Trophic ecology of Trachurus mediterraneus juveniles associated with the jellyfish Rhizostoma pulmo and Cotylorhiza tuberculata
Introduction
Symbiotic interactions are common in nature and are important for sustaining species populations. The association between fish and jellyfish is a temporary commensalism and was described for the first time by Marteens (1671) (Karplus, 2014). Although fish-jellyfish association is considered facultative, the population dynamics of some fish species rely heavily on the abundance of jellyfish (Lynam and Brierley, 2007). There are 96 fish families reported to be associated with floating objects and jellyfishes, especially those of the scyphozoan order, and the most common fish are Carangidae, Stromatidae and Gadidae (Purcell and Arai, 2001). Even though interest in the relationships in the pelagic realm has recently increased (Ohtsuka et al., 2010), the significance of these interactions is poorly understood (Purcell and Arai, 2001). Different hypotheses have been suggested to explain this association (reviewed in Mansueti, 1963; Arai, 1988; Purcell and Arai, 2001): protection to juvenile fish from predation (e.g. Fréon and Dagorn, 2000), provisioning of food by feeding on the zooplankton captured by jellyfish (e.g. Masuda, 2009) or on the actual host jellyfish (e.g. D'Ambra et al., 2015), transportation to favourable areas (e.g. Castro et al., 2002; Masuda, 2009) and “meeting point” for school formation (e.g. Fréon and Dagorn, 2000; Castro et al., 2002; Masuda, 2009). In the Mediterranean, different observations of fish sheltering underneath scyphozoan bells have been reported but very little is known about the trophic interactions between scyphozoan and their hosts and the effect of this association on fish recruitment (D'Ambra and Malej, 2015). In particular, juveniles of Trachurus mediterraneus have been reported to be associated with floating objects (Massutí et al., 1999; Deudero and Morales-Nin, 2001) and scyphozoan jellyfish such as Rhizostoma pulmo, Cotylorhiza tuberculata (D'Ambra and Malej, 2015; Tilves et al., 2018) and Pelagia noctiluca (Sabatés et al., 2018).
R. pulmo and C. tuberculata are two of the most abundant coastal scyphozoan species in the northwestern Mediterranean during the summer period (Gili et al., 2009; Fuentes et al., 2011; D'Ambra et al., 2015) and they can reach large numbers during blooming years (Mariottini and Pane, 2010). Both species feed on planktonic organisms (Perez-Ruzafa et al., 2002), and C. tuberculata has an autotrophic capacity due to the presence of zooxanthellae in the inner tissue (Leone et al., 2013). Although the interest in studying jellyfish has increased in recent years (Purcell et al., 2007), the ecology of this group and the relevance of the relationships between jellyfish and other organisms is still unknown (Karplus, 2014).
The Trachurus genus belongs to the Carangidae family (Perciformes) and is distributed throughout the Mediterranean Sea. Within this genus, the Mediterranean horse mackerel, Trachurus mediterraneus, is a semipelagic species that inhabits the continental shelf and is distributed throughout the Mediterranean and the northeastern Atlantic (Smith-Vaniz, 1986). In the Mediterranean, T. mediterraneus spawns during the spring and early summer (Karlou-Riga, 2000; Raya and Sabatés, 2015), thus juveniles can be found in the pelagic environment in summer and early autumn. T. mediterraneus is a carnivorous species that feeds on zooplanktonic organisms (Deudero and Morales-Nin, 2001; Šantić et al., 2004; Fernandez-Jover et al., 2007). However, there is a lack of information about the diet of juveniles associated with jellyfish.
This study aims to gain a deeper understanding of the ecological role of the association between fish and jellyfish. The specific goals were 1) to analyse the natural diet and feeding selectivity of T. mediterraneus juveniles associated with the jellyfish R. pulmo and C. tuberculata on the Catalan coast (NW Mediterranean), 2) to determine whether the diet composition of the hosted fish could depend on the jellyfish species, and 3) to explore if the fish could feed on the host jellyfish.
Section snippets
Sample collection
Sampling of jellyfish and their associated fish was conducted biweekly off Barcelona (NW Mediterranean; 41° 23′ 2.4´´N, 2° 12′ 17.1″E in a radius of 20 km), from July to September 2011, between 09:00 and 16:00 h. Jellyfish together with their associated fish were collected from the boat using a hand net or by snorkelling near the surface at depths up to 10 m. The jellyfish was identified and measured (bell diameter) and the hosted fish were immediately fixed in 5% formaldehyde buffered with
Prey environment
The ocean zooplankton community (average summer values) collected with each jellyfish species and their associated fish was dominated by cladocerans and copepods (Table 1). Among them, the cladocera Evadne spp. and the Clauso-Para-Calanidae copepods were the most abundant groups, representing >45% and 20%, respectively. Other groups, such as Appendicularia, were also relatively abundant, accounting for 5.51%. A high similarity was found between the zooplankton composition sampled with each
Discussion
The association between juvenile fish and jellyfish is temporary and restricted to a relatively short period in the life of the fish (Karplus, 2014). In our study, the size of T. mediterraneus associated with C. tuberculata and R. pulmo ranged between 11 and 61 mm SL; this last size corresponds to the juvenile pre-recruitment stage (Karlou-Riga, 2000). This size range fits that previously reported for different Trachurus species associated with jellyfish (Mansueti, 1963; Masuda, 2006; Tilves et
Conclusions
The present study reports, for the first time, the natural diet of T. mediterraneus juveniles in association with the jellyfish R. pulmo and C. tuberculata. Both jellyfish species, and their associated fish, were collected in surface waters. However, while the diet of juveniles associated with C. tuberculata was quite similar to that of the surface ambient zooplankton, with the cladocera Evadne spp. and Calanoida copepods as the most abundant prey, the diet of fish associated with R. pulmo was
Funding
This work was supported by the Spanish Ministry of Economy and Competitiveness (CTM2010-18874 and CTM2015-68543-R). JM was supported by a predoctoral FI-AGAUR fellowship of the University and Research Grants Management Agency (AGAUR) of the Government of Catalonia (Generalitat de Catalunya) (FI_B_00412).
Acknowledgments
We are especially grateful to Josep Maria Gili for his advice in the identification of nematocyts. We also thank Vanesa Raya and Balbina Molí for their advice at the laboratory work.
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