Acta Botanica 1-2017 - za web.indd ACTA BOT. CROAT. 76 (1), 2017 91 Acta Bot. Croat. 76 (1), 91–94, 2017 CODEN: ABCRA 25 DOI: 10.1515/botcro-2016-0046 ISSN 0365-0588 eISSN 1847-8476 Short communication Long time no see – rediscovery of peculiar ephemeral fern Anogramma leptophylla (L.) Link in Croatia Vedran Šegota*, Vladimir Hršak, Antun Alegro University of Zagreb, Faculty of Science, Department of Biology, Division of Botany, Marulićev trg 20/II, HR-10000 Zagreb Abstract – Anogramma leptophylla is one of the rarest fern species in Balkan Peninsula. In Croatia, several localities were noted prior to this study, when its presence was confi rmed with a discovery of a small popula- tion on the island of Mljet (Southern Adriatic). This was, after almost 80 years, the fi rst reliable fi nding of this species along Eastern Adriatic. The establishment of A. leptophylla on the western part of the island of Mljet may be attributable to certain favourable environmental conditions, but essentially to higher air and soil hu- midity. Its unusual bryophyte-like life strategy, with short-living annual sporophytes, facilitates its survival under Mediterranean climate, generally unfavourable for pteridophytes. Keywords: Balkan Peninsula, distribution, island of Mljet, pteridophytes Abbreviations: CNHM – Herbarium of Croatian Natural History Museum, ZA – Herbarium Croaticum, ZAGR – Herbarium Facultatis Agronomiae, ZAHO – Herbarium of Ivo and Marija Horvat * Corresponding author, e-mail: vedran.segota@biol.pmf.hr Introduction Unlike the majority of fern species that exhibit perenni- al sporophytes and short-living gametophytes, a few pecu- liar ferns utilize bryophyte-like life strategy (Proskauer 1964, Pangua et al. 2011). With its ephemeral annual sporo- phyte and dormant perennial gametophyte, genus Ano- gramma (Adiantaceae) is one of the most well-known members of this group. The distribution centre of the genus is in the Neotropics (tropical areas of Mexico, Central and South America), where all fi ve species except A. ascensio- nis (endemic from Ascension Island in South Atlantic) can be found, including cosmopolitan A. leptophylla (L.) Link (Tyron et al. 1990, Molnár et al. 2008). Aside from Neo- tropics, A. leptophylla grows in the Mediterranean basin, Macaronesia, Atlantic Europe, tropical and South Africa, Australia and New Zealand (Paugua et al. 2011). Conse- quently, Anogramma leptophylla is the only representative of the genus in European fl ora (Tutin 1993), occurring along the Atlantic coast, the Mediterranean basin and in Crimea (Jalas and Suominen 1972). A. leptophylla is a cosmopolitan species restricted to temperate and tropical zones (Landolt 2010), with prefer- ence for humid regions, usually with alternating wet and dry seasons (Nakazato and Gastony 2003, Studnička 2009). In European context, it is considered an oceanic-suboceanic (Meusel et al. 1965, Dostál 1984) or oceanic-submediterra- nean species (Fischer et al. 2008). Similarly, in the fl ora of Croatia, the species was defi ned as an Atlantic-Mediterra- nean element (Regula-Bevilaqua and Ilijanić 1984). A. leptophylla is recognized in all Croatian checklists (Mayer and Horvatić 1967, Hršak 1994, Nikolić 2016). However, only several localities were noted in Croatia prior to this study, all in the southern part of the country. First known record dates from mid19th century, when Visiani (1852) noted the species in the town of Dubrovnik, cited again later by Schlosser and Vukotinović (1869), Mannag- etta (1901) (including also the adjacent village Zaton) and Hirc (1905). The species was found again in Dubrovnik (precisely on Lapad peninsula) in 1868 by Vodopić, being the only currently available specimen of this species depos- ited in Croatian herbariums (ZA3132). This locality was cited later also by Hirc (1905), and confi rmed by Latzel (1914). The latter author found the species on one more lo- cality – on the island of Mljet, in the vicinity of the sea-port Sobra (Latzel 1914), which was cited later in the analysis of the fl ora of Mljet performed by Regula-Bevilaqua and Ilijanić (1984). Finally, the fern was recorded on the island of Hvar (village of Vrisnik near Jelsa) by Rechinger (1934), and never reported in the southern Adriatic since. Recent ŠEGOTA V., HRŠAK V., ALEGRO A. 92 ACTA BOT. CROAT. 76 (1), 2017 notice on fi nding of A. leptophylla on the northern Adriatic island of Krk, between town of Baška and Halm hill in 2009 (Rottensteiner 2014), with no herbarium specimen avail- able, although unexpected, might be authentic; neverthe- less, it should be carefully examined. Historical and recent fi ndings of A. leptophylla along the Southern Adriatic coast appeared to be on the northern- most border of its areal on Balkan Peninsula, extending southward through Montenegro and Macedonia, down to the Greek mainland and islands, including Crete. Within former Yugoslavia, Mayer and Horvatić (1967) mention only Southern Dalmatia (Croatia) as a locality for A. lep tophylla, however it was recorded in Montenegro (Boka Kotorska: Rose, Sutorina, Vrmac hill above place Muo) by Studnicz- ka (1890), what is cited later by several authors (Mannag- etta 1901, Hayek 1927, Pulević 2005, Stešević and Caković 2013) and Macedonia (Markovi Kuli near Prilep and Bela- sina Mt.) (Hayek 1927, Micevski 1985). Although A. leptophylla is obviously extremely rare in Croatia, it was not estimated according to the IUCN criteria. Material and methods During an extensive fl oristic study of the National Park Mljet (southern Adriatic), a number of fi eldtrips were un- dertaken in the period from 2008 to 2011. Nearly all basic 1/64 MTB fi elds of the Central European fl ora mapping grid (1.5×1.4 km) (Nikolić et al. 1998) within the park were accessed at regular intervals throughout four growing sea- sons. Collected specimen of A. leptophylla, was identifi ed in 2012 using several identifi cation keys and iconographies (Pigniati 1982, Tutin 1993, Kopp and Schneebeli-Graf 1998). Historical literature regarding distribution of A. leptophylla on Eastern Adriatic coast, and all available herbarium col- lections in Croatia (ZA, ZAHO, CNHM and ZAGR) were checked. Results and discussion A small population of A. leptophylla was discovered on 6th May 2010 in the vicinity of the footpath along the north- ern coastline of the Mljet National park, opposite to the neighbouring islet of Kobrava. The fi ndspot is located with- in 3270.213 1/64 MTB fi eld, between Tatinica cove and Rt Križice (Rt Kula) promontory. Between these two locali- ties, there are two coves (Pod Veja Gora and Čartonica) and the Rt Travno Kocje promontory, spreading from west to east. The same direction is followed by the hills above them (Veja gora, 265 m a. s. l.; Vriješće, 296 m a. s. l. and Hripe, 183 m a. s. l.). Some other fern species, such as Polypodium cambricum L., Asplenium ceterach L., A. onopteris L. and A. adianthum-nigrum L., were noted on the same site. At the time of our visit, hardly few plants of A. lepto- phylla were observed; all were in a good state, bearing ma- tured sporangia. Around 10 cm high stem did not bear leaf bases of previous years, clearly indicating that the aboveg- round sporophyte is, beyond any doubt, annual. One speci- men was collected, with both aboveground green sporo- phyte and subterranean pea-like structure called tubercle, and deposited in ZA collection (Fig 1). The population was not further monitored, due to the geographic distance of the island. An examination of major Croatian herbarium collec- tions revealed only one herbarium specimen of A. lepto- phylla, collected in 1898 on Lapad peninsula (part of the town of Dubrovnik), but with only aboveground sporophyte containing ripened sporangia as well (Fig 1). Within the National park Mljet, the specimens of A. lep- tophylla were observed on bare wet soil in limestone rock crevices surrounded by green mats of mosses. The fi ndspot was in the close vicinity of the hiking footpath, which is ap- proximately 5 to 10 m a. s. l. The similar habitat, on the rocks, was also briefl y described at an old fi ndspot on the same island (sea-port Sobra) (Latzel 1914). Similarly, on Iberian peninsula, the species grows in rocky habitats, main- ly in wide cracks of siliceous rocks fi lled with soil (Nogueira 1986); however, it spreads from the lowlands up to about 1000 m a. s. l., under climates varying from typical oceanic to Mediterranean. A. leptophylla is considered to be, to some extent, a pioneer species occupying competitive-free habi- tats such as rock fi ssures with little soil, where, in Mediter- ranean, it is often accompanied with Selaginella denticulata (L.) Spring (Dostál 1984). Similarly, we observed that these kinds of microhabitats on island Mljet were often occupied by S. denticulata, and it appeared to be rather frequent along Fig 1. Anogramma leptophylla, scanned herbarium specimens from island of Mljet, 6th May 2010 (right) and Lapad peninsula (Dubrovnik) 1868 (left), using A3+ scanner Expression 11000XL. ANOGRAMMA LEPTOPHYLLA IN CROATIA ACTA BOT. CROAT. 76 (1), 2017 93 the footpath where A. leptophylla was detected. In order to avoid its competitors, A. leptophylla fi nishes its short life- cycle at the end of spring when ephemeral mosses, liver- worts and minute seed plants start to inhabit the unhostile surfaces. This way it uses its competitive advantage for fast development in favourable seasons. In some inland populations, such as the southern slopes of Swiss and Italian Alps, the species occupies similar mi- crohabitats, like mouths of caves, which provide a suitable microclimate (Lauber and Wagner 1998). In Macedonia, as an extremely rare species, it occupies moist and shaded places beneath large granite rocks (Micevski 1985). The most remote inland population, more than 1000 km from the closest populations in Alps and Southern Adriatic, was re- cently discovered in Carpathian Basin (NE Hungary). Using precise fi eld measurements of the climatic conditions of the site, this remarkable discovery has been explained by the microclimate which provides above-freezing air tempera- ture and high humidity throughout the year (Molnár et al. 2008). To summarize, the species in Europe undoubtedly prefers very specifi c microhabitats characterized by rocky fi ssures with small amount of soil sediment, away from full sun exposure, yet out of reach of frost, in positions at least partially sheltered and shaded by adjacent rocks and/or high- er shrub and tree vegetation (Dostál 1984). This is the case on island of Mljet, where species was found in a site shaded by edges of very compact evergreen vegetation dominated by Quercus ilex L., Juniperus phoenicea L., Phillyrea latti- folia L., Pistacia lentiscus L., Cistus creticus L. subsp. erio- cephalus (Viv) Greuter et Burdet, Erica arborea L., Arbutus unedo L., Myrtus communis L., Viburnum tinus L. and Emerus majus Mill. subsp. emeroides (Boiss. Et Spruner) Soldano et F. Conti. This vegetation is practically impene- trable, owing to dense Ruscus aculeatus L. in the understory and Smilax aspera L. that densely climbs to the canopies. According to Trinajstić (1986), island of Mljet is situat- ed in steno-Mediterranean zone of the Mediterranean re- gion attributed to rather hot and arid conditions, which is unfavourable for A. leptophylla establishment. However, the mean annual precipitation on the western part of the is- land is surprisingly high (up to 1000 mm) (Perčec Tadić 2008), although unevenly distributed. The locality of A. leptophylla, situated on the exposed fl ank of the island and in close vicinity to the sea, enables additional water con- densations over the cooler nights in the summer draught pe- riod. Therefore, it is likely that soil retains somewhat more water under the partial shadow of higher and dense tree and shrub vegetation. This more humid microclimate of the site is also refl ected in the presence of additional submediterra- nean elements such as Pistacia terebinthus L., Fraxinus or- nus L., Laurus nobilis L., and particularly Sesleria autum- nalis (Scop.) F.W.Schultz. Narrow habitat preferences of A. leptophilla might not be the only reason for its rarity in western Balkan. Consider- ing the rather short life-cycle of the aboveground sporo- phyte, some populations have most likely not been observed by botanists. The sporophyte generation does not begin to develop from dormant embryos on perennial tubercles be- fore December, reaching its maturity at the beginning of April. Spore ripening takes place in April and May, followed by sporophyte withering at the beginning of June. Thus, specimens are easily overlooked until next spring. However prothallia, newly produced from the spores, photosynthesize during June and July, and then, if no suitable growing condi- tions exist, they form a dormant tubercle (Pangua et al. 2011). If in some years a very dry spring occurs, sporophyte might not appear at all within the same season, and tubercle remains in a resting state. According to Molnár et al. (2008), dormant tubercles are able to survive for 2.5 years in stress- ful drought conditions. This, among ferns a rare aspect of the life-cycle, indicates its therophytic behaviour and mis- leads to concluding that A. leptophylla is an annual species. Moreover, it resembles bryophyte-like life strategy, which gives this fern some advantages in colonisation and has probably contributed to it wide geographic range (Pangua 2011). In contrast to other ferns among which environmen- tal sex determination is a rule, in A. leptophylla sex is ge- netically controlled, as in the majority of land plants (Pan- gua et al. 2011). Our discovery of A. leptophylla on island of Mljet in May confi rms that its life-cycle is in accordance with those reported for other European populations. A. leptophylla is a cosmopolitan species, and has not been reported as threatened so far. Even though there is an extremely low number of recent fi ndings in Croatia, and there is no evidence that it is still present at other histori- cally known sites, its specifi c habitat is not endangered at all. Therefore, according to IUCN criteria, the species qual- ifi es as data defi cient (DD) and calls for larger fi eld surveys. Considering its specifi c ecological requirements, climate change and global warming could present a major threat for A. leptophylla populations, especially in the Mediterranean basin. Anogramma leptophylla is one of the rarest fern species in Croatia; however, other rare ferns such as Asplenium cu- neifolium Viv., A. sagittatum (DC.) Bange, Hymenophyllum tunbrigense (L.) Sm., Notholaena marantae (L.) Desv. and Woodsia ilvensis (L.) R. Br., each with barely few fi nding localities, also occur in the state territory. Thus, targeted fi eld investigations of these species, including A. leptophyl- la, are of great importance for widening the knowledge on their distribution in the future. Acknowledgements The fi eld research was undertaken within the frames of the “Flora of Mljet NP” project, funded by the National park Mljet. References Dostál, J., 1984: Famile Gymnogramminaceae. 112–115. In: Kramer, K. U. (ed.), Illustrierte Flora von Mitteleuropa. Dritte, völlige neubearbeitete Aufl age. verlag Paul Parey, Berlin. Fischer, M. A., Oswald, K., Adler, W., 2008: Exkursionsfl ora für Österreich, Lichtenstein und Südtirol. Biologiezentrum der Oberösterreichischen Landesmuseum, Linz. Hayek, A., 1927: Prodromus fl orae peninsulae Balcanicae. Reper- torium specierum novarum regni vegetabilis. Band I. Pterido- ŠEGOTA V., HRŠAK V., ALEGRO A. 94 ACTA BOT. CROAT. 76 (1), 2017 phyta, Gymnospermae, Dicotyledone (Apetalae et Choripeta- lae) 19. Dahlem. Hirc, D., 1905: Revision of Croatian fl ora. Rad JAZU 161, 145– 239 (in Croatian). Hršak, V., 1994: Anogramma leptophylla (L.) Link. In: Nikolić (ed.), Flora Croatica. Index fl orae Croaticae. Pars 1. Natura Croatica 4, Suppl. 2, 28. Jalas, J., Suominen, J. (eds.), 1972: Atlas fl orae Europaeae. Distri- bution of vascular plants in Europe. Vol. 1. The Comittee for mapping the fl ora of Europe and Societas Biologica Fennica Vanamo, Helsinki. Kopp, E., Schneebeli-Graf, R, 1998: Illustrierter Leitfaden zum Bestimmen der Farne und farnverwandten Pfl anzen der Schweiz und angrenzender Gebiete. Schweizerische Vereini- gung der Farnfreunde. Switzerland. Landolt, E., 2010: Flora Indicativa. Ökologische Zeigerwerte und biologische Kennzeichen zur Flora der Schweiz und der Al- pen. 1. Aufl age. Haupt Verlag. Latzel, A., 1914: Neuere Ergebnisse der botanischen Erfoschung Dalmatiens und der Herzegovina. Gesellschaft Deutscher Na- turforscher und Ärzte. Leipzig. Lauber, K., Wagner, G., 1998: Flora Helvetica. Verlag Paul Haupt. Bern-Stuttgart-Wien. Mannagetta, B.G. von, 1901: Die Vegetationsverhältnisse der illy- rischen Länder. Wilhelm Engelmann, Leipzig, 1–534. Mayer, E., Horvatić, S., 1967: Anogramma leptophylla. In: Hor- vatić, S. (ed.), Analytical fl ora of Yugoslavia 1/1. Šumarski fakultet Sveučilišta u Zagrebu. Sveučilišna naklada Liber (in Croatian). Meusel, H, Jäger, E., Wienest, E., 1965: Vergleichende Chorologie der Zentraleuropäischen Flora. Text. VEB Gustav Fischer Ver- lag, Jena. Micevski, K., 1985: Flora of FR Macedonia. 1/1, 52. Makedonska akademija na naukite umetnostite, Skopje (in Macedonian). Molnár, C., Baros, Z., Pintér, I., Türke, I. J., Molnár, A., Sramkó, G., 2008: Remote, inland occurrence of the oceanic Anogram- ma leptophylla (L.) Link (Pteridaceae: Taenitidoideae) in Hungary. American Fern Journal 98/3, 128–138. Nakazato, T., Gastony, G. J., 2003: Molecular phylogenetocs of Anogramma species and related genera (Pteridaceae: Taeni- tioideae). Systematic Botany 28, 490–502. Nikolić, T. (ed.), 2016: Anogramma leptophylla. In: Flora Croati- ca database. On-line. University of Zagreb. Faculty of Sci- ence, Division of Botany, Zagreb. Retrieved February 30, 2016 from http://hirc.botanic.hr/fcd. Nikolić, T., Bukovec, D., Šopf, S., Jelaska, S. D., 1998: Mapping of Croatian fl ora – possibilities and standards. Natura Croatica, Periodicum musei historiae naturalis Croatici. 7, Suppl. 1, 1–62. Nogueira, I., 1986: Anogramma Link. In: Castroviejo, S., Laínz, M., López Gonzaléz, G., Montserrat, P., Munoz Garmendia, F., Paiva, J., Villar, L. (eds.), Flora Iberica 1, 63–65. Real Jardín Botaníco, CSIC, Madrid. Pangua, E., Pérey/Ruyafa, I., Pajarón, S., 2011: Gametophyte fea- tures in peculiar annual fern, Anogramma leptphylla. Annales Botanici Fennici 48, 465–472. Perčec Tadić, M., 2008: Mean annual precipitation (Map). In: Zaninović, K. (ed.), Climatological atlas of Croatia 1961– 1990. 1971–2009. DHMZ, Zagreb (in Croatian). Pignatti, S., 1982: Flora d’Italia vol. 1. Edagricole, Bologna. Proskauer, J., 1964: Riccia tuberosa Taylor = Anogramma lepto- phylla (L.) Link, or on the importance of being bryophytic. Journal of the Indian Botanical Society 42, 185–188. Pulević, V., 2005: Material for vascular fl ora of Montenegro. Ad- dition to „Conspectus fl orae Montenegrinae” of J. Rohlena. Republički zavod za zaštitu prirode Crne Gore. Posebna izdanja, Book 2, Podgorica (in Montenegrin). Rechinger, K. H., 1934: Zur Kenntnis der Flora der Halbinsel Pelješac (Sabioncello) und einiger Inseln des Jugoslawischen Adriagebietes (Dalmatien). Magyar Botanikai Lapok 33, 24– 42. Regula-Bevilacqua Lj., Ilijanić, LJ., 1984: Analyse der Flora der Insel Mljet. Acta Botanica Croatica 43, 119–142. Rottensteiner, W. K., 2014: Exkursionsfl ora für Istrien. Verlag des aturwissenschaftlichen Vereins für Kärnten. Klagenfurt. Schlosser, J. C. K., Vukotinović, Lj., 1869: Flora Croatica. Sump- tibus et auspiciis academiae scientiarum et articum slavorum meridionalium, Zagreb, I–CXLI, 1–1362. Stešević, D., Caković, D., 2013: Catalogue of vascular fl ora of Montenegro I. Crnogorska akademija nauka i umetnosti, 33 (in Montenegrin) Studnička, M., 2009: Ferns. Atlas of autochthonous and exotic species. Academia, Praha (in Czech). Studniczka, C., 1890: Beiträge zur Flora von Süddalmatien. Ver- handlungen der Zoologisch-Botanischen Gesellschaft in Wien 40, 55–84. Trinajstić, I., 1986: Phytogeographical division of the forest vege- tation of the Eastern Adriatic Mediterranean area – basic point in the organisation of management of the Mediterranean for- ests. Glasnik za šumske pokuse, special edition 2, 53–67 (in Croatian). Tutin, T. G., 1993: Anogramma leptophylla. In: Tutin, T. G., Burg- es, N. A., Chater, A. O., Edmondson, J. R., Heywood, V. H., Moore, D. M., Valentine, D. H., Walters, S. M., Webb, D. A. (eds.), Flora Europaea vol. 1, 2. ed. Psilotaceae to Platanaceae, 13. Cambridge University Press, New York. Tyron, R., Tyron, F., Kramer, K. U., 1990: Pteridaceae. 230–256, In: Kramer, U. K., Green, P. S. (eds.), The families and genera of vascular plants, Vol. 1. Pterydophytes and gymnosperms. Springer Verlag, Berlin. Visiani, R., 1852: Flora Dalmatica, Lipsiae. Appendix SPECIMINA VISA Vodopić, Mato: Lapad (Dubrovnik) (ad saxa viae in olivato Opuić, Lapad), 1868 (ZA): Šegota, Vedran and Vladimir Hršak: National park Mljet, between Tatinica cove and Rt Križice (Rt Kula) promontory, 2010 (ZA) LITERATURE DATA Visiani: Dubrovnik (ad muros et rupes agri Ragusini, ubi legit Fr. Neumayer. Fruct. A vere in aestatum), 1852; Sch- losser and Vukotinović: Dubrovnik, 1869; Mannagetta, B. G. von: Dubrovnik, village of Zaton (Reicher an Beson- derheiten ist die Festlandküste um Ragusa, d. h. von Malfi bis Ragusa vecchia.), 1901; Hirz: Dubrovnik, Lapad, 1905; Latzel: Sobra (island of Mljet), Lapad peninsula (Dubrov- nik) (an den Felsen in der Nähe des Porto Sovra auf der insel Meleda; auf Lapad bei Ragusa), 1914; Hayek: Da (Dalmatia), 1927; Rechinger: village of Vrisnik (island of Hvar) (H: Grund v. Wegmauern b. Vrisnik, 150 m), 1934; Regula-Bevilaqua and Ilijanić: Mljet, 1984; Rottensteiner: Krk, Baška – Halm, 2014.