Another anuran, the Israel painted frog Discoglossus nigriventer, which belongs to the Discoglossidae, was an endemic species once found in northern Israel that became extinct in the 1950s. Tristram (1884) described another toad species from Israel Bufo regularis that was found in the “wild areas of Judea, south of Beersheba”. This vague description was not treated seriously in later publications (e.g. Flower 1993), and Mendelssohn & Steinitz (1944) note that with the exception of one site (which is not in Israel but in Petra in Jordan) they cannot confirm the presence of this species in Israel.
The distribution area of most amphibian species in Israel is broad and digresses from the borders of Israel. Nevertheless, populations in Israel usually belong to subspecies whose distribution area is limited to the Levant. The spotted salamander’s distribution area for example, extends over all of Europe except for Britain, but in Israel and Lebanon the subspecies S. s. infraimmaculata is found. The distribution area of the banded newt extends up to Russia, but in Israel, Lebanon, Syria and southern Anatolia the subspecies T. v. vittatus is found. Similarly the Syrian spadefoot toad ranges over Asia Minor and Iran, Greece and its islands, Romania, Albania, Yugoslavia, Bulgaria and southern Russia but the subspecies found in Israel, Syria and Lebanon is P. s. syriacus, which is morphologically different from the other 3 subspecies described. Israel is the southernmost limit of the banded newt, the spotted salamander, the tree frog and the Syrian spadefoot toad.
The taxonomic status of some of the amphibian species needs further clarification. The levantine frog was once classified as Rana ridibunda pallas and the tree frog as Hyla arborea. With regard to the tree frog the possibility of another tree frog species in Israel, differentiated from the common species morphologically and in the oscillogram of its courtship song, has been suggested (Grach 1998). Future taxonomic studies will probably clarify the identity of certain populations and will possibly change the status of some of these species and subspecies.
Most amphibians have a typical two-stage life cycle, during which the adults migrate to water bodies during the reproductive season, spawn or bear live tadpoles and return to their terrestrial habitats (Dodd & Cade 1997). Thus in order to characterize the amphibian habitat we must relate to the two life styles that are characteristic of this taxonomic group – the tadpole and the adult. This fact is very significant when considering conservation measures for amphibians, since damage to any one habitat, terrestrial or aquatic, can interrupt the two-stage life cycle, and consequently amphibian populations. The aquatic habitat is particularly sensitive since the reproductive process and the tadpole stage in Israeli amphibians, as in most amphibians, is totally aquatic.
Fertilization in urodeles is internal – the female takes up the spermatophore into her cloaca – whereas in anurans it is external. One urodel species, the spotted salamander, is viviparous, while the other species are oviparous and lay solitary eggs (banded newt), egg clusters (tree frog and Levantine frog) or egg strings (green toad and Syrian spadefoot toad). The characteristics of the aquatic and terrestrial habitats of the six Israeli amphibian species appear in table 1.
The character of aquatic habitats varies from species to species. The Syrian spadefoot toad for example is limited to temporary winter pool only. Its long larval stage (three months at least) exposes tadpoles to the danger of the pool drying up early, which can lead to the death of all the tadpoles in the pool that year. In the green toad and tree frog, which are not limited to one type of water body, and whose larval stage is relatively short (three weeks to a month), it is less common for entire tadpole populations to die. The Levantine frog that reproduces only in mid-spring (May) is limited principally to permanent water bodies or winter pools that contain water until mid-summer.
The terrestrial habitat too is sensitive to changes, particularly for species that tend to return to the same site for the dry season. Terrestrial habitat preservation is problematic and differs from species to species, since unlike the close connection between tadpoles and the aquatic habitat – the degree of association between adults to water sources outside the reproductive season varies from species to species. Information on the location and character of the terrestrial habitat of various Israeli amphibians is limited. Adults of the Levantine frog are known to be closely associated with water sources, and stay in their vicinity during the dry season as well. Unlike them, the link between adult spotted salamanders and water sources varies in different populations. The Tel Dan population is active near rivulets almost throughout the year, whereas the adults in the Galilee and Carmel populations move away from water sources and enter caves and crevices in the ground where they spend the dry season (Degani & Warburg 1978). Other amphibian adults demonstrate an even less of an attachment to water bodies. Tree frog adults move away from water sources at the end of the reproductive season, go into plant thickets, climb on shrubs and low trees and remain active during the day and at night. Adult green toads remain active through the summer but limit activity to cool, humid nights. The information on summering sites of adult Syrian spadefoot toads and banded newts is even scantier. As far as we know they spend the summer deep in the ground in aestivation until the following rainy season.
The dissociation from water sources during the dry season is an important consideration in the conservation of many amphibian species in Israel and the world, since at the beginning of the rainy season we witness massive migration of adults to breeding sites (e.g.: Ewert 1969, Harrison et al. 1983, Sinsch 1987). Some of the species (e.g. Syrian spadefoot toad) migrate each year to habitual breeding sites, while other species (e.g. green toad) apparently assemble in randomly at suitable sites. Studies in Europe and the United States show that most adult mortality occurs during this migration (Honegger 1981, Endel 1987), and that vehicular traffic at a density of 25-40 vehicles per hour on a road crossing the migration route is sufficient to kill 50% of the migrating animals (Kuhn 1987). The phenomenon of breeding-site fidelity is very significant in nature conservation. Studies conducted on species showing breeding-site fidelity in Europe (Heusser 1969, Honegger 1981) showed that following destruction of the aquatic habitat, adults returned to the destroyed habitat for several years and avoided populating alternative habitats in the vicinity. Aquatic habitat destruction thus led to the elimination of the entire population.
Table 1. The terrestrial and aquatic habitats of amphibians in Israel
||Summer: deep soil crevices.
Winter: around water sources.
|Springs, winter pools, flowing streams|
||Summer: cracks in soil.
Winter: Under rocks in the breeding site area.
|Winter pools, spring water-collecting pools, slow-flowing river tributaries.|
||Juveniles (sexually immature) migrate to winter pools.
||Adults are in and around permanent water bodies, pools, reservoirs, springs and streams; tadpoles are in the water.|
||Summer: irrigated fields and gardens.
Winter: shallow burrows under rocks in the breeding site vicinity.
|Winter pools, reservoirs and permanent pools.|
|Syrian Spadefoot Toad
||Summer: deep in the ground.
Winter: relatively shallow burrows in the breeding site vicinity.
||Summer: on trees and bushes including sites far from water sources.
Winter: in vegetation thickets and under rocks in the vicinity of water sources.
|Winter pools, reservoirs, pools and springs.|
The habitat’s geographical location is of major importance in Israel, with its climatic gradient that extends from extreme desert climate in the south to humid Mediterranean in the north. This significance is even more emphasized in light of the fact that Israel is the southern limit of the distribution of four of the amphibian species found in the country. As a result of the climatic gradient, water bodies are commoner in northern Israel than in the southern part of the country. The lifespan of winter pools is correspondingly longer in the north than on the Coastal Plain or the south.
On the other hand, due to lower temperatures in the north, breeding begins later in northern populations than in southern populations of the same species, which significantly shortens the period juveniles pass in dryness from the completion of metamorphosis until the start of the next rainy season. For example, in the central Coastal Plain, the dry post-metamorphic period for Syrian spadefoot toad juveniles from metamorphosis (end of March) to the first winter rain (end of October) is about 7 months as opposed to two-three months in the Upper Galilee (August-September to late October; Gafny 1986, Geffen et al. 1987). Studies have shown that the first post-metamorphic dry season is critical for juvenile survival and attaining maturity and that juvenile mortality is very high at this time (Blair 1953, Scorgie 1980).
Therefore, in the north, there is a greater probability that species whose larval development stage is long (Syrian spadefoot toad, Levantine frog) will complete metamorphosis successfully. Similarly, as a result of their long development, juvenile body size at the end of metamorphosis in northern Israel is larger (e.g. average weight of post metamorphic Syrian spadefoot toad juveniles from Sasa is 7.5 grams as opposed to 2-3 grams in the central Coastal Plain; Gafny 1986). This increases the probability they will survive their first dry season (Newman 1992).
C. The Status of Amphibians in Israel
The number of reports on the drastic decrease of amphibian populations throughout the world has increased during the past two decades (e.g. Phillips 1990, Bishop & Petit 1991, Wake 1991). This decrease has been ascribed to various factors such as global climate changes (Herman & Scott 1991), the rise in ultraviolet radiation (Blaustein et al. 1995), disease (Worthylake & Hovingh 1989, Blaustein et al. 1994, Halliday 1998), habitat destruction (e.g. Johnson 1991, Young 1990) and habitat pollution (Beebee et al. 1990). Many researchers believe that there is no single cause for the deterioration in the global amphibian population but a synergistic combination of many factors (e.g. Wake 1991).
The populations of some Israeli amphibians have also deteriorated drastically during the past twenty years. As described in other parts of the world, population estimates are not based on adult population estimates since this is a hard parameter to measure: different species have different “catchability” (secretive species vs. easily trapped species). Also, their activity pattern (limited to specific nights) does not necessarily objectively reflect the true status of the population (Holmen & Honegger 1981, Wederkinch 1988). Therefore amphibian species status is customarily assessed according to tadpole populations, which is the method chosen to assess the status of amphibian populations in Israel. Nevertheless it should be noted that in species with particularly large clutches (e.g. up to 20,000 eggs in a clutch in the Syrian spadefoot toad in Israel – Gafny 1986), and high hatching success (over 95% in the Syrian spadefoot toad – Gafny 1986) large tadpole populations do not necessarily indicate large, healthy adult populations. In many cases tadpoles cannot complete metamorphosis due to premature drying up of winter pools. Even when the first stage is successful there is still significant mortality during the first dry season in the post-metamorphic juvenile’s life. The opposite situation, on the other hand, is unfeasible, and small, restricted tadpole populations will always be an expression of small adult populations (Wassersug 1991). This means that amphibian population status estimates based on tadpole population size will always be conservative (biased downwards).
Survey results from aquatic habitats in Israel during the last five years (1996-2001) indicate a drastic reduction in the number of populations of most species, including those considered very common in the past (e.g. green toad and tree frog). The current status of Israeli amphibians is presented in the table below. One species, the Israel painted frog, which was endemic to Israel, became extinct following the drainage of the Hula lake in the 1950s, although the small number of specimens found before that, testify to the fact that even before the drainage existing populations were apparently relictual. The populations of two species, Syrian spadefoot toad and banded newt are critically endangered. Another species, tree frog, has been categorized as vulnerable. Only one species, Levantine frog, that is very adaptable to man made water sources (reservoirs, fishponds and even sewage ponds) is in relatively less danger.
D. Disturbance and threat factors in Israel
1. Habitat destruction
Habitat loss and destruction is undoubtedly the major factor contributing to the decline of the amphibian population in Israel (Gafny & Gasith unpubl.) and in the world (e.g. Honegger 1981, Johnson 1991). In many cases this loss has affected the populations so severely that their numbers decreased to below the recovery line, and steps to stop habitat deterioration did not prevent population decline (Johnson 1991, Orchard 1991). Monitoring terrestrial habitat deterioration is even more difficult than aquatic habitat monitoring for reasons listed above (Dodd & Cade 1997).
2. Genetic isolation of populations resulting from habitat fragmentation
Anthropogenic land use elements such as roads, highways, railroads, urban areas and intensively cultivated fields can be impassible to amphibians causing habitat fragmentation. Roads and railroad tracks in Europe were found to reduce the minimal distance necessary for gene exchange between amphibian populations from 10 km in open areas with no roads to 3-4 km in open areas with roads (Reh & Seitz 1990). Moreover, most amphibian species are very sensitive to habitat fragmentation and they develop genetically isolated populations within shorter time periods than other taxonomic groups (12 generations – Reh & Seitz 1990; up to 20 generations – Driscoll 1998, 1999). Despite this short period direct harm to populations from anthropogenic factors can eliminate local amphibian populations before genetic differences develop between fragmented populations (Gibbs 1998).
Amphibian species with small local populations (less than 100 adults per breeding site) are more prone to genetic isolation than species with large local populations (Reh & Seitz 1990, Driscoll 1999). Small populations show a high level of genetic drift, which leads to loss of variability, loss of heterozygosity and fixation of random mutations (Driscoll 1999). This process will eventually lead to deterioration and extinction (Lynch et al. 1995). Among Israeli amphibians small local populations characterize the Syrian spadefoot toad (Gafny 1986) and the spotted salamander (Degani & Warburg 1978), while the green toad and tree frog have relatively large local populations. It would therefore be expected that the first two species would be more sensitive to genetic isolation of populations and their distribution in Israel is indeed disjunct.
The Syrian spadefoot toad has three regional population concentrations that are disjunct: on the central Coastal Plain, the Upper Galilee and the Golan Heights (Gafny 1986). No study has as yet been performed to examine genetic differences between the subpopulations within a region relative to differences between subpopulations from different regions of the spadefoot toad’s distribution area. In the Galilee and the Golan however, aquatic habitats are relatively close to each other (average aerial distances of 2.5 km in the Galilee and 5.2 km in the Golan), so that gene exchange between local subpopulations (within the region) is almost certainly possible. In the central Coastal Plain, on the other hand, habitat destruction and proliferation of roads and urban areas create large distances between local populations (average aerial distance of 20 km). As a result gene exchange between local subpopulations in this area is probably not possible. This aspect is very significant for efforts to rehabilitate this species, and requires preliminary genetic research.
The spotted salamander has three regional population concentrations: in the Carmel, Galilee and Tel Dan, which are apparently isolated from each other. However, studies conducted by Degani and Warburg (Degani & Warburg 1978, Degani 1986, Degani et al. 1999) suggest that within these regions the local subpopulations are not isolated. Degani et al. (1999) report genetic differences between the Tel Dan population and the Carmel and Galilee salamander populations, but explain these differences by habitat differences and not population isolation.
The Levantine frog is the only amphibian species relatively resistant to pollution, and it can be found even in rather polluted environments such as rivers and effluent pools. The remaining species are apparently sensitive to pollution although there are no studies that deal specifically with the affect of pollution on amphibian species in Israel. Studies from other parts of the world indicate that habitat pollution, whether it be limited, diffuse or resulting from pesticide spraying, has a deleterious effect, particularly during the aquatic state in the amphibian life cycle (e.g. Berrill et al. 1993). Mendelssohn & Degani (1984) report serious harm to the banded newt in Israel as a result of environmental pollution and pesticide spraying. They estimate that pollution reduced the Israeli newt population during the early 1980s to only 5% of the population in the 1950s.
4. Collection and trade
There are no reports of massive amphibian collecting in Israel for commercial purposes, although local amphibians (particularly green toads and Levantine frogs) are still used for studying amphibian anatomy at universities and schools in Israel. Amphibian collecting by amateurs is illegal, but although in recent years the Israel Nature and National Parks Protection Authority has intensified enforcement there are still reports of enthusiasts collecting amphibians for keeping as pets.
5. Species introduction
Introduction of exotic species is a real threat to local amphibian populations. Introduction mechanisms can be classified as two types:
a. Introduction for commercial purposes - in the past there were reports of attempts at growing bullfrogs Rana catesbiana, northern leopard frog Rana pipiens and African clawed frog Xenopus laevis commercially in Israel (Gorevitz 1989). Commercial breeding - characteristically includes housing very large quantities of animals in sheds or greenhouses, where they can easily escape into nature, even when precautionary measures are taken. Another problem is the possibility the breeding farm being abandoned due to economic failure (to the best of our knowledge the chance of economic success of commercial captive breeding of amphibians in Israel is minimal). The bullfrog Rana catesbiana is a large, efficient predator that feeds on small rodents and passerines. Wherever this species was introduced for growing, feral populations became established in nature and forced out local amphibian species (Moyle 1973, Orchard 1991). The African clawed frog Xenopus laevis is known to be a species that easily populates new habitats, even in areas far from its natural distribution area (South Africa). Feral populations populated water bodies in California after having escaped from breeding farms. In its natural distribution area the African clawed frog is known to cause extensive damage to fishponds and also as the carrier of many parasites (e.g. Tinsley & Sweetings 1974), and there is danger of infection spreading to local amphibian populations. The northern leopard frog Rana pipiens is known to hybridize with other Ranidae in its natural distribution area and can pose a genetic pollution threat to natural populations of Levantine frogs in Israel.
b. Introduction of animals imported into Israel as pets – exotic amphibians are brought into Israel to be sold commercially as pets both legally and illegally. Since these species are usually imported in small quantities the danger of massive escape of a large population is relatively small and the dangers of rapid introduction of this species into nature likewise small. Nevertheless accumulation of individuals released into nature might in time lead to the establishment of exotic species, which would negatively affect local species populations.
E. Recommendations for conservation
» Protection of remaining natural habitats (rain-pools, ponds, etc.) and action to have them declared nature reserves.
» Amphibian protection should not be limited to aquatic habitats but should include a broad buffer zone to preserve the terrestrial habitat. The width of the buffer zone should be determined according to the biological needs of specific species. For such a buffer zone to be effective more knowledge relating to terrestrial dwelling sites must be obtained (Dodd & Cade 1997).
» Alternative man-made habitats should be dug in nature reserves and populated with eggs or tadpoles of endangered species (Syrian spadefoot toad, banded newt, spotted salamander). Tadpoles should preferably be collected from endangered habitats with little or no chance of rescue, although due to the high mortality of tadpoles until metamorphosis, and since some of the mortality is density dependent, collection of a limited number of tadpoles from existing populations should not affect them significantly.
» Captive breeding nuclei should be established to allow repopulation of artificial habitats as noted above.
» Genetic research on endangered populations should be performed in order to clarify the degree of population isolation and the possibility of populating artificial habitats with populations originating in another distribution area, without harming the local population and reducing genetic diversity (e.g. is it possible to populate artificial pools in the Coastal Plain with spadefoot tadpoles from the Golan?).
» Absolutely prohibit introduction of exotic amphibian species whether for commercial breeding or as pets.
» Intensify enforcement to prevent amphibian collection for commercial purposes or individual breeding.