161 Pillwort-Pilularia-globulifera-L.-in-Lower-Silesia 161 Pillwort Pilularia globulifera L. in Lower Silesia biology and ecology EWA SZCZÊŒNIAK 1, ANDRZEJ SZLACHETKA 2 1) Institute of Plant Biology, University of Wroc³aw, Kanonia 6/8, PL-50-328 Wroc³aw, Poland; e-mail: ewaszcz@biol.uni.wroc.pl 2) Parszowice 81, PL-59-300 Œcinawa, Poland; e-mail: andrzej-szlachetka@wp.pl ABSTRACT: Pilularia globulifera is an endemic species of the sub-atlantic part of Europe, critically endangered in Poland. In Lower Silesia, it has not been reported since 1903. Two new locations were found in the Bory Dolnoœl¹skie district in 2007 and the bigger population of Pilularia became an object of detailed research. Pilularia forms there a dense mat, specimens are vigorous and produce sporocarps. Gametophytes and young sporophytes developed properly. This species forms its own plant community Pilularietum globuliferae R.Tx. 1955 ex Müll. et Görs 1960 and also occurs in rushes of Phragmites australis. ABSTRAKT: Pilularia globulifera jest gatunkiem endemicznym subatlantyckiej czêœci Europy, w Polsce krytycznie zagro onym wymarciem. Na Dolnym Œl¹sku nie by³a notowana po 1903 r. W 2007 r. dwa nowe stanowiska gatunku zosta³y odnalezione w okrêgu Bory Dolnoœl¹skie, populacja z wiêkszego stanowiska objêta zosta³a szczegó³owymi badaniami. Ga³uszka tworzy gêst¹ matê, jest ywotna i wytwarza sporokarpia. Gametofity i m³ode sporofity rozwijaj¹ siê prawid³owo. Gatunek tworzy w³asne zbiorowisko Pilularietum globuliferae R.Tx. 1955 ex Müll. et Görs 1960, ponadto wystêpuje w szuwarze Phragmites australis. KEY WORDS: water ferns, endangered species, Pilularia globulifera, gametophytes Introduction The genus Pilularia (Marsiliaceae) is represented by 6 species of extremely unusual ferns distributed in North and South America, Europe, Pacific Islands, in New Zealand and Australia. Pillworts are coastal or submerged aquatic plants with the numerous cylindrical, lacking blade leaves. The name Pilularia comes from a Latin word pilula, which means a small ball or pill, in reference to the shape of heterosporous sporocarps. SZCZÊŒNIAK E., SZLACHETKA A. 2008. Pillwort Pilularia globulifera L. in Lower Silesia biology and ecology. In: E. Szczêœniak, E. Gola (eds), Club mosses, horsetails and ferns in Poland resources and protection. Institute of Plant Biology, University of Wroc³aw, Wroc³aw, p. 161 171.
162 Ewa-Szczêœniak,-Andrzej-Szlachetka 162 Pilularia globulifera is a European endemic species originally occurring throughout much of the western European lowlands, from southern Scandinavia to the Iberian Peninsula (Page 2004). In Poland, it occurred in western and north-western part (Zaj¹c, Zaj¹c 2001). The occurrence of this sub-atlantic species is now highly reduced. Its number has already declined thus, the species is regarded as critically endangered in Poland ( ukowski, Jackowiak 1993, 2001; Zarzycki, Szel¹g 2006). Pilularia globulifera has not been observed in Lower Silesia since the beginning of the 20 th century and therefore it was included into the regional red list as the regionally extinct species (RE; K¹cki et al. 2003). In 2007, two locations of this species were discovered: a small and vegetative one in a fish pond near Rokitki (Spa³ek 2009), covered by water in 2008; and the bigger one, including plants producing spores, in two neighbouring ponds in the Chocianów Forest District. According to the geobotanical division, both populations are located in the Bory Dolnoœl¹skie District (Kuczyñska 1997). 1. Material and methods Biology and ecology of the species were studied in 2007 and 2008 in the population existing in the Chocianów Forest District. The main objects of this research were to establish morphology and phenology of fern, production of sporocarps, viability of spores, development of gametophytes and young sporophytes, associations with the plant communities, and the way of wintering. Twenty sporocarps were collected twice, before and after the first ground-frost; then, spores and gametophytes were cultivated in distilled water in room temperature. Images of gametophytes were taken in the Department of Morphology and Plant Development, Institute of Plant Biology, University of Wroc³aw. Relevés were recorded using the Braun-Blanquet (1964) method. The phytocoenoses were identified to the plant communities according to Matuszkiewicz (2008). The nomenclature of vascular plants used in this study is given after Mirek et al. (2002). The map of plant distribution was generated using GNOMON software, in 10x10 km squares of the ATPOL grid (Zaj¹c 1978). 2. Species characteristics Pilularia globulifera is a perennial plant, aquatic to helophytic, rooted in the submerged substrate. Adventitious roots and leaves arise at nodes of farcreeping rhizomes, that may reach the length of 50 cm. Roots are long, slen-
163 Pillwort-Pilularia-globulifera-L.-in-Lower-Silesia 163 der, pale-brown and mostly unbranched. Yellow-green leaves are cylindrical, slender, young ones delicate and circinately coiled, adult erect and succulent, about 1 mm in diameter near the base. Sporocarps arise at the base of petioles on unbranched stalks, c. 1 3 mm long. Sporocarps are globose, hard, about 3 mm in diameter, brown, hairy when young but smooth when mature, divided by the indusia into 4 compartments, each containing one sorus. One-spored megasporangia and many-spored microsporangia occur in the same sorus and are released in a mass of mucilage. Gametophytes (prothalli) are endosporic and reduced. 2n=26. Pilularia occurs in shallow water of ponds and temporary pools, and on reservoir margins, where it could form dense mats (Jalas et al. 1999; Page 2004; Watson, Dallwitz 2004). Plants vary in size, and most of this variation seems to be environmentally induced (Page 2004). 2. Results A stand found in 2007 in the Chocianów Forest District is situated in two anthropogenic forest ponds. They have been dug in the wet valley of the small stream and are supplied by the stream, as well as oligotrophic water coming from the drainage system. A southern pond contains more mineral and organic compounds, its bottom is cover by silt and Pilularia occurs there only in the small sandy area in its northern part. A northern pond is poorer and shallower; almost its entire bottom is sandy, only partially covered with the thin layer of mud. Pilularia occurs there in the open sandy banks and at the bottom, in shallow water. The area of the formed mat depends on the water level: in November 2007 it covered more than 1000 m 2, in November 2008 the water level was higher and Pilularia covered only a half of that area. In examinated locations pillwort grows very intensively and forms dense mats of branched long rhizomes (Fig. 1). The longest observed rhizome was 73 cm long and had 23 branches. Leaves were succulent, erect, 3 13 cm long in the terrestrial form and delicate, thin, having 20 cm and more in the aquatic form (Fig. 2). The longest leaf of the aquatic form reached 41,5 cm. The species is able to propagate vegetatively by elongation and fragmentation of creeping rhizomes, and also may reproduce generatively by production of sporocarps and the sexual process. In last two years sporocarps were produced only in the northern pond, in its north-eastern part. The sporocarps were ripe at the end of October and at the beginning of November. The tested plot 25 25 cm was controlled on November 11 th, 2008 and 19 sporocarps were found: five were open and empty, one was open and releasing a jelly-like mass containing macro- and microspores (Fig. 3); remaining thirteen sporocarps were dark brown, hard and closed.
164 Ewa-Szczê niak,-andrzej-szlachetka 164 Fig. 1. Branched rhizome of Pilularia globulifera (phot. E. Szczê niak) Ryc. 1. Rozga³êzione k³¹cze Pilularia globulifera (fot. E. Szczê niak) Fig. 2. Aquatic (A) and terrestrial (B) forms of Pilularia globulifera (phot. E. Szczê niak) Ryc. 2. Wodna (A) i l¹dowa (B) forma Pilularia globulifera (fot. E. Szczê niak)
165 Pillwort-Pilularia-globulifera-L.-in-Lower-Silesia 165 Nine out of twenty sporocarps, collected after the ground-frost, released spores during next two days and this process was rapid. After 14 days, total of fourteen sporocarps released spores, other two were sterile and empty, and last four remained hard and closed. Sporocarps collected before frosts released spores slower: in 14 days only three out of twenty sporocarps became open. Spores were vital and germinated quickly after releasing. Gametophytes were reduced and endosporic. Female prothalli protruded in part from spores (Fig. 4), male prothalli were completely hidden inside spores and released gametes through the split of the spore walls (Fig. 5). Young sporophytes drifted in water; the weight and form of macrospores kept them vertically oriented (Fig. 6), what probably facilitated rooting. The species wintered under water or under a mat of sprouts and dead leaves of Juncus bulbosus (Fig. 7). Under that cover all parts of fern remained green and alive in temperatures c. 10 oc below zero. Fig. 3. Opened sporocarp with spores in a jelly-like mass (phot. E. Szczê niak) Ryc. 3. Otwarte sporangium z zarodnikami w galaretowatej masie (fot. E. Szczê niak)
166 Ewa-Szczê niak,-andrzej-szlachetka 166
167 Pillwort-Pilularia-globulifera-L.-in-Lower-Silesia 167 Fig. 4. Macrospore and female gametophyte (phot. E. Gola, E. Szczêœniak) Ryc. 4. Makrospora i gametofit eñski (fot. E. Gola, E. Szczêœniak) Fig. 5. Opened microspore (phot. E. Gola, E. Szczêœniak) Fyc. 5. Otwarta mikrospora (fot. E. Gola, E. Szczêœniak) Fig. 6. Macrospore with developing young sporophyte (phot. E. Gola, E. Szczêœniak) Ryc. 6. Makrospora z rozwijaj¹cym siê m³odym sporofitem (fot. E. Gola, E. Szczêœniak) The species forms the sub-atlantic plant community Pilularietum globuliferae of the alliance Hydrocotylo-Baldenion R.Tx. et. Dierssen ap. Dierssen 1972 and the class Litorelletea uniflorae Br.-Bl. et R.Tx. 1943 ex Westhoff, Dijk et Pascher 1946. The phytocoenosis in the southern pond is richer in plant species and consists of 15 species. Among them are taxa belonging to the classes Isoëto-Nanojuncetea Br. Bl. et R.Tx. 1943 and Molinio- Arrhenetheretea R.Tx. 1937 (Tab. 1: 1). In the northern pond, the plant community forms 3 zones depending on the water depth which are developed on banks and at the bottom of the ponds. In the driest area, the richest form of the community develops (Tab. 1: 2); together with the increase of water depth, the number of species decreases (Tab. 1: 3 4). Additionally, the pillwort enters the Phragmitetum australis (Gams 1927) Schmale 1939 community, where it occurs between the Phragmites stems in a loose form of rushes (Tab. 1: 5). List of localities in Lower Silesia (Fig. 8); l.n.c. locality not confirmed: AE 17: heath near Osiecznica (Fiek 1881, Schube 1903), l.n.c.; 25: peat bog near D³u yna (Schube 1903), l.n.c.; 26: peat bog near Wêgliniec (Fiek 1881, Schube 1903), l.n.c.; 35: between Jêdrzychowice and arki Œrednie (Fiek 1881, Schube 1903), l.n.c.; BE 10: Krzywa 2007, leg. E. Szczêœniak WRSL; Szlachetka, Szczêœniak 2007, 2008; 11: Rokitki (Spa³ek 2009); 20: between Os³a and Wilczy Las (Fiek 1881, Schube 1903), l.n.c. Fig. 7. Pilularia globulifera covered by a mat of Juncus bulbosus (phot. E. Szczêœniak) Ryc. 7. Pilularia globulifera pokryta warstw¹ Juncus bulbosus (fot. E. Szczêœniak)
168 Ewa-Szczêœniak,-Andrzej-Szlachetka 168 Tab. 1. Plant communities with Pilularia globulifera Tab. 1. Zbiorowiska roœlinne z Pilularia globulifera Succesive number of relevé 1 2 3 4 5 (Nr kolejny zdjêcia) Data (Data) Area (m 2 ) (Powierzchnia) 6 6 6 6 6 Cover of herb layer (%) 80 70 25 15 40 (Pokrycie warstwy zielnej) No. of species (Liczba gatunków) 15 9 5 3 11 Ch. Ass. Pilularietum globuliferae, Ch. All. Hydrocotylo-Baldenion* Ch. Cl. Litorelletea uniflorae** Pilularia globulifera 1 1 1 1 + Hydrocotyle vulgaris* 3 3 1 r. Juncus bulbosus** 2 2 1 1 + Ch. Ass. Phragmitetum australis, Ch. Cl. Phragmitetea* Phragmites australis.... 3 Alisma plantago-aquatica* + + r. + Eleocharis palustris*. + r. + Ch. Cl. Isoëto-Nanojuncetea Carex oederi + r... Gnaphalium uliginosum r... + Plantago intermedia r.... Ch. Cl. Molinio-Arrhenatheretea Lysimachia vulgaris + +.. + Juncus effusus.... 1 Myosotis palustris r.... Epilobium palustre r.... Accompanying species (Towarzysz¹ce) Bidens sp. + r.. r Salix sp. r r.. + Ranunculus flammula 1.... Rorippa palustris +... r Polygonum sp. r.... 1 4: Pilularietum globuliferae, 5: Phragmitetum australis Fig. 8. Distribution of Pilularia globulifera in Lower Silesia Ryc. 8. Rozmieszczenie Pilularia globulifera na Dolnym Œl¹sku
169 Pillwort-Pilularia-globulifera-L.-in-Lower-Silesia 169 3. Discussion Pilularia globulifera is a sub-atlantic species, which penetrates little into the central part of Europe and has its eastern range border in Poland. Its distribution depends on winter temperatures and the availability of oligothrophic and mesotrophic habitats of peat bogs or sandy banks of ponds and lakes. The climate warming is favourable for pillwort because increases the possibility to survive the winter. On the other hand, the climate changes in connection with human activity result in ground water decreasing, which in turn ruins peat bog habitats of Pilularia in Lower Silesia lowlands. Surprisingly, the same factors increase the number of possible locations in ponds a low water level exposes sandy banks and bottoms. In ponds near Chocianów, in the middle of the 20 th century, the water level was higher than now about 0,5 m. Nowadays, ponds are periodically flooded by freshwater in springtime, what stops the development of competitive species, and pillwort can continually pioneer new, bare sites. It can also survive the periods of the complete immersion. It is difficult to say how old Silesian populations are. The occurrence of Pilularia in this part of the Bory Dolnoœl¹skie district has been known since the 19 th century (Fiek 1881). Sporocarps may persist and remain dormant in silt, perhaps for many years (Page 2004). Also birds can transport the fern; a small size of sporocarps makes it very possible. Moreover, in autumn 2008 we observed swans (Cygnus olor) feeding on rhizomes and leaves of Pilularia and Juncus bulbosus, and carrying fragments of both species on feathers. During warm winter, the pillwort can survive as sub-evergreen fragments to renew growth in the following spring. High viability of spores, gametophytes and young sporophytes suggest that species is vigorous and if habitat conditions are favourable, it can spread out. It is possible, that Pilularia occurs in more than these two known stands in Lower Silesia. The species requires more research on chorology, biology and ecology. Pilularia globulifera sporocarps and living plants were collected from investigated population and the species is currently cultivated in the Botanical Garden of the University of Wroc³aw. Both ponds will be protected as the Nature 2000 area Ga³uszki w Chocianowie.
170 Ewa-Szczêœniak,-Andrzej-Szlachetka 170 References BRAUN-BLANQUET J. 1964. Pflanzensoziologie. Grundzüge der Vegetationskunde. Springer Verlag, Wien, New Jork, 865 pp. FIEK E. 1881. Flora von Schlesien preussischen und õsterreichischen Anteils. Phanerogamen und Gefässpflanzen. J. U. Kern s Verl., Breslau, 571 pp. JALAS J., SUOMINEN J., LAMPINEN R. 1999. Atlas Florae Europaeae. Digital database. K CKI Z., DAJDOK Z., SZCZÊŒNIAK E. 2003. Czerwona lista roœlin naczyniowych Dolnego Œl¹ska. In: K CKI Z. (ed.), Zagro one gatunki flory naczyniowej Dolnego Œl¹ska. Inst. Biol. Roœlin Uniwersytetu Wroc³awskiego, Pol. Tow. Przyjació³ Przyrody Pro Natura, Wroc³aw, p. 9 65. KUCZYÑSKI J. 1997. Geobotanical division of Silesia. In: Pawlak W., Atlas of Lower and Opole Silesia. Wroc³aw University, Lower Silesia Atlas Research Center, Wroc³aw, p. 60. MATUSZKIEWICZ W. 2008. Przewodnik do oznaczania zbiorowisk roœlinnych Polski. Vademecum Geobotanicum 3. Wydawnictwo Naukowe PWN, Warszawa, 537 pp. MIREK Z., PIÊKOŒ-MIREK H., ZAJ C A., ZAJ C M. 2002. Flowering plants and pteridophytes of Poland. A checklist. Biodiversity of Poland, 1. W. Szafer Institute of Botany, Polish Academy of Sciences, Kraków, 442 pp. PAGE C.N. 2004. The Ferns of Britain and Ireland. Cambridge University Press. 540 pp. SCHUBE T. 1903. Die Verbreitung der Gefässpflanzen in Schlesien preussischen und õsterreichischen Anteils. R. Nischkowsky Verl. Breslau, 361 pp. SPA EK K. 2009 (in print). Nowe stanowisko ga³uszki kulecznicy Pilularia globulifera na Dolnym Œl¹sku. Chroñmy Przyr. Ojcz. WATSON, L., DALLWITZ, M.J. 2004. The ferns (Filicopsida) of the British Isles. Version: 3 rd March 2008, http://delta-intkey.com ZAJ C A. 1978. Za³o enia metodyczne Atlasu Rozmieszczenia roœlin naczyniowych w Polsce. Wiad. Bot. 22(3): 145 155. ZAJ C A., ZAJ C M. (eds) 2001. Atlas rozmieszczenia roœlin naczyniowych w Polsce. Pracownia Chorologii Komputerowej Instytutu Botaniki Uniwersytetu Jagielloñskiego, Kraków, 714 pp. ZARZYCKI K., SZEL G Z. 2006. Czerwona lista roœlin naczyniowych w Polsce. In: MIREK Z., ZARZYCKI K., WOJEWODA W., SZEL G Z. (eds), Czerwona lista roœlin i grzybów Polski. Inst. Bot. im. W. Szafera, PAN, Kraków, p. 9 20. UKOWSKI W., JACKOWIAK B. 1993. Pilularia globulifera L. - Ga³uszka kulecznica. In: ZARZYCKI K., KA MIERCZAKOWA R. (eds), Polska Czerwona Ksiêga Roœlin (Polish Plant Red Data Book). W. Szafer Inst. of Botany, Inst. of Nature Conservation, Polish Academy of Science, Kraków, p. 36 38. UKOWSKI W., JACKOWIAK B. 2001. Pilularia globulifera L. - Ga³uszka kulecznica. In: KA MIERCZAKOWA R., ZARZYCKI K. (eds), Polska Czerwona Ksiêga Roœlin (Polish Red Data Book of Plants). W. Szafer Inst. of Botany, Inst. of Nature Conservation, Polish Academy of Science, Kraków, p. 63 64.
171 Pillwort-Pilularia-globulifera-L.-in-Lower-Silesia 171 Ga³uszka kulecznica Pilularia globulifera L. na Dolnym Œl¹sku biologia i ekologia Ga³uszka kulecznica Pilularia globulifera jest europejskim endemitem, zwi¹zanym z obszarem subatlantyckim. W ca³ym jej zasiêgu spada liczba stanowisk, w zwi¹zku z tym paproæ zosta³a uznana za zagro on¹ w Europie. W Polsce osi¹ga wschodni¹ granicê zasiêgu, a liczba jej stanowisk jest zale na od warunków klimatycznych, g³ównie temperatur zimowych. Obecnie jest taksonem krytycznie zagro onym wymarciem ( ukowski, Jackowiak 1993, 2001; Zarzycki, Szel¹g 2006). Na Dolnym Œl¹sku po 1945 r. nie by³a notowana i zosta³a uznana za wymar³¹ w regionie (K¹cki i in. 2003). W 2007 roku odnaleziono dwa stanowiska gatunku: nieliczne na stawie hodowlanym w Rokitkach, gdzie nie wytworzy³ sporokarpiów, a stanowisko przesta³o istnieæ po nape³nieniu stawu w 2008 roku (Spa³ek 2009), oraz bardzo obfite wyst¹pienie na stawach w nadleœnictwie Chocianów. W stawie po³udniowym ga³uszka wystêpuje tylko na niewielkiej powierzchni piaszczystego dna z cienk¹ warstw¹ mu³u, w stawie pó³nocnym tworzy zwarte maty, których powierzchnia zale y od poziomu wody. W roku 2007 pokrywa³a ona ok. 1000 m 2, w 2008 zaledwie po³owê tej powierzchni. Pilularia wytwarza tam zarówno formê l¹dow¹ o liœciach d³ugoœci 3 13 cm, jak i formê wodn¹, rosn¹c¹ w zanurzeniu, o d³ugoœci liœci do 41,5 cm (ryc. 2). Intensywnie namna a siê wegetatywnie poprzez rozrost i rozga³êzianie oraz fragmentacjê k³¹czy (ryc. 1). Dotychczas tylko w stawie pó³nocnym stwierdzono wytwarzanie sporokarpiów. Dn. 11 listopada 2008 r. na powierzchni testowej 25 25 cm odnotowano obecnoœæ 19 sporokarpiów, w tym 5 otwartych i pustych, 1 w³aœnie uwolni³o œluz z zarodnikami (ryc. 3), a 13 by³o zamkniêtych, ciemnych i twardych. Makro- i mikrospory s¹ ywotne, wytwarzaj¹ gametofity, zachodzi proces zap³odnienia i rozwój m³odych sporofitów przebiega bez zak³óceñ (ryc. 4 6). Zarodniki s¹ uwalniane szybciej i z wiêkszej liczby sporokarpiów po przech³odzeniu; bez przech³odzenia otwiera siê niewielka iloœæ sporokarpiów, a uwalnianie zarodników trwa d³u ej. Ga³uszka zimuje pod wod¹ lub pod okryciem z pêdów i martwych liœci Juncus bulbosus (ryc. 7). Je eli bêd¹ dostêpne odpowiednie siedliska, populacja nie bêdzie zagro ona. Na badanym stanowisku ga³uszka roœnie na brzegach i dnie dwóch stawów hodowlanych, tworz¹c w³asny zespó³ Pilularietum globuliferae (tab. 1: 1 4) oraz wnika w szuwar trzcinowy (tab. 1: 5). Z tej populacji pobrano materia³ do hodowli zachowawczej w Ogrodzie Botanicznym Uniwersytetu Wroc³awskiego oraz wyst¹piono o powo³anie ostoi Natura 2000 Ga³uszki w Chocianowie dla ochrony jej siedliska. ¹cznie ga³uszka wystêpowa³a na Dolnym Œl¹sku na 7 stanowiskach, z czego na zaledwie 2 po 1945 r. (ryc. 8).