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Silva Balcanica, 15(1)/2014

MORPHOLOGICAL STUDY OF CORNUS MAS L., CRATAEGUS MONOGYNA JACQ. AND SAMBUCUS NIGRA L.

UNDER INDUSTRIAL AND ROAD TRAFFIC POLLUTION

Мaya Kurteva1, Daniela Dimitrova2

1 Institute of Biodiversity and Ecosystem Research – SofiaBulgarian Academy of Sciences

2 Institute of Biophysics and Biomedical Engineering– SofiaBulgarian Academy of Sciences

Abstract

Cornus mas L., Crataegus monogyna Jacq., and Sambucus nigra L. have been stud-ied under industrial and urban pollution in Sofia, with predominant road traffic, as well as along the heavy loaded road Sofia-Svoge during a period of three years: 2008-2010. Three morphological parameters were evaluated: linear growth of the annual twigs (cm), the number of leaves on the twigs and leaf area (cm2). Statistical analysis of data was performed using ANOVA. The carried out morphological analysis showed that the stud-ied shrub species responded to the conditions of industrial and road traffic pollution with considerable changes in the growth and development. All three morphological parameters were suitable for the present study as ‘leaf area’ was the most sensitive index (C. mo-nogyna, S. nigra). For C. mas the adaptation was manifested by changes of ‘growth of the twigs’ and ‘leaf area’. The ‘number of leaves’ was affected in lower degree by pollution factors, but could be used succesfully in industrial poluted regions. Under industrial pollu-tion low values of the measured parameters showed C. mas (Yana), C. monogyna (Pirdop), S. nigra (Yana, Botunets). Under high transport pollution C. mas showed values lower than the control. The present study outlined the range of resistance to air polution and thus the possibility of the species usage for planting in the observed regions. C. monogyna (Tsarigr. Shose Blvd.) and S. nigra (Pirdop) were defined as tolerant ones. C. mas (Pirdop, along the road Sofia-Svoge) and S. nigra (Tsarigr. Shose Blvd.) were considered as medium sensitive with recommendations for a moderate usage at high pollution level. C. mas (E. and H. Georgievi Blvd., Yana), C. monogyna (Pirdop) and S. nigra (Yana, Botunets) were expressed as sensitive and their use in the mentioned regions and other with similar type of pollution is unadvisable.

Key words: air pollution, shrubs, morphological parameters, Bulgaria

INTRODUCTION

Nowadays pollution in megacities and large urban areas has become the most significant threat for the survival of living species all over the world. With the rapid industrialization and bigger urbanization environment pollution has become

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a serious problem. Road traffic is a major source of air pollution in large towns as well as in urban and many rural areas (Colvile et al., 2001; Goyal et al., 2006). Motor vehicles emit a complex mixture of gaseous pollutants including benzene, carbon monoxide (CO), nitrogen oxides (NOx), nitrous acid (HNO2), ammonia (NH3), sulphur dioxide (SO2), volatile organic compounds (VOCs), polycyclic aro-matic hydrocarbons (PAHs) (Colvile et al., 2001; Harrison et al., 2003; Cape et al., 2004), as well as suspended particulate matters, smoke, metals (Cd, Co, Cu, Pb, Zn, Ni) and dust. Particles that contain heavy metals originate as from exhaust emissions as from vehicle wear (Harrison et al., 2003). Among the mentioned pol-lutants heavy metals, PAHs ans sulphides are defined as a toxic or cancerogenic. In spite of developing improvements in combustion engine technology, air pollution in most urban areas is measured as levels defined to be harmful to human health (Calef, Goble, 2007).

Plants, because of their immobility and strong relation to the place of growing, can not escape the adverse environment, and have an ability to identify and to re-sponse to the alterations of environmental conditions. This ability allows using them as sensitive indicators of the changes in the environment and these features are used broadly in the system of biomonitoring of regions with high level of air anthropo-genic pollution. Vegetation is an effective indicator of the overall impact of air pol-lution and the effect observed is a time-average result that is more reliable than the one obtained from direct investigation of the pollutant in air over a short time period (Seyyednejad et al., 2011). In urban environments trees and shrubs play an important role by taking up many gases, particles, aerosols from the air (Joshi, Swami, 2009) thus improving the quality of the air and life (Powe, Willis, 2004; Woo, Je, 2006). The advantages of the broad-leaved trees and shrubs compared to the coniferous are: accelerad development of the twigs, shorter exposure of broadleaved species leaves to the the gases during their development and finally, they possess a bigger ability to regeneration due to the leaves fall at the end of vegetation. Moreover, trees and shrubs are characterized with relatively long life as well as high ability to reflect local conditions (Nali, Lorenzini, 2007). Trees exhibit greater tolerance to environ-mental changes than the rest of the plants (Berlizov et al., 2007).

Morphological studies on trees and shrubs under air pollutioin conditions are among the most used methods for investigation of species state by determination of alterations in the growth and development of the species under high level of in-dustrial or urban, especially road traffic pollution. Morphological responses in high plants are included in the biomonitoring of air polluted regions (Schubert, 1985; Tingey, 1989).

On the basis of available data concerning features of shrubs species and the advantiges of morphological parameters: growth of annual twigs, number of leaves on them and the leaf area, we hypothesized that the following three shrubs species: Cornus mas L., Crataegus monogyna Jacq., and Sambucus nigra L. could be used for an establishment of the range of tolerance to air polution and the ability for planting

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them in the investigated regions by registration of alterations in the mentioned three morphological indexes.

In order to test this hypothesis, the aim of the present study was to determine the gas resistance of Cornus mas L., Crataegus monogyna Jacq. and Sambucus ni-gra L. by tracing the changes of three morphological parameters, characterizing the growth and development of the investigated species under conditions of industrial and road traffic pollution.

The present study included C. mas and S. nigra for first time as objects of morphological investigation in Bulgaria.

MATERIALS AND METHODS

Objects of the research were Cornus mas L. (European Cornel, Male Dog-wood), Crataegus monogyna Jacq. (Common Howthorn, Whitethorn) and Sambucus nigra L. (Elder, Common Elder). C. mas is a small deciduous tree but usually occurs as shrub. It is widespread in Central and South Europe, Crimea, Caucasus and Asia Minor. In Bulgaria the species is widespread but it is scattered – in groups or single - as an understory component of mixed deciduous forests and bushes in the scope 200–1300 m a. s. l. (Delkov, 1992). European Cornel is seldom cultivated but valu-able decorative forms as such with big fruits are also known (Gramatikov, 1992). In our country it is used mainly as fruit tree because of tasted and medicinal fruits. To date the morphological investigation of the species from air polluted regions in Bulgaria still missed.

C. monogyna is spread almost over whole Europe (without the north parts and Caucasus), Northwest Africa and Southwest Asia (Delkov, 1992; Gramatikov, 1992). In Bulgaria the species grows ordinarily like shrub, very seldom as tree, in the forests and bushes, on different places – in river valleys as well as on rocky and calcareous slopes all over the country till to 1400 m. This is a polymorhic species, cultivated seldom. Common Howthorn is quite plastic: it grows in very different soil conditions, including regions under high level of environmental pollution. There were previous investigations with C. monogyna under the impact of pollution in Pirdop (Kurteva et al., 1987), also in the region of the Chemical Works in Devnya (Kurteva, 2008).

S. nigra is a small deciduous tree or shrub. It is distributed in Central and South Europe, Crimea, Caucasus and West Siberia (Delkov, 1992). In Bulgaria it oc-curs in plains and mountainous slopes, usually along the rivers and streams as shrub or tree. Till now this species has not been an object of morphological study in the regions under anthropogenic pollution in Bulgaria.

The indicated shrub species have a different degree of gas resistance to SO2, NOx, NH3, O3 and organogenic compounds according to previous investigations. They are as follows: C. mas - resistant species (Аntipov, 1979), bears air pollu-tion (Delkov, 1992); C. monogyna – from strongly resistant (Ilkun, 1978), resistant

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(Аntipov, 1979), with middle regenerative ability after an injury (Тreshow, 1984; Schubert, 1985), to medium resistant species (Prokopiev, 1978), small sensitive to pollution with SO2 and HF (Dässler, 1981), higher resistant to pollution in Pir-dop compared with the registered one for Devnya region (Kurteva, 2008); S. ni-gra - resistant species (Аntipov, 1979), resistant to pollution with SO2, NH3, F, NOx (Dässler, 1981; Byalobok, 1988). All three species are medium resistant to pollution in Devnya (Zhelyazkov et al., 1986). S. nigra is ranged among the species – bioac-cumulative indicators of aerial heavy metal environmental pollution (Kovács, 1992; Mulgrew, Williams, 2000). Some of the studied species are recommended for plant-ing of zones with high level (S. nigra) (Gateva et al., 1987), at medium level of pol-lution and nearby establishments – local pollutants (C. monogyna) (Dobrovolskiy, 1980; Кondratjuk, 1980), as well as notably suitable for the green zones of Sofia (C. mas, C. monogyna) (Vakarelov, Delkov, 1975).

The industrial pollution of the environment was established nearby Pirdop Cop-per Works (UMPC – Pirdop), with geographic coordinates: 42042/37.67// N 24010/26.80//

E, by the point Pirdop (Pirdop) – close (0.2 km) to the source of pollution, in the zone with the highest degree of pollution. The influence of Kremikovtsi Metallurgical Works was studied by 2 points: Yana Railway Station village (Yana) (42043/54.03// N 23033/24.48// E) and Botunets village (Botunetsc) (42044/31.34// N 23030/58.64// E), both in Sofia district and hardly affected by ferrous industry in Kremikovtsi.

The road traffic pollution was observed mainly in Sofia town, along Tsari-gradsko Shose Blvd. (Tsarigr. Shose Blvd.) (42041/23.14// N 23020/21.24// E), for C. mas - Evlogi and Hristo Georgievi Blvd. (E. and H. Georgievi Blvd.) (420 41/ 27.45//

N 23020/ 22.27// E), as well as along the heavy loaded road Sofia-Svoge (42055/ 09.87//

N 23023/ 17.96// E).The type of pollution and main pollutants in the observed regions during the

period of investigation are presented in Table 1 and the data are according to Na-tional Automatic System for Ecological Monitoring (Newsletters for environmental status of SCSESD at MEW*).

As a control variant (K) individuals of the species from Vitosha Mt. (42036/23.14//

N 23018/04.77// E) (S. nigra, C. monogyna), as ones growing in the yards of Thompson Railway Station village (42055/13.72// N 23023/15.38// E) (C. mas) were used.

The morphological analysis included the determination of following three in-dexes: linear growth of annual twigs (cm), number of leaves, developing on them and leaf area (cm2). The pointed out morphological parameters reflect the changes in the growth, as far as the total drop in the growth of tree and shrub species in the con-ditions of industrial pollution is manifested by a diminution of radial growth, growth in height, linear growth of annual twigs, size and number of needles and leaves (Keller, 1979; Manning, Feder, 1980). The decrease of growth as well as size of the leaves, the change in their shape and a low leaf quantity are common symptoms for the worse state of Betula pendula, Fagus sylvatica L. and Carpinus betulus L. in the forests of Central Europe (Schūtt, 1989). According to Sikora, Chappelka (2004) the

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stunted growth, the premature loss of foliage or the whole defoliation are the types of visible injury to plants under air pollution.

The alterations in growth by measuring of separate organs or the growth of annual twigs according to Gluch (1980) are more sensitive indicators in comparison with the assessment of dry mass of the whole plant. For this reason, the alterations in growth, even though in more cases are non specific, are more sensitive indicator than necroses (Gluch, 1980; Jäger, 1980) and are used broadly for fast and early diagnostics for the state of tree species (Luchkov, 1992), as well as for examination of species ad-aptation to industrial pollution (Dorogan, Djukov, 1990; Korshikov, Tarabrin, 1990). According to Manning, Feder (1980), Halbwachs (1988) and investigations of some authors (Volkova, Belyaeva, 1990; Girs, Zubareva, 1992; Gryshko, 2002), as well as confirmed by our studies (Kurteva, 1999; Kurteva, Merakchiyska-Nikolova, 2004; Kurteva et al., 2004; Kurteva, Stambolieva, 2007; Kurteva, 2008), these morphologi-cal parameters could be used by tracing the alterations in growth and development for determination the state and range of resistance of plants, for early indication or more long-term biomonitoring on the impact of air pollution on plants, as well as in compil-ing a list of tree and shrub species suitable for planting in industrial and urban areas. The plant growth, todether with the changes in morphological responses, can be used as examples of a possible response of plants and their application as bioindicators of environmental pollution (Tingey, 1989; Akkuzu, Ayberk, 2001).

The linear growth of annual twigs was measured linearly (cm), while the feaf as-similation area was determined after Roznjatovskiy (1954) with modifications: instead of on photosensitive paper, the imprints of leaves were taken on plotting paper and their area (cm2), together with the petiole, was determined by weighting method. For the leaf area determination strictly definited leaf on the annual twig was selected.

The investigation was carried out in 3-year period (2008-2010). The mor-

Table 1. Type of pollution in the studied sites

Site Type of pollution Main pollutants

1 Copper smelter in Pirdop (UMPC – Pirdop)

dust, SO2, H2S, aerosols of H2SO4, Cu, Pb, Pb, As, Zn, Cd and NO2

2 Yana Railway Station dust, SO2, phenol, Pb-aerosols, H2S, Pb

3 Botunets village dust, Pb-aerosols, SO2, Cd, Pb

4 Tsarigradsko Shose Blvd., Sofia dust, benzene, NO2, SO2, CO, Cd, Pb, Zn, Ni, CO2, hydrocarbons, aldehydes, aerosols

Legend: 1. UMPC – Pirdop; 2. Yana; 3. Botunets; 4. Tsarigr. Shose Blvd. Pollutants in bold are with concentrations, exceeding LPC (Limited permissible concentration). MEW* - Ministry of Environment and Waters of Bulgaria.

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phological measurements, also the collection of samples for leaf area determina-tion, were conducted in the first half of August when the linear growth of the annual twigs was completed, the number of leaves on them was final and the leaf blades were fully developed and reached ultimate size. The modal individuals of the studied plant species are similar to age, height and form of growth. The sam-ples were collected from the sunny side, at 130-180 cm height from each species in all of points of study.

The data obtained from the morphological analysis was statistically compared using оne-way ANOVA test with Bonferroni’s correction by application of the soft-ware OriginPro 7.0. Statistical significance was evaluated at Р<0.05, Р<0.01 and Р<0.001 (mentioned in figures respectively with one, two and three asterisks). The sample sizes are presented in Table 2.

Table 2. Sample sizes involved in the present study and arranged according to the years, points and morphological criteria investigated

YearPoint

2008 2009 2010

Morphological parameters

Growth of twigs

Num-ber of leaves

Area of leaves

Growth of twigs

Num-ber of leaves

Area of leaves

Growth of twigs

Num-ber of leaves

Area of leaves

Cornus masPirdop 81 81 79 79 79 79 92 92 88Yana 40 41 44 60 60 60 110 110 110Road Sofia - Svoge

98 98 97 76 76 76 118 118 115

E. and H. Georgievi Blvd.

- - - 51 51 55 82 82 88

K (Control) 55 55 54 86 87 88 115 116 99Crataegus monogyna

Pirdop 75 75 68 94 94 94 96 96 107Tsarigr. Shose Blvd.

50 50 56 81 82 87 121 121 141

K (Control) 76 76 76 92 92 92 127 127 138Sambucus nigra

Pirdop 55 55 54 93 93 93 125 125 124Yana 57 57 55 77 76 75 125 125 124Botunets 51 51 51 38 38 38 106 106 109Tsarigr. Shose Blvd.

104 104 96 92 92 94 150 149 148

K (Control) 50 50 50 63 63 61 112 113 86

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RESULTS

Average data of the three parameters from the morphological analysis of the studied species are presented graphically (Fig. 1-3). Moreover, the data outlined ten-dencies in the growth and development of the species studied in the conditions of industrial and road traffic environmental pollution.

The specificity in the variation of the values for the morphological parameters in C. mas from the points of study is presented in Fig.1 A-C.

Fig. 1. Average values of the morphological parameters for Cornus mas, 2008-2010. A – linear growth of the annual twigs (cm); B – number of leaves on the twigs; C- leaf area (cm2). Points of

study: Pirdop, Yana, E. and H. Georgievi Blvd., Road Sofia - Svoge, K-control.Asterisks denote when the obtained mean values of the parameters are statistically different from the

controls: * - at Р<0.05, ** - at Р<0.01 and *** - at Р<0.001

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According to the linear growth of the annual twigs the variation in C. mas was statistically proved in point Pirdop, Yana as well as along the road Sofia-Svoge during 2008. Concerning the number of leaves on the twigs the data was statistically different from the controls in Yana (2008), in the transport pollution along the road Sofia-Svoge in 2009, also, but in lower degree, along E. and H. Georgievi Blvd. (2009). Statictically different measurements regarding the leaf area were observed for the species individuals at points Pirdop in the whole period of the investigation and in Yana during years 2008 and 2010, whereas along the road Sofia-Svoge – only in 2008 (Fig. 1 A-C).

The average twigs growth of European Cornel for the whole period of inves-tigstion was the lowest along E. and H. Georgievi Blvd. (Cornel’s individuals in this point are objects of 2-year study: 2009, 2010), followed by the ones, growing in Yana, as again with growth lower than the control, but with equal values – in Pirdop and along the road Sofia-Svoge (Fig. 1A).

The twigs growth of this plant species in the regions under industrial pollu-tion increased during 2009, more clearly for Pirdop, with a drop at the end of study (2010)(Fig. 1A). Under the impact of autotransport pollution Cornel growth showed a drop started from the beginning to the end of the research (Fig. 1A). Bigger varia-tion in the values during the years was noticed in Pirdop, where the growth of twigs from 3.15 cm (2009) decreased (3.4 times) to 0.93 cm to the end (2010). Similar difference (3.0 times) was registered among the values for the individuals along the road Sofia-Svoge: from 2.77 cm (2008) tо 0.91 cm during 2010. The control values were differentiated particularly strongly (5.4 times), with sharp drop from 5.01 cm (2008) to 0.93 cm (2010) (Fig. 1A). The values among the points with different type of pollution varied remarcably too: 2.77 cm (along the road Sofia-Svoge) – 1.45 cm (Yana) during 2008, for 2009 among the values of the twigs growth in Pirdop (3.15 cm) and along E. and H. Georgievi Blvd. (1.90 cm) (Fig. 1A). The control value was the maximal (2008), occupied medium position (2009) or was very close to the minimal during 2010 year (Fig. 1A).

The smallest growth of Cornel’s twigs was registered along the road Sofia-Svoge (0.91 cm) in 2010, the values were very low as under industrial (Pirdop), as road traffic pollution (along the E. and H. Georgievi Blvd.), respectively 0.93 cm and 0.96 cm again in 2010 year. These results and their connection with extreme climatic factors in the indicated year are discussed in details in section Discussion. Twigs growth was maximal in the control version (2008) – 5.01 cm, while in the polluted regions with more clearly expressed growth were the individuals in Pirdop only (2009) – 3.15 cm (Fig. 1A).

Comparison of the average values with the control showed growth lower than the control in the observed points in the first two years, with exception of individu-als from Pirdop (2009). The growth of twigs was expecially retarded during the first year (2008), with values as follows: 28.9% (Yana), 36.9% (Pirdop) и 55.3% (along the road Sofia-Svoge) from K. During 2009 was registered twigs growth below the

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control value along the E. and H. Georgievi Blvd. as well as in Yana, respectively 76.6% and 82.2%, also for the individuals along the road Sofia-Svoge, but closer to the control (90.3%). To the end of the investigation growth of Cornel twigs de-creased in all of the observed regions compare with the previous years, but because of the sharp drop also in the control growth, the values exceeded the control in the range: 100% (Pirdop) – 134% (Yana). Only Cornel along the road Sofia-Svoge marked growth below (98%) the control one.

The number of leaves on European Cornel twigs for the whole period of in-vestigation was the lowest for the individuals, growing in Yana Railway Station and higher along the E. and H. Georgievi Blvd. Only Cornels along the road Sofia-Svoge developed bigger number of leaves than in the control at the end of study.

Data concerning the number of leaves on C. mas twigs (with exception of the individuals along the road Sofia-Svoge) showed a decrease of their quantity started from the beginning (2008) to the end of study (2010) (Fig. 1B). Bigger variation of data in the years investigated was registered for Cornel along the road Sofia-Svoge: from 2.66 (2009) till to twice bigger number (5.33) during 2010, as in the control version, but with smaller difference between the values: 3.69 (2008) – 2.28 at the end of research.

The difference in the values was significant in 2010 between the individu-als from regions with different type of pollution: along the road Sofia-Svoge (5.33) agaist Pirdop (2.29) (Fig. 1B). The minimal number of leaves was registered dur-ing 2010 in Pirdop – 2.29, whereas Cornel along the road Sofia-Svoge had the best foliation (5.33) also in the same year (Fig. 1B). The control value in respect of the indicated morphological parameter noticed the maximal values (2008, 2009), while at the end of research reached the minimum one for the whole investigated period (Fig. 1B).

Comparison of the data from the polluted regions with the control proved the lower degree of twigs leafing during the first two years in all of the studied points, mainly for Cornels from Yana, with values 2.51 (2008) and 2.50 (2009), which rep-resented 68% and 76.2% respectively from the K. In both points under transport pollution the values during 2009 were quite below the control - 81% (along the road Sofia-Svoge) and 86% (along E. and H. Georgievi Blvd.). Only in 2010 data were juxtaposed to the control (Pirdop, Yana) or exceeded it considerably (234%) (along the road Sofia-Svoge). For this morphological index, like to the mentioned above as regard the twigs growth, the values in the same year were lower than one in the previous years (with exception the point along the road Sofia-Svoge), but because of drop in the control, exceeded it.

The mean values of leaf area for the whole period of the study showed an augmented reduction of leaf area of Cornels from the regions with traffic pollution, mainly along E.and H. Georgievi Blvd. whereas with relatively bigest leaf area in 2009 and 2010, particularly in 2009 (but in the beginning of the study again below K) showed the plants from Pirdop (Fig. 1C).

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The mean values of leaf area in C. mas (with exception of the region of Yana) proved decreasing of leaf area to the end of the study. Maximum variation of the parameter was remarked for the control, in wich the leaf area was reduced from 23.07 cm2 (2008) to 8.35 cm2 (2010; 2.8 times) and moderately in Pirdop (1.3 times more in 2009 (15.88 cm2) compared to 2008 (11.79 cm2)). The lowest values of the same parameter were registered during 2010 (traffic pollution, along the road Sofia-Svoge - 8.73 cm2 and along E. and H. Georgievi Blvd. - 9.30 cm2 as well as in K- 8.35 cm2; Fig. 1C).

The leaves of Cornels had a maximum area in K (during 2008; 23.07 cm2), followed by the individuals in Pirdop - 15.88 cm2 (2009) and 12.70 cm2 (2010) and Yana- 12.36 cm2 (2010) (Fig. 1C). Controls showed various values among the years of study: maximal during 2008, middle value in 2009 and minimal value during 2010.

The comparison of the data between polluted regions and control ones showed a strong reduction of leaf area in Cornels at all of the points of study during 2008 especially along the road Sofia-Svoge and not enough decrease for the individuals from Yana and Pirdop (respectively 43.4%, 50.4% и 51%). During 2009 only Cor-nels along E. and H. Georgievi Blvd. demonstrated area below K (95.3%), whereas in the rest points the values exceeded K in the interval: 104.8% (for the road Sofia-Svoge) and 142.4% (in Pirdop). In the end of the investigation leaf area decreased as under industrial (Pirdop) as in heavely road traffic polution mainly along the road Sofia-Svoge. Because of the observed drop in K, data from the polluted regions re-mained above the control value, especially in Pirdop and Yana (152% and 148%).

It was outlined a tendency for partial compensation among the studied pa-rameters. Thus, the limited leaf area and minimal growth of twigs along the road Sofia-Svoge (2010) was compensated by bigger number of leaves in Cornels. Lim-ited number of leaves and growth of twigs in 2009 year in the region of Yana and along road Sofia-Svoge were partially compensated by the development of bigger leaf area. More limited leafing of the twigs in Pirdop probably was compensated by increasing of the leaf area and the growth of twigs during 2009.

Concerning C. monogyna, the obtained results on morphological parameters at the points of study are presented on Fig. 2 A-C.

Statistical differences between studied individuals and control plants using the parameter ‘growth of the twigs’ were found along Tsarigr. Shose for whole period of investigation and for Pirdop during 2008. According to the morphological index ‘number of leaves on the annual twigs’ the differences between probe and control were statistically significant in Pirdop (for 3-years period) and along Tsarigr. Shose for 2010 and statistically proved variation in ‘leaf area’ showed plants in Pirdop as well as along Tsarigr. Shose, more obviously in Pirdop during all years of study (Fig. 2 A-C).

Comparing the mean values of the parameter ‘growth of the annual twigs’ of C. monogyna, two times slower growth in Pirdop in comparison with plants along Tsarigr. Shose was observed (Fig. 2A) and at these two points the growth of twigs

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decreased during 2010. Minimum value of the mentioned morphological index was registered in Pirdop (1.44 cm), wheares maximum was reached along Tsarigr. Shose (Fig. 2A; 4.19 cm).

Using a comparison among the control and investigated individuals, it could be observed that along Tsarigr. Shose during the whole period the twig growth ex-ceeded the control variant, especially in 2010 (185.7 %), probably due to the mini-mal value of K registered in this year. In Pirdop investigated individuals showed twig growth above control during 2010, contrary to the observed results in another two years of investigation (2009 and especially 2008 - 64.2 %).

Mean values of the parameter ‘number of leaves’ in studied individuals showed a decrease of this parameter in Pirdop compared to Tsarigr. Shose (Fig. 2B) and more importantly, this parameter remained unchanged along Tsarigr. Shose and with almost equal values in Pirdop for 2008 and 2009. During 2010 the number of

Fig. 2. Average values of the morphological parameters for Crataegus monogyna, 2008-2010. A – lin-ear growth of the annual twigs (cm); B – number of leaves on the twigs; C - leaf area (cm2). Points of

study: Pirdop, Tsarigr. Shose Blvd., K- control. The meaning of asterisks and P-values - as in the Fig. 1.

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leaves increased at both points of the investigation (Fig. 2B). On the contrary, in K a tendency of a decrease of the number of leaves from the beginning to the end of the investigation was found.

As shown on Fig. 2C, the mean values of the ‘area of leaves’ found in C. mo-nogyna demonstrated strong reduction in dependence of the existence of an indus-trial pollution, especially in Pirdop. The minimal value of this morphological index was found in 2009 at the same point: 2.30 cm2. The maximim leaf area (7.65 cm2) was registered in K during 2008. Using obtained results it could be mentioned that the index ‘leaf area’ is the most sensitive parameter among the three ones used in the present investigation. The K values exceeded all others vallues of this morphological parameter during the whole period of the investigation (Fig. 2C).

In general, the comparison of the data concerning the leaf area of C. monogy-na showed that this index is the most sensitive, especially for the individuals in the industlial polluted region (Pirdop).

Furthermore, the partial compensation of the reducted leaf area by the de-velopment of higher growth of twigs and by increased leafing could be suggested (Tsarigr. Shose, 2009 and 2010; Pirdop, 2010).

The obtained results of the study of S. nigra are presented in Fig. 3 A-C.Statistical analysis revealed that in Pirdop (2010, 2009) and at the points Yana

and Botunets the parameter ‘twigs growth’ during 2008 was significantly different in the studied compared to the control plants. According to ‘number of leaves on the twigs’, statistical differences in the data were found in Pirdop for the whole period, in Botunets for 2009 and along Tsarigr. Shose in 2008. Finally, the parameter ‘leaf area’ varied in all studied regions and for whole period of the study with different magnitude of statistical variations (Fig. 3 A-C).

In the conditions of industrial pollution, the minimal mean values of the pa-rameter ‘growth of twigs’ were registered in Botunets and Yana, while the maximal value was in Pirdop during 2008 - 6.27 cm. The absolute maximal twigs growth was remarked in 2008 too, but observed in the traffic polluted region Tsarigr. Shose - 6.37 cm (Fig. 3A).

The control values were positioned in the middle of values scale, which phe-nomenon revealed that other factors of the environment as climatic, played an im-portant role on the growth of S. nigra.

The number of leaves on twigs of Elder showed an increase order of leafing as follows: starting with minimal number of leaves along Tsarigr. Shose to Yana and Botunets and up to the plants in Pirdop.

Intriguingly, the values of number of leaves of Elder were very similar each others. Only in Botunets this morphological parameter varied between years of study: from 4.08 (2008) to 2.78 (2010). Maximal leafing of the twigs was found in Pirdop and Botunets, respectively 4.33 and 4.08, whereas the minimal values were registered in the end of study in Botunets (2.78) and Tsarigr. Shose Blvd, (2.92)(Fig. 3B). In general, the number of leaves decreased to the end of the present research.

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The control values occupied medium position (2008, 2010) while in 2009 the minimum value among all measurements was found namely in the control.

Concerning the last morphological parameter investigated, i.e. ‘leaf area’, the mean values were minimal in Yana followed by the individuals in Pirdop and Botu-nets and with relatively biggest area of leaves were plants along Tsarigr. Shose Blvd. (Fig. 3C).

Moreover, leaf area decreased in the end of the study (2010) in all of the studied regions. The minimal values were registered in Yana - 17.45 cm2 (2010) and 19.08 cm2 (2009) as well as in Pirdop during 2010 (23.09 cm2). The maximal leaf area reached the individual from the control: 49.96 cm2 in the beginning of the study (2008). Con-trol values remained maximal for the whole period of the research (Fig. 3C).

The lowest values of the leaf area were noticed for the plants from the indus-

Fig. 3. Average values of the morphological parameters for Sambucus nigra, 2008-2010. A – linear growth of the annual twigs (cm); B – number of leaves on the twigs; C - leaf area (cm2). Points of

study: Pirdop, Yana, Botunets, Tsarigr. Shose Blvd., K- control. The meaning of asterisks and P-values - as in Fig. 1.

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trial regions: Yana - 50.8% (2009) – 57.6% (2008) followed by the the individuals in Pirdop - 52.5% (2008) – 69.6% (2010) and Botounetc: 50.0% (2008) - 83.8% (2010) compared to K. Bigger, but again below the controls, were the values in Elder indi-viduals growing along Tsarigr. Shose Blvd.: 66.8% (2008) – 82.6% (2009).

It was obvious a partial compensation of reduced leaf area in Pirdop for the whole period of the study by the mean of bigger twigs growth and a development of an increased number of leaves. Moreover, the elevated formation of leaves in Yana (for all 3 years) and in Botunets (2008 and 2009), partially compensated the reduced leaf area and the lower growth of the twigs.

DISCUSSION

The plant resistance to the environmental pollution is determined as biologi-cal features of the species studied, as the ecological conditions, among which the atmospheric pollution and climatic factors are of crucial significance. Environmental conditions can be classified after Antipov (1979) as follows: 1) Ecological-edaphic – with significance role in the gas resistance formatting, and 2) Ecological-climatic – with considerable impact on the gas resistance. The joint action of high pollution level with extremal climatic factors affects negatively the resistance of tree spe-cies with proved strong depence of the climatic changes in the environment. Plant adaptation to changing environmental factors including anthropogenic air pollution involve both short-term physiological responses and long-term physiological, struc-tural and morphological alterations. These changes help plants to minimise stress with maximal use of internal and external resources (Dineva, 2004).

In the present study 2010 was expressed as extremal year – with late and cool spring, hailstorms, flood rains, followed by strong and long-term drought. Then the twigs growth of C. mas strongly decreased (Pirdop, in the regions under autotrans-port impact), as well as the leaf area – under the influence of road traffic pollution. In respect of C. monogyna in the indicated year twigs also demonstrated lower growth (along Tsarigr. Shose Blvd. Pirdop) and the leaves had strongly reduced area (Tsarigr. Shose Blvd.). S. nigra during 2010 remarked drop in the twigs growth in all of the studied points (except Yana), mainly for the individuals along to Tsarigr. Shose Blvd., also in Botunets, as well as leaf area reduction, especially along to Tsarigr. Shose Blvd. In 2010 were registered minimal values also in the control variants of C. mas (the number of leaves on the twigs, leaf area, the twigs growth also diminished and closely towards to the minimal one), as C. monogyna - in respect to the growth of twigs and the number of leaves on them. The mentioned above confirmed a strong dependance of the studied species to the climatic factors, which together with air pol-lution are the reason for the retarded growth and development of the shrubs in 2010.

The cool spring in 2010 also contributed significantly to the minimal growth of the twigs of C. mas. The late beginning of the spring, with predominance of very low temperatures, together with the pollution, in our opinion, are the main factors for

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retarded growth of Cornel twigs, the limited number of leaves, thus leaf area reduc-tion. This confirmed established results by Protopopova (1980), who reported that the favourable temperature conditions in the first half of vegetation may be of crucial importance for the growth and development of plants as regard to Tilia cordata Mill. and Syringa vulgaris L. Among the climatic factors in 2010 the strong, as the long drought rended particularly negative influence on the Cornel, as this species, despite of the fact that grows under different conditions, prefers more humid soils (Delkov, 1992). This may explaine the minimal values for the all three morphological param-eters also in the control version of the species to the end of study (2010).

The diminishing of twigs growth for C. mas, as well as for S. nigra in the point Yana (for the whole period of study), was similar to the mentioned for Philadelphus coronarius L. and S. vulgaris in earlier investigation by the author in the same re-gion for the period 1990-1992 years (Kurteva, 1999). A decrease of twigs growth in deciduous species under the impact of environmental pollution was registered by many researchers (Kulagin, 1974; Protopopova, 1980; Ninova et al., 1986; Halbwa-chs, 1988; Volkova, Belyaeva, 1990; Girs, Zubareva, 1992; Kovács, 1992; Gryshko, 2002). Drop in the growth of the twigs in Betula pendula Roth. in the conditions of industrial pollution noticed Kulagin (1974), Volkova, Belyaeva (1990), Ninova et al. (1986), for T. cordata – as in industrial loaded (Volkova, Belyaeva, 1990), as in urban environment (Protopopova, 1980; Frolov, 1981). Such decrease of the growth of the annual twigs according to Korshikov, Tarabrin (1990) is an adaptive response of the tree species in their adaptation to technogenic biotops.

The adaptation of European Cornel to environmental pollution in the region of Yana is connected with the development of bigger (compare to the control) leaf area, mainly in 2010, as a compensation to the decreased growth of the twigs and lower degree of leafing.

In the conditions of road traffic C. mas developed bigger number of leaves, expecially along the road Sofia-Svoge, also, although in lower degree, along the E. and H. Georgievi Blvd., as partially compensation to the sharp drop of twigs growth, as well as strongly redused leaf area. The minimal area of leaves in Cornel individu-als along the road Sofia-Svoge (2010) corresponded to the minimal leaf area, de-termined by the author for Laburnum anagyroides Med. along Tsarigr. Shose Blvd. (Kurteva, Merakchiyska-Nikolova, 2004).

The comparison of the data for C. monogyna in Pirdop from the present study with ones, obtained from earlier investigations in the same region for 1983-1985 years (Kurteva et al., 1987), so in 1987-1988 years (Kurteva, 2008) showed com-mensurable growth, bigger, but again below the control - 91.2% (2009) compared with the measured in 1987 – 85.9% from K. The average growth of Whitethorn now (for the whole period of examination) - 84.7 % compared to the control was signifi-cantly smaller than the registered in the region of Chemical Works – Devnya for the period: 1986-1988 – 134.0% from K (Kurteva, 2008). The number of leaves on the annual twigs now (for the 3-year period) strongly decreased to 94.3 % comparing to

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1983-1985 (135%), as well as in comparison with the period 1987-1988 (124.3 % from K). Data, in respect of the indicated parameter (2008, 2009), were under the control values and are confronted with the remarked for C. monogyna from Devnya region (1987), while the value from 2010 (106.7%), although smaller, was near to the one in the region of Devnya for 1986: 112.2 % compare to K (Kurteva, 2008). Among the 3 studied morphological indexes for C. monogyna from the region of Pirdop in the present investigation the leaf area recorded the hardest drop – with average values for the 3 years – 40% compared to K in comparison with the average values for the periods: 1983-1985 (70%) and 1987-1988 (71%). With relatively big-ger leaf area was the species in Pirdop only during 2010 (50% from K), but this value also could be difficulty commensurate with the minimal for the species in Devnya – 62.6% from K (1986).

Most of the species very often demonstrated hard reduction of leaf area under industrial and urban pollution. Decreasing of leaf area under industrial environmen-tal pollution was registered for T. cordata (Volkova, Belyaeva, 1990), B. pendula (Ninova et al., 1986; Ninova, Dushkova, 1987; Volkova, Belyaeva, 1990), Gledits-chia triacanthos L. and Quercus robur L. (Zachirov, Girshevitch, 1990), Euphorbia hirta (Gupta, Ghouse, 1988), Avicenia marina (Naido, Hicot, 2004), for seedlings of Zizyphus spina--christi, Syzygium cumuni and Olea europaea influenced by the road dust (Hegazi, Kady, 2010) and for Eucalyptus camaldulensis under pollution of oil fields (Seyyednejad, Koochak, 2011). Reduction of leaf area in Populus balsamifera L.under the influence of Copper smelter recorded Schveikina (1990), in the region around Kremikovtsi very strong reduction of the leaf area was registered by Dineva (2005) regarding Acer pseudoplatanus L., A. platanoides L. and B. pendula.

The changes of leaf area is of very important mean for plant as the leaf is the most sensitive part to be contacted and affected by air pollutants as major physi-ological processes are concentrated namely in the leaf (Naveed et al., 2010). De-creasing of leaf area according to number of researchers (Kulagin, 1974; Dashkev-itch, Rahimbaev, 1978; Ninova, Dushkova, 1987; Dorogan, Djukov, 1990; Zachirov, Girshevitch, 1990; Bussotti, 2008) is one of the major symptoms for xerophytiza-tion under pollution. The leaf area reduction according to Dashkevitch, Rahimbaev (1978), Dorogan, Djukov (1990) and Korshikov, Tarabrin (1990) is an adaptive re-sponse, attendant plants as a rule in the extreme conditions of the technogenic envi-ronmental pollution.

The cited data above from the comparative analysis of C. monogyna in Pirdop and Devnya showed a sharp drop of the indexes in the present study (2008-2010), mainly in respect of the leaf area and in lower degree – in the twigs growth. It could be outlined a partial compensation among the studied parameters. Thus, decreased leaf area in 2010 year was partially compensated by a forming of bigger number of leaves, so the growth above the control, such as the mentioned for the species in Devnya (1986). Comparison of the data from Pirdop in respect of extremely drought, as with very high temperatures – 2010 and 1988, confirmed the diminishing of the

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twigs growth in the present study to 121% against 179% (1988) from от K, as well as the development of limited number of leaves (106.7%) compared to 131.8% from K (1988), and a considerable leaf area reduction (50%) compared with the registered one during 1988 (77.3% from K) (Kurteva, 2008).

The comparison of data for C. monogyna in the region of Pirdop from the present study with similar for Spiraea vanhouttei (Brot.) Zbl. in the same region for the period 1983-1985 (Kurteva et al., 1987) showed considerably lower than the control values in respect to the three investigated parameters - 84.7% (twigs growth), 94.3% (number of leaves on the twigs), and 40% from K as regard to the leaf area against ones obtained for Spiraea vanhouttei, respectively 105%, 127% and 90% compared to K. The twigs growth of Whitethorn in the same region in the present research was also below the registered for Tamarix tetrandra Pall. (111% from K) in an earlier investigation in the region (Kurteva et al., 1987).

The morphological values for ‘number of leaves’ and ‘leaf area’ in 2010 year for C. monogyna in Pirdop exceeded the remarked in the previous years (2008 and 2009) that proved the great drouhgt resistance, as well as the plasticity of the species. The stunded growth and the development of Whitethorn in Pirdop are as a result of long-term pollution of the region from Copper smelter activity. The survival of the species is connected with the developing of bigger number of leaves (2010) and rela-tively higher growth, but below the control (2009) as a compensation for the strong reduction of leaf area, especially in 2008 year.

Under the heavy traffic along Tsarigr. Shose Blvd. for the whole period of study C. monogyna showed nearly twice greater growth of twigs (162%) than the ob-served in Pirdop (84.7%) compared to K, that was similar, but bigger than the noticed for Ligustrum vulgare L. (157.5%), as well as for Laburnum anagyroides (126.2%) in the same region (Kurteva, Merakchiyska-Nikolova, 2004). In the conditions of road traffic environmental pollution Whitethorn developed greater twigs growth as well as leafing near (2008) or above the control (2009, 2010), as a compensation for the redused leaf area, particularly in 2010 and 2008 (respectively 58.5% and 61% compared to K). Leaf area reduction under heavy transport pollution was reported by various authors, especially for T. cordata (Frolov, 1981), Guaiacum officinale (Jahan, Iqbal, 1992), Albizia lebbeck (Seednejad et al., 2009), as for hybrid clones of Populus tremula L. x Populus tremuloides Michx., growing away of 15 m from the autoban (Nikula et al., 2011).

S. nigra individuals in the two regions under the impact of Kremikovtzi pol-lution average for the 3-year period of investigation showed lower, but equal growth in both points (80%), as reduced leaf area, mainly in the point Yana (54.1% from K) compared to the noticed for Botunets (69.4% from K). Elder partually compensated by forming of higher number of leaves, in unison with the foliation in L. vulgare closer to Kremikovtsi in 2000 year (Kurteva, Merakchiyska-Nikolova, 2004). The strongly reduced leaf area of Elder in Yana (for 3-year period of research) corre-sponded to the decreasing leaf area for P. coronarius, registered by the author from

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the same point for the period 1990-1992 (Kurteva, 1999). The obvious drop in the leaf area of S. nigra during the extremely dry 2010, in our opinion also would be connected with the proved by Hale et al. (1987) that the tolerance of water content of tissue in drought stress is possible by decrease of leaf area.

The survival of S. nigra in the regions under industrial pollution is connected with the developing of higher number of leaves, mainly from the point in Pirdop, as a partial compensation for the limited growth (Yana, Botounetc), thus the hard reduced leaf area, mainly in Yana and Pirdop. In the conditions of heavy autotraffic S. nigra individuals developed bigger growth of twigs as well as leafing, close to the control one, as compensation to the reduced leaf area. The pointed out cases of increased twigs growth probably are the confirmation to the established by some authors (An-gold, 1997; Laffray et al., 2010), that N from the exhausted gases may be acts as fertilizer too, enhancing the growth of the twigs. An increasing of the twigs growth, so the leaf area was observed for Quercus ilex L. (Gratani et al., 2000) as compensa-tion to the brief life of the leaves under transport pollution.

Paralel to leaf area reduction, it was established a weak increase of the values higher than the controls for C. mas in Pirdop (2009), so in lower degree in Yana (2010). For C. monogyna in Pirdop during 2010 year leaf area also increased com-pared to the previous years (2008, 2009), respectively 33.5% и 37.6% from K, but remained below (50%) the control. Increasing of leaf area in the conditions of in-dustrial and urban pollution was also reported by many authors (Dorogan, Djukov, 1990; Carreras et al., 1996; Gratani et al., 2000; Balasooriya et al., 2009).

CONCLUSIONS

The carried out morphological analysis showed that the studied shrub species responded to the conditions of industrial and road traffic pollution with considerable changes in the growth and development.

All three morphological indexes were appropriated for the aims of the con-ducted study, as the ‘leaf area’ was outlined as the most sensitive paramater (C. mo-nogyna, S. nigra). For C. mas the adaptation was manifested by changes in ‘growth of the annual twigs’ and ‘leaf area’. The number of leaves on the twigs’ was affected in lower degree in a comparisson with other morphological indexes, although this index could be use succesfully in the case of an industrial type of pollution: C. mo-nogyna (Pirdop) and C. mas (Yana) .

It was found a specificity of the species response depending on the type of pollution. Under industrial environmental pollution low values of the measured pa-rameters showed: C. mas (Yana), C. monogyna (Pirdop), S. nigra (Yana, Botounetc). In the conditions of high transport pollution C. mas (E. and H.Georgievi Blvd.). showed values much lower than control ones.

The minimal values of control variants in 2010 year for C. mas (concerning the number of leaves, leaf area), C. monogyna (growth of the twigs, the number of

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leaves), as for S. nigra (number of leaves, 2009), as well as the medium position of the values regarding the growth of the twigs (for all of species), confirmed the impact of another environmental factors, mainly climate, except air pollution, on the growth and development of the investigated species.

The present study determined the range of resistance of investigated species to air polution and possibility of the species usage for planting in the observed re-gions. C. monogyna (Tsarigr. Shose Blvd.) and S. nigra (Pirdop) were defined as tolerant, with higher twigs growth and good decorative effect, suitable for planting in the mentioned regions. C. mas (Pirdop, along the road Sofia-Svoge) and S. ni-gra (Tsarigr. Shose Blvd.) registered lower values of the measured indexes and thus considered as medium sensitive with recommendations for a moderate application at high level of technogenic pollution. With the lowest values, retarded growth and development C. mas (E. and H. Georgievi Blvd., Yana), C. monogyna (Pirdop) and S. nigra (Yana, Botunets) were expressed as sensitive and their use in the mentioned regions and other with similar type of pollution is unadvisable.

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