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Social Learning: Public Information in Insects

2005; Elsevier BV; Volume: 15; Issue: 21 Linguagem: Inglês

10.1016/j.cub.2005.10.018

1879-0445

Lars Chittka, Ellouise Leadbeater,

Animal Behavior and Reproduction

Although it has received less coverage than in vertebrates, the study of insect social learning has a rich history with spectacular examples of how individuals extract knowledge from other animals. Several new studies on crickets and social bees have now shown how insects can adjust their behaviour adaptively by making use of cues generated inadvertently by other individuals. Although it has received less coverage than in vertebrates, the study of insect social learning has a rich history with spectacular examples of how individuals extract knowledge from other animals. Several new studies on crickets and social bees have now shown how insects can adjust their behaviour adaptively by making use of cues generated inadvertently by other individuals. The rapid expansion of the field of social learning in recent decades [1Galef B.G. Laland K.N. Social learning in animals: Empirical studies and theoretical models.Bioscience. 2005; 55: 489-499Crossref Scopus (403) Google Scholar, 2Danchin E. Giraldeau L.A. Valone T.J. Wagner R.H. Public information: From nosy neighbors to cultural evolution.Science. 2004; 305: 487-491Crossref PubMed Scopus (1008) Google Scholar] has almost entirely bypassed the insects. Yet, a close inspection of the literature reveals numerous cases where insects appear to learn by observation, eavesdrop on members of the same or different species, and even engage in teaching other members of a society. In fact, the first hint of observatory learning by animals dates back to Darwin's field notes published by Romanes [3Romanes G.J. Mental evolution in animals. AMS Press, New York1884Google Scholar, 4Galef B.G. Introduction.in: Heynes C.M. Galef B.G. Social learning in animals. Academic Press, San Diego1996Google Scholar]. Darwin suggested that honeybees learn the art of nectar robbing — extracting nectar from flowers via holes bitten into the tubes, without touching the flower's reproductive organs — by observing bumblebees engaged in the activity. Experimental proof for this conjecture remains outstanding, but it is interesting to note that Darwin thought that observatory learning might occur across, rather than within, species (Figure 1). This deserves more consideration, and we will return to it later. Early in the 20th century, researchers became aware that many adult phytophagous insects prefer host species that they themselves had fed on when they were larvae — even where the insect species, as a whole, was a generalist with multiple acceptable hosts [5Hopkins A.D. A discussion of C.G.Hewitt's paper on 'Insect Behavior'.J. Econ. Entomol. 1917; 10: 92-93Google Scholar]. In what has become known as Hopkins' host selection principle, it was thought that the larvae become conditioned to the chemosensory cues associated with food provided by their parents [6Barron A.B. The life and death of Hopkins' host-selection principle.J. Insect Behav. 2001; 14: 725-737Crossref Scopus (201) Google Scholar]. This is a non-trivial suggestion, as the nervous system of a holometabolous insect is extensively rearranged and rewired during metamorphosis [7Technau G. Heisenberg M. Neural reorganization during metamorphosis of the corpora pedunculata in Drosophila-melanogaster.Nature. 1982; 295: 405-407Crossref PubMed Scopus (206) Google Scholar]; nevertheless, there have been convincing studies to show that such pre-imaginal conditioning indeed occurs [8Tully T. Cambiazo V. Kruse L. Memory through metamorphosis in normal and mutant Drosophila.J. Neurosci. 1994; 14: 68-74PubMed Google Scholar]. This shows that insect parents can pass on valuable information about suitable food types to their offspring, simply by placing eggs on suitable host plants, or by provisioning eggs with certain food types [9Williams N.M. Use of novel pollen species by specialist and generalist solitary bees (Hymenoptera: Megachilidae).Oecologia. 2003; 134: 228-237PubMed Google Scholar]. In a similar vein, Kirchner and Lindauer [10Kirchner, W.H. (1987). Tradition im Bienenstaat. Kommunikation zwischen Imagines und der Brut der Honigbiene durch Vibrationssignale. PhD Thesis, Wuerzburg University, supervised by M. Lindauer.Google Scholar] considered the possibility of 'traditions' being established in honeybees colonies. Foragers can be trained to feed at a certain time of day, and it was shown that these learnt temporal preferences are picked up by larvae via vibratory cues. The individuals so taught will display the same preferences when they themselves become foragers. One of the most spectacular examples of social learning occurs in the honeybee dances. Inside the darkness of the hive, successful foragers display a series of stereotypical motor behaviours which inform other foragers of the precise location of floral food, up to several kilometres away from the hive [11v Frisch K. The dance language and orientation of bees. Harvard Univ. Press, Cambridge1967Google Scholar]. Dancers essentially 'teach' recruits by putting them through a symbolised version of the 'real life' flight to the food source. Recruits memorise and decode the information delivered in the dances, and subsequently apply on the flight to the indicated food source [11v Frisch K. The dance language and orientation of bees. Harvard Univ. Press, Cambridge1967Google Scholar]. Note that this constitutes a form of observatory (unrewarded) learning: while dancers occasionally give food samples to recruits by regurgitating food [11v Frisch K. The dance language and orientation of bees. Harvard Univ. Press, Cambridge1967Google Scholar], these food samples are not a prerequisite for successful information transmission (T. Seeley, personal communication). Such mouth-to-mouth contacts between bees, however, serve another function in the context of social learning: successful foragers can teach their nestmates the scent of the food they have located [12Farina W.M. Grueter C. Diaz P.C. Social learning of floral odours inside the honeybee hive.Proc. R. Soc. Lond. B. Biol. Sci. 2005; 272: 1923-1928Crossref Scopus (122) Google Scholar]. With the exception of Darwin's suggestion that honeybees might copy bad habits from bumblebees, the examples above are all cases where the transmission of information is of mutual interest, for example between parents and offspring, or between members of a colony of related individuals. A recent focus in social influences on learning, however, concerns cases where individuals inadvertently leave cues that can be used as publicly available information by other individuals for adaptive behaviour [2Danchin E. Giraldeau L.A. Valone T.J. Wagner R.H. Public information: From nosy neighbors to cultural evolution.Science. 2004; 305: 487-491Crossref PubMed Scopus (1008) Google Scholar]. A relatively simple form is local enhancement, where animals are drawn to sites where conspecifics are present [1Galef B.G. Laland K.N. Social learning in animals: Empirical studies and theoretical models.Bioscience. 2005; 55: 489-499Crossref Scopus (403) Google Scholar]. The newcomers may then learn, on their own, that the site contains valuable food, for example in Vespid wasps [13D'Adamo P. Lozada M. Conspecific and food attraction in the wasp Vespula germanica (Hymenoptera: Vespidae), and their possible contributions to control.Ann. Entomol. Soc. Am. 2005; 98: 236-240Crossref Scopus (24) Google Scholar]. Bumblebees are attracted to members of the same species when they scout for a novel flower species [14Leadbeater E. Chittka L. A new mode of information transfer in foraging bumblebees?.Curr. Biol. 2005; 15: R447-R448Abstract Full Text Full Text PDF PubMed Scopus (79) Google Scholar], and can learn about suitable food sources by observatory learning from unrelated individuals, without the necessity of direct interaction with these individuals, and without the presence of rewards [15Worden, B.D., and Papaj, D.R. (2005). Flower choice copying in bumblebees. Biology Letters DOI: 10.1098/rsbl.2005.0368.Google Scholar]. This means that bees, by observing the activities of other foragers, can bypass the substantial costs of exploring multiple food sources by individual initiative [16Chittka L. Thomson J.D. Waser N.M. Flower constancy, insect psychology, and plant evolution.Naturwiss. 1999; 86: 361-377Crossref Scopus (456) Google Scholar]. In this issue of Current Biology, Isabelle Coolen and co-workers [17Coolen I. Dangles O. Casas J. Social learning in non-colonial insects?.Curr. Biol. 2005; 15 (this issue)Abstract Full Text Full Text PDF PubMed Scopus (85) Google Scholar] report for the first time that insects can use public information to learn about danger, too (Figure2). In an elegant set of experiments, Coolen et al. [17Coolen I. Dangles O. Casas J. Social learning in non-colonial insects?.Curr. Biol. 2005; 15 (this issue)Abstract Full Text Full Text PDF PubMed Scopus (85) Google Scholar] made use of the hiding response that juvenile wood crickets show in the presence of a natural predator, the wolf spider. Observer crickets were placed in leaf-filled boxes accompanied by conspecifics that had either recently experienced a high spider predation threat, and were accordingly tending to hide under the leaves, or that had had no recent interactions with predators. After 6 hours, observers whose companions had been exposed to the dangerous environment were themselves more likely to be found hiding than those whose companions had no recent spider experience. As the observer crickets had no direct interaction with spiders themselves, nor with any material which had been in contact with them, this hiding behaviour could only have been elicited through their 'fearful' conspecifics. The most novel aspect of this study, however, occurred when the authors then removed all demonstrator crickets from the boxes, and found that these behavioural differences could still be observed even 24hours later. Rather than simply hiding when others were hiding, the observer crickets continued to be careful even after their 'knowledgeable' companions had been taken away, suggesting that they had learnt indirectly about the danger level in their surroundings. If crickets usually take a long time to emerge from hiding, these findings could be explained without invoking social learning. But when Coolen et al. [17Coolen I. Dangles O. Casas J. Social learning in non-colonial insects?.Curr. Biol. 2005; 15 (this issue)Abstract Full Text Full Text PDF PubMed Scopus (85) Google Scholar] simulated a stressful, but not predatory, event in a control experiment, crickets re-emerged within 45 min. Furthermore, observer crickets did not show increased hiding behaviour when separated from demonstrators by a partition allowing pheromone exchange but no visual contact, or when placed in boxes that had previously contained crickets in danger from spiders. Intriguingly, rather than simply inducing a hiding response, the behaviour of the fearful demonstrator crickets must have provided their naïve companions with an indirect assessment of a local predation threat — information which may undoubtedly be costly to ignore. That the first clear demonstration of the use of public information about danger in insects was made with a non-colonial species that is not associated with complex social bonds serves only to emphasise, as Coolen et al. [17Coolen I. Dangles O. Casas J. Social learning in non-colonial insects?.Curr. Biol. 2005; 15 (this issue)Abstract Full Text Full Text PDF PubMed Scopus (85) Google Scholar] point out, that learning from others can be adaptive even when individuals are unrelated, and as Darwin suggested, potentially even when they belong to different species. The possibility that animals can obtain useful information from the behaviour of other species is little considered (but see [18Parejo D. Danchin E. Aviles J.M. The heterospecific habitat copying hypothesis: can competitors indicate habitat quality?.Behav. Ecol. 2005; 16: 96-105Crossref Scopus (101) Google Scholar, 19Rainey H.J. Zuberbuhler K. Slater P.J.B. The responses of black-casqued hornbills to predator vocalisations and primate alarm calls.Behaviour. 2004; 141: 1263-1277Crossref Scopus (41) Google Scholar]). Information about water and food availability, food toxicity, predator threats, etc. will often be of relevance for more than one species, and animals would do well to use public information from members of other species. Humans, for example, will certainly have benefited from such observations in evolutionary time. In the 1974 film Animals are beautiful people, for example, Kalahari tribesmen use clever techniques to extract from baboons the information about hidden access to water reserves – essentially by overfeeding the baboons with salt, then following them after release as they rush to the water. Turning to insects, Trigona stingless bees engage in espionage of the scent trails of other bee species to a rich food source, and subsequently take over that food source by driving away or even killing their competitors [20Nieh J.C. Barreto L.S. Contrera F.A.L. Imperatriz-Fonseca V.L. Olfactory eavesdropping by a competitively foraging stingless bee, Trigona spinipes.Proc. R. Soc. Lond. B. Biol. Sci. 2004; 271: 1633-1640Crossref Scopus (65) Google Scholar]. It remains to be determined whether this behaviour is learnt, or a form of inter-specific local enhancement. One of the authors of this dispatch, in his preschool years, attempted to levitate by flapping his arms after observing ducks in the park, and to increase his running speed by imitating the sound of a galloping horse. Neither of these produced satisfactory results, indicating to this author that birds and equines were not suitable role models for locomotion. But the suggestion here is this: some animals might be relatively flexible in what other animals they copy, and subsequently evaluate the usefulness of the copied behaviour, or the usefulness of the particular model in general. The study of heterospecific information transfer could thus be a useful avenue of future research, in both insects and the less successful other animals that populate the planet.