Abstract
Learning can occur through self-experience with the environment, or through the observation of others. The latter allows for adaptive behaviour without trial-and-error, thus maximizing individual fitness. Perhaps given their mostly solitary lifestyle, cuttlefish have seldomly been tested under observational learning scenarios. Here we used a multi-treatment design to disentangle if and how neurally immature cuttlefish Sepia officinalis hatchlings (up to 5 days) incorporate social information into their decision-making, when performing a task where inhibition of predatory behaviour is learned. In the classical social learning treatment using pre-trained demonstrators, observers did not register any predatory behaviour. In the inhibition by social learning treatment, using naïve (or sham) demonstrators, more observers than demonstrators learned the task, while also reaching learning criterion in fewer trials, and performing less number of attacks per trial. Moreover, the performance of demonstrator–observer pairs was highly correlated, indicating that the mere presence of conspecifics did not explain our results by itself. Additionally, observers always reported higher latency time to attack during trials, a trend that was reversed in the positive controls. Lastly, pre-exposure to the stimulus did not improve learning rates. Our findings reveal the vicarious capacity of these invertebrate newborns to learn modulation (inhibition) of predatory behaviour, potentially through emulation (i.e. affordance learning). Despite ongoing changes on neural organization during early ontogeny, cognitively demanding forms of learning are already present in cuttlefish newborns, facilitating behavioural adaptation at a critical life stage, and potentially improving individual fitness in the environment.
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Acknowledgements
We thank Catarina Santos, Maria Rita Pegado, and Marta Pimentel for cuttlefish rearing.
Funding
Research funded by MARE strategic project (UID/MAR/04292/2019), MAR2020 project VALPRAD (MAR-01.04.02-FEAMP-0007), the Portuguese Foundation for Science and Technology (FCT): as PhD (ES, SFRH/BD/131771/2017), Postdoc (VML, PTDC/BIA-BMA/28317/2017) grants, and the DFG Centre of Excellence 2117 “Centre for the Advanced Study of Collective Behaviour” (ID: 422037984).
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ES, VM, and RR conceived the study. ES, VM, CSR, BBLM, BM, AML, and EM reared animals, performed the experiment, and collected the data. ES and CSR analysed the data. All authors contributed to the manuscript, agree to be held accountable for the content therein, and approved the final version of the manuscript.
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Research was conducted under approval of Faculdade de Ciências da Universidade de Lisboa animal welfare body (ORBEA) and Direção-Geral de Alimentação e Veterinária (DGAV), within the framework of project VALPRAD (MAR-01.04.02-FEAMP-0007), in accordance with the requirements imposed by the Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010 on the protection of animals used for scientific purposes.
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Sampaio, E., Ramos, C.S., Bernardino, B.L.M. et al. Neurally underdeveloped cuttlefish newborns exhibit social learning. Anim Cogn 24, 23–32 (2021). https://doi.org/10.1007/s10071-020-01411-1
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DOI: https://doi.org/10.1007/s10071-020-01411-1