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Fish Brain Development in a Changing Ocean

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UNIVERSIDADE DE LISBOA FACULDADE DE CIÊNCIAS DEPARTAMENTO DE BIOLOGIA ANIMAL Fish Brain Development in a Changing Ocean Francisco José Ferraz de Oliveira Soeiro de Carvalho Mestrado em Ecologia Marinha Dissertação orientada por: Professor Doutor Rui Rosa Professor Doutor Ricardo Calado 2018 UNIVERSIDADE DE LISBOA FACULDADE DE CIÊNCIAS DEPARTAMENTO DE BIOLOGIA ANIMAL Fish Brain Development in a Changing Ocean Francisco José Ferraz de Oliveira Soeiro de Carvalho Mestrado em Ecologia Marinha Dissertação orientada por: Professor Doutor Rui Rosa Professor Doutor Ricardo Calado 2018 To the fish and the humans of sea and land Aos peixes e aos humanos do mar e da terra Acknowledgements To the fish and the personnel in the old Guia Lab, from my careful advisor Rui Rosa and my “almost advisor” José Ricardo Paula to the humorous cleaner, And all the colleagues and young researchers with whom countless living hours in and out were shared. To my co-advisor Ricardo Calado and to my reviewer and good friend Tiago Freire. To the scientific community, direct and indirectly contacted in meetings and readings; and to my friends, skipper mates and family, inland and abroad in the seas, I consider and thank you all. III Funding This study was funded by Portuguese national funds through FCT – Fundação para a Ciência e Tecnologia, I.P., within the project MUTUALCHANGE: Bio-ecological responses of marine cleaning mutualisms to climate change (PTDC/MAR-EST/5880/2014). IV Presentations in conferences This work was presented in the following scientific meetings: - XIII Congresso da Sociedade Portuguesa de Etologia, 2016 Carvalho, F.; Paula, J. R.; Lopes, A. R.; Santos, C.; Sampaio, E.; Rosa, R. Effects of Ocean Warming and Acidification on Fish Brain Development Poster presentation at XIII Congresso da Sociedade Portuguesa de Etologia (SPE) 13-14th October 2016 Lisbon, Portugal - Behaviour 2017, a joint meeting of the 35th International Ethological Conference (IEC) and the 2017 Summer Meeting of the Association for the Study of Animal Behaviour (ASAB) Carvalho, F.; Paula, J. R.; Lopes, A. R.; Santos, C.; Rosa, R. Fish Brain Development Under Ocean Warming and Acidification Poster presentation at Behaviour 2017, 35th International Ethological Conference (IEC) 2017 Summer Meeting of the Association for the Study of Animal Behaviour (ASAB) 30th July - 4th August 2017 Estoril, Cascais, Portugal V Abstract Unravelling how marine species invest in brain tissues (or brain regions) matching the fitness-relevant cognitive demands dictated by a changing environment is a priority in climate change-related (ocean warming and acidification) research. Within this context, this dissertation aimed to assess the combined effects of ocean warming (Δ 4 °C) and acidification (Δ 700 µatm pCO2 and Δ 0.4 pH) in the brain development (brain/body mass ratio and brain macro-region growth) of several juvenile fish species from different climate regions. Namely: three species adapted to a more stable (tropical) environment (clown anemonefish Amphiprion ocellaris, orchid dottyback Pseudochromis fridmani and neon goby Elacatinus oceanops), and other three adapted to a less stable (more seasonal; temperate) environment (seabream Diplodus sargus, flatfish Solea senegalensis and meagre Argyrosomus regius). The results show that the temperate species used in this study are only affected by ocean acidification in both total brain and specific brain regions, while the used tropical species are affected by ocean acidification, ocean warming and also by the interaction of ocean warming and ocean acidification. In fact, both total brain and every brain-region except for Telencephalon are affected by future conditions of ocean warming and ocean acidification differently according to each species. The lack of responses to ocean warming by the temperate species is here attributed to the widespread latitudinal distribution of those species, and thus the adaptation to a wider temperature range than tropical species. Curiously, all the significant interactions between the two studied stressors are antagonistic interactions with a cross-tolerance mechanism, meaning that under those interactions, the brain weight is closer to control levels than under each of the stressors separately. Possible behavioural and ecological implications of those results are also discussed. Despite the distinct dichotomic pattern between temperate and tropical habitats, the results among fish species and specific brain macro-regions do not exhibit a subjacent pattern. This different results highlight the idea of species-specific phenotypic responses to these climate change-related stressors. Keywords: Fish brain development, climate change, ocean warming, ocean acidification, temperate and tropical ocean habitats VI Resumo Uma das prioridades da Ecologia Marinha relacionada com as alterações climáticas (aquecimento e acidificação dos oceanos) tem sido perceber como as espécies marinhas investem em tecidos cerebrais (ou regiões cerebrais) de modo a adaptarem-se às necessidades cognitivas relevantes para a aptidão ditada pelo ambiente em mudança. Neste contexto, esta dissertação teve como objetivo avaliar os efeitos combinados do aquecimento (Δ 4° C) e acidificação (Δ 700 µatm pCO2 e Δ 0,4 pH) oceânicos no desenvolvimento encefálico (relação massa encéfalo/ massa corporal e crescimento das macro-regiões do encéfalo) de várias espécies juvenis de peixes de diferentes regiões climáticas, a saber: três espécies adaptadas a um ambiente mais estável (tropical) (o peixe-palhaço Amphiprion ocellaris, o orquídea dottyback Pseudochromis fridmani e o neon-goby-azul Elacatinus oceanops), e outras três adaptadas a um ambiente menos estável (sazonal, temperado) (o sargo Diplodus sargus, o linguado Solea senegalensis e a corvina Argyrosomus regius). Os resultados mostram que as espécies temperadas usadas neste estudo são afetadas apenas pela acidificação do oceano, tanto ao nível da totalidade do encéfalo, como de cada macro-região específica, enquanto as espécies tropicais usadas são afetadas pela acidificação dos oceanos, aquecimento dos oceanos e também pela interação entre aquecimento dos oceanos e acidificação dos oceanos. De facto, tanto a totalidade do encéfalo como as macro-regiões encefálicas, exceto o telencéfalo, são afetados de maneira diferente pelas condições futuras de aquecimento dos oceanos e acidificação dos oceanos de acordo com cada espécie. A falta de respostas ao aquecimento dos oceanos pelas espécies temperadas é aqui atribuída à ampla distribuição latitudinal dessas espécies e, portanto, à adaptação a uma faixa de temperatura mais ampla que as espécies tropicais. Curiosamente, todas as interações significativas entre os dois fatores estudados são interações antagonísticas com um mecanismo de tolerância cruzada, o que significa que nessas interações, o peso do cérebro está mais próximo dos níveis das condições controlo do que sob cada um dos fatores separadamente. Possíveis implicações comportamentais e ecológicas desses resultados também são discutidas. Apesar do padrão dicotómico bem definido entre habitats temperados e tropicais, os resultados entre espécies de peixes e macro-regiões VII encefálicas específicas não exibem um padrão subjacente. Estes diferentes resultados destacam a ideia de respostas fenotípicas específicas de cada espécie em resposta às condições de alterações climáticas futuras. Palavras-chave: Desenvolvimento cerebral dos peixes, alterações climáticas, aquecimento do oceano, acidificação do oceano, habitats marinhos temperados e tropicais VIII Table of contents Acknowledgements ...................................................................................................................... III Funding ......................................................................................................................................... IV Presentations in conferences ........................................................................................................ V Abstract ........................................................................................................................................ VI Resumo ........................................................................................................................................ VII List of figures ................................................................................................................................ XI List of tables ................................................................................................................................ XII List of abbreviations ................................................................................................................... XIII 1 Introduction .......................................................................................................................... 1 1.1 Climate change .............................................................................................................. 1 1.2 Marine ecosystems and climate change ....................................................................... 3 1.3 Ocean acidification ........................................................................................................ 4 1.4 Ocean warming ............................................................................................................. 6 1.5 Animal behaviour under climate change ...................................................................... 9 1.6 Neurobiology and sensory systems
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