cell may have closer parallels to thedynamic action of vertebrate Kif7.

References1. Wong, S.Y., and Reiter, J.F. (2008). The primary

cilium at the crossroads of mammalianhedgehog signaling. Curr. Top Dev. Biol. 85,225–260.

2. Endoh-Yamagami, S., Evangelista, M.,Wilson, D., Wen, X., Theunissen, J.W.,Phamluong, K., Davis, M., Scales, S.J.,Solloway, M.J., de Sauvage, F.J., et al. (2009).The mammalian Cos2 homolog Kif7 plays anessential role in modulating Hh signaltransduction during development. Curr. Biol.19, 1320–1326.

3. Cheung, H.O., Zhang, X., Ribeiro, A., Mo, R.,Makino, S., Puviindran, V., Law, K.K.,Briscoe, J., and Hui, C.C. (2009). The kinesinprotein Kif7 is a critical regulator of Glitranscription factors in mammalian hedgehogsignaling. Sci. Signal 2, ra29.

4. Liem, K.F., Jr., He, M., Ocbina, P.J., andAnderson, K.V. (2009). Mouse Kif7/Costal2 isa cilia-associated protein that regulates Sonichedgehog signaling. Proc. Natl. Acad. USA 106,13377–13382.

5. Whittle, J.R. (1976). Clonal analysis ofa genetically caused duplication of the anteriorwing in Drosophila melanogaster. Dev. Biol.51, 257–268.

6. Saunders, J.W., and Gasseling, M. (1968).Ectodermal-mesenchymal interaction in theorigin of limb symmetry. In Epithelial-Mesenchymal Interaction, R. Fleischmayer andR.E. Billingham, eds. (Baltimore: Williams andWilkins), pp. 78–97.

7. Kalderon, D. (2004). Hedgehog signaling:Costal-2 bridges the transduction gap.Curr. Biol. 14, R67–R69.

8. Farzan, S.F., Ascano, M., Jr., Ogden, S.K.,Sanial, M., Brigui, A., Plessis, A., and

Robbins, D.J. (2008). Costal2 functions asa kinesin-like protein in the hedgehog signaltransduction pathway. Curr. Biol. 18,1215–1220.

9. Tay, S.Y., Ingham, P.W., and Roy, S. (2005).A homologue of the Drosophila kinesin-likeprotein Costal2 regulates Hedgehog signaltransduction in the vertebrate embryo.Development 132, 625–634.

10. Varjosalo, M., Li, S.P., and Taipale, J. (2006).Divergence of hedgehog signal transductionmechanism between Drosophila and mammals.Dev. Cell 10, 177–186.

11. Wolff, C., Roy, S., and Ingham, P.W. (2003).Multiple muscle cell identities induced bydistinct levels and timing of hedgehog activityin the zebrafish embryo. Curr. Biol. 13,1169–1181.

12. Chen, M.H., Gao, N., Kawakami, T., andChuang, P.T. (2005). Mice deficient in thefused homolog do not exhibit phenotypesindicative of perturbed hedgehog signalingduring embryonic development. Mol. CellBiol. 25, 7042–7053.

13. Merchant, M., Evangelista, M., Luoh, S.M.,Frantz, G.D., Chalasani, S., Carano, R.A.,van Hoy, M., Ramirez, J., Ogasawara, A.K.,McFarland, L.M., et al. (2005). Loss of theserine/threonine kinase fused results inpostnatal growth defects and lethality due toprogressive hydrocephalus. Mol. Cell Biol. 25,7054–7068.

14. Svard, J., Heby-Henricson, K., Persson-Lek, M.,Rozell, B., Lauth, M., Bergstrom, A., Ericson, J.,Toftgard, R., and Teglund, S. (2006). Geneticelimination of Suppressor of fused reveals anessential repressor function in the mammalianHedgehog signaling pathway. Dev. Cell 10,187–197.

15. Lunt, S.C., Haynes, T., and Perkins, B.D. (2009).Zebrafish ift57, ift88, and ift172 intraflagellartransport mutants disrupt cilia but do notaffect hedgehog signaling. Dev. Dyn. 238,1744–1759.

16. Aanstad, P., Santos, N., Corbit, K.C.,Scherz, P.J., Trinh le, A., Salvenmoser, W.,Huisken, J., Reiter, J.F., and Stainier, D.Y.(2009). The extracellular domain ofSmoothened regulates ciliary localizationand is required for high-level Hh signaling.Curr. Biol. 19, 1034–1039.

17. Litingtung, Y., Dahn, R.D., Li, Y., Fallon, J.F.,and Chiang, C. (2002). Shh and Gli3 aredispensable for limb skeleton formation butregulate digit number and identity. Nature418, 979–983.

18. Haycraft, C.J., Banizs, B., Aydin-Son, Y.,Zhang, Q., Michaud, E.J., and Yoder, B.K.(2005). Gli2 and Gli3 localize to cilia and requirethe intraflagellar transport protein polaris forprocessing and function. PLoS Genet. 1, e53.

19. Jia, J., Kolterud, A., Zeng, H., Hoover, A.,Teglund, S., Toftgard, R., and Liu, A. (2009).Suppressor of Fused inhibits mammalianHedgehog signaling in the absence of cilia.Dev. Biol. 330, 452–460.

20. Collier, L.S., Suyama, K., Anderson, J.H., andScott, M.P. (2004). Drosophila Costal1mutations are alleles of protein kinase A thatmodulate hedgehog signaling. Genetics 167,783–796.

1Institute of Molecular and Cellular Biology,61, Biopolis Drive, Proteos, Singapore.2Departments of Stem cell and RegenerativeBiology, and Molecular and Cellular Biology,Harvard Stem Cell Institute, HarvardUniversity, 16, Divinity Avenue, Cambridge,MA 02138, USA.E-mail: pingham@imcb.a-star.edu.sg,amcmahon@mcb.harvard.edu

DOI: 10.1016/j.cub.2009.07.060

DispatchR731

Animal Cognition: Aesop’s Fable Fliesfrom Fiction to Fact

A new study shows that rooks are able to spontaneously drop stones into a tubeof water to obtain a floating worm. This sophisticated problem solving raisesintriguing questions about the use of imagination in animals.

Alex H. Taylor and Russell D. Gray

Do Aesop’s fables (Figure 1) reflect thebehaviour of real animals? While talkingfoxes and racing tortoises may beunlikely, Bird and Emery’s recentfindings suggest there may be a kernelof truth to one of Aesop’s most famousstories. In the fable of the crow and thepitcher, a clever crow drops stones intoa jug of water in order to raise the leveland ease its thirst (Figure 1) [1]. Therooks in the experiment reportedrecently in Current Biology by Birdand Emery [2] did something strikinglysimilar — they dropped stones intoa tube of water in order to bring afloating worm within reach. Two of

the four rooks tested were able tospontaneously solve this problem onthe first trial. The rooks were thenable to rapidly learn to drop bigstones, rather than small ones, intothe tube. They also rapidly learntto drop stones only into tubescontaining water, and not thosecontaining sawdust.

At first glance, the way the birdssolved these tasks seems remarkablyinsightful and human-like. The rooksonly put in sufficient stones to bringthe worm within reach, and then didnot continue to add stones once theworm had been removed. The rooksalso appeared to examine the problembefore putting stones into the tube,

consistent with the idea that theyinitially assessed the task. Oneinterpretation of these results is thatthe rooks had immediate causalknowledge of the task [3]. That is,they understood how the stoneswould interact with the water andtherefore could estimate how highthe water would rise once a certainnumber of stones were put into thetube. As the fable tells it, the crowput the stones into the pitcherbecause it knew that this wouldcause the water level to rise.

However, the follow-up experimentspreclude the use of such human-likecausal knowledge. If the rooks hadunderstood how stones interact withwater they should have also knownthat bigger stones would displace morewater. In contrast to this expectation,the rooks did not immediately use largestones when presented with a choicebetween small and large stones,although they quickly learnt to do so.The rooks also did not seem to haveknowledge of the peculiar causal

Current Biology Vol 19 No 17R732

characteristics of water. Whenpresented with a choice betweena tube with water and one withsawdust, the rooks had to learnto choose the water-filled tube. Thefollow-up experiments carried out byBird and Emery [2] therefore exemplifythe common paradox found in studiesof animal cognition. Animals canbehave in apparently complex waysthat lead us to believe they havecognitive abilities just like us.But when we start to probe theirperformance with more revealingtasks, they make mistakes that indicatethat they are solving these tasks usingsimpler cognitive mechanisms. Whatexactly, then, were the rooks thinkingwhen they solved the problem?

In the past, spontaneous problemsolving has been suggested to bebased on ‘insight’, a rather murkyterm that has both folk meaning inhuman language and several technicaldefinitions. Thorpe’s [4] commonlycited definition of insight is, ‘‘thesudden production of new adaptiveresponses not arrived at by trialbehaviour or the solution toa problem by the sudden adaptivereorganization of experience’’.However, use of this term leavesus with a cognitive black box. Whatkind of cognitive mechanisms allowthe sudden reorganisation experience?How does the animal know that thisreorganisation is adaptive?

A related idea that avoids suchvagaries is Dennett’s [5] conception

Figure 1. In Aesop’s fable of ‘‘The Crow andthe Pitcher’’, the thirsty crow drops stonesinto a jug of water in order to raise the leveland ease its thirst. From [1].

of a ‘Popperian creature’. Accordingto Dennett, Popperian creatureshave imagination and so can mentallysimulate the real world and the causalregularities in it. Thus, when thesecreatures are faced with a novelproblem, they can engage in a processof mental conjectures and refutationsto try out various solutions. Given theresults of experiments 2 and 3 of Birdand Emery [2], it seems unlikely thatthe rooks were using such complexcognition. As the crows did notunderstand the differential effects oflarge and small stones on water, orthe effects of stones on water andsawdust, it seems likely that they didnot imagine how the stone wouldinteract with the water before theydropped the stone into the water forthe first time. Thus, the riddle of exactlyhow they managed to spontaneouslysolve the problem without trialand error learning still remains.

An alternative explanation for thespontaneous problem solving residesin the rooks’ previous experience.The birds in this experiment all hadpreviously dropped stones into a tubewith a platform in order to collapse itand release food [6]. On their first trialwith the new experiment they couldhave generalised this past experienceto the new apparatus and dropped thestone down the water-filled tube. Thestone dropping had a positive effect:the water rose and the worm movedcloser. This would have reinforced thestone-dropping behaviour and so setup a perceptual-motor feedback cycle.The crows therefore continued to putstones into the tube until the wormrose within reach. Perceptual-motorfeedback cycles of this type mayalso be able to explain other casesof apparently insightful problemsolving in birds, such as spontaneousstring pulling to obtain foodin ravens [7] and keas [8].

What about our close primaterelatives? Orangutans have recentlybeen shown capable of solving a verysimilar problem to the one Bird andEmery [2] presented to the rooks.Mendes et al. [9] presented orangutanswith a tube quarter-filled with water.Floating on the surface of the waterwas a peanut. To solve the problemthe apes needed to collect water froma drinking container in their mouths andspit it into the tube in order to raise thewater level and gain the peanut. Aftertrying to reach the peanut with theirfingers or mouths, the orangutans spat

water into the tube in order to raise thelevel and so gain the reward on the firsttrial. Interestingly, the apes also solveda control task where there was no waterin the tube, which suggests that thesight of water was not necessary forthe solution of the problem. However,as the apes were already experiencedwater spitters, testing with naı̈veindividuals is needed to confirmthis conclusion.

The crucial issue for theinterpretation of the orangutan problemsolving is the first spitting attempt. AsMendes et al. [9] note, it is unclear if theapes spat the water, saw the effect ithad on the peanut and then repeated it,or if the apes had fully formed thesolution to the problem in their mindsbefore spitting the first mouthful. Inother words, was this a randomlygenerated behaviour that was thenreinforced, or did the apes imaginethe solution and so seek out the waterin order to spit into the tube? Giventhe novelty of the task and the factthat the apes had never used waterto solve other problems, the evidencefor imagination is stronger than thatin the rook study. However, the futureexperiments with opaque tubes andnaı̈ve subjects proposed by Bird andEmery could provide more compellingevidence for imagination in corvids.

References1. Aesop, The Aesop for Children, Illustration by

Milo Winter, Project Gutenberg etext 19994,http://www.gutenberg.org/etext/19994.

2. Bird, C.D., and Emery, N.J. (2009). Rooks usestones to raise the water level to reach a floatingworm. Curr. Biol. 19, 1410–1414.

3. Kummer, H. (1995). Causal knowledge inanimals. In Causal Cognition. A MultidisciplinaryDebate, D. Sperber, D. Premack, andA.J. Premack, eds. (Oxford, UK: ClarendonPress), pp. 26–39.

4. Thorpe, W.H. (1964). Learning and Instinct inAnimals (London: Methuen).

5. Dennett, D.C. (1996). Kinds of Minds: Toward anUnderstanding of Consciousness. (New York:Harper Collins/Basic Books).

6. Bird, C.D., and Emery, N.J. (2009). Insightfulproblem solving and creative tool modificationby captive nontool-using rooks. Proc. Natl.Acad. Sci. USA 106, 10370–10375.

7. Heinrich, B. (1995). An experimentalinvestigation of insight in ravens (Corvus corax).Auk. 112, 994–1003.

8. Werdenich, D., and Huber, L. (2006). A case ofquick problem solving in birds: string-pulling inkeas (Nestor notabilis). Anim. Behav. 71,855–863.

9. Mendes, N., Hanus, D., and Call, J. (2007).Raising the level: orangutans use water as a tool.Biol. Lett. 3, 453–455.

Department of Psychology, University ofAuckland, Auckland 1142, New Zealand.E-mail: rd.gray@auckland.ac.nz

DOI: 10.1016/j.cub.2009.07.055