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Species richness of annual legumes in relation tograzing in Mediterranean vegetation in northernIsraelIMANUEL NOY-MEIR a & DIDI KAPLAN ba Department of Agricultural Botany, Institute of Plant Sciences, Faculty of Agricultural,Food and, Environmental Quality Sciences, The Hebrew University of Jerusalem, P.O.Box 12, Rehovot 76100, Israelb Israel Nature and Parks Authority, Northern Region, P.O. Box 631, Z.H.R. IndustrialPark, Rosh Pinna 12000, IsraelPublished online: 14 Mar 2013.

To cite this article: IMANUEL NOY-MEIR & DIDI KAPLAN (2002) Species richness of annual legumes in relation to grazing inMediterranean vegetation in northern Israel, Israel Journal of Plant Sciences, 50:sup1, 95-109

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Israel Journal of Plant Sciences Vol. 50 2002 pp. S-95–S-109

*Author to whom correspondence should be addressed. E-mail:noymeir@agri.huji.ac.il

Species richness of annual legumes in relation to grazing in Mediterranean vegetationin northern Israel

IMANUEL NOY-MEIR*,a AND DIDI KAPLANb

aDepartment of Agricultural Botany, Institute of Plant Sciences, Faculty of Agricultural, Food andEnvironmental Quality Sciences, The Hebrew University of Jerusalem, P.O. Box 12, Rehovot 76100, Israel

bIsrael Nature and Parks Authority, Northern Region, P.O. Box 631, Z.H.R. Industrial Park,Rosh Pinna 12000, Israel

(Received 10 December 2001)

ABSTRACT

Species richness of annual legumes in step-point transects was analyzed for 79 pairsof grazed and ungrazed sites of Mediterranean vegetation in northern Israel. Sev-enty-eight species of annual legumes belonging to 17 genera were sampled. Speciesrichness of all annual legumes of Medicago and Trifolium was significantly greater,by 25–42%, on the grazed compared to the ungrazed site of site-pairs. Legumerichness was significantly greater on Cretaceous and Eocene sedimentary rockscompared to younger Neogene and Pleistocene sediments, with intermediate rich-ness on basalt. It was significantly lower in sites with 400–500 mm rainfall comparedto 500–900 mm, and in wetland compared to grassland, shrubland, and woodland.Species richness of annual legumes, Medicago and Trifolium, increased signifi-cantly from zero or low grazing intensity to high intensity. A consistent, notsignificant reduction of species richness was observed at extremely high grazingintensity. Many species of small annual legumes increased in cover with grazingintensity. Erect or twining species did not show this response. The tendency ofincreased richness of annual legumes with grazing was confirmed for subhumidMediterranean communities, but it may be reversed at extremely high grazingintensities, or in semiarid communities grazed by sheep, and for some legume taxa.Management for in situ conservation of the entire annual legume flora in productiveMediterranean vegetation requires, in different parts of the landscape, continuationof intense grazing and relative protection from grazing.

INTRODUCTION

The Mediterranean basin is a major center of speciationof annual legumes (Fabaceae), including the generaMedicago (Heyn, 1963; Botanical nomenclature fol-lows Zohary and Feinbrun-Dothan, 1966–1986) andTrifolium (Zohary and Heller, 1984). Two importantroles of annual legumes in Mediterranean grassland,shrubland, and woodland ecosystems are nitrogen fixa-tion and production of protein-rich forage that is prefer-entially consumed by both wild and domestic herbi-vores. In the first millenia of agriculture (9,000 to 5,000BP), at least eight species of annual legumes were

domesticated in this region for human food (pulses) orlivestock forage (Lens, Pisum, three Vicia spp., Cicer,Lathyrus, Trigonella) (Zohary and Hopf, 1988; Smith,1995). Over the following millenia, only a few morespecies were brought into cultivation (e.g., Lupinusalbus, Trifolium alexandrinum). Some annual species ofMedicago have been mentioned as garden plants in north-ern Europe since the 16th century (Heyn, 1963).

In recent centuries, many species of annual legumesfrom the Mediterranean region were introduced to the

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New World (North and South America, Australia) byEuropean colonizers, often unintentionally. Under suit-able conditions, they naturalized, spread spontaneously,and became important components of the vegetation.The 20th century saw a “rediscovery” of the potential ofMediterranean annual legumes to produce high qualityforage for domestic animals and persist under intensivegrazing, also on poor soils and in semiarid climates, andto restore soil nitrogen levels as part of crop rotations.The most striking example is subterranean clover, Trifo-lium subterraneum, a component of Mediterraneannatural communities, naturalized and domesticated inAustralia for sown pastures (Cocks et al., 1980). Austra-lian breeders selected dozens of cultivars from thou-sands of accessions from both natural and naturalizedpopulations. Subsequently, cultivar seeds were exportedto other mediterranean climate regions. A similar pro-cess recurred in the domestication, breeding, and diffu-sion of Medicago polymorpha, M. truncatula, and abouta dozen other species of Mediterranean annual legumes.Cultivars were also experimentally reintroduced in theintensely grazed agropastoral systems of North Africaand the Near East, in the hope that they might help tostabilize and restore their productivity (Ewing, 1999).

The agricultural importance of the newly domesti-cated Mediterranean annual legume species can begauged, among other things, by the volume of publica-tions. For example, in Biological Abstracts, from Janu-ary 1989 to September 2001, there are 624 publicationsthat mention T. subterraneum, 259 for M. truncatula,and 155 for M. polymorpha. Many other wild or semi-domesticated species of Medicago, Trifolium, Vicia,Onobrychis, and other genera are mentioned in substan-tial numbers of publications.

Mediterranean annual legumes are obviously a geneticrecourse of world-wide agricultural and economic value.The in situ conservation of populations of these speciesin their native ecosystems should therefore be an objec-tive of high priority. However, among the thousands ofpublications, there are extremely few that deal directlywith the problems of management for in situ conserva-tion of annual legumes in the Mediterranean basin.There is a limited body of relevant basic research ontaxonomy, biodiversity, ecology, and population genet-ics of annual legumes in Mediterranean countries. InIsrael, Clara Heyn was a pioneer and a leader in thisfield. Her monograph on the annual species ofMedicago (Heyn, 1963) is still the standard interna-tional reference for taxonomists, ecologists, and agrono-mists. Israeli botanists also produced a monumentalmonograph on Trifolium (Zohary and Heller, 1984). Inthe 1960s and early 1970s, “Sephi” Katznelson devel-

oped an intensive research program on Israeli popula-tions of Trifolium, Medicago, and other annual legumesthat ranged from systematics and infraspecific variationand collection to breeding, Rhizobium specificity, andagronomic aspects (e.g., Katznelson, 1974). More re-cent research on annual legumes in Israel includes tax-onomy and biosystematics of the genera Lupinus, Lens,Lathyrus, and Vicia (e.g., Pazy et al., 1981; Plitmann,1981; Ladizinsky and Abbo, 1993; Plitmann et al.,1995; Gil-Ad et al., 2000).

In other Mediterranean countries, valuable informa-tion on distribution, diversity, and variability of annuallegumes has accumulated from “ecogeographic studies”that usually accompanied collection and evaluation ofgenetic material for gene banks and for breeding. Forinstance, comprehensive sampling of species diversityof annual legumes was carried out in southern Spain(Morey, 1977), in Syria (Ehrman and Cocks, 1990;1996; Kattach et al., 1998), and in Morocco (Beale et al.,1991, 1993; Bounejmate et al., 1992a,b; Cremer-Bachand Bach, 1994; El-Mzouri et al., 2000). Infra-specificvariation in natural populations was studied forMedicago polymorpha in Sardinia (Bullitta et al., 1994;Loi et al., 1995) and Tunisia (Hannachi et al., 1998), forTrifolium tomentosum in Algeria (Issolah et al., 2000),and for Trifolium spp. in Turkey (Bennett, 2000). Along-term research program on ecology and agronomyof native annual legumes has been carried out byICARDA in Syria (Russi et al., 1992a,b; Cocks, 1995;Pagnotta et al., 1997; Ghassali et al., 1998). There arealso studies on the genetic diversity of annual legumepopulations in countries where they have been intro-duced and naturalized, e.g., Australia (Fortune et al.,1995; Cocks, 1999) and Chile (Del Pozo et al., 2000).

A key issue in the in situ conservation of annuallegume germplasm in the Mediterranean basin is theeffect of livestock grazing on wild populations and onspecies diversity. Since the beginnings of domesticationof ruminants about 9,000 BP (Smith, 1995), Mediterra-nean ecosystems have been exposed to grazing bysheep, goats, and cattle. To a large extent, plant commu-nities in the region have been shaped by, and adapted tolivestock grazing (Noy-Meir and Seligman, 1979;Perevolotsky and Seligman, 1998). The traditional pas-toral systems in the region must have owed their produc-tivity and stability in great measure to the annual legumecomponent of Mediterranean rangeland. However, inthe last 60 years, there have been changes in the tradi-tional grazing systems around the Mediterranean, withdiverging trends in different parts of the region. North ofthe Mediterranean, traditional open range grazing hasdecreased in most European countries. Large areas of

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former rangeland have been abandoned and other areashave been converted to intensive agricultural systems.By contrast, in most of the countries south and east ofthe Mediterranean, livestock grazing intensity in thetraditional open range system has increased well beyondthe historical levels or those of 1900 (Noy-Meir andSeligman, 1979). There is increasingly greater relianceon supplementary feeding to cover the inevitable deficitin animal nutrition from the range. In Israel, divergingtrends can be observed in different areas. Some range-land areas have been fenced and are managed as cattleranch systems, often involving lower and less continu-ous grazing pressure than before, others have been de-clared nature reserves, and in yet other areas the openrange system prevails.

How do these changes in land use and grazing regimeaffect population dynamics and biodiversity of annuallegumes in their home ecosystems? Are there dangers ofdiversity loss and genetic erosion of legumes in thischanging Mediterranean landscape? How can grazing bemanaged to minimize these dangers and to optimize theconservation of this genetic resource and its diversity?

This paper presents an analysis of data that are rel-evant to these questions, that were obtained in a studydesigned to evaluate the effects of grazing intensity andprotection from grazing on species diversity and compo-sition in nature reserves and adjacent rangeland innorthern Israel.

MATERIALS AND METHODS

Study area

The study area in its broadest sense was the northeasternpart of Israel, including parts of the Galilee and Golanregions as well as Mt. Gilboa (Fig. 1). The climate istypical Mediterranean. Mean annual rainfall in the re-gion varies between 400 and 900 mm, restricted to thesix cooler months of the year with a peak in December–January. Mean temperatures within the region vary be-tween 6 and 14 °C in January and between 23 and 30 °Cin July. The dominant landforms are rocky mountains,hills, and plateaus; the valleys between them are mostlyunder cultivation. The geological and lithological for-mations are diverse. Hard limestone formations of theUpper Cretaceous and Eocene age are dominant in Gali-lee, west of the Jordan River and Lake Kinneret (Sea ofGalilee), while Pleistocene basalt covers most of theGolan on the east. The natural or semi-natural vegeta-tion formations are closely associated with geology.Grasslands and grassy open woodlands are typicallyassociated with basalt in the Golan and on the Korazim

Plateau, and with Eocene limestone on Mt. Kenaan, Mt.Gilboa, and a few other enclaves. On Upper Cretaceoussedimentary rocks in the Mt. Miron block, the prevail-ing climax vegetation is a closed tall sclerophyllousscrub (maquis) dominated by Quercus calliprinos.Where this has been totally or partially cleared, thesuccessional stages in the open patches are dominatedby shrubs (garrigue) or dwarf shrubs (batha), withpatches of herbaceous vegetation between them. A fewnatural wetland areas have been preserved, mainly in theBeth-Saida valley northeast of Lake Kinneret.

The traditional open range grazing system by mixedherds of cattle, sheep, and goats persists in some parts ofthe region, mostly in common grazing lands aroundArab villages. Most of the remaining non-arable range-land is now fenced for commercial grazing, usually bycattle, or, in some cases, sheep or goats. The network ofnature reserves established since the 1960s includes afew large reserves (e.g., Mt. Miron, Yahudiya) andmany smaller ones (Fig. 1) that between them cover avariety of landforms and plant communities. Grazing ispermitted in some parts of the reserves by contracts withherd owners. The need to define criteria for grazingmanagement within nature reserves was the originalmotivation for a monitoring and research program, par-tial results of which are reported here.

Sites sampled

All the sites sampled in this study are fence-contrastsite-pairs, each consisting of a small exclosure orungrazed area (protected sites) and a comparable sitejust outside the exclosure fence (grazed sites) withingrazed paddocks. Most of the exclosures were withinnature reserves, and were fenced between 1981 and1985 in order to obtain information on the effect of thecurrent grazing management or of protection from graz-ing on the vegetation of the reserve. In addition, thestudy included site-pairs outside nature reserves, con-trasting protected sites that had been intentionally orincidentally fenced off (between 1960 and 1985) withadjacent grazed areas or contrasting areas with differentgrazing regimes. Some of the older sites had beensampled in 1982–83 (Noy-Meir et al., 1989). Cattlewere the dominant herbivore in 64 (81%) of the grazedsites. The rest of the sites were grazed by sheep (10%),goats (3%), or only by wild gazelles (Gazella gazellagazella, 6%). The latter sites were in the Haon Escarp-ment nature reserve (see also Kaplan, 1992).

At each site, grazing intensity (GI) was estimated ona scale from 0 to 5, based on signs of plant utilization,trampling, and dung accumulation (Noy-Meir etal., 1989). The six classes can approximately be associ-

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Fig. 1. Map of the study area, withboundaries of declared or approvedNature Reserves.

ated with actual grazing intensities, expressed incow-equivalent × grazing days ha–1 y–1 (CGD/HY), asfollows:

GI Grazing intensity CGD/HY

0 None 01 Low <1202 Moderate 120–1803 High 180–2404 Very high 240–3005 Extremely high >300

Though some sites were sampled repeatedly in dif-ferent years, the results presented here include only datafrom 1989, in which the largest sampling effort wasconcentrated. The full set of sites sampled in 1989 in-cluded 158 sites in 79 fence-contrast site-pairs. In 61 ofthe site-pairs, the fence had been established 4 to 9 years

before sampling; in 8 site-pairs, 10–19 years; and in 5site-pairs, 20–28 years. For some types of statisticalanalysis, we removed the sites in which the main herbi-vore was not cattle, sites in which both sides of the fencewere grazed but at different intensities or by differentherbivores and a few sites where the design was differ-ent from the standard across-fence site-pair. Therestricted set that resulted was a statistically more ho-mogeneous sample including 55 site-pairs (110 sites),each consisting of an ungrazed exclosure and an adja-cent site, grazed by cattle.

Sampling method

A rapid step-point transect method was developed toestimate plant cover and species composition in theprotected and grazed site of each site-pair. The surveywas carried out by teams of two persons: An observer

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with a good knowledge of the local flora and a recorderaccompanying him carrying a palmtop computer. Theobserver paced approximately 500 steps along imagi-nary random lines across the site, or along the fence andat least 1 m distant from it. At a every step a thin metalrod was lowered randomly through the herbaceous veg-etation. At each one of the points, the observer calledout the identity of the species touching the rod and therecorder wrote it on the palmtop, using a predeterminedspecies code consisting of two letters for common spe-cies and six letters for rare species. The data were down-loaded from the palmtop to a PC for storage and analy-sis. This method allowed a team to sample a site in 45 to60 minutes and a site-pair in double that time. All site-pairs were sampled within the spring flowering peak ofthe herbaceous vegetation, between late March andearly May. Though several observers participated in thesurvey, grazed and ungrazed sites of the same site-pairwere always sampled by the same observer. The observ-ers trained together in identifying species in the field.Samples of all species, and especially uncommon ordoubtfully identified species, were collected and stuckon cards to form a field mini-herbarium. Observers metto compare this material and unify the nomenclaturewhere necessary.

The cover of a species in a site was estimated fromthe number of points that hit this species divided by thetotal number of points sampled at the site. Since the totalnumber of points was about 500, species with coverequal to or greater than about 1/500 = 0.2% had areasonable chance to be included in the sample.

The measure of species diversity used in this studywas species richness S, of all annual legumes or a sub-set, defined as the number of species present in a steppoints sample. A calculation considering the area andfoliage density characteristic of annual legume plantssuggests that this would be approximately equivalent tothe number of species present in a cumulative area ofbetween 1 and 4 m2. The species richness on the grazedsite (or more intensely grazed site) of a site-pair wasdenoted as S(g) and the species richness on the protected(or less intensely grazed) site as S(f). The differencebetween the two values, DS = S(g) – S(f) is the grazingdifferential species richness, i.e., the excess of the num-ber of species on the grazed site when positive and thedeficit of the number of species on the grazed site whennegative.

Statistical analysis

Full set (158 sites)Both non-parametric (Kruskal-Wallis test, Sokal and

Rohlf, 1981) and conventional analysis of variance(F-test) were used to test for differences in legume

species richness between geological formations, rainfall(categorized in three classes), vegetation formations, orgrazing intensity classes. Where the tests were signifi-cant (p < 0.05), the Tukey-Cramer HSD (Sokal andRohlf, 1981) test was used for multiple comparisonsbetween classes. The joint effects of geology and graz-ing intensity (both highly significant as single factors)were analyzed in a two-factor least squares general lin-ear model analysis. In the case of significant F-tests, theproportion of variance accounted for by the model wasestimated by the adjusted R2.

The paired t-test and the signed rank test were used totest whether the mean difference in species richnessover site-pairs (N = 79) between the grazed and pro-tected sites (or more and less intensively grazed sites),DS, was significantly different from zero.

Restricted set (110 sites)The same tests used for the full set were applied also

to the restricted set. They gave qualitatively similarresults, but with reduced statistical power due to thesmaller sample size, especially of sites with high graz-ing intensity, and are not presented here in full. Theadvantage of the restricted set was that DS had a simplerbiological meaning, i.e., the difference in species rich-ness between a site grazed by cattle and an ungrazedsite. The paired t-test testing whether DS is significantlydifferent from zero, and the effect of grazing intensityon DS, are presented for the restricted set (N = 55 site-pairs).

Individual speciesThe response of the cover of individual species to

grazing was evaluated in different ways:

1. Plotting mean cover in classes of grazing intensityagainst GI, and testing for existence of significantdifferences in cover between GI classes by theKruskal-Wallis test.

2. The same but aggregating the six GI classes into twoor three larger classes (0–2 vs. 3–5 or 0/1–2/3–5).

3. Testing whether the mean, over site-pairs, of thedifference in cover between the grazed and theungrazed site was significantly different from zero,using the Wilcoxon signed rank test.

The first two tests were applied to the full set of 158sites, while the latter test was applied to the restricted setof 55 site-pairs.

RESULTS

Species set

In the total set of 158 sites, 78 species of annual legumesbelonging to 17 genera were sampled at least once by

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the point-lines. The most important genera were Trifo-lium, with 25 species, and Medicago, with 14 species.Then followed Trigonella and Vicia with 7 species each,and Lathyrus with 6 species. Other genera were repre-sented by 3 species or fewer (Melilotus, Onobrychis,Ononis, Coronilla, Astragalus, Hippocrepis, Hymen-ocarpos, Lupinus, Pisum, Scorpiurus, Tetragonolobus,and Tripodion (=Anthyllis, Pseudoanthyllis).

Mean species richness and grazing difference

In the full set of 158 sites, the mean species richness Swas 6.51 species of annual legumes, and the median was6 species. The lowest number of legume speciessampled in a site was 1 and the maximum was 18 (in asite grazed by sheep in the Mt. Miron area). In therestricted set of 110 sites, contrasting sites grazed bycattle with ungrazed sites, the mean of S was 6.37 andthe median was 6, similar to the full set. In the restrictedset, the minimum number of species was 1 and themaximum 17.

In the restricted set of 55 site-pairs, the mean annuallegume species richness in sites grazed by cattle was7.38 compared to 5.36 in paired ungrazed sites (Table1). The difference in DS was +2.02 species, i.e., in37.7% in favor of grazed sites. This difference washighly significant (p < 0.001) by both conventional andnon-parametric tests for paired samples (Table 1).

In the full set of 79 site-pairs, the results for allannual legumes were very similar to those obtained inthe restricted set. Though the mean difference betweenless and more intensely grazed sites was slightly lessthan in the restricted set, +1.71 species (30%), it washighly significant (Table 1). In this set, the greatersample allowed separate analyses for the most important

genera. The genus Trifolium accounted for 50% of themean total richness of annual legumes, Medicago for16%, Vicia for 6%, and the remaining 14 genera for28%. The species richness of Medicago, Trifolium, and“others” was highly significantly greater in the grazed(or more intensely grazed) sites of site-pairs. The rela-tive increase in richness associated with grazing in thesetaxa varied between 25% and 42%. The species richnessof Vicia was not associated with grazing.

For all site-pairs in the restricted set (N = 55), therewas a strong correlation between species richness on thegrazed S(g) and the protected side S(f) of the fence. Alinear regression equation was highly significant, withp < 0.0001 and R2 = 0.65:

S (g) = 1.89 + 1.02 * S (f)

The intercept (1.89) that was significantly differentfrom zero (p = 0.0057) and the slope of almost 1 indicatethat the additional number (about 2) of legume speciesin the grazed site of each pair does not depend on thespecies richness of the protected site. This was con-firmed by the complete lack of a significant linear rela-tion (p = 0.8212) between DS and S(f) of the protectedsites.

Effects of ecological factors on species richness

The effects of ecological factors on species richness ofannual legumes were analyzed using the means of rich-ness for site-pairs in the full set of 79 site-pairs.

GeologyAn analysis of variance by five geological forma-

tions showed that the species richness of annual legumeswas substantially and significantly greater in sites on

Table 1Species richness per site of all annual legumes and by subsets: means and grazing difference DS. Significance tests refer to the

null hypothesis that DS = 0. In bold, tests and cases where DS is significantly different from zero (p < 0.05)

Set of sites Restricted set Full set Full set Full set Full set Full setSet of species All All Medicago Trifolium Vicia Others

Number of site-pairs 55 79 79 79 79 79

Species richness S Mean of S(f) and S(g) 6.37 6.51 1.09 3.25 0.37 1.80

S(f): ungrazed/less grazed 5.36 5.66 0.90 2.89 0.35 1.52

S(g): grazed/more grazed 7.38 7.37 1.28 3.61 0.39 2.09

Grazing difference +2.02 +1.71 +0.38 +0.72 +0.04 +0.57 DS = S(f) – S(g)

p (t-test: DS = 0) <0.0001 <0.0001 0.0005 <0.0001 0.5670 0.0021p (Signed Rank: DS = 0) 0.000 0.000 0.000 0.000 0.592 0.002

Mean % increase 37.7 30.2 42.3 25.0 10.7 37.5 DS/S(f)

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Cretaceous and Eocene sedimentary rock (mostly lime-stone), compared to sites on younger sediments of boththe Neogene (sandstone and chalk) and the Pleistocene(marl and recent alluvial) (Table 2a). Similar differ-ences were observed for Medicago and Trifoliumspecies richness. Sites on basalt were intermediate inspecies richness in the three cases, but were not signifi-cantly different from the younger sediments. There wereno significant differences in Vicia species richness be-tween geological formations, though it was slightlyhigher on basalt than on other formations. There was anonly marginally significant effect of geology on thenumber of “other” legume species.

In no case was there a significant difference betweenCretaceous (mostly Cenoman-Turonian) and Eocenelimestone, nor between Neogene and Pleistocene sedi-ments. Therefore, these formations were grouped as“old sediments” and “young sediments”, respectively.An analysis of geology by the resulting three classesgave similar but somewhat sharper results than thoseobtained with five classes (Table 2b). Sites on old sedi-mentary rocks were significantly richer in species of allannual legumes, of Medicago, and of Trifolium compared

to sites on both young sediments and basalt. Sites onbasalt were significantly richer in Trifolium speciescompared to young sediments. Species richness of“other” legumes was significantly greater on old sedi-ments compared to basalt, and intermediate but not sig-nificantly different on young sediments.

RainfallSites with low rainfall (<500 mm) had significantly

lower species richness of all annual legumes, of Medi-cago, and of Trifolium compared to sites with medium(500–700 mm) rainfall and (except for Medicago) com-pared to sites with high (>700 mm) rainfall (Table 3).There was no significant difference between the me-dium and high rainfall classes in these three species sets,though Medicago richness was substantially greater inthe medium rainfall class. Vicia species richness washighest in high rainfall (>700 mm) sites, but the effectdid not reach significance. Richness of other legumespecies showed no relation to rainfall.

VegetationWetland sites had substantially and significantly

lower species richness of all annual legumes, of

Table 2Mean species richness S per site of all annual legumes and by subsets, by geological formations, in the full set of 79 site-pairs: a.5 geological classes, b. 3 classes. Significance tests refer to the null hypothesis that there is no difference between classes.N—number of site-pairs in class. In each column, values that do not have letters in common are significantly different by theTukey-Cramer HSD test (p < 0.05). In bold, tests that are significant (p < 0.05) and values of S that are significantly the greatest

in each column

a. N S S S S SSpecies set All Medicago Trifolium Vicia Others

Geology (5 classes)Old sediments

Cretaceous 12 8.42 ab 1.33 ab 4.58 a 0.33 2.17Eocene 23 8.52 a 1.76 a 4.15 a 0.33 2.28

Young sedimentsNeogene 8 3.50 c 0.38 b 1.25 b 0.19 1.69Pleistocene 7 4.00 c 0.29 b 1.21 b 0.36 2.14

Basalt 29 5.57 bc 0.84 b 3.02 ab 0.48 1.22

p (Kruskal-Wallis) 0.0002 0.0002 <0.0001 0.7915 0.0311p (F) 0.0002 0.0002 <0.0001 0.6106 0.0625

Adjusted r2 0.22 0.21 0.30 0.00 0.06

b. N S S S S SSpecies set All Medicago Trifolium Vicia Others

Geology (3 classes)Old sediments 35 8.49 a 1.61 a 4.30 a 0.33 2.24 aYoung sediments 15 3.73 b 0.33 b 1.23 c 0.27 1.90 abBasalt 29 5.57 b 0.84 b 3.02 b 0.48 1.22 b

p (Kruskal-Wallis) <0.0001 <0.0001 <0.0001 0.5011 0.0075p (F) <0.0001 <0.0001 <0.0001 0.3168 0.0137

Adjusted r2 0.24 0.21 0.32 0.01 0.08

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Medicago, and of Trifolium, compared to upland sites(Table 4). Vicia species richness showed no such trendand for other legumes it was indicated but not signifi-cant. There were no significant differences in speciesrichness between upland vegetation formations domi-nated by herbaceous (grassland and open woodland) andby woody plants (batha, garrigue, and maquis).

Effects of grazing intensity on species richness

The effects of grazing intensity on species richness wereanalyzed in the full set of 158 sites. The species richnessof annual legumes was highly significantly related tograzing intensity (GI) estimated in the field on a scalefrom 0 to 5. Diversity was lowest (about 5 species) inungrazed sites (GI = 0), increasing gradually with in-creased grazing intensity to a maximum (11 species) athigh and very high grazing intensity (GI = 3 and 4)(Table 5, Fig. 2). In sites with extremely high grazingintensity (GI = 5), there was a decrease in mean legumerichness compared to the latter intensities. However,because of the small number of sites with GI = 5 andtheir high variability, richness at this grazing intensitywas not significantly different from that at any othergrazing intensity.

The richness of Medicago, Trifolium, and “other”legumes responded to grazing intensity significantlyand in a form similar to the total annual legume richness,i.e., a maximum at high and very high intensity (Table 5,Figs. 3,4). There were slight differences in the responsefunction. Medicago species richness remained low fromno grazing to moderate (GI = 2) grazing and then in-creased suddenly for high (GI = 3) grazing intensity.Grazing intensity accounted for a higher proportion ofvariance in richness for Medicago (24%) than for anyother group. Trifolium species richness increased moregradually and slowly with grazing intensity, and thiswas the case also with “other” legumes. All three groupsshowed the decline of richness at extremely high graz-ing intensity but it was significant only for “other”legumes. Vicia species richness was not significantlyrelated to grazing intensity.

Effects of grazing intensity on difference in speciesrichness associated with grazing

In the restricted set of 55 site-pairs, where one side ofthe fence was ungrazed and cattle grazed on the otherside, the across-fence difference in annual legume speciesrichness, DS, was related to grazing intensity on the

Table 3Mean species richness S per site of all annual legumes and by subsets, by rainfall classes, in the full set of 79 site-pairs. Notation

as in Table 2

N S S S S SSpecies set All Medicago Trifolium Vicia Others

Rainfall <500 mm 32 4.69 b 0.53 b 2.19 b 0.28 1.69 500–700 mm 29 7.83 a 1.71 a 3.81 a 0.33 1.98 >700 mm 18 7.64 a 1.08 ab 4.22 a 0.61 1.72

p (Kruskal-Wallis) 0.0013 <0.0001 0.0002 0.1295 0.6741p (F) 0.0010 <0.0001 0.0002 0.0677 0.6954

Adjusted r2 0.14 0.23 0.18 0.04 0.00

Table 4Mean species richness S per site of all annual legumes and by subsets, by vegetation formations, in the full set of 79 site-pairs.

Notation as in Table 2

N S S S S SSpecies set All Medicago Trifolium Vicia Others

Vegetation Batha + Garrigue + Maquis 13 7.96 a 1.38 a 4.15 a 0.42 2.00 Grassland + Open woodland 57 6.77 a 1.18 a 3.33 a 0.37 1.89 Wetland 9 2.78 b 0.11 b 1.39 b 0.33 0.94

p (Kruskal-Wallis) <0.0001 0.0009 0.0021 0.8937 0.1106p (F) 0.0027 0.0078 0.0033 0.9117 0.1486

Adjusted r2 0.12 0.10 0.12 0.00 0.02

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grazed side (Fig. 5). The grazing-associated speciesrichness increased steadily from low (GI = 1) to high(GI = 3) grazing intensity, consistent with the responseto grazing intensity obtained in the full set of sites. Thedata also indicate a decline in DS when the grazingintensity is extremely high, but the small samples ofsites in this set in the classes “very high” (GI = 4) and“extremely high” (GI = 5) grazing intensity leave a verywide range of error. In any case, when data from veryand extremely high grazing intensity are pooled, theoverall differences in DS associated with grazing inten-sity (5 classes) are significant (Kruskal-Wallis test,p = 0.0229).

Joint effects of geology and grazing intensity onspecies richness

The habitat factor that had the strongest effects onlegume species richness variables was the geologicalformation. Therefore, the joint effects of geology (3classes) and of grazing intensity (6 classes) on richnesswere analyzed in a two-factor least squares general lin-ear model analysis, in the full set of 158 sites. Theresults (Table 6) showed that in the additive two-factormodel both the geology effect and the effect of grazingintensity remained significant (and in most cases highlysignificant) for total legume, Medicago, Trifolium and

Table 5Mean species richness S per site of all annual legumes and by subsets, by grazing intensity (GI) classes on a 0 to 5 scale in the full

set of 158 sites. Notation as in Table 2

N S S S S SSpecies set All Medicago Trifolium Vicia Others

GI Grazing intensity0 None 68 5.31 c 0.76 b 2.71 b 0.38 1.46 b1 Low 38 6.00 c 0.89 b 3.00 ab 0.39 1.71 ab2 Moderate 28 7.21 bc 1.00 b 3.68 ab 0.32 2.21 ab3 High 10 11.20 a 2.60 a 4.80 a 0.60 3.20 a4 Very high 8 10.88 ab 2.75 a 5.13 a 0.13 2.88 ab5 Extremely high 6 6.50 abc 1.67 ab 3.83 ab 0.33 0.67 b

p (Kruskal-Wallis) <0.0001 <0.0001 0.0052 0.4976 0.0019p (F) <0.0001 <0.0002 0.0022 0.6591 0.0018

Adjusted r2 0.16 0.24 0.09 0.00 0.09

Fig. 2. Means ± standard errors (lines) of annual legumespecies richness S by six classes of grazing intensity, in the fullset of 158 sites.

Fig. 3. Means ± standard errors (lines) of Medicago speciesrichness by six classes of grazing intensity, in the full set of158 sites.

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Fig. 5. Means ± standard errors (lines) of the difference inannual legume species richness, DS, between sites grazed bycattle and ungrazed sites in the restricted set of 55 site-pairs,by five classes of grazing intensity on the grazed site.

other legumes species richness. The proportion of vari-ance accounted for (adjusted R2) increased in generalcompared to the levels obtained based on either geologyalone (Table 2) or grazing intensity alone (Table 5).Both geology and grazing effects remained non-signifi-cant for Vicia species richness in the two-factor model.

The geology × grazing interaction effect could not beevaluated in the general linear model because not allcombinations of geology and grazing intensity occurredin the data set. However, the lack of fit test indicated thatthere remained no significant interaction variation. Siteswere grouped, according to the geological formation,into infertile (Cretaceous and Neogene) and fertile soils(all others). No differences were detected in the re-sponse of species richness to grazing between the twogroups. Infertile sites were fewer and did not sustain ashigh grazing intensities as some fertile sites.

Individual species responses to grazing

In the present study, the distribution of 20 species ofannual legumes suggested a positive response to grazing

Fig. 4. Means ± standard errors (lines) of Trifolium speciesrichness by six classes of grazing intensity, in the full set of158 sites.

Table 6Statistics of additive general linear model for species richness per site of all annual legumes and by subsets, in relation to geology

(3 classes) and grazing intensity (6 classes) in the full set of 158 sites. (Significant effects in bold)

General linear model with geology S S S S Sand grazing intensity (additive) All Medicago Trifolium Vicia Others

p — Geology (3 classes) <0.0001 <0.0001 <0.0001 0.0950 0.0036p — Grazing intensity (6 classes) 0.0001 <0.0001 0.0331 0.4699 0.0030Adjusted r2 0.30 0.36 0.31 0.01 0.14

(Table 7). Such a response was indicated by greatercover in grazed (or more intensely grazed) sites com-pared to ungrazed (or less intensely grazed) sites, thatwas significant by at least one of the tests used and inone of the data sets. Seven species showed a significantpositive response by all tests used. Three of these sevenspecies were identified as consistent grazing increasersalso in a previous study, based on a smaller sample offence contrast site-pairs taken in 1982–83 in the sameregion (Noy-Meir et al., 1989), and in other unpublishedwork. Four species of Trifolium that were identified asgrazing increasers in the previous study did not show asignificant response in the present data set. The list of 24species that showed a positive response in the present orin previous studies included 12 species of Trifolium and6 of Medicago, and single species of Astragalus,Coronilla, Hymenocarpos, Onobrychis, Scorpiurus, andTripodion (former Anthyllis or Pseudanthyllis).

The strongest positive response to grazing intensitywas found for Trifolium pilulare, a common species thatwas present in 43% of the sites. Its cover was very low

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Table 7Groups of annual legume species for which there is evidence for positive, intermediate and negative responses to grazing.Species in bold indicates a significant response that was found in the present study; an asterisk indicates the response wasreported by Noy-Meir et al. 1989. ?—indicates a conflicting or doubtful response. Species listed that are not in bold and do not

have an asterisk were classified according to unpublished results

Positive response to grazing Intermediate response to grazing Negative response to grazing

Astragalus hamosus Trifolium purpureum* Lathyrus aphaca*Coronilla scorpioides Trifolium vavilovii*? Pisum fulvumHymenocarpos circinnatus* Vicia palaestinaMedicago orbicularis Vicia seriocarpaMedicago granadensisMedicago polymorphaMedicago rotata*Medicago scutellataMedicago turbinataOnobrychis squarrosaScorpiurus muricatusTrifolium argutum*Trifolium clusiiTrifolium clypeatumTrifolium dasyurum*Trifolium nigrescens*Trifolium pilulare*Trifolium resupinatumTrifolium spumosumTrifolium stellatum*Trifolium subterraneumTrifolium tomentosum*Trifolium vavilovii ?Tripodion tetraphyllum

in ungrazed to moderately grazed sites and rose sharplyto a maximum at very high grazing intensity (GI = 4,Fig. 6). Even this species showed a relative reduction incover at extremely high grazing intensity (GI = 5).Similar response profiles, with peaks of cover at high orvery high grazing intensity (GI = 3–4), were found forother grazing increaser species.

In this study, no annual legume species showed asignificant negative response to grazing, though at leasttwo species tended to be less abundant in intensely(GI = 3–5) grazed sites compared to ungrazed or lightlygrazed (GI = 0–2) sites (Lathyrus aphaca, Viciapalaestina). Evidence from other work (Noy-Meir et al.,1989, and unpublished) confirms that both those and atleast two additional twining annual legume species at-tain higher cover in ungrazed or lightly grazed sites(Pisum, Vicia spp.). In general, those legume speciesthat indicate a tendency to decrease with grazing intensityare too infrequent in the sample to allow a strong test.

Trifolium purpureum was the most common legume

Fig. 6. Means ± standard errors (lines) of Trifolium pilularepercentage cover by six classes of grazing intensity, in the fullset of 158 sites.

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species in the sample (present in 61% of sites) butshowed neither positive nor negative consistent differ-ences in cover in relation to grazing intensity. In thestudy conducted in 1982–83, the varying responses of thisspecies in different sites suggested a modal response, withhighest cover at intermediate grazing intensities (Noy-Meir et al., 1989). Though the modal response could notbe positively confirmed in this study, the classification ofT. purpureum as a species with an intermediate or in-consistent response to grazing was confirmed.

DISCUSSION

Effects of ecological factors

The ecological factor that showed the strongest associa-tion with species richness of annual legumes and ofmajor legume genera was the geological formation. Thehighest legume richness was found in sites on old sedi-mentary rocks, compared to sites on basalt or onyounger sediments. Most of the former sites are onshallow red soils (terra rossa, Xerochrept) among abun-dant outcrops of hard limestone and dolomite. However,this group is edaphically not homogeneous. Terra rossasoils formed on hard rocks of the Upper Cretaceous(Cenomanian and Turonian) in Galilee are typicallyinfertile, with very low levels of available phosphorusand low productivity of the herbaceous layer (Henkin etal., 1996). Phosphorus fertilization on these soils re-sulted in a substantial increase in biomass, in cover ofannual legumes, and in species richness of this group(Henkin et al., 1998, and unpublished). By comparison,terra rossa soils on limestone and chalk of the Eoceneshow higher natural levels of available phosphorus andsupport denser herbaceous vegetation (Rabinovich-Vinand Orshan, 1974). Despite this difference in phospho-rus availability, both Eocene and Cretaceous formationshad equally high legume richness in this study. Appar-ently, many annual legume species are present in thecommunity on infertile Cretaceous soils, though they donot attain their potential abundance until phosphorusenrichment occurs. The stony black soils (Proto-grumusol) on basalt are richer in phosphorus and innitrogen compared to both types of terra rossa, allowingthe development of highly productive herbaceous com-munities dominated by grasses (Gutman and Seligman,1978). The lack of nitrogen limitation and the high grassproductivity can explain the relatively lower richness oflegumes on basalt (except Vicia). Even lower legumerichness was found on two young sedimentary forma-tions that probably represent two ecological extremes.Soils on Pleistocene sediments are fine-textured, oftenoccur in wet sites, and the herbaceous community isdense and dominated by a few species. Soils on Neo-

gene chalk and sandstone east of Lake Kinneret havelow herbaceous productivity, being either dry or infer-tile. No evidence was found in this study for the reversalof the effect of grazing on species richness in nutrientpoor soils (Proulx and Mazumder, 1998).

There are few data from other Mediterranean coun-tries with which to compare these results. In Morocco,species richness of Medicago was positively correlatedwith available phosphorus content, but an opposite trendwas observed for Trifolium (Bounejmate et al., 1992b;Beale et al., 1993). The slight (not significant) discrimi-nation observed here in the richness of the two generabetween Eocene (high P) and Cretaceous (low P) forma-tions (Table 2a) is at least consistent with this trend.

Species richness of legumes was significantly lowerin the drier part of the region, with 400–500 mm rainfall,but did not vary consistently over the rest of the rangefrom 500 to 900 mm. This probably reflects the reducedplant cover in the drier sites (which include most of theNeogene sites) and the fact that some species of annuallegumes reach an ecological limit there. A reduction inannual legume species diversity as rainfall decreases inthe range below 500 mm has also been reported fromother Mediterranean countries (Ehrman and Cocks,1990; El-Mzouri et al., 2000). There were subtle (notsignificant) differences between genera in the responseto rainfall, suggesting that the rainfall levels where theyreach their maximum species richness are rankedMedicago < Trifolium < Vicia. This is consistent withfindings from Morocco, where Medicago species weremost frequent in an intermediate rainfall zone (300–600 mm), while Trifolium species were most frequent inthe high rainfall zone (>500 mm) (Bounejmate et al.,1992b; Beale et al., 1993). In Syria, most Trifoliumspecies were found to prefer higher rainfall areas(Ehrman and Cocks, 1990).

Wetland sites were substantially poorer in species ofannual legumes, and particularly of Medicago and Tri-folium, compared to upland sites dominated by eitherwoody or herbaceous vegetation. Though a few special-ized species of legumes (e.g., Melilotus spp.) can beabundant in these sites, the humid and highly competi-tive conditions are not favorable for the larger group ofsmall legumes.

Effects of grazing

Two apparently contrasting lines of evidence can befound in the literature concerning the effects of live-stock grazing on abundance and species richness ofannual legumes in ecosystems of the Mediterraneanbasin. The plant functional type “annual legumes” andindividual species within it, have often been found to bemore abundant in grazed grassland sites compared to

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sites protected from grazing (Noy-Meir et al., 1989;Hadar et al., 1999; Noy-Meir and Sternberg, 1999;Sternberg et al., 2000). This is consistent with the hy-pothesis that grazing reduces the cover, height, andbiomass of the dominant tall grasses and forbs (particu-larly in productive grassland) and allows the establish-ment and regeneration of small annuals, including mostlegume species (Noy-Meir et al., 1989). According tothis hypothesis, we would expect species richness ofannual legumes to increase with increasing grazing in-tensity.

On the other hand, concern has been expressed thatcontinued and accelerated overgrazing of rangeland inthe Mediterranean basin could result in “genetic ero-sion” and species extinction of annual legumes(Bounejmate et al., 1992; Beale et al., 1993; El-Mzouriet al., 2000). These authors present indirect evidencethat this process has already begun in some areas. Thehypothesis is that the current grazing intensity in largeareas of Mediterranean rangeland (mainly in the southand east of the region) exceeds the grazing tolerance ofmany populations of annual legumes.

The results obtained in the present study on the rela-tionship between annual legume species richness andgrazing intensity are relevant to both conflicting hypoth-eses and suggest a way in which they may be integrated.The results confirm earlier findings from subhumidMediterranaean grasslands that species richness of an-nual legumes, of Medicago and Trifolium, and cover ofmany individual legume species, all increase steadilywith grazing intensity from zero (no grazing) to high orvery high grazing intensity. However, there is one fea-ture of the results that justifies the concern about geneticerosion by overgrazing. Species richness of all annuallegumes and of subsets, and cover of individual species,decreased sharply in the category labelled “extremelyhigh grazing intensity”, with >300 CGD/HY, equivalentto mean yearlong density of >80 cows km–2. Though thesample in this category was small and the decreasetherefore not significant, this result indicates that eventhe tolerance of small annual legumes (e.g., Trifoliumpilulare) to grazing is not unlimited. The declining trendat the highest intensities was probably only weakly ex-pressed in our sample for two reasons. First, most of thesites were grazed by cattle, known to be more limited intheir ability to feed on small prostrate plants comparedto sheep or goats. Second, all of our sites were in therainfall zone of >400 mm, with reasonable growth con-ditions in most years. A decrease in legume speciesrichness was observed in our data already in the 400–500 mm class. A further decrease in legume speciesrichness in the range from 400 mm down to 200 mmrainfall can be expected and has been observed in some

Mediterranean areas (e.g., Ehrman and Cocks, 1990; El-Mzouri et al., 2000). In the semiarid Mediterranean,where the ecological conditions are marginal for manyspecies of annual legumes, their populations can also beexpected to be more susceptible to damage by intensegrazing by sheep and goats, the dominant herbivores inthis zone. Indeed, in a semiarid site with 300 mm insouthern Israel, protection from sheep grazing resultedin significant increases in plant and seed density ofannual legumes (Osem et al., 1999). A difference be-tween subhumid and semiarid ecosystems, both with along history of grazing, in the response of annual le-gume species diversity to actual grazing intensity,would be consistent with the hypotheses of bothMilchunas et al. (1988) and Proulx and Mazumder(1998).

Responses of individual species

The traits that are most strongly associated with re-sponse to grazing in the general species assemblage inMediterranean grassland are growth habit and height(Noy-Meir et al., 1989; Noy-Meir and Sternberg, 1999).The results from this study suggest that this is the casealso within the annual legumes set. The 24 species ofannual legumes for which a positive response to grazing(over most of the range of intensities) was indicated inthis or in previous studies, are mostly plants with low(<15 cm), decumbent, or prostrate growth habits. Someof them have a plastic growth habit and grow eitherdecumbent or erect, depending on the surrounding veg-etation (e.g., Medicago turbinata, Onobrychis squar-rosa). An intermediate response to grazing was indi-cated for Trifolium purpureum, the only annual legumecommon in the region that grows erect and potentiallytall (up to 60 cm) but also shows plasticity in growthhabit. The only annual legumes for which a negativeresponse to grazing was indicated (more clearly in otherstudies than in the present one) are twining species ofVicia, Lathyrus, and Pisum. The twining habit is advan-tageous in foraging for light in dense tall canopies thatdevelop in ungrazed grassland and in grazing refugesamong rocks, but is highly susceptible under intensivegrazing.

A second factor that may be involved in the positiveresponse of many annual legume species to grazing isseed dispersal traits. Some of the species that increasewith grazing have spiny pods that favor external dis-persal by livestock (Onobrychis, Scorpiurus and severalMedicago species), in addition to hard seeds that allowendozoochoric dispersal in most annual legumes. A sub-stantial proportion of seeds of annual legumes con-sumed by sheep pass through the digestive track withoutbeing damaged and their germination rate often increases

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(Russi et al., 1992b). A higher rate of recovery wasobserved in species with smaller seeds (Ghassali et al.,1998). By contrast, Trifolium subterraneum buries itspods and they are not readily available to grazers.

Implications for in situ conservation and grazingmanagement

The present study presents strong evidence that totalprotection from grazing in subhumid Mediterraneancommunities even for only a few years does reducespecies richness of annual legumes, and that this groupattains maximum richness at fairly high grazing intensi-ties. Thus, the continuation of intense grazing in largeareas, including—if necessary—parts of nature re-serves, is a positive factor for the in situ conservation ofviable populations of many species in this ecologicallyand economically important group. This recommenda-tion is particularly relevant in Mediterranean regionswhere, for socio-economic reasons, livestock grazing isdisappearing from large parts of the landscape. On theother hand, the results suggest that extremely high graz-ing can result in a loss of legume diversity, and that thein situ conservation of some annual legume species mayrequire their complete or partial protection from grazingin at least a part of their range of occurrence. This isparticularly urgent in those Mediterranean regionswhere social and economic factors induce increasinglyintensive agropastoral use of rangeland. The particulargeopolitical position of Israel has so far allowed thecoexistence of different land use systems, which fortu-itously tended to favor conservation of the full range ofthe Mediterranean annual legume flora. However, habitatdestruction by urbanization and changing land use pat-terns may erode these circumstances in the future. Moni-toring and intervention of conservation authorities in man-agement of nature reserves and other areas will still benecessary to preserve this valuable genetic resource.

ACKNOWLEDGMENTS

The original research was financed in 1989–90 by agrant from the Israel Nature Reserves Authority (nowthe Israel Authority of Nature and Parks). We are verygrateful to all those persons who took part in the field-work, plant identification, and data processing.

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