Neuroethology of the visual communication in the mourning cuttlefish Sepia plangon

Abstract

Animals communicate in response to different tasks, including alarm calls, allocation of food, courtship, and mating. Different types of signals are used by animals to communicate, such as chemical signals, vocalisations, colour patterns, and movements. Animal colouration and visual communication have fascinated researchers for decades. Behavioural, anatomical and functional studies are commonly used to study visual communication in both vertebrates and invertebrates. Cuttlefish are well known for possessing intricate body patterns. Cuttlefish use these colourful and dynamic displays to communicate with mates, camouflage, and pursue prey. The cuttlefish central nervous system processes all the visual stimuli and coordinates the expression of postures, body movements, skin textures and colourations that form a body pattern. Interestingly, many species of cuttlefish are colour blind but possess polarisation vision and polarisation patterns in their bodies, which are potentially used for communication with conspecifics.The objective of this thesis is to analyse the mechanisms influencing visual communication and colour patterns in a small coastal cuttlefish Sepia plangon. The mourning cuttlefish S. plangon is a small species with a mantle length (ML) < 140 mm. This species inhabits coastal waters and prefers to forage in seaweed and seagrass environments. It is located to a maximum depth of 85 meters and is active during the day.After introducing the topic of this thesis in detail in chapter 1, we analysed the ontogenetic changes of S. plangon body patterns from embryos to adults in chapter 2. The first description of S. plangon eggs and embryos is included in this chapter. However, because the eggs were collected from their natural environment, only late embryonic development was described. The number and complexity of the body patterns of S. plangon changed throughout the lifespan, transitioning from three body patterns in embryos to a maximum of 18 in males. Seven patterns were exclusive to males and used only during reproductive behaviour. Therefore, in chapter 3, we analysed courtship, mating, and agonistic competition of S. plangon. Three sex ratios were used to study mate choice: 1Male(M):1F(F), 2M:1F, and 1M:2F. Polarised and unpolarised filters were placed between the animals to test the effect of modifying polarised stimuli in the reproductive behaviour of S. plangon. 3D printed cuttlefish models were used to manipulate specific traits (two body sizes, two postures, four body patterns) and determine which factor was crucial to successful mating. The components of the body patterns, reproductive behaviours and visual signals were analysed. We found that only sex ratio had a significant effect on male courtship frequency. Agonistic competition between males included visual signals, and most males avoided fighting. Small males (ML < 80 mm) used a deceptive display to mimic female patterns, avoid male competitions, and mate with females. The dynamic changes in body patterns were the most crucial element for successful matings, as the static body pattern in the 3D cuttlefish models did not trigger any reproductive behaviour. Fifty-seven components of the body patterns and 18 body patterns were observed during courtship, mating and male competitions, but further analysis revealed that only four body patterns and six components displayed in a specific order were determinant for mating.In chapter 4, we used magnetic resonance imaging (MRI) and diffusion MRI (dMRI) to investigate ontogenetic changes in brain structure and connectivity of S. plangon. Brain volumes and tractography were estimated from a hatchling, a juvenile, a male, and a female S. plangon. Forty-seven lobes and twelve brain centres were identified. Volumetric differences were found across the motor and visual centres. Tractography estimations revealed new connections in the posterior chromatophore, lateral pedal, posterior pedal, brachial, dorsolateral, interbasal, and optic lobes. The differences in brain volume and connections across the different life stages of S. plangon are likely related to the development of body patterns.The findings from this thesis expand our current knowledge on cuttlefish embryonic development, body pattern changes, visual communication and structural organisation of the brain. Furthermore, this thesis introduces the use of modern technology (MRI) to study the cuttlefish brain, which showed connections in the brain of S. plangon previously unknown.