No evidence of social learning in a socially roosting butterfly in an associative learning task

Insects may acquire social information by active communication and through inadvertent social cues. In a foraging setting, the latter may indicate the presence and quality of resources. Although social learning in foraging contexts is prevalent in eusocial species, this behaviour has been hypothesized to also exist between conspecifics in non-social species with sophisticated behaviours, including Heliconius butterflies. Heliconius are the only butterfly genus with active pollen feeding, a dietary innovation associated with a specialized, spatially faithful foraging behaviour known as trap-lining. Long-standing hypotheses suggest that Heliconius may acquire trap-line information by following experienced individuals. Indeed, Heliconius often aggregate in social roosts, which could act as ‘information centres’, and present conspecific following behaviour, enhancing opportunities for social learning. Here, we provide a direct test of social learning ability in Heliconius using an associative learning task in which naive individuals completed a colour preference test in the presence of demonstrators trained to feed randomly or with a strong colour preference. We found no evidence that Heliconius erato, which roost socially, used social information in this task. Combined with existing field studies, our results add to data which contradict the hypothesized role of social learning in Heliconius foraging behaviour.

[1]  S. Montgomery,et al.  True site fidelity in pollen feeding butterflies , 2021, Functional Ecology.

[2]  C. Nieberding,et al.  The Evolutionary Relevance of Social Learning and Transmission in Non-Social Arthropods with a Focus on Oviposition-Related Behaviors , 2021, Genes.

[3]  S. Montgomery,et al.  Pollen feeding in Heliconius butterflies: the singular evolution of an adaptive suite , 2020, Proceedings of the Royal Society B.

[4]  M. Mizunami,et al.  Appetitive and aversive social learning with living and dead conspecifics in crickets , 2020, Scientific Reports.

[5]  S. Montgomery,et al.  Heliconiini butterflies can learn time-dependent reward associations , 2020, bioRxiv.

[6]  Jenny A Allen Community through Culture: From Insects to Whales: How Social Learning and Culture Manifest across Diverse Animal Communities. , 2019, BioEssays : news and reviews in molecular, cellular and developmental biology.

[7]  Clint J. Perry,et al.  How foresight might support the behavioral flexibility of arthropods , 2019, Current Opinion in Neurobiology.

[8]  Clint J. Perry,et al.  Bumblebees show cognitive flexibility by improving on an observed complex behavior , 2017, Science.

[9]  Clint J. Perry,et al.  Associative Mechanisms Allow for Social Learning and Cultural Transmission of String Pulling in an Insect , 2016, PLoS biology.

[10]  M. Ryan,et al.  The influence of past experience with flower reward quality on social learning in bumblebees , 2015, Animal Behaviour.

[11]  L. Chittka,et al.  Local enhancement or stimulus enhancement? Bumblebee social learning results in a specific pattern of flower preference , 2014, Animal Behaviour.

[12]  R. Dukas,et al.  Adult fruit fly attraction to larvae biases experience and mediates social learning , 2014, Journal of Experimental Biology.

[13]  S. Finkbeiner Communal Roosting in Heliconius Butterflies (Nymphalidae): Roost Recruitment, Establishment, Fidelity, and Resource Use Trends Based on Age and Sex , 2014 .

[14]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[15]  Robert D Reed,et al.  The benefit of being a social butterfly: communal roosting deters predation , 2012, Proceedings of the Royal Society B: Biological Sciences.

[16]  F. Mery,et al.  Spread of Social Information and Dynamics of Social Transmission within Drosophila Groups , 2012, Current Biology.

[17]  J. Mallet Gregarious Roosting and Home Range in Heliconius Butterflies , 2010 .

[18]  R. Dukas,et al.  Social learning about egg-laying substrates in fruitflies , 2009, Proceedings of the Royal Society B: Biological Sciences.

[19]  I. Coolen,et al.  Public Versus Personal Information for Mate Copying in an Invertebrate , 2009, Current Biology.

[20]  P. Ward,et al.  THE IMPORTANCE OF CERTAIN ASSEMBLAGES OF BIRDS AS “INFORMATION‐CENTRES” FOR FOOD‐FINDING , 2008 .

[21]  Kevin N. Laland,et al.  Chapter 3 Social Processes Influencing Learning in Animals: A Review of the Evidence , 2008 .

[22]  R. Dukas Social learning in insects , 2008 .

[23]  Lars Chittka,et al.  Social Learning in Insects — From Miniature Brains to Consensus Building , 2007, Current Biology.

[24]  L. Chittka,et al.  The dynamics of social learning in an insect model, the bumblebee (Bombus terrestris) , 2007, Behavioral Ecology and Sociobiology.

[25]  C. Heyes,et al.  SOCIAL LEARNING IN ANIMALS: CATEGORIES AND MECHANISMS , 1994, Biological reviews of the Cambridge Philosophical Society.

[26]  Nigel R. Franks,et al.  Teaching in tandem-running ants , 2006, Nature.

[27]  D. Papaj,et al.  Flower choice copying in bumblebees , 2005, Biology Letters.

[28]  I. Coolen,et al.  Social Learning in Noncolonial Insects? , 2005, Current Biology.

[29]  C. Grüter,et al.  Social learning of floral odours inside the honeybee hive , 2005, Proceedings of the Royal Society B: Biological Sciences.

[30]  L. Chittka,et al.  A new mode of information transfer in foraging bumblebees? , 2005, Current Biology.

[31]  R. Menzel,et al.  The flight paths of honeybees recruited by the waggle dance , 2005, Nature.

[32]  T. Valone,et al.  Public Information: From Nosy Neighbors to Cultural Evolution , 2004, Science.

[33]  K. Laland Social learning strategies , 2004, Learning & behavior.

[34]  L. Gilbert,et al.  Patterns of pollen exploitation by Heliconius butterflies , 1981, Oecologia.

[35]  D. Chivers,et al.  Learned Recognition of Predation Risk by Enallagma Damselfly Larvae (Odonata, Zygoptera) on the Basis of Chemical Cues , 2004, Journal of Chemical Ecology.

[36]  C. Jiggins,et al.  Patterns of pollen feeding and habitat preference among Heliconius species , 2002 .

[37]  M. Raveret Richter,et al.  Resource choice of social wasps: influence of presence, size and species of resident wasps , 1999, Insectes Sociaux.

[38]  C. Heyes,et al.  SOCIAL LEARNING IN ANIMALS: CATEGORIES AND MECHANISMS , 1994, Biological reviews of the Cambridge Philosophical Society.

[39]  L. Gilbert,et al.  Roost recruitment and resource utilization: observations on a Heliconius charitonia L. roost in Mexico (Nymphalidae). , 1982 .

[40]  K. S. Brown THE BIOLOGY OF HELICONIUS AND RELATED GENERA , 1981 .

[41]  L. Gilbert,et al.  Ovarian Dynamics in Heliconiine Butterflies: Programmed Senescence versus Eternal Youth , 1977, Science.

[42]  L. Cook,et al.  Population structure dynamics and dispersal of the tropical butterfly heliconius charitonius , 1976 .

[43]  L. Gilbert Ecological consequences of a coevolved mutualism between butterflies and plants , 1975, Coevolution of Animals and Plants.

[44]  P. Ehrlich,et al.  Population Structure and Dynamics of the Tropical Butterfly Heliconius ethilla , 1973 .

[45]  L. Gilbert Pollen feeding and reproductive biology of heliconius butterflies. , 1972, Proceedings of the National Academy of Sciences of the United States of America.

[46]  S. Swihart,et al.  Colour selection and learned feeding preferences in the butterfly, Heliconius charitonius Linn , 1970 .

[47]  K. Frisch,et al.  Honeybees: do they use direction and distance information provided by their dancers? , 1967, Science.