Abundance and diversity of amphipods (Crustacea: Peracarida) on shallow algae and seagrass in lagoonal ecosystem of the Mediterranean Tunisian coast

The vegetation in Menzel Jemil consists essentially of five species with a seasonal variation in their distribution. Indeed, G. longissima and G. bursa-pastoris dominate other species in the spring, U. lactuca whose biomass increases from the spring peaked in summer, Cladophora sp. appears in the winter, while C. nodosa, all year round, dominates in autumn. The temporal distribution of G. bursa-pastoris and U. lacuta in Menzel Jemil station is similar to that described by Sahli-Hazami (2004). In the lagoon of Venice, Italy, Fava et al. (1992) describe another seasonal succession of vegetation cover which consists mainly of Ulva rigida; the G. bursa-pastoris is present during the cold season, Cladophora sp. is occasional, and marine phanerogam Zostera noltii is found in limited fields.

Plant species richness in the Menzel Jemil station is lower than that described by Zaouali (1980) and Frisoni et al. (1986) in the lagoon of Bizerte; this could be due to eutrophication resulting in the presence of Ulva lacuta (Anonyme 2000), or the increase in salinity caused a decrease in species diversity (Zaouali 1980).

Monthly plant biomass fluctuates with an increase in early spring, peaking in June, and a decrease in summer. Indeed, the rise in water temperature in the spring causes the increase in plant biomass, but when the temperature reaches its maximum in August, plant biomass starts to decrease to reach the lowest values in winter. Highlighting the close relationship between temperature and plant biomass confirms the work of Antit-Ben Rejeb (2012) which showed the same effect of temperature on the variation of biomass photophilic algae in the bay of Tunis.

In the Bizerte lagoon, water temperature ranges between 9°C in January to 30.86°C in August. Harzallah (2002) and Béjaoui et al. (2008) reported however a seasonal cycle in the lagoons, ranging between 10°C in winter and 28°C in summer, and from 11.5°C in January to 29.5°C in August, respectively. The water salinity ranges from 30.8 in February to 39.2 in August, which is higher than the values reported by ANPE (1990), 30 in winter to 38 in summer (Béjaoui et al. 2005). Thus, seasonal gradients of temperature and water salinity in the Bizerte lagoon are relatively large. Moreover, during the last decade, the temperature and salinity have increased. The evaporation in the lagoon is very important particularly in summer with 166 million m³.year⁻¹. Precipitation does not exceed 146 million m³.year⁻¹ in winter while it is weak and scarce in summer (74 million m³.year⁻¹). The water input from the Ichkeul Lake has dramatically decreased during the last decades as an effect of the construction of dams discharging into this lake (MAERH 2003). This has led to a significant alteration of the water characteristics of the lagoon, particularly a dramatic increase in salinity (Béjaoui et al. 2005).

Dissolved oxygen content shows an obvious seasonal variation. Therefore, low water oxygenation logically characterizes the dry period. These results agree with those of Béjaoui et al. (2008). Nutrient variability appears to be related to two factors, by seawater coming from the ship canal and also by freshwater coming from the Ichkeul Lake and its large catchment area. The high nitrogen anion concentrations (NO⁻ ₃ and NO⁻ ₂) and phosphorous content can be related to the domestic sewage input from towns around the lagoon and specially Menzel Abderrahmen city or to the freshwater from Oued Guenich located on the eastern side of the Bizerte lagoon which is widely open to an agricultural zone where fertilizers are constantly applied. These factors may provide the explanation of the various content of chlorophyll a during the sampling period. However, the turbidity appears to be related to two factors, (i) hydrodynamic conditions and (ii) rainy season, which create water movements. Indeed, studies performed by Harzallah (2003) on the currents of the Bizerte lagoon reveal that the flow of water in both the surface and the bottom follows the wind direction, which is often northwest with low amplitude. Nevertheless, the interpretation of these results must take into account the special conditions of the Bizerte lagoon, which is a transitional area currently affected by many environmental variables (Afli et al. 2008). Moreover, nutrients and chlorophyll a concentrations recorded during the sampling period are lower than those observed before the connection of the urban and industrial waste to the ONAS network (National Sanitation Utility) (MAERH 2003; Béjaoui et al. 2008). Besides, coastal lagoons are considered to be highly productive ecosystems but they are vulnerable to human disturbance as a result of their semi-enclosed situation and their proximity to the sources of terrestrial effluents (Bazairi et al. 2005).

In Menzel Jemil (Bizerte lagoon, Tunisia), 3,620 specimens of amphipods were collected from October 2009 to September 2010 belonging to 8 families and 9 genera; the species are common in Tunisian lagoons (Diawara et al. 2008; Zakhama-Sraieb et al. 2009). Differences in the abundance of the ten species were observed. While G. aequicauda was the most abundant, G. fucicola, C. filosa, and Caprella sp. were recorded for the first time in the Bizerte lagoon. M. gryllotalpa was typically a lagoonal species. Compared to Diawara et al. (2008), the number of amphipod species herein recorded is lower than that found in the Tunis north lagoon; however, a relatively high number of amphipod species are found in the coastal lagoon of Smir (northwest of Morocco) by Chaouti and Bayed (2011), by Cherkoui et al. (2003) in the Bou Regreg estuary Moroccan Atlantic coast, and by Mogias and Kevrekidis (2005) in the Laki lagoon (Northern Aegean).

Our results show that the distribution of the amphipod fauna in the Bizerte lagoon is primarily linked to temperature and salinity. Oscillations in these environmental variables are related to the climatic season. An increase in temperature and salinity is characteristic of the dry season (summer), when the seawater penetrates the lagoon in a greater volume as a result of reduced rainfall, whereas in the wet season (winter), freshwater comes from rivers and the Ichkeul Lake and thereby reduces salinity. These results agree with studies on distribution patterns for other crustaceans in relation to the temperature and salinity of the water, which are considered extremely important for a better understanding of the dynamics of these species (Pinheiro 1991). Variations in temperature and salinity have been cited by a number of authors as important factors for the occurrence of particular amphipod species (Nevis et al. 2009; Mogias and Kevrekidis 2005). In fact, many ecological studies have shown salinity to be the main factor controlling zonation in the structure of the benthic communities (Cacabelos et al. 2010). However, Bazairi et al. (2003) have emphasized that this is not the main factor in brackish environments. Some other authors have demonstrated that modification in habitat complexity affects crustacean assemblages (Sanchez-Jerez et al. 1999; Ayala and Martin 2003; Vazquez-Luis et al. 2008). Indeed, the importance of temperature should be interpreted carefully, since Ysebaert and Herman (2002) pointed out that long-term averages of environmental variables are more important than values obtained during samplings (Cacabelos et al. 2010). Nevertheless, the difference in mean density between months can be explained by the ecological preferences of each species. Amphipod assemblages at the Bizerte lagoon are dominated in terms of density and species richness by the genus Gammarus. The temporal variability of the total density is mainly due to the numerically dominant species, such as G. aequicauda, G. insensibilis, and C. filosa. The seasonal variation in mean density recorded from our study area was similar to that described in other Mediterranean lagoons (Mogias and Kevrekidis 2005; Procaccini and Scipione 1992). With respect to changes in algae and seagrass, which create refuge and food resource to diverse amphipods, an important reduction in species richness was recorded in January in our study contrary to Mogias and Kevrekidis (2005) in July.

Concerning the diversity of the communities, the diversity index (H′) and evenness (J′) values are low in the different seasons. Moreover, abundance and species richness values showed a sharp decrease during December, January, and February when both temperature and salinity diminish, whereas equitability and Shannon-Wiener indexes in the studied amphipod assemblage are more stable over time than those found in other areas.

The temporal distribution of amphipod assemblage studied by analyses of similarity between the samples, based on the abundance of species, exhibited three major assemblages whose distribution is strongly dependent on the water temperature and shows a seasonal pattern. Similar distribution patterns for amphipods and other crustaceans have been reported in several studies (Bazairi et al. 2003; Mogias and Kevrekidis 2005; Lopez De La Rosa et al. 2006; Vazquez-Luis et al. 2008; Nevis et al. 2009; Cacabelos et al. 2010; Zakhama-Sraieb et al. 2010). In fact, canonical correspondence analysis (CCA) made it possible to summarize the overall situation for the species, sampling months, and environmental parameters on a single graph. In accordance with our results, the temperature, turbidity, and chlorophyll a content are the most often reported factors in determining the distribution and composition of amphipods in Menzel Jemil. However, phosphate and nitrite concentrations do not show large variability. Thus, amphipod assemblages are probably not very influenced by their modest variations. On the other hand, these changes in environmental factors in this study may affect algae and seagrass which are support of the amphipod assemblages.

Amphipods play an important role in structuring benthic assemblages (Duffy and Hay 2000) as secondary and tertiary producers in marine communities (Beare and Moore 1996). Amphipods are important source of food for benthic fauna of commercial interest and also very ecologically sensitive organisms and good indicators of natural or disturbed environmental conditions (Conradi et al. 1997). Moreover, benthic databases are essential for comparisons valuable for impact studies or monitoring programs, in order to preserve the environment and the species of commercial importance that they support (Desroy et al. 2002).