Live and dead shrubs and grasses have different facilitative and interfering effects on associated plants in arid Arabian deserts

Journal of Arid Environments 125 (2016) 127e135

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Journal of Arid Environments journal homepage: www.elsevier.com/locate/jaridenv

Live and dead shrubs and grasses have different facilitative and interfering effects on associated plants in arid Arabian deserts Ali El-Keblawy a, b, *, Tamer Kafhaga c, Teresa Navarro d a

Applied Biology Department, Sharjah University and Sharjah Research Academy, Sharjah, United Arab Emirates Department of Biology, Faculty of Education in Al-Arish, Suez Canal University, Egypt c Desert Conservation Reserve, Dubai, United Arab Emirates d
laga, P. O. Box 59, 29080, Ma
laga, Spain Departmento de Biología Vegetal, Universidad de Ma b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 9 February 2015 Received in revised form 3 October 2015 Accepted 7 October 2015 Available online 6 November 2015

The Arab Gulf desert region is dominated by few shrubs and grasses, although mostly devoid of vegetation. The impact of both live and dead shrubs and grasses on plant diversity and community composition on sand dunes of the United Arab Emirates was assessed. Species richness, diversity indices (Simpson, ShannoneWiener, and Brillouin), and plant abundance were significantly greater under dead grasses than in the surrounding open areas. However, the opposite was true for live grasses. Dead and live shrubs did not differ significantly in species richness and abundance. The relative interaction index indicated that live nurse grasses inhibited 13 species and facilitated only one species, whereas dead grasses facilitated 13 species and did not inhibit any species. Live shrubs facilitated four species and inhibited two, but dead shrubs facilitated 10 species and inhibited none. Organic matter and most of the assessed soil nutrients were significantly higher under both shrubs and grasses than in the barren spaces in-between. The facilitative effect of dead grasses on soil characteristics was more obvious. The results support the feasibility of growing nurse shrubs and grasses to restore degraded arid desert environment. © 2015 Elsevier Ltd. All rights reserved.

Keywords: Arid deserts Competition Facilitation Grasses Inhibition Shrubs

1. Introduction Plants can exert influence on their neighbors in myriad ways, resulting in a broad range of harmful or beneficial outcomes. The abundance, performance, and spatial distribution of plant species are markedly related to the strength and sign of their interactions in communities (Roughgarden and Diamond, 1986; Brown et al., 2001). Understory plants can exert both facilitative and competitive effects on larger neighboring “nurse” plants. Their benefits include reduced thermal stress or evapotranspiration (ValienteBanuet and Ezcurra, 1991; Greenlee and Callaway, 1996); improved soil texture, nutrient content, and water availability (Nobel, 1989; Moro et al., 1997; Barnes and Archer, 1999; Pugnaire et al., 2004); and protection from herbivory (Haase et al., 1997; Brown and Ewel, 1987). Conversely, nurse plants can also have negative effects on the survival and establishment of the associated

* Corresponding author. Applied Biology Department, Sharjah University and Sharjah Research Academy, Sharjah, United Arab Emirates. E-mail addresses: [email protected], [email protected] (A. ElKeblawy). http://dx.doi.org/10.1016/j.jaridenv.2015.10.007 0140-1963/© 2015 Elsevier Ltd. All rights reserved.

understory plant community. These plants may interact competitively through light deprivation, competition for water and nutrients, or leaching of allelopathic compounds (Nobel, 1989; Barnes and Archer, 1999; Holmgren et al., 1997; Kitajima and Tilman, 1996; Moro et al., 1997). In general, the net direction and strength of these interactions are considered to depend on the severity of the physical environment (Bertness and Leonard, 1997) and site productivity (Bruno et al., 2003). It has been hypothesized that facilitative interactions may be more prevalent in harsh environments, such as those occurring in arid and semiarid environments
mez-Aparicio et al., (Callaway, 1995; Callaway and Walker, 1997; Go 2004). In terms of depth, grass roots are generally distributed nearer to the surface than shrub roots. In their global analysis of root distribution, Jackson et al. (1996) indicated that 44% of grass roots were found in the top 10 cm of soil, whereas only 21% of shrub roots were found at the same depth. In addition, Schenk and Jackson (2002) collected a data set of >1300 records of root system sizes for individual plants from various water-limited ecosystems, including deserts. They concluded that root system sizes differed among growth forms: annuals < perennial forbs ¼ grasses < semishrubs < shrubs < trees. Furthermore, in the arid Patagonian

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steppe, Soriano et al. (1987) indicated that 54% of the grass-root biomass is located in the top 10 cm of the soil. However, most of the shrub roots are found in the lower layers of the soil (Soriano et al., 1987). Consequently, the root system of grasses allow uptake of water mostly from the upper layers of the soil with frequent and short-duration pulses of water availability. However, shrubs take up most of the water from the lower layers of the soil with infrequent and long-duration pulses of water availability (Sala et al., 1989). As shrubs and grasses use soil water and nutrients differently, their interference or facilitative interactions with the associated plants might be affected. It has been reported that shading by a nurse plant canopy reduces the solar radiation intensity and temperature at the soil surface and, consequently, water losses by evaporation (Moro et al., 1997; Maestre, 2002; El-Bana et al., 2003). However, the canopy effect depends on the density of the crown. Open canopies, such as that of arid grasses and dead shrubs, have less significant effects on shading and water losses by evaporation from soils, compared to live shrubs with denser canopies. Soil fertility is another highly significant factor that would enhance the facilitation effects of both live and dead nurse plants (Belnap, 1995). The soil fertility under recently dead shrubs is expected to be similar to, if not higher than, live shrubs. In addition, live plants can compete with the understory community. Although several studies assessed the facilitative/ inhibitory effects of live nurse shrubs and grasses, few studies compared the effects of dead and live nurse plants on associated plants (Morris and Wood, 1989). The impact of dead and live shrubs and grasses on the physical and chemical characteristics of soil and on the understory vegetation can be assessed. This would further enhance our understanding of the planteplant interactions and the implications for their use in restoring degraded arid desert environments. Several studies have assessed the impact of trees and shrubby plants on the associated plants in the arid lands of the Arab Gulf region (Brown et al., 2001; El-Bana et al., 2003, 2007; El-Keblawy and Abdelfatah, 2014). However, the similar impact of grasses has not been studied. In addition, several studies have assessed the impact of grasses on associated plants in the Mediterranean semiarid climate (Maestre et al., 2003; Padilla and Pugnaire, 2006; Cortina et al., 2011). However, this was not studied in hyperarid environments with highly limited water and nutrients. With their shallow adventitious root systems, grasses rely mainly on atmospheric moisture and sparse rain showers (Jackson et al., 1996; Soriano et al., 1987; El-Keblawy et al., 2009); therefore, grasses and the associated plants are expected to compete intensively on the very limited available resources in the sandy soils of arid lands. However, shrubs, with their deeper root systems that allow water uptake from a deeper layer, are expected to compete less intensively with the associated plants. We hypothesized that live grasses have more competitive and less facilitative effects on their associated species than shrubs do in resource-limited arid environments. In most desert ecosystems, vegetation is spatially heterogeneous, consisting of vegetation patches with alternating areas of bare soil (Bertiller, 1998). Typically, desertification of sandy areas due to wind erosion often results in the dominance of few shrubs
fi and grasses, while most of the land is devoid of vegetation (Ke et al., 2007; Zhao et al., 2007). As dead and live shrubs and grasses exert different interactive effects on the associated species (Morris and Wood, 1989), understanding their facilitative/interfering effects on the survival of understory shrubs and annuals is very important in sustainably restoring degraded arid and semiarid
fi et al., 2007; Zhao et al., ecosystems with potential nurse plants (Ke 2007). The use of nurse plants has been recommended for restoring degraded ecosystems, where physical conditions or grazing

pressure significantly limit plant establishment (Anthelme et al., 2014; Padilla and Pugnaire, 2006). Nurse plants can maintain greater biodiversity (Valiente-Banuet et al., 2006; Valiente-Banuet and Verdú, 2007). As hypothesized, the importance of facilitation increases with increasing severity of the abiotic conditions, therefore also increasing the benefits of nurse plants under stressful conditions, such as arid deserts (Callaway and Walker, 1997; Callaway et al., 2002). The aim of the present study was to assess the impact of live and dead shrubs and grasses on plant diversity and community structure of stable sand dunes in the Dubai Desert Conservation Reserve (DDCR), United Arab Emirates (UAE). The study also aimed to assess the impact of dead and live shrubs and grasses on the physical and chemical properties of soil. 2. Materials and methods 2.1. Study site The DDCR (24e25 latitude and 55e56 longitude) has been declared for conserving the natural flora, fauna, and landscape of the desert ecosystem in Dubai, UAE (Fig. 1). It is an arid area, characterized by two distinctive seasons: a long dry season (April to November) with very high temperatures, and a short season (December to March) with mild to warm temperatures and light rainfall. The mean daily temperature ranges between 12.1  C in January and about 42  C in JuneeAugust. The average rainfall recorded in the long term (1934e2004) is 102.8 mm. However, the variations in annual rainfall are considerable. A maximum of 345 mm was recorded in 1957, whereas a minimum of 3.0 mm was recorded in 1985 (Feulner, 2006). The growing season of the study year (October 2009 to May 2010) was much drier than average; the total rainfall was only 24.4 mm at the new Al-Faqa metrological station (about 15 km away from the study area). The DDCR is a fenced area with a perimeter of about 85 km and an area of 225 km2. The reserve was declared in 2002, and the perimeter was completed in late 2003. The DDCR is mainly a desert ecosystem with sand dunes. The topography is simple, with a dominance of low to mediumehigh sand dunes. The plant community of the DDCR is not rich. It is dominated by few shrubby species, such as Leptadenia pyrotechnica, Calligonum comosum, Dipterygium glaucum, Fagonia indica, Heliotropium digynum, Limeum arabicum, Moltkiopsis ciliata, and Indigofera colutea. Short live ephemerals appear immediately after rainfall, with their life span extending to the end of the season (April/May), depending on the availability of rainfall. Prosopis cineraria is the only tree recorded in the reserve. The DDCR has a large population of wild antelopes, such as oryx and gazelles. These antelopes are given externally sourced feed, which meets probably about half of their dietary requirements. 2.2. Assessing the interactive effects on associated plants Each of the live and dead shrubs and grasses was represented by 30 individuals, except for live grasses being represented by 22 individuals. The selected grasses were undamaged tussocks. Due to overgrazing by the overstock of antelopes in the study area, the number of undamaged grass tussocks was rare during the study year, which received only 24.4 mm of rainfall. Whenever possible, dead plants were selected from among those that died in the last two seasons; the stems were still undamaged and lighter in color, compared with older skeletons. The live nurse shrubs included L. arabicum (seven individuals), Rhanterium epapposum (seven individuals), D. glaucum (eight individuals), and Crotalaria aegyptiaca (eight individuals). The studied nurse grasses were Pennisetum divisum (12 individuals) and

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Fig. 1. Location map of the Dubai Desert Conservation Reserve (DDCR) in the United Arab Emirates.

Panicum turgidum (10 individuals). However, the dead shrubs or grasses could not be easily identified. The average diameter of live nurse shrubs and grasses ranged between 0.8 and 1.2 m, and the average height was about 0.8e1.0 m. A 2.25-m2 quadrat (1.5  1.5 m) was laid under/around each dead or live nurse plant; the center of the quadrats coincided with the center of the individuals. Another quadrat of the same size was

selected in open areas adjacent to each dead or live plant (a minimum of 2 m away from the edge of the nurse individuals). The individuals were randomly selected on stable dunes in the DDCR. The absolute density (the number of plants of a certain species rooted within the 2.25-m2 quadrat) was calculated for each associated species under the nurse plants and in the adjacent open areas. As the plant density is very low in the study area, it was

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expressed as the number per 1000 m2. The species richness (the number of species associated with each of the live and dead shrub and grass categories) and three diversity indices (ShannoneWeaver, Brillouin, and Simpson) were also estimated. These indices are widely used in the literature, and their attributes are discussed in detail by Magurran (1988). Both the Brillouin and Shannon indices are sensitive to the abundance of rare species. The Brillouin index is especially recommended for cases with unguaranteed randomness of the sample. However, the Simpson index measures species dominance, and it is heavily weighted towards the most abundant species and less sensitive to changes in species richness (Magurran, 1988). The relative interaction index (RII) was calculated to assess the facilitative/inhibitory effect of died and live shrubs or grasses on each of the five community attributes (species richness, plant density, and three diversity indices) (Armas et al., 2004). RII ¼ (CAu  CAn)/(CAu þ CAn), where CAu and CAn are a community attribute under the nurse plant and next to them, respectively. The index is symmetrical around zero (no significant interaction), and it is constrained by þ1 (facilitation) and 1 (inhibition). 2.3. Soil analysis For each of five dead or live grasses and shrubs, two composite soil samples were collected from the top 15 cm of the soil, one from underneath (halfway between the trunk and the edge of the canopies), and another from at least 2 m outside the edge of the canopies. A total of 44 soil samples were collected and analyzed for this study. The soil samples were air-dried, ground, homogenized, and passed through a 2-mm sieve to remove large particles. Soil organic matter (OM) content; soil texture (proportions of sand, silt, and clay); electrical conductivity (EC); pH; and the nutrients Na, Ca, Mg, Cl, K, N, and P were estimated. The sodium adsorption ratio (SAR) and exchangeable sodium percentage (ESP) were calculated to further assess the salinity and sodicity. The OM 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 to determine EC and pH using conductivity and pH meters. Available nitrogen was extracted using 2 M KCl and determined by the micro-Kjeldahl method. Available phosphorus was estimated using Olsen's solution (sodium bicarbonate) as an extracting agent. Na, Ca, Mg, Cl, and K were estimated using flame photometry. These methods are outlined in the study by Black (1965). 2.4. Data analysis Contingency c2 tests were used to assess the dependence of the number of associated species on the survival and position from nurse grasses or shrubs. The same test was used to assess the dependence of the number of species under nurse plants on their life-form and survival. One-way analyses of variance (ANOVAs) were used to assess the difference in the density of associated species under and beyond the nurse plants. Three-way ANOVAs were used to evaluate the effects of the life-form (shrub vs. grass), survival (live vs. dead), and position from the nurse plants (under vs. beyond canopies) and their interactions on species density, richness, diversity indices (Simpson, ShannoneWiener, and Brillouin), and the physical and chemical properties of soil. Species density was square-root-transformed to meet the assumption of the ANOVA. This transformation improved the normality of the distribution of the data. The ShapiroeWilk test was used to check the normality of the data distribution. Tukey's honest significant difference post hoc test was used to compare the means when statistically significant differences (p < 0.05) were observed. All statistical methods were performed using SYSTAT, version 13.0.

3. Results 3.1. Impact on species diversity and plant abundance The contingency c2 results indicated that the overall effects of nurse shrubs and grasses, regardless of their survival status, were insignificant (c2 ¼ 1.92 and 2.77, respectively; p > 0.05). The numbers of species under nurse plants and in the adjacent open areas were 31 and 21, respectively, for shrubs, and 32 and 20, respectively, for grasses. These results also indicated that the number of species under and beyond nurse grasses depended significantly on their survival (c2 ¼ 4.97, p < 0.05). Dead grasses hosted around 88% more species under than next to them, but live grasses hosted 60% less species under than next to them (Table 1). The number of species under nurse grasses and shrubs depended significantly on their survival (c2 ¼ 4.39, p < 0.05). Although dead grasses hosted more plants (32 species) than did live grasses (10 species), both did not differ significantly in the number of species (31 and 23 species, respectively). It is interesting to note that live grasses significantly reduced the number of associated species, compared with live shrubs; the numbers of species under live grasses and shrubs were 10 and 23 species, respectively (c2 ¼ 5.12, p < 0.05) (Table 1). The effects of life-form, position, and the interactions between survival and both life-form and position on species dominance, as expressed by the Simpson index, were significant (Table 2). In addition, both the ShannoneWiener and Brillouin indices were significantly affected by survival, position, the interaction between survival and both life-form and position, and the interaction among the three factors (p < 0.05, Table 2). Dead grasses significantly enhanced the three diversity indices, compared with live and dead shrubs and live grasses. Significantly greater values of both the Simpson and ShannoneWiener indices were obtained under dead and live shrubs and dead grasses, than in the adjacent bare ground. For live grasses, however, the three indices did not differ either under and next to them (Table 1). The three-way ANOVA indicated that plant density was significantly affected by survival status, and all interaction among the main factors (p < 0.05, Table 2). Plant density was significantly greater under dead shrubs than beyond them, but the plant density under and beyond live shrubs did not differ significantly. However, live grasses suppressed the growth of associated plants (density was 26% lesser under live grasses than next to them), but dead grasses facilitated the growth of associated plants (density was 83% greater under dead grasses than next to them) (Table 1). 3.2. Impact on plant community structure Live nurse grasses significantly reduced (inhibited) the density of 13 species and significantly increased (facilitated) the density of only Tribulus pentandrus under rather than next to them. However, dead grasses significantly increased the density of 13 species, but it did not reduce the density of any species. The density of five species (Cyperus conglomeratus, Eremobium aegyptiacum, L. arabicum, Gisekia pharnaceoides, and Stipagrostis plumosa) were significantly increased by dead grasses, but significantly reduced by live grasses. T. pentandrus was the only species that was facilitated by both dead and live grasses (Table 3). Live shrubs significantly increased the density of four species and significantly reduced the density on two species. However, dead shrubs significantly increased the density of 10 species, but they did not reduce the density of any species. The density of the perennial herb T. pentandrus was significantly reduced by live shrubs, but significantly increased by dead shrubs (Table 4).

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Table 1 Effects of surviving and dead shrubs and grasses on species richness, plant density (number/1000 m2) and three diversity indices. RII ¼ relative interaction index. Index values around zero indicate no significant interaction, and positive and negative values indicate facilitation and inhibition, respectively. Life-form

Survival status

Position

Richness

Density

Simpson (dominance)

ShannoneWiener

Brillouin

Shrubs

Live

Under Next RII Under Next RII Under Next RII Under Next RII

23 18 0.12 31 20 0.22 10 16 0.23 32 17 0.31

245.7c 243.6c 0.00 373.2b 243.3c 0.21 182.8d 246.8c 0.15 430.5a 234.8c 0.29

0.864b 0.803c 0.04 0.875b 0.801c 0.04 0.842c 0.854c 0.01 0.921a 0.828c 0.05

3.5b 2.94c 0.09 3.69b 3.05c 0.09 2.91c 3.1bc 0.03 4.09a 3.02c 0.15

3.31b 2.79c 0.09 3.53ab 2.9bc 0.10 2.62c 2.87bc 0.05 3.87a 2.85c 0.15

Dead

Grasses

Live

Dead

Means followed by the same letter within a column are not significantly different at p ¼ 0.05.

Table 2 Results of three-way ANOVAs testing the effects of plant life-form, survival status of nurse plants, and the position from the canopy on plant density and some diversity indices.*: p < 0.05,**: p < 0.01, and***: p < 0.001. Source

Density

Simpson (dominance)

ShannoneWiener

Brillouin

Life-form (LF) Survival status (S) Position (P) LF* S LF* P S* P LF* S* P

0.739 23.65*** 0.855 18.75*** 4.79* 19 96*** 6.75**

4.12* 1.75 6.35** 10.32*** 3.12 21.22*** 5.34*

1.24 9.67** 4.65* 9.81** 1.54 14.56*** 12.34***

2.57 4.89* %0.12* 5.33* 2.79 17.78*** 11.45***

Table 3 Impacts of live and dead grasses on average density of associated plants (number/1000 m2). RII ¼ relative interaction index. Index values around zero indicate no significant interaction, and positive and negative values indicate facilitation and inhibition, respectively.*: p < 0.05,**: p < 0.01, and***: p < 0.001 according to one-way ANOVA. Species form

Aerva javanica Arnebia hispidissima Atractylis carduus Bassia muricata Calligonum comosum Centropodia forsskaolii Chrozophora oblongifolia Cyperus conglomeratus Dipterygium glaucum Eragrostis papposa Eremobium aegyptiacum Fagonia indica Farsetia linearis Gisekia pharnaceoides Heliotropium digynum Indigofera colutea Launaea capitata Launaea mucronata Leptadenia pyrotechnica Limeum arabicum Moltkiopsis ciliata Monsonia nivea Morettia parviflora Neurada procumbens Panicum turgidum Paronychia arabica Pennisetum divisum Plantago boissieri Silene villosa Stipagrostis plumosa Tragus racemosus Tribulus arabicus Tribulus pentandrus a

Life-forma

P/S P/S P/S A/H P/S P/G P/S P/Se P/S P/G P/H P/S P/S A/H P/S P/S A/H P/H P/S P/S P/S P/H P/S P/H P/G A/H P/G A/H A/H P/G AH P/H P/H

Live

Dead

Under

Next

0.0 5.0 0.0 0.0 0.0 6.3 0.0 15.0 0.0 0.0 8.3 0.0 0.0 0.0 33.3 0.0 0.0 0.0 0.0 0.0 6.7 0.0 0.0 0.0 0.0 0.0 0.0 8.3 2.0 0.0 0.0 33.3 53.3

0.0 13.3 0.0 0.0 0.0 16.6 0.0 21.6 0.0 0.0 16.6 0.0 0.0 23.3 23.3 0.0 16.7 0.0 0.0 16.7 13.3 23.3 0.0 5.0 0.0 0.0 16.7 0.0 13.3 16.7 0.0 5.0 16.7

P: Perennial, A: Annual, S: Shrub, H: Herb, G: Grass, Se: Sedge.

RII 0.45*

0.45** 0.18**

0.33*

1.00*** 0.18 1.00*

1.00* 0.33** 1.00*** 1.00**

1.00* 1.00 0.74** 1.00* 0.74 0.52**

Under

Next

RII

3.3 12.3 3.3 12.3 13.3 15.0 14.0 53.3 11.0 6.7 37.5 6.7 13.3 33.3 33.3 13.3 6.7 13.3 6.7 36.7 2.0 0.0 14.7 3.3 3.3 6.7 1.2 6.7 13.3 4.0 6.7 3.3 23.3

0.0 21.6 0.0 1.3 0.0 11.3 0.0 36.7 1.0 0.0 22.3 6.7 0.0 16.7 12.0 0.0 13.3 0.0 0.0 13.3 8.0 0.0 0.0 13.3 0.0 0.0 0.0 13.3 10.7 13.3 0.0 0.0 6.7

1.00 0.27 1.00 0.81*** 1.00* 0.14 1.00*** 0.18** 0.83** 1.00 0.25* 0.00 1.00* 0.33* 0.47** 1.00 0.33 1.00 1.00 0.47* 0.60 1.00* 0.60 1.00 1.00 1.00 0.33 0.11 0.54** 1.00 1.00 0.55*

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Table 4 Impact of live and dead shrubs on average density of associated plants (number/1000 m2). RII ¼ relative interaction index. Index values around zero indicate no significant interaction, and positive and negative values indicate facilitation and inhibition, respectively.*: p < 0.05,**: p < 0.01, and***: p < 0.001 according to one-way ANOVA. Species

Aerva javanica Aristida adscensionis Arnebia hispidissima Atractylis carduus Bassia muricata Centropodia forsskaolii Chrozophora oblongifolia Crotalaria aegyptiaca Cyperus conglomeratus Dipterygium glaucum Eragrostis papposa Eremobium aegyptiacum Fagonia indica Farsetia linearis Gisekia pharnaceoides Heliotropium digynum Indigofera colutea Launaea capitata Launaea mucronata Limeum arabicum Lotus sp. Moltkiopsis ciliata Neurada procumbens Pennisetum divisum Plantago boissieri Plantago ovata Silene villosa Stipagrostis plumosa Tragus racemosus Tribulus arabicus Tribulus pentandrus a

Life-forma

P/S P/G P/S P/S A/H P/G P/S P/S P/Se P/S P/G P/H P/S P/S A/H P/S P/S A/H P/H P/S P/S P/S P/H P/G A/H A/H A/H P/G A/H P/S P/H

Live

Dead

Under

Next

0.0 0.0 16.3 0.0 15.0 14.3 0.0 7.3 6.7 3.3 0.0 26.7 6.7 13.3 4.0 16.7 16.7 6.7 6.7 2.0 0.0 2.0 3.3 12.0 6.7 0.0 26.7 2.0 0.0 13.3 4.0

0.0 0.0 3.3 0.0 1.0 21.3 0.0 0.0 6.7 6.7 0.0 33.0 16.7 3.3 0.0 26.7 13.3 0.0 3.3 6.7 0.0 28.3 3.3 0.0 16.7 3.3 33.3 0.0 0.0 0.0 16.7

RII

0.66** 0.88* 0.20 1.00 0.00 0.34 0.11 0.43 0.60* 1.00 0.23 0.11 1.00 0.34 0.54 0.87* 0.00 1.00* 0.43 1.00 0.11 1.00 1.00 0.61*

Under

Next

RII

3.3 3.3 7.0 1.3 25.7 13.7 7.7 3.3 2.0 13.7 6.7 39.7 23.3 1.0 23.3 38.3 1.0 16.7 25.0 13.3 3.3 33.3 3.3 13.3 6.7 0.0 23.3 3.7 2.0 3.3 41.7

0.0 0.0 12.0 0.0 1.3 16.0 0.3 0.0 13.3 0.7 0.0 47.3 0.0 6.7 13.3 8.3 13.7 0.0 6.7 3.3 0.00 41.7 11.7 0.0 13.3 0.0 8.3 3.7 0.0 6.7 11.7

1.00 1.00 0.26 1.00 0.90** 0.08 0.93** 1.00 0.74 0.90* 1.00 0.09 1.00** 0.74 0.27* 0.64*** 0.86 1.00 0.58*** 0.60* 1.00 0.11 0.56 1.00 0.33 0.47* 0.00 1.00 0.34 0.56**

P: Perennial, A: Annual, S: Shrub, H: Herb, G: Grass, Se: Sedge.

C. conglomeratus, E. aegyptiacum, H. digynum, M. ciliata, Silene villosa, G. pharnaceoides, and Centropodia forsskaolii are some of the most dominant species in the study area. The densities of most of these plants were negatively affected by live nurse grasses, but significantly increased by dead grasses (Table 4). However, the densities of six of these dominant plants were not affected by live shrubs, and three were significantly enhanced by dead shrubs (Table 3). It is interesting to note that dead grasses facilitated more perennial shrubs (46.7%, seven out of 15 species) than perennial grasses (33.3%), perennial herbs (28.6%), and annual herbs (25%). Similarly, shrubs (dead or live) facilitated more perennial shrubs (46.7%) and perennial herbs (50%) than perennial grasses (20%) and annual herbs (28.6%) (Tables 3 and 4). 3.3. Impact on physical and chemical properties of soil The results of three-way ANOVA for the effects of plant lifeform, and survival status of nurse plants and the position from their canopy on the physical and chemical attributes of soil are shown in Table 5. In general, the OM content was very low (ranging from 0.3% to 0.7%), but it was significantly greater under nurse grasses, especially dead grasses, than under nurse shrubs. Clay and silt were significantly greater under both dead grasses and shrubs, rather than beyond them. In addition, pH was significantly higher (i.e., more alkaline) adjacent to live shrubs and grasses than under them (Table 6). The sodium and EC values were twice as great under as beyond both live grasses and shrubs, but these values were more than five times greater under dead grasses and shrubs than away from them. Similarly, both SAR and ESP were significantly greater under than

farther from both live and dead shrubs, but the difference was much greater for dead plants (Table 6). This indicates that the soil was more sodic under the dead than live shrubs and grasses. Plant life-form, plant survival, position from nurse plant, and most of their interactions had significant effects on the chemical properties of the soil (p < 0.05, Table 5). Most of the assessed soil nutrients (namely Ca, Mg, K, Cl, and SO4) were significantly greater under than beyond the plants. The values of Ca, Mg, K, Cl, and SO4 were higher under the plants than away from them by about five, four, four, eight, and five times, respectively. In addition, these elements were significantly greater under dead plants than under live plants. The values of Ca, Mg, K, Cl, and SO4 were higher under dead plants than live plants by 2.4, 1.7, 2.3, 2.7, and 3.0 times, respectively. The differences between shrubs and grasses were significant only in terms of Ca and Cl values, which were significantly greater under grasses than under shrubs (Table 6). 4. Discussion In deserts, the presence or absence of neighboring plants is reported to influence plant growth and survival. Further, this has long been associated with planteplant interactions that range from extreme competition to facilitation. Facilitation and competition interactions act simultaneously in determining the structure of communities. The overall effect of nurse plants on their herbaceous understory is determined by the balance between both facilitation and competition (Callaway and Walker, 1997). In the present study, live shrubs played a more significant role in facilitating plant recruitment and survival, and hence enhancing plant diversity, than live grasses, which exert an interference effect. However, plant abundance and most of the diversity indices were significantly

A. El-Keblawy et al. / Journal of Arid Environments 125 (2016) 127e135

133

Table 5 Results of three-way ANOVAs testing the effects of plant life-form, survival status of nurse plants, and the position from their canopy on some physical and chemical attributes of soil.*: p < 0.05,**: p < 0.01, and***: p < 0.001. Variablea

Life-form (LF)

Survival (S)

Position (P)

LF* S

LF* P

S* P

LF* S* P

Organic matter Clay Silt Sand pH EC SAR ESP Na Ca Mg K Cl SO4 N P

7.09* 0.15 0.32 0.11 22.0*** 10.6** 18.4** 18.4*** 14.8** 8.03* 0.86 2.14 12.9** 0.32 0.54 2.19

35.2*** 8.19* 4.50* 2.90 1.25 244.9*** 245.0*** 238.5*** 341.6*** 270.0*** 64.0*** 85.5*** 103.8*** 590.7*** 7.8* 0.89

4.42* 2.65 9.6** 4.20 17.29** 647.8*** 664.2*** 652.8*** 798.1*** 671.0*** 295.6*** 210.2*** 291.6*** 952.4*** 0.25 0.18

0.43 2.24 0.04 0.96 0.80 16.3** 0.02 0.00 11.3** 23.6*** 8.9** 4.5* 13.03** 22.1*** 12.8** 3.02

0.56 1.87 0.00 0.55 1.10 7.92* 1.54 1.33 8.9** 7.3* 3.91 0.39 18.6** 3.03 2.46 2.28

0.04 8.34* 6.30* 1.58 3.00 226.6*** 173.6*** 165.9*** 302.9*** 239.2*** 80.8*** 105.5*** 89.8*** 569.8*** 4.20 0.34

0.06 13.2** 2.09 1.41 1.98 9.3** 1.44 1.26 8.21* 12.5** 2.27 1.04 6.46* 13.6** 3.06 3.25

a

ESP: Exchangeable sodium percentage, SAR: Sodium adsorption ratio.

Table 6 physical and chemical characteristics of soil (means ± standard errors) under and next to dead and live shrubs and grasses. Variablea

Grass

Shrub

Live

Dead

Under OM (%) Clay (%) Silt (%) Sand (%) Ph EC (mS/cm) SAR ESP Na (meq/l) Ca (meq/l) Mg (meq/l) K (meq/l) Cl (meq/l) SO4 (meq/l) N (fog/Kg) P (fog/Kg) a

0.5 2.0 0.6 97.5 7.4 1.3 1.6 1.1 3.3 5.8 3.2 1.1 5.6 2.9 3.2 8.3

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

Next 0.0 0.0 0.3 0.3 0.1 0.1 0.1 0.1 0.2 1.0 0.4 0.2 0.8 0.7 0.3 1.0

0.4 2.1 0.7 97.1 8.0 0.6 1.1 0.3 1.4 2.3 1.3 0.7 0.7 2.5 2.2 9.0

Live

Under ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.1 0.1 0.5 0.6 0.1 0.0 0.1 0.1 0.1 0.2 0.1 0.3 0.1 0.2 0.2 0.8

0.7 2.6 2.3 95.1 7.9 4.0 2.8 2.8 10.6 20.9 7.9 2.7 19.1 19.2 2.5 4.3

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

Next 0.0 0.3 0.3 0.0 0.0 0.2 0.1 0.1 0.6 1.0 0.7 0.1 1.8 0.8 0.2 0.5

0.5 2.0 1.6 96.5 7.9 0.7 1.1 0.4 1.7 3.1 1.4 0.5 1.6 2.9 2.0 7.5

Dead

Under ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.1 0.1 0.1 0.2 0.4 0.1 0.0 0.1 0.2 0.4 0.2 0.0 0.6 0.3 0.5 0.9

0.4 1.9 0.7 97.4 8.0 1.4 1.4 0.8 3.2 6.9 3.5 0.7 4.6 6.0 1.4 7.7

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

Next 0.0 0.2 0.3 0.3 0.0 0.0 0.0 0.0 0.1 0.1 0.2 0.0 0.2 0.1 0.6 1.5

0.3 2.6 0.6 96.8 8.6 0.6 0.9 0.1 1.3 2.7 1.8 0.4 1.6 2.4 0.3 9.1

Under ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.1 0.1 0.1 0.1 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.1 0.1 0.2 0.5

0.6 2.5 1.2 96.3 8.1 3.1 2.5 2.4 8.3 15.7 6.3 2.9 11.7 17.5 3.1 11.0

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

Next 0.0 0.1 0.1 0.0 0.0 0.1 0.0 0.1 0.2 0.2 0.2 0.1 0.1 0.3 0.3 3.3

0.5 1.8 2.5 95.7 8.5 0.6 1.0 0.3 1.4 2.6 1.3 0.4 1.4 2.3 3.9 7.4

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.0 0.1 0.1 0.1 0.0 0.1 0.1 0.1 0.2 0.3 0.1 0.1 0.4 0.3 2.4 0.8

OM: Organic matter, ESP: Exchangeable sodium percentage, SAR: Sodium adsorption ratio.

greater under dead grasses, compared with all other categories (dead and live shrubs and live grasses). The facilitative effect of dead grasses versus the inhibitory effect of live grasses indicates that competition plays a significant role in shaping plant community structure. It is interesting to note that our findings do not match those of previous studies, which reported the facilitative effects of the grasses on shrubs in the Mediterranean semiarid climate. For example, Anthelme and Michalet (2009) showed that the tussock grass P. turgidum facilitated the regeneration of the keystone tree
ne
re
Nature species, Acacia tortilis var. raddiana, in the Aïr-Te Reserve (Sahara, Niger). In addition, Alados et al. (2006) indicated that Stipa tenacissima, a tussock grass found in semiarid southeastern Spain, facilitated other shrubby species in high slopes, but it competed with them in low-slope and flat areas. The discrepancy in grass facilitation in most studies on the Mediterranean semiarid climate of Spain and the inhibition observed in the present study could be attributed to the greater aridity (e.g., the lower rainfall and higher temperatures) of the Arab Gulf region, which may substantially affect competitive interactions between species (Goldberg and Novoplans, 1997). Maestre and Cortina (2004) suggested that a shift from facilitation

to competition under high abiotic stress conditions is likely to occur, even in a semiarid climate. The Mediterranean semiarid climate in Spain has a 30-year average annual precipitation of
rez Cueva, 388 mm and a mean annual temperature of 16e18  C (Pe 1994). However, the mean annual temperatures are about 36  C, and the total amount of rainfall received in the study year was only 24.4 mm at the meteorological station nearest to the study area (AlFaqa). The diverse mechanisms of facilitation in harsh arid and semiarid areas vary based on the life-form of nurse plants. Nurse plants may protect plants from herbivores (Rebollo et al., 2005) and especially seedlings from high irradiance and temperature, consequently reducing evaporative demand (Valiente-Banuet and Ezcurra, 1991). In the present study, live shrubs significantly enhanced the density of two palatable plants (P. divisum and Farsetia linearis) and two unpalatable plants (Arnebia hispidissima and Bassia muricata). All the studied nurse shrubs are palatable and not thorny. Consequently, the facilitation observed in the present study could not have been caused by nurse shrubs protecting the understory vegetation. Several studies focusing on desert shrublands have indicated that seeds are more likely to be trapped under shrub canopies than

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in the openings next to them (Mull and MacMahon, 1996; €rger and Kadmon, 2000). In the present study, the four speTielbo cies that were facilitated by live shrubs have dispersible diaspores that can be trapped by the canopy of the nurse plants. The whole dead plants of both A. hispidissima and B. muricata along with their seeds are dispersed as units that can be trapped under the canopy of a nurse plant. In addition, the diaspores of the other two species are light and adapted for dispersal by winds; P. divisum spikelets are equipped with lemma and palea, and F. linearis fruits have small wings. Consequently, the ability of nurse shrubs to trap seeds could explain the facilitation of species with dispersible seeds. However, the facilitative effect of dead grasses could not be explained by their ability to trap seeds. The open tussocks of dead and live grasses are less capable of trapping seeds than shrubs; nevertheless, dead grasses facilitated the establishment of 13 species, but live shrubs facilitated only four species. Further studies are needed to assess the relationship between the mode of seed dispersal of understory plants and the ability of nurse plants with different growth forms to trap seeds. Under arid and semiarid environments, the competition for water is more important than that for light or nutrients (Casper and Jackson, 1997). Facilitation takes place only if a certain threshold of € rger and Kadmon, 2000). Our study indimoisture is met (Tielbo cated that associated species around live grasses attained significantly lower values of richness, density, and the three diversity indices, in comparison to live shrubs. The amount of soil water that could be received under live shrubs and grasses did not explain this result. During extremely dry years, like that of our study year (total rainfall received was 24.4 mm), rain interception by the shrubs reduces undercanopy wetting such that the germination of facilitators is severely affected in desert habitats (Kidron, 2010). However, stem flow in grasses spatially concentrate the water in the soils under the plants (Guevara-Escobar et al., 2007). The closed canopy of shrubs has greater interception storage capacity, allowing more water loss through evaporation, compared to grasses with open growth form. Nevertheless, the shrubs showed a greater facilitative effect. Our results indicated that the diversity indices were significantly greater under the live shrubs than in the surrounding barren areas. This result could be attributed to greater spatial heterogeneity under shrub canopies. Greater variations in shade intensity and amount of water received under the canopy and increased soil fertility due to litter decomposition are expected (El-Bana et al., 2007). Such a heterogeneity creates more safe sites for the emergence of more species, compared with the more homogeneous barren areas between shrubs. Conversely, the associated plants did not differ significantly in density under and in the open places next to live shrubs. This indicates that the expected interspecific competition between individuals of the associated plants and the nurse shrubs for the limited resources, especially water, might reduce the density of plants under the shrub canopies. In the present study, OM and most of the assessed soil nutrients (e.g., Ca, Mg, K, Cl, and SO4) attained significantly greater concentrations under both shrubs and grasses, compared with the barren spaces between them. In addition, OM and most of these nutrients attained greater values under dead shrubs and grasses than under live shrubs and grasses, leading to a clearly ameliorating effect of dead grasses in many of these variables. The shading and litter fall from nurse plants may provide relatively more appropriate conditions for microbial activity, compared with areas next to them (Moro et al., 1997). Grasses have dense root systems in the upper layer of the soil (Jackson et al., 1996; Soriano et al., 1987), which would further increase soil fertility after decomposition in the wetter years. This could explain the greater abundance and diversity under dead grasses than under live shrubs and grasses and

dead shrubs. Desertification is one of the main types of land degradation in arid and semiarid areas. Overgrazing, mainly by camels, affects >90% of the land on the Arabian Peninsula, 44% of which is severely or very severely degraded (Ferguson et al., 1998; El-Keblawy et al., 2009; Ghazanfar and Osborne, 2010). Where restoration fails due to harsh environmental conditions or intense herbivory, species that minimize these effects could be used to enhance the performance
mez-Aparicio, 2009). Although this of nearby target species (Go “nursing” procedure has found few applications for restoration worldwide, the experimental data are promising, with enhanced plant survival and growth in areas close to nurse plants (Padilla and Pugnaire, 2006). The results of the present study showed significantly enhanced physical and chemical properties of the soil and increased species diversity and abundance under both live and dead shrubs and dead grasses, compared with the surrounding barren spaces. Such results indicate that restoring degraded deserts with nurse plants would improve the structure of plant communities, restoring the degraded arid desert lands of the UAE in particular. Nurse plants can act as natural barriers for reducing wind velocity, increase the deposition of fine soil particles rich in nutrients, and increase soil OMs that enhance the water-holding capacity and seed bank of the soil, the latter enhancing seedling emergence and hence the diversity of floral and faunal communities. Conversely, the barren interplant spaces cause soil erosion by wind and nutrient losses from the landscape (Hennessy et al., 1985; Parsons et al., 2003). Our results indicated that dead grasses and shrubs facilitated more perennial shrubs, compared with other life-forms. The facilitated shrubs act as sources of propagules with significant effects on population dynamics, facilitating a positive interaction between clumped species and, in consequence, the plant spatial aggregation patterns (Tirado and Pugnaire, 2003, 2005). This would ensure that higher biodiversity is maintained in the restored habitats. Interestingly, the shrubs facilitate the environment for several other shrubs under them. Such spatial aggregation patterns of shrub will widen (spread over space) over the successional stages in the restored sites. For restoring the productivity and species diversity of the degraded sandy desert habitats, the present study recommends maintaining and growing more shrubby plants as an early successional stage. Although regular restoration projects span several years until the climax stage, the use of nurse plants for restoration would facilitate the growth of annuals and small shrubs and attract the local fauna within few years (Ghazanfar and Osborne, 2010). Acknowledgments The authors are grateful to Prof. C. L. Alados (Instituto Pirenaico de Ecología C.S.I.C, Zaragoza, Spain) for her critical comments of the manuscript. References Alados, C.L., Gotor, P., Ballester, P., Navas, P., Escos, J., Navarro, T., Cabezudom, B., 2006. Association between competition and facilitation processes and vegetation spatial patterns in alpha steppes. Biol. J. Linn. Soc. 87, 103e113. Anthelme, F., Michalet, R., 2009. Grass-to-tree facilitation in an arid grazed environment (Aïr Mountains, Sahara). Basic Appl. Ecol. 10, 437e446.
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