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Vegetation and soil changes induced by Mesembryanthemum crystallinum L. in a Mediterranean desert ecosystem
Journalof Arid Environments (1991) 20: 321-330
Vegetation and soil changes induced by Mesembryanthemum crystallinum L. in a Mediterranean desert ecosystem R. EI-Ghareeb Department ofBotany, Faculty ofScience, Alexandria University, Egypt (Received 5 January 1990, accepted 14 February 1990) This study evaluates the effects of the invasion of Mesembryanthemum crystallinum on vegetation composition and soil properties in a Mediterranean desert ecosystem, 48 km SW of Alexandria. Values of density, cover and frequency of species, and of soil properties were determined during the growing seasons of 1975 and 1987 in 62 stands. After 12 years, there was approximately a 26-fold increase in the density of Mesembryanthemum crystallinum and about a 68-fold increase in its cover. This was associated with an overall decrease in the total density of annuals of about 68% and an overall decrease in their total cover of about 48%. There was almost no significant difference in the abundance of perennials. The dominance of Mesembryanthemum crystallinum in the study area was associated with a significant increase in soil salinity and the concentration ofNa, Ca and Cl. These were released from the litter of Mesembryanthemum with leaching by rain and produced an unfavourable osmotic environment reducing the germination and growth of annuals.
Introduction The influence of introduced species on populations and communities has attracted the attention of ecologists since the seminal work of Cowles (Cowles, 1899, 1911; Clements, 1916; Keever, 1950; Bunting, 1960; Lieth, 1960; Baker & Stebbins, 1965; Zaret & Paine, 1973; Vivrette & Muller, 1977; Simberloff, 1981; Bertness, 1984). Understanding how invading species influence established communities and native species offers a potentially critical test of the relative importance of interspecific competition (MacArthur & Levins, 1967), predation (Paine, 1966), and species equilibrium (MacArthur & Wilson, 1967) in structuring natural communities. Most of the common documented effects are generated by habitat modification and predation (Simberloff, 1981). Mesembryanthernurn crystal/inurn L. (iceplant, Aizoaceae) was originally introduced to the Mediterrariean region from South Africa (Zohary, 1966), but it is now entirely naturalised in Egypt (Tackholm, 1974). Its spread in the Burg El-Arab area (300 5 4 ' N , 29°33'E, 48 km south-west of Alexandria, Fig. 1) has been monitored by the author since 1970. The plant has covered large areas of some of the natural and disturbed habitats between ridges, in depressions and on railway embankments, reducing the abundance of common plant species. The present study evaluates the effects of this invasion by Mesembryanthernurn crystal/inurn. A detailed description of the vegetation, climate, soil, geology and geomorphology of Present address: Department of Science, College of Basic Education, Shamiya 71509, Kuwait. 0140-1963/911030321
+ 10 $03-00/0
© 1991 Academic Press Limited
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Figure 1. Location of the study area (dotted area).
the Burg EI-Arab area has been given by Ayyad (1973). The study area is 8 m above sea level. The soils are Typic Calciorthids, sandy loams, moderately affected by salts, poor in organic matter, phosphorus and nitrogen (Gomah et al., 1982). The study area is included in Emberger's Mediterranean isoclimatic zone (Le Houerou, 1981). The bioclimatic map of UNESCO (1979) designates its climate as arid with a mild winter and a warm summer. Most of the mean annual rainfall of 168·9 mm falls during the period between October and February. Mesembryanthemurn occurs on the west coast of Africa, around the Mediterranean region, and along the west coast of Chile (Moran, 1950). (Mesembryanthemurn refers to M. crystal/inurn L. unless otherwise stated.) It also occurs along the coasts of California, Baja California, and Mexico (Vivrette & Muller, 1977). In Egypt, the plant is one of the common annuals along the Mediterranean coastal land, and is rare in the Eastern Desert (Tackholm, 1974). Vivrette & Muller (1977) describe the plant as a succulent, prostrate annual herb. Its surface is covered with saccate, unicellular trichomes ranging in size from 1 to 3 mm. These trichomes are filled with a saline solution and are the source of the common name, crystalline ice plant. The seeds germinate with the first rains and with each succeeding rain. Staggered germination could explain the confusion about the annual status of the plant in Dunkle (1950). The seedlings continue rapid vegetative growth until spring. The plants usually flower from March to June and generally fruit from June to August. Seeds are numerous and minute. The fruits (five-celled capsule) open with a heavy fog or rain, releasing a portion of the seeds. The capsules then close as the seeds dry after the rain. This repeated opening and closing eventually ruptures the capsule.
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Methods Sixty-two vegetation stands (10 x 20 m) were selected in the study area during the growing season of 1975. Homogeneity of stands was judged according to physiographic features, with no reference to vegetational criteria except the presence of Mesembryanthemum. Fifty quadrats of uniform size (1 x 2 m) were randomly located within each stand. Species density, frequency and cover were determined and the importance value (relative frequency + relative density + relative cover) was calculated. Sampling of vegetation was repeated during the growing season of 1987. Plant nomenclature follows Tackholm (1974). Soil sampling was carried out at the end of the growing seasons of 1975and 1987in three locations in each stand. A hole was dug to a depth of 30 em, and samples collected from the whole depth. These were mixed, air-dried and passed through a 2 mm sieve in order to separate gravel and debris. The portion finer than 2 mm was kept for physical and chemical determinations. The sand fraction was determined by mechanical separation on a standard testing sieve, silt and clay fractions by the pipette method described by Day (1965). Available phosphorus was extracted with sodium bicarbonate and determined colorimetrically using the method of Olsen et al. (1954) as described by Jackson (1960). Calcium carbonate was determined by the manometric method of Williams (1948). The available micronutrients were extracted with DTPA chelate and determined by atomic absorption analysis (Allen et al., 1974). Total nitrogen analysis was by the Kjeldahl method (Bremner, 1965). The methods used to determine saturation percentage, organic carbon, pH, electric conductivity (EC), Na, K, Ca, Mg, C0 3 , HC0 3 , Cl, and S04 were those ofthe U.S. Salinity Laboratory Staff (1954). Correlation coefficients were calculated between pairs of stands based on vegetation and soil records of 1975 and 1987. These records were transformed to approximate normal distribution: arcsin x/300 for importance values, x + 0'05 for density values, and arcsin for percentages of soil factors. The significance of differences between records of 1975 and those of 1987 of density and cover of species and of soil variables were assessed by the ttest. Vegetation and soil records of 19 stands in which the importance value of Mesembryanthemum was more than 90 were analysed by principal components analysis (PCA) according to the methods ofNie etal. (1975). The PCA was carried out using annuals only. Perennials were excluded because Mesembryanthemum had little effect on their abundance. The change in position of stands on the ordination plane from 1975 to 1987 were then used to demonstrate the effect of the dominance of Mesembryanthemum on the overall composition of the vegetation and the soil properties in the study area.
Results In 12 years, there was an approximately 26-fold increase in the density of Mesembryanthemum and about a 68-fold increase in its cover (Table 1). This was associated with an overall
decrease in the total density of annuals of about 68%. Also there was an overall decrease in their total cover of about 48%. Such decrease was due mainly to Plantago coronopus, Anacyclus alexandrinus, Calendula micrantha, Hordeum murinum, Schismus barbatus and Lophochloa cristata. On the other hand, there was almost no significant difference (p > 0'05) in the total density and cover of perennials, except Plantago albicans and P. lanceolata which exhibited a notable decrease. The correlation coefficient between the records for 1975 and 1987 was 0'74 based on the importance value data of perennials only, and 0'81 based on density data of perennials only. Using the importance value and density data of all species (perennials and annuals), these values were O'31 and O'34 respectively. This indicates that while there has been a remarkable change in the abundance of annuals from 1975 to 1987 (after the invasion and
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Table 1. Means ofdensity (plantl100 m2 ) andcover (cm!100m) of species recorded in 62 stands at the study area in 1975 and 1987. Species are arranged in order of the number of stands of occurrence Density Species
Mesembryanthemum crystallinum Perennials
Eminiumspiculatum Arisarum vulgare Plantago lanceolata Launaeanudicaulis Fagonia cretica Salvia lanigera Plantago albicans Thymelaea hirsuta Asphodelus microcarpus Salsola longifolia Total
Annuals
Plantago coronopus Anacyclus alexandrinus Calendula micrantha Hordeum murinum Schizmus barbatus Lophochloa cristata Filago desertorum Chenolia arabica Bassia muricata Latium rigidum Phalaris canariensis Trigonella stellata Total
1975
1987
Cover 1975
1987
3'4
89,5**
2·1
143,8**
1212·4 525'3 271'6 208'2 151'6 136'2 52,4 15'3 10'9 2·4 2586·2
1280.3 560'6 120,3** 234·6 140·1 131·6 6,2** 20'2 U'8 3·5 2377·5
259·9 171'4 120'7 131'4 144·6 41·5 31,4 71'4 41'2 6'4 1019·9
271·4 172'3 51.3* 129.8 131·4 48·2 4'2** 60'6 40'3 10·2 919·7
23'2 16'2 14·3 14,2 10·4 8'7 8'4 6'3 5'6 5'8 4·3 3'1 120·5
8'2 3'1 ** 2'6** 3'8** 2·1 ** 1'8** 5'1 4'1 3·2 1'7** 1·1** 1·4 38·2
8'6 4'6 2'6 8·4 7· ] 6·1 5'1 4·3 3·9 3·7 1·9 3·8 60·1
3'4 2,8* 1'1* 0'2** 1,4** 0,8** 4'2 4·6 6·8 0'6** 0,1** 2·9 28·9
*Difference from 1975 mean significant (at the 0'05 probability level). **Difference from 1975 mean highly significant (at the 0'01 probability level).
dominance of Mesembryanthemum), the abundance of perennials remained almost the same. PCA made no assumption that two types of stands (of 1975 and 1987) were present, and determined those linear combinations of species abundances that accounted for the greatest percentage of the total variance (Fig. 2, Table 2). The first component accounted for 18·5% of the total variance in plant abundances, and the second component accounted for 12·1%. Although there was a considerable overlap between the stands of 1975 and 1987, the latter formed a relatively compact cluster at the lower left portion of the graph (Fig. 2). Principal component II was more important than principal component I in separating the two groups of stands. Two species with large positive loadings on principal component II were Plantago coronopus and Mesembryanthemum, and two with large negative loadings were Anacyclus alexandrinus and Calendula micrantha (Table 2). Soil properties which tended to have significantly higher values in 1987 included EC (salinity), concentrations ofNa", K+, Caz+, Mi+, Cl" and Mn z+ (Table 3). Fez+, Cu 2+ and Zn 2 + concentrations tended to have lower values in 1987, but their differences were not significant. Most of the other soil properties tested were not significantly altered (see
CHANGES INDUCED BY MESEMBRYANTHEMUM CRYSTALLINUM
325
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Figure 2. Plots of the factor scores of the 19 stands according to peA of the annual species. Stands sampled in 1975 are represented by circles, and stands sampled in 1987 represented by dots.
Table 2. Factor score coefficients for thefirst twoprincipal components of PCAfor the annualflora in thestudy area. Species are arranged in order of thenumber of stands of occurrences Species
Mesembryanthemum crystallinum Plantago coronopus Anacyclus alexandrinus Calendula micrantha Hordeum murinum Schizmus barbatus Lophochloa cristata Filago desertorum Chenolia arabica Bassiamuricata Lolium rigidum Phalaris canariensis Trigonella stellata
Factor score I
Factor score II
+0'018 -0,076 -0,008 -0,071 +0'041 -0'003 +0·003 +0·247 -0'034 -0'117 +0'264 +0·077 -0'078
+0'360 +0'391 -0'160 -0'131 +0'068 +0'003 -0,056 +0·034 +0'028 -0,106 -0,541 -0,113 +0·051
Table 3). The results of the PCA for soil data (Fig. 3, Table 4) indicate again that stands sampled in 1975 and 1987 form relatively distinct and compact clusters. The first component accounted for 27'3% of the variance, and the second accounted for 16,4%. Principal component I had a large positive loading for EC, Na, Ca and CI, and large negative loading for Nand P (Table 4). Discussion The 26-fold increase in the density of Mesembryanthemum and the 68-fold increase in its cover in 12 years resulted in remarkable decreases in the abundance of annuals especially
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grasses. That such decreases were mainly due to the invasion of the study area by Mesembryanthemum and not to variation in rainfall is indicated by the relatively small difference in the mean annual rainfall between 1975 and 1987 (152 mm and 146 mm respectively). The invasion by Mesembryanthemum in Santa Barbara Island (California) has been described by Philbrick (1972) using field reports from Sumner (1958), Dunkle (1950), and his own observations. Sumner (1958) observed the changes in vegetation of Santa Barbara Island during the time of a rapid increase in the rabbit population from 1949 to 1958. By 1958, Sumner observed 'Iceplant had continued to make enormous gains, occupying nearly all ground laid bare by rabbits. More than half the surface of the island now appeared covered by it ...' Dunkle (1950) included a map of the area occupied by Mesembryanthemum in the period 1939-41. Philbrick (1972) observed 'since that time, the iceplant has carpeted a much larger portion of the island, excluding other vegetation, by physical or physiological means'. The successive photographs of Sumner in 1939 and Philbrick in 1970(Philbrick, 1972) show the replacement of Coreopsis gigantea and grasses by Mesembryanthemum. Once they have become established in the grassland communities, individuals of the species grow very large, and eventually dominate the area previously occupied by grassland. The western Mediterranean desert of Egypt has a long history of intensive land use, mainly grazing and rain-fed farming (Kassas, 1972). The stands selected for the present study are not subjected to grazing, as their borders are cleared for barley cultivation. This Table 3. Means(x), standard errors (SE), andranges of soil variables in 62 stands in
the study area in 1975 and 1987. Differences were tested witha ± test 1975
Variable
x
SE
1987 Range
x
SE
Range
p
Sand (%) Silt (%) Clay (%) Saturation percentage Organic carbon (%) CaC03 (%) Total N (%) Available P (p.p.m.) pH EC (mmhos/cm)
83'3 9'8 6·9 34'8 0·58 23'8 0'11 2'21 7'23 9·21
1·9 80·1 -87,8 2·0 -14,6 3'9 2·4 1'4 - 8'9 3·8 30·1 -39'1 0'04 0'20- 0·71 6'9 20'1 -34'0 0'04 0,09- 0'16 0'33 1,13- 5·71 0'05 7'11- 7·81 7,11-14'21 1·4
84·8 7'6 7·6 33·3 0·71 21'9 0'18 2·83 7·41 12·33
2·7 4'2 2'8 4'2 0'06 7'1 0'06 0·54 0·06 1-6
78·1 2·1 1-630·0 0,1921'l 0'040,927,336'40-
89'1 NS 16'4 NS 9·1 NS 41'0 NS NS 0'91 38'0 NS NS 0'28 6·74 NS 7·90 NS 19'81 <0'05
Soluble cations Na K. (meg/I) Ca Mg
45'33 8'82 13'13 24·88
1·8 40'1 -56,2 0'18 6'41-11,81 2'13 11'2 -21'4 2·47 13·1 -39,2
58'00 12'13 17·21 33·11
2'1 0'31 3·2 1·8
38·1 8·569·4 13·7 -
64'3 14·81 31'2 41'4
14·31 115'40 10'82
0·19 2'31 0·19
7'6 - 18'4 NS 60'9 -121'00 <0'005 8·6 - 20'3 NS
1·89 1'68 0·39 0·21
0'14 0'18 0'08 0·01
Soluble anions C0 3 13·52 0'04 8'4 -16,1 HC03 (meg/l) CI 86'36 1'84 61'2 -98'3 10'20 0'03 9·1 -18,1 S04 Available microelements Fe Mn (p.p.m.) CU Zn NS = Not significant (p
2'21 1'32 0·41 0·28
> 0'05).
0·03 0'10 0·01 0·04
1·140'810,070,13-
2·52 2'92 0·51 0·61
0'910.840'070,11-
2·11
HI
0'61 0'71
<0'005 <0·05 <0'005 <0'05
NS NS NS NS
CHANGES INDUCED BY MESEMBRYANTHEMUMCRYSTALLINUM
0
327
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Figure 3. Plots of the factor scores of the 19 stands according to the PCA of 20 soil variables. Circles represent stands sampled in 1975, dots represent the same stands sampled in 1987.
type of disturbance produces an open habit which is often colonised by Mesembryanthemum. Vivrette & Muller (1977) report that open areas or areas sparsely occupied by other plants are easily invaded by Mesembryanthemum. Intense grazing can be followed by an increase in Mesembryanthemum as was seen on Santa Barbara Island (Philbrick, 1972). Invasion is aided by the preferential grazing habits of mice and rabbits (Sumner, 1958). According to Vivrette & Muller (1977), Mesembryanthemum is grazed by rabbits and mice only after most other forms of forage are removed. Mesembryanthemum was not seen to be grazed in the study area. Mesembryanthemum contributes an annual average necromass about 60% (245 kg dry matter/ha) of the annual average necromass of all species in the study area (El Ghareeb, 1991). The plant gradually dries from the base upwards, with the fruits being the last parts to dry. Most of the plants die in the summer, and the dried plant remains in place throughout the next several years. For an annual species, iceplant decomposes very slowly. This is perhaps due to the ring of sclerenchyma associated with the stele of the stem (Vivrette & Muller, 1977). While it has long been known that localization of litter fall can lead to significant modification of soil chemistry beneath trees and shrubs of arid and semi-arid areas (Roberts, 1950; Fireman & Hayward, 1952; Rickard, 1965; Sharma & Tongway, 1973; Tiedemann & Klemmedson, 1973a,b), only a few annuals have been examined in this way. The present study indicates that the dominance of Mesembryanthemum in the study area is associated with a significant increase in soil salinity and the concentration ofNa, Ca and Cl. These salts are leached from the litter by rain and fog. The salts may produce an unfavourable osmotic environment reducing germination and growth of the annual grasses in the study area (e.g. Hordeum murinum, Schismus barbatus, Lophochloa cristata,
328
R. EL-GHAREEB
Table 4. Factor score coefficients for the first two principal components of PCA for soil variables Factor score I
Factor score II
Sand (0/0) Silt (0/0) Clay (0/0) Saturation percentage Organic carbon (%) CaC03 Total N (0/0) Available P (p.p.m.) pH EC (mmhos/cm)
-0'016 +0·012 +0·013 -0'144 -0'095 +0'033 -0'317 -0'218 +0·031 +0·149
-0,013 +0·016 +0·022 +0'191 +0,029 +0'018 -0'113 -0,103 +0·024 -0'137
Soluble cations Na K (meg/l) Ca Mg
+0·178 +0'023 +0'281 +0'196
-0,128 +0'378 -0'012 +0·287
-0,082 +0'192 -0'016
-0'015 -0,124 +0·387
-0'075 +0'086 +0'010 -0,010
-0,019 -0'014 +0'115 -0'129
Variable
Soluble anions HC0 3 (meg/I) CI S04 Available microelements Fe Mn (p.p.m.) Cu Zn
Lolium rigidum). Vivrette & Muller· (l977) reported that throughfall from iceplants which dry up in late summer can have an osmotic level as high as 500 milliosmols with the first autumn rains. This level, which is equivalent to half-strength seawater, retards the germination of many grasses (e.g. Bromus rigidus, Festuca megalura, Hordeum leporinum). They provide evidence that the reduction in number of grass seedlings does not appear to be the result of limiting levels of moisture or light, nor to be due to grazing by small mammals. Retardation in seedling establishment is correlated with high levels of salt found in the soil beneath dried Mesembryanthemum. Thanks are due to Professor M. A. Ayyad for constructive comments upon a version of this paper.
References Allen, S. E., Grimshaw, H. M., Parkinson, J. A. & Quarmby, C. (1974). Chemical Anarysis of Ecological Materials. Oxford, London: Blackwell Scientific Publications. 565 pp. Ayyad, M. A. (1973). Vegetation and environment of the western Mediterranean coastal land of Egypt. I. The habitat of sand dunes. Journal of Ecology, 61: 509-523. Baker, H. G. & Stebbins, G. L. (1965). The Genetics of Colonizing Species. New York: Academic Press. 588 pp. Bertness, M. D. (1984). Habitat and community modification by an introduced herbivorous snail. Ecology, 65: 37{}-381. Bremner, J. M. (1965). Total nitrogen. In: Black, C. A. (Ed.), Methods ofSoil Anarysis Part 2. pp. 1149-1178. Madison: American Society of Agronomy.
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U.S. Salinity Laboratory Staff (1954). Diagnosis and Improvement of Saline and Alkali Soils. U.S. Department of Agriculture, Handbook 60. Washington, D.C.: U.S. Government Printing Office. 160 pp. Vivrette, N. J. & Muller, C. H. (1977). Mechanism of invasion and dominance of coastal grassland by Mesembryanthemum crystallinum. Ecological Monographs, 47: 301-318. Williams, D. E. (1948). A rapid manometric method for the determination of carbonate in soils. Proceedings of the Soil Science Society ofAmerica, 13: 127-129. Zaret, T. M. & Paine, R. T. (1973). Species introduction in a tropical lake. Science, 182: 449-455. Zohary, M. (1966). Flora Palaestina. Part I. Jerusalem. The Israel Academy of Sciences and Humanities. 367 pp.
Vegetation and soil changes induced by Mesembryanthemum crystallinum L. in a Mediterranean desert ecosystem R. EI-Ghareeb Department ofBotany, Faculty ofScience, Alexandria University, Egypt (Received 5 January 1990, accepted 14 February 1990) This study evaluates the effects of the invasion of Mesembryanthemum crystallinum on vegetation composition and soil properties in a Mediterranean desert ecosystem, 48 km SW of Alexandria. Values of density, cover and frequency of species, and of soil properties were determined during the growing seasons of 1975 and 1987 in 62 stands. After 12 years, there was approximately a 26-fold increase in the density of Mesembryanthemum crystallinum and about a 68-fold increase in its cover. This was associated with an overall decrease in the total density of annuals of about 68% and an overall decrease in their total cover of about 48%. There was almost no significant difference in the abundance of perennials. The dominance of Mesembryanthemum crystallinum in the study area was associated with a significant increase in soil salinity and the concentration ofNa, Ca and Cl. These were released from the litter of Mesembryanthemum with leaching by rain and produced an unfavourable osmotic environment reducing the germination and growth of annuals.
Introduction The influence of introduced species on populations and communities has attracted the attention of ecologists since the seminal work of Cowles (Cowles, 1899, 1911; Clements, 1916; Keever, 1950; Bunting, 1960; Lieth, 1960; Baker & Stebbins, 1965; Zaret & Paine, 1973; Vivrette & Muller, 1977; Simberloff, 1981; Bertness, 1984). Understanding how invading species influence established communities and native species offers a potentially critical test of the relative importance of interspecific competition (MacArthur & Levins, 1967), predation (Paine, 1966), and species equilibrium (MacArthur & Wilson, 1967) in structuring natural communities. Most of the common documented effects are generated by habitat modification and predation (Simberloff, 1981). Mesembryanthernurn crystal/inurn L. (iceplant, Aizoaceae) was originally introduced to the Mediterrariean region from South Africa (Zohary, 1966), but it is now entirely naturalised in Egypt (Tackholm, 1974). Its spread in the Burg El-Arab area (300 5 4 ' N , 29°33'E, 48 km south-west of Alexandria, Fig. 1) has been monitored by the author since 1970. The plant has covered large areas of some of the natural and disturbed habitats between ridges, in depressions and on railway embankments, reducing the abundance of common plant species. The present study evaluates the effects of this invasion by Mesembryanthernurn crystal/inurn. A detailed description of the vegetation, climate, soil, geology and geomorphology of Present address: Department of Science, College of Basic Education, Shamiya 71509, Kuwait. 0140-1963/911030321
+ 10 $03-00/0
© 1991 Academic Press Limited
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Figure 1. Location of the study area (dotted area).
the Burg EI-Arab area has been given by Ayyad (1973). The study area is 8 m above sea level. The soils are Typic Calciorthids, sandy loams, moderately affected by salts, poor in organic matter, phosphorus and nitrogen (Gomah et al., 1982). The study area is included in Emberger's Mediterranean isoclimatic zone (Le Houerou, 1981). The bioclimatic map of UNESCO (1979) designates its climate as arid with a mild winter and a warm summer. Most of the mean annual rainfall of 168·9 mm falls during the period between October and February. Mesembryanthemurn occurs on the west coast of Africa, around the Mediterranean region, and along the west coast of Chile (Moran, 1950). (Mesembryanthemurn refers to M. crystal/inurn L. unless otherwise stated.) It also occurs along the coasts of California, Baja California, and Mexico (Vivrette & Muller, 1977). In Egypt, the plant is one of the common annuals along the Mediterranean coastal land, and is rare in the Eastern Desert (Tackholm, 1974). Vivrette & Muller (1977) describe the plant as a succulent, prostrate annual herb. Its surface is covered with saccate, unicellular trichomes ranging in size from 1 to 3 mm. These trichomes are filled with a saline solution and are the source of the common name, crystalline ice plant. The seeds germinate with the first rains and with each succeeding rain. Staggered germination could explain the confusion about the annual status of the plant in Dunkle (1950). The seedlings continue rapid vegetative growth until spring. The plants usually flower from March to June and generally fruit from June to August. Seeds are numerous and minute. The fruits (five-celled capsule) open with a heavy fog or rain, releasing a portion of the seeds. The capsules then close as the seeds dry after the rain. This repeated opening and closing eventually ruptures the capsule.
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Methods Sixty-two vegetation stands (10 x 20 m) were selected in the study area during the growing season of 1975. Homogeneity of stands was judged according to physiographic features, with no reference to vegetational criteria except the presence of Mesembryanthemum. Fifty quadrats of uniform size (1 x 2 m) were randomly located within each stand. Species density, frequency and cover were determined and the importance value (relative frequency + relative density + relative cover) was calculated. Sampling of vegetation was repeated during the growing season of 1987. Plant nomenclature follows Tackholm (1974). Soil sampling was carried out at the end of the growing seasons of 1975and 1987in three locations in each stand. A hole was dug to a depth of 30 em, and samples collected from the whole depth. These were mixed, air-dried and passed through a 2 mm sieve in order to separate gravel and debris. The portion finer than 2 mm was kept for physical and chemical determinations. The sand fraction was determined by mechanical separation on a standard testing sieve, silt and clay fractions by the pipette method described by Day (1965). Available phosphorus was extracted with sodium bicarbonate and determined colorimetrically using the method of Olsen et al. (1954) as described by Jackson (1960). Calcium carbonate was determined by the manometric method of Williams (1948). The available micronutrients were extracted with DTPA chelate and determined by atomic absorption analysis (Allen et al., 1974). Total nitrogen analysis was by the Kjeldahl method (Bremner, 1965). The methods used to determine saturation percentage, organic carbon, pH, electric conductivity (EC), Na, K, Ca, Mg, C0 3 , HC0 3 , Cl, and S04 were those ofthe U.S. Salinity Laboratory Staff (1954). Correlation coefficients were calculated between pairs of stands based on vegetation and soil records of 1975 and 1987. These records were transformed to approximate normal distribution: arcsin x/300 for importance values, x + 0'05 for density values, and arcsin for percentages of soil factors. The significance of differences between records of 1975 and those of 1987 of density and cover of species and of soil variables were assessed by the ttest. Vegetation and soil records of 19 stands in which the importance value of Mesembryanthemum was more than 90 were analysed by principal components analysis (PCA) according to the methods ofNie etal. (1975). The PCA was carried out using annuals only. Perennials were excluded because Mesembryanthemum had little effect on their abundance. The change in position of stands on the ordination plane from 1975 to 1987 were then used to demonstrate the effect of the dominance of Mesembryanthemum on the overall composition of the vegetation and the soil properties in the study area.
Results In 12 years, there was an approximately 26-fold increase in the density of Mesembryanthemum and about a 68-fold increase in its cover (Table 1). This was associated with an overall
decrease in the total density of annuals of about 68%. Also there was an overall decrease in their total cover of about 48%. Such decrease was due mainly to Plantago coronopus, Anacyclus alexandrinus, Calendula micrantha, Hordeum murinum, Schismus barbatus and Lophochloa cristata. On the other hand, there was almost no significant difference (p > 0'05) in the total density and cover of perennials, except Plantago albicans and P. lanceolata which exhibited a notable decrease. The correlation coefficient between the records for 1975 and 1987 was 0'74 based on the importance value data of perennials only, and 0'81 based on density data of perennials only. Using the importance value and density data of all species (perennials and annuals), these values were O'31 and O'34 respectively. This indicates that while there has been a remarkable change in the abundance of annuals from 1975 to 1987 (after the invasion and
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Table 1. Means ofdensity (plantl100 m2 ) andcover (cm!100m) of species recorded in 62 stands at the study area in 1975 and 1987. Species are arranged in order of the number of stands of occurrence Density Species
Mesembryanthemum crystallinum Perennials
Eminiumspiculatum Arisarum vulgare Plantago lanceolata Launaeanudicaulis Fagonia cretica Salvia lanigera Plantago albicans Thymelaea hirsuta Asphodelus microcarpus Salsola longifolia Total
Annuals
Plantago coronopus Anacyclus alexandrinus Calendula micrantha Hordeum murinum Schizmus barbatus Lophochloa cristata Filago desertorum Chenolia arabica Bassia muricata Latium rigidum Phalaris canariensis Trigonella stellata Total
1975
1987
Cover 1975
1987
3'4
89,5**
2·1
143,8**
1212·4 525'3 271'6 208'2 151'6 136'2 52,4 15'3 10'9 2·4 2586·2
1280.3 560'6 120,3** 234·6 140·1 131·6 6,2** 20'2 U'8 3·5 2377·5
259·9 171'4 120'7 131'4 144·6 41·5 31,4 71'4 41'2 6'4 1019·9
271·4 172'3 51.3* 129.8 131·4 48·2 4'2** 60'6 40'3 10·2 919·7
23'2 16'2 14·3 14,2 10·4 8'7 8'4 6'3 5'6 5'8 4·3 3'1 120·5
8'2 3'1 ** 2'6** 3'8** 2·1 ** 1'8** 5'1 4'1 3·2 1'7** 1·1** 1·4 38·2
8'6 4'6 2'6 8·4 7· ] 6·1 5'1 4·3 3·9 3·7 1·9 3·8 60·1
3'4 2,8* 1'1* 0'2** 1,4** 0,8** 4'2 4·6 6·8 0'6** 0,1** 2·9 28·9
*Difference from 1975 mean significant (at the 0'05 probability level). **Difference from 1975 mean highly significant (at the 0'01 probability level).
dominance of Mesembryanthemum), the abundance of perennials remained almost the same. PCA made no assumption that two types of stands (of 1975 and 1987) were present, and determined those linear combinations of species abundances that accounted for the greatest percentage of the total variance (Fig. 2, Table 2). The first component accounted for 18·5% of the total variance in plant abundances, and the second component accounted for 12·1%. Although there was a considerable overlap between the stands of 1975 and 1987, the latter formed a relatively compact cluster at the lower left portion of the graph (Fig. 2). Principal component II was more important than principal component I in separating the two groups of stands. Two species with large positive loadings on principal component II were Plantago coronopus and Mesembryanthemum, and two with large negative loadings were Anacyclus alexandrinus and Calendula micrantha (Table 2). Soil properties which tended to have significantly higher values in 1987 included EC (salinity), concentrations ofNa", K+, Caz+, Mi+, Cl" and Mn z+ (Table 3). Fez+, Cu 2+ and Zn 2 + concentrations tended to have lower values in 1987, but their differences were not significant. Most of the other soil properties tested were not significantly altered (see
CHANGES INDUCED BY MESEMBRYANTHEMUM CRYSTALLINUM
325
4
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Figure 2. Plots of the factor scores of the 19 stands according to peA of the annual species. Stands sampled in 1975 are represented by circles, and stands sampled in 1987 represented by dots.
Table 2. Factor score coefficients for thefirst twoprincipal components of PCAfor the annualflora in thestudy area. Species are arranged in order of thenumber of stands of occurrences Species
Mesembryanthemum crystallinum Plantago coronopus Anacyclus alexandrinus Calendula micrantha Hordeum murinum Schizmus barbatus Lophochloa cristata Filago desertorum Chenolia arabica Bassiamuricata Lolium rigidum Phalaris canariensis Trigonella stellata
Factor score I
Factor score II
+0'018 -0,076 -0,008 -0,071 +0'041 -0'003 +0·003 +0·247 -0'034 -0'117 +0'264 +0·077 -0'078
+0'360 +0'391 -0'160 -0'131 +0'068 +0'003 -0,056 +0·034 +0'028 -0,106 -0,541 -0,113 +0·051
Table 3). The results of the PCA for soil data (Fig. 3, Table 4) indicate again that stands sampled in 1975 and 1987 form relatively distinct and compact clusters. The first component accounted for 27'3% of the variance, and the second accounted for 16,4%. Principal component I had a large positive loading for EC, Na, Ca and CI, and large negative loading for Nand P (Table 4). Discussion The 26-fold increase in the density of Mesembryanthemum and the 68-fold increase in its cover in 12 years resulted in remarkable decreases in the abundance of annuals especially
R. EL-GHAREEB
326
grasses. That such decreases were mainly due to the invasion of the study area by Mesembryanthemum and not to variation in rainfall is indicated by the relatively small difference in the mean annual rainfall between 1975 and 1987 (152 mm and 146 mm respectively). The invasion by Mesembryanthemum in Santa Barbara Island (California) has been described by Philbrick (1972) using field reports from Sumner (1958), Dunkle (1950), and his own observations. Sumner (1958) observed the changes in vegetation of Santa Barbara Island during the time of a rapid increase in the rabbit population from 1949 to 1958. By 1958, Sumner observed 'Iceplant had continued to make enormous gains, occupying nearly all ground laid bare by rabbits. More than half the surface of the island now appeared covered by it ...' Dunkle (1950) included a map of the area occupied by Mesembryanthemum in the period 1939-41. Philbrick (1972) observed 'since that time, the iceplant has carpeted a much larger portion of the island, excluding other vegetation, by physical or physiological means'. The successive photographs of Sumner in 1939 and Philbrick in 1970(Philbrick, 1972) show the replacement of Coreopsis gigantea and grasses by Mesembryanthemum. Once they have become established in the grassland communities, individuals of the species grow very large, and eventually dominate the area previously occupied by grassland. The western Mediterranean desert of Egypt has a long history of intensive land use, mainly grazing and rain-fed farming (Kassas, 1972). The stands selected for the present study are not subjected to grazing, as their borders are cleared for barley cultivation. This Table 3. Means(x), standard errors (SE), andranges of soil variables in 62 stands in
the study area in 1975 and 1987. Differences were tested witha ± test 1975
Variable
x
SE
1987 Range
x
SE
Range
p
Sand (%) Silt (%) Clay (%) Saturation percentage Organic carbon (%) CaC03 (%) Total N (%) Available P (p.p.m.) pH EC (mmhos/cm)
83'3 9'8 6·9 34'8 0·58 23'8 0'11 2'21 7'23 9·21
1·9 80·1 -87,8 2·0 -14,6 3'9 2·4 1'4 - 8'9 3·8 30·1 -39'1 0'04 0'20- 0·71 6'9 20'1 -34'0 0'04 0,09- 0'16 0'33 1,13- 5·71 0'05 7'11- 7·81 7,11-14'21 1·4
84·8 7'6 7·6 33·3 0·71 21'9 0'18 2·83 7·41 12·33
2·7 4'2 2'8 4'2 0'06 7'1 0'06 0·54 0·06 1-6
78·1 2·1 1-630·0 0,1921'l 0'040,927,336'40-
89'1 NS 16'4 NS 9·1 NS 41'0 NS NS 0'91 38'0 NS NS 0'28 6·74 NS 7·90 NS 19'81 <0'05
Soluble cations Na K. (meg/I) Ca Mg
45'33 8'82 13'13 24·88
1·8 40'1 -56,2 0'18 6'41-11,81 2'13 11'2 -21'4 2·47 13·1 -39,2
58'00 12'13 17·21 33·11
2'1 0'31 3·2 1·8
38·1 8·569·4 13·7 -
64'3 14·81 31'2 41'4
14·31 115'40 10'82
0·19 2'31 0·19
7'6 - 18'4 NS 60'9 -121'00 <0'005 8·6 - 20'3 NS
1·89 1'68 0·39 0·21
0'14 0'18 0'08 0·01
Soluble anions C0 3 13·52 0'04 8'4 -16,1 HC03 (meg/l) CI 86'36 1'84 61'2 -98'3 10'20 0'03 9·1 -18,1 S04 Available microelements Fe Mn (p.p.m.) CU Zn NS = Not significant (p
2'21 1'32 0·41 0·28
> 0'05).
0·03 0'10 0·01 0·04
1·140'810,070,13-
2·52 2'92 0·51 0·61
0'910.840'070,11-
2·11
HI
0'61 0'71
<0'005 <0·05 <0'005 <0'05
NS NS NS NS
CHANGES INDUCED BY MESEMBRYANTHEMUMCRYSTALLINUM
0
327
0
10
12
09
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Figure 3. Plots of the factor scores of the 19 stands according to the PCA of 20 soil variables. Circles represent stands sampled in 1975, dots represent the same stands sampled in 1987.
type of disturbance produces an open habit which is often colonised by Mesembryanthemum. Vivrette & Muller (1977) report that open areas or areas sparsely occupied by other plants are easily invaded by Mesembryanthemum. Intense grazing can be followed by an increase in Mesembryanthemum as was seen on Santa Barbara Island (Philbrick, 1972). Invasion is aided by the preferential grazing habits of mice and rabbits (Sumner, 1958). According to Vivrette & Muller (1977), Mesembryanthemum is grazed by rabbits and mice only after most other forms of forage are removed. Mesembryanthemum was not seen to be grazed in the study area. Mesembryanthemum contributes an annual average necromass about 60% (245 kg dry matter/ha) of the annual average necromass of all species in the study area (El Ghareeb, 1991). The plant gradually dries from the base upwards, with the fruits being the last parts to dry. Most of the plants die in the summer, and the dried plant remains in place throughout the next several years. For an annual species, iceplant decomposes very slowly. This is perhaps due to the ring of sclerenchyma associated with the stele of the stem (Vivrette & Muller, 1977). While it has long been known that localization of litter fall can lead to significant modification of soil chemistry beneath trees and shrubs of arid and semi-arid areas (Roberts, 1950; Fireman & Hayward, 1952; Rickard, 1965; Sharma & Tongway, 1973; Tiedemann & Klemmedson, 1973a,b), only a few annuals have been examined in this way. The present study indicates that the dominance of Mesembryanthemum in the study area is associated with a significant increase in soil salinity and the concentration ofNa, Ca and Cl. These salts are leached from the litter by rain and fog. The salts may produce an unfavourable osmotic environment reducing germination and growth of the annual grasses in the study area (e.g. Hordeum murinum, Schismus barbatus, Lophochloa cristata,
328
R. EL-GHAREEB
Table 4. Factor score coefficients for the first two principal components of PCA for soil variables Factor score I
Factor score II
Sand (0/0) Silt (0/0) Clay (0/0) Saturation percentage Organic carbon (%) CaC03 Total N (0/0) Available P (p.p.m.) pH EC (mmhos/cm)
-0'016 +0·012 +0·013 -0'144 -0'095 +0'033 -0'317 -0'218 +0·031 +0·149
-0,013 +0·016 +0·022 +0'191 +0,029 +0'018 -0'113 -0,103 +0·024 -0'137
Soluble cations Na K (meg/l) Ca Mg
+0·178 +0'023 +0'281 +0'196
-0,128 +0'378 -0'012 +0·287
-0,082 +0'192 -0'016
-0'015 -0,124 +0·387
-0'075 +0'086 +0'010 -0,010
-0,019 -0'014 +0'115 -0'129
Variable
Soluble anions HC0 3 (meg/I) CI S04 Available microelements Fe Mn (p.p.m.) Cu Zn
Lolium rigidum). Vivrette & Muller· (l977) reported that throughfall from iceplants which dry up in late summer can have an osmotic level as high as 500 milliosmols with the first autumn rains. This level, which is equivalent to half-strength seawater, retards the germination of many grasses (e.g. Bromus rigidus, Festuca megalura, Hordeum leporinum). They provide evidence that the reduction in number of grass seedlings does not appear to be the result of limiting levels of moisture or light, nor to be due to grazing by small mammals. Retardation in seedling establishment is correlated with high levels of salt found in the soil beneath dried Mesembryanthemum. Thanks are due to Professor M. A. Ayyad for constructive comments upon a version of this paper.
References Allen, S. E., Grimshaw, H. M., Parkinson, J. A. & Quarmby, C. (1974). Chemical Anarysis of Ecological Materials. Oxford, London: Blackwell Scientific Publications. 565 pp. Ayyad, M. A. (1973). Vegetation and environment of the western Mediterranean coastal land of Egypt. I. The habitat of sand dunes. Journal of Ecology, 61: 509-523. Baker, H. G. & Stebbins, G. L. (1965). The Genetics of Colonizing Species. New York: Academic Press. 588 pp. Bertness, M. D. (1984). Habitat and community modification by an introduced herbivorous snail. Ecology, 65: 37{}-381. Bremner, J. M. (1965). Total nitrogen. In: Black, C. A. (Ed.), Methods ofSoil Anarysis Part 2. pp. 1149-1178. Madison: American Society of Agronomy.
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Bunting, A. H. (1960). Some reflections on the ecology of weeds. In: Harper, J. L. (Ed.), The Biology of Weeds. pp. 11-26. Oxford: Blackwell Scientific Publications. 256 pp. Clements, F. E. (1916). Plant Succession. An Anarysis of the Development of Vegetation. Carnegie Institute, Washington Publication No. 242. 512 pp. Cowles, H. C. (1899). The ecologicalrelations of the vegetation on the sand dunes of Lake Michigan. Botanical Gazette, 27: 95-116. . Cowles, H. C. (1911). The causes of vegetative cycles. Botanical Gazette, 51: 161-183. Day, P. R. (1965). Particle fractionation and particle-size analysis. In: Black, C. A. (Ed.),Methodsof Soil Analysis, Part 2. pp. 552-562. Madison: American Society of Agronomy. Dunkle, M. B. (1950). Plant Ecology of theChannel Islands of California. Los Angeles, Publications Allan Hancock Pacific Expedition University So. California Press, 13(3): 247-386. El-Ghareeb, R. (1991). Biomass, phenology and pattern of Mesembryanthemum crystallinum L. in a Mediterranean desert ecosystem (in preparation). Fireman, M. & Hayward, H. E. (1952). Indicator significance of some shrubs in the Escalante Desert, Utah. Botanical Gazette, 114: 143-155. Gomah, A. M., Ismail, H. A., Thabet, M., EI-Eraky, A. M. & Shalaby, E. S. (1982). Regional Environmental Management of Mediterranean Desert Ecosystems of Northern Egypt. Detailed Soil Survey of Burg EI-Arab Pilot Area. Progress Report No.3, Part III, Soil and Water Science Department, Faculty of Agriculture, University of Alexandria, Alexandria. pp. 4Q-65 (mimeogr.). Jackson, M. L. (1960). SoilChemical Anarysis. Englewood Cliffs, New York: Prentice-Hall. 498 pp. Kassas, M. (1972). A brief history ofland-use in Mareotis region, Egypt. Minerva Biologica, 1: 167174. Keever, C. (1950). Causes of succession on old fields ofthe piedmont, North Carolina. Ecological Monographs, 20: 229-250. Le Houerou, H. N. (1981). The arid bioclimates in the Mediterranean isoclimatic zone. Ecologia Mediterranea, 8: 103-114. Lieth, H. (1960). Patterns of change within grassland communities. In: Harper, J. L. (Ed.), The Biology of Weeds. pp. 27-39. Oxford: Blackwell Scientific Publications. 256 pp. MacArthur, R. H. & Levins, R. (1967). The limiting similarity, convergence and divergence of coexisting species. American Naturalist, 101: 377-385. MacArthur, R. H. & Wilson, E. O. (1967). The Theory of Island Biogeography. New Jersey: Princeton University Press. 240 pp. Moran, R. (1950). Mesembryanthemum in California. Madrona, 10: 161-163. Nie, N. H., Hull, C. H., Jenkins, J. G., Steinbrenner, K. & Bent, D. H. (1975). Statistical Package for theSocialSciences. New York: McGraw-Hili. 342 pp. Olsen, S. R., Cole, C. V., Watanabe, F. S. & Dean, L. A. (1954). Estimation of available phosphorus in soils by extraction with sodium bicarbonate. U.S. Department of Agriculture Circular No. 939. 19 pp. Paine, R. T. (1966). Food web complexity and species diversity. American Naturalist, 100: 6575. Philbrick, R. V. (1972). The plants of Santa Barbara Island, California. Madrona, 21: 329-393. Rickard, W. H. (1965). Sodium and potasium accumulation by greesewood and hopsage leaves. Botanical Gazette, 126: 116-119. Roberts, R. C. (1950). Chemical effects of salt-tolerant shrubs on soils. Fourth International Congress of Soil Sciences, 1: 404-406. Sharma, M. L. & Tongway, D. J. (1973). Plant induced soil salinity patterns in two saltbush (Atriplex spp.) communities. Journalof RangeManagement, 26: 121-124. Simberloff, D. (1981). Community effects of introduced species. In: Nitecki, M. (Ed.),BioticCrises in Ecological and Evolutionary Times. pp. 53-81. New York: Academic Press. Sumner, E. L. Jr. (1958). The rabbits of Santa Barbara Island, a progress report and summary. U.S. Natural Park Services Channel Islands of California Natural Monument. 21 pp. Tackholm, V. (1974). Student's Flora of Egypt (2nd Edn). Cairo: Cairo University Press. 888 pp. Tiedemann, A. R. & Klemmedson, J. O. (1973a). Effects of mesquite on physical and chemical properties of the soil. Journalof RangeManagement, 26: 27-29. Tiedemann, A. R. & Klemmedson, J. O. (1973b). Nutrient availability in desert grassland soils under mesquite ( Prosopis juliflora) trees and adjacent open areas. Proceedings of theSoil Science Society of America, 37: 107-111. UNESCO (1977). Map ofthe World Distribution ofArid Regions. MAB, Technical Notes, 7.
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U.S. Salinity Laboratory Staff (1954). Diagnosis and Improvement of Saline and Alkali Soils. U.S. Department of Agriculture, Handbook 60. Washington, D.C.: U.S. Government Printing Office. 160 pp. Vivrette, N. J. & Muller, C. H. (1977). Mechanism of invasion and dominance of coastal grassland by Mesembryanthemum crystallinum. Ecological Monographs, 47: 301-318. Williams, D. E. (1948). A rapid manometric method for the determination of carbonate in soils. Proceedings of the Soil Science Society ofAmerica, 13: 127-129. Zaret, T. M. & Paine, R. T. (1973). Species introduction in a tropical lake. Science, 182: 449-455. Zohary, M. (1966). Flora Palaestina. Part I. Jerusalem. The Israel Academy of Sciences and Humanities. 367 pp.