Dispatch R869

Lars Chittka and Ellouise Leadbeater

The rapid expansion of the field ofsocial learning in recent decades[1,2] has almost entirely bypassedthe insects. Yet, a closeinspection of the literature revealsnumerous cases where insectsappear to learn by observation,eavesdrop on members of thesame or different species, andeven engage in teaching othermembers of a society. In fact, thefirst hint of observatory learningby animals dates back to Darwin’sfield notes published by Romanes[3,4]. Darwin suggested thathoneybees learn the art of nectarrobbing — extracting nectar fromflowers via holes bitten into thetubes, without touching theflower’s reproductive organs — byobserving bumblebees engaged inthe activity. Experimental proof forthis conjecture remainsoutstanding, but it is interesting tonote that Darwin thought thatobservatory learning might occuracross, rather than within, species(Figure 1). This deserves moreconsideration, and we will returnto it later.

Early in the 20th century,researchers became aware thatmany adult phytophagous insectsprefer host species that theythemselves had fed on when theywere larvae — even where theinsect species, as a whole, was ageneralist with multipleacceptable hosts [5]. In what hasbecome known as Hopkins’ hostselection principle, it was thoughtthat the larvae becomeconditioned to the chemosensorycues associated with foodprovided by their parents [6]. Thisis a non-trivial suggestion, as thenervous system of a

holometabolous insect isextensively rearranged andrewired during metamorphosis [7];nevertheless, there have beenconvincing studies to show thatsuch pre-imaginal conditioningindeed occurs [8]. This shows thatinsect parents can pass onvaluable information aboutsuitable food types to theiroffspring, simply by placing eggson suitable host plants, or byprovisioning eggs with certainfood types [9]. In a similar vein,Kirchner and Lindauer [10]considered the possibility of‘traditions’ being established inhoneybees colonies. Foragers canbe trained to feed at a certain timeof day, and it was shown thatthese learnt temporal preferencesare picked up by larvae viavibratory cues. The individuals sotaught will display the samepreferences when theythemselves become foragers.

One of the most spectacularexamples of social learning occursin the honeybee dances. Insidethe darkness of the hive,successful foragers display aseries of stereotypical motorbehaviours which inform otherforagers of the precise location offloral food, up to severalkilometres away from the hive[11]. Dancers essentially ‘teach’recruits by putting them through asymbolised version of the ‘real life’flight to the food source. Recruitsmemorise and decode theinformation delivered in thedances, and subsequently applyon the flight to the indicated foodsource [11]. Note that thisconstitutes a form of observatory(unrewarded) learning: whiledancers occasionally give foodsamples to recruits byregurgitating food [11], these food

samples are not a prerequisite forsuccessful informationtransmission (T. Seeley, personalcommunication). Such mouth-to-mouth contacts between bees,however, serve another function inthe context of social learning:successful foragers can teachtheir nestmates the scent of thefood they have located [12].

With the exception of Darwin’ssuggestion that honeybees mightcopy bad habits frombumblebees, the examples aboveare all cases where thetransmission of information is ofmutual interest, for examplebetween parents and offspring, orbetween members of a colony ofrelated individuals. A recent focusin social influences on learning,however, concerns cases whereindividuals inadvertently leavecues that can be used as publiclyavailable information by otherindividuals for adaptive behaviour[2]. A relatively simple form is localenhancement, where animals aredrawn to sites where conspecificsare present [1]. The newcomersmay then learn, on their own, thatthe site contains valuable food, forexample in Vespid wasps [13].Bumblebees are attracted tomembers of the same specieswhen they scout for a novel flowerspecies [14], and can learn aboutsuitable food sources by

Although it has received less coverage than in vertebrates, the study ofinsect social learning has a rich history with spectacular examples ofhow individuals extract knowledge from other animals. Several newstudies on crickets and social bees have now shown how insects canadjust their behaviour adaptively by making use of cues generatedinadvertently by other individuals.

Figure 1. Learning from other species?

Darwin suggested that honeybees mightlearn from bumblebees not just whichflowers to visit, but also might imitate theparticular motor patterns to best extractthe nectar, via observatory learning.(Photo by J. Spaethe.)

Dispatches

Social Learning: Public Information in Insects

observatory learning fromunrelated individuals, without thenecessity of direct interaction withthese individuals, and without thepresence of rewards [15]. Thismeans that bees, by observing theactivities of other foragers, canbypass the substantial costs ofexploring multiple food sourcesby individual initiative [16].

In this issue of Current Biology,Isabelle Coolen and co-workers[17] report for the first time thatinsects can use public informationto learn about danger, too(Figure 2). In an elegant set ofexperiments, Coolen et al. [17]made use of the hiding responsethat juvenile wood crickets showin the presence of a naturalpredator, the wolf spider.Observer crickets were placed inleaf-filled boxes accompanied byconspecifics that had eitherrecently experienced a high spiderpredation threat, and wereaccordingly tending to hide underthe leaves, or that had had norecent interactions with predators.After 6 hours, observers whosecompanions had been exposed tothe dangerous environment werethemselves more likely to befound hiding than those whosecompanions had no recent spiderexperience. As the observercrickets had no direct interactionwith spiders themselves, nor withany material which had been incontact with them, this hiding

behaviour could only have beenelicited through their ‘fearful’conspecifics. The most novelaspect of this study, however,occurred when the authors thenremoved all demonstrator cricketsfrom the boxes, and found thatthese behavioural differencescould still be observed even24 hours later. Rather than simplyhiding when others were hiding,the observer crickets continued tobe careful even after their‘knowledgeable’ companions hadbeen taken away, suggesting thatthey had learnt indirectly aboutthe danger level in theirsurroundings.

If crickets usually take a longtime to emerge from hiding, thesefindings could be explainedwithout invoking social learning.But when Coolen et al. [17]simulated a stressful, but notpredatory, event in a controlexperiment, crickets re-emergedwithin 45 min. Furthermore,observer crickets did not showincreased hiding behaviour whenseparated from demonstrators bya partition allowing pheromoneexchange but no visual contact, orwhen placed in boxes that hadpreviously contained crickets indanger from spiders. Intriguingly,rather than simply inducing ahiding response, the behaviour ofthe fearful demonstrator cricketsmust have provided their naïvecompanions with an indirect

assessment of a local predationthreat — information which mayundoubtedly be costly to ignore.

That the first cleardemonstration of the use of publicinformation about danger ininsects was made with a non-colonial species that is notassociated with complex socialbonds serves only to emphasise,as Coolen et al. [17] point out, thatlearning from others can beadaptive even when individualsare unrelated, and as Darwinsuggested, potentially even whenthey belong to different species.The possibility that animals canobtain useful information from thebehaviour of other species is littleconsidered (but see [18,19]).

Information about water andfood availability, food toxicity,predator threats, etc. will often beof relevance for more than onespecies, and animals would dowell to use public informationfrom members of other species.Humans, for example, willcertainly have benefited from suchobservations in evolutionary time.In the 1974 film Animals arebeautiful people, for example,Kalahari tribesmen use clevertechniques to extract frombaboons the information abouthidden access to water reserves –essentially by overfeeding thebaboons with salt, then followingthem after release as they rush tothe water. Turning to insects,Trigona stingless bees engage inespionage of the scent trails ofother bee species to a rich foodsource, and subsequently takeover that food source by drivingaway or even killing theircompetitors [20]. It remains to bedetermined whether thisbehaviour is learnt, or a form ofinter-specific local enhancement.

One of the authors of thisdispatch, in his preschool years,attempted to levitate by flappinghis arms after observing ducks inthe park, and to increase hisrunning speed by imitating thesound of a galloping horse.Neither of these producedsatisfactory results, indicating tothis author that birds and equineswere not suitable role models forlocomotion. But the suggestionhere is this: some animals mightbe relatively flexible in what other

Current Biology Vol 15 No 21R870

Figure 2. A lonely cricket in trouble.

In this issue, Coolen et al. [17] report that this cricket could well have avoided itsimpending death — if only it had observed how conspecifics respond to predationthreat. (Photo by O. Dangles.)

animals they copy, andsubsequently evaluate theusefulness of the copiedbehaviour, or the usefulness ofthe particular model in general.The study of heterospecificinformation transfer could thus bea useful avenue of futureresearch, in both insects and theless successful other animals thatpopulate the planet.

References1. Galef, B.G., and Laland, K.N. (2005).

Social learning in animals: Empiricalstudies and theoretical models.Bioscience 55, 489–499.

2. Danchin, E., Giraldeau, L.A., Valone, T.J.,and Wagner, R.H. (2004). Publicinformation: From nosy neighbors tocultural evolution. Science 305, 487–491.

3. Romanes, G.J. (1884). Mental evolutionin animals (New York: AMS Press).

4. Galef, B.G. (1996). Introduction. In Sociallearning in animals, C.M. Heynes andB.G. Galef, eds. (San Diego: AcademicPress).

5. Hopkins, A.D. (1917). A discussion ofC.G.Hewitt’s paper on ‘Insect Behavior’.J. Econ. Entomol. 10, 92–93.

6. Barron, A.B. (2001). The life and death ofHopkins’ host-selection principle. J.

Insect Behav. 14, 725–737.7. Technau, G., and Heisenberg, M. (1982).

Neural reorganization duringmetamorphosis of the corporapedunculata in Drosophila melanogaster.Nature 295, 405–407.

8. Tully, T., Cambiazo, V., and Kruse, L.(1994). Memory through metamorphosisin normal and mutant Drosophila. J.Neurosci. 14, 68–74.

9. Williams, N.M. (2003). Use of novel pollenspecies by specialist and generalistsolitary bees (Hymenoptera:Megachilidae). Oecologia 134, 228–237.

10. Kirchner, W.H. (1987). Tradition imBienenstaat. Kommunikation zwischenImagines und der Brut der Honigbienedurch Vibrationssignale. PhD Thesis,Wuerzburg University, supervised by M.Lindauer.

11. v Frisch, K. (1967). The dance languageand orientation of bees (Cambridge:Harvard Univ. Press).

12. Farina, W.M., Grueter, C., and Diaz, P.C.(2005). Social learning of floral odoursinside the honeybee hive. Proc. R. Soc.Lond. B. Biol. Sci. 272, 1923–1928.

13. D’Adamo, P., and Lozada, M. (2005).Conspecific and food attraction in thewasp Vespula germanica (Hymenoptera:Vespidae), and their possiblecontributions to control. Ann. Entomol.Soc. Am. 98, 236–240.

14. Leadbeater, E., and Chittka, L. (2005). Anew mode of information transfer inforaging bumblebees? Curr. Biol. 15,R447–R448.

15. Worden, B.D., and Papaj, D.R. (2005).Flower choice copying in bumblebees.Biology Letters DOI:10.1098/rsbl.2005.0368.

16. Chittka, L., Thomson, J.D., and Waser,N.M. (1999). Flower constancy, insectpsychology, and plant evolution.Naturwiss. 86, 361–377.

17. Coolen, I., Dangles, O., and Casas, J.(2005). Social learning in non-colonialinsects? Curr. Biol. 15, this issue.

18. Parejo, D., Danchin, E., and Aviles, J.M.(2005). The heterospecific habitatcopying hypothesis: can competitorsindicate habitat quality? Behav. Ecol. 16,96–105.

19. Rainey, H.J., Zuberbuhler, K., and Slater,P.J.B. (2004). The responses of black-casqued hornbills to predatorvocalisations and primate alarm calls.Behaviour 141, 1263–1277.

20. Nieh, J.C., Barreto, L.S., Contrera, F.A.L.,and Imperatriz-Fonseca, V.L. (2004).Olfactory eavesdropping by acompetitively foraging stingless bee,Trigona spinipes. Proc. R. Soc. Lond. B.Biol. Sci. 271, 1633–1640.

School of Biological and ChemicalSciences, Queen Mary University ofLondon, Mile End Road, London E14NS, UK.

DOI: 10.1016/j.cub.2005.10.018

Dispatch R871

Patricia Wadsworth

When a eukaryotic cell divides,within minutes of anaphasechromosome motion the corticalcytoplasm begins to ingress at alocation overlying the positionpreviously occupied by thechromosomes at metaphase. Theremarkable ability of cells tospecify the site of contractile ringformation so precisely hasfascinated and frustratedbiologists for decades. New work[1–3] has now shown that activeRhoA forms a narrow zone at thesite where the contractile ring willform, and identified the RhoGTPase-activating protein(RhoGAP) component of thecentralspindlin complex and theGTP exchange factor for RhoA askey players in the activation ofRhoA.

Microtubules Specify the Site ofContractile Ring FormationIt has long been recognized thatsome component(s) of the mitoticspindle plays a key role indetermining the site of cleavagefurrow formation when aeukaryotic cell divides. Supportfor the idea that the spindledelivers a signal to the cortex hascome from experiments in whichthe spindle was repeatedlyrepositioned in an artificiallyelongated embryonic echinodermcell [4]. The results showed thatmultiple furrows can besequentially specified,demonstrating that the cortex ofthe anaphase cell is globallycompetent to furrow, providedthat the appropriate signal isdelivered and received.Micromanipulation experiments,also performed in echinoderm

blastomeres, showed that twoastral arrays of microtubules,lacking intervening chromosomes,are sufficient to generate thesignal for furrowing [4].

Subsequent work inmammalian and Drosophila cells,in which the geometry of spindle,asters and cortex differs fromthat in large, spherical embryoniccells, suggested that interzonal,not astral, microtubules arerequired for cytokinesis [5]. Giventhese conflicting results, mucheffort has been focused ondetermining which class, orclasses, of microtubules areresponsible for furrow induction.It is now generally agreed thatmicrotubules are the onlystructural component needed forfurrow induction [6], and that theclass, or classes, of microtubulesthat are required depends on celltype. In some cases, twosequential signals from astraland interzonal microtubules areused [5,7]. The finding thatdifferent arrangements ofmicrotubules contribute tospecification of furrowing indifferent organisms and thatmultiple signals may participate

Cytokinesis: Rho Marks the Spot

During cytokinesis of a eukaryotic cell, following the chromosomemovements of anaphase, a contractile ring forms in the cortex midwaybetween the segregating chromosomes and divides the cell into twodaughters. Recent studies have provided new insights into themechanism by which the site of contractile ring assembly is specified.