Journal of Experimental Marine Biology and Ecology 363 (2008) 130–136 Contents lists available at ScienceDirect Journal of Experimental Marine Biology and Ecology journal homepage: www.elsevier.com/locate/jembe Effect of salinity and temperature on feeding physiology and scope for growth of an invasive species (Brachidontes pharaonis - MOLLUSCA: BIVALVIA) within the Mediterranean sea G. Sarà a,⁎, C. Romano b, J. Widdows c, F.J. Staff c a Dipartimento di Ecologia, Università di Palermo, V.le delle Scienze - Ed. 16 - 90128 Palermo, Italy b C.N.R. - IAMC - Laboratorio di Ecologia della Fascia Costiera, Via G. da Verrazzano, 17 - 91014 Castellammare del Golfo (TP) Italy c Plymouth Marine Laboratory, Prospect Place, West Hoe, Plymouth PL1 3DH, United Kingdom ARTICLE INFO ABSTRACT Article history: The Indo-Pacific mytilid Brachidontes pharaonis (Bivalvia, Fischer 1870) offers an excellent model for the study Received 17 January 2008 of “Lessepsian migration” and the successive colonization at new Mediterranean locations. This species in out Accepted 28 June 2008 competing indigenous bivalves is particularly well adapted to Mediterranean conditions and this is likely due to biological characteristics and physio-ecological plasticity. In the present paper, we report on clearance rate Keywords: (CR), respiration rate (RR) and Scope for Growth (SFG) of B. pharaonis collected from a Western Sicilian pond Biological invasions (Southern Tyrrhenian, MED). Physiological variables were determined in response to a range of temperatures Brachidontes pharaonis fi Clearance rate from 11 ° to 20 °C and a broad range of salinities from 15 to 60 psu. Salinity and temperature had a signi cant Lesseptian migration influence on CR of B. pharaonis as there was a general reduction in CR with a decline in temperature from 20 °C Mediterranean to 11 °C and declining salinity from 37 to 15 psu. RR showed a general temperature dependent relationship with Scope for growth highest RR at 20 °C. SFG showed negative values at lowest salinity of 15 psu at all tested temperatures. SFG values were generally the highest at 45 psu (at 11 °C and 20 °C), although SFG showed a maximum at 37 psu at 15 °C. SFG values were positive over the broadest range of salinities (25 to 60 psu) at 20 °C. The plasticity of the physiological rates demonstrated that B. pharaonis had the capacity to maintain positive SFG and tolerate a wide range of temperature/salinity conditions. Possible implications of high physiological plasticity of B. pharaonis in competing against indigenous bivalves are discussed. © 2008 Elsevier B.V. All rights reserved. 1. Introduction (Decottignies et al., 2007) and life history strategy (MacDonald and Bayne, 1993). However, particularly successful invaders are those, Since the opening of the Suez Canal in 1869, more than 300 tropical which are able to feed on a wide variety of food types (viz. “generalist and subtropical species of algae, invertebrates and fish coming from feeders”), showing high fecundity and being able to tolerate broad the Red Sea and the Indian Ocean have dispersed through the Canal fluctuations in salinity and temperature. These organisms being and invaded the Eastern Mediterranean (Por, 1978; Galil, 2000, 2007). characterized by rapid growth rate and high potential of reproductive These have generated evident modifications in the local communities rates would be better colonizers (Kelly and Klasing, 2004). Many as some invaders have locally out competed or replaced native species hypotheses have been formulated in order to identify the properties of while some others are considered pests or cause nuisance (Baines et al., an invasive species and for explaining what determines its success 2005). They may represent one of the major threats to native biological (Jansen et al., 2007). Nevertheless this is still little understood and diversity and they can pose severe economic and ecological problems there are few experimental studies designed to test these hypotheses. (Sarà et al., 2006). Whether a non-indigenous or invasive species Thus, to evaluate potential risk and impacts on natural ecosystems, we persists and spreads in novel environments depends upon many need to understand the biological characteristics and ecological factors: predator pressure may prove to be significant (Safriel et al., plasticity of invasive species (Sarà, 2006). 1980) as also the resistance to diseases and parasites not previously The Indo-Pacific mytilid Brachidontes pharaonis (Bivalvia, Fischer encountered (Gottlieb and Schweighofer, 1996; Calvo et al., 2001), 1870) offers an excellent model for the study of this invasion called genetic variability (Mydlarz et al., 2006), breadth of trophic niche “Lessepsian migration” and the successive colonization of novel Mediterranean environments. Originally from the Indo-Pacific area, mainly south-eastern Asia (Terranova et al., 2007), it appeared to be a species tolerant to high salinity, which has colonised hard substrata as ⁎ Corresponding author. University of Palermo, Via delle Scienze, Pd. 16, I-90128 Palermo, Italy. Tel.: +39 091 6657932; fax/lab: +39 091 6657937. far away as the Red Sea, where it has established dense mussel mats E-mail address: [email protected] (G. Sarà). (Safriel et al., 1980). In the last few decades, this small mytilid has been 0022-0981/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2008.06.030 G. Sarà et al. / Journal of Experimental Marine Biology and Ecology 363 (2008) 130–136 131 able to colonize many intertidal habitats from Israel to the western Experiment II: Animals were also held at a single temperature of Mediterranean coasts. However in western Mediterranean, until 20 °C and three groups were held under hyper-saline conditions of 50, recently (1994–2000; Sarà et al., 2000), B. pharaonis has remained 55 and 60 psu, thereby providing a range of seven salinities from confined in a few suitable habitats with similar environmental features brackish to hyper-saline (i.e. 15 to 60 psu) at a single temperature of to Red Sea Egyptian salt lakes (sensu Safriel et al., 1980; high salinity) 20 °C. Mortality was generally low (3.5%), and the same for most of the such as ephemeral coastal pools and salt-ponds (Sarà et al., 2003). These conditions, but it was slightly higher at 15 psu (6.6%). extreme habitats may function as high-density hot spots (sensu the For each group, clearance rate, food adsorption efficiency and stepping stones hypothesised by Steinitz, 1968) for further spread into respiration rate were measured according to procedures reported the whole western Mediterranean basin to Gibraltar. Instead, in the last by Widdows and Staff (2006).Eachday,fifteen animals were used five-seven years, B. pharaonis has been more frequently found in many to measure the physiological responses for each temperature and salinity marine intertidal habitats of the Tyrrhenian Sea (Sarà and Buffa, 2004; condition. Clearance rate, or the volume of water cleared of suspended Sarà et al., 2007) where it is establishing dense beds on natural particles per hour, was measured in a closed system. Individuals and artificial hard substrata, out competing indigenous bivalves like were placed in separate beakers containing 2 L of filtered seawater Mytilaster minimus and Mytilus galloprovincialis (Safriel and Sasson- positioned on multi-stirrer base plates to keep the water thoroughly frostig, 1988; Sarà et al., 2007). This may reflect that B. pharaonis is mixed and oxygenated. After a period of 20 min, to allow the mussels to spreading throughout the western Mediterranean colonising not only open and resume pumping, algal cells (Isochrysis galbana) were added to small patches of confined hyper-salinity habitats, but also wider zones each beaker to give an initial concentration of 24,000 cells ml−1.Twenty of marine intertidal environments with more oceanic features. ml aliquots were sampled from each container at 20 min intervals over a The aim of the present paper is to study the eco-physiology of period of 80 min, and the decline in cell concentration was monitored B. pharaonis under varying physical factors (temperature and salinity) using a Coulter Counter (Model D). Control tanks, without mussels, and to test the physiological tolerance of this invasive mussel to a broad showed no significant decline in cell concentration over the experimental range of salinities from brackish, through typical elevated Mediterra- period. The clearance rate was then calculated using the following nean salinities, to extreme hyper-saline conditions. B. pharaonis is equation:- known to be well adapted to elevated temperatures, based on its ð −1Þ¼ ð − Þ = ð Þ invasion via the Red Sea, but there is no information on the mussel's CR 1h 2L loge C1 loge C2 time interval h response to the lower temperatures found in the Mediterranean Sea. where C and C are the cell concentrations at the beginning and end Such information will be useful when assessing the species' colonization 1 2 of each time increment (i.e. every 0.33 h). process and predicting its future possible geographical spread. This will Respiration rate was determined by placing individual mussels in also be important when assessing the future potential expansion of glass respirometers (500 ml) containing air-saturated seawater, which invasive species under conditions of increasing temperature and salinity was stirred by a magnetic stirrer bar beneath a perforated glass plate in the Mediterranean Sea, as a result of global warming, where tropical supporting the mussel. The respirometer was sealed and the decline in invasive species would have distinct advantage over native species. oxygen concentration was measured by means of Strathkelvin oxygen electrodes (model 1302) connected to Strathkelvin oxygen meters 2. Materials and methods (model 781). Food absorption efficiency was measured by comparing the 2.1. Sample collection and experimental set-up proportion of organic matter in the algal cells and the mussel faeces. Algal food and faecal samples were collected on washed, ashed and Specimens of the bivalve Brachidontes pharaonis of similar shell pre-weighed GFC filters.