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Conservation approach to the demography and dynamics of protected and unprotected populations of the endemic Ebenus armitagei in the Western Mediterranean Coast of Egypt
ARTICLE IN PRESS Journal for Nature Conservation 18 (2010) 151–158
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Conservation approach to the demography and dynamics of protected and unprotected populations of the endemic Ebenus armitagei in the Western Mediterranean Coast of Egypt A.K. Hegazy a,, H.F. Kabiel a, L. Boulos b, O.S. Sharashy c a
Botany Department, Faculty of Science, Cairo University, Giza 12613, Egypt Botany Department, Faculty of Science, Alexandria University, Alexandria, Egypt c Desert Research Center, Merzik, Libya b
a r t i c l e in fo
abstract
Article history: Received 27 February 2009 Accepted 4 August 2009
Ebenus armitagei Schweinf. & Taubert is a rare and endangered species inhabiting calcareous sea-shore rocky sites in the North Western Mediterranean coastal belt of Egypt. The population demography and dynamics of the only three populations remaining were compared with reference to their level of protection: (1) a protected population inside a biosphere reserve (Omayed); (2) a population inside a coastal guard station (Hekma, protected); and (3) an unprotected population (Hekma). Cuttings taken from plants at the study sites were used to test whether vegetative propagation represents a possible management tool to enhance species recovery. Life table statistics indicated that although protection may ameliorate the status of the species, the three study populations are in drastic decline, having intrinsic rates of population growth (r) of 0.075, 0.119 and 0.143 and reproductive rates (Ro) of 0.179, 0.094 and 0.047 for the Omayed (protected) and Hekma protected and unprotected sites, respectively. The fruits-seeds and the germinable-seedsjuveniles were the most critical transitions in the E. armitagei life cycle, having the highest killing power values. Furthermore, differential seed production and seed predation among the three populations may be caused by the pattern of plant phenology in the study sites. Significant losses of seeds due to insect predation (56.6-94.8%), together with a low percentage of seedling emergence (23.5-26.2%) and low reproductive value of the populations were obstacles for natural regeneration and conservation of the species even at the protected sites. Despite the low success of vegetative propagation (43-54%), the establishment of new populations and the adoption of such a regeneration strategy seem to be necessary for the recovery of the species. & 2009 Elsevier GmbH. All rights reserved.
Keywords: Conservation endangered species life table and fecundity schedule intrinsic rate of population change reproductive rate Phenology Ebenus armitagei
Introduction The Mediterranean coastal strip is the richest phytogeographical region in Egypt where nearly 1000 species are recorded in the western coastal strip out of about 2088 species of flowering plants recorded all over Egypt (Boulos 2009). Vegetation richness and species diversity is attributed to the greater amount of rainfall compared with other parts of Egypt (UNDP/GEF 1999). Many species are threatened due to human impact on natural habitats by overgrazing, overcollection and habitat destruction for mining, quarrying and land reclamation (EEAA 1997; UNDP/GEF 1999). Protection of species and biodiversity within natural reserves and protectorates is intuitively a remedy to attain recovery of endangered species and to reduce extinction risk (Deguise & Kerr
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E-mail address: [email protected] (A.K. Hegazy). 1617-1381/$ - see front matter & 2009 Elsevier GmbH. All rights reserved. doi:10.1016/j.jnc.2009.08.005
2006; Wood & Gross 2008). Scenarios for recovery, where threats to survival are removed in a manner that ensures long-term survival in nature, are mostly species-specific and single species management proved to be as important as multi-species and ecosystem management plans for valuable conservation strategies (Abbit & Scott 2001). Species extinction often follows extended periods of population decline (Lande et al. 2003). Demographic monitoring and understanding the natural history of rare plants are then crucial for population management and conservation (Adams et al. 2005; Lehtila¨ et al. 2006; Massey & Whitson 1980). Survival and reproduction patterns are a prerequisite in order to predict future growth or decline of populations and to help in the selection of appropriate management strategies for species conservation (Donovan & Welden 2001). In this case, reproduction, recruitment and survival are particularly important when attempting to interpret plant rarity (Ellis et al. 2007; Evans et al. 2003). In the present study, we used life table estimates which have proved to
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be a useful tool in the analysis of population dynamics of endangered plants and predicting their fate (Hegazy, 1997; Hegazy et al. 2008). The present work is an approach to study the population demography and dynamics of E. armitagei. Using life table and fecundity schedules, vegetative and phenological traits, we compared protected and unprotected populations.
Materials and methods Study species Ebenus armitagei Schweinf. & Taubert (Family: Leguminosae) is a small (15-25 cm tall) hairy, xerophytic perennial shrub. The leaves are stipulate and compound trifoliate, having oblanceolateoblong leaflets with obtuse to apiculate apices. The flowers are arranged in head-like spikes distinguished by the rose-pink corollas, and the one-seeded pods are included in the persistent calyx (Plate 1). The species is rare and endangered (Boulos 1999). It is endemic to Egypt (North Western Mediterranean coastal belt) and Libya (North Eastern Mediterranean coastal belt), inhabiting calcareous sea-shore rocky sites (Boulos 1997, 1999, 2009; Hegazy, 1997; Jafri & El-Gadi 1980). In Egypt, the species is confined to two known localities namely: the El Omayed biosphere reserve; and Ras El Hekma, west of Alexandria. Conservation considerations of Ebenus armitagei were previously addressed by Hegazy and Eesa (1991) and Hegazy (1997). The main obstacle for a balanced population was attributed to seed predation by insects and overgrazing by local residents’ livestock. Study sites Along the North Western Mediterranean coastal belt of Egypt only three populations of E. armitagei were found (Fig. 1). Two populations are protected: (1) the El Omayed population (Omayed) within El Omayed biosphere reserve (301 440 45.200 N, 291 090 57.200 E), having a population size of 97 individuals distributed over about 0.8 km2; and (2) the Ras El Hekma population (Hekma) within a coastguard station (311 130 51.700 N, 271 510 21.900 E), having a population size of 334 individuals distributed over about 0.5 km2. The third population is located in Hekma, outside the coastguard station (311 130 37.400 N, 271 500 41.500 E); having a population size of 87 individuals distributed over about 1 km2. Inside the coastguard station the species is completely protected from grazing which is the main cause of the overexploitation of the species. While within the El Omayed biosphere reserve, which was designated as a biosphere reserve in 1981 and extended in 1998, a sustainable nomadic land use prevails (UNDP/ GEF 1999). Ras El Hekma was identified by IUCN and the Mediterranean Action Plan as an internationally important area in 1993 (UNDP/GEF 1999). Probably the two Hekma populations studied here basically belong to the same population which was fragmented by the protection of one part of the population inside the coastguard station. The study area is characterised by a mean annual air temperature of about 20 1C with maximum and minimum temperatures of 24 1C and 15 1C respectively, and a total annual precipitation of 140-180 mm. Soil samples were obtained from a depth of 0-20 cm near the root zone of the plants so as not to cause root destruction. Soil samples were obtained from plants at least five metres apart. Three replicate soil samples were collected
Plate 1. An individual plant of Ebenus armitagei (a) and close up view of a flowering branch (b).
from each site. Soil analysis in the study sites was carried out according to Allen et al. (1974). Soil texture fractions were separated by the sieve method and the organic matter in soil samples was determined by the loss-on-ignition method. Soil reaction was determined using a glass electrode pH meter (Model ML 1010) and conductivity was measured using an electrochemical analyser (Model Consort C982). Total element concentration of micronutrients (Ca++, Na+, Mg++, K+, Fe+++) was extracted using hydrogen florid and determined using a spectrophotometer (Model Perkin Elmer A Analyst 100).
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153
Mediterranean Sea Ras El Hekma Protected population to the East Unprotected population to the West
Mediterranean Sea
Omayed Protected population
Alexandria Giza Cairo
Egypt
Aswan
0 5 10 Kilometres
Fig. 1. The study sites of Ebenus armitagei along the Western Mediterranean coast of Egypt.
Demography and life table statistics The population of E. armitagei constitute a coenopopulation including all phases of the life cycle from seed to senescing individuals. Each individual was included in the demographic study and the population was sorted into age classes. Therefore it was assumed that the year-to-year variation in the population stability averages out by dealing with different stages from seeds to senescing individuals (Begon and Mortimer 1986; Hegazy 1990). The life cycle stages of E. armitagei were categorised into flowers, fruits, seed rain, germinable seeds and juvenile and adult stages. Adults were divided into eight age classes: A1 (5-10 years) where plants start to flower at five years old age; A2 (11-15 years); A3 (16-20 years); A4 (21-25 years); A5 (26-30 years); A6 (31-35 years); A7 (36-40 years); and A8 (440 years). To estimate every cohort’s age, live and dead leaves or leaf scars were counted. Based on mean annual leaf increment and mean branch length, age was estimated. Age was confirmed by observing the stem xylem vessel groups in random branch samples (c.f. Hegazy 1992). The life table and fecundity schedule was constructed following Hegazy (1990) and Donovan and Welden (2001). The estimated statistics were: survivorship-the proportion of original cohort surviving to the start of each stage (lx), killing powerreflecting the intensity of mortality (kx ¼ log10Nxlog10Nx+1; Nx ¼ the number of individuals per stage), reproductive valuethe average seed contribution by any individual at a given age to P the population of future generations (Vx ¼ ( N t ¼ xlt/lx) bt; bt ¼ the average number of seeds per individual), net reproductive P rate (Ro ¼ lxbx; the number of individuals alive in the next generation for each individual alive in the present generation), and the intrinsic rate of population change per capita-population P growth rate (r ¼ (Ro ln Ro)/ xlxbx; x ¼ estimated age per years). When Ro ¼ 1, the population is stable (neither growing nor declining in size); Roo1, the population is declining by that proportion each generation; and Ro41, the population is increasing. When r ¼ 0, the population is stabilised; ro0, the population
is declining; and r40, the population is increasing. We calculated the stable age distribution of the population (Cx; the proportion of the population that consists of individuals of age class x when the population has stabilised i.e. reached an equilibrium growth rate) according to (Mertz 1970) by the following equation: Cx ¼ erxlx/ Pk rx lx, where parameters are calculated from life table x ¼ 0e statistics: e is the base of the natural logarithm, lx is the survivorship at age x and r is the population growth rate (Hegazy 1990). At each of the adult age classes, the difference between Cx and the actual proportion to the population was estimated. Discrepancies between monitored and projected stable age class distributions offer insights into the fit of the populations to the current protection status. Population phenology The phenological spectrum of the basic life cycle stages was monitored during January-to-December 2007. The seedling, juvenile/vegetative, flower bud, flowering, flowering/fruiting, fruiting, seed dispersal and dormancy phenophases were monitored. The duration of the sequential phenological stages was recorded for the populations. Seed and vegetative traits The weight of one hundred seeds and proportion predated by invertebrates in the three study populations were estimated. We also investigated germination traits as seed germination (with and without stratification) in Petri dishes, optimum germination temperature (a range from 15-35 1C in dark/light conditions was tested) and the seedling emergence in the plant’s natural soil. For stratification treatment wet seeds were wrapped in wet cloth and kept in the refrigerator (around zero degree centigrade) for three days. A total of 50 woody shoot cuttings, 10 cm length from every population were prepared. Leaves and buds were removed to
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Table 1 Physical and chemical characteristics (Means7SD) of the soil supporting growth of Ebenus armitagei at the study sites.
Organic matter (%) pH Conductivity (ms/cm) Ca++ (ppm) Na+ (ppm) Mg++ (ppm) K+ (ppm) Fe+++ (ppm)
Hekma (Protected)
16.5 (1.2)a 58.1 (3.1)b 25.4 (2.2)b 1.338 7.48 169.9 194.5 30.54 69.35 123.3 62.78
(0.06)b (0.06)a (8.1)a (24.7)a (5.4)a (5.8)b (11.2)b (3.5)b
allow the cutting to use its energy and stored carbohydrates for root and shoot formation. To hasten rooting, increase the number of roots, or to obtain uniform rooting, a rooting hormone (Indole Buteric Acid, IBA) containing a fungicide (Thiram) was applied to the base to prevent possible contamination of the entire supply of rooting zone. Cuttings were planted in a mixture of peat and plant natural soil (50:50). The medium was kept moistened before inserting cuttings, and placed in open greenhouse while the cuttings were rooting and forming new shoots. One way analysis of variance (ANOVA) was performed to compare the soil characteristics and the seed and vegetative traits of the species in the three sites. The degree of significance was tested by Post Hoc tests (Least Significant Difference and Duncan) using SPSS program for Windows (version 11; SPSS, Chicago, Illinois, USA).
Results Soil analysis The protected and unprotected sites at Hekma had similar soil characteristics except for a significantly greater percentage of silt and clay (10.3%) at the protected site compared to the unprotected site (5.8%, Table 1). The Omayed biosphere reserve soil was characterised by a significantly lower percentage of coarse sand (16.5%) compared with 41.2 and 38.6% at the Hekma protected and unprotected sites respectively, and greater percentage of silt and clay (25.4%) among the three study sites. The Omayed soil was also lower in organic matter, pH, conductivity and calcium and sodium concentrations but had higher magnesium, potassium and iron concentrations. The calcium and sodium concentrations reached 743.2 and 94 ppm respectively in Hekma unprotected site compared to 194.5 and 30.5 ppm respectively in Omayed. Magnesium, potassium and iron concentrations were 69.3, 123.3 and 62.8 at Omayed compared with 49.7, 42 and 11.6 at the unprotected Hekma site. Adult population demography An irregular adult age distribution was noticed in the Hekma unprotected E. armitagei population (Fig. 2a). The third and fourth age classes from 16 to 25 years dominated the adult population with contributions of 35.6 and 34.2% respectively. The reproductive value (Vx) of these classes (69.62 and 43.28 respectively) was comparatively lower than that of the A1 and A2 classes (376 and 613.33 respectively) which contributed only 6.8 and 4.1% respectively to the adult population (Fig. 2b).
Hekma (non-Protected)
41.2 (2.2)b 48.5 (3.6)a 10.3 (3.1)b 0.827 7.51 202.1 655.3 86.3 41.6 33.6 10.03
38.6 (3.7)b 55.6 (4.1)ab 5.80 (2.2)a
(0.13)a (0.61)b (15.8)b (73.2)b (8.5)b (5.2)a (8.1)a (1.8)a
0.615 7.52 225.0 743.2 94.14 49.7 42.00 11.62
40%
(0.22)a (0.14)b (12.66)b (55.3)b (11.9)b (11.3)a (3.6)a (2.2)a
Omayed (p) Hekma (p) Hekma (np)
35% 30% % Contribution
Soil texture (%) Coarse sand Fine sand Silt and Clay
Omayed (Protected)
25% 20% 15% 10% 5% 0%
Reproductive value (Vx)
Parameter
A1
A2
A3
A4
A5
A6
A7
A8
A1
A2
A3
A4
A5
A6
A7
A8
1000 900 800 700 600 500 400 300 200 100 0 Adult age classes
Fig. 2. (a) Population structure and (b) reproductive value (Vx) of Ebenus armitagei adult life cycle stages at different sites. Adult age classes: A1 ¼ 5-10 years; A2 ¼ 11-15 years; A3 ¼ 16-20 years; A4 ¼ 21-25 years; A5 ¼ 26-30 years; A6 ¼ 31-35 years; A7 ¼ 36-40 years; and A8 ¼ 441 years. p ¼ protected and np ¼ unprotected populations.
The Hekma protected population showed decreasing distribution in adult individuals from the A1 class (30.3%) to the A8 class (2.6%). The A1 to A5 adults’ classes aging from 5 to 30 years attained the highest Vx, ranging from 328.6 in the A5 class to 470.6 in the A2 class. Almost the same trend was observed in the Omayed protected population with a maximum Vx estimated in A3, A4 and A5 classes and ranging from 736.6 to 918.6. It was noteworthy that the A8 adult (440 years) was only observed in the protected populations. The protected populations appeared to be closer to stability than the unprotected population, especially for Omayed where the difference between the stable age distribution (Cx) and the actual age distribution of adults ranged from 0.01 to 0.09% compared to Hekma (0.02-0.39%, Fig. 3). The difference increased as adult
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The E. armitagei population at Omayed exhibited higher survivorship (lx) values than those at the Hekma protected population at most life cycle stages (Fig. 4a). On the other hand, the unprotected population showed lower lx values than the two protected populations, commencing from flowering until the first adult stage, where lx attained 0.00013 compared to 0.00030 and 0.00025 at Omayed and Hekma respectively. A sudden increase in values was also observed at the third adult stage compared with the protected populations. This was followed by a decline in lx values in the subsequent adult stages. Compared with other life cycle transitions of E. armitagei, the fruits-to-seeds and the germinable seeds-to-juveniles were the most critical, having the highest killing power (kx) values (Fig. 4b). In the fruits-to-seeds transition, the highest kx value occurred in the unprotected Hekma population (1.20), whereas for the germinable seeds-to-juveniles transition, the highest kx value was attained in the Omayed population (2.06). Alternation of higher and lower values of kx was observed in the protected populations in all transitions. In the Hekma non-protected population, kx decreased to 0.94 in the second-to-third adult transition, but then increased to surpass the corresponding values in the protected populations in the fourth-fifth, fifth-sixth and sixth-to-seventh adult transitions. The net reproductive rate (Ro) and population growth rate (r) statistics indicated that the three populations were declining (Fig. 5). The Hekma unprotected population was the most vulnerable, having the lowest Ro (0.047) and r (0.143). The protected populations exhibited higher values, with a maximum Ro (0.179) and r (0.075) at Omayed as compared to 0.094 and 0.119 respectively in the protected Hekma population.
1
Omayed (p) Hekma (p) Hekma (np)
0.1 Survivorship (lx)
Life cycle traits
(Table 2). Seed predation here was 94.8% compared to 61.5 and 56.6% at the Omayed and protected Hekma sites, respectively. The optimum germination temperature of seeds from the three populations ranged from 22.7 to 23.8 1C. Stratification was found to increase seed germination; however differences between seeds from the three populations were not significant. A similar trend was observed for seedling emergence, which ranged from 23.5 to 26.2%. Greater cutting success was attained from material taken from Omayed and the Hekma unprotected sites, which reached 54.2% compared to 43.1% for material from the protected Hekma population.
0.01 0.001 0.0001 0.00001 Fl. Fr. Se.Ger.Juv. A1 A2 A3 A4 A5 A6 A7 A8 2.5 2.0 1.5
Killing power (kx)
individuals became older. In the unprotected Hekma population, this difference was the highest and ranged from 0.37 to 0.77%, in all age stages except the A1 and the A2 classes aging from 5 to 15 years.
155
1.0 0.5 0.0 -0.5 -1.0 -1.5 Fl. Fr. Se.Ger. Juv. A1 A2 A3 A4 A5 A6 A7 A8
Seed and vegetative traits
Life cycle stages
While seeds from Omayed attained a significantly higher mass (0.38 g/100 seeds) than those from the two Hekma sites (protected, 0.34 g/100 seeds; unprotected, 0.33 g/100 seeds), predation by insects was greater at the unprotected site
0.9%
Omayed (p) Hekma (p) Hekma (np)
0.8% 0.7% Difference (%)
Fig. 4. (a) Survivorship (lx, log scale) and (b) killing power (kx) of Ebenus armitagei at different sites. Fl. ¼ flowers, Fr. ¼ fruits, Se. ¼ Seed rain, Ger. ¼ germinable seeds, Juv. ¼ juveniles (o5 years), adult age classes: A1 ¼ 5-10 years; A2 ¼ 11-15 years; A3 ¼ 16-20 years; A4 ¼ 21-25 years; A5 ¼ 26-30 years; A6 ¼ 31-35 years; A7 ¼ 36-40 years; and A8 ¼ 441 years. p ¼ protected and np ¼ unprotected populations.
r
Ro
Omayed (p)
0.6% 0.5% 0.4%
Hekma (p)
0.3% 0.2% 0.1% 0.0%
Hekma (np) A1
A2
A3
A4
A5
A6
A7
A8
Adult age classes Fig. 3. Difference between the stable age distribution (Cx, %) and the actual age distribution (%) to the population of Ebenus armitagei adult life cycle stages at different sites. Adult age classes: A1 ¼ 5-10 years; A2 ¼ 11-15 years; A3 ¼ 16-20 years; A4 ¼ 21-25 years; A5 ¼ 26-30 years; A6 ¼ 31-35 years; A7 ¼ 36-40 years; and A8 ¼ 441 years. p ¼ protected and np ¼ unprotected populations.
-0.2
-0.1
0
0.1
0.2
Value Fig. 5. Reproductive rate (Ro) and intrinsic rate of population increase per capita (r) of Ebenus armitagei at different sites. p ¼ protected populations and np ¼ unprotected populations.
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Table 2 Seed and germination traits and vegetative cutting success of Ebenus armitagei. Parameter
Omayed (Protected)
Seed and germination traits Seed weight (100 seed, g) Seed predation (%) Optimum germination temperature (1C) Seed germination (with stratification, %) Seed germination (without stratification, %) Seedling emergence (%)
0.38 61.5 23.5 44.1 16.7 26.2
Cutting success (%)
54.2 (3.5)b
Hekma (Protected)
(0.005)b (7.2)a (2.6) (3.6) (2.9) (2.5)
0.34 56.6 22.7 49.3 18.3 23.1
Hekma (non-Protected)
(0.006)a (3.4)a (3.5) (9.7) (4.6) (4.7)
0.33 94.8 23.8 39.2 14.8 24.7
43.1 (2.8)a
(0.012)a (4.2)b (2.1) (2.4) (3.5) (2.8)
53.9 (2.2)b
Means and standard deviations (SD, in brackets) are shown. Different letter indicates significant differences within the same row; otherwise, the differences are not significant.
Phenophase
Seedling
Juvenile/Vegetative Flower bud Flowering
Flowering/Fruiting Fruiting Seed dispersal Dormancy J
F
M
A
M
J
J
A
S O N D
Month Fig. 6. Phenophases of the Omayed (’), Hekma protected (
Population phenology traits The phenological behaviour of E. armitagei varied among the three study sites (Fig. 6). The Omayed population was characterised by an earlier phenological pattern than Hekma populations. In the former, the seedling phenophase began in early February and ended in early March, while in the protected and unprotected populations at Hekma this phase extended from the second or third week of February to the end of February, respectively. The unprotected Hekma population exhibited both late phenology and a shorter duration of phenophases, especially in flowering and fruiting. The flower bud, flowering and flowering/ fruiting phenophases started two weeks later in the unprotected Hekma than at Omayed, and one week later than the protected Hekma population. Furthermore, the fruiting phenophase lasted for three weeks (from the first to the third week of May) in the non-protected population as compared to six weeks (end of April to early June) and eleven weeks (mid April to early June) in the Hekma and Omayed protected populations respectively.
Discussion The natural habitat of E. armitagei is threatened by two major factors; habitat destruction and overgrazing. The rocky ridges inhabited by the species have been extensively quarried for construction materials which caused complete destruction of this habitat, in addition to the spread of resorts along the Mediterranean coast (UNDP/GEF 1999). Moreover, the pressure of livestock on E. armitagei and other rangeland species is increasing as a result of the increase in Bedouin populations. In the present study, protection from overgrazing is emphasised at Omayed and Hekma compared to the Hekma unprotected site which is subjected to uncontrolled grazing practice. Survivorship, reproductive value and growth rate of the E. armitagei populations were better at
) and Hekma unprotected (
) populations.
protected sites, especially at Omayed within El Omayed Biosphere Reserve. Additionally, a more balanced adult population structure was attained with fewer differences with the stable stage distribution. The phenological pattern of the species also exhibited earlier and more prolonged phenophases at the protected sites. However, the differences between the two protected populations in species demography may be due to variation in the level of protection: complete prohibition of grazing at Hekma and sustainable grazing management at Omayed, or to the variation in local edaphic and/or environmental factors. The unprotected E. armitagei population showed an irregular adult age class distribution. This feature may be considered a direct result of overgrazing stress causing alteration in the reproductive phenology of the species (Hegazy, 1997; Young et al. 2007). Both the intrinsic rate of population growth and the reproductive rate are considered a measure for fitness (Boersma et al. 1999). Despite the apparent merits of protection in the present study, demographic monitoring indicated drastic declines in the three populations; all showed negative growth rates and reproductive rates of o1. Shedding light on the failure of the species for self regeneration even under protection from grazing and/or habitat destruction and the need for other conservation measures, possibly due to frequent drought and seed predation which limit the species regeneration. The fruits-to-seeds and the germinable seeds-to-juveniles were the most critical transitions in the E. armitagei life cycle, having the highest killing power values, resulting in low seeding emergence. Cavers (1983) suggested that the fate of a plant population may be decided by the pattern of mortality acting upon seed behaviour. For example, the predatory beetle Callosobruchus maculotus (Coleoptera; Bruchidae), which consumes seeds of some wild and cultivated legumes, is responsible for significant seed losses (56.6-94.8%) prior to dispersal of E. armitagei (Hegazy & Eesa, 1991). Predispersal seed predation is key factor that could
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limit reproductive success via decreased viable seed production causing lower population growth rate in rare species ¨ (Munzebergav a 2005; Young et al. 2007). Later phenophases in the unprotected Hekma population compared with the protected ones revealed the presence of an intraspecific phenological plasticity of E. armitagei. The smaller seeds and lower germination in the unprotected population may be related to late flowering phenology (Galen & Stanton 1991). Additionally, the comparatively short period of flowering and fruiting in the unprotected Hekma population resulted in lower reproductive values than at the protected sites. These variations in phenological behaviour of the species emphasises that plant phenology is one of the most sensitive functional traits in relation to environmental changes and disturbances (Garnier et al. 2007; Miller-Rushing & Primack 2008; Post et al. 2008). Fleischner (1994) reported that overgrazing may delay phenology, and according to the species, overexploitation and/or overgrazing may have damaging effects on plants when occurring at specific phenophases (Hendrickson et al. 2005; Olson & Richards 1988). In the unprotected population which is subjected to overgrazing, the relatively shorter fruiting and seed dispersal phenophases, together with the earlier intrusion into dormancy may be possible explanations for the greater susceptibility of seeds to insect predation. Klips et al. (2005) reported that the levels of seed predation can vary a great deal from year-toyear and site-to-site and it is affected by the timing of seed availability. Failure of normal recruitment of E. armitagei in its natural habitat is mainly attributed to the loss of seeds due to insect predation and grazing of reproductive organs associated with the low rate of emergence and survival of seedling. Protection is not always the solution to the conservation of endangered species (e.g. Gurd et al. 2001; Xu & Melick 2007; Zimmerman & Reichard 2005). On the other hand, Hegazy et al. (2008) and Linkie et al. (2008) found that protection from overgrazing and overcollection has an important role for species conservation in cases where threats resulted as a direct response to human impact. In case of E. armitagei the presence of species-specific constraints, including predispersal seed predation and low reproductive values, reduced the effectiveness of protection and resulted in a continuous decline of the populations. Introduction of new individuals by transplantation may be a useful tool. In other cases, transplantation of species has proved to be an effective tool in accelerating local restoration (Cole & Spildie 2006). In the present study, the relative success (43-54%) of vegetative propagation suggests that raising transplants from cuttings could be used to accelerate the recovery of the E. armitagei populations to overcome the problem of seed predation and the low rate of seedling emergence and survival. Regeneration of the species in its natural habitat by use of transplants obtained from seeds faces limitations where up to 95% of seeds are subject to insect predation before maturity stage where collection of enough seeds will not fulfill large scale regeneration from seed. Moreover, the damage caused by the insect Callosobruchus maculotus is not only associated with loss of seeds, other risks such as injury of the embryo and cotyledons are expected which prevent and/or abort germination of the infested seeds (Hegazy & Eesa, 1991).
Conservation considerations As the protected Omayed population, where grazing is managed, is more stable than the protected Hekma population with complete use restriction, then the species responds better to the rational use than to the prevention of grazing.
157
The recovery of E. armitagei populations needs the investment of other regeneration strategies in addition to protection, especially when regeneration from seeds is limited due to intrinsic (low emergence and survival of seedlings) and extrinsic (predation) causes. Conserving species in their natural settings, their own habitat, is key to ensuring their long-term survival. The success of vegetative propagation in E. armitagei suggests one possibility for restoring these populations. Raising new transplants from cuttings and/or seeds to restore the declining natural populations may be essential to maintain them. The cultivation of E. armitagei as an ornamental plant with its lovely pink flowers within the seaside resorts should be encouraged as a partial rehabilitation method for the natural habitat of the species. As the phenological behaviour of the species is influenced by the level of protection, probably the phenological spectrum of the species varies from year to year in the Mediterranean environment characterised by climatic variability. The present work was based on a one year study, more prolonged and detailed monitoring is needed in order to provide a more precise range of time for each phenophase. Systematic census of the species is also recommended in order to monitor the response to the proposed conservation measures in Omayed and Hekma.
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Conservation approach to the demography and dynamics of protected and unprotected populations of the endemic Ebenus armitagei in the Western Mediterranean Coast of Egypt A.K. Hegazy a,, H.F. Kabiel a, L. Boulos b, O.S. Sharashy c a
Botany Department, Faculty of Science, Cairo University, Giza 12613, Egypt Botany Department, Faculty of Science, Alexandria University, Alexandria, Egypt c Desert Research Center, Merzik, Libya b
a r t i c l e in fo
abstract
Article history: Received 27 February 2009 Accepted 4 August 2009
Ebenus armitagei Schweinf. & Taubert is a rare and endangered species inhabiting calcareous sea-shore rocky sites in the North Western Mediterranean coastal belt of Egypt. The population demography and dynamics of the only three populations remaining were compared with reference to their level of protection: (1) a protected population inside a biosphere reserve (Omayed); (2) a population inside a coastal guard station (Hekma, protected); and (3) an unprotected population (Hekma). Cuttings taken from plants at the study sites were used to test whether vegetative propagation represents a possible management tool to enhance species recovery. Life table statistics indicated that although protection may ameliorate the status of the species, the three study populations are in drastic decline, having intrinsic rates of population growth (r) of 0.075, 0.119 and 0.143 and reproductive rates (Ro) of 0.179, 0.094 and 0.047 for the Omayed (protected) and Hekma protected and unprotected sites, respectively. The fruits-seeds and the germinable-seedsjuveniles were the most critical transitions in the E. armitagei life cycle, having the highest killing power values. Furthermore, differential seed production and seed predation among the three populations may be caused by the pattern of plant phenology in the study sites. Significant losses of seeds due to insect predation (56.6-94.8%), together with a low percentage of seedling emergence (23.5-26.2%) and low reproductive value of the populations were obstacles for natural regeneration and conservation of the species even at the protected sites. Despite the low success of vegetative propagation (43-54%), the establishment of new populations and the adoption of such a regeneration strategy seem to be necessary for the recovery of the species. & 2009 Elsevier GmbH. All rights reserved.
Keywords: Conservation endangered species life table and fecundity schedule intrinsic rate of population change reproductive rate Phenology Ebenus armitagei
Introduction The Mediterranean coastal strip is the richest phytogeographical region in Egypt where nearly 1000 species are recorded in the western coastal strip out of about 2088 species of flowering plants recorded all over Egypt (Boulos 2009). Vegetation richness and species diversity is attributed to the greater amount of rainfall compared with other parts of Egypt (UNDP/GEF 1999). Many species are threatened due to human impact on natural habitats by overgrazing, overcollection and habitat destruction for mining, quarrying and land reclamation (EEAA 1997; UNDP/GEF 1999). Protection of species and biodiversity within natural reserves and protectorates is intuitively a remedy to attain recovery of endangered species and to reduce extinction risk (Deguise & Kerr
Corresponding author. Tel.:+202 3567 6651; fax: +202 35727 556.
E-mail address: [email protected] (A.K. Hegazy). 1617-1381/$ - see front matter & 2009 Elsevier GmbH. All rights reserved. doi:10.1016/j.jnc.2009.08.005
2006; Wood & Gross 2008). Scenarios for recovery, where threats to survival are removed in a manner that ensures long-term survival in nature, are mostly species-specific and single species management proved to be as important as multi-species and ecosystem management plans for valuable conservation strategies (Abbit & Scott 2001). Species extinction often follows extended periods of population decline (Lande et al. 2003). Demographic monitoring and understanding the natural history of rare plants are then crucial for population management and conservation (Adams et al. 2005; Lehtila¨ et al. 2006; Massey & Whitson 1980). Survival and reproduction patterns are a prerequisite in order to predict future growth or decline of populations and to help in the selection of appropriate management strategies for species conservation (Donovan & Welden 2001). In this case, reproduction, recruitment and survival are particularly important when attempting to interpret plant rarity (Ellis et al. 2007; Evans et al. 2003). In the present study, we used life table estimates which have proved to
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be a useful tool in the analysis of population dynamics of endangered plants and predicting their fate (Hegazy, 1997; Hegazy et al. 2008). The present work is an approach to study the population demography and dynamics of E. armitagei. Using life table and fecundity schedules, vegetative and phenological traits, we compared protected and unprotected populations.
Materials and methods Study species Ebenus armitagei Schweinf. & Taubert (Family: Leguminosae) is a small (15-25 cm tall) hairy, xerophytic perennial shrub. The leaves are stipulate and compound trifoliate, having oblanceolateoblong leaflets with obtuse to apiculate apices. The flowers are arranged in head-like spikes distinguished by the rose-pink corollas, and the one-seeded pods are included in the persistent calyx (Plate 1). The species is rare and endangered (Boulos 1999). It is endemic to Egypt (North Western Mediterranean coastal belt) and Libya (North Eastern Mediterranean coastal belt), inhabiting calcareous sea-shore rocky sites (Boulos 1997, 1999, 2009; Hegazy, 1997; Jafri & El-Gadi 1980). In Egypt, the species is confined to two known localities namely: the El Omayed biosphere reserve; and Ras El Hekma, west of Alexandria. Conservation considerations of Ebenus armitagei were previously addressed by Hegazy and Eesa (1991) and Hegazy (1997). The main obstacle for a balanced population was attributed to seed predation by insects and overgrazing by local residents’ livestock. Study sites Along the North Western Mediterranean coastal belt of Egypt only three populations of E. armitagei were found (Fig. 1). Two populations are protected: (1) the El Omayed population (Omayed) within El Omayed biosphere reserve (301 440 45.200 N, 291 090 57.200 E), having a population size of 97 individuals distributed over about 0.8 km2; and (2) the Ras El Hekma population (Hekma) within a coastguard station (311 130 51.700 N, 271 510 21.900 E), having a population size of 334 individuals distributed over about 0.5 km2. The third population is located in Hekma, outside the coastguard station (311 130 37.400 N, 271 500 41.500 E); having a population size of 87 individuals distributed over about 1 km2. Inside the coastguard station the species is completely protected from grazing which is the main cause of the overexploitation of the species. While within the El Omayed biosphere reserve, which was designated as a biosphere reserve in 1981 and extended in 1998, a sustainable nomadic land use prevails (UNDP/ GEF 1999). Ras El Hekma was identified by IUCN and the Mediterranean Action Plan as an internationally important area in 1993 (UNDP/GEF 1999). Probably the two Hekma populations studied here basically belong to the same population which was fragmented by the protection of one part of the population inside the coastguard station. The study area is characterised by a mean annual air temperature of about 20 1C with maximum and minimum temperatures of 24 1C and 15 1C respectively, and a total annual precipitation of 140-180 mm. Soil samples were obtained from a depth of 0-20 cm near the root zone of the plants so as not to cause root destruction. Soil samples were obtained from plants at least five metres apart. Three replicate soil samples were collected
Plate 1. An individual plant of Ebenus armitagei (a) and close up view of a flowering branch (b).
from each site. Soil analysis in the study sites was carried out according to Allen et al. (1974). Soil texture fractions were separated by the sieve method and the organic matter in soil samples was determined by the loss-on-ignition method. Soil reaction was determined using a glass electrode pH meter (Model ML 1010) and conductivity was measured using an electrochemical analyser (Model Consort C982). Total element concentration of micronutrients (Ca++, Na+, Mg++, K+, Fe+++) was extracted using hydrogen florid and determined using a spectrophotometer (Model Perkin Elmer A Analyst 100).
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153
Mediterranean Sea Ras El Hekma Protected population to the East Unprotected population to the West
Mediterranean Sea
Omayed Protected population
Alexandria Giza Cairo
Egypt
Aswan
0 5 10 Kilometres
Fig. 1. The study sites of Ebenus armitagei along the Western Mediterranean coast of Egypt.
Demography and life table statistics The population of E. armitagei constitute a coenopopulation including all phases of the life cycle from seed to senescing individuals. Each individual was included in the demographic study and the population was sorted into age classes. Therefore it was assumed that the year-to-year variation in the population stability averages out by dealing with different stages from seeds to senescing individuals (Begon and Mortimer 1986; Hegazy 1990). The life cycle stages of E. armitagei were categorised into flowers, fruits, seed rain, germinable seeds and juvenile and adult stages. Adults were divided into eight age classes: A1 (5-10 years) where plants start to flower at five years old age; A2 (11-15 years); A3 (16-20 years); A4 (21-25 years); A5 (26-30 years); A6 (31-35 years); A7 (36-40 years); and A8 (440 years). To estimate every cohort’s age, live and dead leaves or leaf scars were counted. Based on mean annual leaf increment and mean branch length, age was estimated. Age was confirmed by observing the stem xylem vessel groups in random branch samples (c.f. Hegazy 1992). The life table and fecundity schedule was constructed following Hegazy (1990) and Donovan and Welden (2001). The estimated statistics were: survivorship-the proportion of original cohort surviving to the start of each stage (lx), killing powerreflecting the intensity of mortality (kx ¼ log10Nxlog10Nx+1; Nx ¼ the number of individuals per stage), reproductive valuethe average seed contribution by any individual at a given age to P the population of future generations (Vx ¼ ( N t ¼ xlt/lx) bt; bt ¼ the average number of seeds per individual), net reproductive P rate (Ro ¼ lxbx; the number of individuals alive in the next generation for each individual alive in the present generation), and the intrinsic rate of population change per capita-population P growth rate (r ¼ (Ro ln Ro)/ xlxbx; x ¼ estimated age per years). When Ro ¼ 1, the population is stable (neither growing nor declining in size); Roo1, the population is declining by that proportion each generation; and Ro41, the population is increasing. When r ¼ 0, the population is stabilised; ro0, the population
is declining; and r40, the population is increasing. We calculated the stable age distribution of the population (Cx; the proportion of the population that consists of individuals of age class x when the population has stabilised i.e. reached an equilibrium growth rate) according to (Mertz 1970) by the following equation: Cx ¼ erxlx/ Pk rx lx, where parameters are calculated from life table x ¼ 0e statistics: e is the base of the natural logarithm, lx is the survivorship at age x and r is the population growth rate (Hegazy 1990). At each of the adult age classes, the difference between Cx and the actual proportion to the population was estimated. Discrepancies between monitored and projected stable age class distributions offer insights into the fit of the populations to the current protection status. Population phenology The phenological spectrum of the basic life cycle stages was monitored during January-to-December 2007. The seedling, juvenile/vegetative, flower bud, flowering, flowering/fruiting, fruiting, seed dispersal and dormancy phenophases were monitored. The duration of the sequential phenological stages was recorded for the populations. Seed and vegetative traits The weight of one hundred seeds and proportion predated by invertebrates in the three study populations were estimated. We also investigated germination traits as seed germination (with and without stratification) in Petri dishes, optimum germination temperature (a range from 15-35 1C in dark/light conditions was tested) and the seedling emergence in the plant’s natural soil. For stratification treatment wet seeds were wrapped in wet cloth and kept in the refrigerator (around zero degree centigrade) for three days. A total of 50 woody shoot cuttings, 10 cm length from every population were prepared. Leaves and buds were removed to
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Table 1 Physical and chemical characteristics (Means7SD) of the soil supporting growth of Ebenus armitagei at the study sites.
Organic matter (%) pH Conductivity (ms/cm) Ca++ (ppm) Na+ (ppm) Mg++ (ppm) K+ (ppm) Fe+++ (ppm)
Hekma (Protected)
16.5 (1.2)a 58.1 (3.1)b 25.4 (2.2)b 1.338 7.48 169.9 194.5 30.54 69.35 123.3 62.78
(0.06)b (0.06)a (8.1)a (24.7)a (5.4)a (5.8)b (11.2)b (3.5)b
allow the cutting to use its energy and stored carbohydrates for root and shoot formation. To hasten rooting, increase the number of roots, or to obtain uniform rooting, a rooting hormone (Indole Buteric Acid, IBA) containing a fungicide (Thiram) was applied to the base to prevent possible contamination of the entire supply of rooting zone. Cuttings were planted in a mixture of peat and plant natural soil (50:50). The medium was kept moistened before inserting cuttings, and placed in open greenhouse while the cuttings were rooting and forming new shoots. One way analysis of variance (ANOVA) was performed to compare the soil characteristics and the seed and vegetative traits of the species in the three sites. The degree of significance was tested by Post Hoc tests (Least Significant Difference and Duncan) using SPSS program for Windows (version 11; SPSS, Chicago, Illinois, USA).
Results Soil analysis The protected and unprotected sites at Hekma had similar soil characteristics except for a significantly greater percentage of silt and clay (10.3%) at the protected site compared to the unprotected site (5.8%, Table 1). The Omayed biosphere reserve soil was characterised by a significantly lower percentage of coarse sand (16.5%) compared with 41.2 and 38.6% at the Hekma protected and unprotected sites respectively, and greater percentage of silt and clay (25.4%) among the three study sites. The Omayed soil was also lower in organic matter, pH, conductivity and calcium and sodium concentrations but had higher magnesium, potassium and iron concentrations. The calcium and sodium concentrations reached 743.2 and 94 ppm respectively in Hekma unprotected site compared to 194.5 and 30.5 ppm respectively in Omayed. Magnesium, potassium and iron concentrations were 69.3, 123.3 and 62.8 at Omayed compared with 49.7, 42 and 11.6 at the unprotected Hekma site. Adult population demography An irregular adult age distribution was noticed in the Hekma unprotected E. armitagei population (Fig. 2a). The third and fourth age classes from 16 to 25 years dominated the adult population with contributions of 35.6 and 34.2% respectively. The reproductive value (Vx) of these classes (69.62 and 43.28 respectively) was comparatively lower than that of the A1 and A2 classes (376 and 613.33 respectively) which contributed only 6.8 and 4.1% respectively to the adult population (Fig. 2b).
Hekma (non-Protected)
41.2 (2.2)b 48.5 (3.6)a 10.3 (3.1)b 0.827 7.51 202.1 655.3 86.3 41.6 33.6 10.03
38.6 (3.7)b 55.6 (4.1)ab 5.80 (2.2)a
(0.13)a (0.61)b (15.8)b (73.2)b (8.5)b (5.2)a (8.1)a (1.8)a
0.615 7.52 225.0 743.2 94.14 49.7 42.00 11.62
40%
(0.22)a (0.14)b (12.66)b (55.3)b (11.9)b (11.3)a (3.6)a (2.2)a
Omayed (p) Hekma (p) Hekma (np)
35% 30% % Contribution
Soil texture (%) Coarse sand Fine sand Silt and Clay
Omayed (Protected)
25% 20% 15% 10% 5% 0%
Reproductive value (Vx)
Parameter
A1
A2
A3
A4
A5
A6
A7
A8
A1
A2
A3
A4
A5
A6
A7
A8
1000 900 800 700 600 500 400 300 200 100 0 Adult age classes
Fig. 2. (a) Population structure and (b) reproductive value (Vx) of Ebenus armitagei adult life cycle stages at different sites. Adult age classes: A1 ¼ 5-10 years; A2 ¼ 11-15 years; A3 ¼ 16-20 years; A4 ¼ 21-25 years; A5 ¼ 26-30 years; A6 ¼ 31-35 years; A7 ¼ 36-40 years; and A8 ¼ 441 years. p ¼ protected and np ¼ unprotected populations.
The Hekma protected population showed decreasing distribution in adult individuals from the A1 class (30.3%) to the A8 class (2.6%). The A1 to A5 adults’ classes aging from 5 to 30 years attained the highest Vx, ranging from 328.6 in the A5 class to 470.6 in the A2 class. Almost the same trend was observed in the Omayed protected population with a maximum Vx estimated in A3, A4 and A5 classes and ranging from 736.6 to 918.6. It was noteworthy that the A8 adult (440 years) was only observed in the protected populations. The protected populations appeared to be closer to stability than the unprotected population, especially for Omayed where the difference between the stable age distribution (Cx) and the actual age distribution of adults ranged from 0.01 to 0.09% compared to Hekma (0.02-0.39%, Fig. 3). The difference increased as adult
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The E. armitagei population at Omayed exhibited higher survivorship (lx) values than those at the Hekma protected population at most life cycle stages (Fig. 4a). On the other hand, the unprotected population showed lower lx values than the two protected populations, commencing from flowering until the first adult stage, where lx attained 0.00013 compared to 0.00030 and 0.00025 at Omayed and Hekma respectively. A sudden increase in values was also observed at the third adult stage compared with the protected populations. This was followed by a decline in lx values in the subsequent adult stages. Compared with other life cycle transitions of E. armitagei, the fruits-to-seeds and the germinable seeds-to-juveniles were the most critical, having the highest killing power (kx) values (Fig. 4b). In the fruits-to-seeds transition, the highest kx value occurred in the unprotected Hekma population (1.20), whereas for the germinable seeds-to-juveniles transition, the highest kx value was attained in the Omayed population (2.06). Alternation of higher and lower values of kx was observed in the protected populations in all transitions. In the Hekma non-protected population, kx decreased to 0.94 in the second-to-third adult transition, but then increased to surpass the corresponding values in the protected populations in the fourth-fifth, fifth-sixth and sixth-to-seventh adult transitions. The net reproductive rate (Ro) and population growth rate (r) statistics indicated that the three populations were declining (Fig. 5). The Hekma unprotected population was the most vulnerable, having the lowest Ro (0.047) and r (0.143). The protected populations exhibited higher values, with a maximum Ro (0.179) and r (0.075) at Omayed as compared to 0.094 and 0.119 respectively in the protected Hekma population.
1
Omayed (p) Hekma (p) Hekma (np)
0.1 Survivorship (lx)
Life cycle traits
(Table 2). Seed predation here was 94.8% compared to 61.5 and 56.6% at the Omayed and protected Hekma sites, respectively. The optimum germination temperature of seeds from the three populations ranged from 22.7 to 23.8 1C. Stratification was found to increase seed germination; however differences between seeds from the three populations were not significant. A similar trend was observed for seedling emergence, which ranged from 23.5 to 26.2%. Greater cutting success was attained from material taken from Omayed and the Hekma unprotected sites, which reached 54.2% compared to 43.1% for material from the protected Hekma population.
0.01 0.001 0.0001 0.00001 Fl. Fr. Se.Ger.Juv. A1 A2 A3 A4 A5 A6 A7 A8 2.5 2.0 1.5
Killing power (kx)
individuals became older. In the unprotected Hekma population, this difference was the highest and ranged from 0.37 to 0.77%, in all age stages except the A1 and the A2 classes aging from 5 to 15 years.
155
1.0 0.5 0.0 -0.5 -1.0 -1.5 Fl. Fr. Se.Ger. Juv. A1 A2 A3 A4 A5 A6 A7 A8
Seed and vegetative traits
Life cycle stages
While seeds from Omayed attained a significantly higher mass (0.38 g/100 seeds) than those from the two Hekma sites (protected, 0.34 g/100 seeds; unprotected, 0.33 g/100 seeds), predation by insects was greater at the unprotected site
0.9%
Omayed (p) Hekma (p) Hekma (np)
0.8% 0.7% Difference (%)
Fig. 4. (a) Survivorship (lx, log scale) and (b) killing power (kx) of Ebenus armitagei at different sites. Fl. ¼ flowers, Fr. ¼ fruits, Se. ¼ Seed rain, Ger. ¼ germinable seeds, Juv. ¼ juveniles (o5 years), adult age classes: A1 ¼ 5-10 years; A2 ¼ 11-15 years; A3 ¼ 16-20 years; A4 ¼ 21-25 years; A5 ¼ 26-30 years; A6 ¼ 31-35 years; A7 ¼ 36-40 years; and A8 ¼ 441 years. p ¼ protected and np ¼ unprotected populations.
r
Ro
Omayed (p)
0.6% 0.5% 0.4%
Hekma (p)
0.3% 0.2% 0.1% 0.0%
Hekma (np) A1
A2
A3
A4
A5
A6
A7
A8
Adult age classes Fig. 3. Difference between the stable age distribution (Cx, %) and the actual age distribution (%) to the population of Ebenus armitagei adult life cycle stages at different sites. Adult age classes: A1 ¼ 5-10 years; A2 ¼ 11-15 years; A3 ¼ 16-20 years; A4 ¼ 21-25 years; A5 ¼ 26-30 years; A6 ¼ 31-35 years; A7 ¼ 36-40 years; and A8 ¼ 441 years. p ¼ protected and np ¼ unprotected populations.
-0.2
-0.1
0
0.1
0.2
Value Fig. 5. Reproductive rate (Ro) and intrinsic rate of population increase per capita (r) of Ebenus armitagei at different sites. p ¼ protected populations and np ¼ unprotected populations.
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Table 2 Seed and germination traits and vegetative cutting success of Ebenus armitagei. Parameter
Omayed (Protected)
Seed and germination traits Seed weight (100 seed, g) Seed predation (%) Optimum germination temperature (1C) Seed germination (with stratification, %) Seed germination (without stratification, %) Seedling emergence (%)
0.38 61.5 23.5 44.1 16.7 26.2
Cutting success (%)
54.2 (3.5)b
Hekma (Protected)
(0.005)b (7.2)a (2.6) (3.6) (2.9) (2.5)
0.34 56.6 22.7 49.3 18.3 23.1
Hekma (non-Protected)
(0.006)a (3.4)a (3.5) (9.7) (4.6) (4.7)
0.33 94.8 23.8 39.2 14.8 24.7
43.1 (2.8)a
(0.012)a (4.2)b (2.1) (2.4) (3.5) (2.8)
53.9 (2.2)b
Means and standard deviations (SD, in brackets) are shown. Different letter indicates significant differences within the same row; otherwise, the differences are not significant.
Phenophase
Seedling
Juvenile/Vegetative Flower bud Flowering
Flowering/Fruiting Fruiting Seed dispersal Dormancy J
F
M
A
M
J
J
A
S O N D
Month Fig. 6. Phenophases of the Omayed (’), Hekma protected (
Population phenology traits The phenological behaviour of E. armitagei varied among the three study sites (Fig. 6). The Omayed population was characterised by an earlier phenological pattern than Hekma populations. In the former, the seedling phenophase began in early February and ended in early March, while in the protected and unprotected populations at Hekma this phase extended from the second or third week of February to the end of February, respectively. The unprotected Hekma population exhibited both late phenology and a shorter duration of phenophases, especially in flowering and fruiting. The flower bud, flowering and flowering/ fruiting phenophases started two weeks later in the unprotected Hekma than at Omayed, and one week later than the protected Hekma population. Furthermore, the fruiting phenophase lasted for three weeks (from the first to the third week of May) in the non-protected population as compared to six weeks (end of April to early June) and eleven weeks (mid April to early June) in the Hekma and Omayed protected populations respectively.
Discussion The natural habitat of E. armitagei is threatened by two major factors; habitat destruction and overgrazing. The rocky ridges inhabited by the species have been extensively quarried for construction materials which caused complete destruction of this habitat, in addition to the spread of resorts along the Mediterranean coast (UNDP/GEF 1999). Moreover, the pressure of livestock on E. armitagei and other rangeland species is increasing as a result of the increase in Bedouin populations. In the present study, protection from overgrazing is emphasised at Omayed and Hekma compared to the Hekma unprotected site which is subjected to uncontrolled grazing practice. Survivorship, reproductive value and growth rate of the E. armitagei populations were better at
) and Hekma unprotected (
) populations.
protected sites, especially at Omayed within El Omayed Biosphere Reserve. Additionally, a more balanced adult population structure was attained with fewer differences with the stable stage distribution. The phenological pattern of the species also exhibited earlier and more prolonged phenophases at the protected sites. However, the differences between the two protected populations in species demography may be due to variation in the level of protection: complete prohibition of grazing at Hekma and sustainable grazing management at Omayed, or to the variation in local edaphic and/or environmental factors. The unprotected E. armitagei population showed an irregular adult age class distribution. This feature may be considered a direct result of overgrazing stress causing alteration in the reproductive phenology of the species (Hegazy, 1997; Young et al. 2007). Both the intrinsic rate of population growth and the reproductive rate are considered a measure for fitness (Boersma et al. 1999). Despite the apparent merits of protection in the present study, demographic monitoring indicated drastic declines in the three populations; all showed negative growth rates and reproductive rates of o1. Shedding light on the failure of the species for self regeneration even under protection from grazing and/or habitat destruction and the need for other conservation measures, possibly due to frequent drought and seed predation which limit the species regeneration. The fruits-to-seeds and the germinable seeds-to-juveniles were the most critical transitions in the E. armitagei life cycle, having the highest killing power values, resulting in low seeding emergence. Cavers (1983) suggested that the fate of a plant population may be decided by the pattern of mortality acting upon seed behaviour. For example, the predatory beetle Callosobruchus maculotus (Coleoptera; Bruchidae), which consumes seeds of some wild and cultivated legumes, is responsible for significant seed losses (56.6-94.8%) prior to dispersal of E. armitagei (Hegazy & Eesa, 1991). Predispersal seed predation is key factor that could
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limit reproductive success via decreased viable seed production causing lower population growth rate in rare species ¨ (Munzebergav a 2005; Young et al. 2007). Later phenophases in the unprotected Hekma population compared with the protected ones revealed the presence of an intraspecific phenological plasticity of E. armitagei. The smaller seeds and lower germination in the unprotected population may be related to late flowering phenology (Galen & Stanton 1991). Additionally, the comparatively short period of flowering and fruiting in the unprotected Hekma population resulted in lower reproductive values than at the protected sites. These variations in phenological behaviour of the species emphasises that plant phenology is one of the most sensitive functional traits in relation to environmental changes and disturbances (Garnier et al. 2007; Miller-Rushing & Primack 2008; Post et al. 2008). Fleischner (1994) reported that overgrazing may delay phenology, and according to the species, overexploitation and/or overgrazing may have damaging effects on plants when occurring at specific phenophases (Hendrickson et al. 2005; Olson & Richards 1988). In the unprotected population which is subjected to overgrazing, the relatively shorter fruiting and seed dispersal phenophases, together with the earlier intrusion into dormancy may be possible explanations for the greater susceptibility of seeds to insect predation. Klips et al. (2005) reported that the levels of seed predation can vary a great deal from year-toyear and site-to-site and it is affected by the timing of seed availability. Failure of normal recruitment of E. armitagei in its natural habitat is mainly attributed to the loss of seeds due to insect predation and grazing of reproductive organs associated with the low rate of emergence and survival of seedling. Protection is not always the solution to the conservation of endangered species (e.g. Gurd et al. 2001; Xu & Melick 2007; Zimmerman & Reichard 2005). On the other hand, Hegazy et al. (2008) and Linkie et al. (2008) found that protection from overgrazing and overcollection has an important role for species conservation in cases where threats resulted as a direct response to human impact. In case of E. armitagei the presence of species-specific constraints, including predispersal seed predation and low reproductive values, reduced the effectiveness of protection and resulted in a continuous decline of the populations. Introduction of new individuals by transplantation may be a useful tool. In other cases, transplantation of species has proved to be an effective tool in accelerating local restoration (Cole & Spildie 2006). In the present study, the relative success (43-54%) of vegetative propagation suggests that raising transplants from cuttings could be used to accelerate the recovery of the E. armitagei populations to overcome the problem of seed predation and the low rate of seedling emergence and survival. Regeneration of the species in its natural habitat by use of transplants obtained from seeds faces limitations where up to 95% of seeds are subject to insect predation before maturity stage where collection of enough seeds will not fulfill large scale regeneration from seed. Moreover, the damage caused by the insect Callosobruchus maculotus is not only associated with loss of seeds, other risks such as injury of the embryo and cotyledons are expected which prevent and/or abort germination of the infested seeds (Hegazy & Eesa, 1991).
Conservation considerations As the protected Omayed population, where grazing is managed, is more stable than the protected Hekma population with complete use restriction, then the species responds better to the rational use than to the prevention of grazing.
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The recovery of E. armitagei populations needs the investment of other regeneration strategies in addition to protection, especially when regeneration from seeds is limited due to intrinsic (low emergence and survival of seedlings) and extrinsic (predation) causes. Conserving species in their natural settings, their own habitat, is key to ensuring their long-term survival. The success of vegetative propagation in E. armitagei suggests one possibility for restoring these populations. Raising new transplants from cuttings and/or seeds to restore the declining natural populations may be essential to maintain them. The cultivation of E. armitagei as an ornamental plant with its lovely pink flowers within the seaside resorts should be encouraged as a partial rehabilitation method for the natural habitat of the species. As the phenological behaviour of the species is influenced by the level of protection, probably the phenological spectrum of the species varies from year to year in the Mediterranean environment characterised by climatic variability. The present work was based on a one year study, more prolonged and detailed monitoring is needed in order to provide a more precise range of time for each phenophase. Systematic census of the species is also recommended in order to monitor the response to the proposed conservation measures in Omayed and Hekma.
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