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The impact of intensive agriculture on the bird community of a sand dune desert
ARTICLE IN PRESS Journal of Arid Environments
Journal of Arid Environments 64 (2006) 448–459 www.elsevier.com/locate/jnlabr/yjare
The impact of intensive agriculture on the bird community of a sand dune desert F. Khoury, M. Al-Shamlih Department of Biological Sciences, Hashemite University, P.O. Box 150459, Zarqa 13115, Jordan Received 24 January 2005; received in revised form 7 June 2005; accepted 8 June 2005 Available online 26 July 2005
Abstract Bird community structure and diversity measures in sand dune habitats adjacent to and distant from modern farms in Wadi Araba, south-west Jordan, were compared using 52 line transects for breeding birds and habitat variables. We used a variety of analytical methods, including multi-variate analysis to describe bird assemblages and determine the best indication of agricultural impact in arid ecosystems using quantitative data on birds. A considerable change in the structure of the bird community of sand dunes surrounding farming projects was measured to a distance of up to 1 km, but could neither be related to changes in habitat structure nor to the activity of opportunistic predators as these did not vary significantly between the two samples. The farms included lines of trees and offered a constant source of water, which attracted a variety of opportunistic species. The absence of characteristic ground-dwelling species of open sand dune habitats in the structurally intact sand dunes surrounding farms was likely to be the result of localized, but effectively far-reaching habitat modification and/or competition with some of the opportunistic species, which were common around farms. r 2005 Elsevier Ltd. All rights reserved. Keywords: Hyperarid desert; Sand dunes; Intensive agriculture; Bird communities; Jordan
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E-mail address: [email protected] (F. Khoury). 0140-1963/$ - see front matter r 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.jaridenv.2005.06.006
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1. Introduction Arid deserts generally support a small number of animal species, which is partly attributed to restricted resources and low primary production levels. Recent studies in the arid deserts of Saudi Arabia have reported spatial and temporal variations in the abundance and diversity of birds (Newton and Newton, 1997; van Heezik and Seddon, 1999). These reports have indicated that structural complexity of vegetation might be the principal factor affecting bird diversity in arid areas. The structure of breeding bird communities in the different desert landscapes of Jordan as well as of other parts of the world, has generally received little attention. Moreover, the anthropogenic impact on bird communities of arid ecosystems has been studied only tentatively. Most studies have focused on the effects of grazing, large irrigation projects and invasive plant species on ecosystem function and the diversity of animals, including birds (Rahmani and Soni, 1997; Whitford, 1997; Dean et al., 2002; Desmond, 2004). The hyperarid Wadi Araba in south-western Jordan exhibits a variety of habitat types ranging from sand dunes and alluvial fans to salt marshes and arid acacia savannahs. Although still considered as one of the least populated and spoilt areas of Jordan (Andrews, 1995), current expansion of agricultural projects in Wadi Araba is probably interfering with ecosystem function and modifying the habitats of birds at an increasing rate. The aim of this study was to determine the impact of intensive agricultural practices on bird communities by comparing the community structure and diversity measures of sand dune habitats immediately surrounding farms with those, which are distant but of the same type. We tested a variety of approaches and analytical methods to determine the best indication of agricultural impact in arid landscapes using quantitative data on birds.
2. Study area Wadi Araba, the northern extension of the Great Rift Valley, is a low-lying, flat strip of land between the mountain range of south-west Jordan and the Negev plateau of southern Israel. It stretches between the Gulf of Aqaba in the south and the Dead Sea in the north, with a maximum width of 30 km. The study included the southern and central parts of the Jordanian side of Wadi Araba (c. 301000 N, 351100 E), 60% of which consists of sand dune desert. The climate is generally hot and hyperarid; the mean annual precipitation is approximately 50 mm, while the annual mean evaporation rate lies around 2000 mm (National Atlas of Jordan, 1984). The occasional rainfalls usually occur during the winter months when temperatures are lower than in summer; temperatures range from 4 1C (absolute minimum) in the winter to 45 1C in the summer, with an annual mean of 24 1C (National Atlas of Jordan, 1984). Local disparities in soil and hydrological conditions cause a variety of vegetation and habitat types (Baierle, 1993). The sand dune habitats considered in this study vary from highly mobile sand dunes, nearly devoid of vegetation to more stable and flat sand dunes, where the surface is occasionally covered with a thin layer
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of fine gravel. The vegetation usually consists of a sparse cover dominated by Haloxylon persicum and a substantial annual cover after the rainy season. A few shallow waterbeds intercept the studied sites, which are lined with relatively dense vegetation dominated by H. persicum, and occasionally including the shrubs Calligonum comosum and Retama raetam. There are a few villages, in addition to nomadic Bedouins, but most of the area is unpopulated and considered a closed military zone due to its proximity to the political borders. Nevertheless, grazing by goats and camels of local Bedouins is permitted and widespread all over. Natural herbivores, e.g. Gazella dorcas, occur in small numbers near the borders with Israel. The establishment of large projects of intensive, irrigated farming is ongoing in several parts of the study area, which exploit ground-water for irrigation and include fenced areas lined with introduced trees as windbreakers. A variety of crops are planted, including citrus fruits, guava, mango and date palms, in addition to vegetables, some of which are grown within greenhouses. Irrigation is continuous all year round, using mainly the drip system while fertilizers and pesticides are being used regularly.
3. Methods 3.1. Field methods Quantitative data on birds were collected using the line transect method (Bibby et al., 2000) in the period from March to May 2004, which covered the major part of the breeding season. Thirty-seven line transects (hereafter referred to as F-transects) were randomly selected in sand dune habitats at distances ranging from 0.5 to 8 km from the nearest farms. Each line transect was 1 km in length, with a belt of 100 m on each side. In addition, 15 line transects (hereafter referred to as C-transects) were carried out in the same habitat type adjacent to farms. While carrying out all Ctransects, the observers walked parallel to and at a distance of 80–100 m from the farm fence, thus additionally covering the birds seen at the border of the farms. The individual farms covered areas ranging from 0.5 to 5 km2, and most had a narrow rectangular shape, with a length exceeding 1 km, thus allowing us to carry out full transects parallel to their borders. Line transects were carried out from sunrise to 10:00 a.m.; the duration of each transect ranged from 25 to 35 min, during which all of the birds within the 100-m belts were recorded by two observers walking parallel, at a distance of 20 m. All transects were carried out twice during the study period, but only the first counts were considered for analysis as the second counts did not produce additional data. The varying numbers of transects in both categories (37 Ftransects and 15 C-transects) were according to the proportion of area covered by each category in the study area. We excluded in the analysis all bird species that do not breed in the study area, e.g. migrants and birds resident and breeding in different habitat types in neighbouring areas, which occasionally utilized the study area for feeding, as well as birds detected beyond 100 m and those just flying over the transects. Habitat variables were quantified at three points (at the two ends and at
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the middle) along each line transect to a range of 50 m before being averaged. This allowed a general description and comparison of the habitats of the two groups of samples. Additionally, the activity of mammalian predators (mainly the opportunistic red fox Vulpes vulpes) was determined by counting the number of trails crossing the sandy surface of line transects. All transects in sand dune habitats, including those adjacent to farms had the same length (1 km) and their ground surface was almost totally covered with sand allowing standard counts of fox tracks. Transects were carried out twice and this included track surveys of fox tracks. There were no significant differences between both counts (paired t-test) and we thus considered the first occasion for each transect. Only fresh tracks from the previous night were counted. Due to the sandy surface and prevailing winds, fresh tracks were easily discriminated from older ones. 3.2. Data analysis Analysis conducted at the community level included the construction of dendrograms of the samples (line transects), using group-average clustering from Bray–Curtis similarities on log-transformed bird abundances (Clarke and Warwick, 2001). Moreover, a non-metric multi-dimensional scaling (MDS) ordination was constructed using the software PRIMER v5 (Clarke and Gorley, 2001), to demonstrate the association of the different bird species according to their log-transformed abundances and Bray–Curtis similarities. The numbers of birds were log-transformed (log x+1) for this analysis to down-weight abundant species, allowing not only the mid-range but also the rarer species to exert some influence on the calculation of similarity (Clarke and Warwick, 2001). MDS shows a great ability to represent complex relations accurately in low-dimensional space, and there is no need to delete any rare species. The MDS chooses a configuration of points, which minimizes the degree of stress (distortion between the similarity ranking and the corresponding distance rankings in the ordination plot). A stress value less than 0.1 gives a good ordination with no real prospect of a misleading interpretation (Clarke and Warwick, 2001). Diversity measures were calculated for all samples (transects) in each group (p0.2 km: C-transects and 40.5 km: F-transects) and included species richness (s ¼ number of species), Shannon–Wiener index (H) and evenness (J). The calculations were according to the following formulas: H¼
s X
Pi ln Pi
J ¼ H=H max ,
i¼1
where s is the number of species present in the sample; Pi is the proportion of species i in the sample of s species; H max ¼ ln s. Diversity measures, avian abundances (total number of individuals of all birds) and abundances of particular species were tested for significant differences among samples using the non-parametric Mann–Whitney U-test, as they departed from normality. The Kurskal–Wallis test was also used to compare the abundances of
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avian species among multiple samples (i.e. at varying distances from farms). Analysis of variance (ANOVA) was applied to examine differences in the habitat variables between the two samples. The impact of agriculture on bird assemblages was further analysed by comparing the abundance of all species originally native to Wadi Araba and referred to as ‘naturally occurring’ with the abundance of ‘opportunistic’/ ‘agricophilic’ birds, which benefited from agricultural expansion as indicated by their range expansion into the general area in previous decades (Table 1; Andrews, 1995; Shirihai, 1996). Other species, which are locally expanding their range due to agricultural developments, were included in the first group, as they are known to belong to the original avifauna of natural habitats in Wadi Araba (Andrews, 1995). These are referred to in Table 1 as agriculture-enhanced. We used the t-test to compare the number of ‘naturally occurring’ and ‘opportunistic’ species in each sample group (F- and C-transects).
Table 1 The classification of birds as agriculture-sensitive and agriculture-enhanced ( ¼ ‘naturally occurring’) and ‘opportunistic’ or ‘agricophilic’ and their abbreviations as used in the MDS ordination (Fig. 2) and Table 3 F-transects (n ¼ 37)
C-transects (n ¼ 15)
Agriculture-sensitive SSG: Spotted Sandgrouse Pterocles senegallus BTL: Bar-tailed Lark Ammomanes cincturus TBL: Thick-billed Lark Ramphocoris clotbey THL: Temminck’s Horned Lark Eremophila bilopha HL: Hoopoe Lark Alaemon alaudipes DW: Desert Wheatear Oenanthe deserti
0.1470.09 0.5170.22 0.0570.05 0.1470.09 1.8170.26 0.5570.13
0 0 0 0 0 0
Agriculture-enhanced LGB: Little Green Bee-eater Merops orientalis YVB: Yellow-vented Bulbul Pycnonotus xanthopygos GGS: Great Grey Shrike Lanius excubitora PS: Palestine Sunbird Nectarina osea TF: Trumpeter Finch Bucanetes githagineusa
0.1970.09 0.0570.05 0.0870.06 0 0.0870.06
1.4070.52** 4.1370.96*** 0 0.0770.07 0
Opportunistic/‘Agricophilic’ CD: Collared Dove Streptopelia decaocto LD: Laughing Dove Streptopelia senegalensis CL: Crested Lark Galerida cristata RBR: Rufous Bush Robin Cercotrichas galactotes GW: Graceful Warbler Prinia gracilis DF: Desert Finch Rhodospiza obsolete HS: House Sparrow Passer domesticus
0.8670.23 0.1470.10 0.7870.12 0 0 0.0870.06 0.1170.11
8.2072.14*** 2.4071.39** 1.7370.46** 0.4770.13 1.2070.46 0.2070.14 6.1371.29***
The mean abundances (7S.E.) are shown for transects distant from (F-transects, 40.5 km) and adjacent to farms (C-transects, p0.2 km). a TF and GGS usually prefer different natural habitats in Wadi Araba (Al-Shamlih et al. unpublished data), and were recorded in sandy habitats close to other habitat types, but not adjacent to agriculture. According to Shirihai (1996), these species are known to benefit from agriculture in deserts. **po0:01; ***po0:001 (U-test).
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4. Results A comparison of the habitat variables and red fox activity in F-transects with those of the C-transects showed that the two groups did not differ significantly in habitat structure or in the activity of red foxes (ANOVA, p40:05 for all habitat variables, Table 2). However, the borders of the farms, which included fences and planted trees, were excluded from this analysis. This lead to the conclusion that the impact of agriculture on the immediate surroundings is due to indirect factors produced by farming practices rather than a direct modification of habitat structure. Although it is likely that farming activities cause a general increase in the abundance of red foxes in the whole study area, there was no significant difference in its activity and assumed effect on birds when F-and C-transects were compared (p40:05). 4.1. Sample clusters and bird assemblages The 52 line transects produced 18 species of breeding birds (Table 1), some of which were present in both samples (F-and C-transects). In the dendrogram based on Bray–Curtis similarity coefficients, two large clusters emerged, separating at a similarity coefficient of 10%. The first cluster (Fig. 1, left) included 81% of the
Table 2 The means (7S.D.) of habitat variables (in percent cover), diversity indices, avian abundance and number of individuals belonging to ‘naturally occurring’ and ‘opportunistic’ bird species in the transects distant from farms (F-transects) and those adjacent to farms (C-transects) Habitat variables/indices
F-transects
C- transects
N Ground cover Rock Sand Stone Gravel
0.170.3 92.4714.9 4.274.0 3.373.1
0.570.6 95.778.9 1.370.1 2.571.8
Vegetation cover Herbaceous Dwarf shrubs Shrubs
3.174.0 2.172.2 10.979.1
1.071.7 1.673.3 12.6711.4
Species richness Shannon diversity Evenness Avian abundancea ‘Naturally occurring’ birds ‘Opportunistic’ birds a
37
3.271.7 0.470.2 0.470.2 6.274.5 3.873.3 2.072.7 *
15
5.871.4*** 0.670.1*** 0.670.2 25.7712.2*** 1.372.2 24.3719.1 **
Avian abundance ¼ total number of individuals of all species belonging to a particular group. *po0:05, **po0:01, ***po0:001.
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Fig. 1. Dendrogram of F- and C-transects, using group-average clustering from Bray–Curtis similarities on log-transformed bird abundances. Similarity coefficient in percent.
F-transects, which diverged to smaller subgroups at various similarity levels above 30%. The subdivisions were probably the result of local variations in the sand dune habitat affecting bird species composition. The second cluster (Fig. 1, right) included all C-transects, which also diverged to several subgroups. However, one subgroup (extreme right, Fig. 1) was formed by 88% of the C-transects, which was separated from other transects at a similarity level of 55%. A few F-transects included ‘opportunistic’ species like the Crested Lark Galerida cristata and were located mainly within a distance of 2.5 km to farms (except F3, Fig. 1), thus they appeared in the dendrogram closer to the C-transects. This indicated a spatial gradient of effects on bird assemblages in sand dune habitats ranging to a distance of around 2.5 km from the borders of farms. In the two-dimensional MDS ordination (Fig. 2), two distinct clusters of birds emerged, demonstrating the differences between bird assemblages of the F-and C-transects, which also included birds recorded at the borders of farms. A number of species were found to be characteristic for the sand dune habitats far from farming projects, as they were virtually absent from other habitat types in Wadi Araba (Al-Shamlih et al., unpublished data). They included mainly the ground-dwelling species, Hoopoe Lark Alaemon alaudipes and Desert Wheatear Oenanthe deserti, which co-occurred locally with the Bar-tailed Lark Ammomanes cincturus, Spotted Sandgrouse Pterocles senegallus and other, less frequent species (Fig. 2). These agriculture-sensitive species were completely absent around farms to a distance of around 1 km. The second cluster in Fig. 2 included all bird species, which have recently colonized the general area or have locally expanded their distribution (Table 1) subsequent to agricultural development. Except for the Crested Lark, all of the opportunistic and agricultureenhanced species are known to use shrubs and trees. Some of these species, especially Collared Dove Streptopelia decaocto and Little Green Bee-eater Merops orientalis also occurred in a number of F-transects, but usually at lower frequency and abundances.
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Fig. 2. A two-dimensional MDS ordination of 18 bird species based on log-transformed abundances and Bray–Curtis similarities (stress ¼ 0.06). The superimposed clusters (dashed lines) represent two different bird communities in sand dune habitats distant from farms (cluster on the left) and adjacent to farms (cluster on the right). The full line circles the two most frequent (indicator/sensitive) species of unaffected sand dune habitat. Abbreviations as in Table 1.
4.2. Diversity indices and other indicators The C-transects had significantly higher Shannon indices and species richness than F-transects (U-Test, po0:001 in both cases, Table 2), although characteristic species of sandy habitats were completely absent in the C-transects. These were replaced in the surrounding sandy habitats and at the edges of farms by a number of ‘opportunistic’ species. In addition, avian abundance was significantly higher around and at the edges of farms when compared to the relatively unaffected sand dune habitats, or F-transects (U-test, po0:001). The number of individuals belonging to ‘opportunistic’ bird species, which have colonized Wadi Araba in recent decades was significantly higher than that of ‘naturally occurring’ birds within the C-transects (t ¼ 3:34, p ¼ 0:002), while in the F-transects, the ‘naturally occurring’ birds were more numerous (t ¼ 2:79, p ¼ 0:016, Table 2). Another approach was to examine the differences in ratios of numbers of ‘opportunistic’ to ‘naturally occurring’ birds between the two samples, which also resulted in a significant difference (U-test, po0:001), the ratio in the C-transects being in average more than 30 times higher than in the F-transects. Table 3 demonstrates the rise in numbers of two sensitive species with increasing distance from farms. The Hoopoe Lark increased significantly with distance, particularly 1.6 km beyond its ‘threshold’ distance, which was estimated at around 0.9 km from the nearest farm. Contrasting to the distribution of sensitive species, two of the opportunistic species, which also occurred in a number of F-transects at varying distances, decreased in numbers with increasing distance from farms. The most marked decrease was beyond a few hundred meters from the borders of farms, as their high abundance in C-transects clearly stood out among the samples (Table 3).
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Table 3 The means (7 S.E.) of abundances of two common sensitive species (HL, DW) and two opportunistic species (CD, CL; occurring also in F-transects) at varying distances from farms: C: 0–0.2 km; F1: 0.5–2.5 km; F2: 2.7–8 km
C (n ¼ 15) F1 (n ¼ 19) F2 (n ¼ 18) Threshold distance (sensitive species) (km)
HL
DW
CD
CL
0 1.2670.30 2.3970.38 * 0.9
0 0.4270.16 0.6870.20
8.2072.14 1.0570.40 0.6770.23 ***
1.7370.46 0.7470.33 0.1170.08 ***
0.9
*po0:05, **po0:01, ***po0:001; U-test for two samples (HL, DW) and Kurskal–Wallis test for multiple samples (CD, CL).Threshold distance represents the distance of the nearest transect to farms, in which sensitive species were recorded. Abbreviations as in Table 1.
5. Discussion The cluster analysis comparing the line transects in sandy habitats adjacent to farms and distant from farms confirmed the impact of intensive farming on bird assemblages. In general, transects with similar bird assemblages clustered together and a major split was observed between most F- and C-transects. A few F-transects were similar to C-transects, indicating that the impact of agriculture may exceed a distance of 0.5 km into the surrounding sand dune habitats. Some of these transects contained a relatively dense shrub cover, thus supporting larger numbers of a few species also occurring along the edges of farms, e.g. Collared Dove and Little Green Bee-eater, and lower numbers of ground-dwelling species of the open sand dune habitat. The MDS ordination produced two main clusters of bird species: the first included agriculture-sensitive species, which inhabited unaffected sand dune habitats and avoided structurally intact sand dunes surrounding farms, whereas the second cluster included species which benefited from intensive, irrigated farming activities. The comparison of the abundances of sensitive and opportunistic species at varying distances from farms revealed a strong impact of agriculture on bird community structure to a distance of around 0.9 km. Beyond this ‘threshold’ distance, the impact appeared to decrease gradually in intensity, as indicated by the variation in the abundance of sensitive species. Avian abundance was probably related to a combination of factors such as productivity and the presence of water resources, both of which were higher at the borders of irrigated farms, when compared to the sand dunes, characterized by low productivity and vegetation cover. Despite the higher diversity indices and avian abundance in the C-transects, which was attributed to the increase of opportunistic species, intensive farming in Wadi Araba is probably interfering in the natural processes of the arid ecosystem, as indicated by the local decline of characteristic desert species. Shirihai (1996) pointed to the decline of Spotted Sandgrouse, Hoopoe and Bar-tailed Larks, Desert Wheatear and other desert species in Israel following rural expansion in desert areas. Most of the ‘opportunistic’/‘agricophilic’ species are
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widespread in Jordan, especially along the northern Jordan Valley and rift margins, where some belong there to the native avifauna (Andrews, 1995; Khoury, 2001). These species have invaded other desert landscapes in Jordan following the establishment of large farming projects (Andrews 1995, personal observation). Arid and hyperarid deserts generally support a limited number of bird species and low population densities, due to low productivity, vegetation cover and habitat complexity (Tomoff, 1974; van Heezik and Seddon, 1999; Desmond, 2004). Birds native to arid deserts are highly adapted to their extreme environment (Tieleman, 2002) and most species are thinly distributed due to intense competition for the scarce resources. Such species were found to be sensitive to intensive agriculture, although farming activities artificially increased productivity, including food resources and water availability. On the Jordanian side of Wadi Araba, modern farms still cover a small proportion of the general area, although they are currently increasing in number and area, and consequently fragmenting the natural desert landscape. Being fenced and secluded, these farms did not directly change the habitat structure of the surroundings. Nonetheless, a complete absence of characteristic ground-dwelling species in the structurally intact sand dunes was notable to a distance of nearly 1 km around farms. Knick and Rotenberry (1995) have previously shown that many characteristic birds of open habitats (core species) avoid marginal sites, which are close to the edges of their natural habitats. There was no evidence for a localized effect of the opportunistic, predatory red fox on bird assemblages, as the activity of red foxes was approximately the same over the whole area. The absence of the typical desert species was probably because they avoid vertical structures (windbreaks) forming barriers, which limit daily, local movements and obscure vision important for efficient foraging, display and predator avoidance. Another possible effect is competition with opportunistic species, particularly the Crested Lark, which was also found in several F-transects, mainly within a distance of 2.5 km from the borders of the nearest farm. There was no further evidence for any other effects, e.g. the use of pesticides, which may however affect opportunistic species more severely, as they would be directly exposed (Mclaughin and Mineau, 1995). The diversity measures used in this study failed to demonstrate any negative impact of intensive farming, which actually lead to a partial loss of the native avifauna. Previous studies showed that frequently used community measures, such as species richness, do not reflect the biodiversity with respect to ecosystem function in arid regions because species richness is frequently higher in degraded or modified ecosystems than in the relatively unchanged systems (Whitford, 2002). If the community of ‘naturally occurring’ bird species in sand dune habitats form a functional group, then their ecosystem services may deteriorate rapidly when most of the species of this group are gone (Balvanera et al., 2001). A comparison of ‘opportunistic’ versus ‘naturally occurring’ birds in both samples revealed significant and clear results regarding their general abundances. Being easy to apply and interpret, such an analytical method can be used to monitor changes resulting from intensive farming or other developments in arid environments on the community and ecosystem levels. Ratios of species groups have been previously used to monitor pollution in marine ecosystems (Raffaelli and Mason, 1981).
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A variety of habitats, each with its distinct vegetation and bird assemblage, produces a diverse and unique landscape in Wadi Araba, which is biogeographically classified as a Sudanian penetration zone (Baierle, 1993). Despite the low a-diversity within the sand dune habitat, its distinctive bird community of mainly agriculturesensitive species without doubt contributes to the b-diversity of the general area.
Acknowledgements We thank Khaled Nassar, Hatim Sultan and Rami Awad from the Jordanian Society for Sustainable Development and Dr. Younis Abu Ghalyun for their assistance in field work and logistic support, and Mohammed Ghaleb for giving us a hand in literature search.
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Journal of Arid Environments 64 (2006) 448–459 www.elsevier.com/locate/jnlabr/yjare
The impact of intensive agriculture on the bird community of a sand dune desert F. Khoury, M. Al-Shamlih Department of Biological Sciences, Hashemite University, P.O. Box 150459, Zarqa 13115, Jordan Received 24 January 2005; received in revised form 7 June 2005; accepted 8 June 2005 Available online 26 July 2005
Abstract Bird community structure and diversity measures in sand dune habitats adjacent to and distant from modern farms in Wadi Araba, south-west Jordan, were compared using 52 line transects for breeding birds and habitat variables. We used a variety of analytical methods, including multi-variate analysis to describe bird assemblages and determine the best indication of agricultural impact in arid ecosystems using quantitative data on birds. A considerable change in the structure of the bird community of sand dunes surrounding farming projects was measured to a distance of up to 1 km, but could neither be related to changes in habitat structure nor to the activity of opportunistic predators as these did not vary significantly between the two samples. The farms included lines of trees and offered a constant source of water, which attracted a variety of opportunistic species. The absence of characteristic ground-dwelling species of open sand dune habitats in the structurally intact sand dunes surrounding farms was likely to be the result of localized, but effectively far-reaching habitat modification and/or competition with some of the opportunistic species, which were common around farms. r 2005 Elsevier Ltd. All rights reserved. Keywords: Hyperarid desert; Sand dunes; Intensive agriculture; Bird communities; Jordan
Corresponding author. Tel.: +962 6 5683494.
E-mail address: [email protected] (F. Khoury). 0140-1963/$ - see front matter r 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.jaridenv.2005.06.006
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1. Introduction Arid deserts generally support a small number of animal species, which is partly attributed to restricted resources and low primary production levels. Recent studies in the arid deserts of Saudi Arabia have reported spatial and temporal variations in the abundance and diversity of birds (Newton and Newton, 1997; van Heezik and Seddon, 1999). These reports have indicated that structural complexity of vegetation might be the principal factor affecting bird diversity in arid areas. The structure of breeding bird communities in the different desert landscapes of Jordan as well as of other parts of the world, has generally received little attention. Moreover, the anthropogenic impact on bird communities of arid ecosystems has been studied only tentatively. Most studies have focused on the effects of grazing, large irrigation projects and invasive plant species on ecosystem function and the diversity of animals, including birds (Rahmani and Soni, 1997; Whitford, 1997; Dean et al., 2002; Desmond, 2004). The hyperarid Wadi Araba in south-western Jordan exhibits a variety of habitat types ranging from sand dunes and alluvial fans to salt marshes and arid acacia savannahs. Although still considered as one of the least populated and spoilt areas of Jordan (Andrews, 1995), current expansion of agricultural projects in Wadi Araba is probably interfering with ecosystem function and modifying the habitats of birds at an increasing rate. The aim of this study was to determine the impact of intensive agricultural practices on bird communities by comparing the community structure and diversity measures of sand dune habitats immediately surrounding farms with those, which are distant but of the same type. We tested a variety of approaches and analytical methods to determine the best indication of agricultural impact in arid landscapes using quantitative data on birds.
2. Study area Wadi Araba, the northern extension of the Great Rift Valley, is a low-lying, flat strip of land between the mountain range of south-west Jordan and the Negev plateau of southern Israel. It stretches between the Gulf of Aqaba in the south and the Dead Sea in the north, with a maximum width of 30 km. The study included the southern and central parts of the Jordanian side of Wadi Araba (c. 301000 N, 351100 E), 60% of which consists of sand dune desert. The climate is generally hot and hyperarid; the mean annual precipitation is approximately 50 mm, while the annual mean evaporation rate lies around 2000 mm (National Atlas of Jordan, 1984). The occasional rainfalls usually occur during the winter months when temperatures are lower than in summer; temperatures range from 4 1C (absolute minimum) in the winter to 45 1C in the summer, with an annual mean of 24 1C (National Atlas of Jordan, 1984). Local disparities in soil and hydrological conditions cause a variety of vegetation and habitat types (Baierle, 1993). The sand dune habitats considered in this study vary from highly mobile sand dunes, nearly devoid of vegetation to more stable and flat sand dunes, where the surface is occasionally covered with a thin layer
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of fine gravel. The vegetation usually consists of a sparse cover dominated by Haloxylon persicum and a substantial annual cover after the rainy season. A few shallow waterbeds intercept the studied sites, which are lined with relatively dense vegetation dominated by H. persicum, and occasionally including the shrubs Calligonum comosum and Retama raetam. There are a few villages, in addition to nomadic Bedouins, but most of the area is unpopulated and considered a closed military zone due to its proximity to the political borders. Nevertheless, grazing by goats and camels of local Bedouins is permitted and widespread all over. Natural herbivores, e.g. Gazella dorcas, occur in small numbers near the borders with Israel. The establishment of large projects of intensive, irrigated farming is ongoing in several parts of the study area, which exploit ground-water for irrigation and include fenced areas lined with introduced trees as windbreakers. A variety of crops are planted, including citrus fruits, guava, mango and date palms, in addition to vegetables, some of which are grown within greenhouses. Irrigation is continuous all year round, using mainly the drip system while fertilizers and pesticides are being used regularly.
3. Methods 3.1. Field methods Quantitative data on birds were collected using the line transect method (Bibby et al., 2000) in the period from March to May 2004, which covered the major part of the breeding season. Thirty-seven line transects (hereafter referred to as F-transects) were randomly selected in sand dune habitats at distances ranging from 0.5 to 8 km from the nearest farms. Each line transect was 1 km in length, with a belt of 100 m on each side. In addition, 15 line transects (hereafter referred to as C-transects) were carried out in the same habitat type adjacent to farms. While carrying out all Ctransects, the observers walked parallel to and at a distance of 80–100 m from the farm fence, thus additionally covering the birds seen at the border of the farms. The individual farms covered areas ranging from 0.5 to 5 km2, and most had a narrow rectangular shape, with a length exceeding 1 km, thus allowing us to carry out full transects parallel to their borders. Line transects were carried out from sunrise to 10:00 a.m.; the duration of each transect ranged from 25 to 35 min, during which all of the birds within the 100-m belts were recorded by two observers walking parallel, at a distance of 20 m. All transects were carried out twice during the study period, but only the first counts were considered for analysis as the second counts did not produce additional data. The varying numbers of transects in both categories (37 Ftransects and 15 C-transects) were according to the proportion of area covered by each category in the study area. We excluded in the analysis all bird species that do not breed in the study area, e.g. migrants and birds resident and breeding in different habitat types in neighbouring areas, which occasionally utilized the study area for feeding, as well as birds detected beyond 100 m and those just flying over the transects. Habitat variables were quantified at three points (at the two ends and at
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the middle) along each line transect to a range of 50 m before being averaged. This allowed a general description and comparison of the habitats of the two groups of samples. Additionally, the activity of mammalian predators (mainly the opportunistic red fox Vulpes vulpes) was determined by counting the number of trails crossing the sandy surface of line transects. All transects in sand dune habitats, including those adjacent to farms had the same length (1 km) and their ground surface was almost totally covered with sand allowing standard counts of fox tracks. Transects were carried out twice and this included track surveys of fox tracks. There were no significant differences between both counts (paired t-test) and we thus considered the first occasion for each transect. Only fresh tracks from the previous night were counted. Due to the sandy surface and prevailing winds, fresh tracks were easily discriminated from older ones. 3.2. Data analysis Analysis conducted at the community level included the construction of dendrograms of the samples (line transects), using group-average clustering from Bray–Curtis similarities on log-transformed bird abundances (Clarke and Warwick, 2001). Moreover, a non-metric multi-dimensional scaling (MDS) ordination was constructed using the software PRIMER v5 (Clarke and Gorley, 2001), to demonstrate the association of the different bird species according to their log-transformed abundances and Bray–Curtis similarities. The numbers of birds were log-transformed (log x+1) for this analysis to down-weight abundant species, allowing not only the mid-range but also the rarer species to exert some influence on the calculation of similarity (Clarke and Warwick, 2001). MDS shows a great ability to represent complex relations accurately in low-dimensional space, and there is no need to delete any rare species. The MDS chooses a configuration of points, which minimizes the degree of stress (distortion between the similarity ranking and the corresponding distance rankings in the ordination plot). A stress value less than 0.1 gives a good ordination with no real prospect of a misleading interpretation (Clarke and Warwick, 2001). Diversity measures were calculated for all samples (transects) in each group (p0.2 km: C-transects and 40.5 km: F-transects) and included species richness (s ¼ number of species), Shannon–Wiener index (H) and evenness (J). The calculations were according to the following formulas: H¼
s X
Pi ln Pi
J ¼ H=H max ,
i¼1
where s is the number of species present in the sample; Pi is the proportion of species i in the sample of s species; H max ¼ ln s. Diversity measures, avian abundances (total number of individuals of all birds) and abundances of particular species were tested for significant differences among samples using the non-parametric Mann–Whitney U-test, as they departed from normality. The Kurskal–Wallis test was also used to compare the abundances of
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avian species among multiple samples (i.e. at varying distances from farms). Analysis of variance (ANOVA) was applied to examine differences in the habitat variables between the two samples. The impact of agriculture on bird assemblages was further analysed by comparing the abundance of all species originally native to Wadi Araba and referred to as ‘naturally occurring’ with the abundance of ‘opportunistic’/ ‘agricophilic’ birds, which benefited from agricultural expansion as indicated by their range expansion into the general area in previous decades (Table 1; Andrews, 1995; Shirihai, 1996). Other species, which are locally expanding their range due to agricultural developments, were included in the first group, as they are known to belong to the original avifauna of natural habitats in Wadi Araba (Andrews, 1995). These are referred to in Table 1 as agriculture-enhanced. We used the t-test to compare the number of ‘naturally occurring’ and ‘opportunistic’ species in each sample group (F- and C-transects).
Table 1 The classification of birds as agriculture-sensitive and agriculture-enhanced ( ¼ ‘naturally occurring’) and ‘opportunistic’ or ‘agricophilic’ and their abbreviations as used in the MDS ordination (Fig. 2) and Table 3 F-transects (n ¼ 37)
C-transects (n ¼ 15)
Agriculture-sensitive SSG: Spotted Sandgrouse Pterocles senegallus BTL: Bar-tailed Lark Ammomanes cincturus TBL: Thick-billed Lark Ramphocoris clotbey THL: Temminck’s Horned Lark Eremophila bilopha HL: Hoopoe Lark Alaemon alaudipes DW: Desert Wheatear Oenanthe deserti
0.1470.09 0.5170.22 0.0570.05 0.1470.09 1.8170.26 0.5570.13
0 0 0 0 0 0
Agriculture-enhanced LGB: Little Green Bee-eater Merops orientalis YVB: Yellow-vented Bulbul Pycnonotus xanthopygos GGS: Great Grey Shrike Lanius excubitora PS: Palestine Sunbird Nectarina osea TF: Trumpeter Finch Bucanetes githagineusa
0.1970.09 0.0570.05 0.0870.06 0 0.0870.06
1.4070.52** 4.1370.96*** 0 0.0770.07 0
Opportunistic/‘Agricophilic’ CD: Collared Dove Streptopelia decaocto LD: Laughing Dove Streptopelia senegalensis CL: Crested Lark Galerida cristata RBR: Rufous Bush Robin Cercotrichas galactotes GW: Graceful Warbler Prinia gracilis DF: Desert Finch Rhodospiza obsolete HS: House Sparrow Passer domesticus
0.8670.23 0.1470.10 0.7870.12 0 0 0.0870.06 0.1170.11
8.2072.14*** 2.4071.39** 1.7370.46** 0.4770.13 1.2070.46 0.2070.14 6.1371.29***
The mean abundances (7S.E.) are shown for transects distant from (F-transects, 40.5 km) and adjacent to farms (C-transects, p0.2 km). a TF and GGS usually prefer different natural habitats in Wadi Araba (Al-Shamlih et al. unpublished data), and were recorded in sandy habitats close to other habitat types, but not adjacent to agriculture. According to Shirihai (1996), these species are known to benefit from agriculture in deserts. **po0:01; ***po0:001 (U-test).
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4. Results A comparison of the habitat variables and red fox activity in F-transects with those of the C-transects showed that the two groups did not differ significantly in habitat structure or in the activity of red foxes (ANOVA, p40:05 for all habitat variables, Table 2). However, the borders of the farms, which included fences and planted trees, were excluded from this analysis. This lead to the conclusion that the impact of agriculture on the immediate surroundings is due to indirect factors produced by farming practices rather than a direct modification of habitat structure. Although it is likely that farming activities cause a general increase in the abundance of red foxes in the whole study area, there was no significant difference in its activity and assumed effect on birds when F-and C-transects were compared (p40:05). 4.1. Sample clusters and bird assemblages The 52 line transects produced 18 species of breeding birds (Table 1), some of which were present in both samples (F-and C-transects). In the dendrogram based on Bray–Curtis similarity coefficients, two large clusters emerged, separating at a similarity coefficient of 10%. The first cluster (Fig. 1, left) included 81% of the
Table 2 The means (7S.D.) of habitat variables (in percent cover), diversity indices, avian abundance and number of individuals belonging to ‘naturally occurring’ and ‘opportunistic’ bird species in the transects distant from farms (F-transects) and those adjacent to farms (C-transects) Habitat variables/indices
F-transects
C- transects
N Ground cover Rock Sand Stone Gravel
0.170.3 92.4714.9 4.274.0 3.373.1
0.570.6 95.778.9 1.370.1 2.571.8
Vegetation cover Herbaceous Dwarf shrubs Shrubs
3.174.0 2.172.2 10.979.1
1.071.7 1.673.3 12.6711.4
Species richness Shannon diversity Evenness Avian abundancea ‘Naturally occurring’ birds ‘Opportunistic’ birds a
37
3.271.7 0.470.2 0.470.2 6.274.5 3.873.3 2.072.7 *
15
5.871.4*** 0.670.1*** 0.670.2 25.7712.2*** 1.372.2 24.3719.1 **
Avian abundance ¼ total number of individuals of all species belonging to a particular group. *po0:05, **po0:01, ***po0:001.
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Fig. 1. Dendrogram of F- and C-transects, using group-average clustering from Bray–Curtis similarities on log-transformed bird abundances. Similarity coefficient in percent.
F-transects, which diverged to smaller subgroups at various similarity levels above 30%. The subdivisions were probably the result of local variations in the sand dune habitat affecting bird species composition. The second cluster (Fig. 1, right) included all C-transects, which also diverged to several subgroups. However, one subgroup (extreme right, Fig. 1) was formed by 88% of the C-transects, which was separated from other transects at a similarity level of 55%. A few F-transects included ‘opportunistic’ species like the Crested Lark Galerida cristata and were located mainly within a distance of 2.5 km to farms (except F3, Fig. 1), thus they appeared in the dendrogram closer to the C-transects. This indicated a spatial gradient of effects on bird assemblages in sand dune habitats ranging to a distance of around 2.5 km from the borders of farms. In the two-dimensional MDS ordination (Fig. 2), two distinct clusters of birds emerged, demonstrating the differences between bird assemblages of the F-and C-transects, which also included birds recorded at the borders of farms. A number of species were found to be characteristic for the sand dune habitats far from farming projects, as they were virtually absent from other habitat types in Wadi Araba (Al-Shamlih et al., unpublished data). They included mainly the ground-dwelling species, Hoopoe Lark Alaemon alaudipes and Desert Wheatear Oenanthe deserti, which co-occurred locally with the Bar-tailed Lark Ammomanes cincturus, Spotted Sandgrouse Pterocles senegallus and other, less frequent species (Fig. 2). These agriculture-sensitive species were completely absent around farms to a distance of around 1 km. The second cluster in Fig. 2 included all bird species, which have recently colonized the general area or have locally expanded their distribution (Table 1) subsequent to agricultural development. Except for the Crested Lark, all of the opportunistic and agricultureenhanced species are known to use shrubs and trees. Some of these species, especially Collared Dove Streptopelia decaocto and Little Green Bee-eater Merops orientalis also occurred in a number of F-transects, but usually at lower frequency and abundances.
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Fig. 2. A two-dimensional MDS ordination of 18 bird species based on log-transformed abundances and Bray–Curtis similarities (stress ¼ 0.06). The superimposed clusters (dashed lines) represent two different bird communities in sand dune habitats distant from farms (cluster on the left) and adjacent to farms (cluster on the right). The full line circles the two most frequent (indicator/sensitive) species of unaffected sand dune habitat. Abbreviations as in Table 1.
4.2. Diversity indices and other indicators The C-transects had significantly higher Shannon indices and species richness than F-transects (U-Test, po0:001 in both cases, Table 2), although characteristic species of sandy habitats were completely absent in the C-transects. These were replaced in the surrounding sandy habitats and at the edges of farms by a number of ‘opportunistic’ species. In addition, avian abundance was significantly higher around and at the edges of farms when compared to the relatively unaffected sand dune habitats, or F-transects (U-test, po0:001). The number of individuals belonging to ‘opportunistic’ bird species, which have colonized Wadi Araba in recent decades was significantly higher than that of ‘naturally occurring’ birds within the C-transects (t ¼ 3:34, p ¼ 0:002), while in the F-transects, the ‘naturally occurring’ birds were more numerous (t ¼ 2:79, p ¼ 0:016, Table 2). Another approach was to examine the differences in ratios of numbers of ‘opportunistic’ to ‘naturally occurring’ birds between the two samples, which also resulted in a significant difference (U-test, po0:001), the ratio in the C-transects being in average more than 30 times higher than in the F-transects. Table 3 demonstrates the rise in numbers of two sensitive species with increasing distance from farms. The Hoopoe Lark increased significantly with distance, particularly 1.6 km beyond its ‘threshold’ distance, which was estimated at around 0.9 km from the nearest farm. Contrasting to the distribution of sensitive species, two of the opportunistic species, which also occurred in a number of F-transects at varying distances, decreased in numbers with increasing distance from farms. The most marked decrease was beyond a few hundred meters from the borders of farms, as their high abundance in C-transects clearly stood out among the samples (Table 3).
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Table 3 The means (7 S.E.) of abundances of two common sensitive species (HL, DW) and two opportunistic species (CD, CL; occurring also in F-transects) at varying distances from farms: C: 0–0.2 km; F1: 0.5–2.5 km; F2: 2.7–8 km
C (n ¼ 15) F1 (n ¼ 19) F2 (n ¼ 18) Threshold distance (sensitive species) (km)
HL
DW
CD
CL
0 1.2670.30 2.3970.38 * 0.9
0 0.4270.16 0.6870.20
8.2072.14 1.0570.40 0.6770.23 ***
1.7370.46 0.7470.33 0.1170.08 ***
0.9
*po0:05, **po0:01, ***po0:001; U-test for two samples (HL, DW) and Kurskal–Wallis test for multiple samples (CD, CL).Threshold distance represents the distance of the nearest transect to farms, in which sensitive species were recorded. Abbreviations as in Table 1.
5. Discussion The cluster analysis comparing the line transects in sandy habitats adjacent to farms and distant from farms confirmed the impact of intensive farming on bird assemblages. In general, transects with similar bird assemblages clustered together and a major split was observed between most F- and C-transects. A few F-transects were similar to C-transects, indicating that the impact of agriculture may exceed a distance of 0.5 km into the surrounding sand dune habitats. Some of these transects contained a relatively dense shrub cover, thus supporting larger numbers of a few species also occurring along the edges of farms, e.g. Collared Dove and Little Green Bee-eater, and lower numbers of ground-dwelling species of the open sand dune habitat. The MDS ordination produced two main clusters of bird species: the first included agriculture-sensitive species, which inhabited unaffected sand dune habitats and avoided structurally intact sand dunes surrounding farms, whereas the second cluster included species which benefited from intensive, irrigated farming activities. The comparison of the abundances of sensitive and opportunistic species at varying distances from farms revealed a strong impact of agriculture on bird community structure to a distance of around 0.9 km. Beyond this ‘threshold’ distance, the impact appeared to decrease gradually in intensity, as indicated by the variation in the abundance of sensitive species. Avian abundance was probably related to a combination of factors such as productivity and the presence of water resources, both of which were higher at the borders of irrigated farms, when compared to the sand dunes, characterized by low productivity and vegetation cover. Despite the higher diversity indices and avian abundance in the C-transects, which was attributed to the increase of opportunistic species, intensive farming in Wadi Araba is probably interfering in the natural processes of the arid ecosystem, as indicated by the local decline of characteristic desert species. Shirihai (1996) pointed to the decline of Spotted Sandgrouse, Hoopoe and Bar-tailed Larks, Desert Wheatear and other desert species in Israel following rural expansion in desert areas. Most of the ‘opportunistic’/‘agricophilic’ species are
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widespread in Jordan, especially along the northern Jordan Valley and rift margins, where some belong there to the native avifauna (Andrews, 1995; Khoury, 2001). These species have invaded other desert landscapes in Jordan following the establishment of large farming projects (Andrews 1995, personal observation). Arid and hyperarid deserts generally support a limited number of bird species and low population densities, due to low productivity, vegetation cover and habitat complexity (Tomoff, 1974; van Heezik and Seddon, 1999; Desmond, 2004). Birds native to arid deserts are highly adapted to their extreme environment (Tieleman, 2002) and most species are thinly distributed due to intense competition for the scarce resources. Such species were found to be sensitive to intensive agriculture, although farming activities artificially increased productivity, including food resources and water availability. On the Jordanian side of Wadi Araba, modern farms still cover a small proportion of the general area, although they are currently increasing in number and area, and consequently fragmenting the natural desert landscape. Being fenced and secluded, these farms did not directly change the habitat structure of the surroundings. Nonetheless, a complete absence of characteristic ground-dwelling species in the structurally intact sand dunes was notable to a distance of nearly 1 km around farms. Knick and Rotenberry (1995) have previously shown that many characteristic birds of open habitats (core species) avoid marginal sites, which are close to the edges of their natural habitats. There was no evidence for a localized effect of the opportunistic, predatory red fox on bird assemblages, as the activity of red foxes was approximately the same over the whole area. The absence of the typical desert species was probably because they avoid vertical structures (windbreaks) forming barriers, which limit daily, local movements and obscure vision important for efficient foraging, display and predator avoidance. Another possible effect is competition with opportunistic species, particularly the Crested Lark, which was also found in several F-transects, mainly within a distance of 2.5 km from the borders of the nearest farm. There was no further evidence for any other effects, e.g. the use of pesticides, which may however affect opportunistic species more severely, as they would be directly exposed (Mclaughin and Mineau, 1995). The diversity measures used in this study failed to demonstrate any negative impact of intensive farming, which actually lead to a partial loss of the native avifauna. Previous studies showed that frequently used community measures, such as species richness, do not reflect the biodiversity with respect to ecosystem function in arid regions because species richness is frequently higher in degraded or modified ecosystems than in the relatively unchanged systems (Whitford, 2002). If the community of ‘naturally occurring’ bird species in sand dune habitats form a functional group, then their ecosystem services may deteriorate rapidly when most of the species of this group are gone (Balvanera et al., 2001). A comparison of ‘opportunistic’ versus ‘naturally occurring’ birds in both samples revealed significant and clear results regarding their general abundances. Being easy to apply and interpret, such an analytical method can be used to monitor changes resulting from intensive farming or other developments in arid environments on the community and ecosystem levels. Ratios of species groups have been previously used to monitor pollution in marine ecosystems (Raffaelli and Mason, 1981).
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A variety of habitats, each with its distinct vegetation and bird assemblage, produces a diverse and unique landscape in Wadi Araba, which is biogeographically classified as a Sudanian penetration zone (Baierle, 1993). Despite the low a-diversity within the sand dune habitat, its distinctive bird community of mainly agriculturesensitive species without doubt contributes to the b-diversity of the general area.
Acknowledgements We thank Khaled Nassar, Hatim Sultan and Rami Awad from the Jordanian Society for Sustainable Development and Dr. Younis Abu Ghalyun for their assistance in field work and logistic support, and Mohammed Ghaleb for giving us a hand in literature search.
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