Biological Conservation 147 (2012) 13–21

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Biological Conservation

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Israel’s breeding avifauna: A century of dramatic change ⇑ Yoram Yom-Tov a, , Ohad Hatzofe b, Eli Geffen a a Department of Zoology, Tel Aviv University, Tel Aviv 69978, Israel b Israel Nature and Parks Authority, Am Veolamo 3, Giva’at Shaul 95463, Jerusalem, Israel article info abstract

Article history: During the course of the 20th century many changes took place in the area encompassing Israel and the Received 25 July 2011 Palestinian Authority (hereafter Israel; ca. 28,000 km2): the human population grew from ca. 650,000 Received in revised form 3 January 2012 inhabitants during 1900–1903 (Rupin, 1920) to ca. 10 million in 2008, i.e. a 16-fold increase. This popu- Accepted 5 January 2012 lation increase was accompanied by an increase in land use for human needs – agriculture, aquaculture, Available online 7 February 2012 forestry, construction of buildings and roads, etc., and a dramatic rise in the standard of living. Here we compare the status (distribution and abundance) of the 227 bird species that are breeding or Keywords: have bred in Israel from the beginning of the 20th century to the present day. For each species we doc- Avifauna umented the environmental factors presumed to have affected it, and examined the effects of taxonomic Israel Habitat change order, body mass, diet, world and local distribution and nest location on the status of the avifauna. We Poisoning found that 73.6% of the bird species breeding in Israel had undergone a change in their status during Invasive species the studied period. While several of the examined factors were significantly related to the observed changes, some of them were also interrelated to some degree, making it difficult to single out the factor responsible for a particular change. The main reasons for the changes were nonetheless assessed as hab- itat change, introduction of invasive species and poisoning. Habitat change had many forms, most of which are related to agriculture, including irrigation, aquaculture and construction of water reservoirs; but also included afforestation, preservation of the natural forest, urbanization, gardening and the intro- duction of exotic plants. Habitat change was responsible for a population decline in 64 species and pop- ulation increase in 62 species. Thirteen species, mostly , were impacted by poisoning. Sixteen invasive species, all of tropical origin, were introduced, of which seven were Psittaciformes. Although changes occurred throughout the country, the birds inhabiting the Mediterranean region were more affected than those inhabiting the desert region, reflecting the denser human population in the for- mer region. Ó 2012 Elsevier Ltd. All rights reserved.

1. Introduction due to human activity is the most important cause of these de- clines, followed by hunting and invasive alien species. Habitat It is widely accepted that the world’s avifauna, like many other destruction and degradation as a consequence of agriculture is animals, is in the midst of a serious crisis that is altering the status the greatest threat (Green et al., 2005; Butchart et al., 2010). Agri- of a large proportion of this fauna. In their recent review, Butchart culture is the prime cause of habitat loss worldwide and the area et al. (2010) provide a summary of the present status of the world’s currently occupied by agriculture comprises 11% of total land cover birds and the most important pressures they face today. They show (FAO, 2007). that since 1988 there has been a steady and continuing deteriora- The effects of the above crisis have not been evenly distributed tion in the status of the world’s birds, and many birds in terrestrial, with some countries having been impacted more than others. Hu- freshwater and marine ecosystems have declined in status over the mid tropical countries have been the most affected, mainly due to last 20 years. This is particularly true in the tropics, but the spread forest loss, which has been followed by catastrophic extinctions and intensification of agriculture in temperate regions has had a (Butchart et al., 2010). In Singapore, for example, local extinctions similar effect (Hoffman, 2011; Perry et al., 2011). Nearly half of were found among a wide range of terrestrial and freshwater taxa, the bird species worldwide show a declining population, 132 and substantial rates of extinctions occurred among forest special- (about 1.3%) species have become extinct since 1600, 44% are sta- ists, with the greatest proportion of extinct taxa (34–87%) being in ble and 7% are increasing (Butchart et al., 2010). Habitat change butterflies, fish, birds and mammals (Brook et al., 2003). However, changes in the status of birds have not been confined to the tropics ⇑ Corresponding author. Tel.: +972 36409058; fax: +972 3 6409403. but have also occurred in major temperate regions. For example, E-mail address: [email protected] (Y. Yom-Tov). many farmland species declined in Europe due to changes in their

0006-3207/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2012.01.005 14 Y. Yom-Tov et al. / Biological Conservation 147 (2012) 13–21 habitat and to global warming (Georgy et al., 2005, 2008; Ivits pools, rivers and streams) has resulted in the disappearance of et al., 2011). Dramatic population declines also occurred in North most aquatic habitats (Yom-Tov and Mendelssohn, 1988). On the America, especially in grassland and arid land habitats, and have other hand, the establishment of aquaculture (currently occupying been attributed mainly to habitat loss due to agriculture and 22 km2) and ca. 550 water reservoirs has created new wetlands urbanization (Butchart et al., 2010). Declining trends of woodland, (Yom-Tov, in press). grassland and heathland have been reported in Australia (Olsen, At the beginning of the 20th century the natural forest occupied 2008). In these areas as well as others, habitat loss is the most about 100 km2 (A. Rabinowitz, pers. comm.), and currently covers important factor impacting bird populations, with agriculture, about 350 km2 (Omi, 1978; Statistical Abstracts of Israel, 2009), drainage of wetlands, unsustainable forestry and urbanization in addition to 1020 km2 of afforested areas (Statistical Abstracts being the main causes (Stanner and Bourdeau, 1995; Vie et al., of Israel, 2010). In addition, extensive gardening in urban areas 2008; Butchart et al., 2010). Green et al. (2005) claimed that agri- as well as in agricultural settlements has added wooded areas to culture poses the greatest threat to birds worldwide. The impact of where none existed at the beginning of the 20th century. agriculture takes various forms, such as expansion of cultivated Growth of the human population, accompanied by a rise in liv- areas, aquaculture and construction of water reservoirs, drainage ing standards, has also led to a significant increase in the amount of of water bodies, increased food availability to species commensal domestic solid waste produced (more than 4.5 million tons in with humans (including bird predators) in the form of garbage 2000; Statistical Abstracts of Israel, 2007). Many small and even and surplus agricultural products, as well as poisoning. Pesticide medium-size settlements and military bases have created their residues negatively affect many birds, but deliberate poisoning to own, illegal, garbage dumps, where the waste remains largely un- prevent damage to crop and livestock is also quite common (Mine- treated. Garbage in Israel comprises about 40% organic material, au et al., 1999). and until recently this percentage had been as high as 75%, provid- Invasive alien species pose the second major threat to birds ing a readily available source of food for birds and mammals (Ost- after habitat change (Schmitz and Simberloff, 1997; Parker et al., rovsky et al., 2009). These changes (and many others) have had a 1999; Butchart et al., 2010). The success of invaders depends on major, in many cases fatal, effect on the status, distribution and the suitability of the abiotic environment for the exotic species at abundance of vertebrates in Israel. Nathan et al. (1996) have shown the introduction site (Blackburn and Duncan, 2001). Invasive alien that many of the birds inhabiting Israel are at the southern periph- species often compete and interfere with native species, and many ery of their distribution, and are more likely to stop breeding due tend to become pests (Parker et al., 1999). Several alien invaders to their inherent vulnerability to human pressure. have become established in Israel, and their number is growing Global warming has been shown to impact the distribution of (Hatzofe and Yom-Tov, 2002). animals, and many bird species have extended their ranges to The area encompassing Israel and the Palestinian Authority is the north (reviewed by Hughes, 2000; Parmesan and Yohe, 2003; small (ca. 28,000 km2), located in the eastern Mediterranean be- Root et al., 2003). Worldwide, global mean surface temperatures tween the Mediterranean Sea and the Jordan River, a region far have increased by 0.6 °C since the late 19th century (IPCC, 2007). from the tropics. It lies between latitudes 29°300N and 33°200N In Israel, average minimum summer temperatures increased by on the verge of the Saharo-Arabian desert belt, and has been inhab- an average of 0.26 °C per decade during the second half of the ited by humans for approximately one million years (Bar-Yosef and 20th century (Ben-Gai et al., 1999). Garfunkel, 2008). During the course of the 20th century many Here we document the changes in the breeding avifauna of Is- changes took place in this area: the human population grew from rael from the beginning of the 20th century to 2010. We assess ca. 650,000 inhabitants during 1900–1903 (Rupin, 1920) to ca. 10 the causes of the observed trends, compare the changes that have million in 2008 (of which 7.4 million inside Israel proper; Statisti- taken place in the desert to those in the Mediterranean areas, and cal Abstracts of Israel, 2010), i.e. a 16-fold increase in population discuss future prospect for this avifauna. Israel is a small, densely (during that period, the entire world population increased by populated country, and the changes observed in its avifauna pres- ‘‘only’’ 3.5-fold). This population increase in Israel has been accom- ent an example of what may also occur in other countries due to panied by an increased use of land by humans – for agriculture, the massive and rapid increase in the human population. forestry, urbanization, construction of buildings and roads, etc. Agricultural methods have changed dramatically since the 2. Material and methods beginning of the 20th century. The area of worked land has in- creased by about 50% to ca. 2950 km2 (Avitsur, 1977; Statistical Data on past (since the1930s) and present (2010) status of birds Abstracts of Israel, 2010), the irrigated area has increased by ca. that are known to have bred or now breed in the area of the former 135-fold, from 15 km2 at the beginning of the 20th century British Mandate of Palestine (Israel, the Palestinian Authority and (Avitsur, 1977) to ca. 2000 km2 approximately 100 years later the Israeli Golan Heights; ca. 28,000 km2) were acquired from (Statistical Abstracts of Israel, 2009). Irrigated agriculture has also the literature (Aharoni, 1923; Bodenheimer, 1932; Merom, 1960; been developed in desert areas that previously had no agriculture Smoli, 1968; Inbar, 1975–1982; Paz, 1986; Mindell, 1987; Yom- at all. For example, since 1950 about 20 settlements have been Tov and Mendelssohn, 1988; Nathan et al., 1996; Shirihai, 1996; established along the Arava Valley between the Dead Sea and the Shoham et al., 1997; Mendelssohn and Yom-Tov, 1999; Dolev and Red Sea (a stretch of 150 km) where none had existed before Pervulotzky, 2002; Hatzofe and Yom-Tov, 2002; Sapir, 2003; Alon, 1950, cultivating a total of ca. 50 km2, and thus creating desert 2010). Much of the additional data on species occurrence (including oases. Israel has a thriving, modern agriculture that uses pest con- alien invading species), dispersal of local species to new areas in trol methods. Over 400 permitted chemical compounds are listed Israel and breeding appear in the Hebrew journals, such as the in Israel for agricultural use, and available in more than a thousand nature monthly ‘‘Teva Va’aretz’’ (Nature and Land, 1958–1994) forms (Lichtanier, 2009). They include pesticides such as insecti- and the raptor journal ‘‘HaOzniya’’ (The Torgos, 1980–2005). In cides, molluscicides, rodenticides, fumigants, plant growth regula- addition, we have incorporated recent data from the data base of tors and other chemicals (Lichtanier, 2009) that may affect bird life the Nature Reserve and Parks Authority of Israel, and the Israeli directly or indirectly. Birding Website (http://www.israbirding.com (see details below). The increased demand for water for agriculture, industry and We have not included about a dozen species that have only re- direct human consumption and land for cultivation and building, cently started to appear in the study area (i.e. Erithacus rubecula at the expense of wetlands (i.e. the Hula Lake, swamps, winter and Fringilla coelebs) and either do not breed there yet, or have Y. Yom-Tov et al. / Biological Conservation 147 (2012) 13–21 15 performed or attempted only a single breeding event (e.g., Sturnus Lebanon roseus and Aquila rapax) during the study period. Most of the sources listed above do not provide quantitative data on local N breeding densities, but report on the appearance/disappearance Syria of a species at a given locale and on detected trends in species’ pop- ulation size (hereafter ‘status’). Our data file encompasses all 227 bird species that breed or have bred in Israel. The only previous attempt to quantify popula- tion size of the birds of Israel (Shirihai, 1996) was based on rough assessments by field ornithologists. However, numerical data based on field surveys and regular counts exist for only about 50 species, mostly diurnal and nocturnal raptors, water birds and whose breeding range is restricted to small areas (i.e. Mount Hermon and southern Negev), and which are regularly counted by ornithologists and rangers of the Nature Reserve and Tel Aviv Parks Authority of Israel (NPA). The present study is based on observations by about 80 field ornithologists and 30 knowledge- able rangers of the NPA who report to the Information Centre of Jerusalem the NPA, the Israel Ringing Centre and the Israeli Birding Website (http://www.israbirding.com). These data contributed sufficient material upon which to base the present analysis. However, the majority of species had never been systematically studied and Beer Sheva the data for them are not quantitative. This presented a weakness for the study, and has prevented us from carrying out a more quan- titative approach in analysis of the data. For each species we have noted its status change, if any (depen- dent variable). We used two criteria (trends in population dynam- ics and trends in size of distribution range in Israel; Nathan et al., 1996; Batten et al., 1990), to assign a species to one of the first three of the four categories defined below. These criteria are widely used in Red Data books, including in the Israeli Red Data Book (IRDB, Dolev and Pervulotzky, 2002). For example, IRDB de- fines a status by recording changes in the area used, changes in the quality of the areas used, number of sites that a species ob- served and trends in population size. A species was defined as declining or increasing if one or both of the above trends were Egypt Jordan judged to have changed during the study period (1930s to 2010). We used four categories of change for status (no change, decrease [including species that stopped breeding in the study area], in- 50 km crease or alien invader). For each species we noted several inde- pendent variables that may have been related to status change. For independent variables, we used one continuous variable, body Fig. 1. The Mediterranean (clear area) and desert (gray area) regions in Israel. mass, and six categorical variables: order, diet (herbivore, insecti- vore, predator or omnivore), nest location (ground, vegetation, concern) with NT (near threatened) into one category, and CR cliffs or holes), climatic origin (wide, temperate, desert or tropical), (critically endangered) with EN (endangered) to another. The data climatic zone in Israel (throughout the study area, Mediterranean are presented in an electronic supplement. or desert; Fig. 1), and reason for change (habitat change, introduc- tion, poisoning, unknown, no change). Climatic origin largely over- 3. Statistics laps the zoogeographical distribution of the species. Data on body mass, diet, nest location and distribution were accumulated from We used ordinal logistic regression to test the effect of categor- the literature (Cramp and Simmons, 1977–1994; Hoyo et al., ical independent variables on the direction of change (dependent 1992–2011; Dunning, 2008). Alien invading species (i.e. success- variable). Body mass (continuous) was added as a covariate. The fully established) were defined as those that were not known to direction of change was assigned 1 for decrease, 0 for no change breed in the Levant prior to their importation and release by and 1 for increase in population size. The whole model test com- man, or escape, such as several Psittaciformes. This category does pares the full (intercepts and all effects) and the reduced (only 2 not include species breeding in neighbouring countries that ex- the intercepts) models using the likelihood-ratio v test. We used panded their breeding range to include the study area during the the goodness of fit test to determine whether including additional studied period (e.g. the cattle Bubulcus ). variables or interactions would improve model fit. The likelihood- 2 Status change of each of the species in the study area (i.e. IRDB) ratio v was also used for testing the effect of each independent was compared to changes in its distribution or abundance in its variable on the direction of population change. All calculations global range. For these data we used one or more of the following were performed in JMP v9.0 (SAS Inc.). sources: BirdLife International data zone (www.birdlife.org/dataz- one), Wetland International, 2006 (mainly on water fowl) and 4. Results Delany et al., 2009 (for waders). We also compared the status we assigned to a species to that of the IRDB. IRDB uses seven status Of the 227 bird species that are breeding or once bred in the categories, which we reduced to five by combining LC (least study area only 26.4% did not undergo a change in status during 16 Y. Yom-Tov et al. / Biological Conservation 147 (2012) 13–21 the studied period. Population size and/or distribution area of Table 2 37.0% of the species declined, 29.5% increased and 7.0% of species The effect of body mass, nest location, diet, order, climatic origin and climatic zone, as well as reason for change, on change in the populations of resident bird species in were alien invaders (Table 1). The ‘‘declined’’ category includes Israel, with and without introduced species, during the past 100 years. The effects are 19 species that have stopped breeding in Israel. Passeriformes con- order by probability. Number of species is indicated in parenthesis. stituted the largest order (108 species; 47.5%). Data on the propor- Effect df Likelihood ratio v2 P tions of status change of species comparing passerines to other orders revealed that the former were less likely to show a change All species (226) Whole model 35 150.9 <0.0001 in status than all the other orders combined (Table 1). Our status Lack of fit 411 340.8 0.9951 categories (decline, increase and no change) are very closely asso- Order 19 43.2 0.0012 ciated to those of the Israel Red Data Book (regionally extinct, crit- Body mass 1 11.1 0.0008 ically endangered and endangered, vulnerable, not threatened and Climatic zone 2 27.8 <0.0001 least concern; Dolev and Pervulotzky, 2002), and status was signif- Climatic origin 3 13.5 0.0037 Reason for change 4 19.0 0.0008 icantly related to IRDB categories (logistic regression: likelihood Nest location 3 6.1 0.1066 2 ratio v4 ¼ 84:2, P < 0.0001, misclassification rate = 0.47). Diet 3 1.9 0.5932 Order, body mass, reason for change, climatic origin and cli- Native only (210) matic zone (but not nest location and diet) were significantly re- Whole model 33 116.2 <0.0001 lated to the changes that occurred in the status of birds (Table 2 Lack of fit 381 340.8 0.9314 and Figs. 2 and 3). The results remained valid after removal of Order 18 43.2 0.0008 Body mass 1 11.1 0.0008 the introduced species from the analysis (Tables 1 and 2). Below Climatic zone 2 27.8 <0.0001 we detail the changes that took place in each of the factors that Climatic origin 3 13.5 0.0037 were significantly related to changes. Reason for change 3 10.4 0.0155 Order was significantly related to status change (Table 2 and Nest location 3 6.1 0.1066 Fig. 2). The main changes occurred among eight orders (Table 1 Diet 3 1.9 0.5932 and Fig. 2). Removal of all introduced species resulted in retaining the above trend (Table 2 and Fig. 2). Body mass was significantly related to status change (Table 2), Changes occurred throughout the country (Tables 1 and 2, and heavier birds (i.e. Falconiformes, Ciconiiformes and Gruifor- Fig. 3). Most species breeding throughout Israel increased. How- mes) tended to change more than lighter ones. Removal of the ever, of the 158 species breeding only in the Mediterranean region introduced species yielded very similar results (Table 2). 70 declined and 39 species increased. In the desert region the Reason for change had a significant effect, and more so when trends were mixed and similar number of species increased or de- the introduced species were included (Table 2). The main reasons clined (Table 1). These trends remained roughly the same after for change were habitat alternation, introduction of alien invasive removing all introduced species (Table 2). species and poisoning. Habitat alteration was responsible for de- Trends of status change in Israel were only partly related to glo- crease in 64 species and increase in 62 species. As stated above, bal trends in status (logistic regression on native species only: like- 2 16 alien species were introduced, of which seven were Psittacifor- lihood ratio v3 ¼ 30:9, P < 0.0001, misclassification rate = 0.50), but mes. Thirteen species, mostly Falconiformes, were negatively af- the proportion of birds whose status changed outside Israel was fected by poisoning. smaller than in Israel (64.0% and 73.6%, respectively). The corre- spondence between the global and Israeli trends was not complete, and of the 227 species in our sample only 152 (67.5%) of the Israeli ones revealed a similar trend to that of the global trend of the same Table 1 species. Of the 85 species breeding in Israel and decreasing glob- Type of change in breeding status among 227 bird species known to breed (or have ally, 49 (58.3%) declined also in Israel, whereas 22 (25.8%) in- bred) in Israel over the last 100 years sorted by order and region. The detailed order lists only those with more than three species breeding in Israel. Most species (73.6%) creased and 14 did not change. Eleven of the species that have undergone a change in their status during the studied period. N denotes the increased in Israel dwelt in aquatic habitats, comprising three number of species. , four , two waders and two rails. Among the 47 spe- Order or group N Decline N Increase Invasive No change cies that increased globally, 29 (61.7%) increased also in Israel, (%) N (%) N (%) N (%) while six (14.9%) declined. Four of the seven species that declined All species 227 84 (37.0) 67 (29.5) 16 (7.0) 60 (26.4) were raptors, affected mainly by secondary poisoning but also by electrocution and hunting. Nine of the 16 species that were invad- By order 10 4 4 2 ers to Israel had also invaded other countries. Of the 82 species Apodiformes 4 1 3 whose global population was stable, 27 (32.9%) declined and 16 3 3 (19.5%) increased in Israel. 10 5 4 1 Climatic origin (i.e. global zones) was significantly related to Ciconiiformes 11 1 8 1 1 Columbiformes 5 2 2 1 status change (Table 2). This was due to two trends: all the intro- 7 3 4 duced alien species were from tropical zones; and 18 (of 30) other Falconiformes 24 16 5 3 species that had originated from a tropical zone increased, while 4 3 1 nine (of 27) desert species declined. Removal of all invading spe- 5 1 4 cies did not change this trend (Table 2 and Fig. 3). Lariiformes 7 4 3 Passerines 108 31 25 5 47 Several of the examined parameters are also interrelated to Psittaciformes 7 7 some degree. For example, there is a strong association between Pteroclidiformes 5 4 1 2 order and body mass (logistic regression: likelihood ratio v19 ¼ Strigiformes 9 3 3 3 2 189:1, P < 0.0001), order and diet (likelihood ratio v57 ¼ 352:4, By Region P < 0.0001), and order and climatic origin (likelihood ratio Throughout Israel 23 1 (4.3) 16 (69.6) 3 (13.0) 3 (13.0) v2 ¼ 118:5, P < 0.0001). These associations are partly due to the Mediterranean 158 70 (44.3) 39 (25.5) 11 (7.0) 38 (24.0) 57 Desert 46 13 (28.2) 12 (26.1) 2 (4.3) 19 (41.3) fact that all the Falconiformes in our sample are carnivores, and most of them are heavier than 1 kg. Body mass was significantly Y. Yom-Tov et al. / Biological Conservation 147 (2012) 13–21 17

change in Israel are significantly related to global trends in status, as far as we are aware the proportion of birds outside Israel whose a status has changed is smaller than the change in Israel (Butchart et al., 2010). Moreover, the changes in Israel do not necessarily resemble those elsewhere, and species that declined in Israel may have increased elsewhere (This study; BirdLife International data zone; Wetland International, 2006; Delany et al., 2009), as ex- pected by the higher rate of human population growth in Israel than in many other places worldwide (see above) and vice versa, showing that change in a species status is largely a local affair. As far as we are aware, the changes in Israel have been more pro- nounced than reported for other countries located in temperate re- gions of the world. Several factors are responsible for this major change, the most important of which is habitat alteration, which has affected 126 species (62 increased while 64 declined, including 19 that stopped breeding) of the 166 species that changed their distribution or abundance during the study period. Most other examined parame- ters (i.e. systematic order, body mass, climatic origin and zone, but not diet and nest location) had a significant effect on the status of Israel’s breeding avifauna. Furthermore, several of the factors were interrelated, making it difficult to single out the factor responsible for a certain change. Nevertheless, the main reasons for the changes were assessed as habitat change, introduction of invasive b species and poisoning. Habitat alteration has taken many forms, most of which are re- lated to agriculture. Agriculture poses the greatest threat to birds worldwide (Green et al., 2005), and in Israel it includes aquaculture and construction of water reservoirs, drainage of water bodies, expansion of cultivated areas in Mediterranean and desert regions, afforestation, gardening, increased food availability in the forms of garbage and a surplus of agricultural products, as well as poison- ing. Some of these factors may affect animals, and often act in syn- ergy, making it difficult to determine which is the key factor. Below we discuss the effect of each of these forms of habitat alteration and, where appropriate, their relation to others. Aquaculture and water reservoirs: Despite the fact that in a dry country such as Israel, where most natural water bodies (such as the Hula Lake and adjacent swamp and many rivers and streams) have dried up, many aquatic birds have increased. This has been due to two factors: whereas the now desiccated previous water bodies were rich in weed beds, the new ones are largely expanses of open water consisting of fish ponds and water reservoirs. The in- crease in man-made water bodies has enabled several species of Fig. 2. Probability that population size increased (gray bars) or declined (black various avian orders to increase due to increased fish availability bars) in all bird orders (a) and only in native birds (b) breeding in Israel. The and expanded or new breeding habitats along the shores of fish- probabilities were calculated using ordinal logistic regression. ponds and water reservoirs. The presence of herons benefits fishery management in that they reduce the density of uncontrolled fish related to type of change, with the heaviest birds, (mainly com- fry, eliminate unhealthy fish, eliminate predators of stocked fish posed of Falconiformes) most affected. and indicate unhealthy conditions in the ponds (Ashkenazi and Yom-Tov, 1995, 1997). 5. Discussion Expansion of cultivated areas: Sixty-four species failed to adjust to these changes and have declined. Many of these species are Although our results are based on qualitative rather than quan- ground-nesters whose nesting grounds were altered by agricul- titative data, they have allowed us to analyze population trends of tural practices that increased the cultivated areas. For example, Israel’s avifauna and assess their causes. They show that Israel’s large open areas in semi-desert in the north-western Negev have avifauna (227 species breed or have bred) had undergone a dra- become potato fields, thus eliminating important nesting grounds matic change over the course of a century, a change that has af- for several species including the endangered houbara (Chl- fected 73.6% of species; a. much larger proportion than that amydotis undulata). Overgrazing by Bedouin herds in this region reported worldwide (about 50%: Butchart et al., 2010). Changes has exacerbated this decrease. The establishment of agricultural were more pronounced in the Mediterranean region of Israel than areas in the salt marshes south of the Dead Sea has reduced the in the arid region due to the majority of the human population (ca. available suitable habitat for the small population of the Nubian 90%) residing in the former region, with their activities conse- nightjar (Caprimulgus nubicus) and the 80 pairs that bred there dur- quently mainly impacting there. However, ca. 70% of the species ing the 1980s had been reduced to 15 by 2010 (Perlman, 2011). that breed throughout the country have increased, indicating their Newly-established agricultural settlements in the Arava Valley ecological resilience and opportunism. Although trends of status were formerly sand dunes. Their take-over by agriculture rendered 18 Y. Yom-Tov et al. / Biological Conservation 147 (2012) 13–21

a b

ab

Fig. 3. Probability that population size increased (gray bars) or declined (black bars) in relation to climatic origin, climatic zone, and due to various possible causes in all birds (a) and only in native birds (b) found in Israel. The probabilities were calculated using ordinal logistic regression. this habitat unfavorable to their avian inhabitants (i.e Alaemon lowered the levels of aquifers, with the consequent death of Acacia alaudipes), hence the reduction of several species in these areas trees. This was further exacerbated by the use of pesticides in near- and elsewhere in the desert. On the other hand, the establishment by settlements and agriculture. Similarly, in the Mediterranean re- of desert agricultural settlements, which have created artificial gion, several species declined due to the major expansion of oases in the midst of the desert has enabled the expansion of Med- irrigated areas that are cultivated throughout the year, including iterranean-region birds into desert areas. This is also true for some the birds’ breeding seasons. Ploughing and other agricultural prac- species of tropical origin for which Israel is on the northern periph- tices destroy nesting grounds for sand grouse species and some ery of their range. These species formerly inhabited the few oases and are the main causes for the decrease of these species. in the Arava valley, but have expanded their range to new settle- Afforestation: Afforestation, much of it composed of pine and ments established along the Arava and the Jordan valley north of it. eucalyptus, has benefited only a few species. On the other hand, Prolonged periods of drought and diversion of the course of the increase in land cover due to afforestation and recovery of the streams for road construction and agriculture reduced water avail- Mediterranean chaparral has reduced open habitats, and the ability along the Arava Valley, causing high mortality of Acacia change in land cover has hindered the ability of raptors that forage trees (Ashkenazi, 1995), the only suitable habitat for the Arabian in open habitats to locate prey (Sela, 1977; Friedemann et al., 2011). warbler (Sylvia leucomelaena) in Israel, and their population de- Gardening: The increase in gardening and especially the intro- clined accordingly (Perlman, 2011). In some areas water pumping duction of exotic plants, in addition to the creation of irrigated Y. Yom-Tov et al. / Biological Conservation 147 (2012) 13–21 19 lawns, unknown a century ago in Israel, as well as the expansion of species are tropical in origin, but have managed to establish breed- citrus orchards and pecan plantations, enabled several species that ing populations in the Mediterranean region, probably aided by were previously restricted to the chaparral to extend their distribu- global warming. Hatzofe and Yom-Tov (2002) showed that birds tion to towns and villages south of their former range, some of of tropical origin were significantly likely to become established them to arid habitats as far south as the central Negev. Gardening breeders in Israel. Several of the alien invaders have been very suc- in desert settlements has benefited several species of tropical ori- cessful: flocks of thousands of P. krameri roost in the coastal plain, gin enabling them to expand their distribution in the Rift Valley and cause extensive damage to pecan plantation. The common and west of it. myna (Acridotheres tristis) has spread throughout the Mediterra- Increased food availability: One expression of the increase in nean region and now extends its distribution to desert areas. standard of living is the increased rate of accumulation of organic In addition, birds of tropical origin already breeding in Israel garbage, including unconsumed human food as well as increased were shown to be more likely to extend their breeding range there food availability from farming. Much of this organic material is than birds of northern distribution (Hatzofe and Yom-Tov, 2002). It available to commensal mammals (i.e. Canis aureus, Vulpes vulpes), is difficult to determine the primary factor for this trend, but these the wild boar (Sus scrofa) and to feral cats and dogs due to impro- authors interpreted it as a reaction to global warming, although per garbage management, with bins penetrable to mammals and other factors, such as changes in agricultural practices and habitat (Brickner-Braun et al., 2007). Some poultry farmers discard alteration, also contribute or may even be the primary causes. carcasses in the open, and garbage dumps are often open to com- Since the 1960s, several species of tropical origin that breed south mensal animals, as a result of which commensal birds (mainly Cor- of Israel started to appear in Israel and then to breed there. This vidae) have increased in both Mediterranean and desert areas. This phenomenon is particularly pronounced in the Arava Valley, the increase has a negative effect mainly on ground-nesting birds. closest region to Africa and Arabia and the warmest in Israel. Glo- Crows and ravens prey on eggs and nestlings and attack even rel- bal warming has been shown to impact the distribution of animals, atively large birds, such as black kites (Milvus migrans) and Egyp- and many bird species extended their ranges to the north (re- tian vultures (Neophron percnopterus), while cattle (B. ibis) viewed by Parmesan and Yohe, 2003; Root et al., 2003). It is rea- follow tractors ploughing fields and prey on the exposed reptiles sonable to assume that the above phenomena are related to or amphibians in winter pools. On the other hand, the increasing global warming in synergism with agriculture, irrigation and gar- breeding population of the hooded crows (Corvus corone) popula- dening, similar to what has been reported elsewhere (Beaumont tion has increased the number of nests, leading to an increase et al., 2006). Range expansion probably occurred only after these in this species’ parasitic (Clamator glandarius). The bulky species had already increased their geographical range north of and sturdy empty crow nests are often re-used by Asio otus and their indigenous tropical range (but south of Israel) due to land Falco subuteo, both of which have increased in number. use changes, mainly agricultural development and gardening, all The two other important reasons for change in status of the Israeli the way from their original range to the study area. avifauna are those of poisoning and the introduction of alien species. Farmland pesticides have a serious impact on birds worldwide, and 6. Future prospects it has been estimated that in the USA alone 672 million birds are exposed to them, 10% of which die as a result (Williams, 1997). In At present we are witnessing a trend of impoverishment and Israel, 13 breeding species, mostly Falconiformes, were negatively simplification of Israel’s avifauna, and the prospects for its future impacted during the 1960s by secondary poisoning (Mendelssohn, are that it will become much less diverse. Populations of dozens 1962, 1972; Mendelssohn and Paz, 1977; Mendelssohn et al., of species that have not adapted to the above changes will probably 1979), and most of them did not recover to their former densities. continue their decline and may disappear altogether from Israel. Pesticide residues negatively affect many carnivorous and insectiv- The most likely species to be affected are the large raptors, species orous birds, but deliberate poisoning to prevent damage to crop and inhabiting open habitats such as batha (low shrub areas) and des- livestock is quite common (Mineau et al., 1999). Poisoning still per- ert. On the other hand, species of tropical origin, either local or inva- sists today: 38% of all poisoning cases that involve wildlife are sive, are likely to increase due to the continuing effect of global caused by illegal use of pesticides; and 22% are caused by cattle warming and the continued increase in irrigated areas in the desert. ranchers who quarrel over grazing areas and poison each other’s Similarly, species commensal with humans will increase in num- herds, whose carcasses are then consumed by raptors (Leader bers and extend their distribution from the Mediterranean region et al., 2009). Indeed, during 3 years of survey (2006–2008) a poison- to the desert, often at the expense of species native to these areas. ing event was detected on average every third day (Leader et al., As in other areas around the world, it is essential to reduce the 2009). Two events of mass poisoning of Gyps fulvus in the Mediterra- human ‘‘ecological footprint’’ in Israel. It requires only some very nean region during the last decade resulted in the mortality of 40–50 simple measures to mitigate the above trends: careful control of individuals (including many chicks in their nests) in 1998 and more the expansion of agriculture into arid regions, which will reduce than 30 in 2007, which constituted between a third and a half of the the destruction of important avian habitats; protection of nature breeding population in the Mediterranean region of Israel at the reserves and other areas, still not seriously affected, from urbaniza- time of their poisoning. The increase of commensals, which in turn tion and human encroachment; minimizing the effect of develop- damage crops and plastic water pipes, leads frustrated farmers to ment where it takes place; controlling the influx of invasive deploy poisoned carcasses, thus also killing un-targeted raptors. In species by careful control of imported species to zoos and bird 2011 a pair of Haliaeetus albicilla, part of a 20-year re-introduction breeders; reducing the use of exotic plants in gardening and effort, died this way. encouraging the planting of local trees and plants; law enactment, Worldwide, invasive alien species pose the second major threat such as a law to regulate the use of pesticides, and enforcement of to birds after habitat change (Schmitz and Simberloff, 1997; the laws that require proper garbage handling and cremation or re- D’Antonio and Kark, 2002; Butchart et al., 2010). Sixteen invasive moval of cattle and poultry carcasses; the eradication of feral cats alien species have become established in Israel, the first of which and dogs that have penetrated into the wild, in order to eliminate was Psittacula krameri (Dvir, 1985). Many of the introductions are their predation pressure on wildlife; and finally, helping individual due to neglect by the authorities, but in at least one case of inva- struggling species, such as raptors (i.e. G. fulvus) to recover by care- sion, Corvus splendens, the species first invaded a neighbouring ful management, captive breeding and, where necessary, also re- country and later expanded its territory to Israel. All the introduced introduction programs. 20 Y. Yom-Tov et al. / Biological Conservation 147 (2012) 13–21

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