Effect of urban habitat heterogeneity on functional traits plasticity of the invasive species Calotropis procera (Aiton) W.T. Aiton Emad Farahat, Tarek Galal, Maha ElMidany & Loutfy Hassan
Rendiconti Lincei SCIENZE FISICHE E NATURALI ISSN 2037-4631 Rend. Fis. Acc. Lincei DOI 10.1007/s12210-015-0408-3
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Author's personal copy Rend. Fis. Acc. Lincei DOI 10.1007/s12210-015-0408-3
Effect of urban habitat heterogeneity on functional traits plasticity of the invasive species Calotropis procera (Aiton) W.T. Aiton Emad Farahat1,2 • Tarek Galal1 • Maha El-Midany1 • Loutfy Hassan1
Received: 23 December 2014 / Accepted: 1 March 2015 Ó Accademia Nazionale dei Lincei 2015
Abstract Microhabitat heterogeneity with a high environmental variability affects the persistence of species and their population dynamics. This study investigated the effect of urban habitat heterogeneity on the morphological and reproductive traits as well as foliar nutrient contents of Calotropis procera. Sixty-three permanent stands (5 9 5 m) were selected to represent the micro-variations in four urban habitats of C. procera in Cairo, Egypt. C. procera populations showed significant variations in the size structure, biomass and density between the studied habitats. Size class distribution was bell- or biomodal shaped in most habitats, which suggests that C. procera adopts an adult-persistence population survival strategy. It was characterized by low episodic recruitment rates and relative stability. C. procera had significant plasticity in morphological and reproductive traits with changing of soil edaphic factors in urban habitats. Foliar Na, K and P concentrations were significantly different in the studied habitats, in addition to their significant correlations with the same elements in soil. The variation in the functional traits of the plant indicated its ability to persist under urban habitat conditions. It is likely that C. procera may dominate in the future the urban habitats under extensive degradation of the natural habitats of native species.
& Emad Farahat
[email protected] 1
Botany and Microbiology Department, Faculty of Science, Helwan University, Cairo, Egypt
2
Present Address: Department of Earth Sciences, Regional Climate Group, University of Gothenburg, Gothenburg, Sweden
Keywords Giant milkweed Urban habitats Functional traits Growth plasticity Size structure Biomass Invasion risk
1 Introduction Urban areas are unique habitats, where large populations of humans build dense dwellings. These areas have been significantly modified from their former natural state into what are known as urban ecosystems. With extensive degradation of natural habitats and attendant biota, urban areas are often characterized by low biodiversity, introduction of non-native (invasive) species, simplified species composition and community structure (McKinney 2002; Lundholm and Marlin 2006; Jim and Chen 2010). Distribution and abundance of a plant species within a particular climatic zone are determined by environmental factors, especially soil conditions, interactions with other species and dispersal. The size structure and growth of a plant population are determined by temporal variation in several biotic and abiotic factors that have acted on both past and current individuals in the population (Bullock et al. 1996; Hutchings 1997). The spatial structure of plant populations is also a legacy of the spatial arrangement of parent plants and the historical interactions between them (Hutchings 1997). Inferring mechanisms from known size class distributions can be challenging and necessitates a holistic, integrated approach, with maximal use of available data (Cousins et al. 2014). Understanding the ecological performance of invasive species relative to the entire native community is important in understanding and managing both the mechanisms and the potential impacts of invasion. Functional traits reflect a species’ interactions with the biotic and abiotic
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environment (McGill et al. 2006). These traits demonstrate differences in resource use and life history strategy among plants, reflecting important fundamental niche axes along which species are differentiated. Because they are related to one or more components of plant fitness (Violle and Jiang 2009), they are good candidates to study the causes of invasion across a wide range of ecological conditions (Tecco et al. 2010). Calotropis procera (Aiton) W.T. Aiton (Asclepiadaceae) is a perennial xerophytic medicinal shrub or small tree that grows as a wasteland plant and reproduces by seeds. It is native to tropical and subtropical Africa and Asia and common in the Middle East. This plant can tolerate adverse climatic conditions and poor soils (Parsons and Cuthbertson 2001; Lottermoser 2011). It has an evergreen behavior under field conditions, from young plant to the reproductive stage (Frosi et al. 2012). Recently, increased urbanization in Cairo, Egypt, has led to decrease in the biodiversity of native plant species and exponential increase in the invasiveness of many species such as C. procera (El-Midany 2014). The impacts of urbanization on native species are poorly studied, but educating a highly urbanized human population about these impacts can greatly improve species management in all ecosystems (McKinney 2002). In addition, the impact of urban habitat heterogeneity and its associated disturbances on the growth dynamics of C. procera is not well documented. Microhabitat heterogeneity with a high environmental variability affects persistence of species and demography of populations. Moreover, plasticity of a species has a crucial role in altering its population dynamics (Miner et al. 2005; Hegazy et al. 2010). Accordingly, our hypothesis is that C. procera as a new invading species of urban habitats will display plastic changes in its functional traits and its foliar nutrient contents, which reflect the edaphic resource gradients when present. The aim of the present study is to analyze the functional traits of C. procera in relation to abiotic conditions, considering population density, size structure, biomass and morphological and reproductive characters as an intra-specific plasticity that improves survival of the species in heterogeneous microhabitats. Plant–soil relationship in different microhabitats was also investigated.
2 Methods 2.1 Study area and stand selection The present study area belongs to ‘‘regenerated habitats’’, which is human induced or naturally regenerating and occurs on all types of disturbed ground. It is located in Helwan region (29°510 N, 31°200 E), which is one of the major
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industrial urban areas, 25 km south Cairo, Egypt. Cement, automobiles, iron, steel, textiles and wood furniture are the main industrial activities in this region. Various vegetation types are present in the area, but there is no predominant ground cover (Abdel Hameed et al. 2009). Rainfall in the study area occurs in the cold season from October to May, while summer is practically rainless and the mean annual rainfall in the area is 4.7 mm year-1. The mean annual minimum temperature is 13.4 °C, maximum temperature is 30.3 °C and average relative humidity is 54.9 % (courtesy of Egyptian Meteorological Organization). We selected four urban microhabitats (habitats, hereafter) which represent the current distribution of the species in Cairo, which are residential areas, fallow (abandoned) lands, roadsides and railway sides. The age of the different habitats is not well documented, but seems from the ongoing activities that the fallow land and railway habitats are older than the other two habitats. The residential habitat is characterized by anthropogenic activities more than the other habitats. On the contrary, fallow lands receive episodic water supply from many resources (Personal observation). We could not estimate the exact ages of the habitats due to the absence of distinct annual rings in the plant stems. All the selected populations in this study were healthy with no apparent physical damage to the individuals. In our study area, C. procera forms pure stands without or with few associated weeds such as Alhagi graecorum, Convolvulus arvensis, Solanum nigrum and Cynodon dactylon (El-Midany 2014). Sixty-three permanent stands (quadrats, 5 9 5 m) were selected to represent the micro-variations of C. procera in the selected urban habitats: residential areas, 26 quadrats; roadsides, 8 quadrats; railway sides, 19 quadrats; and fallow lands, 10 quadrats. These sampled quadrats were visited monthly during the period from February 2012 to January 2013 for measuring the growth dynamics of the study species. 2.2 Functional traits In each quadrat, all the individuals of C. procera were permanently marked by colored tags and their density was measured (i.e., number of individuals/unit area). The number of branches of each individual in the quadrat was counted at the first month of this study; then three main branches were marked for counting their lateral branches monthly from February 2012 to January 2013. The number of leaves/branches was counted monthly through random selection of five different branches, while the leaf area was determined by the trace paper method. At each marked branch, the numbers of flowers and fruits were determined. The mean fruit length and width as well as weight were measured in a set of 20 fruits from each location. For each habitat, the seed traits of C. procera including its number,
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length and width were estimated. The annual means of the measured morphological and reproductive traits were calculated. The aboveground biomass of C. procera individuals was calculated from the equation: y ¼ 0:154x þ 1:307, where y is the shoot dry weight and x is its volume (El-Midany 2014). The biomass per unit area was calculated using the individual plant method (Moore and Chapman 1986): Biomass (kg ha-1) = mean shoot weight (kg dry weight ind.-1) 9 density (ind. ha-1). The ratio of height to diameter varies from one habitat to another; therefore, the estimation of both variables seems to be best for expressing the shrub size (Shaltout and Ayyad 1990). The tree height (H) and average crown diameter (D) (based on 3 measurements ind.-1) were estimated for each permanent marked individual and their volumes were calculated as cylinders. The size index of each individual was calculated as the average of its height and diameter: (H ? D)/2 (modified from Crisp and Lange 1976), and used to classify the population in each habitat into six size classes (\0.5, 0.5–1, 1–1.5, 1.5–2.5, 2.5–3.5, [3.5 m). The absolute frequency of individuals and mean height and diameter per individual in each size class were then calculated. The size frequency distribution of the whole population was also calculated. The height to diameter ratio (H/D) per individual was determined according to Shaltout and Ayyad (1988).
classified according to particles size into: gravels, coarse sand, fine sand, silt and clay. Moisture content was determined using aluminum pans (Allen et al. 1986). Soil extracts were prepared to meet the requirements for different determinants, 1:5 (w/v) soils (g):distilled water (ml). This extract was used to determine pH values using a glass electrode pH meter (Model 9107 BN, ORION type) and electrical conductivity (EC) with conductivity meter 60 Sensor Operating Instruction Corning. Carbonates and bicarbonates were determined by titration against 0.1 N HCl using phenolphthalein and methyl orange as indicators. Chlorides, sulfates, total N, total P, Na, K, Ca and Mg were analyzed following Allen et al. (1986). 2.5 Statistical analysis One-way analysis of variance (ANOVA) was applied to assess the significance of variations in the growth variables, nutrient elements and soil variables in the different studied habitats. Simple linear correlation coefficient (r) was calculated for assessing the type of relationship between the spatial variations in the estimated soil variables in relation to the plant growth variables as well as the foliar mineral contents (SPSS 2006). Principal component analysis (PCA) was carried out for soil parameters as a discrimination tool for the studied populations in their habitats (CAP Software Program 1999).
2.3 Plant analysis Three composite leaf samples were collected from different C. procera individuals in each habitat in plastic bags. The samples were left to air dry and then oven dry at 60 °C to constant weight, and then ground into a powder using a metal-free plastic mill. Nutrients were extracted from 1 g samples using mixed-acid digestion method. Total N was measured by Kjeldahl method and total phosphorus (P) by applying molybdenum blue using a spectrophotometer (CECIL CE 1021). Sodium, calcium and potassium were determined using flame photometer (CORNING M410), while magnesium was determined using atomic absorption (Shimadzu AA-6200). All these methods are outlined by Allen (1989). 2.4 Soil analysis Three soil samples were collected from each habitat at the end of the growing season (January 2013) from the first 50 cm of the superficial soil. The soil samples were brought to the laboratory in plastic bags shortly after collection; air dried, passed through a 2 mm sieve to remove debris and then packed in paper bags to be ready for mechanical and chemical analysis (Allen et al. 1986). Soil texture was determined by using the sieve method and
3 Results 3.1 Morphological traits The plant populations in different habitats are distinguished morphologically by many characteristic traits. Plant individuals in fallow lands had the highest stem height (H) and crown diameter (D) (2.4 and 2.2 m, respectively), while short individuals were recorded in residential areas (H = 1.4, D = 1.1 m) (Table 1). There was a significant linear correlation between H and D of the plant individuals in different habitats (Table 1). The mean H/D ratio was more than unity in all habitats with the highest ratio (2.0) in railways, while the lowest (1.2) was recorded for population’s individuals on roadsides and fallow lands. The total mean of size index and mean individual’s volume had significant differences among the studied populations (Table 1). Plant individuals in fallow lands had the highest values of both parameters (2.3 m, 14.6 m3, respectively), while in residential areas it had the lowest (1.3 m, 6.0 m3, respectively). C. procera had the highest biomass (4636.9 kg ha-1) on roadsides, while the lowest (1941.1 kg ha-1) was in residential areas. Likewise, the highest individual’s density (8529.9 ind. ha-1) was
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Author's personal copy Rend. Fis. Acc. Lincei Table 1 Morphological traits and biomass of Calotropis procera in different habitats
Habitats
Residential areas
Roadsides
Fallow lands
Railways
Height (m)
1.4 ± 1.1a
1.6 ± 0.9a
2.4 ± 1.0b
1.9 ± 1.3ab
8.7***
1.2 ± 1.2a
10.7***
Diameter (m)
1.1 ± 1.1
a
1.6 ± 1.1
ab
b
2.2 ± 1.0
F value
H/D
1.7 ± 0.7
1.2 ± 0.3
1.2 ± 0.2
2.0 ± 1.0
r
0.95***
0.76***
0.94***
0.90***
Size index (m)
1.3 ± 1.1a
1.6 ± 0.9a
2.3 ± 1.0b
1.6 ± 1.2a
3
a
a
Volume (m )
6.0 ± 14.8
6.6 ± 12.0
No. of branches
15.1 ± 29.9a
21.4 ± 23.1a
No. of leaves branch-1
14.9 ± 5.0a
2
14.6 ± 22.6 20.4 ± 3.2b c
Leaf area (cm )
129.2 ± 33.2
Leaf length (cm)
16.2 ± 0.8b
17.7 ± 0.7c
17.9 ± 0.7c
b
c
c
149.4 ± 10.6
7.9 ± 17.2
64.8 ± 63.0b
15.5 ± 2.6a b
b
151.4 ± 12.1
c
13.3***
16.5 ± 2.9a
20.5***
106.1 ± 10.8a
24.2***
14.7 ± 0.8a
72.8***
10.3 ± 0.6
Biomass (kg ha-1)
1941.1
4636.9
4115.5
3692.8
Density (ind. ha-1)
901.5
8529.9
1111.9
1466.1
11.6 ± 0.5
2.7*
23.6 ± 44.4a
Leaf width (cm)
11.4 ± 0.5
9.7*** a
9.6 ± 0.6
a
57.2***
Mean ± standard deviation is shown. Different letters indicate significant differences within the same row. The minimum and maximum values are italicised r correlation coefficient between height and crown diameter * p \ 0.05, ** p \ 0.01, *** p \ 0.001
recorded on roadsides, while the lowest (901.5 ind. ha-1) was in residential areas. The total number of branches of C. procera plants showed significant difference among their habitats. Fallow lands had the maximum number of branches (64.8 branches ind.-1) and number of leaves (20.4 leaves branch-1), while residential areas had the lowest (15.1 branches ind.-1, 14.9 leaves branch-1, respectively) (Table 1). The maximum leaf length, width and area (17.9, 11.6 cm and 151.4 cm2, respectively) were recorded for plant individuals in fallow lands, while the minimum values (14.7, 9.6 cm and 106.1 cm2, respectively) were in the railway habitat. 3.2 Size structure The size class distributions of C. procera population in the different habitats attained one of the following patterns (Fig. 1): (a) bimodal size distribution in railways, (b) symmetrical (i.e., bell shaped) in fallow lands and roadsides and (c) positively skewed in residential areas. The contribution of juvenile individuals with size up to 1.5 m was obvious in residential areas, roadsides and railways (70.2, 60.0 and 54.5 %). The converse was true for the occurrence of adults (height 1.5–[3.5 m), where 80 % adult individuals were recorded in fallow lands (Fig. 1). 3.3 Reproductive traits Significant differences in the mean length, width and weight of C. procera fruits in the different habitats were recorded (Table 2). The produced fruits had their
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maximum length, width and weight (12.7, 13.5 cm and 44.0 g, respectively) in railway habitat, while the minimum values (11.4, 9.3 cm and 36.8 g respectively) were found on roadsides. The seed traits of C. procera including its number, length and width were significantly different in the different habitats (Table 2). The mean seed number had the maximum value (439.8 seeds fruit-1) in residential areas, while the minimum (390.0 seeds fruit-1) was counted in railway individuals. Seeds collected from fallow lands had the highest length and width (7.5 and 5.4 mm, respectively), while it had the lowest length (6.1 mm) and width (3.9 mm), respectively, in residential areas and roadsides. There was no significant difference in seed weight of plants collected from different habitats (mean weight was 0.1 g 10 seeds-1).
3.4 Nutrient concentrations The analysis of foliar inorganic elements of C. procera revealed that there were significant differences in P, K and Na between plants in the different urban habitats (Table 3). Leaves collected from the residential habitats had the highest concentrations of total N (20.2 mg g-1), P (3.6 mg g-1), Na (11.3 mg g-1) and Mg (10.0 mg g-1), but the lowest of K (28.4 mg g-1) and Ca (35.8 mg g-1). In fallow lands, plant leaves had the highest concentration of K (36.7 mg g-1) and Ca (42.3 mg g-1), but had the lowest total N (11.5 mg g-1) and Na (3.6 mg g-1). Railway habitat plants had the same K concentration as fallow lands, but it had the lowest concentration of total P (2.6 mg g-1) and Mg (6.9 mg g-1) (Table 3).
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3.5 Soil properties The PCA carried out on the matrix of four habitats and 24 soil characters revealed two principal components accounting for 56.8 % (Axis 1) and 31.8 % (Axis 1) of the variance (Fig. 2). The variation between the four habitats was mostly reflected on Axis 1. Residential areas and roadsides were clearly distinguished from the railway and fallow lands by the greater percentage of K, SO4, soil EC and soil texture fractions (gravel and silt). The fallow lands have opposite trend to other habitats and distinguished from them by the greater percentage of soil moisture content, Cu, Cl and N content. It was obvious that the railway habitat has distinctly greater percentages of heavy metals (Cd, Zn, Mn and Pb) and soil pH. 3.6 Plant–soil correlation The correlation between soil variables in all habitats and plant foliar nutrients showed that soil EC, Cl, SO4, Ca and Mg had significant positive correlation with foliar total P (r = 0.64, 0.66, 0.57, 0.73 and 0.74, respectively), as well as the soil EC, HCO3, Cl, SO4 and Mg with foliar Na (r = 0.58, 0.68, 0.63, 0.59 and 0.58, respectively) (Table 4). In contrast, some other soil variables had significant negative correlations with foliar inorganic elements, e.g., soil EC, HCO3, Cl, SO4, Ca and Mg with foliar K.
4 Discussion
Fig. 1 Size class frequency distribution of Calotropis procera in the different urban habitats. Different size classes are coded as follows: 1 \0.5 m, 2 0.5–1 m, 3 1–1.5 m, 4 1.5–2.5 m, 5 2.5–3.5 m, 6 [3.5 m
Table 2 Reproductive traits of Calotropis procera (Mean ± SD)
Habitats
Studies on plant population size structure provide important baseline information for monitoring and management of the species (Crisp and Lange 1976). The study of size variability is important for understanding not only the population structure, but also the process and mechanism
Residential areas
Roadsides
Fallow lands
Railways
F value
Fruit traits Length (cm) Width (cm)
12.4 ± 1.1b
11.4 ± 1.8a
12.6 ± 1.0a
12.7 ± 1.9a
14.6***
b
a
a
13.5 ± 17.0a
4.0** 3.6*
9.5 ± 0.1
9.3 ± 2.4
43.5 ± 5.6b
36.8 ± 8.7ab
37.0 ± 6.4a
44.0 ± 7.7ab
Number/fruit
439.8 ± 95.2
402.4 ± 33.0
409.8 ± 37.2
390.0 ± 28.9
Length (mm)
a
6.1 ± 1.1
6.5 ± 0.8
a
b
a
28.2***
Width (mm)
4.2 ± 1.0b
3.9 ± 0.5a
5.4 ± 0.5c
4.4 ± 0.6b
45.5***
Weight (g 10 seeds-1)
0.1 ± 0.04
0.1 ± 0.04
0.1 ± 0.02
0.1 ± 0.02
Weight (g) Seed traits
9.6 ± 0.8
7.5 ± 0.6
6.3 ± 0.5
0.7
3.3
Different letters indicate significant differences within the same row. The minimum and maximum values are italicized * p \ 0.05, ** p \ 0.01, *** p \ 0.001
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Author's personal copy Rend. Fis. Acc. Lincei Table 3 Foliar nutrient concentrations (mean ± SD, mg g-1) of Calotropis procera
Element
Total N
Habitats Residential areas
Roadsides
Fallow lands
Railways
F value
20.2 ± 4.6
13.2 ± 8.3
11.5 ± 1.0
19.8 ± 14.1
0.3
P
3.6 ± 0.4b
2.7 ± 0.2a
3.1 ± 0.3ab
2.6 ± 0.2a
K
28.4 ± 2.4a
31.9 ± 2.4ab
36.7 ± 3.2b
7.7**
36.7 ± 3.2b
Na
11.3 ± 0.6b
9.9 ± 2.4b
3.6 ± 2.4a
6.3*
Ca
35.8 ± 3.2
36.6 ± 4.3
42.3 ± 5.4
38.7 ± 2.2
1.6
Mg
10.0 ± 0.5
9.9 ± 2.0
7.8 ± 4.4
6.9 ± 1.9
1.0
6.7 ± 1.8ab
9.2**
Different letters indicates significant differences within the same row. The minimum and maximum values are italicized * p \ 0.05, ** p \ 0.01, *** p \ 0.001
Fig. 2 Ordination biplot of the first two principal components of a PCA carried out on the matrix of the four habitats and 24 soil characters
of interaction between individuals. Plant size is an important factor in competitive ability and, therefore, the structure of vegetation (Nilson et al. 1991). The height and diameter of record-size individuals are important because they reveal the maximum size attained by functionally different species groups, which are crucial to various ecological and evolutionary hypotheses (Niklas et al. 2006). The presence of significant difference between stem height, diameter, size index and plant volume of C. procera in the present study reflected the growth plasticity of this species at disturbed habitats. It was obvious that the height/diameter ratio gives general view for the growth habit of the plant architecture. This ratio was more than unity for C. procera individuals in all habitats, which means that the individual’s height exceeds, on average, its diameter and therefore the individual expands vertically rather than horizontally. Leaves of C. procera are opposite decussate (Boulos 2000), while the leaf inclination angle is 76.5 ± 1.5 (El-Midany 2014) which helps in more self-
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shading of the trees and decreases the drought stress on plants. Eid (2002) and Slima (2006) reported similar conclusions about the architecture of Ipomea carnea and Pluchea dioscorides, respectively, in disturbed and undisturbed habitats in the Nile delta, and Galal (2011) on Tamarix nilotica in Wadi El-Gimal, Red Sea. In some hyperarid regions, this ratio is less than unity for many woody species, which may be a strategy of the desert plants to provide safety for their self-regeneration, as the horizontal expansion usually provides shade that leads to decrease the severe heating effect and increase soil moisture (Shaltout and Mady 1993). The morphological traits of C. procera showed that the individuals from fallow lands had large sizes with the highest values of stem height, diameter and size index, as well as leaf length and width. High growth of individuals in fallow lands, compared to the other habitats, may presumably be due to their relatively high N content (Fig. 2), less anthropogenic disturbances (e.g., cutting, burning) and episodic water resources (personal observations). But we
Author's personal copy Rend. Fis. Acc. Lincei Table 4 Simple linear correlation coefficient (r) between soil variables and inorganic elements of Calotropis procera leaves Soil variables
Foliar elements P
K
Na
Gravels
0.23
0.29
-0.61*
Coarse sand
0.27
0.10
-0.41
Fine sand Silt
0.57 0.17
-0.17 -0.34
-0.12 0.54
Clay
-0.42
-0.04
0.35
MC
-0.55
0.61*
-0.40
pH
-0.63*
0.69*
-0.49
EC
0.64*
-0.79**
0.58*
P
-0.34
-0.23
N
0.41
0.27
-0.66*
0.77**
-0.80**
CO3
-0.21
0.45
HCO3
0.02
-0.63*
0.68*
Cl
0.66*
-0.82**
0.63*
SO4
0.57*
-0.60*
0.59*
Ca
0.73**
-0.74**
0.57
Mg
0.74**
-0.71*
0.58*
K
0.24
0.22
-0.56
Na
0.20
-0.54
0.48
* p \ 0.05, ** p \ 0.01. Only significant correlations are shown
could not exclude the age differences, besides habitat differences, as another factor affecting population growth. Since C. procera stems have no distinct annual rings, we could not estimate the age of plants in each habitat (ElMidany 2014). Conversely, plant populations in residential habitats had the lowest height, diameter, size index and number of leaves, associated with the lowest soil moisture content, EC and high Na ions. This is reflected on the soil salinity content, which suppresses plant growth. However, it has been reported that C. procera is a drought-resistant, salt-tolerant species and survives in a range of soil types. In the present study, it was observed that C. procera population in saline soils of the study area (e.g., in residential habitats) had small individual size and low density that may be due to the depressive effect of soil salinity on plant growth. This corroborates the results of many investigators which showed that this plant is salt tolerant to some extent and cannot cope with high soil salinity (Parsons and Cuthbertson 2001; Francis 2003; Orwa et al. 2009; El-Midany 2014). The presence of self-shading and high Na concentrations in the leaves of C. procera at residential habitats can be considered as an adaptation strategy to drought and salinity stresses, respectively, as suggested for this species by Ibrahim (2013) and for some xerophytic plants by (Shaltout and Mady 1993). Although soils in residential habitats had the highest content of the most analyzed nutrients, the plant
individuals had the lowest size index, volume, biomass and density. We can attribute this in particular to high anthropogenic disturbances in this habitat and scarce water supply. As mentioned above, we could not exclude the age effect on these morphological characteristics. Ross et al. (2002) found that the anthropogenic disturbance coupled with fragmentation of habitats had a stronger and immediate effect in reducing native species’ richness and increasing exotic species’ richness than did fragmentation alone. According to the habitat type, C. procera populations in residential habitats were characterized by positively skewed size distribution. It has a relatively large number of smallsized individuals, but the overall population seems to be in a declining status. The presence of bell-shaped and positively skewed distribution of C. procera populations in fallow lands and roadsides, respectively, may be a reflectance to the multi-stemmed growth habit of the plants that had many compact individuals. Consequently, this leads to the dominance of individuals in intermediate size-classes and the bell-shaped size class distribution (SCD). Some studies suggested that bell-shaped SCD may result from episodic recruitment (Venter and Witkowski 2010; Helm and Witkowski 2012), possibly during high rainfall years or after fire, when seedlings take advantage of increased light, nutrients and space. In our study area, rainfall and episodic water supply were the main reasons causing pulsed recruitment of the plant seeds. Francis (2003) reported that seedlings of C. procera often grow in large numbers after rainy periods, but only a few survive the first season. Venter and Witkowski (2010) reported mostly bell-shaped and positively skewed SCD pattern in their study on the population size structure of baobabs (Adansonia digitata L.) in South Africa. Due to the peculiar traits of the species (i.e., long-lived, low adult mortality and recruitment rates), Venter and Witkowski (2010) suggest that the deviation from an inverse J SCD may not necessarily showed an unstable or declining population. Bimodal SCD in C. procera populations in railways is suggested to display also an episodic recruitment by which the plant can persist as reported for many forest and savanna trees (Everard et al. 1995; Helm and Witkowski 2012). Nevertheless, we cannot conclude that size distribution alone is a good predictor of future population trends in the urbanized habitats, since size distribution is also affected by other demographic variables that vary enormously between species. The variations in seed traits have been presumed to be genetically, rather than environmentally controlled. However, many authors suggested that variation in seed weight depends on various environmental factors experienced by the mother plant during development and maturation such as drought (Schimpf 1977; Khaliliaqdama et al. 2013), temperature (Severino and Auld 2014) and maternal
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nutrients (Gomaa and Xavier Pico´ 2011). The presence of non-significant differences in seed weights of plant individuals may indicate that changes in edaphic factors had no effect on the amount of reserved food inside seeds. Conversely, the presence of significant variations in the other fruit and seed traits among sites may be closely related to the variation in the plant vigor and age, or other environmental factors. Leaf mineral nutrients affect the photosynthetic performance of plants and the mechanisms involving the enzyme Rubisco (e.g., Stitt et al. 1991). The concentrations of foliar nutrients in C. procera populations reflect the heterogeneity of chemical resources at each site. Foliar Na, K and P concentrations were the only significantly different nutrients between plant populations and correlated significantly with the same elements in the soil. Relatively low concentration of some macronutrients in urban habitats compared with natural habitats was reported by Maisto et al. (2013) for Quercus ilex leaves in southern Italy. We can conclude that, in addition to soil characteristics, the other environmental factors in each habitat (e.g., anthropogenic inputs and soil moisture) are responsible for limiting population growth and survival. In the present study, soil was relatively saline and this may be because of its poor drainage, allowing high evaporation rates from the soil surface (Provin and Pitt 2001). Munzbergove and Ward (2002) reported that the increase in soil salinity under certain woody plants is a common phenomenon in the arid region.
5 Conclusion To our knowledge, the data presented here are the first species-level data on C. procera in urban habitats. In the present study, C. procera populations had significant plasticity in morphological and reproductive traits with changing of soil edaphic factors in urban habitats. Under urban conditions, the plant had bell-shaped and bimodal size distribution patterns, which suggested that C. procera adopts an adult-persistence population survival strategy. In addition, it suggested that these size distributions might result from episodic recruitment, which we believe to be the predominant way of plant establishment in urban habitats. The plant individuals were characterized by small size and low density in relatively saline soil. Therefore, we conclude that salinity and water availability may act as limiting factors for C. procera distribution in urban habitats. With its high plasticity and reported allelochemical effects on other plants (Frosi et al. 2012), C. procera may dominate in the future in urban habitats under extensive degradation of the natural habitats
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of native species. The results of the present study can help in the management and monitoring of the invasive plant C. procera in urban habitats as a proactive step toward conservation of other native species. Acknowledgments We conducted this work at Helwan University, Egypt and the University funded this work directly through the laboratory facilities, provided for the authors.
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