Marine Biodiversity Records, page 1 of 7. #2006 Marine Biological Association of the United Kingdom doi:10.1017/S175526720600087X; Vol. 1; e8; 2008 Published online A new lessepsian species in the western Mediterranean ( pharaonis : ): density, resource allocation and biomass g. sarÆ, c. romano and a. mazzola Dipartimento di Biologia Animale, Universita` di Palermo, Via Archirafi, 18, 90123 Palermo, Italy

The present study reports on population dynamics and growth performance relative to a lesser known exotic invasive species (Brachidontes pharaonis) inhabiting the southern Mediterranean. The study was carried out in western Sicily, where B. pharaonis is present on both the submerged and emerged surfaces of a hyperhaline saltpan. Individuals were scraped, counted and measured for shell length, total weight, somatic, gonadic and shell biomass. Brachidontes pharaonis intensively colonized all hard substrates of the saltpan with annual average densities of 375 + 293 ind. 400 cm22 with density peaks in autumn as a function of habitat. The occurrence of juveniles was different for mediolittoral and infralittoral populations as was mean size, spawning periods and annual organic matter biomass. Organic matter allocated to the shells represented 56.4% (of the total), gonad allocation was 7.3%, while somatic allocation averaged 36.3% for both populations. Brachidontes pharaonis reached high individual density, rare among temperate members of the genus Mytilus in Mediterranean and European waters, but common in tropical dense beds. Considering its invasive potential and the recent warming trend of the Mediterranean, in the future B. pharaonis may actively invade more habitats, threatening indigenous bivalve species which may be unable to compete with B. pharaonis in terms of reproductive effort and density.

Keywords: mussel, Brachidontes pharaonis, lessepsian, invasive species, Mediterranean

INTRODUCTION Other invasive bivalves, like Musculista senoushia and Dreissena polimorpha, have rapidly spread from their geo- Biological invasion by non-indigenous species is among the graphical origins through Europe and North America. main concerns for alteration of ecosystem dynamics and These two species of non-indigenous bivalves are considered world-wide community structure (Carlton, 1992, 1999). In pests because of their capacity to interfere with human aquatic habitats, successful invaders are abundant, have activity and with the survival of similar native species broad feeding niches in their native range, and are able to (Inoue & Yamamuro, 2000; Allen & Williams, 2003; Mistri, live in a wide range of physical conditions (Ehrlich, 1984; 2003). Although B. pharaonis does not seem, to date, to McMahon, 2002). When they find appropriate life conditions, have the same explosive invasive potential as other invader they may form highly dense mats, competing for space and species, its dispersion range, though no smaller, has yet to resources with indigenous species, altering the functioning be studied adequately. In recent decades the rapid warming of entire ecosystems. The bivalve mollusc Brachidontes of European Mediterranean waters (the mean temperature pharaonis (Fischer P., 1870) is just such an invader. of the Mediterranean has increased at least 38C from Originally from the Indo-Pacific area, mainly south-eastern 20–218Cto23–248C and salinity has risen by at least Asia, it has colonised hard substrata as far away as the Red 1–2 psu in less than ten years) is creating favourable con- Sea, where it has established dense mussel mats (Gilboa, ditions for invasion by some exotic species (Root et al., 1976). In the last few decades this small mytilid has been 2005), possibly enhancing the invasive capacity of B. able to colonize many intertidal habitats from Israel to the pharaonis, a species well-adapted to tropical temperatures western Mediterranean coasts via the Suez Canal, which (Safriel & Sasson Frostig, 1988). To predict a species’ possible opened in 1869. To date, in the western Mediterranean, B. dispersion route and degree of diffusion, it is first necessary pharaonis is confined to a few high temperature, high salinity to assess its capacity to adapt to new environments habitats where it has established dense beds on hard substrata. (McMahon, 2002). This study reports on population It has been predicted that from these areas, B. pharaonis will dynamics and growth of this invasive species inhabiting the continue its migration towards North Africa and Gibraltar southern Mediterranean. Our main objectives are: (a) to (Sara` et al., 2000). investigate B. pharaonis bivalve density, demography and size; and (b) to study its resource allocations. The overall

Corresponding author: aim is to assess the tolerance limits of this species in order G. Sara´ to predict the degree and capacity of its dispersal in new Email: [email protected] environments.

Downloaded from https://www.cambridge.org/core. University of Athens, on 08 Oct 2021 at 00:33:05, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms1 . https://doi.org/10.1017/S175526720600087X 2g.sarÆet al.

MATERIALS AND METHODS

Study area and sample collection The study was carried out in the Stagnone di Marsala saltpan system (western Sicily: 378520N128280E) between January and December 1999. Brachidontes pharaonis is present in an enclosed cooling vat (60,000 m2; 48,000 m3; 80 cm average depth) of an evaporation basin and dominates the mediolit- toral (hereafter, emergent or surface population; SF) and the upper infralittoral (i.e. the constantly submerged water stones on the bottom—hereafter, submerged population; SB) substrata. A channel is occasionally opened by salt workers to allow the inflow of water from the adjacent sound, the Stag-none di Marsala. At other times, the balance between evaporation and rainfall controls the hydrodynamics and the water level. The basin is characterized by daily wind- induced cycles of resuspension/deposition of sediments Fig. 1. Seasonal means of water temperature (8C; left axis – filled square) and (Sara` et al., 2000). The sand-mud bottom is covered by salinity (‰; right axis, open circle). Standard deviations are reported. the sea grass Cymodocea nodosa, while Cystoseira sp., Chaetomorpha linum (O.F. Mu¨ller) Ku¨tzing and Laurencia Statistical analyses and elaboration papillosa (C. Agardh) Greville are the dominant macroalgae. In the vat, phytoplankton density is quite low (Sara` et al., Shell length frequency distributions in 3-mm size-class inter- 1999, 2000; Pusceddu et al., 1999), with annual average vals, were developed from pooled quadrats for each plot chlorophyll-a concentrations of 0.9 + 0.4 mg121 (range during each season. Shell length and total weight seasonal 0.5–1.7 mg121), while the microphytobenthic biomass, as data from each population (SF and SB) were transformed expressed by chlorophyll-a concentrations measured in sedi- into natural logarithms and fitted to the allometric regression ments, shows a higher annual average than that measured model (TW ¼ aSLb; Gould, 1966; LaBarbera, 1989). in the western Mediterranean (3.9 + 2.1 mgg21 - range Differences between population densities were assessed with 1.6–6.7 mgg21; G. Sara`, unpublished data). the U-test (Sokal & Rolhf, 1981), while differences in pro- portion of resource allocation (soma, gonads and shell AFDWs) between the two populations in each season were Sampling tested with a Q-test (Sokal & Rolhf, 1981). Brachidontes pharaonis populations were sampled four times from December 1998 to November 1999. Samples from three RESULTS plots (about 1 m2 each) were randomly chosen from the upper margin of the saltpan wall, from the lower parts of the wall, Density and demography and from the submerged stones. In each plot, a quadrat (20 cm 20 cm ¼ 400 cm2) used three times delimited the Brachidontes pharaonis densely covered all hard substrates of area (400 cm2) from which all individuals were scraped by the saltpan with an annual average number of individuals of means of a putty knife and counted directly in the field. The 375 + 293 per 400 cm2. Brachidontes pharaonis colonized seasonal mean data presented in this paper represent the surface substrates (on annual average 499 + 380 individuals average mean of the quadrat samples for the three plots per 400 cm2) with a peak density in autumn (P , 0.05) and (+standard error). lowest densities in summer (P , 0.05; Figure 2). In contrast the submerged B. pharaonis population (on annual average 252 + 122 individuals per 400 cm2) showed a significant Population dynamics and biomass density peak in winter and lowest density in summer. The mode of the emergent population throughout the year About 10% of individuals from each quadrat were randomly was the 21–24 mm size-class (Figure 3). Smaller individuals chosen and brought back to the laboratory where they were (about 1 cm long) appeared mainly in spring and autumn rinsed free of silt and debris. Shell lengths (SL, the greatest representing 4% and 2% of the population, respectively. anterior-posterior axis; mm) of all individuals were measured Individuals in the largest size-class (.33-mm, to 36-mm to the nearest 0.1 mm with a digital calliper and the total wet and over) of the population were present, although in low weight (TW, g) of individuals emptied of cavity water was numbers (~1–1.5%), throughout the year. The dominant measured to the nearest 0.1 mg. Shells and soft tissues were modal class of the submerged population was larger than separated and dried to a constant weight at 1058C (~48 h) that of the emergent population (24–27 mm in winter). The and were then combusted at 5008C for 4 h to obtain occurrence of juveniles was spread throughout the year, as ash-free dry weights of valves and somatic tissue (AFDW; g) individuals from the small size-class (between 6 and 15 mm) to the nearest 0.1 mg. In all individuals greater than 10 mm were present in winter, spring and summer, at about 9%, SL, gonads were separated from somatic tissue and analysed 6% and 5.5%, respectively. Larger individuals (size-class to obtain ash-free dry weights of the gonadic tissues 30–36 mm) were present only in spring and summer and (AFDW gonad; g). represented 5% and 6.3% of the total population.

Downloaded from https://www.cambridge.org/core. University of Athens, on 08 Oct 2021 at 00:33:05, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S175526720600087X brachidontes pharaonis: an invasive bivalve in the southern mediterranean 3

submerged population showed highest peaks in summer and autumn (see Table 1 intercept values). Submerged individuals have a slightly higher allometry (b ¼ 2.4) than the emergent population throughout the year (b ¼ 2.2); allometry was lower in winter when the submerged population showed a minimum (b slope ¼ 2.0) and higher in summer (b ¼ ~2.6) for both populations.

Resource allocation The annual biomass organic matter (Figure 4) was on average 0.15 + 0.07 mg in the emergent population and 0.14 + 0.02 mg for the submerged group. Emergent AFDW was not different (P . 0.05) from submerged AFDW in winter and similar in summer and autumn. The OM biomass was signifi- cantly higher in the submerged population in spring. Differential organic matter allocation between shells, gonads Fig. 2. Seasonal mean density of Brachidontes pharaonis (individuals per and flesh is reported in Figure 5. Organic matter allocated 400 cm2) collected in triple replicates from surface and submerged to the shells represented on average 56.4 + 8.8% (of the populations by means 400 cm2 quadrats. Standard deviations are reported. total) for both populations. Shell organic matter was on average higher in the surface population (60.4 + 1.9% and Growth 52.4 + 11.1% emergent and submerged populations, respect- ively), and both populations showed peaks in autumn (about In Table 1 the outcome of seasonal regressions of each popu- at 63%) and lower values in winter (60% and 39%, emergent lation are summarized. The surface population showed and submerged populations, respectively). Gonad organic highest intercept values in winter and summer, while the matter allocation represented on average 7.3 + 4.2% of the

Fig. 3. Seasonal length-frequency histograms of Brachidontes pharaonis populations (Size class ¼ 3 mm).

Downloaded from https://www.cambridge.org/core. University of Athens, on 08 Oct 2021 at 00:33:05, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S175526720600087X 4g.sarÆet al.

Table 1. Seasonal ln-transformed length-total weight relationships of each population of Brachidontes pharaonis.

SF SB

a + SE b + SE R Pa+ SE b + SE R P

Winter 28.0 0.16 2.6 0.05 0.94 26.5 0.18 2.0 0.05 0.87 Spring 27.5 0.17 2.4 0.05 0.88 28.1 0.19 2.5 0.06 0.95 Summer 28.0 0.22 2.6 0.07 0.95 28.4 0.19 2.7 0.06 0.96 Autumn 27.5 0.12 2.4 0.04 0.88 28.5 0.17 2.7 0.05 0.95

(SF, surface population; SB, submerged population; +SE, standard error for means; a, regression intercept; b, regression slope; , P , 0.05; , P , 0.01; , P , 0.001; n.s. ¼ not-significant difference - P . 0.05).

total for both populations. Gonad allocation was seasonally beds ( perna; Hicks et al., 2001) and among small myti- higher in the submerged population (8.3 + 5.4% vs 7.0 + lids such as Musculista senoushia, another Mediterranean 3.4% in surface). The emergent population showed peaks in invader bivalve. The latter occurs at densities typically up gonad allocation during the winter (11.3%) and spring 10,000 ind. m22 in the northern Adriatic where they are threa- (8.5%), whereas peaks occurred in the submerged population tening endemic populations of other bivalves and most in spring (12.2%) and summer (12.8%). Adriatic shellfish farms (Mistri, 2003). Unlike other small Somatic allocation of organic matter represented on mytilids, there is little data on the worldwide density and dis- average 36.3 + 9.2% of the total for both populations, tribution of Brachidontes pharaonis. It reaches about 9000 ind. though it was higher in the submerged population (40.1 + m22 in India (Rajagopal et al., 2003) and in South East Asia 12.6% vs 32.6 + 2.1% in surface). The submerged popu- (Morton, 1988). Nevertheless, the density of B. pharaonis lation’s main peak of somatic allocation was verified in appears to increase as one moves from Indo-Pacific habitats winter (about 60%), while it was highest during summer through the Red Sea (density 4000 ind. m22; Safriel & (35%) in the surface population. Sasson-Frostig, 1988), and the Suez Canal lakes (density 6100 ind. m22; Mohammed, 1997). On the Israeli coasts and in the eastern Mediterranean, however, its density abruptly decreases (density 100 ind. m22; Safriel & DISCUSSION Sasson-Frostig, 1988). Going toward the Western Basin the species reaches its highest density in the saltpan discussed In western Sicily Brachidontes pharaonis reached high indi- here. In the study area B. pharaonis reached a mean shell 22 vidual density (annual average about 10,000 + 7300 ind. m ) length of about 22 mm with a maximum size over 22 with peaks in autumn (over 25,000 ind. m ). Such densities 36–40 mm. By contrast, studies on B. pharaonis from other are rare among temperate members of the genus Mytilus in parts of the world showed that shell length in Hong Kong Mediterranean and European waters. In central Tyrrhenian reached about 20 mm maximum (Morton, 1988), and waters, Ardizzone et al. (1996) found Mytilus galloprovincialis 22 mm in India (Rajagopal et al., 2003). When moving to 22 beds did not exceed 13,000 ind. m in sporadic yearly peaks, the Red Sea and the eastern Mediterranean, however, mean while in the Adriatic M. galloprovincialis bed densities were shell length decreased to about 18 mm maximum in the Red 22 not more than 2000 ind m (Ceccherelli & Rossi, 1984). Sea (Gilboa, 1976), on the Israeli coasts (Safriel & Ritte, Similar densities, however, are common in tropical mussel 1985), and in the Egyptian Suez sites (Mohammed, 1992,

Fig. 4. Seasonal total biomass (mg) of Brachidontes pharaonis from surface Fig. 5. Seasonal percentages of differential allocation to soma, shell and and submerged populations. gonads of Brachidontes pharaonis from surface and submerged populations.

Downloaded from https://www.cambridge.org/core. University of Athens, on 08 Oct 2021 at 00:33:05, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S175526720600087X brachidontes pharaonis: an invasive bivalve in the southern mediterranean 5

1997). Moreover, our results, compared with the literature, population. Thus, the production of shell organic matter substantiate the hypothesis that B. pharaonis in the Sicilian seems to be a preferential activity in the emergent population saltpan found physical conditions and food availability of B. pharaonis. This strategy may be a way to lessen the long which guaranteed species fitness, enabling it to exploit most periods of emersion by maintaining humidity inside the pallial of the site’s niche availability. cavity. Many studies report that shell biomass production in The saltpan offered a mesocosm-like occasion to study the several species of marine invertebrates continued in the response of B. pharaonis to two different chemical and phys- absence of feeding and that shell growth still occurred in ical conditions: emersion and immersion. Although surface starved molluscs even when tissue growth was negative and submerged Brachidontes pharaonis were very close to (Lewis & Cerrato, 1997). This might reflect a strategy to each other, they showed slightly different fitness expression increase the habitable volume of shells in anticipation of which was probably due to location rather than other causal future soft tissue growth (Palmer, 1981). In the surface popu- factors. lation of B. pharaonis somatic and gonadic biomass only Organisms attached to the surface substrata inhabited a accounted for the remaining 40% of available energy for allo- more fluctuating environment, as they were exposed to air cation for most of the year. Surface gonads reached their main and desiccation for long periods of time (only being sprayed peak of allocation in winter and spring, even if they had a by the water from wave movements). By contrast, the sub- small proportion of mature spawned individuals (about 5%) merged population experienced a more stable environment throughout the other seasons. Though the environmental con- since they were submerged in water throughout the year. ditions experienced by the emergent population were overall On one hand, air exposure acts as a limiting factor in bivalves, more extreme than the submerged population, and they altering and reducing recruitment success, making recruit- needed to allocate energy to the shell, surface individuals ment asynchronous because of the unpredictable pattern of were able to maintain their reproductive cycle to guarantee emersion (McQuaid et al., 2000a,b). On the other hand, a population turn-over. This pattern is similar to the asyn- larvae or juveniles need the stable conditions found only in chronous reproductive cycles observed in tropical/subtropical the water column, not in intertidal sites exposed to air mytilids, which may be stimulated to spawn during unpredict- (Bayne, 1976). As a response to more stable conditions, able changes in food availability (Sara` et al., 2000, 2003) or due initial length in the submerged population was significantly to a sudden change of environmental conditions (Griffiths & smaller over time than in the surface population. In addition, Griffiths, 1987). The seasonal allocation of organic matter the effect of air exposure (i.e. desiccation) reduces the struc- observed in the submerged population mirrored a more tural complexity of the surface beds by reducing competition stable environment. Submerged individuals, similar to many for space and resources from the other benthic species usually other temperate bivalves, allocated less energy to shell inhabiting the Brachidontes beds in the saltpan. Thus, B. (Hicks et al., 2001), showing more flexibility in the exploita- pharaonis appears able to better exploit this space, producing tion of the acquired energy from food. Like temperate myti- high density. When the saltpan is occasionally filled with sea- lids, the submerged population showed a single continuous, water by salt workers, in spring and autumn, the surface of all major annual reproductive effort marked by complete loss hard substrata is completely covered. During these periods, we of mature gametes from the gonad (Thompson, 1979; Dix & found about 3% of small individuals on the surface. This Ferguson, 1984). Like other temperate mytilids, spawning suggests that even short periods of submersion are sufficient periods in submerged specimens were generally restricted to to guarantee recruitment in the surface population. late spring and early summer months. For example, spawning Slopes in both populations of B. pharaonis were never was more temporally restricted and seasonally synchronous higher than about 2.7 and therefore very close to the allometry in populations of Mytilus galloprovincialis than in populations threshold (b ¼ 3; Gould, 1966; LaBarbera, 1989). Such a of the tropical/subtropical species as A. ater, C. meridionalis, finding suggests that Sicilian B. pharaonis maintained biome- and Perna perna (van Erkom Schurink & Griffiths, 1991; trical relationships over time both in conditions of emersion Abada-Boudjema & Dauvin, 1995; Hicks et al., 2001). and immersion. Nevertheless, allometry decreased in winter in submerged individuals suggesting that, although they experienced the stability of the total immersion in water, Implications for biodiversity equilibrium of low winter temperatures (about 108C; Sara` et al., 1999) Western Basin limited their physiological activity (Bayne, 1976). Such con- ditions were likely more limiting than the air exposure experi- To date, Brachidontes pharaonis is restricted in the Western enced by surface individuals that, although desiccated due to Basin to a few of environments with chemical-physical partial emersion, continued their physiological activities. As characteristics very similar to its provenance habitats. Yet it confirmation, Sara` et al. (2000) observed a decrease in the has reached the western Mediterranean in not more than physiological activity of B. pharaonis which corresponded to 60–70 y from the opening of Suez Canal. It is not possible low winter temperatures. to forecast what type of ‘invasive potentiality’ will be Also the total AFDW values did not significantly differ adopted by a species such as B. pharaonis as a response to between the two populations. Both populations reached the the further increase of Mediterranean temperatures predicted same organic matter biomass in spite of the different air for the next decades. Nevertheless, our results showed that exposure conditions at each location. Nevertheless, a slightly B. pharaonis appears to have all the characteristics needed different response to air exposure reflected a slight difference to reach and colonize several coastal environments in the in resource allocation to shells, gonads and somatic tissue. Mediterranean. Brachidontes pharaonis appears to increase Accordingly, the surface population allocated, on an its density and size moving toward the western annual basis, significantly more than 10% of resources to Mediterranean Basin and to do well in both emersion and building the organic matrix of the shell than the submerged immersion conditions, allowing growth performance able to

Downloaded from https://www.cambridge.org/core. University of Athens, on 08 Oct 2021 at 00:33:05, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S175526720600087X 6g.sarÆet al.

guarantee high reproductive success. Physiological plasticity Gould S.J. (1966) Allometry and size in ontogeny and phylogeny. permits the species to tolerate highly stressed conditions Biological Reviews 41, 587–640. including resistance to air exposure and variable water temp- Griffiths C.L. and Griffiths R.J. (1987) Bivalvia. In Pandian T.J. and eratures and food availability. Thus, the Sicilian population Vernberg F.J. (ed.) energetics, Vol 2. Bivalvia through represents an important larval reservoir for this invasive Reptilia, New York: Academic Press. species and the saltpan site may function as a stepping-stone Hicks D.W., Tunnell J.W. Jr and McMahon R.F. (2001) Population to invasion of the Western Basin, actively threatening the bio- dynamics of the non-indigenous brown mussel Perna perna in the diversity of mediolittoral community. Because a warming Gulf of Mexico compared to other world-wide populations. Marine trend may elicit a response by B. pharaonis, permitting the Ecology Progress Series 211, 181–192. invasion of more habitats, the stable core areas and the diffu- Inoue T. and Yamamuro M. (2000) Respiration and ingestion rates of the sion of this species should be studied with careful attention. filter-feeding bivalve Musculista senhousia: implications for water- quality control. Journal of Marine System 26, 183–192. LaBarbera M. (1989) Analysing body size as a factor in ecology and evol- ACKNOWLEDGEMENTS ution. Annual Review of Ecology and Systematics 20, 97–117. The author would to thank Dr M. Caruso (Palermo, Italy) Lewis D.E. and Cerrato R.M. (1997) Growth uncoupling and the for his generous technical support during field sampling relationship between shell growth and metabolism in the soft shell clam Mya arenaria. Marine Ecology Progress Series 158, 177–189. and laboratory analyses. This work was funded by the Ministero Politiche Agricole (MiPA, Italy) and the Ministero McMahon R.F. (2002) Evolutionary and physiological adaptations of dell’Universita` Ricerca Scientifica e Tecnologica (MIUR, aquatic invasive : r selection versus resistance. Canadian Italy). Journal of Fisheries and Aquatic Sciences 59, 1235–1244. McQuaid C.D. and Lindsay T.L. (2000a) Effect of wave exposure on growth and mortality rates of the mussel Perna perna: bottom up regu- REFERENCES lation of intertidal populations. Marine Ecology Progress Series 206, 147–154. Abada-Boudjema Y. and Dauvin J. (1995) Recruitment and life span of McQuaid C.D., Lindsay J.R. and Lindsay T.L. (2000b) Interactive effects two natural mussel populations Perna perna (Linneaus) and Mytilus of wave exposure and tidal height on population structure of the galloprovincialis (Lamarck) from the Algerian Coast. Journal of mussel Perna perna. Marine Biology 137, 925–932. Molluscan Studies 61, 467–481. Mistri M. (2003) Foraging behaviour and mutual interference in the Allen B.J. and Williams S.L. (2003) Native eelgrass Zostera marina con- Mediterranean shore crab, Carcinus aestuarii, preying upon the immi- trols growth and reproduction of an invasive mussel through food grant mussel Musculista senhousia. Estuarine, Coastal and Shelf limitation. Marine Ecology Progress Series 254, 57–67. Science 56, 155–159. Ardizzone G.D., Belluscio A., Gravina M.F. and Somaschini A. (1996) Mohammed S.Z. (1992) The interaction between adults and recruitments Colonization and disappearance of Mytilus galloprovincialis Lam. on in the Brachidontes variabilis L. (Lamellibranchiata) bed in the Bitter an artificial habitat in the . Estuarine, Coastal and Great Lake, Suez Canal. Quaternary University Science Journal 12, Shelf Science 43, 665–676. 228–232. Bayne B.L. (1976) Marine , their ecology and physiology. Mohammed S.Z. (1997) Influence of age structure of Brachidontes varia- Cambridge: Cambridge University Press. bilis on the community structure of its associated fauna in the Greater Bitter Lake, Suez Canal. Journal of Egyptian German Zoology 24, Carlton J.T. (1992) Introduced marine and estuarine mollusks of North 51–67. America: an end-of-the-20th-century perspective. Journal Shellfish Research 11, 489–505. Morton B. (1988) The population dynamics and reproductive cycle of Brachidontes variabilis (Bivalvia: Mytilidae) in a Hong Kong man- Carlton J.T. (1999) Molluscan invasions in marine and estuarine commu- grove. Malacological Review 21, 109–117. nities. Malacologia 41, 439–454. Pusceddu A., Sara` G., Armeni M., Fabiano M. and Mazzola A. (1999) Ceccherelli V.U. and Rossi R. (1984) Settlement, growth and production Seasonal and spatial changes in sediment organic matter composition of the mussel Mytilus galloprovincialis. Marine Ecology Progress Series of a semi-enclosed marine system (W-Mediterranean Sea). 16, 173–184. Hydrobiologia 397, 59–70. Dix T.G. and Ferguson A. (1984) Cycles of reproduction and condition in Rajagopal S., Venugopalan V.P., Van der Velde G. and Jenner H.A. Tasmanian blue mussels, Mytilus edulis planulatus. Australian Journal (2003) Tolerance of five species of tropical marine mussels to continu- of Marine and Freshwater Research 35, 307–313. ous chlorination. Marine Environment Research 55, 277–291. Ehrlich P.R. (1984) Which animal will invade? In Mooney H.A. and Root T.L., MacMynowski D.P., Mastrandrea M.D. and Schneider S.H. Drake J.A. (eds) Ecology of biological invasions of North America (2005) Human-modified temperatures induce species changes: joint and Hawaii, New York: Springer-Verlag. attribution. Proceedings of the National Academy of Sciences 102, Erkom Schurink C. van and Griffiths C.L. (1991) A comparison of 7465–7469. reproductive cycles and reproductive output in four southern Safriel U.N. and Ritte U. (1985) Suez Canal migration and Mediterranean African mussel species. Marine Ecology Progress Series 76, 123–134. colonization - their relative importance in . Gilboa A. (1976) Experiments in mytilids recolonization. MS Dissertation, Rapports de la Commission International pour l’Exploration Hebrew University of Jerusalem, Israel. Scientifique de la Mer Me´diterrane´e 29, 259–263.

Downloaded from https://www.cambridge.org/core. University of Athens, on 08 Oct 2021 at 00:33:05, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S175526720600087X brachidontes pharaonis: an invasive bivalve in the southern mediterranean 7

Safriel U.N. and Sasson-Frostig Z. (1988) Can colonising mussel out- Thompson R.J. (1979) Fecundity and reproductive effort in the blue compete indigenous mussel? Journal of Experimental Marine Biology mussel (Mytilus edulis), the sea urchin (Strongylocentrotus droeba- and Ecology 117, 211–226. chiensis) and the snow crab (Chionoecetes opilio) from populations in Nova Scotia and Newfoundland. Journal of Fisheries Research Sara` G., Leonardi M. and Mazzola A. (1999) Spatial and temporal Board Canada 36, 955–964. changes of suspended matter in relation to wind and vegetation cover in a Mediterranean shallow coastal environment. Chemistry and Ecology 16, 151–173. Sara` G., Romano C., Caruso M. and Mazzola A. (2000) The new Correspondence should be addressed to: Lessepsian entry Brachidontes pharaonis (Fischer P., 1870) (Bivalvia, G. Sara` Mytilidae) in the western Mediterranean: a physiological analysis Dipartimento di Biologio Animale under varying natural conditions. Journal of Shellfish Research 19, Universita` di Palermo 967–977. Via Archirafi 18 Sara` G., Vizzini S. and Mazzola A. (2003) Sources of carbon and dietary 90123 Palermo habits of new Lessepsian entry Brachidontes pharaonis (Bivalvia, Italy Mytilidae) in the western Mediterranean. Marine Biology 143, email: [email protected] 713–722. Submitted 7 May 2005 Sokal R.R. and Rohlf F.J. (1981) Biometry. San Francisco: W.H. Freeman. Accepted 30 September 2006 and Published 1 October 2006 on MBA website

Downloaded from https://www.cambridge.org/core. University of Athens, on 08 Oct 2021 at 00:33:05, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S175526720600087X