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Ecology of Gelatinous Carnivores in the Mondego Estuary: the Role of Siphonophores

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Ecology of Gelatinous Carnivores in the Mondego Estuary: the Role of Siphonophores Ecology of gelatinous carnivores in the Mondego estuary: the role of siphonophores Doctoral thesis in Biosciences, scientific area of Ecology, supervised by Prof. Dr. Miguel Ângelo do Carmo Pardal, by Prof. Dr. Ulisses Miranda Azeiteiro and by Dr. Sónia Cristina Ferreira Cotrim Marques, presented to the Department of Life Sciences of the Faculty of Sciences and Technology of the University of Coimbra Tese de doutoramento em Biociências, ramo de especialização em Ecologia, orientada por Professor Doutor Miguel Ângelo do Carmo Pardal, por Professor Doutor Ulisses Miranda Azeiteiro, e por Doutora Sónia Cristina Ferreira Cotrim Marques e apresentada ao Departamento de Ciências da Vida da Faculdade de Ciências e Tecnologia da Universidade de Coimbra Mariaelena D’Ambrosio Department of Life Sciences – University of Coimbra Coimbra, 2017 This Thesis was supported by: The CFE - Center for Functional Ecology, University of Coimbra and by the Portuguese Foundation for Science and Technology (FCT) through a Ph.D. grant attributed to Mariaelena D’Ambrosio (SFRH/BD/91541/2012) subsidized by the European Social Fund and MCTES (Portuguese Ministry of Science, Technology and Higher Education), through the POPH (Human Potential Operational Programme), QREN (National Strategic Reference Framework) and COMPETE (Programa Operacional Factores de Competitividade). Cover image: Siphonophores’s illustration of Ernst Haeckel (1834-1919) from: “Art forms in nature”, 1904. This thesis includes three manuscripts listed below, published or submitted for publication in scientific journals in the areas of ecology and marine biology: Chapter I D’Ambrosio, M, Molinero JC, Azeiteiro UM, Pardal MA, Primo AL, Nyitrai D, Marques SC (2016). Interannual abundance changes of gelatinous carnivore zooplankton unveil climate- driven hydrographic variations in the Iberian Peninsula, Portugal. Marine Environmental Research 120: 103–110. DOI:10.1016/j.marenvres.2016.07.012 Chapter II D’Ambrosio M, Primo AL, Pardal MA, Martinho F, Guerrero E, Marques SC. Spatial distribution and seasonal patterns of the siphonophores Muggiaea atlantica and Muggiaea kochii in a temperate estuarine ecosystem. (Under revisions on August 2017 in Estuarine Coastal and Shelf Science). Chapter III D’Ambrosio M, Molinero JM, Pardal MA, Guerrero E, Martinho F, Falcão J, Azeiteiro UM, Cruz J, Marques SC. Diel variations in the feeding behavior of Muggiaea atlantica in the Mondego Estuary. (Submitted on October 2017 in Journal of Plankton Research). For Maristel and Alessio | 7 CONTENTS CONTENTS…………………………………………………………………………………………………………………..……………..7 ABSTRACT ....................................................................................................................................... 11 KEYWORDS ................................................................................................................................. 13 RESUMO .......................................................................................................................................... 15 PALAVRAS-CHAVES .................................................................................................................... 17 CHAPTER 1 ...................................................................................................................................... 19 General introduction .................................................................................................................. 19 1.1 Gelatinous carnivore zooplankton ........................................................................... 19 1.2. Siphonophores and calicophorans Muggiaea Atlantica (Cunningham, 1892) And Muggiaea Kochii (Will, 1844) ................................................................................................ 22 1.2.1 Structure of the colony......................................................................................... 23 1.2.2 Life cycle ................................................................................................................ 24 1.3 The importance of the estuarine systems ...................................................................... 27 1.4 The Mondego estuary as case study ............................................................................... 29 1.5. Thesis aims and general objectives ............................................................................... 31 CHAPTER 2 ...................................................................................................................................... 33 Interannual abundance changes of gelatinous carnivore zooplankton unveil climate-driven hydrographic variations in the Iberian Peninsula, Portugal .................................................... 33 2.1 Abstract ...................................................................................................................... 33 2.2 Keywords ................................................................................................................... 34 2.3 Introduction ............................................................................................................... 34 2.4 Materials and methods ............................................................................................. 35 2.4.1 Study area......................................................................................................... 35 2.4.2 Biological data .................................................................................................. 36 2.4.3 Physical data .................................................................................................... 37 2.4.4 Statistical analysis ............................................................................................ 37 2.5 Results ........................................................................................................................ 39 2.5.1 Gelatinous carnivore zooplankton abundance and composition ................. 39 2.5.2 Environmental variability ................................................................................ 42 2.5.3 Couplings between NAO, regional climate and gelatinous carnivore organisms’ variability............................................................................................................. 43 2.5.4 Interannual and seasonal changes of gelatinous carnivore zooplankton in the Mondego estuary ................................................................................................................... 44 2.6. Discussion ........................................................................................................................ 46 2.6.1 Climate variability and gelatinous carnivore zooplankton ................................. 46 2.6.2 Gelatinous carnivore zooplankton community in Mondego estuary ................. 47 2.7 Acknowledgements ................................................................................................... 49 8 | CHAPTER 3 ....................................................................................................................................... 51 Spatial distribution and seasonal patterns of the siphonophores Muggiaea atlantica and Muggiaea kochii in a temperate estuarine ecosystem ............................................................ 51 3.1 Abstract ...................................................................................................................... 51 3.2 Keywords .................................................................................................................... 51 3.3 Introduction ............................................................................................................... 52 3.4 Materials and methods ............................................................................................. 54 3.4.1 Study site .......................................................................................................... 54 3.4.2 Sample collection ............................................................................................. 55 3.4.3 Statistical analysis ............................................................................................ 57 3.5 Results ........................................................................................................................ 57 3.5.1 Environmental parameters .............................................................................. 57 3.5.2 Temporal and spatial variation of M. atlantica and M. kochii nectophores 59 3.5.3 Temporal and spatial variation of Muggiaea spp. gonophores .................... 61 3.5.4 Temporal and spatial availability of the potential prey ................................. 62 3.5.5 Relationships between biological and environmental factors ...................... 64 3.6 Discussion ................................................................................................................... 65 3.6.1 Muggiaea spp. and hydrology of the Mondego estuary ............................... 65 3.6.2 Muggiea spp. abundance and distribution ..................................................... 66 3.6.3 Prey influence on Muggiaea spp. distribution ............................................... 69 3.7 Acknowledgements ................................................................................................... 70 CHAPTER 4 ....................................................................................................................................... 71 Diel variations in the feeding
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