BIOMASS ALLOCATION IN Ziziphus spina-christi AND THE INVASIVE SPECIES Prosopis juliflora

Invasion by the exotic species Prosopis juliflora has become a major threat to native plants in Saudi Arabia as the species continues its spread into different regions of the country. Ziziphus spina-christi is a native tree that is common in Saudi Arabia. The objective of this study was to determine how both species would benefit from the availability of sufficient resources without competition. To gain a better understanding of growth under such conditions, a greenhouse experiment was conducted in which seedlings of both species were grown under favorable conditions for 6 months. During this period, growth performance was evaluated three times at intervals of 30, 90, and 180 days. Growth performance varied between the two species during one or more of the studied periods. Significant differences between the species were observed for root mass fraction, number of root tips, root to shoot ratio, height, stem diameter, stem dry weight, stem mass fraction, leaf area, leaf mass fraction, and chlorophyll a and b contents. The relative growth rate (RGR) and relative height growth rate were higher in P. juliflora at 30–90 days, whereas leaf area ratio and net assimilation rate were higher for Z. spina-christi at 90–180 days. Remarkably, the RGR for diameter in P. juliflora was almost double that in Z. spina-christi at 30–90 days and 90–180 days. The results obtained reflect a strategic difference in the biomass allocation to different plant components by the two species, whereby P. juliflora allocates higher biomass to the stems and Z. spina-christi allocates higher biomass to the roots.


INTRODUCTION
In invaded regions, invasive alien species are released from the pressure of their native herbivores and parasites (KEANE; CRAWLEY, 2002), and the reduction in resources allocated to herbivore defense is invested in growth (BLOSSEY;NOTZOLD, 1995;TORCHIN et al., 2003).In an environment where resources are not limited, leaf traits are most important for successful invaders to take advantage with rapid growth, whereas integration with traits related to root tissue is an important factor for plant performance in different environments (DIAZ et al., 2004).Successful invasive species tend to allocate less biomass to roots than native species (WILLIAMS; BLACK, 1994;WILSEY;POLLEY, 2006), but tend to allocate high amounts of resources to stems and branches for canopy support (RADOSEVICH, et al., 2007).Under favorable conditions and without competition, invasive species generally have a higher relative growth rate (RGR), leaf area ratio (LAR), and/or specific leaf area (SLA) than related non-invasive species (FENG et al., 2008;GROTKOPP;REJMÁNEK, 2007;GROTKOPP et al., 2002).Disproportionate allocation to aboveground tissue is a pattern that enables invasive species to achieve high growth rates in undisturbed environments (BURNS et al., 2007).
Quantifying the growth rate of invasive species in contrast to natives is a starting point in understanding the dynamics of tree invasion.Many comparative studies have shown that native plant species have lower growth rates than invasive plants (AKASAKA;TSUYUZAKI, 2005;GLEASON;ARES, 2004).In most cases, higher growth rates are associated with the efficiency of using and allocating resources, which are traits that contribute to the higher performance of invasive species (PORTÉ et al., 2011).Consequently, higher resource allocation plasticity plays a key role in invasion (CALDWELL et al., 1981).
Most studies on plant growth have been designed to evaluate the response of plants to one or more stress conditions; however, only few studies have measured plant growth responses under favorable conditions.Variations in RGR among species are most apparent when plants are grown under favorable conditions (GROTKOPP; REJMÁNEK, 2007).The present study accordingly aimed to quantify RGR and biomass allocation and the patterns of resource allocation and utilization under favorable conditions in a native (Ziziphus spina-christi) and an invasive (Prosopis juliflora) Biomass allocation ALSHAHRANI, T. S.
Biosci.J., Uberlândia, v. 33, n. 2, p. 390-400, Mar./Apr.2017 woody plant species.The preliminary assumption made in this study was that both native and invasive species will exhibit the same patterns of resource allocation under the same growth conditions.

MATERIAL AND METHODS
Seeds of Z. spina-christi and P. juliflora were collected from 12 trees in central Saudi Arabia.Seeds of both species were separately sown in 10 × 10 × 32 cm plastic pots filled with sterilized sand.A total of 96 pots were established in monoculture, with 48 pots containing only Z. spinachristi and 48 pots containing only P. juliflora seedlings in a completely randomized design.A complete nutrient solution, Johnson's solution (JOHNSON et al., 1957), was used to fertilize the seedlings: 200 ml per pot administered once a week throughout the experiment.The seedlings were grown in a greenhouse at 30°C (D/N), and under a 13-hour photoperiod with illumination provided by HPS lights (400 W).Seedlings were watered with 120 ml tap water once a week.On the basis of the complete unfolding of the first true leaf, plants were harvested at intervals of 30, 90, and 180 days thereafter.
For each interval and before harvesting plants, the following data were measured: number of leaves, plant height (cm) from the cotyledon scars to the stem apex, and stem diameter (mm) at the cotyledon scar using a digital caliper (±0.04 mm).The number of leaves was counted for every seedling, and leaf area was measured for all leaves using a leaf area meter (L-COR 3100; LiCor Inc., Lincoln, NB, USA).
After removing soil from the roots with water, the roots of each species were spread over a computer scanner (UMAX 4000U with 1200 dpi by 2400 dpi resolution) and scanned at 600 dpi using Adobe Photoshop 5.5 (Adobe, 2001).The images were analyzed using WinRhizo software (Regent Instruments Inc., 2002) to measure total root length, volume, surface area, and number of tips.Roots, stems, and leaves were separately dried at 75°C for 48 h to obtain dry weights.RGR, net assimilation rate (NAR), and LAR were calculated according to Dash et al. (2013).

Statistical analysis
Data were statistically analyzed using the General Linear Model procedure in the Statistical Analysis System package (SAS 9.1 for Windows; SAS Institute Inc., Cary, NC, USA).Two-way ANOVA was used to examine the effect of species, days, and their interaction on dependent variables.
Multiple comparisons among pairs of means were performed using Bonferroni's multiple comparison test based on least square means, and all test results were evaluated at a significance level of α = 0.05.

RESULTS
The results presented below include only those showing a variation between the two species throughout the three harvest intervals.The variation in root traits was significant in one or more intervals, including root mass fraction, number of tips, and root to shoot ratio (Figure 1 A, B, and C).The root mass fraction and root to shoot ratio of the invasive species P. juliflora remained almost constant over time during the three harvest periods.In contrast, the root mass fraction and root to shoot ratio of Z. spinachristi increased over time.The total root length, root surface area, root volume, and root dry weight did not vary significantly between the two species during any harvest interval (Figure 1 D, E, F, and G, respectively).
Figure 2 shows the stem traits of height, diameter, dry weight, and mass fraction.The results indicated significant differences in stem traits between the two species in one or more interval.The height of P. juliflora seedlings increased rapidly and at the final harvest time, P. juliflora exceeded Z. spina-christi in height (Figure 2 A).Stem diameter increased over time, and the diameter in the invasive species exceeded that in the native species at 90 and 180 days (Figure 2 B).Stem dry weight was significantly higher in P. juliflora than in Z. spinachristi at 90 and 180 days (Figure 2 C).Additionally, the stem mass fraction was higher for the invasive species compared to the native species.Stem mass fraction tended to be constant in the native species throughout the three harvest times (Figure 2 D).Total dry weight did not vary significantly between the two species during any harvest interval (Figure 2 E).
The results indicated that leaf area and leaf mass fraction were higher for Z. spina-christi compared to P. juliflora.Leaf area increased with time in both species (Fig. 3 A), but leaf mass fraction decreased with time in the two species (Figure 3 B).SLA and leaf dry weight were not significantly different between the two species in any harvest interval (Figure 3 C, D).
At 90 days, the leaf content of chl a (µg/ml) was significantly higher in Z. spina-christi compared with P. juliflora.In contrast, the chl b content of P. juliflora was significantly higher at 30 days (Table 1).Biomass allocation ALSHAHRANI, T. S.

DISCUSSION
Changes in biomass allocation toward plant organs are assumed to take place in order to maximize the capture of limited resources.However, the two species examined in the present study had different patterns of biomass allocation.There was a notable constancy in stem fraction throughout the experimental period in Z. spinachristi, whereas the root mass fraction was constant in P. juliflora.In dry tropical areas, the success of an invasive species depends mostly on the ability to allocate biomass to its different organs (GUPTA; NARAYAN, 2012).Invasive species, including shrubs, trees and grasses, tend to allocate most of their resources to the aboveground parts (stems, branches, and leaves) and less to roots (RADOSEVICH et al., 2007;WILLIAMS;BLACK, 1994;WILSEY;POLLEY, 2006;QIN et al., 2012).Qin et al. (2012) showed that the invasive species Ambrosia artemisiifolia modified biomass allocation in response to different irradiance environments by increasing biomass allocation to stems and decreasing the allocation to roots at lower irradiance levels.This biomass allocation pattern indicates that successful invasion depends on environmental conditions.Alshahrani ( 2004) found that P. juliflora allocated above-ground biomass toward the stem instead of leaves, which contrasts to the allocation pattern in Z. spina-christi.However, the observed increase in shoot biomass concomitant with an increase in stem diameter in P. juliflora is consistent with the findings of Claridge and Franklin (2002).It is remarkable that the RGR for stem diameter in P. juliflora was approximately twice the value in Z. spina-christi for both 30-90day and 90-180-day intervals.
Successful invasion depends mainly on the efficiency with which invasive species use limited resources or on their ability to use them selectively Biomass allocation ALSHAHRANI, T. S.
Biosci.J., Uberlândia, v. 33, n. 2, p. 390-400, Mar./Apr.2017 at times when they are unavailable to the native species (VITOUSEK, 1996).Biomass allocation may also affect the success of invasive plants, whereby increasing biomass allocation to leaves may increase LAR.Indeed, some successful invasive species do allocate more biomass to leaves and less to roots than native species (KNAPP et al., 1998;WILLIAMS;BLACK, 1994;WILSEY;POLLEY, 2006).Although this pattern of biomass allocation may promote irradiance capture, it may also impair water and nutrient absorption, again indicating that invasion success may be environmentally dependent.The high root to shoot ratio in Z. spina-christi illustrated that species growing in nutritionally poor soils, e.g., desert, normally have higher biomass allocation to the roots (CHAPIN, 1980;LYNCH, 1995).
Although it is seldom found that an invasive species outperforms native species under all conditions (ZHENG et al., 2009), increasing resource availability often facilitates alien plant invasions (DAEHLER, 2003).Therefore, environmental conditions should be considered when identifying the traits contributing to invasiveness.However, these results of the present study were obtained under controlled conditions without nutrient or moisture shortage, and in the absence of other biotic interactions, e.g., speciesspecies interactions that could change the growth rate.Alshahrani (2004) found that under high levels of nitrogen, in mixed plantings, most measured parameters of P. juliflora exceeded the corresponding parameters of Z. spina-christi.Height, leaf area, total dry weight, and total chlorophyll ab were reduced for Z. spina-christi seedlings grown with increasing proportions of P. juliflora.In addition, although P. juliflora tended to be more aggressive at high nitrogen levels, the aggressiveness and relative yield of P. juliflora decreased as its proportion increased in mixed culture.At low nitrogen levels, the growth of Z. spina-christi exceeded that of P. juliflora in most growth parameters, illustrating that Z. spina-christi had a competitive advantage over P. juliflora at low nitrogen levels.
The high RGR in P. juliflora may reflect the invasive plant's ability to achieve higher RGR by increasing the rate of photosynthesis or decreasing the rate of respiration (JAMES; DRENOVSKY, 2007).In the present study, there was a gradual decrease in LAR in both species during the experimental periods, and the differences in RGR may be due to a decrease in LAR, since LAR is the major component of RGR.Variations in LAR will thus have a significant effect on the values of RGR.
The reductions in SLA and LAR over time are consistent with the findings of Dias-Filho and De Carvalho (2000) and Crisóstomo et al. (2007).Prosopis juliflora tends to shed its leaves heavily under normal conditions (GOEL et al., 1989).This pattern indicates that invasive plants have less leaf area than natives (DURAND; GOLDSTEIN, 2001).Furthermore, the stability of the root mass fraction in P. juliflora may contribute to its higher RGR.Decreasing root systems in plants will decrease the root respiratory load, leading to increased carbon accumulation (D'ANTONIO et al., 2001).
Many studies have demonstrated that native species growing in arid and semiarid regions are adapted to soil nutrient deficiency and exhibit a lower RGR in comparison to their invasive counterparts (CRONK;FULLER, 1995;PATTISON et al., 1998;GARCIA-SERRANO et al., 2005).It is well known that invasive species have higher growth rates compared with natives (AKASAKA; TSUYUZAKI, 2005; GLEASON; ARES, 2004).The ecological advantage of a high RGR allows invasive plant to capture resources rapidly, occupy space, and reduce the time between vegetative growth and reproduction (POORTER, 1989).However, the low RGR of native species can be advantageous in that some researchers have suggested that natural selection in nutrient-poor environments has targeted one of the underlying components of RGR instead of RGR itself (LAMBERS; DIJKSTRA, 1987).For example, traits that contribute to the conservation and efficient use of resources in resource-poor systems are advantageous; however, these traits may simultaneously lower RGR.There is no strong agreement on whether introduced species differ from natives in their aboveground growth rates, and characteristics based on belowground growth are poorly understood.For instance, Vilà and Wiener (2004) found that native species exhibited greater aboveground growth rates in comparison with introduced species, whereas Ehrenfeld (2003) found that biomass and net primary productivity were higher in invaded sites in 14 out of 18 cases.Conversely, Daehler (2003) found no difference between native and introduced species.
In conclusion, the results of the present study reveal a strategic alteration in biomass allocation to different plant components under favorable conditions by an invasive (P.juliflora) and a native (Z.spina-christi) species over the course of the experiment.However, in contrast to P. juliflora, which allocated higher biomass to the stem, Z. spina-christi allocated higher biomass to the roots.It is important, nevertheless, to emphasize Biomass allocation ALSHAHRANI, T. S.

Figure 1 .Figure 2 .Figure 3 .
Figure 1.Changes over time in root traits for the native species Ziziphus spina-christi and the invasive species Prosopis juliflora.

Table 1 .
Chlorophyll a and b in Prosopis juliflora and Ziziphus spina-christi monitored for 30, 90, and 180 days.
*Data presented are ANOVA least square means (standard deviations in parentheses)

Table 2 .
Relative height growth rate, root elongation rate and diameter relative growth rate for Prosopis juliflora and Ziziphus spina-christi for two monitored periods.
* Data presented are ANOVA least square means (standard deviations in parentheses)

Table 3 .
Relative growth rate (RGR), Leaf Area Ratio (LAR) and Net Assimilation Rate (NAR) in Prosopis juliflora and Ziziphus spina-christi for two monitored periods.
*Data presented are ANOVA least square means (standard deviation in parentheses)