Relationship of Animals to the Cyclamen Cyclamen Fatrense Halda Et Soják: Pollinators, Consumers and Occasional Visitors
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Biologia 68/3: 517—524, 2013 Section Zoology DOI: 10.2478/s11756-013-0178-2 Relationship of animals to the cyclamen Cyclamen fatrense Halda et Soják: pollinators, consumers and occasional visitors Peter Turis1 &ĽubomírVidlička2,3 1The administration of the Low Tatras National Park, Lazovná 10,SK-97401 Banská Bystrica, Slovakia; e-mail: [email protected] 2Institute of Zoology, Slovak Academy of Sciences, Dúbravská cesta 9,SK-84506 Bratislava, Slovakia and 3Department of Biology, Faculty of Education, Comenius University, Moskovská 2, Bratislava, Slovakia; e-mail: [email protected] Abstract: The West-Carpathian endemic Cyclamen fatrense is a forests species. Its distribution area lies at the northern margin of distribution area of the Cyclamen genus. Several studies have focused on the pollinators and consumers of representatives of this genus, but they mention only some more important animal species. The aim of our study was to determine the species spectrum of animals having a relationship to C. fatrense in its natural environment and to define mutual relationships between this plant and animals based on comparison of phenologic manifestations of cyclamen and known ecologic data about its visitors. In course of different phenophases of C. fatrense we recorded 127 invertebrate taxa on this plant. Among them 7 taxa were identified as consumers, 29 taxa as potential consumers, 5 taxa as potential pollinators and 91 had an indifferent relationship to the cyclamen. Damaging or direct consummation of cyclamens by vertebrates has not been observed. Key words: Cyclamen fatrense; pollinators; consumers Introduction Affre et al. 1995; Affre & Thompson 1997; Schwartz- Tzachor et al. 2006). Species of Cyclamen L. (Primulaceae) are distributed Several authors report on animals participating predominantly in the Mediterranean area. From among on spreading fruits and seeds of the cyclamen. Ac- 20 known species (Davis et al. 1999) the northernmost cording to Kerner (1898), the spiral-like rolled stalks occurring species are Cyclamen purpurascens Mill. and of fruits are, at occasional attaching, spread by some Cyclamen fatrense Halda et Soják. While C. purpuras- vertebrates. In connection with seed propagation, the cens grows on a wide territory from the Swiss Jura and myrmecochoria is mostly mentioned (Hildebrand 1898; West Alps to Balkan Mts (Meusel et al. 1978), C. fa- Nordhagen 1932; Kovanda 1992). Affre et al. (1995) trense is considered as a subendemic of the small moun- even discovered one ant species participating on seed tain range Veľká Fatra in West Carpathians in Slovakia transport. (Kliment 1999). Both species have very similar shape In connection with occurrence of animals on C. fa- and differ from each other mainly by form and color of trense only a finding of the weevil Phyllobius argenta- leaves (Halda & Soják 1971). tus (L., 1758) (Coleoptera: Curculionidae) in an empty Relationships of animals to the Cyclamen species capsule has been published (Turis 2008). are presented on several levels. Most authors mention In the framework of the running ecobiological in- herbivory of molluscs, Diptera and caterpillars, which vestigation of C. fatrense, it is important to know eat leaves, fruits or tubers of cyclamens in natural as wide as possible spectrum of animals visiting this habitats (Hildebrand 1898; Hering 1957; Affre et al. plants in order to define: (i) occasional visitors with- 1995; Reiprich 2001). L¨udi (1975) mentions damaging out obvious consequences for the plant, (ii) visitors of buds, leaves, tubers and roots of cultivated individu- with more significant consequences for the plant (phy- als by aphids, caterpillars, thrips, beetle larvae, nema- tophages damaging vegetative or generative organs), todes, molluscs and rodents. (iii) pollinators. Other animals are reported in connection with the Cyclamen genus as pollinators in relation with their re- Brief description of Cyclamen fatrense production. In wild plants, this role is only rarely played Cyclamen fatrense is a hemicryptophyte or geophyte by bees, bumblebees and ants. Hildebrand (1898) ob- bound to forests of submountain and mountain zone. served these hymenopterans on flowers of the cultivated Usually a single stem reaching to the layer of leaves cyclamens. More frequently the cyclamens are polli- fallen from the surrounding trees, grows from the tuber. nated by night moths, thrips or hoverflies (L¨udi 1975; From the terminal part of stem the permanent leaves c 2013 Institute of Zoology, Slovak Academy of Sciences 518 P. Turis &Ľ.Vidlička grow and, in summer, striking, moderately smelling flowers in various shade of rose color. Flowering lasts approximately from July until late October. Peduncle of fertilized flowers spiral-like rolls on the ground surface and the fruits ripe in next summer. Absence of elaio- some on seed is important for potential relationships with animals. Production of nectar in flowers has not been observed. In Cyclamen repandum Sm., Cyclamen hederifolium Aiton and Cyclamen persicum Mill. nec- tar is not produced (Affre & Thompson 1997; Schwartz- Tzachor et al. 2006), while Affre et al. (1995) mentioned its absence in the whole Cyclamen genus. Fig. 1. Localization of the research area (grey circle – wider sur- rounding of the Motyčky village). Material and methods Invertebrates on Cyclamen fatrense were collected individ- ually in 2006–2007. Observations and catches were carried When evaluating significance of melliphages for pollination out in the snow-free period (approximately March – Novem- we took in consideration a period of their occurrence in re- ber), usually once a week. The invertebrates were sampled lation to the period of cyclamen flowering. (leg. P. Turis) from the above-ground parts of plants during light period of the day and were preserved in alcohol and Study area distributed to specialists for identification. Relationships of vertebrates (forest rodents, wild boars, Observation and collection of animals were carried out red deer, roe deer etc.) to cyclamens were evaluated on base mainly in the eastern part of the species area in the Veľká of visual observations in 2006–2008. Fatra Mts and the Starohorské vrchy Mts. The studied ter- Nomenclature of invertebrate taxa and their systematic ritory has an area of 1,763 ha and lies at altitudes of 450– arrangement in the Table 1 was used according to Fauna Eu- 1100 m (Turis & Žiačik 2008). The broadleaved and mixed ropaea (de Jong 2010). Trophical characteristics of individ- forests belonging phytocenologically into association Carici ual taxa are based on oral information from the specialists albae-Fagetum Moor 1952 (Kanka et al. 2008) are domi- and on published data (Buchar et al. 1995; Buchar & Kůrka nant. The major part of research was performed in a wider 1998; Doskočil 1977; Jasič 1984, Kočárek et al. 2005; Pfleger surrounding of the Motyčky village (48◦50–53 N, 19◦7–12 1988; Zahradník 1987). E, Central Slovakia, Banská Bystrica district, 680 m a.s.l.; Relations of the recorded animals to C. fatrense given Fig. 1). in Table 1 are characterized according to trophic relation of the caught developmental stages and on direct field observa- Results tions. We consider the zoophages, parasites and saprophages to have an indifferent relation to cyclamens, similarly as phytophages obviously specialized on other plant species During the two-year investigation we recorded 127 taxa (except for cyclamen). Other phytophages are taken as po- of invertebrates (107 species and representatives of fur- tential consumers, while the phytophages directly observed ther 12 genera, 7 families and 1 order, which could to eat leaves or flowers of cyclamens are taken as consumers. not be precisely identified) (Table 1). We recorded Fig. 2. Survey of orders and number of invertebrate taxa recorded on Cyclamen fatrense in years 2006–2007. Animals on Cyclamen fatrense 519 Table 1. Systematic survey of invertebrates recorded on Cyclamen fatrense in 2006–2007. Recorded on Period of collection Taxon TR RP LFlFrFPEFP Phyllum: Mollusca Clase: Gastropoda 1. order: Pulmonata Arianta arbustorum (L., 1758) (Helicidae) + + + P PC Arion fuscus (O.F. M¨uller, 1774) (Arionidae) + + + P PC Bielzia coerulans (M. Bielz, 1851) (Limacidae) + + P PC Cochlodina laminata (Montagu, 1803) (Clausiliidae) + + P PC Columella edentula (Draparnaud, 1805) (Vertiginidae) + + + P PC Faustina faustina (Rossm¨assler, 1835) (Helicidae) + + + P PC Deroceras sp. (Limacidae) + + PC Ena montana (Draparnaud, 1801) (Enidae) + + P PC Euconulus fulvus (O.F. M¨uller, 1774) (Euconulidae) + + P PC Merdigera obscura (O.F. M¨uller, 1774) (Enidae) + + + P PC Monachoides incarnatus (O.F. M¨uller, 1774) (Hygromiidae) + + P PC Monachoides vicinus (Rossm¨assler, 1842) (Hygromiidae) + + + P PC Petasina unidentata (Draparnaud, 1805) (Hygromiidae) + + P PC Punctum pygmaeum (Draparnaud, 1801) (Punctidae) + + P PC Trochulus hispidus (L., 1758) (Hygromiidae) + + + P PC Malacolimax tenellus (O.F. M¨uller, 1774) (Limacidae) + + P PC Phyllum: Arthropoda A. class: Arachnida 1. order: Mesostigmata Holoparasitus sp. (Parasitidae) + + ZI Pergamasus mediocris Berlese, 1904 (Parasitidae) + + ZI Veigaia nemorensis (C.L. Koch, 1839) (Veigaiidae) + + ZI 2. order: Prostigmata Anystis sp. (Anystidae) + + + ZI Bdellodes longirostris (Hermann. 1804) (Bdellidae) + + ZI Trombidiidae + + + Z I 3. order: Oribatida Oribatida + + Z I 4. order: Araneae Clubiona lutescens Westring, 1851 (Clubionidae) + + + ZI Diplocephalus picinus (Blackwall, 1841) (Linyphiidae) + + Z I Enoplognatha ovata (Clerck,