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Impacts of native and invasive exotic Prosopis congeners on soil properties and associated flora in the arid United Arab Emirates
Journal of Arid Environments 100-101 (2014) 1e8
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Impacts of native and invasive exotic Prosopis congeners on soil properties and associated flora in the arid United Arab Emirates Ali El-Keblawy a, *, Mahmoud Ali Abdelfatah b, c a
Department of Applied Biology, Faculty of Science, Sharjah University, P.O. Box 27272, Sharjah, United Arab Emirates Soil Quality Department, Environment Agency e Abu Dhabi, P.O. Box 45553, Abu Dhabi, United Arab Emirates c Soils and Water Sciences Department, Faculty of Agriculture, Fayoum University, P.O. Box 63514, Fayoum, Egypt b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 17 November 2012 Received in revised form 28 September 2013 Accepted 3 October 2013 Available online 26 October 2013
The native Prosopis cineraria and exotic invasive P. juliflora are present in arid habitats of the United Arab Emirates (UAE). The objective of this study was to assess the impacts of allelopathy and soil properties on plants associated with the two species in arid deserts. Density and other community attributes of the associated species were assessed beneath, at the margin and outside the canopies of 20 Prosopis individuals. Aqueous extracts of fresh and old leaves of both Prosopis species were assessed on germination of five native plants. Soil samples were collected from beneath and next to canopies of the two species and their chemical properties were analyzed. The effect on the associated flora was depressive for P. juliflora, but was positive for P. cineraria canopy. The depressive effect of P. juliflora was more obvious on the annual compared with perennial plants. The negative effect of the aqueous extract of P. juliflora was much greater on germination, especially for annual plants. Canopies of both species improved soil properties that would facilitate the association of other native plants. The allelopathic effect of P. juliflora, however, may override its facilitative effect and consequently resulted in a depressive effect on the associated flora. Ó 2013 Elsevier Ltd. All rights reserved.
Keywords: Allelopathy Desert habitats Invasive plants Native plants Soil salinity Species diversity
1. Introduction Desert shrubs and trees play a major role in stabilizing the fragile desert ecosystems in arid regions. In many deserts, trees are considered as keystone species as they support the life of many other faunal and floral species (Munzbergova and Ward, 2002). Desert trees can influence their understory vegetation in many ways, resulting in a broad range of detrimental or beneficial outcomes. The beneficial effects of desert trees on the environment beneath their canopies include the reduction in the extremes of environmental temperatures (Greenlee and Callaway, 1996), provision of suitable amounts of photosynthetically active radiation to understorey plants (Smith and Knapp, 2001), improved soil texture and nutrient content (Moro et al., 1997; Nobel, 1989; Pugnaire et al., 2004), increased soil moisture (Belsky, 1994) and protection against herbivory (McAuliffe, 1984). Conversely, desert trees can also have negative effects on seedling survival and establishment in their
* Corresponding author. Permanent address: Department of Biology, Faculty of Education in Al-Arish, Suez Canal University, Egypt. E-mail addresses: [email protected], [email protected] (A. ElKeblawy). 0140-1963/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jaridenv.2013.10.001
understorey community. These competitive interactions may be through light deprivation, competition for water and nutrients, or leaching of allelopathic compounds (Bais et al., 2003; Brewer, 2002; Moro et al., 1997; Nobel, 1989). Detrimental and beneficial mechanisms do not act in isolation from each other in nature. The relative importance of these two processes in a particular plant community determines the structure of that community (Callaway and Walker, 1997). Biological invasions are recognized as one of the most important causes of ecosystem degradation and biodiversity loss worldwide (Mack et al., 2001; Vitousek et al., 1996). The depressive effect of some exotic species on the associated flora has been attributed to allelopathy, which is an interference mechanism by which plants release chemicals that affect other plants (Bais et al., 2003; Brewer, 2002; Callaway and Ridenour, 2004). This allelopathic interference has been argued to be one of the mechanisms by which exotics may become successful invaders (Inderjit et al., 2008; Stinson et al., 2006). A congeneric, or phylogenetic, approach was used to examine allelopathy as a mechanism for invasion. This approach involves comparative studies of exotic species with natives in the same genus (Inderjit et al., 2008). Native plants typically do not share a co-evolutionary history with the exotic invasive species, and
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therefore greater allelopathic effects of the invasive are expected on the native plants in such ecosystems. The ‘novel weapons hypothesis’ indicated that allelochemicals produced by the invaders are new to the native plant communities (Bais et al., 2003; Callaway and Ridenour, 2004). Assessment of the impact of allelopathy of two congeneric species on the germination of their associated species might shed light on the mechanisms of the coexistence of native plants with native and exotic competitors. Only a few studies compared the allelopathic effects of invasive and native competitors on the associated native plants (but see Inderjit et al., 2008). Prosopis juliflora and P. cineraria are among a few trees growing in the arid deserts of the UAE and currently occupying the same habitats. They constitute a major ecological feature in the Northern Emirates of the UAE. P. cineraria is a slow growing tree native to the dry and arid regions of Arabia and India and is beneficial for the growth and development of other species (Abdel Bari et al., 2007). It is rarely, if ever, seen as a weedy species and has not been successfully introduced into other parts of the world (Pasiecznik et al., 2001). P. juliflora, however, is an exotic species from Central and South America and grows luxuriantly on sandy soils with high groundwater tables in the UAE. It has been introduced on a large scale in the artificial forests of the UAE because of its faster growth and soil-binding capacity. Recently, it has escaped plantations and come to dominate many plant communities, and is considered a weed. It is highly aggressive and coppices so well that it crowds out native vegetation (El-Keblawy and Al-Rawai, 2005, 2007; Tiwari, 1999). Both P. cineraria and P. juliflora possess phenolic compounds. However, the leaf leachates and extracts of P. juliflora showed allelopathic effects against native species in its invasion range, whereas extracts from leaves of P. cineraria collected and applied in the same way, do not (Goel and Behl, 1998; Inderjit et al., 2008; Kaur et al., 2012). A water-soluble extract from different parts of P. juliflora, including litter and rhizosphere soil, has resulted in the inhibition of seed germination of many species. However, most of the tested assay plants do not naturally grow near P. juliflora. For example, aqueous extracts from soil under the canopy and from different parts of P. juliflora inhibited germination and early seedling growth of various cultivars of Zea mays, Triticum aestivum and Albizia lebbeck (Noor et al., 1995). In addition, Al-Humaid and Warrag (1998) concluded that P. juliflora leaves contain water-soluble allelopathins that could inhibit seed germination and retard rates of germination and seedling growth in Cynodon dactylon. In pot studies of the allelopathic effects of leaf litter of P. juliflora, Chellamuthu et al. (1997) indicated that germination of black gram (Vigna mungo), and sorghum (Sorghum bicolor) was significantly reduced with the maximum reduction occurring at 2% incorporation of P. juliflora leaf litter. The selection of bioassay species is crucial to the study of allelopathy because the effect of biochemicals can vary dramatically among test species (Inderjit, 2006; Inderjit and Nilsen, 2003; Perry et al., 2005). The aims of the present study were to assess the impacts of (1) allelopathy of fresh and old leaves of the native P. cineraria and exotic invasive P. juliflora on the germination of five native plants naturally growing with them, (2) soil chemical properties beneath and around the two Prosopis species on their associated plants in the arid environment of the UAE. This is especially important as the two congers are growing together in the same soil type and have the same associated native plants. We assume that the differential response of the native plant germination to the allelochemicals of the two congers would help in understanding the extent of the detrimental effect of allelopathy in both species. In addition, it is assumed that the balance between the facilitative effect of soil properties and the negative effect of
allelopathy would also help in understanding the invasive ability of exotic P. juliflora. 2. Materials and methods 2.1. Study area A study site in Fujairah Emirate on the eastern coast of the UAE (25140 27.6800 N and 56 210 24.1400 E) was selected to ensure a reasonable degree of physiognomic homogeneity and with homogenous distribution and densities of both P. juliflora and P. cineraria. Individuals of the two species covering medium and large trees were selected for study. In some communities of P. cineraria that were invaded by P. juliflora, the invader was found to negatively affect the growth and vigor of the native P. cineraria. These places were excluded from the study. 2.2. Impacts on associated flora A total of 20 stands were located randomly around the two Prosopis species (10 stands for each). A Prosopis tree (P. juliflora or P. cineraria) was located near the center of each stand to serve as a focal point. The area of each stand was 225 m2 (15 15 m). In each stand, nine one m2 quadrats were distributed on three transects; 3 quadrats beneath; 3 at the margin; and 3 beyond the canopy of each selected Prosopis. A species list was compiled in each stand. The absolute density (number of plants of a certain species rooted within one m2) was estimated for each associated plant species beneath, at the margin and beyond the canopies of the two Prosopis species. Other community attributes were also estimated, including species number, species richness (average number of species per stand), and species evenness (estimated by ShannoneWeaver index). 2.3. Soil analysis In each stand, two composite soil samples were collected from the upper 10 cm of the soil, one from underneath (halfway between the trunk and the edge of the canopy) and another from at least 2 m outside the margin of the canopy. A total of 40 soil samples were collected and analyzed for this study. Soil samples were air dried, ground, homogenized, and sieved through a 2 mm sieve to remove large particles. Soil organic matter content, pH, salinity and the nutrients N, P, Na, and K were estimated. Organic matter content was estimated using loss of mass by combustion at 430 C on the <2 mm soil fraction. Soil water extracts (1:2.5 of soil:water) were prepared for determination of electrical conductivity (EC) and pH using conductivity and pH meters. Available nitrogen was extracted using 2 M KCl and determined by the micro-Kjeldahl method. Available phosphorous was estimated using Olsen’s solution (sodium bicarbonate) as an extracting agent. Na and K were estimated by using flame photometry. These methods are outlined in Black (1965). 2.4. Assessment of allelopathic effects Fresh and old leaf samples were collected from underneath P. cineraria and P. juliflora individuals in the studied community. Fresh leaves fallen within one year were distinguished by their very light color, while leaves older than one year were darker. All samples were air dried at room temperature and subsamples were ground to pass through a 3-mm sieve. Dried materials from all samples were extracted in distilled water at 25 g 100 ml1 for 24 h at 25 C. Following extraction, coarse plant materials were removed with a 2-mm sieve. Extracts were then passed through a
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2.5. Statistical analysis Differences in the total number of species in the various positions from the individual Prosopis plants (beneath, edge, and beyond the canopy) were assessed using c2 tests. One-way ANOVAs were used to compare the density of associated species at different positions from Prosopis canopies. Two-way analyses of variance
Number of associated species
A: Number of associated species 20 15 10 5 0
P. cineraria P. juliflora Prosopis sp
Shannon-Weaver index
2.0 1.5 1.0 0.5 0.0
3. Results The overall number of associated species did not differ between the stands of the two Prosopis sp. (20 species for P. juliflora and 21 species for P. cineraria). However, the number of associated species was significantly reduced beneath P. juliflora (c2 ¼ 6.68, P < 0.05), but not beneath P. cineraria canopies (c2 ¼ 0.054, P > 0.05). The number of species beneath P. juliflora was almost one third the number of species beneath P. cineraria and in the open stands between the canopies (Fig. 1 a). Results of two-way ANOVAs showed significant effects for both Prosopis sp., position from the canopy and their interaction on evenness, and richness and density of associated species (P < 0.05, Table 1). The exception was the impact of Prosopis sp. on richness of associated species (P > 0.05). In P. juliflora, evenness, richness and density of associated species were significantly lower beneath the canopy, compared with outside and at the margin of the
C: Richness of associated species
P. cineraria P. juliflora Prosopis sp
8 6 4 2 0
P. cineraria P. juliflora Prosopis sp
D: Density of associated species (number/100m2) Density of associated species
B: Evenness of associated species
(ANOVA) were used to evaluate the effect of the main factors (Prosopis species and position from the canopy) on species density, evenness, and richness, and soil properties. Three-way ANOVA was used to assess the impacts of Prosopis species, leaf age and extract concentration on final germination percentage of the five assayed native plants. Species density was square-root-transformed to meet the assumption of the ANOVA. This transformation improved the normality of the distribution of the data. ShapiroeWilk test was used to check the normality of the data distribution. Tukey’s Honest Significant Difference post hoc test was used for comparison of means when statistical significant differences (P < 0.05) were observed. All statistical methods were performed using SYSTAT, version 11.0.
Richness of associated species
Whatman filter paper and centrifuged at 12,000 rpm for 20 min. These 25% (w/v) extracts of dried materials were further diluted to obtain 2, 4, 6 and 8% solutions. Seeds of five native plants growing naturally with the studied populations of P. juliflora and P. cineraria were collected. The plants include one annual herb (Plantago ovata), two annual grasses (Tragus racemosus and Eragrostis barrelieri) and two perennial grasses (Sporobolus arabicus and Cenchrus ciliaris). Seeds were separated from the litter and dry stored in brown paper pages until their use in germination tests. The germination was conducted in 9 cm Petri-dishes containing one disk of Whatman No. 1 filter paper, with 10 ml of test solution. Each dish was wrapped with Para film as an added precaution against loss of water by evaporation. For each species, dishes were arranged in an incubator set at 15/25 C in 12 h dark/ 12 h light, with light coincide with 25 C in a completely randomized design with two Prosopis species (P. juliflora and P. cineraria) and four concentrations of each extract. Three replicate dishes were used for each treatment, each with 25 seeds. Sterile distilled water was used as a control. Radical emergence was the criterion for germination. Germinated seedlings were counted and removed every second day for 20 days following seeds sowing.
3
1000 750 500 250 0
P. cineraria P. juliflora Prosopis sp
Fig. 1. Effects of position relative to the canopy of Prosopis juliflora and Prosopis cineraria on total number of species, evenness, richness and density (number/100 m2) of associated species. Black bars ¼ Beneath canopy, White bars ¼ margin of canopy and gray bars ¼ outside of canopy.
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Table 1 Two way ANOVAs (F-values) for the effects of Prosopis sp., position from the canopy, and their interaction on evenness, richness and density of associated species. *: P < 0.05, **: P < 0.01, and ***: P < 0.001. Community attributes
Species (S)
Position from canopy (P)
S*P
Species evenness Species richness Species density
4.40* 2.41 8.25**
9.41*** 22.30*** 28.8***
5.91* 8.42*** 23.47***
The densities of both C. ciliaris and S. arabicus did not differ significantly between beneath and beyond the canopies (Table 2). The number of annuals that attained significantly lower densities under P. juliflora canopies (9 species) was significantly greater than the number of perennials (2 species) (c2 ¼ 5.680, P < 0.05; the 11 perennials and 9 annuals recorded with P. juliflora were used as expected values). 3.2. Effect of P. cineraria on species composition
canopy. Conversely, evenness and density did not differ significantly at the margin versus beyond the canopies of P. Juliflora individuals (Fig. 1). In P. cineraria, evenness and richness of associated species did not differ significantly beneath and at the margin of the canopy, but both were significantly lower compared with beyond the canopy. However, the density was significantly greater at the margin, compared with beneath and beyond the canopy (Fig. 1). The comparison of the two Prosopis species indicates that both evenness and richness of associated species were significantly greater underneath P. cineraria compared with underneath P. juliflora canopy. However, these variables did not differ between the margin and beyond the canopies of the two Prosopis species (Fig. 1). 3.1. Effect of P. juliflora on species composition One-way ANOVAs showed that the density of 13 species, out a total of the 20 species recorded in the P. juliflora community, was significantly reduced beneath, compared with outside the canopies (P < 0.05, Table 2). Most of these species were not present under the canopies. In addition, five other species were completely absent under P. juliflora canopies, so their densities did not differ significantly beyond vs. beneath the canopy (P > 0.05). The depressive impact of the P. juliflora canopy was less obvious on perennial plants, especially grasses, compared with annual plants. Six species attained a minimum of eight individuals per 100 m2; two perennial grasses (C. ciliaris, S. arabicus), one perennial tree (P. juliflora), one perennial herb (Aizoon canariense) and two annual herbs (T. racemosus and Gypsophila bellidifolia).
Table 2 Effect of Prosopis juliflora canopy on density of associated species (number (number of individuals per 100 m2). *: P < 0.05, **: P < 0.01, and ***: P < 0.001. Species
Acacia tortilis Aizoon canariense Amaranthus viridis Arnebia hispidissima Astragalus annularis Cenchrus ciliaris Eragrostis barrelieri Gypsophila bellidifolia Launaea capitata Malva parviflora Paronychia arabica Plantago ovata Prosopis juliflora Rhazya stricta Spergularia marina Sporobolus arabicus Stipagrostis plumosa Tephrosia apollinea Tragus racemosus Tribulus terrestris a
Life cyclea
P P A A A P A A P A A A P P A P P P A A
A ¼ annuals, P ¼ perennials.
The impact of P. cineraria canopy on density was significant for 13 species, out a total of the 21 species recorded in its stands (P < 0.05, Table 3). The densities were significantly increased at the canopy margin for nine species and beneath the canopies for two species and both at margin and beneath the canopies for one species. However, the density was significantly reduced beneath vs. beyond the canopy in only one species (E. barrelieri, Table 3). 3.3. Effect of Prosopis species on soil properties Two-way ANOVA indicated significant effects for Prosopis species on EC, Na and organic C % (P < 0.05). In addition, position from canopy and the interaction between species and position from canopy had significant effects on most of the studied soil characters (P < 0.05, Appendix A). Values of K, N, organic C %, and P were significantly greater beneath, compared to beyond the canopies of both P. juliflora and P. cineraria. Relative position to the canopy significantly affected pH, EC, Na, HCO3 and organic C % in P. juliflora, but not in P. cineraria. Values of EC, HCO3 and organic C % were significantly increased, but pH significantly decreased beneath, compared with outside P. juliflora canopy. The P. cineraria canopy, however, did not affect any of these soil factors (Table 4). 3.4. Impacts of aqueous extracts on seed germination of five native plants Three-way ANOVA showed significant effects for the main factors (Prosopis species, leaf age and extract concentration) and most of their interactions on final germination percentage of the Table 3 Effect of Prosopis cineraria canopy on density of associated species (number of individuals per 100 m2). *: P < 0.05, **: P < 0.01, and ***: P < 0.001. Species
Life cyclea
Acacia tortilis Aeluropus massauensis Aizoon canariense Amaranthus viridis Astragalus annularis Cenchrus ciliaris Chenopodium murale Chrozophora oblongifolia Eragrostis barrelieri Euphorbia serpens Gypsophila bellidifolia Launaea capitata Lotus garcinii Paronychia arabica Plantago ovata Prosopis juliflora Spergularia marina Sporobolus arabicus Stipa capensis Tragus racemosus Tribulus terrestris
P P P A A P A P A A A P P A A P A P P A A
Position from canopy Beneath
Margin
Beyond
0.0 12.5 0.0 0.0 0.0 25.0 0.0 8.3 0.0 0.0 0.0 0.0 9.1 0.0 0.0 12.0 0.0 0.0 18.0 0.0
17.0 72.0 0.0 8.3 0.0 58.3 0.0 0.0 8.3 8.3 33.3 65.0 21.7 8.3 0.0 14.7 7.2 0.0 35.0 0.0
8.0 90.8 36.7 38.3 8.3 16.7 38.3 25.0 0.0 18.3 16.7 40.7 31.7 8.3 13.3 10.0 9.3 16.7 45.0 21.6
F *** * *** *** ** * *** ** *** *** *
* *
a
A ¼ annuals, P ¼ perennials.
Position from canopy Beneath
Margin
Beyond
0.0 23.0 67.7 21.2 16.7 38.7 24.2 0.0 13.3 10.2 66.67 0.0 0.0 0.0 6.7 12.7 54.4 15.0 7.5 12.0 5.0
12.1 0.0 34.3 112 100 36.6 75.8 100 14.4 43.4 22.2 0.0 32.3 0.0 53.3 13.3 195.5 16.7 33.3 17.0 32.3
0.0 10.2 33.3 13 11.1 22.8 21.4 0.0 68.9 12.1 20.3 11.1 31.0 33.3 10.0 2.7 113.3 16.7 0.0 9.0 21.2
F
* *** * *** * *** *** ***
*** * *** ** ***
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Table 4 Effects of Prosopis juliflora and Prosopis cineraria canopies on the mean values of some soil characters. Species
Place from canopy
pH
EC (dS m1)
HCO3 (M eq l1)
Na (meq l1)
K (meq l1)
N (ppm)
P (ppm)
Organic C (%)
P. juliflora
Beyond Beneath Beyond Beneath
7.43a 7.04b 7.43a 7.35a
1.40b 6.61a 1.40a 2.41a
1.16a 1.26a 1.16a 1.00a
12.6b 21.7a 12.6a 13.5a
6.5b 9.35a 6.5b 8.9a
2.7b 4.6a 2.7b 3.5a
0.41a 0.56a 0.41b 065a
11.38b 24.94a 11.38b 14.80b
P. cineraria
five studies species (P < 0.05, Appendix B). Generally, seeds of the different species treated with aqueous extracts of P. juliflora attained significantly lower germination, compared with their controls (seeds without treatments) and seeds treated with different concentrations of P. cineraria extracts. Higher concentrations of old leaves of P. juliflora were significantly more effective in inhabiting the germination of C. ciliaris and S. arabicus, compared with higher concentrations of fresh leaves. In E. barrelieri, higher concentrations of fresh leaves in both species were more effective, compared with the same concentrations of old leaves (Fig. 2). Seeds of the two perennial grasses C. ciliaris and S. arabicus germinated in all concentrations of both P. cineraria and P. juliflora extracts. The final germination of the non-treated seeds (control) of the two species didn’t differ from most concentrations of fresh and old leaf extracts of P. cineraria. However, the germination of the two species attained significantly lower values in most concentrations of P. juliflora (Fig. 2). The seed germination of the two annual grasses (T. racemosus and E. barrelieri) differs according to Prosopis species, leaf age and extracts concentration. Germination of T. racemosus seeds was significantly reduced in higher concentrations (6% and 8%) of both fresh and old leaf extracts of both P. juliflora and P. cineraria, but seeds of E. barrelieri attained greater germination in up to 8% of old leaf extract of the Prosopis species. The result indicates that the annual E. barrelieri grass can tolerate the fresh, but not the old extract of the two Prosopis species (Fig. 2). The germination of the annual P. ovata was completely inhibited in 6% and 8% of both fresh and old leaf extracts of P. juliflora. However, the seeds of this species were able to germinate in up to 8% extract of P. cineraria leaves, especially the old leaves (Fig. 2). 4. Discussion The results of our study indicated that P. juliflora significantly reduced the evenness, richness and density of the associated plants beneath, compared with open places beyond their canopies. However, P. cineraria either did not reduce these variables or significantly increased them. These results support other studies showed interference effects for P. juliflora and facilitative effects for P. cineraria. For example, in the artificial forests of the UAE, the exotic Eucalyptus and P. juliflora trees had resulted in significant reductions in species diversity and abundance of understory species, compared to the native P. cineraria and Acacia arabica (ElKeblawy and Ksiksi, 2005). In addition, in a semiarid plantation in Haryana, India, Jalota et al. (2000) reported that only two species dominated P. juliflora plantations, but 25 different species were found in the indigenous Dalbergia sissoo plantations. Another study in India investigated the vegetation succession on salt-affected soils after five years of plantation with two exotic salt bushes and three tree species, and found that only three species were recorded with P. juliflora, compared to 7e8 species with other trees (Arya, 2003). Furthermore, Aggarwal et al. (1976) found that the canopies of the invasive P. juliflora had far fewer understory species than any of four other forestry trees studied, whereas the native congener,
P. cineraria, was associated with higher understory diversity than any other species. Recently, Kaur et al. (2012) reported that P. cineraria had much weaker effects on species richness compared with P. juliflora. Many studies have suggested that allelopathy contributes to the ability of exotic species to become dominant in invaded plant communities (Adetayo et al., 2005; Inderjit et al., 2008). The greater depressive effect of P. juliflora on the associated species, compared to its congener P. cineraria, could be attributed to the more susceptibility of the associated species to specific allelochemicals produced by the invader, compared with the native tree. According to the ‘novel weapons hypothesis’, these chemicals are new to the native plant communities in the UAE (Bais et al., 2003; Callaway and Ridenour, 2004). Similar results have been reported for another two congeners Lantana camara and L. indica. The first species, which is exotic invasive throughout Asia, has allelopathic effects, but its corresponding native congener L. indica does not have the same strong effects on native species in India (Inderjit et al., 2008). Our study showed that seed germination of five native plants associated with the Prosopis species was significantly inhibited with the aqueous extracts of P. juliflora, compared with control (non-treated) seeds and seeds treated with different concentrations of P. cineraria extracts. Conversely, seeds of four native species germinated to significant proportions in the extract of both fresh and old leaves of P. cineraria, especially in the lower concentrations (2% and 4%, Fig. 2). Chellamuthu et al. (1997) suggested that the allelopathic effect of P. juliflora leaf litter is due to the presence of phenolic compounds. Nakano et al. (2001) suggested that L-tryptophan may play an important role in the allelopathy of P. juliflora leaves. The content of L-tryptophan in the exudates of freeze-dried mesquite leaves (1 mg eq.) was estimated to be 4.8 103 mM (Nakano et al., 2001). In addition, Nakano et al. (2004) isolated syringin and (-)-lariciresinol from the aqueous foliar leachate of P. juliflora, and also detected these chemicals in rhizosphere soil. Several studies reported the presence of allelopathic compounds in both P. juliflora and P. cineraria. For example, Kaur et al. (2012) detected L-tryptophan in leaf leachates of both P. juliflora and P. cineraria, but the amounts were 73% higher in leaf leachate of the former than that of the latter. Similarly, Inderjit et al. (2008) compared soils collected from the rhizospheres of the two Prosopis species and found that soils beneath the exotic P. juliflora contained 63.2% higher concentrations of total phenolics than soil beneath the native P. cineraria. These findings could explain the relatively lower allelopathic effects of higher concentration of P. cineraria, aqueous extracts (6% and 8%), especially on seed germination of the annuals T. racemosus and P. ovata (Fig. 2). In the hyper-arid habitats of the UAE, there is a noticeable accumulation of litter underneath the P. juliflora, compared with P. cineraria canopies (El-Keblawy, personal observation). Litter falling to the ground during periods of stress can alter the physical, chemical, and biotic environment in which seeds germinate and seedlings grow (Facelli and Carson, 1991).
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Prosopis cineraria
Prosopis juliflora 100 Final germination (%)
Final germination (%)
Cenchrus ciliaris
100 80 60 40 20 0
0
Final germination (%)
Final germination (%)
Sporobolus arabicus
60 40 20 0
Final germination (%)
Final germination (%)
Eragrostis barrelieri
60 40 20 0
80 60 40 20 0
2 4 6 8 Extract concentration (%)
0
2 4 6 8 Extract concentration (%)
0
2 4 6 8 Extract concentration (%)
0
2 4 6 8 Extract concentration (%)
40 20
80 60 40 20
80 60 40 20 0
2 4 6 8 Extract concentration (%)
100 Final germination (%)
100 Final germination (%)
0
60
100 Final germination (%)
Final germination (%)
Tragus racemosus
2 4 6 8 Extract concentration (%)
80
0
2 4 6 8 Extract concentration (%)
100
Plantago ovata
0
100
80
80 60 40 20 0
20
0
2 4 6 8 Extract concentration (%)
100
0
40
100
80
0
60
0
2 4 6 8 Extract concentration (%)
100
0
80
0
2 4 6 8 Extract concentration (%)
80 60 40 20 0
Fig. 2. Effects of different concentrations of extracts of fresh and old leaves of Prosopis cineraria and Prosopis juliflora on final germination percentage (mean SE) of five desert species of the UAE. Gray bars ¼ control, black bars ¼ fresh leaves and hatched bars ¼ old leaves.
A. El-Keblawy, M.A. Abdelfatah / Journal of Arid Environments 100-101 (2014) 1e8
Consequently, litter can have a significant influence on emergence and growth of understorey species. In some exotic invaders, litter leachates have shown negative effects on seed germination, establishment and seedling growth of associated species (Chellamuthu et al., 1997). The greater accumulation of litter underneath the P. juliflora canopy could partially explain the greater inhibition of understory vegetation of this species. Kaur et al. (2012) reported that experimentally applied P. juliflora litter caused far greater mortality of native Indian species than litter from P. cineraria. In addition, P. juliflora leaf leachate showed negative effects on root growth of three common crop species of north-west India whereas P. cineraria leaf leachate had positive effects (Kaur et al., 2012). There is strong evidence from arid lands of nurse plants that facilitate establishment of other species (Franco and Nobel, 1989; McAuliffe, 1984). The nurse plant’s canopy structure may influence the success of seedling establishment, in particular in relation to shade intensity and rainfall interception (Padilla and Pugnaire, 2006). In P. cineraria, density of associated species was significantly greater at the margin, compared with beneath and beyond the canopy (Fig. 1). Similarly, the depressive effect of P. juliflora canopy was diminished at the margin; evenness and density did not differ significantly at the margin versus beyond the canopies of both Prosopis species. This suggests that the microenvironment at the margin of the canopies is more favorable, compared with both underneath and beyond the canopies. During small precipitation events, canopies might limit water availability in their understories by intercepting rainwater and directing it to the areas at the margins of canopies through flow along branches and leaves, making the soil at the margin wetter than in open and underneath the canopies (Padilla and Pugnaire, 2006). The pattern of higher soil fertility under canopies of desert shrubs and trees, compared with in adjacent open areas, is well documented in arid lands (Zhao et al., 2007). Many Prosopis species create “resource islands” with higher levels of organic matter and other macro-nutrients in soils beneath their canopies, which makes them stronger facilitators for other species (Kaur et al., 2012; Rossi and Villagra, 2003). For example, Kaur et al. (2012) showed that both P. juliflora and P. cineraria form resource islands by accumulating total organic N and organic carbon in their rhizosphere soil. In addition, Aggarwal et al. (1993) found that soil nitrogen, phosphorus, and potassium were higher under P. cineraria canopies than in open fields. Our results showed significant increases in the concentrations of K, N and P beneath, compared with beyond the canopies of both P. juliflora and P. cineraria. Unlike P. cineraria, P. juliflora increased soluble salts (EC) and decreased the pH underneath their canopy. Kaur et al. (2012) arrived to a similar result, regarding the soluble salts. The significant decrease in soil pH under the canopy of P. juliflora could be attributed to acidic nature of phenolic compounds. Species interactions involve a complex balance of competition (“negative”) and facilitation (“positive”) interactions (Brooker and Callaghan, 1998). Facilitation and interference interactions do not occur in isolation from each other. The overall effect of one species on another may be dependent on physical factors and the combination of competition for different resources, allelochemicals released into the environment, and facilitative factors such as shade and protection from herbivory (Callaway et al., 1991). In deserts, several shrubs have facilitative effects on the growth of some associated annuals, but also produce allelochemicals that suppress the growth of the same annuals (Callaway and Walker, 1997). In the present study, both Prosopis species have facilitative effects in relation to the available nutrients; their canopies increased the most important macronutrients K, N and P. In addition, both species increased the
7
organic matter contents (the increase was significant only in P. juliflora), which would also increase the water holding capacity that would improve soil texture and increase soil moistures. However, it appears that the allelopathic effects of the litters of P. juliflora may override its potential positive effects on soil fertility. Phenolic compounds of the allelochemicals in soils could reduce the water and nutrients uptake. For example, net uptake of P, K, and water by cucumber seedlings was reduced 57, 75, and 29%, respectively, when the whole root system was exposed to ferulic acid, an allelopathic phenolic acid. In addition, plant transpiration was reduced in a linear manner as the fraction of the cucumber roots in contact with ferulic acid increased (Lyu and Blum, 1990). The relative importance of facilitative and competitive interactions in a particular plant community determines the structure of that community (Callaway and Walker, 1997; Callaway et al., 1991). Our study showed a less depressive impact for the P. juliflora canopy on perennial plants, especially grasses, compared with annual plants. Similarly, Jalota et al. (2000) indicated that the two dominated species in P. juliflora plantations in the semi-arid Haryana in India were the perennial grasses Dactyloctenium aegyptium and Dichanthium annulatum. The positive presence of the perennial grasses C. ciliaris and S. arabicus that was observed in our study in the neighborhood area of P. juliflora, compared with annual plants, could be attributed partially to the high tolerance of the seeds of these plants during the germination stage to the presence of allelochemicals released from the leaves of the invader. Both the two perennial grasses germinated to high proportion, even in the highest concentration of the aqueous extract (8%) of the old and fresh leaves of P. juliflora. In addition, the greater ability of the perennial grasses, compared with annuals, to capitalize on more nutrients could be also account for their higher density underneath P. juliflora canopy. Conversely, the significant reduction in the density of the annuals underneath and at the margin of the P. juliflora could be explained mainly by the lower tolerance of the germination stage of these species to the released allelochemicals. The results of the study indicated significant reduction in germination of the seeds of the three annuals (E. barrelieri, T. racemosus and P. ovata) in most concentrations of fresh or old leaves or both of P. juliflora. Acknowledgments The authors would like to thank Dr Colin Pain, Honorary Assistant Professor at the University of Sevilla, Spain, for his critical revision of the manuscript. Thanks are also extended to Prof Inderjit Singh, University of Delhi, India, for his valuable comments on the manuscripts. Appendices Appendix A. Results of two-way ANOVA (F-values) for the effects of Prosopis juliflora and Prosopis cineraria canopies on some soil characters. ns: insignificant different at P ¼ 0.05, *: P < 0.05, ** and P < 0.01, and ***: P < 0.001.
Source of variation
pH
EC
HCO3
Na
K
N
P
Organic C
Species (S) Position from canopy (P) S*P
ns ns
* **
ns ns
* *
ns *
ns *
ns *
* *
**
*
ns
*
*
*
**
**
8
A. El-Keblawy, M.A. Abdelfatah / Journal of Arid Environments 100-101 (2014) 1e8
Appendix B. Results of three-way ANOVA (F-values) for the effects of species (Prosopis cineraria and P. juliflora), leaves age and extract concentration on final germination of seeds of five plants in the UAE. *: P < 0.05, **: P < 0.01, and ***: P < 0.001.
Source Species (S) Leaf age (A) Extract concentration (C) S*A S*C A*C S*A*C Error
df
Tragus racemosus
Eragrostis barrelieri
Plantago ovata
Sporobolus arabicus
Cenchrus ciliaris
1 1 3
154.9*** 50.6*** 460.9***
330.9*** 526.0*** 10.9***
77.9*** 5.96* 44.9***
238.3*** 17.5*** 77.5***
171.9*** 26.2*** 108.8***
1 3 3 3 48
54.2*** 5.0** 7.3*** 10.5*
239.6*** 2.29 6.14** 0.31
38.4*** 7.8*** 35.6*** 1.07
103.5*** 27.8*** 4.13** 5.98**
25.1*** 15.9*** 2.84* 1.25
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El-Keblawy, A., Al-Rawai, A., 2007. Impacts of the invasive exotic Prosopis juliflora (Sw.) D.C. on the native flora and soils of the UAE. Plant Ecol. 130, 23e35. Facelli, J.M., Carson, W.P., 1991. Heterogeneity of plant litter accumulation in successional communities. B. Torrey Bot. Club 118, 62e66. Franco, A.C., Nobel, P.S., 1989. Effect of nurse plants on the microhabitat and growth of cacti. J. Ecol. 77, 870e886. Goel, V.L., Behl, H.M., 1998. Screening of Prosopis germplasm for afforestation of degraded soil sites: performance, leaf nutrient status and influence on soil properties. J. Sustain. For. 8, 1e13. Greenlee, J., Callaway, R.M., 1996. Effects of abiotic stress on the relative importance of interference and facilitation. Am. Nat. 148, 386e396. Inderjit, 2006. Experimental complexities in evaluating the allelopathic activities in laboratory bioassays: a case study. Soil Biol. Biochem. 38, 256e262. Inderjit, Nilsen, E.T., 2003. Bioassays and field studies for allelopathy in terrestrial plants: progress and problems. Crit. Rev. Plant Sci. 22, 221e238. Inderjit, Seastedt, T.R., Callaway, R.M., Pollock, J.L., Kaur, J., 2008. Allelopathy and plant invasions: traditional, congeneric, and biogeographical approaches. Biol. Invas. 10, 875e890. Jalota, R.K., Sangha, K.K., Kohli, R.K., 2000. Under-storey vegetation of forest plantations in N-W India e an ecological economic assessment. J. Trop. Med. Plants 1, 115e124. Kaur, R., Gonzáles, W.L., Llambi, L.D., Soriano, P.J., Callaway, R.M., Rout, M.E., Gallaher, T.J., Inderjit, 2012. Community impacts of Prosopis juliflora invasion: biogeographic and congeneric comparisons. PLoS ONE 7, e44966. Lyu, S., Blum, U., 1990. Effects of ferulic acid, an allelopathic compound, on net P, K, and water uptake by cucumber seedlings in a split-root system. J. Chem. Ecol. 16, 2429e2439. Mack, M.C., D’Antonio, C.M., Ley, R., 2001. Alteration of ecosystem nitrogen dynamics by exotic plants: a case study of C4 grasses in Hawaii. Ecol. Appl. 11, 1323e1335. McAuliffe, J.R., 1984. Prey refugia and the distributions of two Sonoran desert cacti. Oecologia 65, 82e85. Moro, M.J., Pugnaire, F.I., Haase, P., Puigdefábregas, J., 1997. Effect of the canopy of Retama sphaerocarpa on its understorey in a semiarid environment. Funct. Ecol. 11, 425e431. Munzbergova, Z., Ward, D., 2002. Acacia trees as keystone species in Negev desert ecosystems. J. Veg. Sci. 13, 227e236. Nakano, H., Fujii, Y., Suzuki, T., Yamada, K., Kosemura, S., Yamamura, S., Hasegawa, K., 2001. A growth-inhibitory substance exuded from freeze-dried mesquite (Prosopis juliflora (Sw.) D.C.) leaves. Plant Growth Regul. 33, 165e168. Nakano, H., Nakajima,.E, Hiradate, S., Fujii, Y., Yamada, K., Shigemori, H., Hasegawa, K., 2004. Growth inhibitory alkaloids from mesquite (Prosopis juliflora (Sw.) D.C.) leaves. Phytochemistry 65, 587e591. Nobel, P.S., 1989. Temperature, water availability, and nutrient levels at various soil depths e consequences for shallow-rooted desert succulents, including nurse plant effects. Am. J. Bot. 76, 1486e1492. Noor, M., Salam, U., Khan, M.A., 1995. Allelopathic effects of Prosopis juliflora Swartz. J. Arid Environ. 31, 83e90. Padilla, F.M., Pugnaire, F.I., 2006. The role of nurse plants in the restoration of degraded environments. Front. Ecol. Environ. 4, 196e202. Pasiecznik, N.M., Felker, P., Harris, P.J.C., Harsh, L.N., Cruz, G., Tewari, J.C., Cadoret, K., Maldonado, L.J., 2001. The Prosopis juliflora e Prosopis pallida Complex: a Monograph. HDRA, Coventry, UK. Perry, L.G., Johnson, C., Alford, E.R., Vivanco, J.M., Paschke, M.W., 2005. Screening of grassland plants for restoration after spotted knapweed invasion. Restor. Ecol. 13, 725e735. Pugnaire, F.I., Armas, C., Valladares, F., 2004. Soil as a mediator in planteplant interactions in a semi-arid community. J. Veg. Sci. 15, 85e92. Rossi, B.E., Villagra, P.E., 2003. Effects of Prosopis flexuosa on soil properties and the spatial pattern of understory species in arid Argentina. J. Veg. Sci. 14, 543e550. Smith, M.D., Knapp, A.K., 2001. Physiological and morphological traits of exotic, invasive exotic, and native plant species in tallgrass prairie. Int. J. Plant Sci. 163, 785e792. Stinson, K.A., Campbell, S.A., Powell, J.R., Wolfe, B.E., Callaway, R.M., Thelen, G.C., Hallett, S.G., Prati, D., Klironomos, J.N., 2006. Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol. 4, 140e145. Tiwari, J.W.K., 1999. Exotic weed Prosopis juliflora in Gujarat and Rajasthan, India e boon or bane. Tigerpaper 26, 21e25. Vitousek, P.M., D’Antonio, C.M., Loope, L.L., Westbrooks, R., 1996. Biological invasions as global environmental change. Am. Sci. 84, 468e478. Zhao, H.L., Zhou, R.L., Su, Y.Z., Zhanga, H., Zhaoa, L., Drakec, S., 2007. Shrub facilitation of desert land restoration in the Horqin Sand Land of Inner Mongolia. Ecol. Eng. 31, 1e8.
Contents lists available at ScienceDirect
Journal of Arid Environments journal homepage: www.elsevier.com/locate/jaridenv
Impacts of native and invasive exotic Prosopis congeners on soil properties and associated flora in the arid United Arab Emirates Ali El-Keblawy a, *, Mahmoud Ali Abdelfatah b, c a
Department of Applied Biology, Faculty of Science, Sharjah University, P.O. Box 27272, Sharjah, United Arab Emirates Soil Quality Department, Environment Agency e Abu Dhabi, P.O. Box 45553, Abu Dhabi, United Arab Emirates c Soils and Water Sciences Department, Faculty of Agriculture, Fayoum University, P.O. Box 63514, Fayoum, Egypt b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 17 November 2012 Received in revised form 28 September 2013 Accepted 3 October 2013 Available online 26 October 2013
The native Prosopis cineraria and exotic invasive P. juliflora are present in arid habitats of the United Arab Emirates (UAE). The objective of this study was to assess the impacts of allelopathy and soil properties on plants associated with the two species in arid deserts. Density and other community attributes of the associated species were assessed beneath, at the margin and outside the canopies of 20 Prosopis individuals. Aqueous extracts of fresh and old leaves of both Prosopis species were assessed on germination of five native plants. Soil samples were collected from beneath and next to canopies of the two species and their chemical properties were analyzed. The effect on the associated flora was depressive for P. juliflora, but was positive for P. cineraria canopy. The depressive effect of P. juliflora was more obvious on the annual compared with perennial plants. The negative effect of the aqueous extract of P. juliflora was much greater on germination, especially for annual plants. Canopies of both species improved soil properties that would facilitate the association of other native plants. The allelopathic effect of P. juliflora, however, may override its facilitative effect and consequently resulted in a depressive effect on the associated flora. Ó 2013 Elsevier Ltd. All rights reserved.
Keywords: Allelopathy Desert habitats Invasive plants Native plants Soil salinity Species diversity
1. Introduction Desert shrubs and trees play a major role in stabilizing the fragile desert ecosystems in arid regions. In many deserts, trees are considered as keystone species as they support the life of many other faunal and floral species (Munzbergova and Ward, 2002). Desert trees can influence their understory vegetation in many ways, resulting in a broad range of detrimental or beneficial outcomes. The beneficial effects of desert trees on the environment beneath their canopies include the reduction in the extremes of environmental temperatures (Greenlee and Callaway, 1996), provision of suitable amounts of photosynthetically active radiation to understorey plants (Smith and Knapp, 2001), improved soil texture and nutrient content (Moro et al., 1997; Nobel, 1989; Pugnaire et al., 2004), increased soil moisture (Belsky, 1994) and protection against herbivory (McAuliffe, 1984). Conversely, desert trees can also have negative effects on seedling survival and establishment in their
* Corresponding author. Permanent address: Department of Biology, Faculty of Education in Al-Arish, Suez Canal University, Egypt. E-mail addresses: [email protected], [email protected] (A. ElKeblawy). 0140-1963/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jaridenv.2013.10.001
understorey community. These competitive interactions may be through light deprivation, competition for water and nutrients, or leaching of allelopathic compounds (Bais et al., 2003; Brewer, 2002; Moro et al., 1997; Nobel, 1989). Detrimental and beneficial mechanisms do not act in isolation from each other in nature. The relative importance of these two processes in a particular plant community determines the structure of that community (Callaway and Walker, 1997). Biological invasions are recognized as one of the most important causes of ecosystem degradation and biodiversity loss worldwide (Mack et al., 2001; Vitousek et al., 1996). The depressive effect of some exotic species on the associated flora has been attributed to allelopathy, which is an interference mechanism by which plants release chemicals that affect other plants (Bais et al., 2003; Brewer, 2002; Callaway and Ridenour, 2004). This allelopathic interference has been argued to be one of the mechanisms by which exotics may become successful invaders (Inderjit et al., 2008; Stinson et al., 2006). A congeneric, or phylogenetic, approach was used to examine allelopathy as a mechanism for invasion. This approach involves comparative studies of exotic species with natives in the same genus (Inderjit et al., 2008). Native plants typically do not share a co-evolutionary history with the exotic invasive species, and
2
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therefore greater allelopathic effects of the invasive are expected on the native plants in such ecosystems. The ‘novel weapons hypothesis’ indicated that allelochemicals produced by the invaders are new to the native plant communities (Bais et al., 2003; Callaway and Ridenour, 2004). Assessment of the impact of allelopathy of two congeneric species on the germination of their associated species might shed light on the mechanisms of the coexistence of native plants with native and exotic competitors. Only a few studies compared the allelopathic effects of invasive and native competitors on the associated native plants (but see Inderjit et al., 2008). Prosopis juliflora and P. cineraria are among a few trees growing in the arid deserts of the UAE and currently occupying the same habitats. They constitute a major ecological feature in the Northern Emirates of the UAE. P. cineraria is a slow growing tree native to the dry and arid regions of Arabia and India and is beneficial for the growth and development of other species (Abdel Bari et al., 2007). It is rarely, if ever, seen as a weedy species and has not been successfully introduced into other parts of the world (Pasiecznik et al., 2001). P. juliflora, however, is an exotic species from Central and South America and grows luxuriantly on sandy soils with high groundwater tables in the UAE. It has been introduced on a large scale in the artificial forests of the UAE because of its faster growth and soil-binding capacity. Recently, it has escaped plantations and come to dominate many plant communities, and is considered a weed. It is highly aggressive and coppices so well that it crowds out native vegetation (El-Keblawy and Al-Rawai, 2005, 2007; Tiwari, 1999). Both P. cineraria and P. juliflora possess phenolic compounds. However, the leaf leachates and extracts of P. juliflora showed allelopathic effects against native species in its invasion range, whereas extracts from leaves of P. cineraria collected and applied in the same way, do not (Goel and Behl, 1998; Inderjit et al., 2008; Kaur et al., 2012). A water-soluble extract from different parts of P. juliflora, including litter and rhizosphere soil, has resulted in the inhibition of seed germination of many species. However, most of the tested assay plants do not naturally grow near P. juliflora. For example, aqueous extracts from soil under the canopy and from different parts of P. juliflora inhibited germination and early seedling growth of various cultivars of Zea mays, Triticum aestivum and Albizia lebbeck (Noor et al., 1995). In addition, Al-Humaid and Warrag (1998) concluded that P. juliflora leaves contain water-soluble allelopathins that could inhibit seed germination and retard rates of germination and seedling growth in Cynodon dactylon. In pot studies of the allelopathic effects of leaf litter of P. juliflora, Chellamuthu et al. (1997) indicated that germination of black gram (Vigna mungo), and sorghum (Sorghum bicolor) was significantly reduced with the maximum reduction occurring at 2% incorporation of P. juliflora leaf litter. The selection of bioassay species is crucial to the study of allelopathy because the effect of biochemicals can vary dramatically among test species (Inderjit, 2006; Inderjit and Nilsen, 2003; Perry et al., 2005). The aims of the present study were to assess the impacts of (1) allelopathy of fresh and old leaves of the native P. cineraria and exotic invasive P. juliflora on the germination of five native plants naturally growing with them, (2) soil chemical properties beneath and around the two Prosopis species on their associated plants in the arid environment of the UAE. This is especially important as the two congers are growing together in the same soil type and have the same associated native plants. We assume that the differential response of the native plant germination to the allelochemicals of the two congers would help in understanding the extent of the detrimental effect of allelopathy in both species. In addition, it is assumed that the balance between the facilitative effect of soil properties and the negative effect of
allelopathy would also help in understanding the invasive ability of exotic P. juliflora. 2. Materials and methods 2.1. Study area A study site in Fujairah Emirate on the eastern coast of the UAE (25140 27.6800 N and 56 210 24.1400 E) was selected to ensure a reasonable degree of physiognomic homogeneity and with homogenous distribution and densities of both P. juliflora and P. cineraria. Individuals of the two species covering medium and large trees were selected for study. In some communities of P. cineraria that were invaded by P. juliflora, the invader was found to negatively affect the growth and vigor of the native P. cineraria. These places were excluded from the study. 2.2. Impacts on associated flora A total of 20 stands were located randomly around the two Prosopis species (10 stands for each). A Prosopis tree (P. juliflora or P. cineraria) was located near the center of each stand to serve as a focal point. The area of each stand was 225 m2 (15 15 m). In each stand, nine one m2 quadrats were distributed on three transects; 3 quadrats beneath; 3 at the margin; and 3 beyond the canopy of each selected Prosopis. A species list was compiled in each stand. The absolute density (number of plants of a certain species rooted within one m2) was estimated for each associated plant species beneath, at the margin and beyond the canopies of the two Prosopis species. Other community attributes were also estimated, including species number, species richness (average number of species per stand), and species evenness (estimated by ShannoneWeaver index). 2.3. Soil analysis In each stand, two composite soil samples were collected from the upper 10 cm of the soil, one from underneath (halfway between the trunk and the edge of the canopy) and another from at least 2 m outside the margin of the canopy. A total of 40 soil samples were collected and analyzed for this study. Soil samples were air dried, ground, homogenized, and sieved through a 2 mm sieve to remove large particles. Soil organic matter content, pH, salinity and the nutrients N, P, Na, and K were estimated. Organic matter content was estimated using loss of mass by combustion at 430 C on the <2 mm soil fraction. Soil water extracts (1:2.5 of soil:water) were prepared for determination of electrical conductivity (EC) and pH using conductivity and pH meters. Available nitrogen was extracted using 2 M KCl and determined by the micro-Kjeldahl method. Available phosphorous was estimated using Olsen’s solution (sodium bicarbonate) as an extracting agent. Na and K were estimated by using flame photometry. These methods are outlined in Black (1965). 2.4. Assessment of allelopathic effects Fresh and old leaf samples were collected from underneath P. cineraria and P. juliflora individuals in the studied community. Fresh leaves fallen within one year were distinguished by their very light color, while leaves older than one year were darker. All samples were air dried at room temperature and subsamples were ground to pass through a 3-mm sieve. Dried materials from all samples were extracted in distilled water at 25 g 100 ml1 for 24 h at 25 C. Following extraction, coarse plant materials were removed with a 2-mm sieve. Extracts were then passed through a
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2.5. Statistical analysis Differences in the total number of species in the various positions from the individual Prosopis plants (beneath, edge, and beyond the canopy) were assessed using c2 tests. One-way ANOVAs were used to compare the density of associated species at different positions from Prosopis canopies. Two-way analyses of variance
Number of associated species
A: Number of associated species 20 15 10 5 0
P. cineraria P. juliflora Prosopis sp
Shannon-Weaver index
2.0 1.5 1.0 0.5 0.0
3. Results The overall number of associated species did not differ between the stands of the two Prosopis sp. (20 species for P. juliflora and 21 species for P. cineraria). However, the number of associated species was significantly reduced beneath P. juliflora (c2 ¼ 6.68, P < 0.05), but not beneath P. cineraria canopies (c2 ¼ 0.054, P > 0.05). The number of species beneath P. juliflora was almost one third the number of species beneath P. cineraria and in the open stands between the canopies (Fig. 1 a). Results of two-way ANOVAs showed significant effects for both Prosopis sp., position from the canopy and their interaction on evenness, and richness and density of associated species (P < 0.05, Table 1). The exception was the impact of Prosopis sp. on richness of associated species (P > 0.05). In P. juliflora, evenness, richness and density of associated species were significantly lower beneath the canopy, compared with outside and at the margin of the
C: Richness of associated species
P. cineraria P. juliflora Prosopis sp
8 6 4 2 0
P. cineraria P. juliflora Prosopis sp
D: Density of associated species (number/100m2) Density of associated species
B: Evenness of associated species
(ANOVA) were used to evaluate the effect of the main factors (Prosopis species and position from the canopy) on species density, evenness, and richness, and soil properties. Three-way ANOVA was used to assess the impacts of Prosopis species, leaf age and extract concentration on final germination percentage of the five assayed native plants. Species density was square-root-transformed to meet the assumption of the ANOVA. This transformation improved the normality of the distribution of the data. ShapiroeWilk test was used to check the normality of the data distribution. Tukey’s Honest Significant Difference post hoc test was used for comparison of means when statistical significant differences (P < 0.05) were observed. All statistical methods were performed using SYSTAT, version 11.0.
Richness of associated species
Whatman filter paper and centrifuged at 12,000 rpm for 20 min. These 25% (w/v) extracts of dried materials were further diluted to obtain 2, 4, 6 and 8% solutions. Seeds of five native plants growing naturally with the studied populations of P. juliflora and P. cineraria were collected. The plants include one annual herb (Plantago ovata), two annual grasses (Tragus racemosus and Eragrostis barrelieri) and two perennial grasses (Sporobolus arabicus and Cenchrus ciliaris). Seeds were separated from the litter and dry stored in brown paper pages until their use in germination tests. The germination was conducted in 9 cm Petri-dishes containing one disk of Whatman No. 1 filter paper, with 10 ml of test solution. Each dish was wrapped with Para film as an added precaution against loss of water by evaporation. For each species, dishes were arranged in an incubator set at 15/25 C in 12 h dark/ 12 h light, with light coincide with 25 C in a completely randomized design with two Prosopis species (P. juliflora and P. cineraria) and four concentrations of each extract. Three replicate dishes were used for each treatment, each with 25 seeds. Sterile distilled water was used as a control. Radical emergence was the criterion for germination. Germinated seedlings were counted and removed every second day for 20 days following seeds sowing.
3
1000 750 500 250 0
P. cineraria P. juliflora Prosopis sp
Fig. 1. Effects of position relative to the canopy of Prosopis juliflora and Prosopis cineraria on total number of species, evenness, richness and density (number/100 m2) of associated species. Black bars ¼ Beneath canopy, White bars ¼ margin of canopy and gray bars ¼ outside of canopy.
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Table 1 Two way ANOVAs (F-values) for the effects of Prosopis sp., position from the canopy, and their interaction on evenness, richness and density of associated species. *: P < 0.05, **: P < 0.01, and ***: P < 0.001. Community attributes
Species (S)
Position from canopy (P)
S*P
Species evenness Species richness Species density
4.40* 2.41 8.25**
9.41*** 22.30*** 28.8***
5.91* 8.42*** 23.47***
The densities of both C. ciliaris and S. arabicus did not differ significantly between beneath and beyond the canopies (Table 2). The number of annuals that attained significantly lower densities under P. juliflora canopies (9 species) was significantly greater than the number of perennials (2 species) (c2 ¼ 5.680, P < 0.05; the 11 perennials and 9 annuals recorded with P. juliflora were used as expected values). 3.2. Effect of P. cineraria on species composition
canopy. Conversely, evenness and density did not differ significantly at the margin versus beyond the canopies of P. Juliflora individuals (Fig. 1). In P. cineraria, evenness and richness of associated species did not differ significantly beneath and at the margin of the canopy, but both were significantly lower compared with beyond the canopy. However, the density was significantly greater at the margin, compared with beneath and beyond the canopy (Fig. 1). The comparison of the two Prosopis species indicates that both evenness and richness of associated species were significantly greater underneath P. cineraria compared with underneath P. juliflora canopy. However, these variables did not differ between the margin and beyond the canopies of the two Prosopis species (Fig. 1). 3.1. Effect of P. juliflora on species composition One-way ANOVAs showed that the density of 13 species, out a total of the 20 species recorded in the P. juliflora community, was significantly reduced beneath, compared with outside the canopies (P < 0.05, Table 2). Most of these species were not present under the canopies. In addition, five other species were completely absent under P. juliflora canopies, so their densities did not differ significantly beyond vs. beneath the canopy (P > 0.05). The depressive impact of the P. juliflora canopy was less obvious on perennial plants, especially grasses, compared with annual plants. Six species attained a minimum of eight individuals per 100 m2; two perennial grasses (C. ciliaris, S. arabicus), one perennial tree (P. juliflora), one perennial herb (Aizoon canariense) and two annual herbs (T. racemosus and Gypsophila bellidifolia).
Table 2 Effect of Prosopis juliflora canopy on density of associated species (number (number of individuals per 100 m2). *: P < 0.05, **: P < 0.01, and ***: P < 0.001. Species
Acacia tortilis Aizoon canariense Amaranthus viridis Arnebia hispidissima Astragalus annularis Cenchrus ciliaris Eragrostis barrelieri Gypsophila bellidifolia Launaea capitata Malva parviflora Paronychia arabica Plantago ovata Prosopis juliflora Rhazya stricta Spergularia marina Sporobolus arabicus Stipagrostis plumosa Tephrosia apollinea Tragus racemosus Tribulus terrestris a
Life cyclea
P P A A A P A A P A A A P P A P P P A A
A ¼ annuals, P ¼ perennials.
The impact of P. cineraria canopy on density was significant for 13 species, out a total of the 21 species recorded in its stands (P < 0.05, Table 3). The densities were significantly increased at the canopy margin for nine species and beneath the canopies for two species and both at margin and beneath the canopies for one species. However, the density was significantly reduced beneath vs. beyond the canopy in only one species (E. barrelieri, Table 3). 3.3. Effect of Prosopis species on soil properties Two-way ANOVA indicated significant effects for Prosopis species on EC, Na and organic C % (P < 0.05). In addition, position from canopy and the interaction between species and position from canopy had significant effects on most of the studied soil characters (P < 0.05, Appendix A). Values of K, N, organic C %, and P were significantly greater beneath, compared to beyond the canopies of both P. juliflora and P. cineraria. Relative position to the canopy significantly affected pH, EC, Na, HCO3 and organic C % in P. juliflora, but not in P. cineraria. Values of EC, HCO3 and organic C % were significantly increased, but pH significantly decreased beneath, compared with outside P. juliflora canopy. The P. cineraria canopy, however, did not affect any of these soil factors (Table 4). 3.4. Impacts of aqueous extracts on seed germination of five native plants Three-way ANOVA showed significant effects for the main factors (Prosopis species, leaf age and extract concentration) and most of their interactions on final germination percentage of the Table 3 Effect of Prosopis cineraria canopy on density of associated species (number of individuals per 100 m2). *: P < 0.05, **: P < 0.01, and ***: P < 0.001. Species
Life cyclea
Acacia tortilis Aeluropus massauensis Aizoon canariense Amaranthus viridis Astragalus annularis Cenchrus ciliaris Chenopodium murale Chrozophora oblongifolia Eragrostis barrelieri Euphorbia serpens Gypsophila bellidifolia Launaea capitata Lotus garcinii Paronychia arabica Plantago ovata Prosopis juliflora Spergularia marina Sporobolus arabicus Stipa capensis Tragus racemosus Tribulus terrestris
P P P A A P A P A A A P P A A P A P P A A
Position from canopy Beneath
Margin
Beyond
0.0 12.5 0.0 0.0 0.0 25.0 0.0 8.3 0.0 0.0 0.0 0.0 9.1 0.0 0.0 12.0 0.0 0.0 18.0 0.0
17.0 72.0 0.0 8.3 0.0 58.3 0.0 0.0 8.3 8.3 33.3 65.0 21.7 8.3 0.0 14.7 7.2 0.0 35.0 0.0
8.0 90.8 36.7 38.3 8.3 16.7 38.3 25.0 0.0 18.3 16.7 40.7 31.7 8.3 13.3 10.0 9.3 16.7 45.0 21.6
F *** * *** *** ** * *** ** *** *** *
* *
a
A ¼ annuals, P ¼ perennials.
Position from canopy Beneath
Margin
Beyond
0.0 23.0 67.7 21.2 16.7 38.7 24.2 0.0 13.3 10.2 66.67 0.0 0.0 0.0 6.7 12.7 54.4 15.0 7.5 12.0 5.0
12.1 0.0 34.3 112 100 36.6 75.8 100 14.4 43.4 22.2 0.0 32.3 0.0 53.3 13.3 195.5 16.7 33.3 17.0 32.3
0.0 10.2 33.3 13 11.1 22.8 21.4 0.0 68.9 12.1 20.3 11.1 31.0 33.3 10.0 2.7 113.3 16.7 0.0 9.0 21.2
F
* *** * *** * *** *** ***
*** * *** ** ***
A. El-Keblawy, M.A. Abdelfatah / Journal of Arid Environments 100-101 (2014) 1e8
5
Table 4 Effects of Prosopis juliflora and Prosopis cineraria canopies on the mean values of some soil characters. Species
Place from canopy
pH
EC (dS m1)
HCO3 (M eq l1)
Na (meq l1)
K (meq l1)
N (ppm)
P (ppm)
Organic C (%)
P. juliflora
Beyond Beneath Beyond Beneath
7.43a 7.04b 7.43a 7.35a
1.40b 6.61a 1.40a 2.41a
1.16a 1.26a 1.16a 1.00a
12.6b 21.7a 12.6a 13.5a
6.5b 9.35a 6.5b 8.9a
2.7b 4.6a 2.7b 3.5a
0.41a 0.56a 0.41b 065a
11.38b 24.94a 11.38b 14.80b
P. cineraria
five studies species (P < 0.05, Appendix B). Generally, seeds of the different species treated with aqueous extracts of P. juliflora attained significantly lower germination, compared with their controls (seeds without treatments) and seeds treated with different concentrations of P. cineraria extracts. Higher concentrations of old leaves of P. juliflora were significantly more effective in inhabiting the germination of C. ciliaris and S. arabicus, compared with higher concentrations of fresh leaves. In E. barrelieri, higher concentrations of fresh leaves in both species were more effective, compared with the same concentrations of old leaves (Fig. 2). Seeds of the two perennial grasses C. ciliaris and S. arabicus germinated in all concentrations of both P. cineraria and P. juliflora extracts. The final germination of the non-treated seeds (control) of the two species didn’t differ from most concentrations of fresh and old leaf extracts of P. cineraria. However, the germination of the two species attained significantly lower values in most concentrations of P. juliflora (Fig. 2). The seed germination of the two annual grasses (T. racemosus and E. barrelieri) differs according to Prosopis species, leaf age and extracts concentration. Germination of T. racemosus seeds was significantly reduced in higher concentrations (6% and 8%) of both fresh and old leaf extracts of both P. juliflora and P. cineraria, but seeds of E. barrelieri attained greater germination in up to 8% of old leaf extract of the Prosopis species. The result indicates that the annual E. barrelieri grass can tolerate the fresh, but not the old extract of the two Prosopis species (Fig. 2). The germination of the annual P. ovata was completely inhibited in 6% and 8% of both fresh and old leaf extracts of P. juliflora. However, the seeds of this species were able to germinate in up to 8% extract of P. cineraria leaves, especially the old leaves (Fig. 2). 4. Discussion The results of our study indicated that P. juliflora significantly reduced the evenness, richness and density of the associated plants beneath, compared with open places beyond their canopies. However, P. cineraria either did not reduce these variables or significantly increased them. These results support other studies showed interference effects for P. juliflora and facilitative effects for P. cineraria. For example, in the artificial forests of the UAE, the exotic Eucalyptus and P. juliflora trees had resulted in significant reductions in species diversity and abundance of understory species, compared to the native P. cineraria and Acacia arabica (ElKeblawy and Ksiksi, 2005). In addition, in a semiarid plantation in Haryana, India, Jalota et al. (2000) reported that only two species dominated P. juliflora plantations, but 25 different species were found in the indigenous Dalbergia sissoo plantations. Another study in India investigated the vegetation succession on salt-affected soils after five years of plantation with two exotic salt bushes and three tree species, and found that only three species were recorded with P. juliflora, compared to 7e8 species with other trees (Arya, 2003). Furthermore, Aggarwal et al. (1976) found that the canopies of the invasive P. juliflora had far fewer understory species than any of four other forestry trees studied, whereas the native congener,
P. cineraria, was associated with higher understory diversity than any other species. Recently, Kaur et al. (2012) reported that P. cineraria had much weaker effects on species richness compared with P. juliflora. Many studies have suggested that allelopathy contributes to the ability of exotic species to become dominant in invaded plant communities (Adetayo et al., 2005; Inderjit et al., 2008). The greater depressive effect of P. juliflora on the associated species, compared to its congener P. cineraria, could be attributed to the more susceptibility of the associated species to specific allelochemicals produced by the invader, compared with the native tree. According to the ‘novel weapons hypothesis’, these chemicals are new to the native plant communities in the UAE (Bais et al., 2003; Callaway and Ridenour, 2004). Similar results have been reported for another two congeners Lantana camara and L. indica. The first species, which is exotic invasive throughout Asia, has allelopathic effects, but its corresponding native congener L. indica does not have the same strong effects on native species in India (Inderjit et al., 2008). Our study showed that seed germination of five native plants associated with the Prosopis species was significantly inhibited with the aqueous extracts of P. juliflora, compared with control (non-treated) seeds and seeds treated with different concentrations of P. cineraria extracts. Conversely, seeds of four native species germinated to significant proportions in the extract of both fresh and old leaves of P. cineraria, especially in the lower concentrations (2% and 4%, Fig. 2). Chellamuthu et al. (1997) suggested that the allelopathic effect of P. juliflora leaf litter is due to the presence of phenolic compounds. Nakano et al. (2001) suggested that L-tryptophan may play an important role in the allelopathy of P. juliflora leaves. The content of L-tryptophan in the exudates of freeze-dried mesquite leaves (1 mg eq.) was estimated to be 4.8 103 mM (Nakano et al., 2001). In addition, Nakano et al. (2004) isolated syringin and (-)-lariciresinol from the aqueous foliar leachate of P. juliflora, and also detected these chemicals in rhizosphere soil. Several studies reported the presence of allelopathic compounds in both P. juliflora and P. cineraria. For example, Kaur et al. (2012) detected L-tryptophan in leaf leachates of both P. juliflora and P. cineraria, but the amounts were 73% higher in leaf leachate of the former than that of the latter. Similarly, Inderjit et al. (2008) compared soils collected from the rhizospheres of the two Prosopis species and found that soils beneath the exotic P. juliflora contained 63.2% higher concentrations of total phenolics than soil beneath the native P. cineraria. These findings could explain the relatively lower allelopathic effects of higher concentration of P. cineraria, aqueous extracts (6% and 8%), especially on seed germination of the annuals T. racemosus and P. ovata (Fig. 2). In the hyper-arid habitats of the UAE, there is a noticeable accumulation of litter underneath the P. juliflora, compared with P. cineraria canopies (El-Keblawy, personal observation). Litter falling to the ground during periods of stress can alter the physical, chemical, and biotic environment in which seeds germinate and seedlings grow (Facelli and Carson, 1991).
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Prosopis cineraria
Prosopis juliflora 100 Final germination (%)
Final germination (%)
Cenchrus ciliaris
100 80 60 40 20 0
0
Final germination (%)
Final germination (%)
Sporobolus arabicus
60 40 20 0
Final germination (%)
Final germination (%)
Eragrostis barrelieri
60 40 20 0
80 60 40 20 0
2 4 6 8 Extract concentration (%)
0
2 4 6 8 Extract concentration (%)
0
2 4 6 8 Extract concentration (%)
0
2 4 6 8 Extract concentration (%)
40 20
80 60 40 20
80 60 40 20 0
2 4 6 8 Extract concentration (%)
100 Final germination (%)
100 Final germination (%)
0
60
100 Final germination (%)
Final germination (%)
Tragus racemosus
2 4 6 8 Extract concentration (%)
80
0
2 4 6 8 Extract concentration (%)
100
Plantago ovata
0
100
80
80 60 40 20 0
20
0
2 4 6 8 Extract concentration (%)
100
0
40
100
80
0
60
0
2 4 6 8 Extract concentration (%)
100
0
80
0
2 4 6 8 Extract concentration (%)
80 60 40 20 0
Fig. 2. Effects of different concentrations of extracts of fresh and old leaves of Prosopis cineraria and Prosopis juliflora on final germination percentage (mean SE) of five desert species of the UAE. Gray bars ¼ control, black bars ¼ fresh leaves and hatched bars ¼ old leaves.
A. El-Keblawy, M.A. Abdelfatah / Journal of Arid Environments 100-101 (2014) 1e8
Consequently, litter can have a significant influence on emergence and growth of understorey species. In some exotic invaders, litter leachates have shown negative effects on seed germination, establishment and seedling growth of associated species (Chellamuthu et al., 1997). The greater accumulation of litter underneath the P. juliflora canopy could partially explain the greater inhibition of understory vegetation of this species. Kaur et al. (2012) reported that experimentally applied P. juliflora litter caused far greater mortality of native Indian species than litter from P. cineraria. In addition, P. juliflora leaf leachate showed negative effects on root growth of three common crop species of north-west India whereas P. cineraria leaf leachate had positive effects (Kaur et al., 2012). There is strong evidence from arid lands of nurse plants that facilitate establishment of other species (Franco and Nobel, 1989; McAuliffe, 1984). The nurse plant’s canopy structure may influence the success of seedling establishment, in particular in relation to shade intensity and rainfall interception (Padilla and Pugnaire, 2006). In P. cineraria, density of associated species was significantly greater at the margin, compared with beneath and beyond the canopy (Fig. 1). Similarly, the depressive effect of P. juliflora canopy was diminished at the margin; evenness and density did not differ significantly at the margin versus beyond the canopies of both Prosopis species. This suggests that the microenvironment at the margin of the canopies is more favorable, compared with both underneath and beyond the canopies. During small precipitation events, canopies might limit water availability in their understories by intercepting rainwater and directing it to the areas at the margins of canopies through flow along branches and leaves, making the soil at the margin wetter than in open and underneath the canopies (Padilla and Pugnaire, 2006). The pattern of higher soil fertility under canopies of desert shrubs and trees, compared with in adjacent open areas, is well documented in arid lands (Zhao et al., 2007). Many Prosopis species create “resource islands” with higher levels of organic matter and other macro-nutrients in soils beneath their canopies, which makes them stronger facilitators for other species (Kaur et al., 2012; Rossi and Villagra, 2003). For example, Kaur et al. (2012) showed that both P. juliflora and P. cineraria form resource islands by accumulating total organic N and organic carbon in their rhizosphere soil. In addition, Aggarwal et al. (1993) found that soil nitrogen, phosphorus, and potassium were higher under P. cineraria canopies than in open fields. Our results showed significant increases in the concentrations of K, N and P beneath, compared with beyond the canopies of both P. juliflora and P. cineraria. Unlike P. cineraria, P. juliflora increased soluble salts (EC) and decreased the pH underneath their canopy. Kaur et al. (2012) arrived to a similar result, regarding the soluble salts. The significant decrease in soil pH under the canopy of P. juliflora could be attributed to acidic nature of phenolic compounds. Species interactions involve a complex balance of competition (“negative”) and facilitation (“positive”) interactions (Brooker and Callaghan, 1998). Facilitation and interference interactions do not occur in isolation from each other. The overall effect of one species on another may be dependent on physical factors and the combination of competition for different resources, allelochemicals released into the environment, and facilitative factors such as shade and protection from herbivory (Callaway et al., 1991). In deserts, several shrubs have facilitative effects on the growth of some associated annuals, but also produce allelochemicals that suppress the growth of the same annuals (Callaway and Walker, 1997). In the present study, both Prosopis species have facilitative effects in relation to the available nutrients; their canopies increased the most important macronutrients K, N and P. In addition, both species increased the
7
organic matter contents (the increase was significant only in P. juliflora), which would also increase the water holding capacity that would improve soil texture and increase soil moistures. However, it appears that the allelopathic effects of the litters of P. juliflora may override its potential positive effects on soil fertility. Phenolic compounds of the allelochemicals in soils could reduce the water and nutrients uptake. For example, net uptake of P, K, and water by cucumber seedlings was reduced 57, 75, and 29%, respectively, when the whole root system was exposed to ferulic acid, an allelopathic phenolic acid. In addition, plant transpiration was reduced in a linear manner as the fraction of the cucumber roots in contact with ferulic acid increased (Lyu and Blum, 1990). The relative importance of facilitative and competitive interactions in a particular plant community determines the structure of that community (Callaway and Walker, 1997; Callaway et al., 1991). Our study showed a less depressive impact for the P. juliflora canopy on perennial plants, especially grasses, compared with annual plants. Similarly, Jalota et al. (2000) indicated that the two dominated species in P. juliflora plantations in the semi-arid Haryana in India were the perennial grasses Dactyloctenium aegyptium and Dichanthium annulatum. The positive presence of the perennial grasses C. ciliaris and S. arabicus that was observed in our study in the neighborhood area of P. juliflora, compared with annual plants, could be attributed partially to the high tolerance of the seeds of these plants during the germination stage to the presence of allelochemicals released from the leaves of the invader. Both the two perennial grasses germinated to high proportion, even in the highest concentration of the aqueous extract (8%) of the old and fresh leaves of P. juliflora. In addition, the greater ability of the perennial grasses, compared with annuals, to capitalize on more nutrients could be also account for their higher density underneath P. juliflora canopy. Conversely, the significant reduction in the density of the annuals underneath and at the margin of the P. juliflora could be explained mainly by the lower tolerance of the germination stage of these species to the released allelochemicals. The results of the study indicated significant reduction in germination of the seeds of the three annuals (E. barrelieri, T. racemosus and P. ovata) in most concentrations of fresh or old leaves or both of P. juliflora. Acknowledgments The authors would like to thank Dr Colin Pain, Honorary Assistant Professor at the University of Sevilla, Spain, for his critical revision of the manuscript. Thanks are also extended to Prof Inderjit Singh, University of Delhi, India, for his valuable comments on the manuscripts. Appendices Appendix A. Results of two-way ANOVA (F-values) for the effects of Prosopis juliflora and Prosopis cineraria canopies on some soil characters. ns: insignificant different at P ¼ 0.05, *: P < 0.05, ** and P < 0.01, and ***: P < 0.001.
Source of variation
pH
EC
HCO3
Na
K
N
P
Organic C
Species (S) Position from canopy (P) S*P
ns ns
* **
ns ns
* *
ns *
ns *
ns *
* *
**
*
ns
*
*
*
**
**
8
A. El-Keblawy, M.A. Abdelfatah / Journal of Arid Environments 100-101 (2014) 1e8
Appendix B. Results of three-way ANOVA (F-values) for the effects of species (Prosopis cineraria and P. juliflora), leaves age and extract concentration on final germination of seeds of five plants in the UAE. *: P < 0.05, **: P < 0.01, and ***: P < 0.001.
Source Species (S) Leaf age (A) Extract concentration (C) S*A S*C A*C S*A*C Error
df
Tragus racemosus
Eragrostis barrelieri
Plantago ovata
Sporobolus arabicus
Cenchrus ciliaris
1 1 3
154.9*** 50.6*** 460.9***
330.9*** 526.0*** 10.9***
77.9*** 5.96* 44.9***
238.3*** 17.5*** 77.5***
171.9*** 26.2*** 108.8***
1 3 3 3 48
54.2*** 5.0** 7.3*** 10.5*
239.6*** 2.29 6.14** 0.31
38.4*** 7.8*** 35.6*** 1.07
103.5*** 27.8*** 4.13** 5.98**
25.1*** 15.9*** 2.84* 1.25
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