Diet and Physiological Responses of Spondyliosoma Cantharus (Linnaeus, 1758) to the Caulerpa Racemosa Var

Journal of Experimental Marine Biology and Ecology 380 (2009) 11–19 Contents lists available at ScienceDirect Journal of Experimental Marine Biology and Ecology journal homepage: www.elsevier.com/locate/jembe Diet and physiological responses of Spondyliosoma cantharus (Linnaeus, 1758) to the Caulerpa racemosa var. cylindracea invasion Antonio Box a,⁎, Salud Deudero a,b, Antoni Sureda c, Andreu Blanco a, Josep Alòs d, Jorge Terrados d, Antoni Maria Grau e, Francisco Riera e a Laboratorio de Biología Marina Universidad de las Islas Baleares, Ctra Valldemossa Km 7.5 CP: 07122 Balearic Islands, Spain b Instituto Español de Oceanografia. Centro Oceanográfico de Baleares. P.O. Box 29107015, Palma de Mallorca, Spain c Sciences of the Physical Activity Laboratory, Fundamental Biology and Healthy Sciences Department, University of the Balearic Islands, Ctra. Valldemossa Km 7.5, E-07122 — Palma de Mallorca, Balearic Islands, Spain d Mediterranean Institute for Advanced Studies, IMEDEA (CSIC-UIB), C/ Miquel Marqués 21 E-07190, Esporles, Balearic Islands, Spain e Direcció General de Pesca, Govern de les Illes Balears, C/ Foners 10, 07006 Palma de Mallorca, Balearic Islands, Spain article info abstract Article history: Marine invasions are a worldwide problem that involves changes in communities and the acclimation of Received 30 January 2009 organisms to them. The invasive Chlorophyte Caulerpa racemosa var. cylindracea is widespread in the Received in revised form 11 August 2009 Mediterranean and colonises large areas from 0 to 70 m in depth. The omnivorous fish Spondyliosoma cantharus Accepted 12 August 2009 presents a high frequency of occurrence of C. racemosa in the stomach contents at invaded areas (76.3%) while no presence of C. racemosa was detected in control areas. The isotopic composition of muscle differed significantly Keywords: between invaded and non-invaded sites for δ13C(−16.67‰±0.09 and −17.67‰±0.08, respectively), δ15N Antioxidant enzymes ‰ ‰ Balearic Islands (10.22 ±0.22 and 9.32 ±0.18, respectively) and the C:N ratio (2.01±0.0002 and 1.96±0.009, respectively). Caulerpa racemosa Despite the high frequency of occurrence of C. racemosa in the stomach contents of S. cantharus and its important 13 15 Spondyliosoma cantharus contribution to the δ C source (20.7%±16.2), the contribution of C. racemosa to the δ NinS. cantharus food Stable isotopes sources was very low (6.6%±5.8). Other invertebrate prey such as decapods and polychaetes were more important contributors to the δ15N source at both invaded and non-invaded sites. Activation of enzymatic pathways (catalase, superoxide dismutase, glutathione-s-tranferase, 7-ethoxy resorufin O-de-ethylase) but not a significant increase in lipid peroxidation MDA (0.49±0.01 nmol/mg prot at non-invaded and 0.53±0.01 nmol/ mg prot at invaded sites) was observed in S. cantharus individuals living in C. racemosa-invaded sites compared with control specimens. The low δ15NcontributionvaluesofC. racemosa by S. cantharus together with the toxicity demonstrated by the activation of the antioxidant defences and the important contribution of invertebrate prey to the δ15N could mean that the ingestion of C. racemosa by S. cantharus might be unintentional during the predation of invertebrate preys living underneath the entanglement of the C. racemosa fronds and stolons mats. © 2009 Elsevier B.V. All rights reserved. 1. Introduction Boudouresque (Verlaque et al., 2003). Distance between south-west Australia and the Mediterranean points to Ship trafficandtheaquaria Around 100 macrophytes species are thought to have been trade as possible introduction vectors. Only 17 years after its first introduced into the Mediterranean Sea (Ribera, 2002). The invasive observation, C. racemosa var cylindracea (hereafter C. racemosa)has variety of Caulerpa racemosa (Forsskal) J. Agardh (Chlorophyta, Bryopsi- colonised 12 countries (Italy, Greece, Albania, Cyprus, France, Turkey, dales, Caulerpaceae) was observed for the first time in the Mediterra- Malta, Spain, Tunisia, Croatia, Algeria and Libya) (Klein and Verlaque, nean Sea in Libya in 1990 (Nizamuddin, 1991). Morphological and 2008). C. racemosa spreads in sheltered and exposed areas, colonising all molecular studies indicate that the invasive variety of C. racemosa in the kinds of substrates ranging from 0 to 70 m in depth (Argyrou et al., 1999; Mediterranean is similar to the south-west Australian endemic C. Piazzi and Cinelli, 1999; Zuljevic et al., 2003; Klein and Verlaque, 2008), racemosa var. laetevirens f. cylindracea (Sonder) Weber-van Bosse spreading over coralligenous bottoms and colonising important areas, therefore, the invasive form of C. racemosa in the Mediterranean was constituting an important threat to such communities (Piazzi et al., named as C. racemosa var. cylindracea (Sonder) Verlaque, Huisman et 2007; Klein and Verlaque, 2008). The fish Spondyliosoma cantharus (Linnaeus, 1978) (Black seabream) is a common species in the western Mediterranean and can be found ⁎ Corresponding author. Tel.: +34 971 17 33 52; fax: +34 971 17 31 84. over seagrass beds, especially in the case of juvenile individuals, and E-mail address: [email protected] (A. Box). rocky and sandy bottoms to about 300 m depth (Bauchot and Hureau, 0022-0981/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2009.08.010 12 A. Box et al. / Journal of Experimental Marine Biology and Ecology 380 (2009) 11–19 1990), Isolated rocks and reefs produce a concentration of larger contaminants in marine pollution monitoring (Sarkar et al., 2006). S. cantharus individuals. Previous studies about S. cantharus diet found Altogether, the detoxification process and the presence of the toxins that this species is an omnivorous fish with a wide spectrum of prey in the environment could lead to an increased production of reactive such as mysidacea, crustacean, polychaete, (Bell and Harmelin-Vivien, oxygen species (ROS). Thus, detoxification and antioxidant enzymes 1983), algae, copepods, amphipods and hydrozoans (Quéro, 1984; play a crucial role in maintaining cell homeostasis. These enzymes Goncalves and Erzini, 1998; Pita et al., 2002; Dulčić et al., 2006). have been proposed as biomarkers of contaminant-mediated oxida- According to these previous studies S. cantharus is considered as an tive stress in a variety of marine organisms, and their induction opportunist fish. The colonisation of the S. cantharus habitat, such as reflects a specific response to pollutants or toxins (Cossu et al., 1997). coralligenous bottoms, by invasive species could lead to changes in the The aim of the present work was to evaluate the importance of C. feeding strategies of this omnivorous species (Goncalves and Erzini, racemosa in the S. cantharus diet and the response of the detoxification 1998). The presence of Caulerpa species also leads to the presence of and antioxidant systems in the liver of individuals of this species toxic compounds inside the invaded area (Amade et al., 1994; Jung et al., living and feeding on C. racemosa-invaded areas. 2002; Box, 2008) and thus, the activation of the antioxidant defence systems we evidenced in the fish Coris julis (Linnaeus, 1758) living in 2. Materials and methods C. racemosa mats (Sureda et al., 2006) and in the invertebrate Bittium reticulatum (da Costa, 1778) introduced in aquariums containing 2.1. Study areas C. racemosa (Sureda et al., 2009). The use of stable isotope analyses in marine ecosystems is increasing, S. cantharus individuals were captured in Mallorca (SanTelmo, particularly for the measurement of carbon and nitrogen isotope Palma Bay, Cap Vermell and Alcudia Bay), Ibiza (Santa Eulalia and assimilation by organisms from food sources in trophic webs (Pinnegar Tagomago) and Formentera in the proximity of rocky areas at 36– and Polunin, 1999) and for the detection of the impact of fish farming 70 m depth. Once captured the stomach content was removed and the waste on adjacent environments (Sarà et al., 2004; Vizzini and Mazzola, presence or absence of C. racemosa in the stomach was recorded. 2006; Dolenec et al., 2007). In comparison to stomach content analysis, Having located individuals with/without C. racemosa in the stomach which provides information on recently ingested food sources, carbon contents, two invaded/non-invaded sites, i.e. colonised/non-colonised and nitrogen stable isotope analyses are a powerful tool for deciphering by C. racemosa, were checked visually by SCUBA (when possible until the cycling and contribution of multiple organic sources in food web 40 m depth). Areas invaded by C. racemosa were located in Palma Bay, dynamics (Deniro and Epstein, 1978; Fry and Sherr, 1984; Cabana and on the Mallorcan south coast, where C. racemosa is widespread Rasmussen, 1996; Pinnegar and Polunin, 2000; Fisher et al., 2001; (Gamundi-Boyeras et al., 2006) and S. cantharus is very common. Two Lorrain et al., 2002; Carabel et al., 2006; Marín Leal et al., 2008) providing different sites inside the bay (separated by more than 8 nautical information on the long-term diets of organisms (Dubois et al., 2007). miles) with a similar depth ranging from 25 to 34 m with coordinates The discrimination of organic matter sources has been made 39°29'55.24 N 2°42’33.85’’ E and 39°27'11.96" N 2°32'25.76"E respec- possible by the addition of C:N ratios to 13C determinations (Meyers, tively were selected as invaded areas. A non-invaded area was selected 1994). The use of δ13C values as evidence of dietary and trophic on the Mallorcan north coast and two sampling sites separated by more differences among species was validated by the examination of the than 10 nautical miles (Cap Vermell 39°34'42.48" N 3°24'40.12" E and relationship between biomass δ13C and biomass C:N (Dunton, 2001). Alcudia Bay 39°47'21.70" N and 3°18'35.40" E) were selected for capture The application of IsoSource mixing models to the main isotopic of S.

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