Cirillo, Emanuela (2026) How the brain controls natural behaviour in Octopus vulgaris: problem solving, arms strategies, sensory integration, and welfare standards. [Tesi di dottorato]

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Abstract

Cephalopods exhibit an extraordinary level of behavioural complexity, characterized by flexible problem-solving abilities, rapid learning, and sophisticated sensory-motor integration. However, the investigation of these cognitive capacities requires a highly controlled and ethically rigorous environment. This doctoral thesis presents a comprehensive study conducted at the Octopus Core (Department of Biology, University of Naples Federico II) under the scientific supervision of Prof. Anna Di Cosmo currently the only facility authorized in Italy to utilize Octopus vulgaris as a research model. Leveraging this unique institutional framework, the research integrates a novel investigation into integrated multisensory problem solving with the establishment of refined welfare protocols in full compliance with European Directive 2010/63/EU, updated in 2024. The first topic of the study addressed the critical need for standardized welfare benchmarks to ensure the validity of behavioural data. It has been validated and refined anaesthesia protocol combining magnesium chloride (MgCl2) pre-treatment with low-dose isoflurane (1%), demonstrating that this method minimizes respiratory depression and facilitates rapid recovery compared to traditional techniques. Furthermore, the molecular and physiological footprint of stress induced by capture and transport has been identified. By analyzing the expression of stress-related genes Estrogen Receptor (ER), Catalase (CAT), and Heat Shock Protein 70 (HSP70), we identified significant sex-specific responses. Males exhibited a clear upregulation of these markers, whereas females showed downregulation, likely modulated by reproductive status. These findings highlighted the necessity of a mandatory 15-day acclimatization period and suggest that males may provide more consistent baselines for experimental replicability. Building upon this optimized welfare foundation, the core of the thesis investigated the cognitive dynamics of O. vulgaris using a novel “unique device”. It has been developed a transparent three-choice device to test the hypothesis that octopuses utilize a hierarchy of sensory inputs and arm strategies to solve foraging challenges. In a Pre-training phase, subjects (N=8) showed rapid associative and procedural learning, significantly reducing problem-solving latency from >130 seconds (Day 1) to <70 seconds (Day 6) as they mastered the motor manipulation of the device. In the subsequent Experimental phase, animals were challenged to discriminate between a real anchovy and two visually realistic, 3D-printed thermoplastic polyurethane (TPU) mimics. Despite the visual ambiguity, octopuses maintained an exceptionally efficient performance with low latency (~20 seconds) and no decline in success rates. This sustained efficiency reveals that O. vulgaris does not rely solely on vision but rapidly integrates chemo tactile information via the arm suckers, showing also an arm’s peculiar strategy. The suckers act as "embodied" sensory organs, allowing the animal to filter out the artificial stimuli almost instantaneously upon contact, thereby bypassing the need for prolonged visual re-evaluation. In conclusion, this Ph.D. thesis explores how sensory integration across the octopus’s central brain and semi-autonomous arms gives rise to flexible problem-solving, adaptive camouflage, and advanced motor control. The arm strategy highlights how each arm integrates tactile and chemical cues to perform tasks autonomously yet synchronizes with the central brain for coordinated behavior.

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