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Biology, Ecology and Ecophysiology of the Box Jellyfish Biology, Ecology and Ecophysiology of the Box Jellyfishcarybdea Marsupialis (Cnidaria: Cubozoa)

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Biology, Ecology and Ecophysiology of the Box Jellyfish Biology, Ecology and Ecophysiology of the Box Jellyfishcarybdea Marsupialis (Cnidaria: Cubozoa) Biology, ecology and ecophysiology of the box M. J. ACEVEDO jellyfish Carybdea marsupialis (Cnidaria: Cubozoa) Carybdea marsupialis MELISSA J. ACEVEDO DUDLEY PhD Thesis September 2016 Biology, ecology and ecophysiology of the box jellyfish Biology, ecology and ecophysiology of the box jellyfishCarybdea marsupialis (Cnidaria: Cubozoa) Biologia, ecologia i ecofisiologia de la cubomedusa Carybdea marsupialis (Cnidaria: Cubozoa) Melissa Judith Acevedo Dudley Memòria presentada per optar al grau de Doctor per la Universitat Politècnica de Catalunya (UPC), Programa de Doctorat en Ciències del Mar (RD 99/2011). Tesi realitzada a l’Institut de Ciències del Mar (CSIC). Director: Dr. Albert Calbet (ICM-CSIC) Co-directora: Dra. Verónica Fuentes (ICM-CSIC) Tutor/Ponent: Dr. Xavier Gironella (UPC) Barcelona – Setembre 2016 The author has been financed by a FI-DGR pre-doctoral fellowship (AGAUR, Generalitat de Catalunya). The research presented in this thesis has been carried out in the framework of the LIFE CUBOMED project (LIFE08 NAT/ES/0064). The design in the cover is a modification of an original drawing by Ernesto Azzurro. “There is always an open book for all eyes: nature” Jean Jacques Rousseau “The growth of human populations is exerting an unbearable pressure on natural systems that, obviously, are on the edge of collapse […] the principles we invented to regulate our activities (economy, with its infinite growth) are in conflict with natural principles (ecology, with the finiteness of natural systems) […] Jellyfish are just a symptom of this situation, another warning that Nature is giving us!” Ferdinando Boero (FAO Report 2013) Thesis contents Summary / Resumen ...........................................................................................................................1 General introduction ............................................................................................................................3 Objectives and thesis outline ..............................................................................................................13 Chapter 1 Revision of the genus Carybdea (Cnidaria: Cubozoa: Carybdeidae): the identity of its type species Carybdea marsupialis ............................................................................... 15 Chapter 2 Maintenance, feeding and growth of Carybdea marsupialis (Cnidaria: Cubozoa) in the laboratory .................................................................................................................................51 Chapter 3 Trophic ecology and potential predation impact of Carybdea marsupialis (Cnidaria: Cubozoa) in the NW Mediterranean ................................................................................67 Chapter 4 Influence of human impacts on and forecasting of the occurrence of the box jellyfish Carybdea marsupialis in the Mediterranean coasts ......................................................89 General discussion............................................................................................................................115 Conclusions ......................................................................................................................................125 Acknowledgements / Agradecimientos ...........................................................................................127 1 Summary / Resumen Over the last years, the sightings of the cubomedusa Carybdea marsupialis have increased in the Mediterranean Sea and this has been linked to an increase in its abundance. Consequently, this phD thesis addresses some questions regarding the possible causes and effects of this phenomenon. Firstly, the taxonomy and distribution of the species have been revised and updated. Moreover, laboratory experiments were conducted to study the development and ecophysiology of this animal. These results were complemented with field studies on the gut contents and trophic markers ofC. marsupialis. Finally, the results of a four years monitoring in the coast of Denia (Spain), as well as the sightings of the species reported along the Mediterranean, provided solid evidence on the main factors affecting the distribution of C. marsupialis. Overall, the species seems to be favoured by high nutrient inputs from anthropogenic origin, and other human activities as coastal constructions. Los avistamientos de la cubomedusa Carybdea marsupialis han aumentado en el Mar Mediterráneo en los últimos años, hecho que ha sido atribuido a un incremento en su abundancia. El objetivo de esta tesis doctoral es responder algunas preguntas relacionadas con las posibles causas y efectos de este fenómeno. En primer lugar, se han actualizado la taxonomía y la distribución de la especie. Además, se han llevado a cabo experimentos relacionados con su desarrollo y ecofisiología. Estos resultados se han complementado con estudios de sus contenidos estomacales y marcadores tróficos en el campo. Finalmente, un monitoreo durante cuatro años en la costa de Denia (España), junto con los avistamientos de esta cubomedusa en el Mediterráneo, han proporcionado evidencias sólidas acerca de los factores principales que afectan la distribución de C. marsupialis. En general, la especie parece verse favorecida por el aporte de nutrientes de origen antropogénico, y por otras actividades humanas como las construcciones costeras. 3 General introduction Cubozoans, or box jellyfish, have received considerable attention from scientists and authorities from coastal areas because several species of this group represent a serious threat for human health. Numerous fatalities in tropical and subtropical coastal regions have been attributed to box jellyfish, also called cubomedusae or sea wasps (Bentlage et al. 2009; Keesing et al. 2016). The most venomous species are found in Australia, where they can cause important socio-economic losses (Bailey et al. 2004). Box jellyfish have been considered inconspicuous animals in the Mediterranean. However, in July 2008 a cubomedusae population outbreak was detected in Denia (NW Mediterranean, Spain), reaching unusual very high densities in some turistic beaches (Bordehore et al. 2011). The region is a popular turistic area, specially during the summer months, and several beach users were affected due to the presence of these organisms in the coast. That year, the Red Cross emergency services recorded more than 3,330 jellyfish stings along 17 km of coastline (Bordehore et al. 2011). This event had a significant impact on the media, wich highlighted “the detection of a new exotic species in the Mediterranean” identified as the cubomedusae Carybdea marsupialis (Van den Berg 2010). The sting of this species has been described to be painful but non fatal to humans, producing dermatitis (Peca et al. 1997). However, a sting case that resulted in cutaneous and systemic manifestations have been recently reported (Bordehore et al. 2015a). This escenario triggered the adoption of a monitoring strategy in order to develop management recommendations (Bordehore et al. 2011). Consequently, the LIFE CUBOMED project (www.cubomed.eu), comprising this and other PhD thesis (Bordehore 2014; Canepa 2014), started in 2010 with that purpose. The first necessary step was the correct identification of the species and the determination of its natural range of distribution. A significant progress in the taxonomy of cubozoans has taken place in the recent years (Gershwin 2005, Bentlage et al. 2010), thus we started our investigations from that point in order to properly determine the origin of the cubozoan species present in the Mediterranean. Afterwards, we proceed with the compilation and clarification of some basic and lacking information about the biology and ecology of the species in order to elucidate the possible drivers of the blooming episodes. Cubozoan life cycle As other cnidarians, cubozoans are characterized by alternation of benthic polyp and free- swimming medusa generations. The investigations in this thesis are focused on the cubomedusa stage; polyps have been observed in the wild only once for a carybdeid species (Studebaker 1972). We unsuccessfully searched for the polyps of C. marsupialis in the sea during the samplings conducted in the framework of the LIFE CUBOMED project. Moreover, during the PhD I have carried out several trials to rear a culture of C. marsupialis polyps in the laboratory; I managed to obtain the planulae 4 Introduction Fig. 1 Life cycle of Carybdea. (1) Male and female mating; (2) release of the fertilized egg into de water column; (3) settlement of planula larva on substrate after aprox. 2 days; (4) benthic polyp phase; (5) new polyps budding from existing polyps; (6) polyp metamorphosing into juvenile medusa; (7) release of juvenile cubomedusa. Drawing adapted from Studebaker (1972), University of Puerto Rico. Source: Bordehore et al. 2015b. larvae and the primary creeping polyps, but unfortunately the polyps did not survive. Hence, the knowledge for this life stage is still limited. Although the life cycle has not been completely clarified forC. marsupialis in the Mediterranean, similarities with another Carybdea sp. (= C. xaymacana, formerly considered as C. marsupialis, as demonstrated in Chapter 1 in this thesis) from Puerto Rico (Fig. 1) have been theorized (Studebaker 1972; Bordehore et al. 2015b). Fig. 2 Gonads of Carybdea marsupialis: (A) female gonads cross-section, scale bar = 10 μm; (B) male go- nads cross-section, scale bar = 50 μm. Pictures: Jimena García (USP). Introduction 5 Cubomedusae
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