Biogeography, diversity and conservation of the inland water fish communities in Israel

Biological Conservation 89 (1999) 1±9

Biogeography, diversity and conservation of the inland water ®sh communities in Israel Menachem Goren a,*, Reuven Ortal b,y a

Department of Zoology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv 69978, Israel b Department of Aquatic Ecology, Nature Reserves Authority, 78 Yirmeyahu St., Jerusalem 94467, Israel Received 16 April 1998; received in revised form 19 October 1998; accepted 21 October 1998

Abstract The inland ®sh fauna of Israel comprises 32 indigenous species belonging to eight families, and 14±16 introduced species. The native ®shes of Israel are of di€erent biogeographical origins: Africa, Central Asia, Levant, the Mediterranean and the Red Sea. The ®shes inhabit three separate water systems which have been divided in this work into 12 subunits, which di€er from each other in their ecological features. Twelve of the species are endemic to their catchments. Three of the species, all from the upper Jordan Valley, are extinct. The richest ichthyofauna is in the Jordan River Valley with 26 species, 19 of which are found in Lake Kinneret. The distribution patterns of the indigenous species have been updated and the ®sh assemblages in the di€erent systems are characterized. The human impact on ®sh biodiversity in Israel is documented here for the ®rst time, including changes in ®sh distribution patterns. # 1999 Elsevier Science Ltd. All rights reserved. Keywords: Inland-water ®shes; Israel; Biodiversity

1. Introduction The inland water ®shes of Israel have been studied since the ®rst description of Tilapia galileae by Artedi (in Hasselquist, 1857), more than 200 years ago. Research gained pace toward the end of the 19th century when Lortet (1875, 1876, 1883, Plates 6±18) and Tristram (1865, 1884) described the ichthyofauna of the region. Since then a vast amount of information has been published. The systematic and biogeographical aspects of the inland water ®shes have been studied by Banarescu et al. (1982), Ben Tuvia (1978, 1981), Ben-Tuvia et al. (1992), Coad (1984), Coad et al. (1983), Goren (1972, 1974, 1983), Goren et al. (1973), Krupp (1987), Krupp and Schneider (1989), Pellegrin (1923, 1933), Por (1989), Steinitz (1952, 1953, 1954, 1959), Steinitz and Ben Tuvia (1957), Tortonese (1938, 1952), Trewavas (1942, 1965) and Tristram (1865, 1884). Thirty-two indigenous species belonging to eight families inhabit in the inland water systems of Israel (Goren, 1983). In addition there are about 14±16 introduced species (Goren, 1983; Welcomme, 1988). The * Corresponding author. E-mail: [email protected] y E-mail: [email protected]

native ®shes of Israel are of di€erent biogeographical origins: Africa, Central Asia, Levant, the Mediterranean and the Red Sea. In spite of the numerous published articles, no integrated study has yet been made of the biodiversity of ®shes in the various parts of the water systems, with regard to the geographical origin of the species and the ecological characteristic of the habitats. This information is essential to prevent the continued extinction of ®shes in the various systems and to enable appropriate management of the aquatic habitats. The objectives of this study are: (1) to update the distribution patterns of the indigenous species; (2) to analyze and characterize the ®sh assemblages of the Israeli riverine systems; (3) to document the changes in distribution patterns, resulting from recent human activity; and (4) to suggest the necessary measures to protect the ichthyofauna of Israel. 2. The riverine system of Israel (Fig. 1) Since the post glacial period, the ®sh have inhabited three riverine systems, each of which can be divided into subunits as follows.

0006-3207/99/$Ðsee front matter # 1999 Elsevier Science Ltd. All rights reserved. PII: S0006-3207(98)00127-X

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M. Goren, R. Ortal/Biological Conservation 89 (1999) 1±9

2.2. The Jordan Valley system The Jordan Valley is part of the Syro-African Rift system. The core of the Jordan Valley system is the Jordan River which runs in a north±south direction from the slopes of Mount Hermon to the Dead Sea. The main water sources of the Jordan are the Dan, the Hermon (Banias) and the Senir (Hazbani) rivers. Numerous additional tributaries in Lebanon, Syria, Israel and Jordan drain from the Galilee mountains, Golan Heights, Judean and Samarian Hills. The Irbid and Ajlun mountain streams also empty into the river along its course. Two lakes were once located in its middle region and interrupted its ¯ow: Lake Hula in the central Hula Valley, which was arti®cially drained in the early 1950s; and Lake Kinneret (also known as Lake of Galilee or Lake of Tiberias), which is today the largest natural lake in the Middle East (ca. 170 km2). All sections of the Jordan Valley system are connected to each other via the Jordan River. The system is divided in this work into six subunits as follows:

Fig. 1. The water network of Israel.

2.1. The coastal system The coastal system comprises about 10 rivers and their tributaries, each with a separate drainage region. At the present time most of these rivers have become partially dry due to abstraction, and all are polluted to a certain extent. The rivers in this system run in an eastwest direction. The upper reaches of most of them are mountainous, originating in small springs and characterized by shallow water (for most of the year) and rocky beds with sandy pockets. The lower regions of the rivers run through the coastal plain, fed mostly by water from large springs merging at the foot of the mountains. The river beds comprise ®ne sediment with submerged vegetation. The coastal system is divided in this work into four units (basins) as follows: 1. Southern coastal system from Yarqon R. to Soreq R. (= s-c) (Alexander R. is not included as this river became severely polluted before sucient collections could be made). 2. Central coastal system from Taninnim R. to Daliyya R. (= c-c). 3. Qishon R. (=Q). 4. Northern coastal system from Na'aman R. to Keziv R. (= n-c).

1. Central Golan Heights platforms (=c-g). Small shallow streams with basalt rocky bed, some with submerged vegetation. 2. Upper reaches of the rivers (=u-r) running along both sides of the Jordan Valley. The bed is mostly rocky with many pockets of soft bottom. During the dry season, sections of the rivers dry up and the remaining streams are shallow with a few scattered ponds (0.5±2 m). During the rainy season the rivers become replenished. 3. Lower regions of the rivers in the Jordan system (= l-r). Water depth of these regions is 0.5±2.5 m all year long. The bed is either rocky or soft. Some of the pools feature submerged vegetation throughout the year. Occasional ¯oods cause a temporary 1±2 m rise in water level. 4. Central Hula Valley (including lake) (=c-h). An area which used to be a shallow lake surrounded by swamps (part of them seasonal); a large area of the muddy bed was covered by submerged vegetation. After the draining of the lake and swamps, a nature reserve (including a large shallow pond and swamps) was established. The main ¯ow of the water in the centre of the valley is carried via parallel canals which merge at the southern end of the valley. 5. Lake Kinneret (= K), a medium size (ca. 170 km2) young lake (12,000±18,000 years), with a maximum depth of 43 m. The bottom comprises mostly soft sediment. The substratum of the littoral zone varies from soft to rocky (the proportions depend on the water level). The northern part of the lake is an area of shallow lagoons with submerged vegetation. In cases of several successive

M. Goren, R. Ortal/Biological Conservation 89 (1999) 1±9

years of low water level, large parts of the littoral belt become covered by submerged vegetation. 6. Bet She'an±Yizrael Valleys (=b-s). An area of springs and rivers, some with saline water and constant high temperature (>20 C). 2.3. The Dead Sea Valley system The Dead Sea Valley system is a southern, isolated part of the Jordan River system. It comprises small springs scattered at the north-western and southern margins of the Valley. The springs are shallow with soft substrates, and some of them form small shallow pools with submerged algae. There is no freshwater link at the present time between the north-western and southern springs. The two subunits are: 1. The southern springs (= s-d) run in a south±north direction. The streams are scattered over a wide area of salty marsh, surrounded by Tamarix and Phragmites. 2. The north-western springs (= n-d) run in a west± east direction. The major area of springs is Ein Feshkha (Enot Zuqim), with several additional small springs scattered over the area of Ein Auar (Enot Qane, a few kilometres south of Ein Feshkha). 3. Methods 3.1. Distribution The distribution patterns of the di€erent species were obtained by analysis of >2500 catalogued samples deposited in the ®sh collections of the Zoological Museum at Tel Aviv University; the ®sh collection of the Hebrew University of Jerusalem, the inland water ecological survey laboratory collection of the Nature Reserves Authority, Jerusalem, and published data (as listed above) and on unpublished data accumulated by the authors during 30 years of ®eld studies. 3.2. Sampling methods The ®sh were collected using a variety of methods: traps of various types and sizes, nets of various lengths and mesh (gill net; trammel nets, hand nets, beach seines, etc.) and electro ®shing (up to 20 A, 450 V). 4. Results and discussion 4.1. Biodiversity 4.1.1. Fish communities in the water network of Israel The ®shes of African origin comprise the largest group in the water systems of Israel (28% of ®sh fauna) (Table 1).

3

The two other major groups are ®shes of Eurasian and of Middle Eastern origin (22% and 19%, respectively). Fishes from other sources form 413% each. Three of the native species became extinct after the drainage of Lake Hula. The coastal system is dominated by two groups: the catadromous ®shes Anguilla anguilla and several mullets (Mugilidae)Ðwhich do not occur naturally in other water systems; and by African ®shes (Cichlidae and Clariidae). An additional species found throughout the entire system in the cyprinodont ®sh Aphanius mento. The cyprinid ®sh in the coastal system show a de®nite trend: the greatest number of species are found in the centre of the system (including Qishon R., 3±4 species); while only 1±2 cyprinid species found in the northern and southern parts. Two of the cyprinid species found in the Qishon R. have never been found in other parts of the coastal system. No balitorid species have ever been found in any part of the coastal system. The Jordan Valley system is the richest of these systems, dominated by cyprinid and cichlid ®shes (10 and 7 species respectively). Approximately one-third of the species are of African origin (all the cichlids and the cat®sh) whereas most of the others are of Asiatic (Mesopotamian) origin. The richest part of this system is Lake Kinneret, with 19 species. The upper courses of the rivers in the Jordan Valley system (u-r) are characterized by the presence of depauperate fauna, consisting of three species: Capoeta damascina, Garra rufa and Nemacheilus jordanicus. The central Golan platform, although part of the Jordan Valley system, represents a di€erent, and impoverished section. The lowest number of species were found in the upper reaches of the central Golan Heights streams (c-g). The two species Pseudophoxinus drusensis and Nemacheilus panthera, which inhabit the water bodies of this region, are not found elsewhere in the system. The Dead Sea inland water systems are inhabited by only ®ve species: Aphanius dispar richardsoni is found in both sections of the system; Garra ghoerensis is restricted to the southern part of the system; and Aphanius mento, Sarotherodon galilaeus and Tilapia zillii are found only in its north-eastern part. 4.1.2. Biogeographical processes Biodiversity in inland water systems re¯ects the interaction between the available stock of species and environmental conditions. The stock of species in a system is the end product of the initial genetic pool and a variety of evolutionary processes, such as speciation, extinction and in®ltration from other systems, all of which make a contribution over time. Changes in water systems can alter the distribution of the ®sh as well as in¯uence their evolution. Because ®sh inhabit water, they can be used as good indicators for changes in water systems. By studying the detailed distribution of the ®sh, and possessing a good knowledge of their biology, we can trace even

4

M. Goren, R. Ortal/Biological Conservation 89 (1999) 1±9

Table 1 List of the water inland ®shes of Israele Origin

Recent distribution Coastal system

Jordan Valley system

Dead Sea

s-c c-c Q n-c

c-g u-r

l-r c-h K b-s

n-d

s-d

Anguillidae Anguilla anguilla (Linnaeus, 1758)

Mediterranean

+ + + +

±

±

± ±

± ±

±

±

Cyprinidae Acanthobrama lissneri (Tortonese, 1952)a Acanthobrama telavivensis (Goren et al., 1973)b Barbus canis (Valenciennes, 1842) Barbus longiceps (Valenciennes, 1842) Capoeta damascina (Valenciennes, 1842) Garra ghoerensis (Krupp, 1987)c Garra rufa (Heckel, 1843) Hemigrammocapoeta nana (Heckel, 1843) Mirogrex hulensis (Goren et al., 1973)ad Mirogrex terraesanctae (Steinitz, 1952)a Pseudophoxinus drusensis (Pellegrin, 1933) Pseudophoxinus kervillei (Pellegrin, 1911)

Middle East Middle East Asia±Africa Asia Middle East Asia Asia Middle East Middle East Middle East Asia±Europe Asia±Europe

± + ± ± ± ± ± ± ± ± ± ±

± + ± ± + ± + ± ± ± ± ±

+ ± ± ± ? ± + + ± ± ± ±

± + ± ± + ± ± ± ± ± ± ±

± ± ± ± ± ± ± ± ± ± + ±

± ± ± ± + ± + ± ± ± ± ±

+ ± + + + ± + + ± ± ± +

+ ± + + + ± + + + ± ± +

+ ± + + + ± + + ± + ± +

+ ± + + + ± + + ± ± ± ±

± ± ± ± ± ± ? ± ± ± ± ±

± ± ± ± ± + ± ± ± ± ± ±

Balitoridae Nemacheilus dori (Goren and Banarescu, 1982)a Nemacheilus jordanicus (Banarescu and Nalbant, 1966) Nemacheilus panthera (Heckel, 1843) Nemacheilus tigris (Heckel, 1843) Nun galilaeus (GuÈnther, 1864)ad

Asia±Europe Asia±Europe Asia±Europe Asia±Europe Asia±Europe

± ± ± ± ±

± ± ± ± ±

± ± ± ± ±

± ± ± ± ±

± ± + ± ±

± + ±(+) ± ±

+ + ± ± ±

± + ± ±

± ± ± + +

+ + ± ± ±

± ± ± ± ±

± ± ± ± ±

Clariidae Clarias gariepinus (Burchell, 1822)

Africa

+ + + +

±

±

++ ++

±

±

Cyprinodontidae Aphanius mento (Heckel, 1843) Aphanius dispar richardsoni (Boulenger, 1907)c

Asia Red Sea

+ + + + ± ± ± ±

± ±

± ±

± + ++ ± ± ± ±

+ +

± +

Mugilidae Mugil cephalus (Linnaeus, 1758) Liza ramada (Risso, 1810)

Mediterranean Mediterranean

+ + + + + + + +

± ±

± ±

± ± ± ±

± ± ± ±

± ±

± ±

Blenniidae Salaria ¯uviatilis (Asso, 1801)

Mediterranean

±

+ ±

±

±

±

± ±

+±

±

±

Cichlidae Astatotilapia ¯aviijosephi (Lortet, 1883, Plates 6±18)a Oreochromis aureus (Stiendachner, 1864)a Oreochromis niloticus (Linnaeus, 1758) Sarotherodon galilaeus (Artedi, 1757) Tilapia zillii (Gervais, 1848) Tristamella sacra (GuÈnther, 1864) Tristramella simonis intermedia (Steinitz and Ben-Tuvia, 1960)d Tristramella simonis simonis (GuÈnther, 1864)a

Africa Africa Africa Africa Africa Africa Africa Africa

± + + + + ± ± ±

± + ± + + ± ± ±

± ± ± + + ± ± ±

± ± ± ± ± ± ± ±

± ± ± ± ± ± ± ±

± + ± + + ± ± ±

+ + ± + + + ± +

± + ± + + ± ± ±

± ± ± ± ± ± ± ±

Total number of species

32

10 12 11 9

2

3

13 15 19 14

5

2

a

± + ± + + ± ± ±

± + ± + + ± + ±

+ + ± + + ± ± ±

Endemic to the Jordan R. system (A. lissneri is found also in Qishon R.). Endemic to coastal system. c Endemic to Dead Sea system. d Extinct species. e Coastal system: s-c: southern coastal system (Yarqon R.±Soreq R.); c-c: central coastal system (Taninim R±Daliyya R.); Q: Qishon R.; n-c: northern coastal system (Na'aman R.±Keziv R.). Jordan Valley system: c-g: central Golan Hights platform; u-r: upper reaches of the rivers in the Jordan system; l-r: lower parts of the rivers in the Jordan system; c-h: central Hula Valley (inc. former lake); K: Lake Kinneret; b-s: Bet She'an± Yizrael Valleys. Dead Sea system: n-d: n.w. springs; s-d: southern springs. b

M. Goren, R. Ortal/Biological Conservation 89 (1999) 1±9

minor changes in the hydrological history of a region that can not be traced otherwise. The presence of two groups of cichlids in the Jordan Valley may indicate at least two waves of migration from the coastal system: the former included the ancestors of Tristramella sacra, T. simonis and Astatotilapia ¯aviijosephi; and the more recent one enabled the migration of other cichlids such as Oreochromis aureus, Sarotherodon galilaeus and Tilapia zillii, whose conspeci®c relatives are quite abundant in Africa. The pattern of distribution of cyprinid ®sh in the coastal system may indicate at least three waves of migration from the Jordan Valley. The ®rst brought the ancestors of Acanthobrama telavivensis, which is endemic to the coastal system, and water links then enabled the dispersal of this species throughout the entire coastal system. The absence of other cyprinid species from the southern coastal system is remarkable and can be explained either by special ecological conditions (such as muddy substrata) in the Bet-She'an - Qishon Valleys corridor during the period of migration, or by the absence of other cyprinids in Bet-Shean Valley at that time. The presence of Capoeta damascina and Garra rufa in the central coastal system together with A. telavivensis may point to the second link with the Jordan Valley. Connection with the northern and southern parts of the coastal system had already been broken by this time and these ®sh could not penetrate into them. The presence of Acanthobrama lissneri and Hemigrammocapoeta nana in Qishon R. which interrupted the continuous distribution of A. telavivensis, may be an indicator for a third, more recent penetration of ®sh into the coastal system. 4.2. Human impact on ®sh biodiversity 4.2.1. Introduced species The introduction of ®sh into Israel dates back to the 1920s when mosquito ®sh were introduced as an antimalaria agent, and to the late 1930s when Cyprinus carpio was introduced for aquaculture purposes. Since then, about 15 introduced species have been found in the inland waters of Israel, and additional species have been reported from ®sh ponds as aquaculture subjects (Ben-Tuvia, 1981; Goren, 1983; Welcomme, 1988) (Table 3). Some of the feral species have already established breeding populations, a few are regularly stocked and others are occasionally recorded from natural waters. Mugilid ®sh, which occur naturally in the coastal system, are regularly stocked in Lake Kinneret (Jordan Valley system). The eel Anguilla anguilla has been stocked unintentionally with the mugilid ®sh. Due to lack of previous data, it is dicult to estimate the impact of the introduction of these ®sh into the systems. The mosquito ®sh dominate the open shallow water of ponds and lakes, whereas Aphanius is found only in the

5

vegetated habitats. In the Southern Dead Sea area, the introduction of mosquito ®sh probably caused the extinction of Garra ghoerensis from most of the system. The running water aquaculture of exotic trout, salmon and sturgeon in the Jordan River sources (Dan, Hermon and Senir Rivers) led to the inadvertent introduction of these species to the Jordan River and Lake Kinneret. These predatory species, which are currently being found even in nature reserves, are a€ecting the local invertebrate communities. There is no direct evidence of additional damage by introduced species to the ichthyofauna, but it may be assumed that the trout a€ect the native ®sh fauna through food competition (Degani et al., 1987) and direct predation on post larvae. The main reason for introduced ®shes being found in natural waters is their escape from the commercial ponds where they are reared for human consumption. An additional source is the prosperous exotic hobby®sh industry (Table 3). These species, as well as various types of ®shpond hybrids, occasionally escape and are found in natural habitats. Other exotic species have not yet been recorded from natural habitats, but are expected to appear, sooner or later. Commercial aquaculture is a source for cichlid hybrids as is well documented at the Tel Aviv University museum. As these ®sh are partly or completely sterile they do not establish viable populations, but those ®sh which are partially fertile, may cause genetic contamination, especially for the species O. aureus. The national water carrier, which brings water from Lake Kinneret to the coastal plain and southern Israel, serves as an important factor in altering ®sh distribution patterns. An additional vector is the Yarqon R. diversion project, which is connected to the national water carrier. Laventer (1974) reported that open reservoirs in areas where no ®sh had previously been found, had become inhabited by Kinneret ®sh which had in®ltrated mainly through the national water carrier. Although mechanical ®lters prevent ®sh in®ltration from the Jordan valley reservoirs into the coastal region, at least one specimen of Acantobrama lissneri was collected from a water pipe in the southern part (Negev) of the National Water Carrier (10 cm long specimen deposited in the Tel Aviv Museum). 4.2.2. Human impact on ®sh biodiversity through changes in the habitats While the natural changes (geological and evolutionary) and human impact on the aquatic ecosystem prior to the 1950s caused changes in habitat structure and ®sh biodiversity at a ``geological'' (very slow) pace, the changes over the last 50 years have been dramatic and traumatic to the systems and to their resident fauna. Three major changes, which have taken place especially since the 1950s, have a€ected the aquatic habitats, and as a consequence, the ®sh biodiversity: (1) water

6

M. Goren, R. Ortal/Biological Conservation 89 (1999) 1±9

diversion has caused a severe reduction in river water levels (especially due to pumping of water from the aquifers which feed the rivers); (2) drainage rehabilitation has changed the structure of many rivers; and (3) water pollution from domestic and industrial sources has led to high levels of pollutants, mainly in the coastal rivers (Gasith, 1992). These changes have a€ected the entire aquatic system. Two rivers in the coastal system (Soreq and Alexander) have become completely polluted and all their native species are now extinct. Only the cat®sh Clarias gariepinus, which probably survives in small tributaries of these rivers, can occasionally be found there. All other coastal rivers are either partly polluted or dry. In most of them the small populations of native ®sh are restricted to the relatively clean river heads (Yarqon, Qishon, Na'aman etc.). Taninnim is exceptional as the only remaining coastal river with running water throughout the year; it su€ers from the least anthropogenic impact and probably sustains its original species. To date, only one species, Oreochromis niloticus, which was recorded only from the Yarqon, has become extinct in the coastal system. The Jordan Valley system experiences much less water pollution than the coastal system, despite having undergone more dramatic environmental and structural changes, including: (1) the complete drainage of Lake Hula and its swamps; (2) a sharp decrease in water level in the rivers during the dry season; (3) changes in water ¯ow regime as a result of water course rehabilitation; (4) damming of the Lake Kinneret out¯ow and the release of water into the lower Jordan R. only during occasional ¯oods, thus only rarely enabling downstream ®sh migration; and (5) the development of an intensive inland aquaculture industry, which adds a high nutrient load and introduces into the system ®sh such as carp Cyprinus carpio, silver carp Hypophthalmichthys molitrix and mullet Liza ramada, Mugil cephalus as well as predatory ®sh such as trout Oncorhynchus mykiss, sturgeon (hybrid of Huso huso), eel Anguilla anguilla, swordtail Xipohphorus helleri and mosquito ®sh Gambusia anis. The most drastic event in this system took place in the Hula Valley, where the water regime has twice undergone change. First, in the 1950s, when Lake Hula and the surrounding swamps (ca. 6000 ha) were drained for soil reclamation and ¯ood control. This caused a major destruction of the ichthyofauna which included 17 indigenous species, three of which (Mirogrex hulensis, Nun galilaeus and Tristramella simonis intermedia) were endemic to the lake (Table 2), and two of which were exotic species. A small nature reserve (ca. 300 ha) was concomitantly established at the margins of the former lake which partly saved the aquatic biota. For a while this was a success and most of the ichthyofauna survived. A survey made by the ®rst author in 1968 (Goren, unpublished data), 15 years after the reserve was cre-

Table 2 Loss of ®sh fauna in Lake Hula between 1953 and 1995 1953 1968 1995 Cyprinidae Barbus canis (Valenciennes, 1842) Barbus longiceps (Valenciennes, 1842) Capoeta damascina (Valenciennes, 1842) Mirogrex hulensis (Goren et al., 1973) Acanthobrama lissneri (Tortonese, 1952) Pseudophoxinus kervillei (Pellegrin, 1911) Garra rufa (Heckel, 1843) Hemigrammocapoeta nana (Heckel, 1843) Cyprinus carpio (Linnaeus, 1758)a Hypophthalmichthys molitrix (Valenciennes, 1844)a

+ + + + + + + + +

+ + + + + + + + + +

+

+

Balitoridae Nemacheilus jordanicus (Banarescu and Nalbant, 1966) Nun galilaeus (GuÈnther, 1864) Nemacheilus panthera (Heckel, 1843)

+ +

Clariidae Clarias gariepinus (Burchell, 1822)

+

+

Cyprinodontidae Aphanius mento (Heckel, 1843)

+

+

Poeciliidae Gambusia anis (Baird and Girard, 1853)a

+

+

+ + + +

+ + +

Cichlidae Tilapia zillii (Gervais, 1848) Oreochromis aureus (Stiendachner, 1864) Sarotherodon galilaeus (Artedi, 1757) Tristramella simonis intermedia (Steinitz and Ben-Tuvia, 1960) Mugilidae Liza ramada (Risso, 1810)a Mugil cephalus (Linnaeus, 1758)a

+ +

+

+

+ +

Native species

17

14

2

Introduced species

2

5

2

Total

19

19

4

a

Introduced species.

ated, revealed 14 indigenous species, including Mirogrex hulensis and ®ve exotic species in the nature reserve (Table 2). During the ®rst period, the Enan hot springs (about 20 C) ¯owed into the reserve, providing a refuge of warm water for the cichlids during the cold periods of winter, when the winter ¯oods removed the bottom sediment, leaving small areas of the reserve with stony beds. This clear running water enabled the growth of aquatic vegetation such as Myriophyllum spicatum and provided the ®sh with a suitable spawning ground. The second major change was during the 1970s, when mass diversion of water from the Enan springs caused a

M. Goren, R. Ortal/Biological Conservation 89 (1999) 1±9 Table 3 List of introduced ®shes found in natural water bodies in Israel Species found in natural aquatic systems 1. Acipenseridae hybrid of Huso huso (Linnaeus, 1758) (?) 2. Anguillidae Anguilla anguilla (Linnaeus, 1758)a 3. Salmonidae Oncorhynchus mykiss (Walbaum, 1792)b 4. Salmonidae Oncorhynchus kisutsch (Walbaum, 1792) 5. Cyprinidae Carassius carassius (Linnaeus, 1758) 6. Cyprinidae Ctenopharyngodon idella (Valenciennes, 1844) 7. Cyprinidae Cyprinus carpio (Linnaeus, 1758)b 8. Cyprinidae Hypophthaimichthys molitrix (Valenciennes, 1844) 9. Poeci¯idae Gambusia anis (Baird and Girard, 1853)b 10. Poeciliidae Xiphpohorus helleri (Heckel, 1848)b 11. Poeciliidae Poecilia velifera (Regan, 1914) 12. Serranidae Dicentrarchus labrax (Linnaeus, 1758)a 13. Cichlidae Cichlosoma nigrofasciatum (GuÈnther, 1867)b 14. Cichlidae Hybrids of Oreochromis aureus  0. niloticus 15. Mugilidae Liza ramada (Risso, 1826)a 16. Mugilidae Mugil cephalus (Linnaeus, 1758)a Species introduced into arti®cial ponds, not yet found in natural systems 1. Cyprinidae Aristichthys nobilis (Richardson, 1845) 2. Cyprinidae Catla catla (Hamilton-Buchanan, 1822) 3. Cyprinidae Mylopharyngodon piceus (Richardson, 1846) 4. Cyprinidae Tinca tinca (Linnaeus, 1758) 5. Catastomidae Ictiobus cyprinella (Valenciennes, 1844) 6. Atherinidae Basilichthys bonariensis (Valenciennes, 1835) 7. Cichlidae Oreochromis mossambicus (Peters, 1852) a Occurred naturally in the coastal system, stocked in the Jordan Valley system. b Breed naturally in the wild.

decline in both the warm water discharge and ¯ood water; the stony canal beds became covered by sediment and the water became turbid. The result was the elimination of suitable spawning grounds for many species, as well as the destruction of a thermal refuge for the cichlids. Under the new water regime, the Enan waterpipe diverted only 50 m3/h into the reserve, which has been found to be insucient to maintain its needs. A second major problem since then has been caused by nutrient overload of the water sources and an insucient water regime management in the reserve. Only four species are still found today in the reserve (Table 2): two original species, the cat®sh Clarias gariepinus and the cyprinid Hemigrammocapoeta nana, and two exotic species, the carp Cyprinus carpio and the mosquito ®sh Gambusia anis. The situation was exaggerated by the Hula reserve management policy which aimed mainly at protecting waterfowl and supplying their food. This policy turned the main water bodies into something resembling ®shponds and led to the almost total destruction of the Hula natural ichthyofauna, including the extinction of the endemic species Mirogrex hulensis. Such adverse results could have been at least partly prevented by applying a more comprehensive approach. In Bet She'an Valley, the ®sh fauna has survived continuous changes in the habitat structure. However, the

7

ongoing reclamation projects are causing fragmentation and isolation of water bodies and a severe reduction in ®sh populations, as well as endangering the Nemacheilus spp. whose taxonomic status is not yet clear. The Dead Sea system is a€ected by the continuous decrease in water level caused mainly by the diversion of 80±90% of the water from the southern part of the Jordan River and by the mineral industry on its southern part. The reduction in water level a€ects the water ¯ow and habitat structure of the springs surrounding the Dead Sea. This has reduced ®sh population size in several springs but has not yet endangered them. 4.3. Conservation of ®sh The conservation policy for the Israeli inland ichthyofauna is based on protecting their important habitats as nature reserves. One hundred and twenty out of over 400 nature reserves in Israel are marine and wetland reserves with a total of over 2000 km2. These reserves feature all types of wetland and host all native ®sh species. In contrast to many marine taxa, none of the inland-water ®sh species of Israel has been declared a protected species. The three ®sh which are now extinct, were eliminated from Israeli wetlands prior to the passage of the National Parks, Nature Reserves, National Monuments and Memorial Sites Law in 1963. Only one species, Mirogrex hulensis, was eliminated in the Hula Nature Reserve after the passage of the law, as a consequence of changing the amount and quality of the water supply, as well as the management policy which was oriented to waterfowl welfare. The sport of inland-water ®shing is not popular in Israel, and far less developed than coastal ®shing. The main sport ®shery includes carps and cichlid species in the upper Jordan water-system, and exotic salmonids in the Jordan River sources (Dan, Hermon and Senir). This sport is completely forbidden in inland-water nature reserves. Sport ®shing in the coastal drainage basin hardly exists due to high levels of water pollution. In these rivers, which are connected to the Mediterranean, the penetration of anadromous species such as the European eel and mullets has been observed. This phenomenon mainly occurs in the Na'aman R. up to the En Afeq Nature Reserve, Ramsar site. The protection of rare species or small fragile populations, take place through habitat conservation. For example the rare species of Nemacheilus dori is protected in the En Malqoah Nature Reserve (Bet She'an valley), Nemacheilus panthera in some small springs in the Golan Heights Nature Reserves and Garra ghorensis in the southern Dead Sea springs area (Neot HaKikkar Nature Reserve). A di€erent kind of problem is the increase in amounts of water being pumped form Lake Kinneret. As a result,

8

M. Goren, R. Ortal/Biological Conservation 89 (1999) 1±9

the amplitude of the water level in the lake which used to be 1±2 m, has recently increased to 2±4 m. This a€ect ®sh biodiversity in the littoral zone of the lake (Gasith et al., in press). The expected additional increase in amounts of pumped water preset a threat to the Lake Kinneret populations of some species such as Garra rufa, Nemacheilus tigris and Astatotilapia ¯aviijosephi which depend on availability of rocky habitats in the lake. Goren and Gasith (in press), who rely on the results of their long term research in the lake, suggested to maintain ®sh biodiversity in the lake through creating alternative habitats for the ®shes and through management of ®shery by applying proper regulations. 5. Conclusion The coastal water system has been adversely a€ected more than any other. Since the 1950s, the rivers in this system have su€ered heavy pollution as well as a severe drop in water level during the dry season. As described above, these changes a€ect mainly the coastal system where parts of the rivers dry up during summer and most of the rest turn into sewage canals. So far only one species, Oreochromis niloticus, has become extinct in this system and an e€ort has been made recently to halt further deterioration of water quality and to rehabilitate the coastal system in order to prevent further extinction of species. In the Jordan Valley system the major problem results from changes in habitat structure (which have caused fragmentation of the ®sh population) and a decrease in structural complexity (which has eliminated breeding sites and shelters). These changes have so far caused the extinction of three endemic species in the Hula Valley. Like most Middle East countries, Israel su€ers from an increasing shortage of water. The resulting increased demand for a more ``rational'' use of this limited resource, may thereby jeopardize the aquatic ecosystems and the ®sh that inhabit them. The pressure is especially heavy on the water resources in the Jordan Valley and, therefore, prospects for the future well-being of the ichthyofauna in this region are gloomy. Under modern conditions of a changing environment in an arid country such as Israel, only proper management, which includes the assurance of minimal amounts of water to the various habitats during the dry seasons, and the protection on the structural complexity of the habitats, can ensure the maintenance of biodiversity in the human a€ected habitats. In contrast to the understanding in developed countries for the need to conserve inland aquatic habitats and their fauna, such planing is not on the agenda of most Middle East countries. As re¯ected in over twenty articles assembled by Crivelii and Maitland (1995), and from other publications such as Crivelii (1995) and

Maitland and Crivelii (1996) the scienti®c background (information, knowledge and scientists) for conservation for northern Mediterranean ®shes exists, and detailed conservation proposals have been formulated. In most of the eastern Mediterranean, however, the science of ®sh conservation is very undeveloped. Conservation of all aquatic biota needs to be planned on a regional basis, and surveys of the inland water systems of the whole of the eastern Mediterranean region are badly needed. Acknowledgements The authors are grateful to Dr. D. Golani of the Hebrew University of Jerusalem for access to the ®sh collection and for his critical comments. We also thank Ms. N. Paz of Tel Aviv University and Dr. S. Nemtzov of the Nature Reserves Authority for editing this paper.

References Artedi, P., 1757. Sparus Galilaeus. In 1757 Iter Palaestinum, eller vesa til Heliga Landet, foÈraÈttad ifraÊn ar 1749 til 1752. ed. F. Hasselquist, XIV+619 pp. Stockholm, Sweden. Asso, I.J. de, 1801. IntroduccioÂn aÂla Ichthyologia oriental de EspanÄa. Anales de Ciencias Naturales del Institute Jose Acosta 10, 28±52. Baird, S.F., Girard, C., 1853. Descriptions of new species of ®shes collected by Mr. John H. Clark, on the U.S. and Mexican Boundary Survey, under Lt. Col. Jas. D. Graham. Proceedings of the Academy of Natural Science, Philadelphia 6, 387±390. Banarescu, P., Nalbant, T.T., 1966. Zwei neue Schmerlen der Gattung Noemacheilus (Pisces, Cobitidae) aus Jordanien. Mitteilungen aus dem hamburgischen zoologischen Museum und Institut 63, 329±336. Banarescu, P.M., Nalbant, T.T., Goren, M., 1982. The noemacheiline loaches from Israel (Pisces: Cobitidae: Noemacheilinae) Israel. Journal of Zoology 31, 1±25. Ben-Tuvia, A., 1978. Fishes. In: Serruya, C. (Ed.), Lake Kinneret Monographiae Biologicae. Dr. W. Junk. The Hague, pp. 407±430 Ben-Tuvia, A., 1981. Man-induced changes in the freshwater ®sh fauna of Israel. Fishery Management 12 (4), 139±148. Ben-Tuvia, A., Davido€, E.B., Shapiro, J., She¯er, D., 1992. Biology and management of Lake Kinneret ®sheries. Israeli Journal of Aquaculture Bamidgeh 44, 48±65. Boulenger, G.A., 1907. Zoology of Egypt. The Fishes of the Nile. 2 vols, 578 pp. London. Burchell, W., 1822. Travels in the Interior of Southern Africa. Vol 1, 425 pp. London. Coad, B., 1984. Acanthobrama centisquamis Heckel and the validity of the genus Mirogrex Goren, Fishelson and Trewavas (Osteichthyes: Cyprinidae). Hydrobiologia 109, 275±278. Coad, B.W., Alkahem, H.F., Behnke, R.J., 1983. Acanthobrama hadiyensis a new species of cyprinid ®sh from Saudi Arabia. National Museum of Natural Sciences, Canada, 2, 1±6. Crivelii, A.J., 1995. The freshwater ®sh endemic to the northern Mediterranean region: An action plan for their conservation. Tour du Valat, Arles. 1±171. Crivelii, A.J., Maitland, P.S. (Eds.), 1995. Endemic Freshwater Fishes of the Northern Mediterranean Basin: Status, Taxonomy and Conservation (special issue). Biological Conservation 72, 121±337. Degani, G., Bromley, H.J., Ortal, R., Netzer, Y., Harari, N., 1987. Diet of the rainbow trout (Salmo gardneri) in a thermally constant stream. Vie Milieu 37 (2), 99±103. Gasith, A., 1992. Conservation and management of the coastal streams of Israel: an assessment of stream status and prospect for rehabilitation. In: Boon, P.J., Calow, P., Petts, G.E. (Eds.), River Conservation and Management. Wiley, New York, pp. 51±64.

M. Goren, R. Ortal/Biological Conservation 89 (1999) 1±9 Gasith, A., Gafny, S., Goren, M. Availability and importance of structured habitats for the ®sh community in lake Kinneret (Israel). Archeive fur Hydrobiologie, in press Gervais, F.L.P., 1848. Sur les animaux veÂrteÂbres de l'AlgeÂrie, envisage rous le double rapport de geÂographie zoologique et de la domestication. Annales des Sciences Naturelles (Zoologie) 10 (3), 202±208. Goren, M., 1972. The populations of Pseudophoxinus zeregi (Heckel) in Israel and Syria and the status of Pseudophoxinus (Pararhodeus) drusensis (Pellegrin) (Pisces: Cyprinidae). Zoological Journal of the Linnean Society 51 (2), 141±145. Goren, M., 1974. The freshwater ®shes of Israel. Israel Journal of Zoology 23, 67±118. Goren, M., 1983. Freshwater Fishes of Israel: Biology and Taxonomy Hakibbutz Hameuchad Publishing House, Tel Aviv. (in Hebrew). Goren, M., Banarescu, P.M., 1982. Orthrias dori n. sp. In The Noemacheiline Loaches from Israel (Pisces: Cobitidae: Noemacheilinae). eds. P.M. Banarescu, T.T. Nalbant. Isreal Journal of Zoology 31, 1±25. Goren, M., Fishelson, E., Trewavas, E., 1973. The cyprinid ®shes of Acanthobrama Heckel and related genera. Bulletin of the British Museum (Natural History) Zoology 24, 291±315. Goren, M., Gasith, A., 1998. The maintenance of ®sh biodiversity in habitats a€ected by human activity in lake Kinneret. In: Rossiter, A., Kawanabe, H. (Eds.), Biology of Ancient Lakes. In press. GuÈnther, A., 1864. Report on a collection of ®shes from Palestine. Proceedings of the Zoological Society, London 488±493. GuÈnther, A., 1867. On the identity of Alepisauras (Lowe) with Plagyodus (Steller). Annals and Magazine of Natural History (Series 3) 19 (111), 185±187. Hasselquist, F., 1757. Iter Palestinum, eller vesa til Heliga Landet, foÈraÈttad ifraÊn ar 1749 til 1752, Stockholm. Hamilton-Buchanan, T., 1822. An account of the Fishes of the Ganges. VII+405 pp. Edinburgh, UK. Heckel, J.J., 1843. Ichthyologie. In: J. Russegger: Reise in Griechenland, Unteraegypten, im noÈrdlichen Syrien und SuÈdoÈstlichen Kleinasien, ed. J. Russegger. Vol. 1 (2), pp. 991±1099. Stuttgart, Germany. Heckel, J.J., 1848. Eine neue Gattung von Poecilien mit rochenartigem Anklammerungs-Organe. Sitzungsberichte Akademi Wissenschaften. Vol. 1, pp. 289±303, Pls. 8±9. Vienna, Austria. Krupp, F., 1987. Freshwater ichthyogeography of the Levant. In: Krupp, F., Schneider, W., Kinzelbach, R. (Eds.), Proceeding and Symposium on the Fauna and Zoogeography of the Middle East. Beihefte zum TAVO A 28, 229±237. Krupp, F., Schneider, W., 1989. The ®shes of the Jordan River drainage basin and Azraq Oasis. Fauna of Saudi Arabia 10, 347±416. Laventer, H., 1974. The Israeli Water SystemÐThe Reservoirs. Mekorot (in Hebrew). Linnaeus, C., 1758. Systema Naturae. Edn. 10. 1. 824 pp. (Reprint 1956, London). Lortet, L., 1875. Sur un poissons du Lac de Tiberade le Chromis paterfamilias, qui incube ses oeufes dans la cavite buccale. Comptes rendus hebdomadaires des SeÂances de l'AcadeÂmie des Sciences, Paris, 81, 1196±1198. Lortet, L. 1876. Le Chromis paterfamilias du lac de Tiberade. La Nature, Paris, 4 (1), 81±82. Lortet, L., 1883. Poissons et reptiles du lac de Tiberade. Archives du MuseÂum d'Histoire naturelle de Lyon 3, 99±181. Maitland, P.S., Crivelli, A.J. 1996. Conservation of freshwater ®sh. Conservation of Mediterranean Wetlands. Tour du Valat, Arles 7, 1±94. Pellegrin, J., 1923. Etude sur les poisson rapportes par M. Henri Gadeau de Kerville de son voyage zoologique en Syrie. In: H. Gadeau de Kerville en Syrie, Voyage Zoology, vol. 4, pp. 1±39. J.B. BaillieÁre et Fils, Paris. Pellegrin, J., 1933. Description d'un poisson nouveau de la Syrie meÂridionale apparetenant au genera Phoxinellus. Bulletin du Museum d'Histoire Naturelle, Paris 5, 368±369. Peters, W.C.H., 1852. Diagnosen von neuen Fluss®schen aus Mossambique. Monatlichen publication der Akademi Wissenschaften, pp. 275±276, 681±685. Berlin, Germany.

9

Por, F.D., 1989. The legacy of TethysÐan aquatic biogeography of the Levant. In: Monographiae Baiologicae, vol. 63. Springer, New York. Regan, C.T., 1914. Description of a new cyprinodont ®sh of the genus Mollienisia from Yucatan. Annals and Magazine of Natural History (Series 8) 13 (75), 338. Richardson, J., 1845. Ichthyology. Part 3. In The Zoology of the Voyage of H.M.S. Sulphur, under the Command of Captain Sir Edward Belcher, R.N., C.B., F.R.G.S., etc., during the years 1836± 42, No. 10, ed. R.B. Hinds, pp. 99±150, Pls. 55±64. Smith, Elder & Co., London. Richardson, J., 1846. Report on the ichthyology of the seas of China and Japan. Advancement of Science 15th Meeting [1845], 187±320. Risso, A., 1810. Ichthyologie de Nice, ou Histoire Naturelle des Poissons du DeÁpartment des Alpes Maritimes, XXXVI+388 pp.+11 pls. Paris, France. Risso, A., 1826. Histoire Naturelle des Principales Productions de l'Europe MeÂridionale et particulieÁrement de Celles des Environs de Nice et des Alpes Maritimes, Vol. 3, 480 pp. Paris, France. Steindachner, F., 1864. Ichthyologische Mitteilungen (VII). Verhandlungen der Zoologisch-botanischen Gesellschaft in Wien 4, 223±232. Steinitz, H., 1952. Acanthobrama terraesanctae sp.n. from Lake Tiberias, Israel. Annals and Magazine of Natural History 5 (12), 293±298. Steinitz, H., 1953. The freshwater ®shes of Palestine. An annotated list. Bulletin of the Research Council of Israel 3B, 207±227. Steinitz, H., 1954. The distribution and evolution of the freshwater ®shes of Palestine. Publication of the Hydrobiological Research Institute, Faculty of Science, University of Istanbul. B1, 225± 275. Steinitz, H., 1959. Dr. H. Lissner's study of the biology of Acanthobrama terraesanctae in Lake Tiberias. Bulletin of Sea Fisheries Research Station, Israel B8, 43±64. Steinitz, H., Ben-Tuvia, A., 1957. The hybrids of Barbus longiceps C.V. and Varicorhinus damascinus C.V. (Cyprinidae, Teleostei). Bulletin of the Research Council of Israel 6B, 176±188. Steinitz, H., Ben-Tuvia, A., 1960. The cichlid ®shes of the genus Tristramella Trewavas. Annals and Magazine of Natural History 3, 161±175. Tortonese, E., 1938. Viaggio del Enrico Festa in Palestina e in Siria (1893), Pesci. Bullettino del Museo di Zoologia dell'Universita di Torino 3, 15±20. Tortonese, E., 1952. On a new cyprinoid ®sh of the genus Acanthobrama from Palestine. Annals and Magazine of Natural History 5 (12), 271±272. Trewavas, E., 1942. The cichlid ®shes of Syria and Palestine. Annals and Magazine of Natural History 9 (11), 526±536. Trewavas, E., 1965. Tilapia aurea (Steindachner) and the status of Tilapia nilotica exul, T. monadi and T. lamassoni (Pisces: Cichlidae) Israel. Journal of Zoology 14, 258±276. Tristram, H.B., 1865. The Land of Israel, XX+651 pp.+12 pls, 2 maps. London, UK. Tristram, H.B., 1884. The Survey of Western Palestine: The Fauna and Flora of Palestine, XXII+455 pp. London, UK. Welcomme, R.L., 1988. International introductions of inland aquatic species. FAO ®sheries technical paper 294. Rome. 318 pp. Valenciennes, A., 1835. In 1828±1849. Histoire naturelle des Poissons (22 vols), eds G. Cuvier, A. Valenciennes, Vol. 10, XXIV+482 pp.+pls, pp. 280±306. Paris, France. Valenciennes, A., 1842. In 1828±1849. Histoire naturelle des Poissons (22 vols), eds G. Cuvier, A. Valenciennes, Vol. 16, XXIII+472 pp.+pls, pp. 456±486. Paris, France. Valenciennes, A., 1844. In 1828±1849. Histoire naturelle des Poissons (22 vols), eds G. Cuvier, A. Valenciennes, Vol. 17, XX+497 pp.+pls, pp. 487±519. Paris, France. Walbaum, J.J., 1792. Petri Artedi sueci genera Piscium in quibus systema totum ichthyologiae proponitur cum classibus, ordinibus, generum characteribus, specierum di€erentiis, observationibus plurimis. Ichthyologiae Pars III. Grypeswaldiae, [ed. II], 723 pp., 3 pl.