith R v. 2.15.1[43].
criterion in the first transfer task. Two NCCs and one tool-
using WPF met criterion in the second transfer task. As we
(vii) Comparison of novelty reactions and motivation between
foundpreviously,performancewasbestinthethirdtransfer
corvid species task where three NCCs and six WPFs met criterion. No
individuals solvedthe fourthtransfer task.
Novelty reactions between carrion crows and NCCs were
To furtherassesstransfer differences between NCCs and
assessed intwo differentways.
WPFs, we pooled data from the first two transfer tasks for
First, we presented individuals with a novel object
each bird and calculated the proportion of trials in which
(greendog-toyball,electronicsupplementarymaterial,figure
birdsmade acorrect choiceto thetotal trials received in the
S1) and measured latency to first contact. Birds received one
first two sessions. We used only datafrom the first two ses-
10min session per day during which they were separated
sions of each transfer, because the sample size of NCCs
fromotherbirds.Iftheydidnotapproachtheobjectwithina
declined to four after the second transfer task since one
session, the novel object was removed and the individual
subjectfellill.Therewasnosignificantdifferenceintransfer
receivedanothersessionthenextday.Thetestendedafterthe
performance between NCCs (median proportional correct¼
sessioninwhichthebirdsfirsttouchedtheobjectorafter13ses-
1.58, range¼1.21–1.74) and WPFs (median¼1.79, range¼
sions,ifindividualsdidnotapproachbefore.Eachbirdreceived
1.53–2.22) according to this measure (Mann–Whitney
a value calculated by adding the total session time until it
U-test: N ¼5, N ¼8; U¼9; p¼0.124).
touched the object for the first time. Birdsthat did not touch NCC WPF
theballwithin13sessionsreceivedaceilingvaluewhichwas
(ii) Experiment 2: the reversal task
calculated by adding one to the highest latency to touch the
ball among the other crows. The Mann–Whitney U-test was All individuals met the learning criterion during the acqui-
usedtocompareballtouchlatenciesbetweenthespecies. sition phase and also in the reversal phase, with the
reversal task 5
(a) acquisition phase (b) reversal phase (c) cane task
rstb
bility 1 .royalso
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pro typ
success 0 CC CC CC ublishing.o
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proba ransR
cess Soc
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su 0 NCC NCC NCC 36
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2
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1 1
bility 20418
a
b
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pr
s
s
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c
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su 0 WPF WPF WPF
0 20 40 60 80 100 120 140 0 20 40 60 80 100 120 140 0 50 100 150
trial number trial number trial number
Figure 2. Logistic regression models of success probabilityacrosstrial number for two-choice learning tasks. (a) Acquisition phase and (b) reversal phase in the
reversaltask,(c)thecanetask.Eachrowreferstooneofthethreetestgroups(CC,carrioncrows;NCC,NewCaledoniancrows;WPF,woodpeckerfinches.Pointsrefer
totheproportionofcorrecttrialsperblockof10trialsforeachindividual.Dataandmodelsfromthehoodedcrows,asubgroupofthecarrioncrows,aredenotedby
dashed lines and solid black points. Graphs from WPFs were adapted from [38].
exceptionofonecarrioncrow,twoNCCsandoneWPFinthe andNCCs(Fischer’sexacttest,p¼1),norwasthereasignifi-
reversalphase.NCCsandcarrioncrowsdidnotdifferintheir cant difference in proportional success between NCCs and
speedof learningeitherintheacquisitionphase (acquisition WPFs(Fisher’s exact test, p¼0.673).
phase model: group(cid:2)trial number: x2¼0.02, p¼0.882; Comparisonlatencytosuccess.Whenthelength(inseconds)
1
figure 2) or in the reversal phase (reversal phase model: of all sessions was summed for each individual and species
species(cid:2)trial number: x2¼0.14, p¼0.711; figure 2) comparisons conducted, we found no significant differences
1
although individuals clearly improvedinboth phases of the either between NCCs (median¼6269s, range¼82–9000)
task (acquisition phase-corvid model: trial number: z¼6.52, andcarrioncrows(median¼1740s,range¼34–9000;Mann–
p,0.0001; reversal phase model: trial number: z¼6.92, Whitney U-test: N ¼9, N ¼8, U¼30.5, p¼0.623) or
CC NCC
p,0.0001; figure 2). Overall success probability also did between WPFs (median¼9000s, range¼50–9000) and
not differ between these species in the acquisition phase NCCs (Mann–Whitney U-test: N ¼18, N ¼8, U¼55,
WPF NCC
(species: x2¼0.17, p¼0.682; figure 2) and in the reversal p¼0.327).
1
phase(species:x2¼0.76,p¼0.383;figure2).
1
In the acquisitionphase, WPFs were significantly faster in
(iv) Comparison of novelty reactions and motivation between
their learning speed than NCCs (acquisition phase model:
species(cid:2)trial number:x2¼10.08,p¼0.001;figure2)butnot corvid species
1
in the reversal phase (reversal phase model: species(cid:2)trial Therewasnoevidenceofasignificantspeciesdifferenceeither
number:x2¼0.001,p¼0.974; figure 2).Therewas no species inthemedianmeantimestoapproachthecaneapparatus(car-
1
difference in overall success probability in the reversal phase rion crows: median approach time¼6.16s, range¼4.68–
(reversalphasemodel:species:x2¼0.0005,p¼0.982;figure2) 48.48; NCCs: median¼6.75s, range¼2.12 –21.98; Mann–
1
though individuals clearly improved over trials in this phase Whitney U-test: N ¼7, N ¼8, U¼18, p¼0.281) or in
CC NCC
(reversalphasemodel:z¼8.53,p,0.001;figure2). the median mean times to touch the cane (carrion crows:
median cane touch time¼8.92s, range¼6.74–61.20; NCCs:
median¼8.79s, range¼4.42 –25.78; Mann–Whitney U-test:
(iii) Experiment 3: the novel box-opening task N ¼7,N ¼8,U¼19,p¼0.336)duringthefirst50trials.
CC NCC
Five NCCs, eight WPFs and six carrion crows successfully There was no significant difference between NCCs
solved the task within six sessions. Therewas no significant (median latency¼7475s, range¼328–7475) and carrion
difference in proportional success between carrion crows crows (median latency¼3152s, range¼4–7474) in the
latency with which they touched the ball (Mann–Whitney species,havingonlypresentedonetestofphysicalcognition. 6
U-test: N ¼7, N ¼8, U¼12,p¼0.068). Finally, the lack of identical rearing conditions between
CC NCC
groups is a common problem with long-lived and unusual rstb
species that require significant funds to raise and maintain. .ro
(c) Discussion and main conclusions from our study y
These problems are linked to some of the more universal als
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Our previous study [38] did not confirm the presence of challenges confronting researchers incomparativecognition. c
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enhancedphysicalcognitiveabilitiesintheWPF,whencom- In the following, we address some potential solutions for ty
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paredwithacloselyrelatednon-tool-usingspecies.However, these challenges and touch upon our suggestions for future b
lis
in line with the prediction that tool-use evolved with researchon tool-related cognition. h
in
enhanced physical cognitive abilities, this study found that g.o
NCCs outperformed carrion crows in the cane task, but not rg
in two general learning tasks. This difference in corvids but 3. Outlook P
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not Darwin’s finches matches the expectation that sophisti- il
T
cated cognitive tool-related adaptations should be found in (a) Troubleshooting the physical cognitive adaptive ra
n
s
species with sophisticated tool-use, as NCCs substantially R
exceed WPFs in tool diversity and the complexity of tool specialization hypothesis: getting ahead of So
c
manufacture(reviewedin [28]). ourselves? B
3
The difference in NCC and carrion crow performance 6
Theecologicalapproachinunderstandingadaptivebehaviour 8:
cannotbeexplainedbydifferentlevelsofneophobiaormotiv- 2
andunderlyingcognitivemechanismsisaniterativeprocessof 01
ation,becausewefoundnosignificantdifferenceineitherofour 2
investigation, synthesizing hypotheses and predictions both 04
twomeasuresbetweenthetwospecies,butitmightbeattribu- 1
from the functional and mechanistic perspective. A classic 8
tabletotheunaccustomedcognitiveloadthatthemanipulation
example of this process has been described in detail by
ofatoolimposedonthenon-tool-usingspecies[45].
Smuldersetal.[51]forfoodcaching.Differencesinbrainmor-
However, there are several reasons to treat the results
phology between caching and non-caching species and
with caution. One is that the comparison groups of corvids
seasonallyvaryingbrainmorphology inseveral food-caching
did not share identical rearing conditions: most of the
speciesfromparidstocorvidshavebeencentralfindingsfuel-
NCCs were wild-caught, whereas all of the carrion crows
ling the cognitive adaptive specialization hypothesis for food
werehand-raised.Althoughthiscouldhavehadasubstantial
storers(reviewedin[52]).Inthefood-cachingparadigms,eco-
effectontheresults,itisdifficulttopredictexactlyinwhich
logical knowledge not only helped to point to memory as a
direction. Another reason is that none of the carrion crows
likely solution to the problem which food hoarders face in
reached the learning criterion in the cane task and, thus,
thewild,butlaterithelpedtorefinethehypothesistofitvar-
the performance of this large-brained corvid was worse
iousecologicalcircumstancesoffoodhoardinganimals.More
than that of the STFs. This is surprising, especially given
specifically,therealizationthatonlyasubgroupoffoodhoar-
the excellent performance of other non-tool-using corvids,
dersneedtoremembercachelocationsforalongperiodlead
suchas rooksinphysical tasks[36,46].
totheproposalthatonlythesespeciesshouldhaveaduration
Also,thecomparisonoflarge-brainedcorvidsanddistantly
ofspatialmemorylongerthanthatofotherspecies.Thus,the
relatedWPFsdidnotexposeasignificantdifferenceinphysical
spatial memory hypothesis for food hoarding comes from
taskperformancebetweenthesetool-usingspecieseitherinthe
knowledge of the function of food hoarding in animals and
initialcanetaskorinthecanetransfertaskperformance.The
isinformedbythedetailsofecology.
lackofadifferenceinthecanetransfertasksisverysurprising
Inthecase oftool-use,therehasbeen adisproportionate
giventheperformanceofNCCsinothertasksthatindicateat
focus on human-like complex cognitive mechanisms like
leastsomesensitivitytophysicalrulesandtransfertosimilar
causal understanding that may be involved in animal tool-
problems [35,47,48]. One way of understanding these results
use. However, gradual improvements through associative
is that NCCs may simply use simple perceptional cues in
processes (i.e. associative learning of spatial relationships,
some situations but not in others [23,49]. Also, perhaps the
attention towards relevant cues) could improve efficiency of
cane task poses a problem that is irrelevant to these species’
flexible and context-specific tool-use just as well as complex
natural tool-use, and thus imposes anunanticipated measure
mechanisms and thus should be included in predictions.
ofdifficultyonbothspecies.Finally,itmaybethattheperform-
Also,recentdatasuggestthattheunderlyingcognitivemech-
ance of NCCs, who usually engage in sophisticated tool-use,
anisms of even supposedly sophisticated tool-users such as
maysomehowbeimpairedwhenforcedtoengageinartificial
chimpanzees and NCCs are a mixture of complex and
tasksinvolvingchoicesbetweentwooptions[50]orinvolving
simple mechanisms and those in between [23]. We suggest
restricted object manipulation as necessitated by the cane
thatfuturestudiesputlessweightondistinguishingbetween
task. For future studies, we suggest inclusion of two groups
complex and simple cognition in tool-use and that they are
of tool-users: one which uses freely manipulable tools and
carefultorootpredictionsabouttool-relatedcognitivemech-
onewhichusesthepre-insertedtools.Wefurtherrecommend,
anismsindetailedexaminationofthetoolproblemsfacedby
wherepossible,theavoidanceofbinarychoicetasks.
animalsin their natural context.
Ourdataonthephysicalcognitiveadaptivespecialization
hypothesis are subject to some of the criticisms shared by
manystudiesofcomparativecognition.Foronething,cogni- (b) Roadmap for future comparative studies of tool-use
tive characteristics other than the one of interest could have
and cognition
been taxed by the tasks, leading to a pattern that does not
fitourprediction.Wealsomayhavemissedthecrucialsub- Asweseeit,therearecurrentlytwomainapproachestotake
category of physical cognition that differs between the inadvancingourunderstandingofthecognitivemechanisms
underlyingtool-relatedcognition.Oneistorefinehypotheses, robustnessofanobservedpattern.Anotherhugechallengeof 7
whereastheotheristorefinemethodology. comparativecognitionisthatweoftenareunawareofthefull
suite of cognitive mechanisms influencing performance in a rstb
(i) Using knowledge of tool-use in a natural context to refine giventask.Consequently,weareoftennotclearabouttheques- .ro
y
hypotheses tions posed, an issue which is compounded in multi-species als
o
comparisons.Ideally,taskdesignsshouldaccountforthediffer- c
NCCs exemplify how knowledge of ecologyand natural his- entspecies‘non-focal’cognitivetraits,thatis,thosetraitswhich iety
p
tory has been useful in suggesting areas of cognition for u
arenotatthefocusofanexperiment,butcanneverthelesshavea b
experimental investigation. For example, geographical vari- lis
strong,sometimescentralinfluenceontaskperformance,such h
ation in NCC tools has been touted as suggestive of in
cumulative cultural evolution [53]. Along with other field adsiffaetrteenncteiosni,nmpoetrivceaptitoionnan[5d7,5te8m].pAeragmoeondt ebxuatmaplsloe ospfecthieiss g.org
studiesthathavedemonstratedtheexistenceofampleoppor-
approach is the study of Chappell et al. [59] that presents a
P
tunities for social transmission of information in this species, h
detailedanalysisoftherelationshipbetweenperseveranceand il
thissuggeststhatitmaybepromisingtolookatsociallearning impulsivity on innovation in tool-use problems with human Tra
n
in NCCs [53]. Furthermore, the observation that NCCs use s
children.Onesolutionistodeveloptaskbatteriesthatinclude R
barbed pandanus tools in the appropriate orientation in the tests of such general psychological variables in addition to So
wild (in order to be functional the tool must be held such c
those specifically probing only the cognitive trait(s) of focal B
that the hooks on the barbed edge face backwards from the 3
interest [58,60].Here,itisimportantto‘findtherightitemsto 6
8
tool tip) lead researchers to question the cognition involved :
test’byrootingpredictionsinspeciesecologyandobservation 2
0
in this behaviour [54]. One explanation put forth was that 1
andthetasksmustberevisedasnecessary.Thereisonemajor 2
NCCs might have a human-like underlying understanding 04
conundruminherentinthetaskbatteryapproachformultiple 1
ofthephysicalpropertiesofhooks,leadingtoanunderstand- 8
species(andalsomoregenerallyincomparativecognition):in
ing of the functional features of the tool. Another is that the
order to yield comparable data, tasks must be standardized,
behaviour might also be the result of simple associative
yet some species-specific task modifications are a ‘necessary
mechanisms—possibly trial and error learning. Subsequent
evil’toincreaseecologicalvalidityandthelikelihoodthateach
experimental investigation with wild-living crows or those
speciesisbeingaskedthesamequestion.Thecruxofthepro-
held briefly in captivity showed limited attendance of the
blem is that we often do not know in advance what the
crows to the functional orientation of the barbs and also
cognitive, motor and perceptual disparities between species
that when tools are dropped and/or picked up in the non-
areandhowtheywillinfluencetaskperformance.Dangerlies
functional orientation, repositioning arises from simple
in succumbing to the temptation of ‘quick and dirty’ exper-
associative strategies. In conclusion, the authors state their
iments that simply apply pre-existing paradigms to new
view that correct functional tool orientation in the wild may
specieswithoutsufficientthoughtdevotedtotailoringthepro-
simplybetheoutcomeofapplyingthecorrectproceduralrules
blem to the species at hand [61]. Intimate knowledge of a
ofpandanustoolmanufacture([54],butseealso[55]).Thisisa
speciesthroughcarefulobservationbothinthefieldandinthe
laudableexampleofanobservationfromthewildthatwasrig-
laboratory is the best help in designing comparable studies
orouslytestedusingsemi-wildexperimentsthatweredevised
and ecologically valid paradigms. In combination with an
to differentiate between the so-called high-level and low-level
improvedunderstandingofanimal’soverallpsychologicalpro-
underlying cognitive abilities. Its results clearly illustrate that
files (i.e. motivation, temperament, motor and perceptual
whatseemscomplexisnotnecessarilyso.Otherobservational
abilities,etc.),ausefulframeworkinspiredbyArtificialIntelli-
fieldstudiesonbeardedcapuchinmonkeys(Sapajuslibidinosus)
gence could help to decompose demands of cognitive tasks
andchimpanzeesinspiredthehypothesisthatenduringartefacts
into their component parts [62]. This would help clarify the
playanimportantroleforsomenonhumanspeciesinlearningto
natureoftheproblem,takingintoaccounttheinformationavail-
usetoolsbysupportingpersistentpractice[56].Tosummarize,
abletotheanimalsandpossibleproblemsolutions.
detailed knowledge of the behaviour from wild populations
One further issue we faced in this study is the interpret-
willhelptoidentifythetypeoftheproblemsthatanimalsare
ation of failure. Should we accept the null hypothesis that
facedwithinnatureandthusgeneratemoreaccuratehypotheses
carrion crows simply do not have enhanced physical cogni-
concerning the underlying mechanisms of their behaviour.
tion? Our comparative results suggest that this may not be
Thereby,itisessentialtoadheretotheprincipleofparsimony
justified and that further testing is needed to understand
andpresumethelowestdenominatorofcognitivemechanisms
these results. Seed et al. [63] recently reviewed this topic in
requiredforsolvingtheproblem.Improvedknowledgeofecol-
detailandsuggestthatunderstandingfailurescanbeachieved,
ogyandtool-useinanaturalcontextwillhelptoformulatemore
for example, by deconstructing a task and lowering task
precise andappropriate predictions concerning which specific
demands while asking the same question and by testing the
cognitivemechanismsmightbelinkedtotool-use.
species in several different analogous tasks [64]. Another
waytounderstandfailuresistolookatwhetherthedifference
(ii) Improving methods
betweenindividualsthatpassand fail canbecorrelated with
Notonlydoweneedmorebackgroundinformationonspecies’ variationinanotherpsychologicaltrait[63].Theseapproaches
natural behaviour to inform predictions, but we could also mightbefruitfulinfutureattemptstounderstandourresults.
benefit greatly from improvements in methodology. Much To conclude, in the field of comparative cognition, con-
wouldbegainedifmorestudiesadoptedarigorouscompara- siderableprogresshasbeenmadebyadoptinganintegrative
tive approach with interspecific comparison between at least approachinunderstandinganimalcognition[65].Theprocess
onetool-usingandonenon-tool-usingspecies,usingthesame of the ecological approach is nonlinear, oscillating bet-
or at least a comparable methodology. Including more non- weenpredictionsgeneratedfromfunctionalandmechanistic
tool-using species in the comparison will furthermore ensure knowledge of a behaviour. Thus, an understanding of the
relationshipsbetweencognitionandbehaviourrequirescon- non-animal experiments in accordance with the Austrian Animal 8
sideration of both ultimate and proximate standpoints. The Experiments Act (§ 2. Federal Law Gazette No. 501/1989) and no
best approach to choose at a given time is determined by lainceimncaelwcaarserteaqkuerir,eedn.sEuxrpinegrimnoenatnsiwmearlescwonedreuchtaerdmbeydanbyextpheerieexnpceerd- rstb
commonsense.However,theecologicalcontextofbehaviour imental procedure. All individuals participated and entered the .ro
y
must always be kept in mind, especially during laboratory experimentalcompartmentsvoluntarily.Focalindividualswereres- als
o
studiesofmechanism. cued from the wild when taken out of the nest at a young age by c
ie
unfavourableweatherconditions.Individualswereheldincaptivity ty
Permissiontoconductexperimentswiththewoodpeckerfincheswas at theKLF(licenceAT00009917) before andaftercompletionofthe pu
b
granted by the Gala´pagos National Park and the Charles Darwin presentstudy. lis
research station (Project PC-16-07, permit no. PR.PT.P004.R02). For hin
tghreanetexdperbiymetnhtes gwoivthernthmeenctrowof sUppecpieers BatavMarPiaIOi,npGeremrmissainoyn (wAazs. Acknowledgements.WewouldliketothankKlemenKoseljforgivingus g.org
55.2-1-54-2531-87-08).TheworkwiththecarrioncrowsatKLFcom- helpful comments on the statistics and Berenika Mioduszewska,
plied with guidelines provided by the Austrian Federal Act on the ChristianBlumandIrmgardNeumayrforpracticalhelp. Ph
ProtectionofAnimals(AnimalProtectionAct-§24Abs.1Z1and Funding statement. We thank the German Research Foundation (DFG, ilT
2;§25Abs.3 – TSchG,BGBl.INr.118/2004Art.2).Furthermore, grantno.Sl816/14)andtheMaxPlanckInstituteforOrnithologyand ran
s
as our experiments are purely appetitive, strictly non-invasive and the Austrian Science Fund (FWF, grant no. V95 –B17) for providing R
based exclusively on behavioural tests, they are classified as fundingforthisproject. So
c
B
3
6
8
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1
2
0
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