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Biological Interactions Between Fish and Jellyfish in the Northwestern Mediterranean

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Biological Interactions Between Fish and Jellyfish in the Northwestern Mediterranean Biological interactions between fish and jellyfish in the northwestern Mediterranean Uxue Tilves Barcelona 2018 Biological interactions between sh and jellysh in the northwestern Mediterranean Interacciones biológicas entre meduas y peces y sus implicaciones ecológicas en el Mediterráneo Noroccidental Uxue Tilves Matheu Memoria presentada para optar al grado de Doctor por la Universitat Politècnica de Catalunya (UPC), Programa de doctorado en Ciencias del Mar (RD 99/2011). Tesis realizada en el Institut de Ciències del Mar (CSIC). Directora: Dra. Ana Maria Sabatés Freijó (ICM-CSIC) Co-directora: Dra. Verónica Lorena Fuentes (ICM-CSIC) Tutor/Ponente: Dr. Manuel Espino Infantes (UPC) Barcelona is student has been supported by a pre-doctoral fellowship of the FPI program (Spanish Ministry of Economy and Competitiveness). e research carried out in the present study has been developed in the frame of the FISHJELLY project, CTM2010-18874 and CTM2015- 68543-R. Cover design by Laura López. Visual design by Eduardo Gil. esis contents THESIS CONTENTS Sum m a r y 9 Gen eral In tro d uctio n 11 Obje ctive s a n d the sis o utlin e 30 Digestion times and predation potentials of Pelagia noctiluca eating CHAPTER 1 sh larvae an d cop ep od s in the NW Med iterran33 ean Sea Natural diet and predationPelagia noctiluca im pactso n fis hof CHAPTER 2 eggs an d larvae in the NW Med iterran ean57 Tro p hic in teractio n s Pelagiao f the noctiluca jellysh i n t he NW Mediterranean: evidence from stable isotope signatures and fatty CHAPTER 3 a ci d co m p o s i t i o n 79 As s o ci a t i o n s be t we e n s h a n d je l l ys h i n t he NW CHAPTER 4 Med iterran ean 105 Gen eral D iscussio n 131 Ge n e ra l Co n clusio n 141 Ackn o wled gem en ts 145 Ap p e n d i ce s 149 Summary 9 SUMMARY Jellysh are important components of marine ecosystems, being a key link between lower and higher trophic levels. Jellysh blooms occur sporadically and unpredictably in coastal areas and oen have important socio-economic consequences for sheries and tourism. is PhD thesis addresses some questions regarding the potential impact, positive and/or negative, that jellysh have on sh populations in the Catalan coast (NW Mediterranean). Firstly, the natural diet of one of the most abundant jellysh in the aa, rethe scyphomedusa Pelagia noctiluca , was studied analyzing its gut contents and conducting biomarker analyses (stable isotopes and fatty acids). ese results were complemented with laboratory experiments to calculate their digestion times and also with the records of sh larvae and jellysh abundances in the eld. All together, these results were used to estimate the potential feeding impact ofP. noctiluca on sh eggs and larvae and competition between both groups of organisms. Results suggest that the potential consumption of ichthyoplankton by the jellysh and competition between them may be high. Secondly, the association between the jellysh Rhizostoma pulmo and Cotylorhiza tuberculata and the carangid shes Trachurus mediterraneus, Trachurus trachurus and Caranx rhonchus was studied in detail. For this purpuse, eld observations of jellysh and their hosted sh were carried out during Summary 10 summer to describe sh behavior. Moreover, Las medusas son componentes laboratory experiments were performed to importantes de los ecosistemas marinos ya determine the survival capability of the jellysh- que son un vínculo clave entre el zooplancton associated sh to the venom of their hosts. más pequeño y los niveles trócos superiores. Finally, biomarker analyses were conducted to L as proliferaciones de medusas ocurren understand the signicance of the association. esporádica e impredeciblemente en áreas All this information demonstrated the benet costeras y con frecuencia tienen importantes of the association for the sh. consecuencias socioeconómicas para la pesca y el turismo. Esta tesis doctoral aborda algunas cuestiones relacionadas con el potencial impacto de las medusas, tanto positivo como negativo, sobre las poblaciones de peces en la costa catalana (NO Mediterráneo). En primer lugar, se estudió la dieta natural de una de las medusas más abundante en la zona,Pelagia noctiluca , analizando su contenido estomacal y sus biomarcadores (isótopos estables y ácidos grasos). Estos resultados se complementaron con sus tiempos de digestión (obtenidos mediante experimentos de laboratorio) y también con las abundancias en mar abierto de larvas de peces y medusas. En conjunto, estos resultados demostraron que el potencial impacto de depredación deP. noctiluca sobre huevos y larvas de peces es alto y que existe una probable competencia entre ambos grupos por el alimento. En segundo lugar, se estudió la asociación entre las medusasRhizostoma pulmo y Cotylorhiza tuberculata y los peces carángidos Trachurus mediterraneus , Trachurus trachurus y Caranx rhonchus . Para ello, se estudió durante el perí odo de verano el comportamiento en el mar de los peces asociados. Además, se realizaron experimentos de laboratorio para determinar la capacidad de supervivencia de estos peces al veneno de sus medusas antrionas. Finalmente, se realizaron análisis de biomarcadores para comprender la importancia de estas asociaciones. Toda esta información demostró el benecio obtenido por los peces cuando se asocian a medusas. General Introduction 11 GENERAL INTRODUCTION Gelatinous zooplankton: what is it? Sin ce gelatinous zooplankton refers to several groups of planktonic organisms, taxonomically and functionally diverse, and taking into account that dierent authors do not always refer to the same groups using this denition, it is important to dene which groups we indicate in this work. e term gelatinous zooplankton comprises those organisms with similarities in their body (high water content and gelatinous consistency) and in having a planktonic stage within their life cycle. us, this terminology includes pelagic cnidarians and ctenophores (comb jellies), and pelagic tunicates (invertebrate chordates: salps, doliolids and pyrosomes). What is called jellysh refers to the pelagic stages of four classes of the Cnidaria subphyla: Hydrozoa, Cubozoa, Scyphozoa and Staurozoa. As the rest of the members of the phylum Cnidaria, all of them possess mechanoreceptor cells called cnidocytes (stinging cells) that are used for defense/oense purposes when cnidarians interact with other organisms. Gelatinous zooplankton is an important component of pelagic ecosystems (Mills 1995, Purcell et al. 2007), because they play a key role as predators and competitors that can modulate the structure and dynamics of planktonic food webs (Purcell 1997, Purcell & Arai 2001, Arai General Introduction 12 2005). ey have been considered a trophic 2012, Condon et al. 2012). Whether there is an dead-ends for decades (Sommer et al. 2002, increase of jellysh blooms or not, evidences Lynam et al. 2006) due to their high water (> suggest that jellysh populations experienced 97%) and low carbon (up to 2.9%) content prolonged periods of high abundance (Condon (Lucas et al. 2011), but nowadays several et al. 2013). evidences highlighted the importance of these organisms as prey for diverse marine predators, Dierent mechanisms are thought to be such as sea birds, invertebrates, leatherback responsible for the upward trend of gelatinous sea turtles and an underestimated number of zooplankton and, although the increasing sh species (Arai 1988, Purcell & Arai 2001, pattern may be local, the mechanisms involved Arai 2005). As an example, Pelagia noctiluca could act at a global scale. ese factors has been found to be part of the diet of the shinclude climate change, which may enhance Boops boops in the Mediterranean (Milisenda et reproduction rates and favour species wider al. 2014), although the scyphomedusae have 20 dispersion (Brodeur et al. 1999, Lynam et al. times less energy density than the co-occurring 2004, Purcell 2005, Attrill 2007); introduction sh (Cardona et al. 2012). Another example is of alien species (Shiganova 1998, Graham the bristle worm,Hermodice carunculata, which & Bahya 2007); eutrophication, which may has been indicated as a consumer Cassiopeaof increase nutrients and zooplankton availability spp. in the Bahamas (Stoner & Layman 2015). (Arai 2005, Purcell & Benović 1999); habitat modication, by increasing suitable substrates Jellysh blooms for polyp settlement (Duarte et al. 2013); and removal of jellysh predators by overshing Most jellysh are considered as planktonic (Purcell & Benović 1999, Lynam et al. 2006). organisms, which means they live suspended in the water column with limited movements Increase of gelatinous organisms is against the currents and occasionally form considered as a potential indicator of ecological “blooms” (rapid increases in abundance within changes in marine ecosystems (Mills 2001, a short period of time) (Graham et al. 2001, Purcell 2005, Purcell et al. 2007, Richardson Hamner & Dawson 2009). When these rapid et al. 2009) usually dominated by forage shes changes in jellysh abundance are due to a rapid (Boero 2013). Jellysh populations present population growth, they are considered a “true extended periods of high abundance (Condon bloom” (hereaer called simply bloom) while et al. 2013) and in ecosystems supporting major the re-distribution or re-dispersion of a stable forage sh sheries these periods of high jellysh population by environmental forcing is called abundance coincide with low abundance of “apparent bloom” (Graham et al. 2001). Jellysh sh (Decker et al. 2014, Brodeur et al. 2014, blooms appear to be increasing in number and Mianzan et al. 2014) suggesting a jellysh-sh frequency in some areas of the world (Brodeur replacement cycles (Robinson et al. 2014). It et al. 2002, Purcell 2005, Attrill et al. 2007), but should be pointed out that jellysh are known there is still controversy about their increase to be able to survive in degraded environments at a global scale (Mills 2001, Brotz & Pauly due to dierent physiological and biological General Introduction 13 attributes that give them an advantage over other animals (including shes) and could explain the shi in ecosystem structure (Richardson et al.
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