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ISRAEL JOURNAL OF ZOOLOGY, Vol. 48, 2002, pp. 351Ð357

NOTE: GLOBAL WARMING AND RECENT CHANGES IN ISRAEL’S AVIFAUNA

OHAD HATZOFEa AND YORAM YOM-TOVb,* aDivision of Science and Conservation, Israel Nature and Parks Authority, 3 Am Ve’Olamo Street, Jerusalem 95463, Israel bDepartment of Zoology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv 69978, Israel

Global mean surface temperatures have increased by 0.6 ¼C since the late 19th century (IPCC, 1995). In Israel, average minimum summer temperatures increased by an aver- age of 0.26 ¼C per decade during the second half of the 20th century (Ben-Gai et al., 1999). Global warming may affect the physiology, distribution, phenology, and adapta- tion of plants and animals (for review, see Hughes, 2000). For example, animals whose distribution is limited by cold temperatures may extend their range to higher latitudes when areas beyond their present range become warmer. The aim of this note is to examine the hypothesis that global warming is partly responsible for the establishment of several bird species new to Israel, and for the extended breeding ranges of others. If so, we suggest that species originating from the tropics are more likely to become established in Israel, or to extend their breeding range there. Since its establishment in 1948, Israel has gone through tremendous changes: The human population has increased by about tenfold, the standard of living has risen considerably, and patterns of land use and agricultural practices have seen dramatic alteration. These and other changes have affected the distribution and abundance of Israel’s wildlife (Yom-Tov and Mendelssohn, 1988; Mendelssohn and Yom-Tov, 1999). While populations of many species decreased in size, several species benefited from the above changes and their populations increased. The first comprehensive report on the distribution and breeding range of the birds of Israel appeared about forty years ago (Merom, 1960), and forms the basis for this note. We assumed that species of tropical origin are more likely to spread than those of northern origin, and categorized all species into one of three categories according to origin: tropical, northern (Palearctic and Holarctic), and wide range (occurring in both tropical and Palearctic regions or cosmo- politan) in order to test this assumption.

ESTABLISHMENT OF NEW SPECIES Several species of birds new to Israel started to breed in Israel during the study period (1960Ð2002). Some species appear to have arrived independently, while others appear to have been introduced, either intentionally or unintentionally, by man. In some cases it is difficult to know to which group a species belongs. The species can be divided into three categories:

*Author to whom correspondence should be addressed. E-mail: [email protected] Accepted March 2003. 352 O. HATZOFE AND Y. YOM-TOV Isr. J. Zool.

SPECIES REACHING ISRAEL INDEPENDENTLY The buzzard (Buteo buteo) is a common Palearctic passage migrant and wintering species in Israel. The first nest of this species was found in the northern Golan in 1991, and the breeding population has spread to the Upper Galilee. At present at least seven breeding pairs are known. The striated (Butroides striatus) is a tropical species whose breeding record closest to Israel was in southern Sinai (Shirihai, 1996); it bred for the first time in Elat in 2002 (Yosef et al., 2002). The central African black bush robin (Cercotrichas podobe) was first observed in the southern Arava Valley in 1981 (Eames, 1986), and became a rare spring and summer visitor (Shirihai, 1996). It apparently started to breed in this region during the 1990s. The Indian silverbill (Euodice malabarica) appeared during the 1980s and quickly spread along the Arava and Jordan valleys from Elat to the Sea of Galilee. Flocks of hundreds are seen in these areas as well as in the Negev and even in the Mediterranean region. The Namaqua dove (Oena capensis), an African species, was first collected in 1961 in the northwestern Negev, and since then became established in the Arava and Jordan valleys. The first recorded breeding was reported in 1986 (Mindell, 1986/7). This species lives in the vicinity of cultivated areas. The golden oriole (Oriolus oriolus) is a common passage migrant in Israel, but since 1980 two to five pairs have bred annually in the Hula Nature Reserve in the Galilee (Shirihai, 1996). The purple gallinule (Porphyrio porphyrio), an African species also breeding in the Caspian Sea area and Turkey, is an occasional visitor to Israel. The first apparent breeding record is of an adult accompanied by a chick, seen near Yeruham Lake in the central Negev in summer 2002. Liechtenstein’s (Pterocles lichtensteinii) is a SaharoÐSindian desert species that became an established breeder in the Negev Desert several decades ago, mainly in the Elat area. Its establishment in Israel has been attributed to the availability of new drinking resources and agricultural fields (Shirihai, 1996).

SPECIES THAT ACCOMPANY MAN, BUT WITH NO DIRECT EVIDENCE OF INTRODUCTION The ring-necked parakeet (Psittacula krameri) apparently spread naturally from Egypt, where it was introduced from India, although there is a possibility that the Israeli population originated from escaped or released pets during the 1960s (Dvir, 1988). It started breeding during the 1980s, and is now very common in the coastal plain and northern valleys, as well as along the Jordan Valley. Roosts of thousands are located along the coastal plain and other areas. There are reports that the local population of the ring-necked parakeet includes some moustached parakeets (Psittacula alexandri), a southeastern Asia species that has been observed in the Bet Shean Valley (Trevor Ellery, pers. comm. 2001). The Indian house (Corvus splendens) first appeared in Elat in 1976 (Paz, 1987) Vol. 48, 2002 GLOBAL WARMING AND CHANGES IN AVIFAUNA 353 where about 300 individuals are living presently, and is occasionally seen north of Elat along the Arava Valley.

SPECIES INTRODUCED BY MAN The black-hooded parakeet (Nandayus nenday), a South American bird, appeared during the 1970s in Emek Hefer and south of the Carmel Mountains, where it became an established breeder during the 1990s (Arieh Keller, pers. comm.). The (Myiopsitta monachus) is another South American species that established itself in Israel during the 1990s, and breeds in the Tel Aviv area, where flocks of more than a hundred birds have been observed (Asaf Meiroz, pers. comm.). Several species of , mynas, and at least one weaver were apparently intro- duced by the owners of a bird park situated near the Yarkon River in Tel Aviv. These include the superb (Spreo superbus), an East African species, and the African glossy starling (Lamprotornis spp), as well as southeastern Asia species such as the black-collared starling (Sturnus nigricollis), the (Acrodotheres tristis), the vinous-breasted starling (Sturnus burmannicus), and the East African masked weaver (Ploceus velatus). Careless handling and possibly intentional and unlawful release are responsible for these introductions. As might be expected from adaptable species, the common myna is now well established in many parts of Israel, including the Mediterranean coastal plain and along the Dead Sea, while the other species are still largely restricted to the Tel Aviv area. The same bird park is apparently responsible for the introduction of the Bahama pintail (Anas bahamensis) that is occasionally seen in the Tel Aviv area, where single pairs try to breed. The Egyptian (Alopochen aegyptiacus) is another escapee from zoos (apparently mainly from the Tel AvivÐRamat Gan Safari park) that started to breed in the Tel Aviv area in 1978 (Shirihai, 1996). The (Phalacrocorax carbo) breeds in the Jerusalem Biblical Zoo and in the Ramat GanÐTel Aviv Zoological center, and several individuals that hatched there were re- leased and have started to breed within the zoo confines, but never outside it. None of the species introduced by man are included in this analysis.

EXTENSION OF BREEDING RANGE During the study period, many species of birds expanded their range within Israel (Mendelssohn and Yom-Tov, 1999; Table 1). The reasons assumed for these range expansions are numerous, and in some cases more than one factor has affected a species. Most of the species that extended their breeding range were affected by habitat change, gardening, creation of water reservoirs, and fishponds, as well as changes in agricultural practices, especially, increased areas of irrigation. Mendelssohn and Yom-Tov (1999) noted 28 species of birds whose breeding range has increased since the establishment of the State of Israel. These include birds preferring a forest-like habitat, such as the great (Parus major), blackbird (Turdus merula), Syrian (Dendroscopus syriacus), and sparrowhawk (Accipiter nisus); birds that inhabit wetlands, such as the night heron (Nyctycorax nyctycorax), little (Egretta garzetta), little 354 O. HATZOFE AND Y. YOM-TOV Isr. J. Zool.

Table 1 Species that extended their breeding range within Israel during the last 50 years. Assumed causes for the range extension are mostly from Mendelssohn and Yom-Tov (1999), with some of our additions (OH and YYT). The list is organized by taxonomic order and species within each order Assumed causes for range extension Order World Habitat Garbage and Fishponds Species distribution changea other foodb and water reservoirsc Podicipitiformes Tachybaptus ruficollis W+

Pelecaniformes Phalacrocorax pygmaeus N+

Ciconiiformes Ardeola ralloides T ++ Bubulcus W ++ Egretta garzetta T ++ Nycticorax nycticorax W + Plegadis falcinellus T +

Anseriformes Anas platyrhynchos N +

Accipitiformes Accipiter nisus N+ Falco subbuteo N+

Charadriiformes Himantopus himantopus W+ Vanellus spinosus T+

Columbiformes Columba livia W+ Streptopelia decaocto T+ Streptopelia senegalensis T+

Strigiformes Asio otus N++ Otus scops N+

Coraciiformes Ceryle rudis T+ Merops orientalis T+

Piciformes Dendroscopus syriacus N+ continues next page Vol. 48, 2002 GLOBAL WARMING AND CHANGES IN AVIFAUNA 355

Table 1 continued Assumed causes for range extension Order World Habitat Garbage and Fishponds Species distribution changea other foodb and water reservoirsc Passeriformes Corvus corone N++ Corvus corax N+ Corvus monedula N+ Corvus ruficollis T++ Delichon urbica N+ Garrulus glandarius N+ Hirundo daurica T+ Hirundo rustica N+ Nectarinia osea T+ Onychognathus tristrami T+ Parus major N+ Passer domesticus W++ Pycnonotus barbatus T+ Troglodytes troglodytes N+ Turdus merula N+ N—Holarctic or Palearctic, T—tropical, W—wide distribution in both tropical and northern regions. aIncreased gardening, irrigation, afforestation, availability of drinking and breeding sites, and changes in agricultural practices. bIncreased availability of garbage and other food. cIncreased areas of fishponds and water reservoirs.

(Tachybaptus ruficollis), stilt (Himantopus himantopus), and spur-winged (Vanellus spinosus); and commensal species such as the house sparrow (Passer domesticus), (Columba livia), (Corvus corone), jackdaw (Cor- vus monedula), and others. Additional details can be found in Mendelssohn and Yom- Tov (1999). Since the publication of Mendelssohn and Yom-Tov’s (1999) paper, it has become apparent that several more species have recently started to breed in Israel. The sparrowhawk (Accipiter nisus) was known as a rare local breeder in northern Israel (Hardy, 1946, quoted by Shirihai, 1996), but since the 1980s is known to breed in the Carmel, Ramot Menashe, and even in the Shefela area (Frumkin and Adar, 1989). The pale (Carpospiza brachydactyla) was known to breed on Mount Hermon but is now also breeding in eastern Samaria south of Mt. Amasa (Griffin et al., 2001). The raven (Corvus corax) used to breed only in the Mediterranean region, but since the early 1980s breeding pairs have appeared in many wadis in the Judean and Negev deserts as far south as Mitzpe Ramon. The hobby (Falco subbuteo) has extended its breeding range to the northern Negev, apparently due to availability of nesting sites in hooded ’ nests. Tristram’s grackle (Onychognathus tristramii) breeds regularly in 356 O. HATZOFE AND Y. YOM-TOV Isr. J. Zool. desert oases in the lower Jordan and along the Arava valleys, extended its breeding range west to Arad and Beer Sheva. The pigmy cormorant (Phalacrocorax pygmeus) used to breed in the Hula Valley, but was decimated during the 1960s. During the 1990s the local population increased and it now also breeds in the Bet Shean and the Jordan valleys. The (Troglodytes troglodytes) breeds regularly in forests in northern Israel and started to breed in the Judean Hills near and in Jerusalem during the 1980s (Shirihai, 1996), apparently due to the availability of suitable nesting sites. According to our categorization of origin, we note that of the eight species arriving in Israel independently, six are tropical and two have a northern distribution. The three species that accompany man, but for which there is no direct evidence that they were introduced, are of tropical origin. All the species known to be introduced by man are of tropical origin, but we did not include them in this analysis because, as far as we know, no Palearctic species have been introduced by man into Israel and thus could serve as a control. Of the 35 species that have expanded their breeding range within Israel (Table 1), 6 (17.1%) have a wide distribution, 16 (45.7%) are Palearctic or Holarctic, and 13 (37.1%) are tropical. Using data on the origin of Israeli birds (Yom-Tov, 1988), we similarly categorized all 160 bird species breeding in Israel in 1988: 15 (9.4%) have a wide distribution, 120 (75.0%) are Holarctic or Palearctic, and 25 (15.6%) are tropical. The percent frequencies of the Palearctic and tropical groups differ significantly from each other (chi-square = 16.3, p = 0.0001), indicating that birds of tropical origin are significantly more likely to have extended their range than birds of northern distribution. The above results show that during the study period birds of tropical origin were significantly more likely to become established breeders in Israel, and those breeding already were more likely to extend their breeding range there, than birds of northern distribution. Hence, these data support our hypothesis that global warming is at least partly responsible for these phenomena, although other factors, such as changes in agricultural practices and habitat change, also contribute or may even be the primary causes. It is also possible that tropical birds are quicker to take advantage of the many habitat changes that occurred in Israel than birds of northern origin, but we have no evidence for this.

ACKNOWLEDGMENTS We are grateful to Trevor Ellery, Arieh Keller, Asaf Meiroz, and Yoav Perlman for information, David Winkler and an anonymous referee for their comments on the manuscript, and to Naomi Paz for editorial comments. This work was supported by the Israel Cohen Chair for Environmental Zoology to YYT.

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