Habitat and associated fauna of Lithophaga lithophaga (Linne 1758) in the bay of Bizerta (Tunisia).
KEY WORDS: Lithophaga lithophaga, biodiversity, ecology, Bay of Bizerta, Tunisia
The mollusc, Lithophaga lithophaga (Linne, 1758), lives in the littoral marine ecosystem in limestone rocks. The species is distributed throughout the Mediterranean, the Red Sea and the Atlantic Ocean coasts. It can be also found along the Portuguese coast and the North African coast down to Senegal (Gargominy et al. 1999). It is very appreciated by human consumers because of its high quality as a food resource. Despite the prohibition of its fishing and marketing (Shafee 1999), the collection of this bivalve occurs clandestinely in several countries and involves the irreversible destruction of its habitat (Alvarez & Altaba 1999, Gargominy et al. 1999, Shafee 1999). This overexploitation and habitat degradation has caused serious local ecological damage to Lithophaga populations. The most damaged areas are reportedly on some parts of the Italian and former-Yugoslavian coast (Ministero de Medio Ambiente 2000).
Previous studies referring to L. lithophaga on the Tunisian coastal areas are limited to a bivalve inventory by Zouari (1985) and entry of this mollusc in the red list of threatened species where it is exploited clandestinely, particularly in the channel and the bay of Bizerta, by Jaafar (2004). Jaafar et al. (2004) also described the shell perturbations in the bay of Bizerta's population. In other Mediterranean coasts, the morphology was studied by Poutiers (1987), Gargominy et al. (1999) and Cossignani et al. (1992). Kleemann (1973a, Kleemann 1973b, Kleemann 1974), Galinou-Mitsoudi and Sinis (1994, Galinou-Mitsoudi & Sinis 1995 and Galinou-Mitsoudi & Sinis 1997) studied the ecobiology of individuals collected from the northern Adriatic Sea (Istrian coast) and in the Evoikos gulf (Greece).
The ecology of L. lithophaga has not been previously studied in Tunisia. Consequently, the objective of our research is to report on the ecology of this bivalve and to improve our knowledge about the ecosystem conditions required by L. lithophaga to thrive. Such information could contribute to the aquaculture of this species in the future. The work therefore lies within the scope of the national ESREB Project (Assessment of Benthic Resources Stocks and Seabed Ecosystems). Initially, the study defines the species habitat and the associated fauna.
In the Tunisian coastal areas, the progressive deterioration of marine rock ecosystems is an increasingly widespread problem as greater human activities combined with climate change disturb natural aquatic ecosystems (Jaafar, 2004). The study of Lithophaga lithophaga is of special importance because the future of this species in many Mediterranean areas is seriously threatened. There is an urgent need to evaluate the stock of L. lithophaga so that environmental base-lines can be established. Only when sufficient data on the distribution and requirements of this mollusc are known, can exploitation be managed to help safeguard the species and assure its sustainability.
MATERIAL AND METHODS
Sampling and Habitat Structure
From October 2002 to September 2003, sampling of rocks containing L. lithophaga was done at monthly intervals by scuba diving. Sampling was carried out at 3-4 m depth in the infralittoral zone of Bizerta Bay (Fig. l). On each occasion, 120-150 individuals were extracted in the laboratory from detached blocks of limestome rock. This was carried out by breaking the blocks with a pneumatic drill. This enabled us to examine the calcareous substratum and to identify the benthic community associated with the lithophagous bivalve. Individual's bivalves were recovered, sorted, identified, counted, and preserved in alcohol (70%).
To describe the individual's population density per rocky block, we proceeded during the winter and spring of 2003, to calculate volume determinations of 33 rocky blocks. Each sample is submerged in a graduated plastic basin and the variation of the water level gives the real volume of the stone. This operation was carried out before breakage and extraction of the whole of the individuals living in this stone fragment. The mineralogical structure of the rocks was investigated using thin sections according to Hatira (1988).
[FIGURE 1 OMITTED]
Bio-ecological Data Processing
To study the faunal diversity, we have calculated 6 ecological indexes:
(1) Relative abundance, pi = n/N x 100 represents the relationship between the number of individuals of a given species (n) and the total number of individuals of all species (N) present in the station; (2) The specific richness S, defined as being the rough number of species collected during all the study period (Mackenzie et al. 2000); (3) The diversity index of Shannon and Weaver (1963) H' = -[Summation] (ni/N X log2 ni/N) nT = number of the individuals of each species, N = total number of the various species. It makes possible to compare and evaluate space and/or temporal diversity of various communities living in the same station; (3) Equitability, Es = H' / log 2 S, which varies from 0-1 (species with equal abundances), measures the degree of diversity of a biotope; (4) Constancy is the relationship, this index is expressed in percentage, between the number of statements, which contains this species and the whole of the statements. If C [greater than or equal to] 75%, the species are permanent in the rocky habitat. When 50% [less than or equal to] C < 75%, the species are constant in the site. When 25% [less than or equal to] C < 50%, the associated species are accessory. If C < 25%, the associated species are incidentally present or accidental: (5) Interspecific association and competition are expressed by the Southwood index: Ia = 2 [(ji / A + B) - 0.5], which makes it possible to highlight the interspecific relations (Southwood 1966). ji = total number of individuals of species A and B where these 2 species are present simultaneously, A = total number of individuals of species A collected during 12 too; (6) B = total individuals number of the species B collected during 12 mo. The index Ia varies between +1 (total affinity) and -1 (total incompatibility).
The Habitat Substratum of Lithophaga lithophaga
Microscopic observations of the thin sections made from the limestone blocks showed an ordered and well-directed laminar mineralogical structure in a biomicritic matrix. The existence of such a structure indicates that the calcareous mud was originally deposited in a calm, shallow, and deep area where rock lithification occurred gradually. The biomicritic matrix contained benthic Foraminifera such as Bulliminidae and Globigerinidae (Fig. 2).
Remains of Ostracoda and some radiolarians were also observed in this facies. Argillaceous particles were found in this rocky habitat. The absence of pores shows that it is a hard stone, not crumbly, and mechanically difficult to perforate. The nature of the fossil composition of this rock enabled us to determine the age as Eocene.
During 12-mo sampling, the number of individuals of Lithophaga lithophaga extracted from each limestone block was compared with the volume. Results did not show any correlation between the habitat volume and the number of specimens (Fig. 3). Large and small blocks sheltered either high or low numbers of individuals. The repeated observations of the various rocky blocks sampled during three years, from 2003-2006, showed that the bivalve has most affinity for flat rocks inclined towards the bottom.
The L. lithophaga habitat presents an important biotope for numerous marine species. The majority of the benthic fauna listed in this rocky habitat was extracted from burrows and tubes associated with the shell of this mollusc. Other lithophagous bivalves such as Striarca lactea, Petricola lithophaga, Lithophaga aristata, and Gastrochaena dubia were also observed in the same blocks. These lithophagous bivalves represented 58.61% in average of the total associated fauna (Table 1). The maximum abundance was recorded in October (80.48%) and the minimum in January (48.11%).
The average abundance of gastropod species was 3.9% of the total fauna; with the following significant monthly variations: 0.57% in November and 7.37% in March (Table 1). Chiton olivaceus shows 1.2% in average abundance of the total associated fauna; with 4.44% recorded in June and 0% in October, November, January, and July.
The studied area shows a high total species richness with 30 species. The recorded monthly values varied from 11 species in January to 25 in February (Fig. 4). The specific richness is low from October to January and can be explained by the low salinity and temperature in January and the high concentration of the dissolved oxygen during autumnal period. The constancy values for each species are grouped (Table 1) and four association groups are identified (Table 2).
[FIGURE 2 OMITTED]
[FIGURE 3 OMITTED]
Specific Diversity and Equitability
During the study period, Shannon-Weaver index values fluctuate between 1.49 bits (October) and 3.18 bits (May) with an average of 2.26 bits. Rocky habitats in the bay of Bizerta are moderately diversified (Fig. 5) comparatively to other sites in the Mediterranean Sea (Peres, 1978). The equitability index values are lower in autumn and higher during summer, spring and winter periods (Fig. 6).
[FIGURE 4 OMITTED]
Time variations in the relative abundances showed the dominance of L. lithophaga during the study period. The annual average of relative abundance is 53.15% with a maximum of 78% in October and a minimum of 40% in May (Table 1).
Aspidosiphon muelleri and Phascolosoma vulgare have also relatively high abundances (3% to 22% and 3% to 21% respectively). The lowest values were recorded in November and September for the first species and September for the second. The maximum values were recorded in January and April respectively (Table 1).
[FIGURE 5 OMITTED]
Constancy and Inter-specific Association
Analysis of various values of the Southwood index combined with the constancy estimate indicated four biocenotic groups (Table 2). The first group includes lithophagous and benthic species associated with Lithopaga lithophaga throughout the year. The second group is mainly represented by gastropods and crustacean species. They are usually absent from the site from the end of autumn to the beginning of winter. The third group with values of -0.5 = la < 0 is represented by the additional species mainly observed for a period of three to six months in the site depending on the biologic cycle (food, reproduction period, or hibernation). The last benthic community shows a low affinity and includes accidental species with la < -0.5. They are observed for a period of one to three months and are considered as visitors.
DISCUSSION AND CONCLUSION
The bivalve Lithophaga lithophaga is greatly prized in Mediterranean fish markets, but it is strictly protected by legislation (Convention of Berne and the European Union Habitat Directive following the protocols of Geneva and Barcelona). The commercial exploitation of this species is prohibited in 12 countries (Cyprus, Croatia, France, Greece, Italy, Malta, Morocco, Portugal, Serbia and Montenegro, Slovenia, Spain, Tunisia, and Turkey). Nevertheless, about 5 kg/week are estimated to be collected clandestinely from the Bizerta lagoon. However, it is difficult to know the real quantity collected from Tunisian coasts.
[FIGURE 6 OMITTED]
According to Poutiers (1987), the productivity in Yugoslavia was 30 tons/year. In Morocco, this species is also collected clandestinely (Shafee 1999). Compared with Tunisian exploitation, the quantities collected in the neighboring countries seem to be high. This mollusc lives exclusively in limestone rocks and is absent in volcanic rocks (Simunovi & Grubeli 1992). It inhabits tunnels and dissolves the rocky blocks with acid secretions to penetrate deeper into the substratum. The acid is produced by specialized glands in the anterior end of the organism (Mojetta & Ghisotti 1996). In Bizerta lagoon, the mineralogical study revealed no porosity in rocks and this hard material requires chemical processes to make boreholes.
The distribution of the species in limestone is linked to several parameters: hydrodynamic, rock shape, and site exposure to the current. According to Simunovi and Grubeli (1992), L. lithophaga prefers habitats with strong currents and especially vertical faces of the rocks where it makes borehole 10-20 cm long. Kleemann (1973a) noted that the inclined position of the rock constitutes a fundamental and significant characteristic for the biological cycle of L. lithophaga. This inclined face oriented to the sediment is more appreciated by larvae in preparation of the first stage of the metamorphosis. In the Gulf of Trieste, the growth of L. lithophaga was found to be better in a calcareous sedimentary substrate than in the other substrates like corals (Valli et al. 1986). Galinou-Mitsoudi and Sinis (1997) considered 2-4 m in depth as the optimum density of this species.
The Shannon index values oscillate from 1.49-3.10 and show that the area is fairly diversified. Low values of the Shannon diversity index (1.49-2.3) were recorded from October to January (Fig. 4). Dajoz (1996) attributed lower diversity index values to an unbalanced distribution of the species densities caused by the dominance of just one or two species in the ecosystem. According to Peres (1978), this index can reach the maximum of 4 bits in some Mediterranean coastal communities.
Most mollusc species have high abundances in spring, summer, and winter. L. lithophaga is the most abundant and constant species in this monitored area. Contrary to what Kleemann (1974) showed, there is no competition for space between L. lithophaga and the lithophagous species Gastrochaena dubia (Fig. 2). This same author notes that L. lithophaga exerts a specific competition towards Petricola lithophaga. In this study, the Southwood index is high for these two species, this probably excludes any competition between them. An incompatibility is noted for Amphitrite johnsoni larvae and Hesione pantherina with all the species. This incompatibility can probably be explained by an accidental presence of both species in this biotope. Vermilia agglutinata and Serpula vermicularis have low Southwood index with L. lithophaga. Indeed, these two species live in tubes adhering to the mytilid periostracum and the tube openings are near to the mussel siphons. It is probably an adaptation for feeding by these commensal polychaetes. Sphearoma serratum crustacean is occasionally recorded in this habitat but it moves considerably (Laulier & Lejuez 1986). Clibanarius erythropus could be considered in this study as a competitive species because of the low index.
[FIGURE 7 OMITTED]
Some habitats of L. lithophaga communicate with other boreholes made by Striarca lactea (Fig. 7) and sometimes those occupied by the sipunculids. The observations of Schembri and Jaccarini (1978) show that the cavity of L. lithophaga cannot communicate with another animal's borehole seem unjustified. Moreover, the ecological index values show a strong affinity between these three species. Kleemann (1974) did note intraspecific competition between the lithophagous species, except for Gastrochaena dubia. Our observations confirm the existence of competition between the individuals of L. lithophaga. Indeed, in the same block, all the perforating communications of L. lithophaga have a similar size and there are no communications between large and small boreholes (Fig. 8).
[FIGURE 8 OMITTED]
Alvarez, R. M. Y. & C. R. Altaba. 1999. Un bivalvo marino protegido se captura y se vende como marisco. Quercus 164:50-51.
Cossignani, T., V. Cossignani, A. Di Nisio & M. Passamonti. 1992. Atlante deel conchglie del medio Adriatico. Mostra Mondiale Malacologia, Cupra Maritina (Italy). Informatore Pliceno Ed., Ancona. 40 pp.
Dajoz, R. 1996. Precis d ecologie. 6eme Edition. Dunod. 551 pp. Galinou-Mitsoudi, S. & A. I. Sinis. 1994. Reproductive cycle and fecundity of the date mussel, Lithophaga lithophaga, (L.) (Bivalvia: Mytilidae) in Evoikos Gulf (Greece). Bios. Macedonia, Greece 2: 17-22.
Galinou-Mitsoudi, S. & A. I. Sinis. 1995. Age and growth of Lithophaga lithophaga (Linne, 1758) (Bivalvia, Mytilidae) based on annual growth lines in the shell. J. Molluscan Stud. 61:435-453.
Galinou-Mitsoudi, S. & A. I. Sinis. 1997. Population dynamics of the date mussel, Lithophaga lithophaga, (Linne, 1758) (Bivalvia: Mytilidae) in the Evoikos Gulf, Greece. Helgolander Meeresunters 51:137-154.
Gargominy, O., P. Bouchet & D. Moreno. 1999. Lithophaga lithophaga (Linne, 1758) Museum National d'Histoire Naturelle: pp. 1-5.
Hatira, N. 1988. Les concentrations de Zn, Pb, Sr, (Ba) dans le cortex des diapirs de Trias salifere: exemple du diapir de Sakiet- Koucha (Tunisie Septentrionale). Comparaison avec d'autres massifs Tunisiens et avec les Cap- Rocks du Gulf Coast (USA). Doctorat, Universite P. & M. Curie Paris VI. 288 pp.
Jaafar, F. 2004. Ecologie et perturbations coquillieres de la datte de mer Lithophaga lithophaga (Linne, 1758) recoltee au Nord de la Tunisie: la baie de Bizerte. DEA, Faculte des Sciences de Bizerte. 73 pp.
Jaafar, F., N. Trigui-El-Menif, M. Le Pennec & M. Boumaiza. 2004. Perturbations coquillieres chez le mollusque bivalve Lithophaga lithophaga pre1eve dans la baie de Bizerte (Tunisie). Bulletin Societe Zoologique de France 129:419-426.
Kleemann, K. H. 1973a. Der Gesteinsabbau dursh Atzmuschelr an Kalkke.sten. Oecologia, 13: 377-395. Kleemann, K.H. 1973b. Lithophaga lithophaga (L) (Bivalvia) in different limestone. Malacologia 14:345-347.
Kleemann, K. H., 1974. Beitrag sur Kenntnis des verhaltens von Lithophaga lithophaga (L) (Bivalvia) in Bohrloch. Sitzungsberichten Oester. Akademie wissenschaften (Mathem. Nauturn. K1), 182:201-210.
Laulier, M. & R. Lejuez. 1986. Sphaeroma serratum (Crustace Isopode) espece polytypique. Cahiers de Biologie Marine 27:329-330.
Mackenzie, A., A. S. Ball & S. R. Virdee. 2000. L'essentiel en ecologie, Berti editions, Paris. 368 pp.
Ministero de Medio Ambiente. 2000. Biology, conservation, and protection problems of date shell (Lithophaga lithophaga) in Spain, Abstract. Madrid. 2 pp.
Mojetta, A. & A. Ghisotti. 1996. Flore et faune de la Mediterranee. Collection Guide Vert. 317 pp.
Peres, J. M. 1978. Vulnerabilite des ecosystemes mediterraneens a la pollution. Ocean Management 3:205-217.
Poutiers, J. M. 1987. Bivalves. Fiches FAO d'identification des especes pour les besoins de la peche en Mediterranee et Mer Noire. Zone de peche 37. 1:440-446.
Schembri, P. J. & V. Jaccarini. 1978. Some aspects of the Echiuran worm Bonellia Viridis and associated fauna. Mar. Biol. 47:55-61.
Shafee, S. M. 1999. Peche des bivalves sur la cote mediterraneenne marocaine: catalogue d'especes exploitees et d'engins utilises. Rapport FAO-COPEMED Alicante, Espagne. 57 pp.
Shannon, C. E. & W. Weaver. 1963. The mathematical theory of communication. Illinois University Press. Urbana 117 pp.
Simunovi, A. & I. Grubeli. 1992. Biological and ecological studies of the date shell (Lithophaga lithophaga L.) from the eastern Adriatic Sea. Period Biol. 94:187-192.
Southwood, T. R. E. 1966. Ecological methods, with particular reference to the study of insect population. London: Methuen. An. Co. Ed. 391 pp.
Valli, G., P. Nodari & R. Sponza. 1986. Experimental breeding of Lithophaga lithophaga (L.) (Bivalvia, Mytilacea) and study of the reproductive cycle in the Gulf of Trieste. Nova Thalassi 8:1-13.
Zouari, S. 1985. Contribution a l'etude systematique des Lamellibranches des cotes tunisiennes DEA. Univ. Tunis. 245 pp.
NAJOUA TRIGUI EL-MENIF, (1) * FERDAOUS JAAFAR KEFI, (1) MOHAMMED RAMDANI, (2) ROGER FLOWER (3) AND MONCEF BOUMAIZA (2)
(1) Universite de Carthage, Faculte des Sciences, Biologie, Biosurveillance de l'Environnement, Bizerte, Tunisie; (2) Institut Scientifique, Universite Mohamed V Agdal, Oceanographie Biologie, BP 703, Rabat, Maroc; (3) University College London, ECRC, Geography, 26, Bedford Way, London, UK
* Corresponding author. E-mail: email@example.com
TABLE 1. Abundances and constancy of the fauna in the rocky biotope. Abundance % Constancy Species % Average Bivalvia Lithophaga lithophaga 100 53.15 Striarca lactea 91.67 2.31 Petricola lithophaga 91.67 1.09 Lithophaga aristata 91.67 0.86 Gastrochaena dubia 75 1.02 Gastropods Diodora gibberula 66.67 0.86 Gibbula magus 58.33 0.59 Columbella rustica 83.33 1.25 Nassarius incrassatus 100 1.19 Polyplacophora Chiton olivaceus 66.67 1.22 Sipunculoida Aspidosiphon mulleri 100 7.41 Phascolosoma vulgare 100 12.75 Crustacea Alpheus macrocheles 100 7.38 Athanas nithescens 91.67 1.22 Xantho incisus 66.67 1.15 Pilumnus hirtellus 58.33 0.69 Clibanarius erythropus 41.67 0.23 Sphaeroma serratum 50 0.89 Cymodocea truncata 16.67 0.1 Pisidia longicornis 16.67 0.13 Polychaeta Eunice siciliencis 83.33 0.76 Eunice torquata 58.33 1.29 Amphitrite johnostoni 83.33 0.26 Lepidonotus clava 50 0.33 Vermilia agglutinata 25 0.2 Serpula vermicularis 25 0.26 Hesione pantherina 8.33 0.07 Amphitrite johnsoni larvae 8.33 0.03 Echinoderma Holothuria sp 16.67 0.1 Fish Gobius lavescens 58.33 0.59 Abundance % Species Max Min Bivalvia Lithophaga lithophaga 77.7 40.7 Striarca lactea 2.66 0 Petricola lithophaga 2.24 0 Lithophaga aristata 2.35 0 Gastrochaena dubia 2.44 0 Gastropods Diodora gibberula 1.93 0 Gibbula magus 1.63 0 Columbella rustica 3.81 0 Nassarius incrassatus 2.9 0.42 Polyplacophora Chiton olivaceus 4.48 0 Sipunculoida Aspidosiphon mulleri 21.9 2.91 Phascolosoma vulgare 19.1 3.59 Crustacea Alpheus macrocheles 12.6 2.6 Athanas nithescens 2.35 0 Xantho incisus 4.22 0 Pilumnus hirtellus 2.6 0 Clibanarius erythropus 0.97 0 Sphaeroma serratum 4.11 0 Cymodocea truncata 0.9 0 Pisidia longicornis 0.81 0 Polychaeta Eunice siciliencis 2.16 0 Eunice torquata 0.48 0 Amphitrite johnostoni 2.75 0 Lepidonotus clava 1.22 0 Vermilia agglutinata 1.22 0 Serpula vermicularis 1.21 0 Hesione pantherina 0.95 0 Amphitrite johnsoni larvae 0.58 0 Echinoderma Holothuria sp 0.95 0 Fish Gobius lavescens 2.16 0 TABLE 2. Classification of the associated fauna according the Southwood index and constancy. Permanent species: Lithophaga lithophaga, >75% of total samples Petricola lithophaga, 1a [greater than Striarca lactea, Lithophaga aristata, or equal to] 0.5 Nassarius incrassatus, Columbella Group I rustica, Aspidosiphon muelleri, Phascolosoma vulgare, Amphitrite johnstoni, Eunice siciliensis, Alpheus macrocheles, Athanas nitescens, Gastrochaena dubia Constant Species: Diodora gibberula, Gibbula magus, 50% to 75% Chiton olivaceus, Gobius flavescens, 0 < Ia <0.5 Xantho incisius, Eunice torquata, Group II Pilummus hirtellus Additional Species: Vermilia agglutinata Serpula 25% to 50% vermicularis Sphaeroma serratum. -0.5 < Ia <0 Lepidonotus clava and Clibanarius Group III erythropus Accidental species: Cymodocea truncata Pisidia longicornis <25% Hesione pantherina, Amphitrite Ia [less than johnstoni larvae and or equal to] 0.5 Holothuria sp Goup IV