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Journal of Arid Environments 100-101 (2014) 1e8
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Journal of Arid Environments
journal homepage: www.elsevier .com/locate/ jar idenv
Impacts of native and invasive exotic Prosopis congeners on soilproperties and associated flora in the arid United Arab Emirates
Ali El-Keblawy a,*, Mahmoud Ali Abdelfatah b,c
aDepartment of Applied Biology, Faculty of Science, Sharjah University, P.O. Box 27272, Sharjah, United Arab Emiratesb Soil Quality Department, Environment Agency e Abu Dhabi, P.O. Box 45553, Abu Dhabi, United Arab Emiratesc Soils and Water Sciences Department, Faculty of Agriculture, Fayoum University, P.O. Box 63514, Fayoum, Egypt
a r t i c l e i n f o
Article history:Received 17 November 2012Received in revised form28 September 2013Accepted 3 October 2013Available online 26 October 2013
Keywords:AllelopathyDesert habitatsInvasive plantsNative plantsSoil salinitySpecies diversity
* Corresponding author. Permanent address: DepaEducation in Al-Arish, Suez Canal University, Egypt.
E-mail addresses: [email protected], akKeblawy).
0140-1963/$ e see front matter � 2013 Elsevier Ltd.http://dx.doi.org/10.1016/j.jaridenv.2013.10.001
a b s t r a c t
The native Prosopis cineraria and exotic invasive P. juliflora are present in arid habitats of the United ArabEmirates (UAE). The objective of this study was to assess the impacts of allelopathy and soil properties onplants associated with the two species in arid deserts. Density and other community attributes of theassociated species were assessed beneath, at the margin and outside the canopies of 20 Prosopis in-dividuals. Aqueous extracts of fresh and old leaves of both Prosopis species were assessed on germinationof five native plants. Soil samples were collected from beneath and next to canopies of the two speciesand their chemical properties were analyzed. The effect on the associated flora was depressive forP. juliflora, but was positive for P. cineraria canopy. The depressive effect of P. juliflora was more obviouson the annual compared with perennial plants. The negative effect of the aqueous extract of P. juliflorawas much greater on germination, especially for annual plants. Canopies of both species improved soilproperties 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 theassociated flora.
� 2013 Elsevier Ltd. All rights reserved.
1. Introduction
Desert shrubs and trees play a major role in stabilizing thefragile desert ecosystems in arid regions. In many deserts, trees areconsidered as keystone species as they support the life of manyother faunal and floral species (Munzbergova and Ward, 2002).Desert trees can influence their understory vegetation in manyways, resulting in a broad range of detrimental or beneficial out-comes. The beneficial effects of desert trees on the environmentbeneath their canopies include the reduction in the extremes ofenvironmental temperatures (Greenlee and Callaway, 1996), pro-vision of suitable amounts of photosynthetically active radiation tounderstorey plants (Smith and Knapp, 2001), improved soil textureand nutrient content (Moro et al., 1997; Nobel,1989; Pugnaire et al.,2004), increased soil moisture (Belsky,1994) and protection againstherbivory (McAuliffe, 1984). Conversely, desert trees can also havenegative effects on seedling survival and establishment in their
rtment of Biology, Faculty of
[email protected] (A. El-
All rights reserved.
understorey community. These competitive interactions may bethrough light deprivation, competition for water and nutrients, orleaching of allelopathic compounds (Bais et al., 2003; Brewer, 2002;Moro et al., 1997; Nobel, 1989). Detrimental and beneficial mech-anisms do not act in isolation from each other in nature. The rela-tive importance of these two processes in a particular plantcommunity determines the structure of that community (Callawayand Walker, 1997).
Biological invasions are recognized as one of the most importantcauses of ecosystem degradation and biodiversity loss worldwide(Mack et al., 2001; Vitousek et al., 1996). The depressive effect ofsome exotic species on the associated flora has been attributed toallelopathy, which is an interference mechanism by which plantsrelease chemicals that affect other plants (Bais et al., 2003; Brewer,2002; Callaway and Ridenour, 2004). This allelopathic interferencehas been argued to be one of the mechanisms bywhich exotics maybecome successful invaders (Inderjit et al., 2008; Stinson et al.,2006).
A congeneric, or phylogenetic, approach was used to examineallelopathy as a mechanism for invasion. This approach involvescomparative studies of exotic species with natives in the samegenus (Inderjit et al., 2008). Native plants typically do not share aco-evolutionary history with the exotic invasive species, and
A. El-Keblawy, M.A. Abdelfatah / Journal of Arid Environments 100-101 (2014) 1e82
therefore greater allelopathic effects of the invasive are expectedon the native plants in such ecosystems. The ‘novel weapons hy-pothesis’ indicated that allelochemicals produced by the invadersare new to the native plant communities (Bais et al., 2003;Callaway and Ridenour, 2004). Assessment of the impact of alle-lopathy of two congeneric species on the germination of theirassociated species might shed light on the mechanisms of thecoexistence of native plants with native and exotic competitors.Only a few studies compared the allelopathic effects of invasiveand native competitors on the associated native plants (but seeInderjit et al., 2008).
Prosopis juliflora and P. cineraria are among a few trees growingin the arid deserts of the UAE and currently occupying the samehabitats. They constitute a major ecological feature in the NorthernEmirates of the UAE. P. cineraria is a slow growing tree native to thedry and arid regions of Arabia and India and is beneficial for thegrowth and development of other species (Abdel Bari et al., 2007).It is rarely, if ever, seen as a weedy species and has not been suc-cessfully introduced into other parts of the world (Pasiecznik et al.,2001). P. juliflora, however, is an exotic species from Central andSouth America and grows luxuriantly on sandy soils with highgroundwater tables in the UAE. It has been introduced on a largescale in the artificial forests of the UAE because of its faster growthand soil-binding capacity. Recently, it has escaped plantations andcome to dominate many plant communities, and is considered aweed. It is highly aggressive and coppices so well that it crowds outnative 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 showedallelopathic effects against native species in its invasion range,whereas extracts from leaves of P. cineraria collected and appliedin the same way, do not (Goel and Behl, 1998; Inderjit et al.,2008; Kaur et al., 2012). A water-soluble extract from differentparts of P. juliflora, including litter and rhizosphere soil, hasresulted in the inhibition of seed germination of many species.However, most of the tested assay plants do not naturally grownear P. juliflora. For example, aqueous extracts from soil under thecanopy and from different parts of P. juliflora inhibited germi-nation and early seedling growth of various cultivars of Zea mays,Triticum aestivum and Albizia lebbeck (Noor et al., 1995). Inaddition, Al-Humaid and Warrag (1998) concluded that P. julifloraleaves contain water-soluble allelopathins that could inhibit seedgermination and retard rates of germination and seedling growthin Cynodon dactylon. In pot studies of the allelopathic effects ofleaf litter of P. juliflora, Chellamuthu et al. (1997) indicated thatgermination of black gram (Vigna mungo), and sorghum (Sorghumbicolor) was significantly reduced with the maximum reductionoccurring at 2% incorporation of P. juliflora leaf litter. The selec-tion of bioassay species is crucial to the study of allelopathybecause the effect of biochemicals can vary dramatically amongtest species (Inderjit, 2006; Inderjit and Nilsen, 2003; Perry et al.,2005). The aims of the present study were to assess the impactsof (1) allelopathy of fresh and old leaves of the native P. cinerariaand exotic invasive P. juliflora on the germination of five nativeplants naturally growing with them, (2) soil chemical propertiesbeneath and around the two Prosopis species on their associatedplants in the arid environment of the UAE. This is especiallyimportant as the two congers are growing together in the samesoil type and have the same associated native plants. We assumethat the differential response of the native plant germination tothe allelochemicals of the two congers would help in under-standing the extent of the detrimental effect of allelopathy inboth species. In addition, it is assumed that the balance betweenthe facilitative effect of soil properties and the negative effect of
allelopathy would also help in understanding the invasive abilityof exotic P. juliflora.
2. Materials and methods
2.1. Study area
A study site in Fujairah Emirate on the eastern coast of the UAE(25�140 27.6800 N and 56�210 24.1400 E) was selected to ensure areasonable degree of physiognomic homogeneity and with ho-mogenous distribution and densities of both P. juliflora andP. cineraria. Individuals of the two species covering medium andlarge trees were selected for study. In some communities ofP. cineraria that were invaded by P. juliflora, the invader was foundto 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 twoProsopis species (10 stands for each). A Prosopis tree (P. juliflora orP. cineraria) was located near the center of each stand to serve as afocal point. The area of each stand was 225 m2 (15 � 15 m). In eachstand, nine one m2 quadrats were distributed on three transects; 3quadrats beneath; 3 at the margin; and 3 beyond the canopy ofeach selected Prosopis. A species list was compiled in each stand.The absolute density (number of plants of a certain species rootedwithin one m2) was estimated for each associated plant speciesbeneath, at the margin and beyond the canopies of the two Prosopisspecies. Other community attributes were also estimated, includingspecies number, species richness (average number of species perstand), and species evenness (estimated by ShannoneWeaverindex).
2.3. Soil analysis
In each stand, two composite soil samples were collected fromthe upper 10 cm of the soil, one from underneath (halfway betweenthe trunk and the edge of the canopy) and another from at least 2 moutside the margin of the canopy. A total of 40 soil samples werecollected and analyzed for this study. Soil samples were air dried,ground, homogenized, and sieved through a 2 mm sieve to removelarge particles. Soil organic matter content, pH, salinity and thenutrients N, P, Na, and K were estimated. Organic matter contentwas 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) wereprepared for determination of electrical conductivity (EC) and pHusing conductivity and pHmeters. Available nitrogenwas extractedusing 2 M KCl and determined by the micro-Kjeldahl method.Available phosphorous was estimated using Olsen’s solution (so-dium bicarbonate) as an extracting agent. Na and K were estimatedby using flame photometry. These methods are outlined in Black(1965).
2.4. Assessment of allelopathic effects
Fresh and old leaf samples were collected from underneathP. cineraria and P. juliflora individuals in the studied community.Fresh leaves fallen within one year were distinguished by theirvery light color, while leaves older than one year were darker. Allsamples were air dried at room temperature and subsampleswere ground to pass through a 3-mm sieve. Dried materials fromall samples were extracted in distilled water at 25 g 100 ml�1 for24 h at 25 �C. Following extraction, coarse plant materials wereremoved with a 2-mm sieve. Extracts were then passed through a
A. El-Keblawy, M.A. Abdelfatah / Journal of Arid Environments 100-101 (2014) 1e8 3
Whatman filter paper and centrifuged at 12,000 rpm for 20 min.These 25% (w/v) extracts of dried materials were further dilutedto obtain 2, 4, 6 and 8% solutions. Seeds of five native plantsgrowing naturally with the studied populations of P. juliflora andP. cineraria were collected. The plants include one annual herb(Plantago ovata), two annual grasses (Tragus racemosus and Era-grostis barrelieri) and two perennial grasses (Sporobolus arabicusand Cenchrus ciliaris). Seeds were separated from the litter anddry stored in brown paper pages until their use in germinationtests.
The germination was conducted in 9 cm Petri-dishes contain-ing one disk of Whatman No. 1 filter paper, with 10 ml of testsolution. Each dish was wrapped with Para film as an addedprecaution 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 ran-domized design with two Prosopis species (P. juliflora andP. cineraria) and four concentrations of each extract. Three repli-cate dishes were used for each treatment, each with 25 seeds.Sterile distilled water was used as a control. Radical emergencewas the criterion for germination. Germinated seedlings werecounted and removed every second day for 20 days followingseeds sowing.
2.5. Statistical analysis
Differences in the total number of species in the various posi-tions from the individual Prosopis plants (beneath, edge, andbeyond the canopy) were assessed using c2 tests. One-way ANOVAswere used to compare the density of associated species at differentpositions from Prosopis canopies. Two-way analyses of variance
A: Number of associated species C
B: Evenness of associated species D
P. cineraria P. juliflora
Prosopis sp
0
5
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15
20
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P. cineraria P. juliflora
Prosopis sp
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Fig. 1. Effects of position relative to the canopy of Prosopis juliflora and Prosopis cineraria onspecies. Black bars ¼ Beneath canopy, White bars ¼ margin of canopy and gray bars ¼ out
(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 ANOVAwasused to assess the impacts of Prosopis species, leaf age and extractconcentration on final germination percentage of the five assayednative plants. Species density was square-root-transformed tomeetthe assumption of the ANOVA. This transformation improved thenormality of the distribution of the data. ShapiroeWilk test wasused to check the normality of the data distribution. Tukey’s HonestSignificant Difference post hoc test was used for comparison ofmeans when statistical significant differences (P < 0.05) wereobserved. All statistical methods were performed using SYSTAT,version 11.0.
3. Results
The overall number of associated species did not differ betweenthe stands of the two Prosopis sp. (20 species for P. juliflora and 21species for P. cineraria). However, the number of associated specieswas 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). Thenumber of species beneath P. juliflora was almost one third thenumber of species beneath P. cineraria and in the open stands be-tween the canopies (Fig. 1 a).
Results of two-way ANOVAs showed significant effects for bothProsopis sp., position from the canopy and their interaction onevenness, and richness and density of associated species (P < 0.05,Table 1). The exception was the impact of Prosopis sp. on richnessof associated species (P > 0.05). In P. juliflora, evenness, richnessand density of associated species were significantly lower beneaththe canopy, compared with outside and at the margin of the
: Richness of associated species
: Density of associated species (number/100m2)
P. cineraria P. juliflora
Prosopis sp
0
2
4
6
8
Ric
hn
es
so
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sp
ec
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s
P. cineraria P. juliflora
Prosopis sp
0
250
500
750
1000
De
ns
ity
of
as
so
cia
te
ds
pe
cie
s
total number of species, evenness, richness and density (number/100 m2) of associatedside of canopy.
Table 1Twoway 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 4.40* 9.41*** 5.91*Species richness 2.41 22.30*** 8.42***Species density 8.25** 28.8*** 23.47***
A. El-Keblawy, M.A. Abdelfatah / Journal of Arid Environments 100-101 (2014) 1e84
canopy. Conversely, evenness and density did not differ signifi-cantly at the margin versus beyond the canopies of P. Juliflora in-dividuals (Fig. 1).
In P. cineraria, evenness and richness of associated species didnot differ significantly beneath and at the margin of the canopy,but both were significantly lower compared with beyond thecanopy. However, the density was significantly greater at themargin, compared with beneath and beyond the canopy (Fig. 1).The comparison of the two Prosopis species indicates that bothevenness and richness of associated species were significantlygreater underneath P. cineraria compared with underneathP. juliflora canopy. However, these variables did not differ betweenthe 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 atotal of the 20 species recorded in the P. juliflora community, wassignificantly reduced beneath, compared with outside the can-opies (P < 0.05, Table 2). Most of these species were not presentunder the canopies. In addition, five other species werecompletely absent under P. juliflora canopies, so their densities didnot differ significantly beyond vs. beneath the canopy (P > 0.05).The depressive impact of the P. juliflora canopy was less obviouson perennial plants, especially grasses, compared with annualplants. Six species attained a minimum of eight individuals per100 m2; two perennial grasses (C. ciliaris, S. arabicus), oneperennial tree (P. juliflora), one perennial herb (Aizoon canariense)and two annual herbs (T. racemosus and Gypsophila bellidifolia).
Table 2Effect of Prosopis juliflora canopy on density of associated species (number (numberof individuals per 100 m2). *: P < 0.05, **: P < 0.01, and ***: P < 0.001.
Species Life cyclea Position from canopy
Beneath Margin Beyond F
Acacia tortilis P 0.0 17.0 8.0Aizoon canariense P 12.5 72.0 90.8 ***Amaranthus viridis A 0.0 0.0 36.7 *Arnebia hispidissima A 0.0 8.3 38.3 ***Astragalus annularis A 0.0 0.0 8.3Cenchrus ciliaris P 25.0 58.3 16.7 ***Eragrostis barrelieri A 0.0 0.0 38.3 **Gypsophila bellidifolia A 8.3 0.0 25.0 *Launaea capitata P 0.0 8.3 0.0Malva parviflora A 0.0 8.3 18.3 ***Paronychia arabica A 0.0 33.3 16.7 **Plantago ovata A 0.0 65.0 40.7 ***Prosopis juliflora P 9.1 21.7 31.7 ***Rhazya stricta P 0.0 8.3 8.3Spergularia marina A 0.0 0.0 13.3 *Sporobolus arabicus P 12.0 14.7 10.0Stipagrostis plumosa P 0.0 7.2 9.3Tephrosia apollinea P 0.0 0.0 16.7Tragus racemosus A 18.0 35.0 45.0 *Tribulus terrestris A 0.0 0.0 21.6 *
a A ¼ annuals, P ¼ perennials.
The densities of both C. ciliaris and S. arabicus did not differsignificantly between beneath and beyond the canopies (Table 2).The number of annuals that attained significantly lower densitiesunder P. juliflora canopies (9 species) was significantly greaterthan the number of perennials (2 species) (c2 ¼ 5.680, P < 0.05;the 11 perennials and 9 annuals recorded with P. juliflora wereused as expected values).
3.2. Effect of P. cineraria on species composition
The impact of P. cineraria canopy on density was significant for13 species, out a total of the 21 species recorded in its stands(P < 0.05, Table 3). The densities were significantly increased at thecanopy margin for nine species and beneath the canopies for twospecies and both at margin and beneath the canopies for onespecies. 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 spe-cies on EC, Na and organic C % (P < 0.05). In addition, position fromcanopy and the interaction between species and position fromcanopy had significant effects onmost of the studied soil characters(P < 0.05, Appendix A). Values of K, N, organic C %, and P weresignificantly greater beneath, compared to beyond the canopies ofboth P. juliflora and P. cineraria. Relative position to the canopysignificantly affected pH, EC, Na, HCO3 and organic C % in P. juliflora,but not in P. cineraria. Values of EC, HCO3 and organic C % weresignificantly 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 nativeplants
Three-way ANOVA showed significant effects for the mainfactors (Prosopis species, leaf age and extract concentration) andmost of their interactions on final germination percentage of the
Table 3Effect of Prosopis cineraria canopy on density of associated species (number of in-dividuals per 100 m2). *: P < 0.05, **: P < 0.01, and ***: P < 0.001.
Species Life cyclea Position from canopy
Beneath Margin Beyond F
Acacia tortilis P 0.0 12.1 0.0Aeluropus massauensis P 23.0 0.0 10.2Aizoon canariense P 67.7 34.3 33.3 *Amaranthus viridis A 21.2 112 13 ***Astragalus annularis A 16.7 100 11.1 *Cenchrus ciliaris P 38.7 36.6 22.8Chenopodium murale A 24.2 75.8 21.4 ***Chrozophora oblongifolia P 0.0 100 0.0 *Eragrostis barrelieri A 13.3 14.4 68.9 ***Euphorbia serpens A 10.2 43.4 12.1 ***Gypsophila bellidifolia A 66.67 22.2 20.3 ***Launaea capitata P 0.0 0.0 11.1Lotus garcinii P 0.0 32.3 31.0Paronychia arabica A 0.0 0.0 33.3Plantago ovata A 6.7 53.3 10.0 ***Prosopis juliflora P 12.7 13.3 2.7 *Spergularia marina A 54.4 195.5 113.3 ***Sporobolus arabicus P 15.0 16.7 16.7Stipa capensis P 7.5 33.3 0.0 **Tragus racemosus A 12.0 17.0 9.0Tribulus terrestris A 5.0 32.3 21.2 ***
a A ¼ annuals, P ¼ perennials.
Table 4Effects of Prosopis juliflora and Prosopis cineraria canopies on the mean values of some soil characters.
Species Place from canopy pH EC (dS m�1) HCO3 (M eq l�1) Na (meq l�1) K (meq l�1) N (ppm) P (ppm) Organic C (%)
P. juliflora Beyond 7.43a 1.40b 1.16a 12.6b 6.5b 2.7b 0.41a 11.38b
Beneath 7.04b 6.61a 1.26a 21.7a 9.35a 4.6a 0.56a 24.94a
P. cineraria Beyond 7.43a 1.40a 1.16a 12.6a 6.5b 2.7b 0.41b 11.38b
Beneath 7.35a 2.41a 1.00a 13.5a 8.9a 3.5a 065a 14.80b
A. El-Keblawy, M.A. Abdelfatah / Journal of Arid Environments 100-101 (2014) 1e8 5
five studies species (P < 0.05, Appendix B). Generally, seeds of thedifferent species treated with aqueous extracts of P. julifloraattained significantly lower germination, compared with theircontrols (seeds without treatments) and seeds treated withdifferent concentrations of P. cineraria extracts. Higher concen-trations of old leaves of P. juliflorawere significantly more effectivein inhabiting the germination of C. ciliaris and S. arabicus,compared with higher concentrations of fresh leaves. InE. barrelieri, higher concentrations of fresh leaves in both specieswere more effective, compared with the same concentrations ofold leaves (Fig. 2).
Seeds of the two perennial grasses C. ciliaris and S. arabicusgerminated in all concentrations of both P. cineraria and P. julifloraextracts. The final germination of the non-treated seeds (control) ofthe two species didn’t differ from most concentrations of fresh andold leaf extracts of P. cineraria. However, the germination of the twospecies attained significantly lower values in most concentrationsof P. juliflora (Fig. 2).
The seed germination of the two annual grasses (T. racemosusand E. barrelieri) differs according to Prosopis species, leaf age andextracts concentration. Germination of T. racemosus seeds wassignificantly reduced in higher concentrations (6% and 8%) of bothfresh and old leaf extracts of both P. juliflora and P. cineraria, butseeds of E. barrelieri attained greater germination in up to 8% of oldleaf extract of the Prosopis species. The result indicates that theannual E. barrelieri grass can tolerate the fresh, but not the oldextract of the two Prosopis species (Fig. 2). The germination of theannual P. ovatawas completely inhibited in 6% and 8% of both freshand old leaf extracts of P. juliflora. However, the seeds of this specieswere 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 significantlyreduced the evenness, richness and density of the associated plantsbeneath, compared with open places beyond their canopies.However, P. cineraria either did not reduce these variables orsignificantly increased them. These results support other studiesshowed interference effects for P. juliflora and facilitative effects forP. cineraria. For example, in the artificial forests of the UAE, theexotic Eucalyptus and P. juliflora trees had resulted in significantreductions in species diversity and abundance of understory spe-cies, compared to the native P. cineraria and Acacia arabica (El-Keblawy and Ksiksi, 2005). In addition, in a semiarid plantation inHaryana, India, Jalota et al. (2000) reported that only two speciesdominated P. juliflora plantations, but 25 different species werefound in the indigenous Dalbergia sissoo plantations. Another studyin India investigated the vegetation succession on salt-affected soilsafter five years of plantation with two exotic salt bushes and threetree species, and found that only three species were recorded withP. juliflora, compared to 7e8 species with other trees (Arya, 2003).Furthermore, Aggarwal et al. (1976) found that the canopies of theinvasive P. juliflora had far fewer understory species than any of fourother forestry trees studied, whereas the native congener,
P. cineraria, was associated with higher understory diversity thanany other species. Recently, Kaur et al. (2012) reported thatP. cineraria had much weaker effects on species richness comparedwith P. juliflora.
Many studies have suggested that allelopathy contributes to theability of exotic species to become dominant in invaded plantcommunities (Adetayo et al., 2005; Inderjit et al., 2008). The greaterdepressive effect of P. juliflora on the associated species, comparedto its congener P. cineraria, could be attributed to the more sus-ceptibility of the associated species to specific allelochemicalsproduced by the invader, compared with the native tree. Accordingto the ‘novel weapons hypothesis’, these chemicals are new to thenative plant communities in the UAE (Bais et al., 2003; Callawayand Ridenour, 2004). Similar results have been reported foranother two congeners Lantana camara and L. indica. The firstspecies, which is exotic invasive throughout Asia, has allelopathiceffects, but its corresponding native congener L. indica does nothave the same strong effects on native species in India (Inderjitet al., 2008).
Our study showed that seed germination of five native plantsassociated with the Prosopis species was significantly inhibitedwith the aqueous extracts of P. juliflora, compared with control(non-treated) seeds and seeds treated with different concentra-tions of P. cineraria extracts. Conversely, seeds of four native spe-cies germinated to significant proportions in the extract of bothfresh and old leaves of P. cineraria, especially in the lower con-centrations (2% and 4%, Fig. 2). Chellamuthu et al. (1997) suggestedthat the allelopathic effect of P. juliflora leaf litter is due to thepresence of phenolic compounds. Nakano et al. (2001) suggestedthat L-tryptophan may play an important role in the allelopathy ofP. juliflora leaves. The content of L-tryptophan in the exudates offreeze-dried mesquite leaves (1 mg eq.) was estimated to be4.8 � 10�3 mM (Nakano et al., 2001). In addition, Nakano et al.(2004) isolated syringin and (-)-lariciresinol from the aqueousfoliar leachate of P. juliflora, and also detected these chemicals inrhizosphere soil.
Several studies reported the presence of allelopathic com-pounds in both P. juliflora and P. cineraria. For example, Kaur et al.(2012) detected L-tryptophan in leaf leachates of both P. julifloraand P. cineraria, but the amounts were 73% higher in leaf leachateof the former than that of the latter. Similarly, Inderjit et al.(2008) compared soils collected from the rhizospheres of thetwo Prosopis species and found that soils beneath the exoticP. juliflora contained 63.2% higher concentrations of total phe-nolics than soil beneath the native P. cineraria. These findingscould explain the relatively lower allelopathic effects of higherconcentration of P. cineraria, aqueous extracts (6% and 8%),especially on seed germination of the annuals T. racemosus andP. ovata (Fig. 2).
In the hyper-arid habitats of the UAE, there is a noticeableaccumulation of litter underneath the P. juliflora, compared withP. cineraria canopies (El-Keblawy, personal observation). Litterfalling to the ground during periods of stress can alter thephysical, chemical, and biotic environment in which seedsgerminate and seedlings grow (Facelli and Carson, 1991).
Prosopis cineraria Prosopis juliflora
Cen
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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 desertspecies 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) 1e86
Source of variation pH EC HCO3 Na K N P Organic C
Species (S) ns * ns * ns ns ns *Position from
canopy (P)ns ** ns * * * * *
S*P ** * ns * * * ** **
A. El-Keblawy, M.A. Abdelfatah / Journal of Arid Environments 100-101 (2014) 1e8 7
Consequently, litter can have a significant influence on emer-gence and growth of understorey species. In some exotic in-vaders, litter leachates have shown negative effects on seedgermination, establishment and seedling growth of associatedspecies (Chellamuthu et al., 1997). The greater accumulation oflitter underneath the P. juliflora canopy could partially explainthe greater inhibition of understory vegetation of this species.Kaur et al. (2012) reported that experimentally applied P. julifloralitter caused far greater mortality of native Indian species thanlitter from P. cineraria. In addition, P. juliflora leaf leachateshowed negative effects on root growth of three common cropspecies of north-west India whereas P. cineraria leaf leachate hadpositive effects (Kaur et al., 2012).
There is strong evidence from arid lands of nurse plants thatfacilitate establishment of other species (Franco and Nobel, 1989;McAuliffe, 1984). The nurse plant’s canopy structure may influ-ence the success of seedling establishment, in particular in relationto shade intensity and rainfall interception (Padilla and Pugnaire,2006). In P. cineraria, density of associated species was signifi-cantly greater at the margin, compared with beneath and beyondthe canopy (Fig. 1). Similarly, the depressive effect of P. julifloracanopy was diminished at the margin; evenness and density didnot differ significantly at the margin versus beyond the canopies ofboth Prosopis species. This suggests that the microenvironment atthe margin of the canopies is more favorable, compared with bothunderneath and beyond the canopies. During small precipitationevents, canopies might limit water availability in their understoriesby intercepting rainwater and directing it to the areas at the mar-gins of canopies through flow along branches and leaves, makingthe soil at the margin wetter than in open and underneath thecanopies (Padilla and Pugnaire, 2006).
The pattern of higher soil fertility under canopies of desertshrubs and trees, compared with in adjacent open areas, is welldocumented in arid lands (Zhao et al., 2007). Many Prosopis speciescreate “resource islands” with higher levels of organic matter andother macro-nutrients in soils beneath their canopies, whichmakesthem stronger facilitators for other species (Kaur et al., 2012; Rossiand Villagra, 2003). For example, Kaur et al. (2012) showed thatboth P. juliflora and P. cineraria form resource islands by accumu-lating total organic N and organic carbon in their rhizosphere soil.In addition, Aggarwal et al. (1993) found that soil nitrogen, phos-phorus, and potassiumwere higher under P. cineraria canopies thanin open fields. Our results showed significant increases in theconcentrations of K, N and P beneath, compared with beyond thecanopies of both P. juliflora and P. cineraria. Unlike P. cineraria,P. juliflora increased soluble salts (EC) and decreased the pH un-derneath their canopy. Kaur et al. (2012) arrived to a similar result,regarding the soluble salts. The significant decrease in soil pH un-der the canopy of P. juliflora could be attributed to acidic nature ofphenolic compounds.
Species interactions involve a complex balance of competition(“negative”) and facilitation (“positive”) interactions (Brookerand Callaghan, 1998). Facilitation and interference interactionsdo not occur in isolation from each other. The overall effect ofone species on another may be dependent on physical factors andthe combination of competition for different resources, alle-lochemicals released into the environment, and facilitative fac-tors such as shade and protection from herbivory (Callaway et al.,1991). In deserts, several shrubs have facilitative effects on thegrowth of some associated annuals, but also produce alle-lochemicals that suppress the growth of the same annuals(Callaway and Walker, 1997). In the present study, both Prosopisspecies have facilitative effects in relation to the available nu-trients; their canopies increased the most important macro-nutrients K, N and P. In addition, both species increased the
organic matter contents (the increase was significant only inP. juliflora), which would also increase the water holding capacitythat would improve soil texture and increase soil moistures.However, it appears that the allelopathic effects of the litters ofP. juliflora may override its potential positive effects on soilfertility. Phenolic compounds of the allelochemicals in soils couldreduce the water and nutrients uptake. For example, net uptakeof P, K, and water by cucumber seedlings was reduced 57, 75, and29%, respectively, when the whole root system was exposed toferulic acid, an allelopathic phenolic acid. In addition, planttranspiration was reduced in a linear manner as the fraction ofthe cucumber roots in contact with ferulic acid increased (Lyuand Blum, 1990).
The relative importance of facilitative and competitive in-teractions in a particular plant community determines the struc-ture of that community (Callaway andWalker, 1997; Callaway et al.,1991). Our study showed a less depressive impact for the P. julifloracanopy on perennial plants, especially grasses, compared withannual plants. Similarly, Jalota et al. (2000) indicated that the twodominated species in P. juliflora plantations in the semi-arid Har-yana in India were the perennial grasses Dactyloctenium aegyptiumand Dichanthium annulatum. The positive presence of the perennialgrasses C. ciliaris and S. arabicus that was observed in our study inthe neighborhood area of P. juliflora, compared with annual plants,could be attributed partially to the high tolerance of the seeds ofthese plants during the germination stage to the presence of alle-lochemicals released from the leaves of the invader. Both the twoperennial grasses germinated to high proportion, even in thehighest concentration of the aqueous extract (8%) of the old andfresh leaves of P. juliflora. In addition, the greater ability of theperennial grasses, compared with annuals, to capitalize on morenutrients could be also account for their higher density underneathP. juliflora canopy. Conversely, the significant reduction in thedensity of the annuals underneath and at the margin of theP. juliflora could be explained mainly by the lower tolerance of thegermination stage of these species to the released allelochemicals.The results of the study indicated significant reduction in germi-nation of the seeds of the three annuals (E. barrelieri, T. racemosusand P. ovata) in most concentrations of fresh or old leaves or both ofP. juliflora.
Acknowledgments
The authors would like to thank Dr Colin Pain, Honorary Assis-tant Professor at the University of Sevilla, Spain, for his criticalrevision of themanuscript. Thanks are also extended to Prof InderjitSingh, University of Delhi, India, for his valuable comments on themanuscripts.
Appendices
Appendix A. Results of two-way ANOVA (F-values) for the effects ofProsopis juliflora and Prosopis cineraria canopies on some soilcharacters. ns: insignificant different at P ¼ 0.05, *: P < 0.05, ** andP < 0.01, and ***: P < 0.001.
A. El-Keblawy, M.A. Abdelfatah / Journal of Arid Environments 100-101 (2014) 1e88
Appendix B. Results of three-way ANOVA (F-values) for the effectsof species (Prosopis cineraria and P. juliflora), leaves age and extractconcentration on final germination of seeds of five plants in the UAE.*: P < 0.05, **: P < 0.01, and ***: P < 0.001.
Source df Tragusracemosus
Eragrostisbarrelieri
Plantagoovata
Sporobolusarabicus
Cenchrusciliaris
Species (S) 1 154.9*** 330.9*** 77.9*** 238.3*** 171.9***Leaf age (A) 1 50.6*** 526.0*** 5.96* 17.5*** 26.2***Extract
concentration(C)
3 460.9*** 10.9*** 44.9*** 77.5*** 108.8***
S*A 1 54.2*** 239.6*** 38.4*** 103.5*** 25.1***S*C 3 5.0** 2.29 7.8*** 27.8*** 15.9***A*C 3 7.3*** 6.14** 35.6*** 4.13** 2.84*S*A*C 3 10.5* 0.31 1.07 5.98** 1.25Error 48
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