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Published online 25 April 2006
Published in Crop Sci 46:1360-1370 (2006)
© 2006 Crop Science Society of America
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PLANT GENETIC RESOURCES

Ecogeography and Demography of Cicer judaicum Boiss., a Wild Annual Relative of Domesticated Chickpea

Roi Ben-Davida, Simcha Lev-Yadunb, Canan Canc and Shahal Abboa,*

a The Robert H. Smith Institute of Plant Science and Genetics in Agriculture, The Hebrew University of Jerusalem, P.O. Box 12, Rehovot 76100, Israel
b Department of Biology, Faculty of Science and Science Education, University of Haifa-Oranim, Tivon 36006, Israel
c Department of Biology, University of Gaziantep, 27310, Turkey

* Corresponding author (abbo{at}agri.huji.ac.il)


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Chickpea (Cicer arietinum L.) is a major pulse crop in the Indian subcontinent and other world regions and is characterized by narrow adaptation relative to other cool season food legumes. Comparative ecophysiology employing closely related wild species is a powerful tool to broaden the understanding of the genetic and physiological basis of crop adaptation. However, meager data are available on the ecological preferences of annual wild Cicer species. Moreover, the geographic range, its size, shape, and boundaries as well as its internal structure have never been studied for any of the wild Cicer taxa, thereby limiting our understanding of Cicer biology. Accordingly, this work focused on Israeli C. judaicum Boiss. a wild annual relative of chickpea. We defined the range of the species across the Mediterranean zone of Israel, characterized the ecogeographical profile of its habitats and studied two populated sites at the macro- and microsite levels in terms of plant density, frequency, and niche physical characteristics. Throughout the survey area the species is mostly confined to stony and rocky niches where competition with more aggressive annuals is small. This habitat preference dictates a patchy distribution pattern at all levels, from local niche to the region and beyond.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
CHICKPEA is a grain legume associated with the initiation of agriculture in the Neolithic Near East (Lev-Yadun et al., 2000; Zohary and Hopf, 2000). Annual world production of chickpea amounts to approximately 8 x 106 Mg, a lion's share of it (94%) in developing countries, mainly in the Indian subcontinent (FAO, 2006). Large population sectors in India and its neighboring countries, many of them vegetarian, depend on chickpea as a main dietary protein source, while in developed countries it is considered a health food (e.g., Abbo et al., 2005).

In a recent review on the evolution of domesticated chickpea (Abbo et al., 2003), the authors suggested that the restricted distribution of C. reticulatum Ladiz. (the immediate wild progenitor) poses severe limitations on the adaptation of the crop. These authors hypothesized that the narrow adaptation of C. reticulatum (as deduced from its restricted natural distribution) represents (or stems from) limited genetic variation in key adaptive loci (e.g., temperature and day-length response genes and edaphic requirements). Further, this narrow genetic variation could partly account for the adaptive limitations of domesticated chickpea compared with other cool season grain legumes (e.g., Abbo et al., 2003; Siddique et al., 1999; Turner et al., 2001). Indeed, in their review of pulse crops adaptation in the Canadian and U.S. northern Great Plains, Miller et al. (2002) noted that chickpea has an "unusual response to growth season rainfall" and that pea and lentils had broader adaptation compared with chickpea. Miller et al. (2002) also stressed that "comparative adaptation among pulse crops remains poorly understood." Regardless of the evolutionary and agronomic reasons for the failure of chickpea to occupy a major niche among the autumn sown crops of temperate latitudes, understanding the genetic and physiological basis of adaptation is fundamental for future improvement of chickpea and other crop plants (e.g., Evans, 1993).

The closely related wild relatives of crop plants provide excellent material to study the potential adaptation spectrum of the respective crops (Evans, 1993). Ecophysiology and comparative physiology are key components in such an approach (therein), provided there is a wide range of germplasm lines representing a sufficiently wide ecological spectrum. In the case of Cicer, however, the number of independent wild annual accessions found in genebanks is relatively small (Berger et al., 2003). The data available from the annual Cicer world collection indicate that they provide incomplete coverage of the geographical distribution of the taxa and thus probably also of their genetic diversity (Berger et al., 2003).

As part of our ongoing project aimed at broadening the understanding of the genetic and physiological basis of chickpea adaptation, we focused in this study on C. judaicum, an annual wild taxon and a member of the tertiary genepool of the cultigen (Ladizinsky and Adler, 1976). This species is cross-compatible with C. bijugum Rech. f., which grows in higher latitudes (Ladizinsky and Adler, 1976), making both taxa suitable parents for segregating populations to study the genetic basis of adaptation (Abbo et al., 2003; Berger et al., 2003). The specific aims of this work were as follows: first, to define the geographic range of C. judaicum across the Mediterranean zones of Israel and characterize this range by its size, shape, boundaries and internal structure; second, to identify ecogeographic patterns in the distribution of C. judaicum by using Geographic Information Systems (GIS) and multivariate analyses; and third, to characterize the local spatial pattern of C. judaicum plants, their density, frequency, and preferred microhabitats by focusing on two selected populations.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Survey Procedure
A field survey was held during the growth seasons (November–April) of 2002, 2003, 2004, and 2005 searching for C. judaicum populations across 236 sites in central and northern Israel, excluding most of the West Bank area. First, localities that were documented in the herbarium of the Hebrew University of Jerusalem or in the "ROTEM" database (BioGis, 2002) were visited. Second, typical "like-habitats" were sampled using the "search image" concept (Engels et al., 1995). To establish presence or absence patterns, ecogeographic data was collected for each site irrespectively of whether C. judaicum was found. In each site, latitude, longitude, and altitude were determined by GPS, and location descriptors (geographical region, road or settlement name, proximity to prominent land marks) and site physical characteristics (habitat type, slope, aspect, and precise location of target species plants at the site, if found) were recorded. Ecogeographical data were extracted from the Geographic Information System (GIS) center of the Hebrew University of Jerusalem and from maps of the Israel meteorological service (for annual and monthly rainfall, monthly minimum and maximum temperature, soil type, lithology, associated species, vegetation cover, and distance to nearer settlement, road, or reserve). To ensure independence between observations and avoid autocorrelations, a minimal distance of 2 km between sites was kept (Legendre, 1993; Guisan and Zimmerman, 2000). On the basis of the presence–absence data, a "dot map" was constructed by the GIS software ArcView3.2 (ESRI, 2002).

Multivariate Analysis
The following 11 ecogeographical variables were used in all multivariate techniques: longitude (Ln), latitude (Lt), altitude (Al), annual rainfall (Rn-A), mean and minimum temperature in January, representing peak winter conditions (mean and minimum winter temperature- Tmean-W, Tmin-W), mean and maximum temperature in August representing peak summer conditions (mean and maximum summer temperature—Tmean-S, Tmax-S), slope direction relative to the north (S-D), slope rate in percentage (S-R), and distance to sea (Dis-S). For the implementation of discriminant analysis and hierarchical clustering analyses, the ecogeographical data were standardized by dividing each descriptor by its range (maximum–minimum).

Discriminant Analysis
The availability of presence–absence data, from the 236 survey sites, allowed the use of a group discriminant technique aimed to optimize the prediction model performance (Robertson et al., 2003). This was made deliberately to optimize the prediction model performance (Robertson et al., 2003). Canonical discriminant analysis was performed with absent–present as the initial classification criterion. The prediction model group- discrimination technique was based on variables that may affect plant growth directly (Rn-A,Tmean-W, Tmin-W, Tmean-S, and Tmax-S) and indirect variables mediating their effect via the direct variables (Ln, Lt, Al, S-D, S-R, and Dis-S) (defined by Austin, 1985). The relatively limited geographical range of the survey justifies the utilization of indirect variables (Guisan and Zimmerman, 2000). Subsequently, the effects of the qualitative variables of soil type and lithology were assessed through a GIS query. Discriminant analysis was preformed by the JMP 5.0 statistical package (SAS Institute, 2001).

Hierarchical Clustering
Ward's hierarchical clustering (Ward, 1963) was used to identify discrete groups of C. judaicum populated sites, after Delacy et al. (1996) and Berger and Speijers (2003).

PCA Analysis
Principal component analysis (PCA) of the continuous ecogeographical variables was used to identify a smaller number of principal components to account for most of the ecogeographical variance among 52 sites populated with C. judaicum. PCA was based on the correlation matrix and presented as biplot ordinations of populated sites (PC scores) and ecogeographical variables (PC factor loading). Actual populated sites were depicted in the ordination by plotting sites' principal component scores using a unique symbol for each cluster of sites. Three components were extracted by Eigenvales >1 to ensure meaningful implementation of the data by each factor. PCA and hierarchical clustering was applied by SPSS v.12 (SPSS, 2002).

Ecological Assay
The ecological assay, aimed at characterizing the local conditions at the populated site level, was preformed at Nahal A'naba and Nahal Mea'ra (Fig. 1 ) on four different dates (March 2002 and three dates during 2003 season: early January, end of February and early April). In addition, two long transects, extending from south to north and from west to east, were undertaken in each site during the 2003 season to obtain a rough estimate of the spatial size of the two populations.


Figure 1
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  		Fig. 1. Distribution map of C. judaicum sites across Israel. Collection sites of C. judaicum specimen deposited at the Hebrew University of Jerusalem Herbarium ({circ}), sites found in this work ({blacktriangleup}).

 
The N. A'naba site is located southeast of Modii'n town and consists of four slopes: southeast, west, northwest and east facing slopes. The N. Mea'ra site is located at Judea foothills and consists of two contrasting, south and north facing slopes. Both sites are under seasonal grazing, cattle at N. A'naba and sheep at N. Mea'ra.

Demographic surveys in both sites were performed along random transects across the different slopes (2–4 transects per slope) aiming to maximize microsite topographic variability. Transects position relative to slope direction was random. Each transect (50 x 0.5 m) consisted of 25 sampling units of 1 m2 each. Two ecological parameters were measured in each sampling unit, namely, frequency and plant density. Frequency (presence, regardless of the number of individuals, or absence of C. judaicum from the sampling units) was measured as "Rooted (plant) Frequency" (Greig-Smith, 1964) on the four visiting dates. Average frequency of each transect was transformed by the transformation arcsin{surd}x (0 < x < 1) (Sokal and Rohlf, 1997). Plant density (number of plants in each sampling unit) was measured during the 2003 season only. Average plant density of each transect was transformed to {surd}(x + 1) for analysis of variance and Tukey Kremer test (after Noy-Meir et al., 1991b). A third ecological parameter, the distribution pattern (I value), was calculated for each transect out of the plant density data, with I = (variance of sampling units within the transect)/(average plant density in the transect) (Kershaw, 1973).

To assess the effect of site and sampling date on the three ecological variables (frequency, plant density, and distribution pattern), analysis of variance (ANOVA) was implemented. An unbalanced factorial model was employed with Yijk as the score of the kth transect sampled at the jth sampling date from the ith site for each of the three ecological variables, by the formula:

Formula
where µ is the general mean, {alpha}I is the site factor with fixed effect [i = 1 (N. A'naba), i = 2 (N. Mea'ra)], ßj is the sampling date factor with fixed effect [j = 1 (early January), j = 2 (end of February), j = 3 (early April)], {alpha}I x ßj is the effect of the interaction between the jth sampling date and ith site, and eijk is the effect of the kth transect in the ijth {alpha}I x ßj combination (k = 1 to n).

On the basis of the frequency data, a total of 160 populated patches were detected in both sites, 99 at the N. A'naba site and 61 at the N. Mea'ra site. This nonbiased sample of 160 patches was used for the assessment of descriptive statistics of patch characteristics at both sites and comparisons between sites (Student's t test).

General habitat classification was recorded for each sampling unit (644 in total). Each of the 25 sampling units in each transect was assigned to 1 of 10 microhabitat classes: rocky, stony, exposed, grove, and their six combinations. Compositional habitat diversity was measured by calculating Shannon diversity index (SDI) (Magurran, 1988) for each transect,

Formula
where pi is the proportion of m2 sampling unit at each transect classified to the ith class.

To examine the association between frequency data and habitat type, a {chi}2 test for discrete variables was performed.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Survey
Overall, 52 C. judaicum populations were found in this survey from Haela Valley (Aviezer) in the south to Nazareth Mountains in the north (Fig. 1). The northern population (Hasolelim) and the southern population (Aviezer) are only 120 km apart. Hasolelim is also the eastern most populated site and is located 30 km from West Carmel, the western most population (two km off the Mediterranean seashore). Incorporation of herbarium data into the map (Fig. 1) enabled us to define the range of the species in Israel from historical perspective. The present geographical range found in this survey is in accord with the historical range with the exception of an herbarium specimen collection around Metula (E35°34' N33°16') in the upper Galilee (Fig. 1). In our survey, no population was found north of the Nazareth mountains (E35°15' N32°45') anywhere in the lower and upper Galilee, despite intense efforts.

The Israeli C. judaicum populated sites fall into two main groups, northern and southern. This finding partly reflects the poor sampling within the Palestinian Authority area of Samaria and Judea and the dense human infrastructure in the Sharon plain and lower parts of Samaria, which severely disturbed known C. judaicum natural habitats. The main geographic regions in Israel in which C. judaicum was absent include Lakhish, the costal plain, Mt. Gilboa, western Galilee, upper Galilee, and the Golan heights.

Ecogeographical Characterization of C. judaicum Sites
The altitude of C. judaicum sites ranges from 41 m above sea level (a.s.l.) in Nahal Narbata to 749 m a.s.l. in Mevo Beitar. The average altitude across all the populated sites is 322 ± 15 m. Each year, a typical C. judaicum site gets between 55 and 65 rainy days (>0.01 mm rainfall). The mean annual rainfall (Rn-A) ranges from 473 mm in Aviezer to 665 mm in Mey A'mi, with an average of 564 ± 8 mm across sites. The main rainfall share (73%) occurs during the vegetative phase of the C. judaicum plants (mid November to mid February), with the rest occurring either as germinating showers (4% of the rainfall) or during flowering and podding stages (26%, see Table 1). In the winter, the minimum temperature at C. judaicum sites is relatively high, ranging between 7 and 9.5°C. In November, at the beginning of the growth season, the minimum–maximum range is 13.4 to 22.6°C, and becoming colder in December (9.52–18.6°C) and January (2.4–17°C). At the end of the winter, temperatures are relatively mild, ranging between 7.8 and 17.6°C (Table 1.).


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  		Table 1. Mean ± SE and ranges of seasonal rainfall and temperatures (during the growth season) for sites with C. judaicum populations in Israel.

 
The survey data do not show any habitat preference of the species to a certain slope aspect. Populations are located at southern (37% of the populations), western (32.6%), northern (24%), and eastern slopes (6.5%). This distribution pattern of the populated sites is not significantly different from the division of slope aspects among all survey sites. The low frequency of east facing slopes is dictated by the topographic structure of the Judea and Samaria Mountain ranges, which dominates the survey areas. The slope rate of the populated sites is moderate to medium, though some are completely flat or steep, both at about 10% frequency.

At 89.2% of the C. judaicum sites, the soil is defined as Red Mediterranean, which consists of Terra Rossa and brown rendzina soils (21 and 20 of the population sites, respectively). These two types of soils are well aerated, have good water percolation and high field capacity (Ravikovitch, 1969). In accordance with the country's lithology, Terra Rossa soils are usually formed on hard limestone and dolomite bedrock (90% of Terra Rossa soils), while the brown rendzina sites mostly rest on chalk (76% of them).

Vegetation Characteristics of C. judaicum Sites
About 40% of the populated sites are dispersed in planted forests (mostly pine) and 30% in natural habitats, both much disturbed by human activity. Among the vegetation forms in the populated sites, batha, dense and open garigue, maquis, and park vegetation were recorded. In the natural habitats the common perennial species found were the following: Quercus calliprinos Webb., Quercus ithaburensis Decaisne, Pistacia lentiscus L., Ceratonia siliqua L., Rhamnus lycioides L. subsp. graeca (Boiss. et Reuter) Tutin, Sarcopoterium spinosum (L.) Spach, Calicotome villosa (Poiret) Link and Majorana syriaca (L.) Rafin. Common annuals at the sites were Trifolium spp., Medicago spp., Vicia spp., and Onobrychis spp.

Discriminant Analysis
The discrimination between sites designated "C. judaicum present" and "C. judaicum absent" was found significant by the Wilks' Lambda test [P(F) ≤ 0.0001]. The output data of C. judaicum absence sites that were classified into the C. judaicum present group can be used to highlight areas of unpopulated sites with the potential to host C. judaicum (Fig. 2 ). The western lower Galilee (6 sites), Mt Carmel (3), west Samaria (4), and south Judea mountains (24) are such areas. In this respect, the Galilee region is unique, since no population was found there so far. This region is between Hasolelim (northern most population of the current survey) and Metula, where the northern most specimen of the Hebrew University Herbarium was collected by the late M. Zohary in 1965.


Figure 2
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  		Fig. 2. Prediction of sites with a potential to host C. judaicum. Analysis is based on ecogeographical data from 236 survey sites. The prediction model group discrimination techniques used records of 9 quantitative variables. In a succeeding stage the qualitative variables of soil type and lithology were applied as selecting factors by the GIS software. Sites where C. judaicum may be found ({blacksquare}), sites where the species is unlikely to grow ({circ}).

 
Ecogeographic Clusters and PCA Analysis
The hierarchical clustering procedure assembled the 52 C. judaicum sites into three distinct clusters. This three-cluster solution accounts for 87% of the variation in the data set. Cluster no. 2 is the biggest including 29 populated site, while Clusters 1 and 3 contain 13 and 9 populated sites, respectively.

PCA extracted three principal components (Eigenvalues > 1), accounting collectively for 85.5% of the variance. Principal component 1 [PC1] (x-axis, Fig. 3 , Table 2) explains 46.2% of the dataset variation. This axis is loaded positively with altitude, distance from the sea, longitude, mean annual rainfall, and slope. PC1 is also negatively loaded with winter and summer temperature variables. PC 2 (y-axis, Fig. 3, Table 2) explains 29.5% of the dataset variation, and is positively loaded with latitude and mean annual rainfall. PC2 is also negatively loaded with maximum summer temperature and distance from the sea. The angle to north variable exhibits weak factor loadings for PC1 and PC2. In addition, PC3 positive factor loading is dominated almost exclusively by the angle to north variable, but is associated with only 9.9% of the dataset variation with a marginal Eigenvalue (Table 2).


Figure 3
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  		Fig. 3. Principal components analysis (based on the correlation matrix) of the 52 C. judaicum sites from Israel, based on ecogeographic variables (indicated in materials and methods). Biplot vectors indicate strength and direction of factor loadings for PC1 and PC2. Points are sites scores with cluster membership (see Table 3) illustrated with different symbols.

 

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  		Table 3. The C. judaicum populated sites across Israel merged into three ecogeographic clusters. For each cluster means ± SE of ecogeographic descriptors and number of populated sites are listed. The hierarchical clustering analysis was preformed on the 52 populated sites using 11 ecogeographic variables (indicated in materials and methods) after Ward (1963). To compare means, Tukey Kramer test was performed. In each variable, means labeled with different letters differ significantly at {alpha} = 0.05.

 

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  		Table 2. Factor loadings for principal components with Eigenvalues > 1 and % of variance explained by each component.

 
The position of C. judaicum sites marked by clusters on the plane of the first two PC axes highlights the ecogeographic variation between and within clusters. Cluster 1 scores mostly concentrated at the positive part of the PC2. It consists of northern sites from the lower Galilee, Mt Carmel, and western Samaria. These sites characterized mainly by high rainfall and relatively short distance from the Mediterranean Sea. Cluster 2, the largest cluster includes sites from the Shfela and the Judea foothills. These sites scores mostly concentrated at the negative part of the PCA chart. It consists of western sites characterized mainly by short distance from the Mediterranean Sea, low altitude as well as low rainfall, relatively high winter temperature, and relatively intermediate-to-high summer temperature. Cluster 2, holds the widest ecogeographic range as expressed by site score distribution (Fig. 3). The nine sites of Cluster 3, originating from the Judean Mountains, are plotted along the positive part of PC1 reflecting southern location, high seasonal rainfall, and low winter and summer temperatures (Fig. 3, Table 3).

Population Demography
Most of the C. judaicum populations were small and plants occurred sporadically in space, as little groups or as individuals. At the microsite level, C. judaicum plants occupied different habitats such as open grassland, rocky crevices, ancient dry stone walls, and rubble mounds.

The estimated spatial size of N. A'naba population, on the basis of the two frequency transects, was about 1280 x 903 m (estimated area of 115.5 x 104 m2). In practice, there was a continuum of C. judaicum plants and the population was delimited to the north and east by the newly developed area of Moddi'n town (observations suggests that the original range was much wider). The estimated size of the N. Mea'ra population was smaller, being 784 x 110 m (estimated area of 8.6 x 104 m2).

Population Ecological Parameters
In all three ecological descriptors, there were differences between sites (Table 4). I values of both sites yielded a ratio higher than 1, pointing to a patchy distribution of the two populations. I ratio was significantly higher at N. A'naba than at N. Mea'ra (5.6 and 2.9, respectively, see Table 4), indicating a more aggregated pattern. This patchy pattern is in accord with the habitat heterogeneity of the two sites (Fig. 4 ).


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  		Table 4. Demographic parameters of C. judaicum populations at N. A'naba and N. Mea'ra, and distribution of plants in the populated patches therein. Data are mean ± SE of the distribution pattern within site and within patch (I), frequency of C. judaicum plants in each site and density values within site and patches, estimate patch area, distance between patches, number of plants per patch and variance of number of plants within spot. All patch descriptors data except for distribution pattern are based on 99 patches sampled at N. A'naba and 61 patches at N. Mea'ra. Probability of F and t values indicates the significance of differences between the two sites when applying ANOVA to the listed parameters.

 

Figure 4
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  		Fig. 4. The distribution of the different microhabitat types among populated sampled units. Numbers within pie slices indicate the total populated sample units of each category.

 
The frequency and density values are significantly higher in N. A'naba population than in the N. Mea'ra population (Table 4). At N. A'naba, C. judaicum plants were found in 228 out of a total of 601 sampling units (frequency of 0.37). At N. Mea'ra, the species was observed only in 97 out of 575 sampling units (frequency of 0.14). The density parameter was tested across three sampling dates during the 2003 season. Significant changes in density values were observed in both sites during the growth season (comparing early January with the end of February and early April, Fig. 5 ). Unlike the seasonal changes in the density values, the measured frequency values in January did not differ from February or April records.


Figure 5
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  		Fig. 5. Values of mean ± S.E. plant density at N. A'naba and N. Mea'ra sites on three sampling dates. The influence of the sampling date factor on plant density was significant P(F) < 0.0001. Tukey Kramer test was applied for comparing plant density between sampling dates at each site. Columns labeled with different letters differ significantly (within sites) at {alpha} = 0.05.

 
Populated Patch Descriptors
The patchy distribution of C. judaicum population, as seen in both sites, stressed the need to focus on the populated patch level. Some of the patch descriptors are significantly different in the two sites (Table 4). Patches are bigger and thicker at N. A'naba than at N. Mea'ra, as evident from the number of plants, estimated patch area, and plant density within the patch. Average distance between populated patches of 8.2 m was calculated for both sites. Distribution pattern values of I > 1, I = 1, and I < 1 represent patchy, random, and regular distribution pattern, respectively. The secondary aggregation found within patches at N. A'naba (I = 2.3), could be a possible indication for microheterogeneity at the patch level. Another indication for such secondary aggregation is the high variance within the patch detected at N. A'naba population (Table 4). Unlike the secondary aggregation at N. A'naba site, the distribution pattern of C. judaicum plants at N. Mea'ra within patches was fairly regular.

Microhabitat Characterization
Habitats with stony characteristics were the most common in the tested sites. The majority of the sampling units were counted as one of the following: stony, stony–exposed, or rocky–stony. Heterogeneity of habitats was observed in all tested slopes with the highest SDI value detected at the north facing slope of N. Mea'ra and at the northwest slope of N. A'naba (Table 5). The SDI value in those two microsites are significantly different from the lowest SDI value found at the south facing slope of N. Mea'ra. No significant differences in micro habitat diversity were found between the four slopes of N. A'naba site (Table 5). The three slopes of N. A'naba with the intermediate SDI values (eastern, south eastern and western) had the highest frequency, number of patches, and density of C. judaicum in a patch. Frequency of C. judaicum was particularly low on the northern slope of N. Mea'ra (Table 5).


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  		Table 5. Microhabitat spatial pattern and landscape structure of slopes inhabited by C. judaicum at the two tested sites. Slopes means ± SE of Shannon diversity index together with frequency and patch number per transect are indicated. The classification of microhabitats was made on 475 of 1 m2 units sampled during the 2003 season at N. A'naba and N. Mea'ra. Calculation and analyses were made along each transect separately, each including 25 sampling units. To compare means, Tukey Kramer test was performed. In each column, means labeled with different letters differ significantly at {alpha} = 0.05.

 
The frequency of C. judaicum in all habitat types with stony or rocky components was higher than 20% and above 40% in rocky–stony habitats (Fig. 4). The distribution of the different habitat types within the two groups of populated and unpopulated sampling units was nonrandom as evident from the Pearson test ({chi}2 = 77, P({chi}2) < .0001), a hint for differential habitat preference of the species. Of all populated sampling units, 87.6% were characterized as stony or rocky habitats. Indeed, out of 191 populated sampling units, 91 were defined as rocky–stony, 47 as stony, and 28 as stony–exposed (Fig. 4).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Cicer judaicum Distribution Range: Size, Boundaries and Internal Structure
Ecologists concerned with the size of geographic range of species pointed out that, in certain cases, the range decreases with decreasing elevation (Brown et al., 1996). Apparently, this observation also holds true when comparing the distribution range of C. judaicum to the present known distribution of other annual Cicer species (Berger et al., 2003). Accordingly, C. judaicum distribution area is smaller than the ranges of C. reticulatum and C. echinospermum P. H. Davis and considerably smaller than those of its two closely related species C. pinnatifidum Jaub. & Spach and C. bijugum (in order of magnitude difference).

The internal structure of the C. judaicum distribution range explains the irregularity of the population spatial scattering. (Fig. 1, 2). Many areas within the overall Israeli distribution area are uninhabited (zero local abundance). This internal structure characteristic, discussed in a general theoretical context by Brown et al. (1996), makes any attempt to estimate the general frequency of C. judaicum problematic. Nevertheless, the relatively low abundance of the species is an established fact throughout Israel.

The absence of C. judaicum from the upper Galilee and the Golan Heights may account for the ecogeographic adaptive preferences of the species. The apparent distribution range may reflect avoidance of sites with relatively low winter temperature, mild to high annual rainfall, and intermediate altitude (>800 m above sea level in this survey), as expressed by the relatively low occupancy of sites scores in the positive quarter of the PCA chart (Fig. 3).

Cicer judaicum populations were found in different types of habitats, from Mediterranean forest in Hasolelim and rocky slopes at N. Mea'ra to planted pine forest in Kesalon and Mevo Beitar. We never encountered C. judaicum in a ruderal context such as road sides, settlements, and field edges. Only in one case (Nataf) plants were found along the edge of a countryside paved road (seldom sprayed against weeds). In two other cases, Givat Ada and Talmon, populations were found in newly constructed sites. It remains to be seen if in the long run the species will survive in the two latter localities. In traditional farming sites, still prevalent in the Palestinian Authority, C. judaicum plants were observed in olive groves margins (Ebtan and Ras-Karkar). Interestingly, C. pinnatifidum, which thrives in similar contexts, were observed (by Can and Abbo) in Gaziantep province (near Burç) and along the Golbasi-Adiyaman road in eastern Turkey.

About 39% of the survey sites were within nature reserves. Yet, C. judaicum populations were found only in three out of these 17 protected sites, suggesting poor prospects for in situ conservation of this species. It is probably safe to say that the high rate of infrastructure development in Israel, a densely settled country, puts most Israeli populations of the species at risk of extinction. For instance, such extinction has already occurred around Jerusalem where specimens were collected from what is now within the city area (e.g., latest collections from the 1970s within the Giva'at-Ram campus of the Hebrew University).

Another aspect of natural habitats disturbance is the process of fragmentation, an outcome of breaking the continuity of a natural habitat area by zones of construction or other human interference. This includes two components: first, the reduction in habitat area, and second, the formation of isolated populated islands derived from an original continuous populated space. One possible outcome of such isolation might be limited (or absence of) gene flow, followed by increased differentiation and/or decreased fitness. In the long run, this process could proceed to full extinction (Frankham et al., 2002). In the case of C. judaicum, a self-pollinating species with limited cross pollination, severe reduction in population size might have profound and radical effects on the population allele pool. In fact, the relatively small distribution range of the species in Israel suggests a pessimistic prospect. This subject, however, needs to be considered in a much wider context of the Mediterranean basin as a whole. This region suffers from 95% loss of primary habitats resulting in the second largest portion of endangered plant species after the tropical rainforests (Myers et al., 2000). The latter authors defined the Mediterranean basin as a "hotspot" from a biodiversity standpoint, hosting 13 000 endemic species, 50% of the region's total number of plants.

The distribution map (Fig. 1) highlights the confinement of Israeli C. judaicum populations into a relatively narrow range. The world collection, however, includes accessions from Lebanon and Syria, areas which presently are beyond our reach. Notably, both C. judaicum and C. pinnatifidum (a closely related annual species) are reported to grow sympatrically in the Damascus basin, Syria (van der Maesen, 1972). Cicer judaicum was also reported in eastern Turkey (Fig. 1 of Berger et al., 2003). However, in a recent survey in eastern Turkey (by C. Can and S. Abbo), these claims could not be confirmed, as not a single C. judaicum population was found in Gaziantep, Adiyaman, Urfa, Marash, Diyarbakir, and Mardin provinces. Rather, thriving populations of C. pinnatifidum were easily located in all the above Turkish provinces. In our view, the pattern observed in eastern Turkey and the complete absence of C. judaicum populations from the northern parts of Israel calls for reevaluation of herbaria materials, detailed surveys in other eastern Mediterranean countries, and reconsideration of current distribution data of these two taxa.

Prediction of Potential C. judaicum Habitats
Since the biology of C. judaicum (like most wild Cicer species) is not well known, any information regarding factors limiting its distribution is significant. We implemented a correlative predictive model (Robertson et al., 2003), which pointed to three areas with a potential to host habitats of C. judaicum, namely, the Judean Mountains and foothills, west Samaria, and lower Galilee (Fig. 2). Further exploration in those areas might be rewarding. Since we have surveyed those three regions quite intensively, we suspect that, if present, C. judaicum must be relatively rare in these areas. Nonetheless, the unpopulated lower Galilee region which was highlighted by the prediction model is an attractive area because it harbors many locations in which no C. judaicum was recorded thus far.

The use of ecogeographical data from such surveys may be somewhat problematic. This is because of inherent extrapolation errors and the scattering of meteorological stations that do not expose the full relevant microclimate spectrum (Guisan and Zimmerman, 2000). In addition, our work was restricted by political borders (to the north and east of the survey area) with the possible result of exposing only part of the true distribution picture. This is not exceptional, as political boundaries limitation is a common feature in many studies of species geographic range (Gaston, 1990). Consequently, our prediction model results should be approached with caution.

A positive correlation between abundance and distribution range is expected when the reference habitat (in which abundance was measured) is common throughout the range over which distribution is recorded (Gaston and Lawton, 1990). Gaston (1996) claimed that this positive correlation may cause some measurement errors of underestimating the distribution and occurrence of species with lower local density. Across the Israeli sites, planted forests and natural habitats with the "search image" formed during this survey were not rare, thereby supporting the possibility of such positive correlation. It seems that C. judaicum may be an interesting case to test the above hypothesis due to its apparent low density (in most sites) and relatively restricted geographic range.

Population Demography
The N. Anaba and N. Meara sites (depicted in Fig. 1) were chosen for a detailed two-season demographic assay at the population level. Estimate of local population density is often being used as a predictor for the overall geographic range of species. The spatial distribution of individual C. judaicum plants within the population space is patchy (Table 5). A major factor determining plant spatial distribution is the mode of seed dispersal (Perevolotsky and Polak, 2001). Cicer judaicum is a short-stature plant most of whose pods fall to the ground and shatter only thereafter, thus minimizing long distance and even seed dispersal. This may account for the relatively limited size of C. judaicum patches. A second important factor is the occurrence and spatial distribution of safe-sites for germination. Heterogeneous habitats are usually a mosaic of such safe and unsafe patches for the establishment of particular species (Crawley, 1997).

Density values in annual plant populations may vary between seasons (Noy-Meir et al., 1991b). Because of the short time frame of our study, we dealt only with intraseasonal changes. In both sites, plant density was higher during the early winter compared with mid winter and early spring, apparently for two reasons (Fig. 5): first, the intensive cattle grazing that occurs at N. Anaba in early February (N. Mea'ra site was also exposed to sheep grazing), and second, the ease of identifying the four-to-five leaf stage plantlets, which are common in early winter. At this timing, the stems of the common grasses have not yet elongated, leaving the C. judaicum young plants unmasked by the grass canopy, hence easy to find (Fig. 6 ). Intraseasonal fluctuations were detected also in the frequency variable, but those were not statistically significant (data not shown). Notably, the correlation between the density variable and the frequency variable, although significant (p = 0.005), is only 0.48. Therefore, frequency values will not automatically correspond to changes in density, particularly in light of the aggregated spatial distribution pattern of the species.


Figure 6
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  		Fig. 6. Young C. judaicum plant photo was taken on December at N. Mea'ra site (a, left panel). A C. judaicum plant among dense grasses, mainly Hordeum spontaneum photo was taken on February at N. A'naba (b, right panel).

 
Populated Patch Descriptors
The north facing slope of N. Mea'ra and the northwest facing slope of N. Anaba are characterized by the highest compositional habitat diversity values (SDI, Table 5). Significant portions of these slopes support growth of shrubs associated with Mediterranean garigue. Consequently, and probably because of competition, C. judaicum plants occur therein at low frequency values, small number of patches per transect, and lower density within patches (Table 5).

Wild Mediterranean grasses [like barley, Hordeum spontaneum C. Koch, and wheat, Triticum dicoccoides (Koern. ex Asch. & Graebner)] covering vast tracts of land across the eastern Mediterranean, are much more abundant compared with wild legumes (e.g., wild lentil and pea) as evident from seed yield data of wild populations (Harlan, 1967; Kislev et al., 2004; Ladizinsky, 1975, 1987). Surprisingly, when measured at the populated patch level, C. judaicum density values are comparable with those measured for wild emmer wheat, T. dicoccoides Aarons. (0.4–4.8 plants per m2), as recorded in Ammiad, Israel, a rich site in the heartland of wild wheat range (Noy-Meir et al., 1991b).

Microhabitat Characterization
Cicer judaicum is much more abundant in microsites with a stony component (Fig. 4). Whether the effect is exerted through soil moisture, modification of grazing pressure, competition with more aggressive species, or any combination of the above factors still remains to be determined. Similarly, in wild emmer wheat, a species with strong affinity to rocky habitats too, the major determinants of habitat preference are water availability mediated through water run-off from rocks into the soil, and a reduction in direct radiation and wind speed affecting evaporation from the soil (Noy-Meir et al., 1991a, 1991b). Presumably, in such habitats, C. judaicum may germinate early and be ensured better establishment than in more exposed and open microhabitats. In that case its microhabitat preference could be viewed as competitive release. Also, stony and rocky surface provides relative protection from cattle grazing by limiting movement, while in exposed microhabitat grazing pressure is stronger (Noy-Meir et al., 1991a).

Concluding Remarks
This work combined macroecogeographical and microecological observations aiming to analyze the factors that determine the boundaries of C. judaicum distribution and its physical population structure in Israel. No such work has ever been reported for any wild Cicer species (Berger et al., 2003). Therefore, this work represents a significant step toward better understanding of the biology of wild Cicer in general and its annual species in particular (Abbo et al., 2003). To make the above information useful for future improvement of the chickpea crop, further research is required to determine the genetic basis of the macro- and microecological preferences of this and other wild Cicer species.


   ACKNOWLEDGMENTS
 
R. Ben-David is indebted to the Israeli Gene Bank for stipend support.

Received for publication October 12, 2005.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
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