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Biuletyn Ogrodów Botanicznych, 12: 11–22, 2003

THE DISTRIBUTION OF LIGULARIA SIBIRICA (L.) CASS. IN AND CHANGES IN ITS POPULATION

Rozmieszczenie Ligularia sibirica (L.) Cass. w Estonii i zmiany jej populacji

Ülle KUKK

Environmental Protection Institute of the Estonian Agricultural University, Akadeemia 4, 51003 Tartu, Estonia

ABSTRACT 1992; Roosaluste and Kukk T. 2001). Objective reasons can come from the age of taxon, bio- The distribution of Ligularia sibirica (L.) logical and ecological peculiarities, and the Cass. has considerably diminished in the recent location inside the borders of distribution area, 30 years in Estonia. Using herbaria, literature, the relic status etc. Subjective reasons can be and 8-year monitoring data a distribution map of caused by several forms of human activities different periods is presented in the article. The influencing and changing habitats, by cessation analysis of the monitoring data indicates the of the management of semi-natural habitats, or diminishing of the size and vitality of the major- by direct physical destruction of . ity of preserved subpopulations. The cessation of Usually, the reasons do not function alone but mowing and grazing, in addition melioration and are closely connected. However, for making pollution of habitats in floodplain and paludified recommendations for conservation it is essen- grasslands have caused their overgrowing with tial to know them. The basic biological data is a shrubs and forest, which is suggested as the main ground for management decisions. reason of the decrease. The location of Ligularia The aim of the present study is to compare sibirica on the border of distribution area as an the past and current distribution and habitat affecting agent has been discussed as well. descriptions of Ligularia sibirica in Estonia; and analyze the data of ecology and population KEY WORDS: Ligularia sibirica (L.) Cass., dynamics, to elucidate the situation and main distribution, population size, monitoring, habi- reasons for the changes. tats, land use. MATERIAL AND METHODS INTRODUCTION and general distribution Siberian groundsel (Ligularia sibirica (L.) Ligularia sibirica is a stout 100–130 (even up Cass.) is one of the species that has become the to 170 cm) tall perennial from the family centre of attention in the western part of its dis- Compositae (Fig. 1). The rhizome is short and tribution area. Its rarity in most Eastern and thick, its stems erect, mostly not ramified. The Central European countries (Appendix 3., 1999) lower leaves are kidney-shaped, long-stalked and has impelled us to set about studying and moni- sheathing at the base, to 30 m across, all toothed, toring it, elucidate the reasons for the decrease the upper leaves are much smaller and stalkless. and to find the best conservation measures. The Numerous yellow flower heads stand in a spike- number of localities in Estonia has always been like cluster. The seeds are supplied with pappus. small and has continually diminished in the past Ligularia sibirica is widely distributed in the decades. The current situation demands quick continental zone of Eurasia. The main distribu- reaction and active conservation measures to tion area is the European part of and the maintain the localities still preserved. Siberian taiga zone, reaching the southern coast There are several reasons why plants are of the Okhotsk Sea and Yakutia (Hultén & Fries rare. Generally the reasons of their rarity can be 1986, Poyarkova 1961). The species occurs, but divided into two groups (Fiedler and Ahouse is not threatened, in Murmansk and Pskow

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of local literature (Eichwald 1937, Frey 1965, Kukk Ü. 1999, Laasimer 1978, Sammul 2001), the database of the Environmental Protection Institute of the Estonian Agricultural University, the herbarium specimens stored in the Institute of Zoology and Botany of the Estonian Agricultural University and Tartu University, and the data of inventory of old localities of rare plants. In 1969, the first inventory of them was started in Estonia, and it has been continued regularly. A distribution map of Ligularia sibiri- ca has been compiled using the UTM grid sys- tem (the size of the grid squares of 10 × 10 km within the 50 × 50 km quadrangles). The populations of Ligularia have been inventoried repeatedly since 1983. Germination tests were carried out in 1985 and 1986. In 1994, systematic monitoring was started. We intended to find out: a) the extent and tendency of the changes in population size and viability, Fig. 1. Ligularia sibirica (L.) Cass. in Southern Estonia. b) the reasons of changes which have happened both to population and habitat. Therefore, in 1994–1996 permanent monitoring plots with regions, but it is endangered in the northern part the size of 10 × 10 m were established in four of Leningrad region (Kotiranta et al. 1998). It is sites, named after the names of villages: Anne, mainly confined to Eastern , being very Sootaga, Väägvere and Tagula (Fig. 2). The rare in , , , Byelorussia, plot location was chosen in the spots of the , Czech and Slovak Republics, mean frequency of specimen what was estimat- , , , and ed visually. On the figures the sites were (Andru‰aitis 1985, Hegi 1987, Kneblová 1950, marked with the first letter(s) of the site name: Procházka & Pivniãková 1999, ·egulja & Krga A, S, V, T. The rest of the sites (Edise, Jõhvi, 1990, Fischer 1991, Olaczek 2001). According Kikaste, Õisu) where the number of plants was to Hegi (1987), the represents the subarc- small were studied without plot establishment. tic-Siberian element in the Central European Flora. The species does not occur in , and Scandinavia, and in the great part of West European countries (Ingelög et al. 1993). Estonia remains on the border of its con- tinuous distribution area, and Ligularia sibirica is considered a relic from the boreal climatic period. The species is included in the Red Data Book of Estonia in Category 1 (endangered), and since 1936 it has been legally protected. Since 1994, it has been strongly protected in Category I (Kukk Ü. 1999). In Estonia, there are three categories of species protection, consider- ing the degree and specific features of a pro- Fig. 2. The distribution of Ligularia sibirica (L.) tection regime. Cass. in Estonia. G existing localities Monitoring methods ✚ extinct localities The available information about the distribu- monitoring sites tion of Ligularia sibirica is based on the sources A, S, T, V signs of the monitoring sites

12 The distribution of Ligularia sibirica (L.) Cass.

The sites were monitored with the interval of Ligularia sibirica has been found in 17 1 to 3 years. The habitat description includes UTM squares. If the minimum distance vegetation type, the coverage (in percent) of between two different subpopulations is deter- shrub and herb layers, the list of associated herb mined to be at least one km, 18 localities have species and their abundance on a 5-point scale, been found altogether. More than a half of them growth conditions, surrounding habitats, and have disappeared since 1969. At present, 8 sub- the sources of human impacts. The habitats populations are known, placed in six 10 × 10 were classified into site types according to the km squares (Fig. 2). Still existing sites of hierarchical classification of natural habitat Ligularia sibirica are located in eastern and types compiled by Paal (1997). Soil properties southern part of Estonia only, the distribution were estimated on the basis of Paal’s classifica- line goes in NE-SW direction through the main- tion (1997). Light conditions of habitats were land of Estonia. Approximately half of the estimated on visual basis. The habitats were localities have vanished and some of the pre- divided into open (no shade), semi-open (partial served ones are very small. shade) or closed (total shade). The area of population, the total number of Life cycle plants (when possible), and abundance in a com- The beginning of Ligularia sibirica vegeta- munity were the parameters recorded. The tion falls into the end of April or the beginning population size was counted at every monitor- of May, when a basal leaf rosette develops. The ing time (4 to 7 times) in four sites, and two flowering period starts in the middle of July and times in all localities. In the monitoring plot all lasts till the middle of August. The seeds ripen tussocks were counted, and coverage (in per- at the end of August or in September and spread cent) was estimated. The number and height of usually by wind. Distribution by animals is also generative shoots in tussock, the proportion of possible. The data of the seed germination abili- different life cycle stages (vegetative, genera- ty are different: according to our experience it tive, juveniles) were counted; the type and level was very low in open ground, and reached about of damages, and viability of plants were record- 50% in greenhouse conditions. Procházka and ed on a 3-point scale. The analyzed parameters Pivniãková (1999) have given much higher ger- were: the total number of specimens in every mination ability in the . subpopulation; the number of specimens in Vegetative reproduction is possible by rhizome a plot (100 m2); the proportion of flowering splitting, but it is ineffective because of its slow plants, vegetative adults and seedlings; the growth, which is about 6 mm per year (Sammul, number and height of flowering shoots in a tus- unpublished). At the same time, this could sock. In data analysis, the population indexes explain why Ligularia sibirica often grows in were calculated so that the first recorded esti- clumps from 2 to 5 perennial ramets. Ramifying mate has the value of 100, which the following of the rhizome is connected with flowering. estimates were compared to. A new bud forms on the rhizome of a flowering ramet. The life span of a genet may be about 10 RESULTS years. The biology of Ligularia sibirica still needs additional study. Distribution in Estonia The first data about the plant go back to the Habitats beginning of the 19th century (Germann 1807) In general Ligularia sibirica grows in paludi- when Ligularia sibirica was found in the sur- fied grasslands and shrubberies, forest plains, roundings of Tartu town. The next data about minerotrophic fens and floodplain grasslands, the findings in Southern and North-Eastern which are its favoured habitats elsewhere in Estonia come from the end of the 19th and the Eastern and Central Europe (Pax 1898 and beginning of the 20th century (Lehmann 1895, 1908, Braun-Blanquet 1928 from ·egulja & Lippmaa 1932, Eichwald 1937, Precht 1938, Krga, 1990). In Estonia the habitats of the Frey 1965, Laasimer 1978 etc). The most recent species are not calcareous. finding is from 1995 in South Estonia, and a new The Estonian habitats belong to the type addition to it was discovered in 2002. classes of floodplain forests and grasslands,

13 Ülle Kukk paludified grasslands, and mires. The list of them (Jõhvi) is threatened by a dumping ground accompanying species in Estonian habitats is nearby. A common feature for all the sites is presented in the Appendix. Half-open spots that they are not grazed and mowed any more, near the shrubs and trees seem to be favoured, and overgrowing with shrubs and forestation but the plants feel well in scanty open areas as takes place with an increasing speed. well. Soils of Estonian habitats are rather acidic. In Anne site the habitat type has been deter- Alluvial soils and gley-podzols may be distin- mined as floodplain grassland, with main fea- guished. Both alkaline soil (·egulja & Krga tures of Geranio palustris-Filipenduletum and 1990) and acidic soil habitats (Procházka & Calamagrostietum canescentis. In 8 years Pivniãková 1999) have been found in Central noticeable changes in the species composition Europe. have taken place (Appendix). Several new hemerophilous species as Artemisia spp., Analysis of monitoring data Urtica dioica, Rubus idaeus have been added. The population size of Ligularia sibirica A probable cause may be fire spreading across has been counted at every monitoring time (4 to dry grass in springs. Serratula tinctoria grow- 7 times) in four sites and two times in all the ing in the same habitat seems to supress localities. In three sites the number of plants Ligularia sibirica. Its abundance and coverage was estimated in hundreds – the numbers were is increasing every year. The influence of me- ~400 to ~800. In two sites the sizes decreased lioration (communication channels nearer than within 9 years accordingly from 111 to 29, and 300 m, and ditches) is obvious, though it was from 96 (in 1996) to 60 (in 2002). carried out years ago. Mowing has ceased in the Three localities were small and in 2001 they site and overgrowing with shrubs and trees is consisted of a few plants only. The populations taking place. have decreased considerably within the recent Väägvere and Sootaga sites could also be 20 years. Two sites have meliorated, but they considered as wet floodplain grassland site have remained without use, and have over- types as well, but the more exact community grown with shrubs and trees, one site has been determination is quite difficult because of the damaged by rubbish and pollution, and has afforestation process. Floodplain willow shrub- decreased three times compared to 1969. bery dominates in Väägvere site. In the herb Altogether, the number of tussocks found in layer Phragmites communis and Calama- Estonia is approximately 1600. More than 90% grostis canescens are more and more dominat- of them grow in three localities. ing. High-growing herbs/graminoids and over- The number of tussocks on the plot repre- growing with shrubs have strongly worsened sents the average situation of the subpopulation. light conditions. In Sootaga site a paludified The changes in Anne site were especially con- Filipendula ulmaria birch forest is developing spicuous between 1994 and 1997. Then the instead of a grassland. The tendency to over- monitoring interval was shortened to one year. growing was especially noticeable during the The number of specimens diminished steadily, last monitoring times in 2001 and 2002. and the population index in 2001 was 20 in In Tagula site Geranio palustris-Fili- comparison with 1994 (the number of tussocks penduletum and Caricetum paniceae-nigrae was lessened five times). In Väägvere site alongside with Filipendula ulmaria birch forest indexes of 130, 150 and 63 were fluctuating; in dominate. The herb layer is rich in species and Sootaga site the indexes of 86 and 60 indicated lush, the first signs of overgrowing with wil- a decrease as well. Only in Tagula site the lows have been revealed. Though, the light rich indexes 169 and 356 indicated the increase. patches seem to be more favoured. The Õisu Comparing the data of different subpopulations site could be determined as pine swamp forest, the tendency is downward everywhere except with stunted Picea abies, Betula pubescens and in Tagula site, which reveals a distinct increase, B. humilis. and there are fluctuations in Väägvere site. The habitats of the smaller subpopulations The population density (number of tus- could be determined as paludified or floodplain socks/m2) has been very low in Anne site and grasslands of transitional stage to forest. One of decreased even 5 times in 7 years: from 0.35 to

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The distribution of Ligularia sibirica (L.) Cass. 3 4 cd. / cont. Appendix 33 23 22 23 2 134 233 x x32 3 224 333 333 333 222 222 22 333 222 222 322 333 x 22 1 3

44554 344 544 2 2 223222 2443223222 222333 333 333243 344 x 122 333 33334 2224 34 234567 8910111213141516171819 AAAAAA S SS TTTVVVVÕÕ 1994 1997 1998 1999 2000 2001 1996 1998 2001 1994 1997 2000 1994 1997 1999 2001 1996 2002 1 Sign of Site Species/year Acorus calamus Aegopodium podagraria Agropyron repens Anemone nemorosa Angelica sylvestris Anthriscus sylvestris Artemisia vulgaris stricta Betula humilis Briza media Calamagrostis canescens Calamagrostis stricta Caltha palustris Campanula glomerata Carex acuta Carex cespitosa Carex filiformis Carex flava Carex hostiana Carex inflata Carex nigra Carex panicea Centaurea jacea Cirsium heterophyllum Cirsium oleraceum Crepis paludosa Dactylorhiza fuchsii Dactylorhiza incarnata Deschampsia cespitosa Accompanied species on different sites and years.

17 Ülle Kukk 1 23 33 322 2 2 34422 22 xxx 2333222 2 x x2 22434 22 11 222 422 3444 x 232 22 2x2323233323 2 441 222 22 x3 22 44x2x 3x 44 454454 4444443x x3 22222 33334x 333222 323 xx 333222 333 x 3 234567 8910111213141516171819 1 Ranunculus acer Epipactis palustris limosum Equisetum palustre Equisetum pratense Eriophorum angustifolium Festuca pratensis Filipendula ulmaria Galeopsis speciosa Galium boreale Galium mollugo Galium palustre Geranium palustre Inula salicina Juncus bufonius Lathyrus pratense Listera ovata Luzula pallidula Lysimachia vulgaris Lythrum salicaria Melampyrum nemorosum Melica nutans Molinia coerulea Orobanche pallidiflora Pastinaca sylvestris Peucedanum palustre Phragmites australis Pimpinella major Polygonatum multiflorum Polygonum bistorta Potentilla anserina Potentilla erecta

18 The distribution of Ligularia sibirica (L.) Cass. 34 1 xxxx xxxx 1 3 222 123 233 xxxxxxxx x xx xxx 22 23 333 x 32 2 333333122 33334 33 454454 332443 333333223 3332 222xx xxxxx x 222 xxxxxxxxxx xxxxxxxxxx 234567 8910111213141516171819 1 Pinus sylvestris Rubus idaeus Rubus saxatilis Rumex acetosa Scirpus sylvaticus Serratula tinctoria Sesleria coerulea Succisa pratensis flavum Thalictrum lucidum Trollius europaeus Tussilago farfara Valeriana officinalis Veronica longifolia Vicia cracca Viola canina Viola epipsila Viola palustris Salix spp. Frangula alnus Padus avium Rhamnus catharcticus Sorbus aucuparia Populus tremula Betula pendula Picea abies “Explanation of signs: A, S, V, T, Õ – abbreviations of the names of sites; 1, 2, 3, 4, 5 – estimation of abundance; x – mark of occurrence”

19 Ülle Kukk the other hand Ligularia sibirica is viable in The more frequent occurrence near the shrubs Austria (Fischer 1991), but climatic conditions noticed already by Eichwald (1937) could be in mountainous region can be very different and explained with the intensive use of grasslands incomparable to those in Estonia. for grazing and mowing in the active farming All the parameters measured or estimated period (the first part of the 20th century). The during the monitoring show the continuing only areas for surviving turned out to be the decrease of Siberian groundsel in Estonia. In edges of shrubberies. At that time much more the majority of subpopulations, especially when manual work was used in farming (mowing the light conditions have worsened, the rela- with scythes, small-power machinery etc). tionship between the development stages is Open and half-open habitats suitable for seed changing steadily towards the increase of the dispersal formed much greater part of grass- number of vegetative plants and the decrease of lands. Later, after the collectivization of agri- generative plants and juveniles. The seed pro- culture the grasslands remained without use, duction and sexual reproduction diminish in formation of shrubberies started and open areas shade. Vegetative reproduction via ramification decreased during the years. of rhizome does not represent an effective way Franklin (1980) has suggested that popula- for reproduction. tions with effective sizes of 500 or more would Low germinating capacity of seeds and slow be sufficient to maintain long-term evolutionary vegetative reproduction do not favour plant dis- potential. Lande (1995) has argued that even an persal as well. Seed production proceeds in effective size of 5000 is required. Generally, some sites only, and even if it happens, the dis- effective population sizes are substantially persal of seeds is complicated because of close lower than actual population sizes because of plant association and thickened undergrowth. the fluctuations in size (Lande 1995). In this A dense and high herb layer does not create case, only three subpopulations of Ligularia good conditions for germination in a site as sibirica could be able to survive in Estonia. well. Besides, there could be biological causes Therefore, without careful management and as allelopathy or mycorrhiza, which can have protection Ligularia sibirica could vanish dur- an essential effect on seed germination and root ing the next decades at least in most of its habi- growth. Root and shoot competition can be one tats. A protection and management plan has presumable reason for decrease (Ligularia- been compiled and according to it clear cutting Serratula relations in Anne site). A vast majo- and mowing are the most essential management rity of vascular plants have mycorrhizal associa- measures foreseen for the improvement of the tions with fungi (Silvertown & Lovett Doust demographic situation. A parallel monitoring 1995), and plant-plant interactions should should evaluate the success of management become a subject for further study. activities. A single reason cannot be pointed out for the decrease of the Ligularia sibirica population in ACKNOWLEDGEMENTS Estonia. Taking into account all the circum- stances discussed above, the survival of The author wishes to thank the colleague Ligularia sibirica can be influenced by both E. Hurt for help by monitoring and composition phytogeographical and biological reasons. of figures, and M. Sammul for the new infor- However, the main reason of the diminution of mation about distribution data. Many thanks to the size and viability of subpopulations seems A. Kalda and J. Truu for useful advise by habi- to be caused by the changes in growth condi- tat and other data analysis and K. Muoni for the tions. The plants survive in more open habitats, revision of English. but suffer in shade, especially flowering and fruiting cease. The only subpopulation where REFERENCES the number of individuals has increased and the proportion of life stages is in balance grows in Andru‰aitis G. (ed.) 1985. Latvijas PSR SarkanÇ a paludified grassland near a stream and spring grÇmata. Riga, ZinÇtne, pp. 1-526. fen where water and light conditions remain Appendix 3. Implementation of Recommendation quite stable due to slow overgrowing process. No. 40 (1993) concerning species in Appendix

20 The distribution of Ligularia sibirica (L.) Cass.

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