Fish Biodiversity in the Vermetid Reef Of Shiqmona (Israel)
Abstract
Abstract. A study of the structure of the fish community associated with a vermetid reef at Shiqmona, Israel, revealed the highest fish biodiversity (36 species) of any habitat along the Mediterranean coast of Israel. Despite the prevalence of fish of Erythrean origin in the Levantine littoral, the benthic fish community at the site is entirely autochthonous. The families richest in members were the Blenniidae and the Gobiidae. Eighteen species are benthic, sixteen supra-benthic and two pelagic.
Problem
The Israeli coast, at the southeastern corner of the Mediterranean, lies along the warmest, saltiest and most oligotrophic part of the sea. With summer surface temperatures reaching 30 °C, salinity values of 39.5, and concentrations of nutrients close to detection limits (Azov, 1991), quantitative and qualitative faunal impoverishment have been assumed to be inevitable (Fredj, 1974). The composition of the biota has been significantly altered by anthropogenic changes: the opening of the Suez Canal in 1864, linking the Red Sea with the Mediterranean, allowed hundreds of Erythrean species to settle along the Levantine infralittoral (Por, 1978). Some abundant invaders are exploited commercially and usually form up to 40 – 50 % of the fish crop in the shallow water (< 100 m) along the Israeli coast (Golani & Ben Tuvia, 1993), others constitute a nuisance or economic burden, while yet others outcompete the native species, either wholly or in part, for their habitat space (Galil, 1999).
Although the faunal composition off the Israeli coast has been studied extensively, few works have dealt with the littoral zone (Gilat, 1964; Lipkin & Safriel, 1971; Goren, 1980; Galil & Lewinson, 1981; Fishelson & Haran, 1986; Rinkevich et al., 1998), with but a single article on the ecology of littoral fish (Diamant et al., 1986). The aim of this research was to examine the structure of the fish community associated with the vermetid reef at Shiqmona, which possesses the highest biodiversity of any habitat along the Mediterranean coast of Israel (Goren & Galil, 1996).
Material and Methods
1. Research site
Shiqmona reef is located at the margins of the headland formed by Mount Carmel, at the southern end of Haifa Bay (Fig. 1), and is composed of a series of offshore rounded platforms with raised rims, running parallel to the coast, interspaced by shallow channels. The reefs have formed in the infralittoral fringe on an exposed rocky shore under high energy conditions. They have been formed by sessile gastropods, the gregarious vermetids Dendropoma petraeum (Monterosato) and Vermetus triqueter (Bivona); both are endemic to the Mediterranean (Safriel, 1966, 1975). Water depth at the reef’s seaward face is 1 – 3 m. The porous structure of the vermetid reef and the underlining aeolanthic sandstone allows for a rich community of endoliths: sponges, bivalves and crustaceans. The resulting local organic enrichment combined with the structural complexity of the edifice has led to the establishment of an extraordinarily dense ichthyofauna of great diversity (Goren & Galil, 1996).
Research site.
2. Methods
Fish were collected six times between November 1995 and December 1996 by applying Rotenonne solution to an area of ca. 100 m2 at adjacent sites of similar morphology and wave pattern.
After preliminary sorting at the Israel Oceanographic & Limnological Research Institute, the fish were transferred to the ichthyological laboratory at Tel Aviv University for identification to the species level and further study. Each specimen was measured (total length, to 1.0 mm) and weighed (to 0.01 g).
The following parameters were calculated for each sample:
(1) Species richness (= number of species);
(2) Species diversity (Shannon-Wiener diversity index) was calculated as
where S = number of species in the sample; Pi = the proportion of the ith species in the sample (= ni/N, ni = number of fish belonging to species i, N = total number of fish in the sample);
(3) Evenness was calculated as J = Hmax/H′ where Hmax is the highest possible value for H′ in a certain community;
(4) Index of similarity between two samples (expressed in %) was calculated as
where Pij and Pik are the proportion of the species i in the communities j and k, respectively. The index of similarity was calculated for individuals and biomass separately (Goren, 1979).
3. Terminology
For terminology we follow “The Dictionary of Ecology, Evolution and Systematics” (Lincoln et al., 1997):Benthic fish: fish living on the seafloor; Supra-benthic fish: fish living above but close to substratum; Pelagic fish: fish inhabiting the open waters.
Results
1. Systematic and biogeographic structure of Shiqmona fish community
Thirty six species belonging to 15 families were identified from Shiqmona reef (Table 1). The families richest in members were the Blenniidae and the Gobiidae, with 9 and 4 species, respectively.
| individuals | biomass | |||
|---|---|---|---|---|
| no. | % of total | g | % of total | |
| benthic species | ||||
| Blenniidae | ||||
| Aidablennius sphynx (Valenciennes 1836) | 110 | 2.02 | 126.75 | 0.25 |
| Coryphoblennius galerita (Linnaeus 1758) | 17 | 0.31 | 24.12 | 0.05 |
| Lipophrys canevai (Vinciguerra 1880) | 30 | 0.55 | 30.04 | 0.06 |
| L. trigloides (Valenciennes 1836) | 187 | 3.43 | 561.35 | 1.09 |
| Parablennius gattorugine (Brunnich 1768) | 71 | 1.3 | 617.12 | 1.2 |
| P. incognitus (Bath 1968) | 276 | 5.06 | 204.4 | 0.4 |
| P. sanguinolentus (Pallas 1811) | 43 | 0.79 | 319.13 | 0.62 |
| P. zvonimiri (Kolombatovic 1892) | 626 | 11.48 | 847.13 | 1.64 |
| Scartella cristata (Linnaeus 1758) | 491 | 9.01 | 936.4 | 1.82 |
| Gobiidae | ||||
| Gobius bucchichi Steindachner 1870 | 92 | 1.69 | 415.29 | 0.81 |
| G. cobitis Pallas 1811 | 62 | 1.14 | 1261.09 | 2.45 |
| G. paganellus Linnaeus 1758 | 230 | 4.22 | 1814.49 | 3.52 |
| Zebrus zebrus (Risso 1826) | 3 | 0.06 | 1.34 | 0 |
| Scorpaenidae | ||||
| Scorpaena porcus Linnaeus 1758 | 1 | 0.02 | 90.42 | 0.18 |
| S. maderensis Valenciennes 1833 | 63 | 1.16 | 573.45 | 1.11 |
| S. scrofa Linnaeus 1758 | 2 | 0.04 | 207.41 | 0.4 |
| Clinidae | ||||
| Clinitrachus argentatus (Risso 1810) | 55 | 1.01 | 84.3 | 0.16 |
| Tripterygiidae | ||||
| Tripterygion delaisi Cadenat & Blache 1971 | 222 | 4.07 | 126.46 | 0.25 |
| total for benthic species | 2581 | 47.35 | 8240.69 | 16.01 |
| supra-benthic species | ||||
| Sparidae | ||||
| Boops boops (Linnaeus 1758) | 6 | 0.11 | 1.57 | 0 |
| Diplodus sargus (Linnaeus 1758) | 133 | 2.43 | 5173.64 | 10.03 |
| Lithognatus mormyrus (Linnaeus 1758) | 10 | 0.18 | 196.28 | 0.38 |
| Labridae | ||||
| Coris julis (Linnaeus 1758) | 3 | 0.06 | 0.42 | 0 |
| Symphodus roissali (Risso 1810) | 201 | 3.69 | 1953.36 | 3.79 |
| Thalassoma pavo (Linnaeus 1758) | 288 | 5.28 | 3390.99 | 6.58 |
| Serranidae | ||||
| Epinephelus aeneus (Geoffroy Saint-Hilaire 1817) | 1 | 0.02 | 14.35 | 0.03 |
| E. marginatus (Lowe 1834) | 6 | 0.11 | 788.95 | 1.53 |
| Serranus scriba (Linnaeus 1758) | 1 | 0.02 | 139.52 | 0.27 |
| Sciaenidae | ||||
| Umbrina cirrosa (Linnaeus 1758) | 1 | 0.02 | 94.18 | 0.18 |
| Moronidae | ||||
| Dicentrarchus labrax (Linnaeus 1758) | 1 | 0.02 | 288.1 | 0.56 |
| Mullidae | ||||
| Mullus surmuletus Linnaeus 1758 | 1 | 0.02 | 23.7 | 0.05 |
| Mugilidae | ||||
| Oedalechilus labeo (Cuvier 1829) | 175 | 3.21 | 1880.21 | 3.65 |
| Siganidae | ||||
| Siganus luridus (Rüppell 1828)* | 159 | 2.92 | 10 534.26 | 20.42 |
| S. rivulatus (Forsskal 1775)* | 311 | 5.7 | 6343.31 | 12.31 |
| Pempheridae | ||||
| Pempheris vanicolensis Cuvier & Valenciennes 1831* | 635 | 11.65 | 7774.44 | 15.08 |
| total for supra-benthic species | 1932 | 35.44 | 38 597.28 | 74.87 |
| pelagic species | ||||
| Atherinidae | ||||
| Atherina boyeri Risso 1810 | 2 | 0.04 | 4.93 | 0.01 |
| Atherinomorus lacunosus (Forster 1801)* | 937 | 17.19 | 4707.69 | 9.13 |
| total for pelagic species | 939 | 17.22 | 4712.62 | 9.14 |
| total | 5452 | 100.00 | 51 550.59 | 100.00 |
The fish were separated into three categories: benthic (18 species), supra-benthic (16 species) and pelagic fish which occasionally approached the littoral (2 species) (Table 1). Four of the species (Pempheris vanicolensis, Siganus luridus, S. rivulatus and Atherinomorus lacunosus) are of Erythrean origin, yet none of the benthic fish were of Erythrean origin.
2. Ecological analysis of Shiqmona fish community
A total of 5,452 specimens weighing 51,550 g were collected. Of the five most abundant species (> 300 specimens) –Atherinomorus lacunosus, Pempheris vanicolensis, Siganus rivulatus, Parablennius zvonimiri and Scartella cristata– the first three were of Erythrean origin. Of the four species that contributed more than 10 % each of the total biomass –Pempheris vanicolensis, Siganus luridus, S. rivulatus and Diplodus sargus – the first three were of Erythrean origin. Analysis of distribution of the specimens and biomass among families revealed that the three most abundant families (with a total of > 750 specimens) were the Blenniidae, Atherinidae and Pempheridae (Fig. 2). The families that contributed most to biomass (> 4000 g) were Siganidae, Pempheridae, Labridae and Atherinidae.
Dispersal of individuals and biomass among the fish families in Shiqmona reef.
Variations in the number of species, specimens and biomass are presented in Fig. 3. The number of species in a sample varied from 19 to 27. With the exception of April 1996, when number of individuals and biomass were extremely low, the number of specimens varied from 723 to 1446, and the biomass values from 8,000 to 11,800 g. Benthic, supra-benthic and pelagic fish comprised 47 %, 35 %, 17 % of the specimens, and 16 %, 75 %, 9 % of the biomass respectively (Table 1).
Variations in the number of specimens and biomass in Shiqmona reef during the research period (number of species on top of columns).
The values of species diversity and evenness ranged, except in May, from 3.50 – 3.95, and 0.78 – 0.83, respectively (Fig. 4). The similarity indices for consecutive samples in both specimen and biomass analyses were > 50 %, except for the May – September period when the value decreased to 21 – 22 % (Fig. 5).
Variation in species diversity and evenness in Shiqmona reef during the research period.
Similarity between the consecutive samples in Shiqmona reef during the research period.
A comparison between fishes of Mediterranean origin and fishes of Red Sea origin (Table 2) shows that none of the benthic species is of Red Sea origin, whereas four of the non-benthic species stem from the Red Sea. Analysis of the relative abundance of the two groups shows that Red Sea fishes form > 70 % of specimens and > 67 % of the biomass of the non-benthic fish.
| species | individuals | biomass | |||||
| category | n | %* | n | %* | g | %* | |
| benthic fish | Mediterranean | 18 | 100 | 2581 | 100 | 8240 | 100 |
| Erythrean | 0 | 0 | 0 | 0 | 0 | 0 | |
| non-benthic fish | Mediterranean | 14 | 77.8 | 829 | 28.9 | 13 950 | 32.2 |
| Erythrean | 4 | 22.2 | 2042 | 71.1 | 29 359 | 67.8 | |
Discussion
The fish fauna of the Levant basin comprises 410 species, about 63 % of the fish species known from the entire Mediterranean (Golani, 1996; Goren & Galil, 1997), of which between 55 and 60 species inhabit the rocky littoral. Finding two-thirds of the ichthyofauna of the Levantine rocky littoral in a small area hints at possible high habitat complexity and biotic diversity.
Diamant et al. (1986) collected 26 species of fish from the rocky littoral at Dor, 25 km south of Shiqmona, of which 17 species were collected in Shiqmona too. At Dor more non-benthic species (e. g. Sparidae) were collected, whereas at Shiqmona benthic species form the majority, due perhaps to the wider rocky littoral which presents more ecological niches than in Dor. The fish fauna of Shiqmona reef lacks many supra-benthic species that appear at the interface between the rocky substrate and the sandy bottom.
Analysis of the species composition also revealed that even though the number of benthic/non-benthic specimens is similar, the biomass of benthic fish is one fifth of the total biomass, e. g. the average non-benthic fish is larger than the average benthic fish. The pelagic Atherinomorus lacunosus and the supra-benthic Pempheris vanicolensis and Siganus rivulatus, that are among the most abundant species on the rocky littoral (individuals and biomass), feed on the vermetid reef but spend most of their time outside the reef zone. This illustrates the importance of the reef as a food resource for the fish as well as a channel for nutrient transformation from the reef to the adjacent area.
The average number of species per family is 2.4, much lower than in the rest of the Mediterranean and less than one third that observed in tropical seas (Goren, 1993). At Shiqmona, as elsewhere in the western Mediterranean, blennies and gobies contribute the most species (Macpherson, 1994; Nieto & Alberto, 1993 – 94). However, whereas 9 out of the 17 locally known blennies were collected at Shiqmona, only 4 out of 16 locally known gobies were found. This could be due to the greater niche specificity of the gobies, a hypothesis that is under study.
Species diversity at Shiqmona was higher than at Dor (3.50 – 3.95 and < 2.86, respectively). The difference might arise from the high morphological complexity (Gasith & Gafny, 1998; Gasith et al., 2000), enabling high species richness of benthic fish in a small area, and from the distance of the littoral to the edge of the rocky area, which is expressed in the relative paucity of supra-benthic fish.
Comparison of the consecutive bimonthly samples (Fig. 5) indicates that the fish community in Shiqmona is unstable. This may result from sample variations due to sea conditions, the occasional entry of a great number of pelagic fish into the littoral, and the massive recruitment of young fish following the breeding seasons. The last explanation (recruitment) is relevant especially for the very low similarity between the samples of May and September, as most rocky littoral fish in the Eastern Mediterranean breed during spring and summer.
Erythrean fish make up nearly 50 % of the commercial trawl catch biomass (Golani & Ben Tuvia, 1995), so it was no surprise that Erythrean fish comprise almost 25 % of the species, 40 % of the specimens and over 50 % of the biomass of the supra-benthic species at Shiqmona. However, none of the benthic fish are of Red Sea origin, an unexpected result considering the abundance of the Erythrean fish in the neighboring habitats.
Safriel & Ritte (1980) suggested that overlap in ecological conditions between the rocky littoral in the northern Red Sea and the Levant, and a large pool of potential immigrants, would favour invasion of Erythrean benthic fish of the rocky littoral along the Levantine coast. However, none of the blennies, gobies and tripterygoid fish of the rocky littoral of the Red Sea have established a population in Shiqmona or elsewhere in the Mediterranean.
Most benthic fish in Shiqmona are short-lived substrate spawners with short pelagic larval stage which limits their distribution, and are characterized by restricted niches that prevent them from seeking different locations when temperatures rise. The combination of these factors could have enabled the evolution of Eastern Mediterranean ecotypes. Therefore, we suggest that this unexpected finding could be explained by pre-adaptation of the local fish to the unique extreme ecological conditions prevailing in the rocky littoral of the Eastern Mediterranean; this enabled them to compete successfully with the relevant Red Sea invader fish.
Summary
1) The fish community of Shiqmona reef comprises 36 species identified to 15 families.
2) The families richest in species were: Blenniidae and Gobiidae.
3) Eighteen species were characterized as benthic, sixteen as supra-benthic, and two as pelagic.
4) Four of the fish species at Shiqmona are of Red Sea origin.
5) None of benthic species at Shiqmona reef are of Red Sea origin.
6) Of the non-benthic fish at Shiqmona, species of Red Sea origin constitute > 70 % of the specimens and > 67 % of the biomass.
7) Atherinomorus lacunosus, Pempheris vanicolensis, Siganus rivulatus, Parablennius zvonimiri and Scartella cristata were the most abundant species at Shiqmona; the first three species are of Red Sea origin.
8) Pempheris vanicolensis, Siganus luridus, S. rivulatus and Diplodus sargus each made up more that 10 % of the biomass; the first three species are of Red Sea origin.
9) The values of species diversity and evenness ranged, except in May, between 3.50 – 3.95, and 0.78 – 0.83 respectively.
Acknowledgements
The Nature Protection and National Parks Authority has commissioned the study of the Shiqmona vermetid reef and its inhabitants. We thank Ms. R. Szmit and Ms. D. Friedman, who collected and sorted the material, as well as the diving crew of IOLR.
