Bumblebees acquire alternative puzzle-box solutions via social learning
The astonishing behavioural repertoires of social insects have been thought largely innate, but these insects have repeatedly demonstrated remarkable capacities for both individual and social learning. Using the bumblebee Bombus terrestris as a model, we developed a two-option puzzle box task and us...
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Published in | PLoS biology Vol. 21; no. 3; p. e3002019 |
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Main Authors | , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
Public Library of Science
07.03.2023
Public Library of Science (PLoS) |
Subjects | |
Online Access | Get full text |
ISSN | 1545-7885 1544-9173 1545-7885 |
DOI | 10.1371/journal.pbio.3002019 |
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Abstract | The astonishing behavioural repertoires of social insects have been thought largely innate, but these insects have repeatedly demonstrated remarkable capacities for both individual and social learning. Using the bumblebee
Bombus terrestris
as a model, we developed a two-option puzzle box task and used open diffusion paradigms to observe the transmission of novel, nonnatural foraging behaviours through populations. Box-opening behaviour spread through colonies seeded with a demonstrator trained to perform 1 of the 2 possible behavioural variants, and the observers acquired the demonstrated variant. This preference persisted among observers even when the alternative technique was discovered. In control diffusion experiments that lacked a demonstrator, some bees spontaneously opened the puzzle boxes but were significantly less proficient than those that learned in the presence of a demonstrator. This suggested that social learning was crucial to proper acquisition of box opening. Additional open diffusion experiments where 2 behavioural variants were initially present in similar proportions ended with a single variant becoming dominant, due to stochastic processes. We discuss whether these results, which replicate those found in primates and birds, might indicate a capacity for culture in bumblebees. |
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AbstractList | The astonishing behavioural repertoires of social insects have been thought largely innate, but these insects have repeatedly demonstrated remarkable capacities for both individual and social learning. Using the bumblebee Bombus terrestris as a model, we developed a two-option puzzle box task and used open diffusion paradigms to observe the transmission of novel, nonnatural foraging behaviours through populations. Box-opening behaviour spread through colonies seeded with a demonstrator trained to perform 1 of the 2 possible behavioural variants, and the observers acquired the demonstrated variant. This preference persisted among observers even when the alternative technique was discovered. In control diffusion experiments that lacked a demonstrator, some bees spontaneously opened the puzzle boxes but were significantly less proficient than those that learned in the presence of a demonstrator. This suggested that social learning was crucial to proper acquisition of box opening. Additional open diffusion experiments where 2 behavioural variants were initially present in similar proportions ended with a single variant becoming dominant, due to stochastic processes. We discuss whether these results, which replicate those found in primates and birds, might indicate a capacity for culture in bumblebees. The astonishing behavioural repertoires of social insects have been thought largely innate, but these insects have repeatedly demonstrated remarkable capacities for both individual and social learning. Using the bumblebee Bombus terrestris as a model, we developed a two-option puzzle box task and used open diffusion paradigms to observe the transmission of novel, nonnatural foraging behaviours through populations. Box-opening behaviour spread through colonies seeded with a demonstrator trained to perform 1 of the 2 possible behavioural variants, and the observers acquired the demonstrated variant. This preference persisted among observers even when the alternative technique was discovered. In control diffusion experiments that lacked a demonstrator, some bees spontaneously opened the puzzle boxes but were significantly less proficient than those that learned in the presence of a demonstrator. This suggested that social learning was crucial to proper acquisition of box opening. Additional open diffusion experiments where 2 behavioural variants were initially present in similar proportions ended with a single variant becoming dominant, due to stochastic processes. We discuss whether these results, which replicate those found in primates and birds, might indicate a capacity for culture in bumblebees.The astonishing behavioural repertoires of social insects have been thought largely innate, but these insects have repeatedly demonstrated remarkable capacities for both individual and social learning. Using the bumblebee Bombus terrestris as a model, we developed a two-option puzzle box task and used open diffusion paradigms to observe the transmission of novel, nonnatural foraging behaviours through populations. Box-opening behaviour spread through colonies seeded with a demonstrator trained to perform 1 of the 2 possible behavioural variants, and the observers acquired the demonstrated variant. This preference persisted among observers even when the alternative technique was discovered. In control diffusion experiments that lacked a demonstrator, some bees spontaneously opened the puzzle boxes but were significantly less proficient than those that learned in the presence of a demonstrator. This suggested that social learning was crucial to proper acquisition of box opening. Additional open diffusion experiments where 2 behavioural variants were initially present in similar proportions ended with a single variant becoming dominant, due to stochastic processes. We discuss whether these results, which replicate those found in primates and birds, might indicate a capacity for culture in bumblebees. The astonishing behavioural repertoires of social insects have been thought largely innate, but these insects have repeatedly demonstrated remarkable capacities for both individual and social learning. Using the bumblebee Bombus terrestris as a model, we developed a two-option puzzle box task and used open diffusion paradigms to observe the transmission of novel, nonnatural foraging behaviours through populations. Box-opening behaviour spread through colonies seeded with a demonstrator trained to perform 1 of the 2 possible behavioural variants, and the observers acquired the demonstrated variant. This preference persisted among observers even when the alternative technique was discovered. In control diffusion experiments that lacked a demonstrator, some bees spontaneously opened the puzzle boxes but were significantly less proficient than those that learned in the presence of a demonstrator. This suggested that social learning was crucial to proper acquisition of box opening. Additional open diffusion experiments where 2 behavioural variants were initially present in similar proportions ended with a single variant becoming dominant, due to stochastic processes. We discuss whether these results, which replicate those found in primates and birds, might indicate a capacity for culture in bumblebees. The astonishing behavioural repertoires of social insects have been thought largely innate, but these insects have repeatedly demonstrated remarkable capacities for both individual and social learning. Using the bumblebee Bombus terrestris as a model, we developed a two-option puzzle box task and used open diffusion paradigms to observe the transmission of novel, nonnatural foraging behaviours through populations. Box-opening behaviour spread through colonies seeded with a demonstrator trained to perform 1 of the 2 possible behavioural variants, and the observers acquired the demonstrated variant. This preference persisted among observers even when the alternative technique was discovered. In control diffusion experiments that lacked a demonstrator, some bees spontaneously opened the puzzle boxes but were significantly less proficient than those that learned in the presence of a demonstrator. This suggested that social learning was crucial to proper acquisition of box opening. Additional open diffusion experiments where 2 behavioural variants were initially present in similar proportions ended with a single variant becoming dominant, due to stochastic processes. We discuss whether these results, which replicate those found in primates and birds, might indicate a capacity for culture in bumblebees. The astonishing behavioral repertoires of social insects have been thought largely innate, but this study shows that populations of bumblebees are capable of acquiring and maintaining arbitrary variants of a complex, novel, non-natural foraging behavior, and can maintain these as "behavioral traditions." |
Audience | Academic |
Author | Mohammed, Yaseen Kowalewska, Amelia Lockwood, Charlotte Chittka, Lars Bridges, Alice D. MaBouDi, HaDi Romero González, José Eric Procenko, Olga Woodgate, Joseph L. |
AuthorAffiliation | School of Biological and Behavioural Sciences, Queen Mary University of London, London, United Kingdom Emory University, UNITED STATES |
AuthorAffiliation_xml | – name: School of Biological and Behavioural Sciences, Queen Mary University of London, London, United Kingdom – name: Emory University, UNITED STATES |
Author_xml | – sequence: 1 givenname: Alice D. orcidid: 0000-0002-6538-9737 surname: Bridges fullname: Bridges, Alice D. – sequence: 2 givenname: HaDi surname: MaBouDi fullname: MaBouDi, HaDi – sequence: 3 givenname: Olga surname: Procenko fullname: Procenko, Olga – sequence: 4 givenname: Charlotte surname: Lockwood fullname: Lockwood, Charlotte – sequence: 5 givenname: Yaseen surname: Mohammed fullname: Mohammed, Yaseen – sequence: 6 givenname: Amelia surname: Kowalewska fullname: Kowalewska, Amelia – sequence: 7 givenname: José Eric surname: Romero González fullname: Romero González, José Eric – sequence: 8 givenname: Joseph L. surname: Woodgate fullname: Woodgate, Joseph L. – sequence: 9 givenname: Lars orcidid: 0000-0001-8153-1732 surname: Chittka fullname: Chittka, Lars |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/36881588$$D View this record in MEDLINE/PubMed |
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ContentType | Journal Article |
Copyright | Copyright: © 2023 Bridges et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. COPYRIGHT 2023 Public Library of Science 2023 Bridges et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2023 Bridges et al 2023 Bridges et al |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Current address: Bioscience Institute, Newcastle University, Henry Wellcome Building, Newcastle upon Tyne, United Kingdom Current address: Department of Computer Science, University of Sheffield, Sheffield, United Kingdom Current address: Department of Psychology, School of Public Health, Southern Medical University, Guangzhou, China The authors have declared that no competing interests exist. |
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SubjectTerms | Analysis Animals Bees Behavior Biology and Life Sciences Boxes Bumblebees Design Diffusion Experiments Foraging Foraging behavior Innovations Insects Learning Monkeys & apes Observational learning Observers Seeds Social behavior Social discrimination learning Social Learning Social Sciences Stochastic processes Stochasticity |
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