My Msc.Marine Biology. Mariana Cruz. University of Algrave.2019
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MARIANA ANASTÁCIO CRUZ JELLYFISH, A THREAT OR AN OPPORTUNITY? THE NON-INDIGENOUS BLACKFORDIA VIRGINICA AS A POTENTIAL FOOD SOURCE FOR HUMANS AND AQUATIC ORGANISMS UNIVERSIDADE DO ALGARVE Faculdade de Ciências e Tecnologia 2019 MARIANA ANASTÁCIO CRUZ JELLYFISH, A THREAT OR AN OPPORTUNITY? THE NON-INDIGENOUS BLACKFORDIA VIRGINICA AS A POTENTIAL FOOD SOURCE FOR HUMANS AND AQUATIC ORGANISMS Mestrado em Biologia Marinha Supervisors: Drª Ester Dias; Drª. Luísa Custódio UNIVERSIDADE DO ALGARVE Faculdade de Ciências e Tecnologia 2019 ii JELLYFISH, A THREAT OR AN OPPORTUNITY? THE NON-INDIGENOUS BLACKFORDIA VIRGINICA AS A POTENTIAL FOOD SOURCE FOR HUMANS AND AQUATIC ORGANISMS Author: Mariana Anastácio Cruz¹ Thesis supervised by: Dr. Ester Dias², Prof. Dr. Luísa Custódio3 Affiliation address: 1Faculdade de Ciências e Tecnologia, Universidade do Algarve, 8005-139 Faro, Portugal; 2 CIIMAR Universidade do Porto, 4450-208Matosinhos, Portugal; 3 CCMAR Universidade do Algarve, 8005-139 Faro, Portugal Corresponding author- E-mail address: [email protected] Scientific area: Marine Biology Keywords: Exotic jellyfish; blue crab, Guadiana estuary;, nutrional composition; stable isotopes Palavras-chave: Medusa exótica; caranguejo azul, Estuário do Guadiana, , composição nutricional, isotopos estáveis Date: 30th of September 2019 Title of dissertation: Jellyfish, a threat or an opportunity? The non-indigenous Blackfordia virginica as a potential food source for humans and aquatic organisms iii JELLYFISH, A THREAT OR AN OPPORTUNITY? THE NON-INDIGENOUS BLACKFORDIA VIRGINICA AS A POTENTIAL FOOD SOURCE FOR HUMANS AND AQUATIC ORGANISMS Copyright Mariana Anastácio Cruz A Universidade do Algarve tem o direito, perpétuo e sem limites geográficos, de arquivar e publicitar este trabalho através de exemplares impressos reproduzidos em papel ou de forma digital, ou por qualquer outro meio conhecido ou que venha a ser inventado, de o divulgar através de repositories científicos e de admitir a sua cópia e distribuição com objetivos educacionais ou de investigação, não comerciais, desde que seja dado crédito ao autor e editor. Declaração de autoria de Trabalho Declaro ser a autora deste trabalho, que é original e inédito. Autores e trabalhos consultados estão devidamente citados no texto e constam da listagem de refências incluida. Mariana Anastácio Cruz iv ACKNOWLEDGMENTS To my supervisor Dr. Ester Dias for the valuable support during all the experiment, for being always available to guide me, to teach me and for provided me knowledge about the stable isotopes, making possible the development of this study; and to my supervisor Prof. Dr. Luísa Custódio for her valuable support on biochemical analysis, for the infinite patience and assistance during laboratory experiments and to teach me about nutritional value techniques, making also possible the development of this study. To Prof. Dr. Alexandra Teodósio for the encouragement, sympathy and for being always available to answer my questions. For giving me the first highlights on zooplankton and invertebrates since the very beginning that encouraged me to do this work. To all the people that helped me during the field and laboratory work namely to Joana Cruz, Vânia Baptista and João Encarnação for their patience, assistance and advices during samples preparation for SIA and field sampling in the Guadiana estuary; to Vera Gomes for her assistance during proteins, minerals and FAMEs analysis and to Cláudia Aragão and Marta Valente for their assistance with amino acids and molecular analysis, respectively. To Jellyfisheries project (Towards an integrated approach to enhance predictive accuracy of jellyfish impact on coastal marine ecosystems) and to Plurianual (CCMAR) to support all the analysis during the experiment. To my forever friends for being always there for me. To the masters in marine biology and amazing friends who helped me, sometimes with just a few words of support. But mostly to the most important human beings of my life, my moom Isabel, my dad Paulo, my little sister Raquel and all my family for giving me this amazing opportunity and for their endless support in every single minute of my journey. I am especially greatful to my big love and friend João, who always stood by me during most both stressful and happiest moments and who always believed in me, even when I did not. And of course to my dog Baltazar for giving me such good times of joy and love. v ABSTRACT Anthropogenic activites such as those producing environmental changes have promoted the proliferation and establishment of non-indigenous species (NIS) in estuaries worldwide and the Guadiana estuary (Southern-Iberian Peninsula) is no exception. The extensive human development in this estuary, including river flow regulation, favoured the colonization by several NIS such as the black sea jellyfish Blackfordia virginica and more recently the blue crab Callinectes sapidus. The seasonal occurrence of B. virginica blooms have become a reason of concern due to reports of considerable economic and ecological impacts to fisheries and to the local food webs. However due to jellyfish properties, they represent an opportunity as an alternative food source for humans, while contributing to control their biomass in invaded ecosystems. Therefore, the objective of this work was to evaluate the nutritional profile of this jellyfish, testing the hypothethis that B. virginica represents an alternative and healthy food source if it follows the same composition of other known edible jellyfish. However, they may also represent a threat to the ecosystem if consumed by other NIS. Thus, the second objective of this work was to evaluate the contribution of B. virginica to the diet of opportunistic consumers in the middle Guadiana estuary, testing the hypothethis that generalist predators such as the NIS blue crab Callinectes sapidus and the indigenous green crab Carcinus maenas will benefit from B. virginica seasonal blooms by consuming this jellyfish. For the evaluation of the nutritional profile the determination of the total lipids (modified protocol of the Bligh & Dyer method), crude protein, (elementar analysis of nitrogen), ash content (incineration), fatty acids methyl esters, (gas chromatography-mass spectrometer; GC-MS), aminoacids (high pressure liquid chromatography; HPLC reverse phase), and minerals (microwave plasma – atomic emission spectrometry; MP-AES) were made. To investigate the contribution of B. virginica to the diet of the selected consumers, the presence of this jellyfish was investigated in the stomach contents of both crab species, through molecular analysis (DNA-PCR). Afterwards, its contribution to these consumers' biomass was determined using carbon (13C:13C/12C) and nitrogen (15N:15N/14N) stable isotope analysis. Results suggest that B. virginica dry biomass is mainly composed by essential minerals, and proteins rather than lipids. Blackfordia virginica composition resembled other edible jellyfish. Nonetheless the presence of cadmium, which is a toxic element, was high (3 mg/Kg) which meand they have a great potential to be used as food for humans if cadmium levels decrease. In addition, molecular analysis revealed the presence of B. virginica only in blue crab gut contents, although the Bayesian stable isotope mixing model did not show any relevant contribution to their biomass. Therefore the use of B. virginica for human consumption can represent an opportunity to decrease the abundance of this species in vi the ecosystem through commercial exploitation, while representing a threat if other NIS, mainly the blue crab, can take advantage of this species by consuming it. Keywords: Exotic jellyfish; blue crab, Guadiana estuary;, nutrional composition; stable isotopes vi i RESUMO Nos últimos anos as atividades antropogénicas têm promovido o aparecimento e colonização de espécies não indígenas em estuários distribuídos por todo o mundo e o estuário do Guadiana (Sul de Portugal) não é exceção. O estuário do Guadiana tem sofrido ao longo dos tempos diversos impactos antropogénicos, incluindo, a construção da barragem do Alqueva em 2002 que promoveu a regulação do caudal do rio. Com a regulação do caudal, a salinidade da água tornou-se mais alta e mais estável, principalmente na zona do meio estuário que antes da construção da barragem era caracterizada por grandes variações de salinidade. Assim, as condições de salinidade mais altas e estáveis, juntamente com o facto desta zona ser caracterizada por ter uma baixa abundância e diversidade de espécies indígenas promoveram o aparecimento e suporte de espécies marinhas não indígenas como a medusa do mar negro Blackfordia virginica e mais recentemente o caranguejo azul Callinectes sapidus. A B. virginica tornou-se a espécie não indígena com uma maior distribuição no estuário e os seus blooms sazonais tornaram-se um motivo de preocupação devido aos seus consideráveis impactos tanto a nível económico como ecológico. Por exemplo, após o aparecimento desta espécie, foi observado uma diminuição na abundância de todos os organismos zooplantónicos incluindo de larvas e ovos de peixes. No entanto, devido às propriedades das medusas, como o alto teor em proteínas e minerais e o baixo teor lípidos, estas podem representar uma oportunidade como fonte de alimento para a população humana e assim contribuir para o controle dos seus blooms nos ecossistemas. De facto, com o aumento da população humana e consequente redução dos “stocks” de peixe, as fontes de alimento alternativas e saudáveis nunca