Ecologica Montenegrina 24: 58-65 (2019) This journal is available online at: www.biotaxa.org/em

Comparative Characteristics of the Greek Juniper (Juniperus excelsa Beieb.) Populations in the Southeastern Crimea

VIKTORIA YU. LETUKHOVA & IRINA L. POTAPENKO

Department of Biodiversity Studies and Ecological Monitoring, T. I. Vyazemsky Karadag Research Station – Nature Reserve of Russian Academy of Sciences, Nauki Str. 24, 298188 Feodosia, Russia. E-mail: [email protected]

Received 20 July 2019 │ Accepted by V. Pešić: 1 November 2019 │ Published online 3 December 2019.

Abstract Population studies of a relic Mediterranean species Juniperus excelsa Bieb. in the southeastern Crimea were conducted. We laid out test plots in such sites of the region: Semidvorje (a natural landmark of local significance); Kanaka (a botanical reserve of national significance); Novy Svet (a botanical reserve of national significance); Kiziltash (a natural landmark having no any conservation status); Karadag (a state nature reserve). The density of Greek juniper populations is approximately similar, varying within 400–500 plants/ha. We have estimated age structure, age index and regeneration index of studied populations. They are dominated by normal left-sided age spectra. It has been established that the current level of recreational load does not pose a threat to the existence of juniper communities: the intensity of natural regeneration is rather high. However, the threats for juniper forests may be a reduction their area due to the construction of new resort facilities and their infrastructure, as well as illegal tree cutting.

Key words: rare species, Greek juniper population, southeastern Crimea, Russia.

Introduction

The Greek juniper (Juniperus excelsa Bieb.) is a relic Mediterranean species listed on the Red Data Book of the Russian Federation and the Red Data Book of the Republic of Crimea (under the category of species with “Decreasing number”). It has a disjunctive range being distributed fragmentary over the Crimea, the Balkan Peninsula, Cyprus Island, Asia Minor, and western Transcaucasia (Miheev 2008; Fateryga 2015). In the Crimea, Greek juniper is at the northern boundary of its range, where it grows under extreme conditions. To date, the ancient Mediterranean forests have shrunk to only small groves scattered along the coast, urgently need protection. As is commonly known, the anthropogenic factor negatively affects the state of juniper open woodlands: exposed to anthropogenic impacts, these communities rapidly degrade and then recover very slowly (Fateryga 2009; Kuznetsova 2009). For this reason, almost all the communities in the southeastern Crimea are now protected and assigned one or another conservation status. However, due to the continuous tourists’ flow, the increased recreational load in summer, and too liberal interpretation of laws by the local authorities and business companies, the juniper communities still require constant monitoring.

Ecologica Montenegrina, 24, 2019, 58-65

LETUKHOVA & POTAPENKO

The goal of the work is to conduct comparative studies of the unique juniper populations in the southeastern Crimea and to identify the factors posing threat to them.

Material and Methods

The material for this publication was the data collected from various sites of natural growth of Greek juniper in the eastern part of the Crimean South Coast (Fig. 1):  Semidvorje, a natural landmark of local significance, established in 1964, having an area of 5 ha, and situated 7 km east of the city of Alushta;  Kanaka, a botanical reserve of national significance since 1987, having an area of 160 ha and situated east of the village of Rybachye;  Novy Svet, a botanical reserve of national significance since 1974, having an area of 470 ha and situated in the vicinity of the same-name village;  Kiziltash, a natural landmark in the vicinity of the village of Krasnokamenka, having no any conservation status;  Karadag, a state nature reserve since 1979, having an area of 2065 ha and situated 30 km west of the town of Feodosia.

Figure 1. Map of the research area.

Thus, the studies were conducted in the territories of four protected sites, of which two were created exclusively for the conservation of this species: Semidvorje and Kanaka (Yena et al. 2004). At each site we laid out test plots (Table 1), where the total number of Greek juniper trees was counted, population density was measured, and the inventory measurements of the oldest trees were performed according to the generally accepted techniques. The exception was the Karadag-3 plot, the unpublished data on which were provided by M.E. Kuznetsov. The sizes of the test plots at the Karadag-1 and Karadag-2 sites were smaller than usual, because the rough terrain (rocks and rock outcrops) did not allow us to establish a standard 50 × 50 m plot. In some places, the plots were laid out both in an officially protected area and beyond (Kanaka-2). Age structure of population was studied using the method of A.A. Uranov (Uranov et al. 1977). Age characteristics of plants (juvenile (Jv), immature (Im), virginyle (V), young generative (G1), middle generative (G2), old generative (G3), and senile (S)) were determined by the method of A.N. Grigorov (Grigorov 1983).

Ecologica Montenegrina, 24, 2019, 58-65 59

COMPARATIVE CHARACTERISTICS OF THE GREEK JUNIPER IN THE SOUTHEASTERN CRIMEA

Table 1. The localities' characteristics in the southeastern Crimea.

Parameters Locality Area Altitude Location Aspect Slope (°) (ha) (m) the East part of the Semidvorje 0,25 E 40 20 area

Kanaka-1 Yanturu mountain 0,25 E 50 20 Staurny Burmu Kanaka-2 0,25 SW 80 15 mountain Karadag-1 Karagach ridge 0,17 N 230 30

Karadag-2 Karagach ridge 0,17 N 200 30

Karadag-3 Karagach ridge 0,32 S 170 35 Socharchikon-Kaja Kizyltash 0,25 S 365 15 mountain the North part of the Novy Svet-1 0,25 SE 100 20 area Novy Svet-2 Sokol mountain 0,25 SW 100 25

To assess age level, the age index developed by A.A. Uranov was applied (Uranov et al. 1977). When assessing regeneration, we used the “regeneration index” (Kricsfalusy & Mező-Kricsfalusy 1994), which was calculated as the percentage of the number of plantlets, juvenile, and immature plants to the number of generative individuals. Age of trees was determined by the method of Yu.V. Plugatar (Plugatar 2011). To describe a plant community with J. excelsa, the methods of geobotanical studies were used; for this, the complete species composition of phytocenosis in the test plot, as well as its vertical and horizontal structure, was identified.

Results and discussion

By phytocenosis composition, all the communities with J. excelsa in the southeastern Crimea are divided into two groups: homogeneous thickets and mixed open woodlands (or forests). In the form of almost homogenous thickets, Greek juniper grows in Novy Svet, Kiziltash, and, to a greater extent, in Karadag, where this species can penetrate (on the northern slope of the Karagach Range) beyond the boundary of oak- ash forest, forming mixed transitional communities. Other species of woody plants are also present here (in Novy Svet, these are Pistacia mutica and Paliurus spina-christi; in Kiziltash, Juniperus oxycedrus and Quercus pubescens; in Karadag, Juniperus oxycedrus, Pistacia mutica, and Sorbus graeca), but their proportion is insignificant. The highest canopy closure was recorded from Novy Svet-1 (0.8–0.9); the lowest, from the Karadag (0.2–0.4). In Kiziltash, the canopy closure is also quite high, reaching 0.5–0.6. In Kanaka and Semidvorye, the plant communities with J. excelsa are somewhat different from those described above. Here J. excelsa is a component of oak-juniper open woodlands and forests, where its proportion decreases to 10–30%, the proportion Quercus pubescens increases to 30–50%, and there are also single Pistacia mutica trees. In Semidvorye, the understory and shrub layer is weakly expressed and is represented only by single individuals of Paliurus spina-christi, whereas the participation of understory in the plant communities in Kanaka is substantial. Here the plant cover of the shrub layer is 50–60%. It includes Carpinus orientalis, Paliurus spina-christi, Rosa corymbifera, and Pyrus elaeagnifolia.

60

LETUKHOVA & POTAPENKO

The grass layer also varies between all the investigated sites, both in plant cover and in species composition, and has its phytocenotic features. The sparsest grass cover (with about 10%) was recorded from Kanaka; the densest one, from Karadag (plant cover 90%). In Kanaka and Semidvorye, the grass layer is dominated by xerophytic gramineous plants (Festuca valesiaca and Poa annua), as well as by annual species typical of the Mediterranean flora (Alyssum umbellatum, Crucianella angustifolia, and Trigonella gladiata). In addition, Achnatherum bromoides (a gramineous plant common for the Crimean Southern Coast) dominates some sites in Semidvorje (on gentle slopes in the lower areas and foothills). The grass cover of Kiziltash most sharply differs from that of other juniper communities: here petrophytic species dominate (Asphodeline taurica, Haplophyllum suaveolens, Helianthemum nummularium, Iberis taurica, Onosma taurica, and Sedum hispanicum). The grass cover in Novy Svet is characterized by Asphodeline communities (with Asphodeline taurica at the Novy Svet-1 site and with A. lutea at Novy Svet-2), which, in turn, are a special variant of petrophytic steppes. Other species present here are as follows: Bothriochloa ischaemum, Festuca valesiaca, Stipa sp., Alyssum obtusifolium, and Teucrium polium. In Karadag, xerophytic gramineous grasses dominate herbaceous communities on the southern slopes (Festuca valesiaca, Elytrigia maeotica, and Bromopsis cappadocica); on the northern slopes, the grass layer is formed by species characteristic of meadow-like and true steppes (Alopecurus vaginatus, Millium vernale, Poa bulbosa, Stipa pontica, as well as Filipendula vulgaris, Myosotis micrantha, Pyrethrum corymbosum, and Viola kitaibeliana). The results of the studies at the test plots are presented in Table 2. The density of Greek juniper populations in them is approximately similar, varying within 400–500 plants/ha. The exception was the plots in Novy Svet and Karadag. The high population density at Novy Svet-1 is related with the large proportion of pre-generative individuals (more than 50%). The low density at Novy Svet-2 and Karadag-1, in our opinion, can be explained by the fact that these plots were laid out in the transitional juniper communities near the pine plantations (Novy Svet-2) or at the boundary of the oak-ash forest (Karadag-1).

Table 2. Characteristics of J. excelsa populations in different localities.

Population parameters Population density (plants Locality Reproduction per ha) Age index index (%) 1* 2* 3* 4* Semidvorje 316 140 0 456 0,19 160 Kanaka-1 416 68 0 484 0,16 453 Kanaka-2 468 33 0 501 0,12 950 Karadag-1 177 53 0 230 0,20 278 Karadag-2 277 165 0 443 0,26 89 Karadag-3 43 515 36 594 0,49 0 Kizyltash 92 384 0 476 0,55 5 Novy Svet-1 616 440 12 1068 0,31 115 Novy Svet-2 56 188 44 288 0,53 15

1* – density of pregenerative plants; 2* – density of generative plants; 3* – density of postgenerative plants; 4* – general population density.

The lowest age index was observed in Kanaka (0.12–0.16), which indicates a predominance of pre- generative individuals in the population; the highest, in Kiziltash (0.55). Almost all the sites showed high values of intensity of regeneration of J. excelsa. The highest regeneration index was recorded from Kanaka (453–950%); the lowest, from Karadag-3 (0%) and Kiziltash (5%). On average for the southeastern Crimea, the regeneration index of J. excelsa was 256%, which is a very good value. An analysis of the age spectrum has shown that all the populations studied are normal, but incomplete in members (Figs. 2–4). As follows from the figures, most of the populations have a pronounced left-sided spectrum: their composition is dominated by pre-generative individuals. At three plots (Kiziltash, Karadag-3, and Novy Svet-2), the populations have a right-sided spectrum, with their composition dominated by generative plants.

Ecologica Montenegrina, 24, 2019, 58-65 61

COMPARATIVE CHARACTERISTICS OF THE GREEK JUNIPER IN THE SOUTHEASTERN CRIMEA

Figure 2. Age structure of the J. excelsa populations in Semidvorje and Kanaka.

Figure 3. Age structure of the J. excelsa population in Karadag.

Thus, most of the J. excelsa populations studied show a good natural regeneration, with generative plants providing abundant self-seeding capable of germination and survival throughout the period of so- called “shadow phase” in their development (when young plants grow under the canopy of mature trees). The exception was the population in Kiziltash and at Karadag-3, where the lowest regeneration index was recorded. In our opinion, the low value of the index here is associated with extreme growth conditions, where juniper suffers, first, moisture shortage. This opinion is shared by other authors also (Kuznetsov 2009). With transition to the “light phase” of development (when grown-up plants emerge through the canopy), plants come into competition with generative ones, due to which the number of virginal individuals naturally decreases. This becomes particularly pronounced in the homogeneous juniper communities, characterized by high canopy closure (Novy Svet, Kiziltash, Karadag-3). In the mixed oak and juniper communities (in Semidvorje and Kanaka), the decrease in the proportion of virginal individuals is not so sharp, since oaks do not form dense and closed canopy, and under them young juniper plants can normally grow and develop.

62

LETUKHOVA & POTAPENKO

Figure 4. Age structure of the J. excelsa populations in Kizyltash and Novy Svet.

The oldest juniper trees in the southeastern Crimea were found in the Kanaka populations. At the studied plot, there are two trees with a trunk diameter of 90 and 95 cm, which correspond to an age of more than 700 years. The oldest trees at the sites of Novy Svet, Kiziltash, and Semidvorje have trunk diameters of 67 cm, 56 cm, and 59 cm, respectively; these trees reach, respectively, 6.5 m, 7 m, and 12 m in height. Thus, the age of the trees is estimated at ca. 500 years. In Karadag, the oldest trees have a trunk diameter of 20–25 cm, a height of 6–7 m, and, correspondingly, their age is ca. 200 years. The study of the structure of the J. excelsa populations at the permanent test plots in the southeastern Crimea did not reveal any effect of the anthropogenic factor on them. However, it should be taken into account that, when selecting sites, we paid attention primarily to the sites typical of the entire population, and did not lay them out in places with increased anthropogenic load (near ecological paths or tourists’ attractions). First, the area of these test plots is relatively small compared to the entire population range. Second, the effect of recreational load on the regeneration and age structure of Greek juniper in the Crimea has already been studied in detail by other authors (Tyagniryadno 2009; Fateryga 2009; Fateryga & Krainyuk 2009). These studies show that, even in places frequently attended by tourists, the general trend in the condition of the populations is quite favorable. For example, at various stages of recreational degression in the Kanaka and Novy Svet populations, the regeneration index varied from 71 to 180 (Tyagniryadno 2009). At the same time, similar studies, conducted 30–40 years ago, provided less optimistic results (Grigorov & Gramotenko 1984). Then, an examination of the Greek juniper open woodlands in Kanaka showed that their age spectrum was dominated by generative plants, and a significant part of plantlets and undergrowth were in a depressed state and drying out. The main economic activities that posed threat, according to the authors, were cattle grazing, tree cutting, recreational use of territories, expansion of the area of resorts constructed, and terracing of slopes. Over the past period, it became possible to eliminate some of these factors, and this has positively influenced the condition of the juniper communities. For example, due to the closure of sheep farms in the territory of Kanaka, the area of the juniper population here began to expand, and the species is currently occupying new areas: only pre-regenerative and young generative plants are found outside the botanical reserve, on the other side of Kanaka glen, on Mount Staurny Burmu (where the Kanaka-2 plot was laid out) (Fig. 1). Operations on slope terracing and planting alien trees have also been ceased. However, the other factors still exert their influence today. Of the most threatening ones are the construction of infrastructure and the expansion of territories of resorts and recreation centers intruding into the juniper communities. Unfortunately, most of these communities grow in the lower maritime zone, which is very attractive for resort construction. Despite most juniper woodlands are now protected, there are objects illegally built within their boundaries. We observed such situation in Novy Svet, Kanaka, and Semidvorje. It frequently occurs that illegal construction does not stop even on very steep slopes and on screes. In addition, illegal cutting of juniper trees still continues, as handcrafts made from juniper are in high demand among tourists and visitors of the Crimea. Thus, in spite of the fact that the juniper communities of the southeastern Crimea are quite well protected by the nature conservation laws,

Ecologica Montenegrina, 24, 2019, 58-65 63

COMPARATIVE CHARACTERISTICS OF THE GREEK JUNIPER IN THE SOUTHEASTERN CRIMEA

these are not always fully implemented in practice. Only the strict compliance with the regulations of the Russian Federation and the environmental education of the local population will help preserve these unique wild habitats in the Crimea.

Conclusions

1 - By phytocenosis composition, all the communities with J. excelsa in the southeastern Crimea are divided into two groups: almost homogeneous thickets (presence of other species here is insignificant) and mixed open woodlands, where J. excelsa is a component of oak-juniper communities (with the juniper proportion of 10–30% and the proportion of Quercus pubescens of 30–50%). The grass layer varies between all the investigated sites both in projective cover and in species composition. 2 - The populations under study are dominated by normal left-sided age spectra; the populations with right- sided spectra have been found in Kiziltash, as well as at the Karadag-3 and Novy Svet-2 sites. A high regeneration index has been recorded from all the test plots in the southeastern Crimea (except for the Karadag-3 and Kiziltash sites). Its average value is 256%. 3 - Most juniper communities in the southeastern Crimea are characterized by a weak anthropogenic disturbance; many have begun to recover after the cessation of cattle grazing. Of modern threats, the construction of resort facilities and illegal tree cutting should be specially noted.

Acknowledgements. Work was supported by the research project of T.I. Vyazemsky Karadag Scientific Station – Nature Reserve of RAS (№ АААА-А19-119012490044-3).

References

Fateryga, V.V. (2015) Greek juniper (Juniperus excels M. Bieb). In: Yena, A.V. & Fateryga, A.V. (Eds). Red Book of the Republic of Crimea: plants, algae and fungi. IT “Arial”, Simferopol, p. 64. (in Russian). Fateryga, V.V. & Krainyuk, E.S. (2009) Determination of recreation deformation of grass cover in juniper forests in eastern part of the South Coast of the Crimea. Ecosystems of Crimea, their Optimization and Conservation. Thematic collection of scientific papers. 19, pp. 24–32. (in Russian) Fateryga, V.V. (2009) Condition of high-juniper forests of Crimean South coast with different recreational load. In: The Nature Reserves of Crimea. Theory, Practice and Perspectives of Conservation Business in Black Sea Region. Materials of the 5th International Scientific-Practical Conference (Simferopol, 2009, October 22–23), SPD Baranovsky, Simferopol, pp. 245–249. (in Russian) Grigorov, A.N. & Gramotenko, A.P. (1984) Open woodlands of Juniperus excelsa in Natural Boundary Kanaka. In: Natural Ecosystems of Southern Coast of the Crimea and their Conservation. Collected Scientific Works. 94, 46–55. (in Russian). Grigorov, A.N. (1983) Greek juniper (Juniperus excelsa) in the Crimea (Bioecological properties, regeneration and protection). Thesis for the Degree of Candidate of Biological Science. the Nicita Botanical Garden, Yalta, 22 pp. (in Russian). Kricsfalusy, V.V. & Mező-Kricsfalusy, G.M. (1994) Population Biology of Plants: manual for higher school students of biology. Univ. Press, Uzhgorod, 80 pp. (in Ukrainian). Kuznetsov, M.E. (2009) Estimation of condition of the Juniperus excelsa Bieb. populations at protected areas of the South-eastern Crimea region. In: Gaevskaya, A.V., Morozova, A.L. (Eds.) Karadag – 2009: Collection of scientific papers dedicated to the 95th anniversary of the Karadag Research Station and 30th anniversary of the Karadag Nature Reserve of the National Academy of Sciences of Ukraine. ECOSI-Gidrofizika, Sevastopol, pp. 109–115. (in Russian) Kuznetsova, E.I. (2009) Juniper forests and woodlands of the Abrau Peninsula (the North-Western Caucasus). Moscow University Bulletin. Series 5. Geography, 2, 76–80. (in Russian).

64

LETUKHOVA & POTAPENKO

Miheev A.D (2008) Greek juniper (Juniperus excels Bieb). In: Trutnev, Yu.P. (Ed.). Red Data Book of Russia Federation (plants and fungi). Tovarishchestvo Nauchnyh Isdanii KMK Publ., Мoscow, pp. 552–553. (in Russian). Plugatar, Ju.V. (2011) The methodics of determination of the trees age. Scientific Notes of the “Cape Martyan” Nature Reserve. 2, 122–148. (in Russian). Tyagniryadno, V.V. (2009) Regeneration of Greek juniper during recreation in Eastern Crimea. Bulletin Taras Shevchenko National University of Kyiv, 25–27, 8–10. (in Russian). Uranov, A.A., Zaugolnova, L.B., Smirnova, O.V. and oth. (1977) Plant cenopopulations (development and relationships), Nauka, Moscow, 131 pp. (in Russian) Yena, V.G, Yena, Al.V. & Yena, An.V. (2004) Protected Landscapes of Tavrida. Business-Inform, Simferopol, 424 pp. (in Russian).

Ecologica Montenegrina, 24, 2019, 58-65 65