Biodiversity Data Journal Biodiversity Data Journal Biodiversity Data Journal BDJ 1314-2836 1314-2828 Pensoft Publishers Biodiversity Data Journal 10.3897/BDJ.3.e5610 3921 Taxonomic paper Nymphalidae Evolution (Adaptation) and Conservation Population Management, Harvesting, and Monitoring Finland Europe Melampyrum sylvaticum as a pre-diapause host plant of the scarce fritillary (Euphydryas maturna) in Finland Nieminen Marko marko.nieminen@faunatica.fi § Metapopulation Research Centre, Department of Biosciences, University of Helsinki, Finland Faunatica Oy, Espoo, Finland

Corresponding author: Marko Nieminen (marko.nieminen@faunatica.fi).

Academic editor: Rodolphe Rougerie

2015 17 07 2015 3 e5610 08 07 2015 13 07 2015 Marko Nieminen This is an open access article distributed under the terms of the Creative Commons Attribution License 4.0 (CC-BY), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Background

The scarce fritillary Euphydryas (Hypodryas) maturna (L.) is included in the Habitats Directive's Annexes II and IV(a). Therefore, it is crucially important to be able to define the habitat and breeding places of E. maturna in a correct and unbiased way.

New information

Data on a previously unknown pre-diapause main host plant, the small cow-wheat (Melampyrum sylvaticum L.), of Euphydryas maturna in Finland is presented.

Euphydryas maturna Finland Habitats Directive host plant Melampyrum sylvaticum scarce fritillary
Introduction

The scarce fritillary Euphydryas (Hypodryas) maturna (Linnaeus, 1758) is a high-profile species within the European Union, as it has been included in the Habitats Directive's (Council Directive 92/43/EEC of 21 May 1992 on the conservation of natural habitats and of wild fauna and flora) Annexes II and IV(a). Based on the Annex II, special conservation areas (i.e. Natura 2000 areas) need to be designated for E. maturna. The Annex IV lists species in need of strict protection, and those species and their breeding and resting places are protected by national legislation, which also applies to Finland. Therefore, the ability to define the habitat and breeding places of E. maturna in a correct and unbiased way is crucially important for both protecting the species effectively and not making uninformed administrative decisions which may be economically very costly. Euphydryas maturna is a wide-spread species in SW Finland, and it has been assessed as Least Concern by the IUCN criteria in Finland (Kaitila et al. 2010).

The species of the tribe Melitaeini, to which E. maturna belongs, feed mainly on plants containing secondary plant metabolites called iridoids (Bowers 1983, Wahlberg 2001). Iridoids are used for oviposition-plant selection, and as feeding stimulants and defensive chemicals by larvae (e.g. Bowers 1983, Nieminen et al. 2003, Wahlberg 2001). Larval host plants are the key part for the definition of breeding habitat for specialized herbivores such as E. maturna. Numerous plant species have been recorded as pre-diapause (Table 1) and/or post-diapause hosts of E. maturna throughout its range (see e.g. Wahlberg 1998, Dolek et al. 2013). In Finland, the common cow-wheat (Melampyrum pratense L.) has been recorded as the main host plant (Wahlberg 1998). Here, I present data on a previously unknown pre-diapause main host plant, the small cow-wheat (Melampyrum sylvaticum L.), of Euphydryas maturna in Finland.

Materials and methods

Larval groups of E. maturna were systematically searched from an area of ca. 3.5 km2 within the municipalities of Sipoo and Pornainen in southern Finland (coordinates of the midpoint of the study area: 60.45072N, 25.30928E). All larval groups were georeferenced with GPS and photographed, and a sample of each host plant was collected for identification. Plant samples were identified by Henry Väre (Finnish Museum of Natural History, Helsinki). Fieldwork was made by MN and Kari Nupponen between August 27 and September 11 in 2014.

Taxon treatments Euphydryas maturna (Linnaeus, 1758) Materials

Type status: Other material. Occurrence: occurrenceRemarks: number of larval groups counted (with unknown number of larvae per group); recordedBy: Marko Nieminen; individualCount: 120; lifeStage: larva; Taxon: scientificName: Euphydryas maturna; order: Lepidoptera; family: Nymphalidae; genus: Euphydryas; specificEpithet: maturna; taxonRank: species; Location: country: Finland; stateProvince: Uusimaa; municipality: Sipoo; locality: Brusas; verbatimElevation: 60 m; verbatimCoordinates: 60°26.73'N 25°17.95'E; verbatimLatitude: 60°26.73'N; verbatimLongitude: 25°17.95'E; decimalLatitude: 60.4455; decimalLongitude: 25.2992; Identification: identifiedBy: Marko Nieminen; dateIdentified: 2014; Event: samplingProtocol: visual search; eventDate: 2014-08-27/09-11; Record Level: language: en; basisOfRecord: Photographed; source: marko.nieminen@faunatica.fi

Type status: Other material. Occurrence: occurrenceRemarks: number of larval groups counted (with unknown number of larvae per group); recordedBy: Marko Nieminen; individualCount: 23; lifeStage: larva; Taxon: scientificName: Euphydryas maturna; order: Lepidoptera; family: Nymphalidae; genus: Euphydryas; specificEpithet: maturna; taxonRank: species; Location: country: Finland; stateProvince: Uusimaa; municipality: Pornainen; locality: Mäkelä; verbatimElevation: 60 m; verbatimCoordinates: 60°27.32'N 25°17.94'E; verbatimLatitude: 60°27.32'N; verbatimLongitude: 25°17.94'E; decimalLatitude: 60.4554; decimalLongitude: 25.2991; Identification: identifiedBy: Marko Nieminen; dateIdentified: 2014; Event: samplingProtocol: visual search; eventDate: 2014-08-27/09-11; Record Level: language: en; basisOfRecord: Photographed; source: marko.nieminen@faunatica.fi

Type status: Other material. Occurrence: occurrenceRemarks: number of larval groups counted (with unknown number of larvae per group); recordedBy: Kari Nupponen; individualCount: 24; lifeStage: larva; Taxon: scientificName: Euphydryas maturna; order: Lepidoptera; family: Nymphalidae; genus: Euphydryas; specificEpithet: maturna; taxonRank: species; Location: country: Finland; stateProvince: Uusimaa; municipality: Pornainen; locality: Honkasenkalliot; verbatimElevation: 60 m; verbatimCoordinates: 60°26.51'N 25°19.27'E; verbatimLatitude: 60°26.51'N; verbatimLongitude: 25°19.27'E; decimalLatitude: 60.4419; decimalLongitude: 25.3211; Identification: identifiedBy: Kari Nupponen; dateIdentified: 2014; Event: samplingProtocol: visual search; eventDate: 2014-09-10/11; Record Level: language: en; basisOfRecord: Photographed; source: marko.nieminen@faunatica.fi

Ecology

Totally 167 larval groups were located, all on Melampyrum spp. (Fig. 1). In some cases, at least two original larval groups had probably merged. All larval groups were either in clear-cuts (usually close to the edges, and sometimes within the forest 0-5 m from the clear-cut [Figs 2, 4]), in thinned and light commercial forests (Figs 3, 4), or in open powerline corridors (Fig. 5).

Due to the dry conditions in July and August, many or even all host plants had withered especially in open rocky areas. Therefore, reliable identifications based on plant morphology were possible for 121 samples. Of the identified samples, 30 plants (25%) were M. pratense and 91 plants (75%) M. sylvaticum. In addition, three larval groups have been found in the same area in the autumn of 2013, all on M. sylvaticum (Jari-Pekka Kaitila, personal observations).

Discussion

The regional host plant use of E. maturna is highly variable throughout its range (Table 1), but is apparently restricted to only a couple of preferred species used for oviposition within any particular region. For example, Fraxinus is the most regularly used oviposition-plant genus in the Central Europe (e.g. Cizek and Konvicka 2005, Levente 2005, Freese et al. 2006, Dolek et al. 2013), whereas lower plants such as Veronica longifolia are often used in the eastern areas (e.g. Korshunov and Gorbunov 1995, Gorbunov and Kosterin 2007). However, it seems common that the post-diapause larvae feed on a wider spectrum of host plants than are used for oviposition (Gorbunov and Kosterin 2007, Dolek et al. 2013), for example Plantago lanceolata is frequently used after diapause in Austria (Freese et al. 2006). There may be regional differences in preference also within the Finnish range, as all females observed during their search for oviposition-plants ignored M. sylvaticum in a study performed about 200 km to the northeast of this study area (Wahlberg 1998). Moreover, the importance of other host plants than M. pratense and M. sylvaticum still remain uncertain throughout Finland.

The use of M. sylvaticum as a host plant (Fig. 1) considerably increases both the suitable breeding area of E. maturna and the amount of resources available for it. In the study area, the increase in both of these variables must be manyfold, but remains to be quantified. Melampyrum pratense is much more vulnerable to desiccation and withering because it grows in drier sites than M. sylvaticum. The ability to use both of these Melampyrum species is extremely important in dry summers such as 2014, when more than 90% of host plants had withered in several sites. That high rate of dry host plants has likely increased mortality of groups of small larvae and may also decrease overwintering success due to starvation of larvae, which are common phenomena in another larval group-forming species Melitaea cinxia in Finland (e.g. Kuussaari et al. 2004).

Some leaves of Vaccinium myrtillus had been eaten within some larval webs. Even though I could not confirm that E. maturna larvae had eaten them, it is, however, likely because other herbivorous larvae were not observed and Melampyrum individuals were almost completely dry in and around these larval nests. Therefore, larvae may have used V. myrtillus to rescue themselves from starvation. The same explanation may apply to the odd observations of larvae feeding on e.g. Fagus, Populus and Salix regularly referred to in the literature (e.g. Korshunov and Gorbunov 1995, Gorbunov and Kosterin 2007, Dolek et al. 2013). A further explanation for 'odd' host records is that the actual host plants often become consumed completely leaving only non-host plants visible among and next to larval webs.

Acknowledgements

I thank Kari Nupponen for help in the field work and collecting information on host use in Russia and adjacent areas, Henry Väre for the identification of host plant samples, and Jari-Pekka Kaitila for his observations on M. sylvaticum as a host plant of E. maturna in the same area in 2013. The field work was financed by Lemminkäinen Infra Oy.

References Bowers M. Deane 1983 The role of iridoid glycosides in host-plant specificity of checkerspot butterflies Journal of Chemical Ecology 9 4 475 493 http://dx.doi.org/10.1007/bf00990220 10.1007/bf00990220 Cizek Oldrich Konvicka Martin 2005 What is a patch in a dynamic metapopulation? Mobility of an endangered woodland butterfly, Euphydryas maturna Ecography 28 6 791 800 http://dx.doi.org/10.1111/j.2005.0906-7590.04268.x 10.1111/j.2005.0906-7590.04268.x Dolek Matthias Freese-Hager Anja Geyer Adi Balletto Emilio Bonelli Simona 2013 Multiple oviposition and larval feeding strategies in Euphydryas maturna (Linné, 1758) (Nymphalidae) at two disjoint European sites Journal of Insect Conservation 17 2 357 366 http://dx.doi.org/10.1007/s10841-012-9516-x 10.1007/s10841-012-9516-x Eliasson C. 1991 Studier av boknätfjärilens, Euphydryas maturna (Lepidoptera. Nymphalidae, förekomst och biologi i Västmanland Entomologisk tidskrift 112 113 124 Eliasson C. U. Shaw M. R. 2003 Prolonged life cycles, oviposition sites, foodplants and Cotesia parasitoids of Melitaeini butterflies in Sweden Oedippus 21 1 52 Freese A. Benes J. Bolz R. Cizek O. Dolek M. Geyer A. Gros P. Konvicka M. Liegl A. Stettmer C. 2006 Habitat use of the endangered butterfly Euphydryas maturna and forestry in Central Europe Animal Conservation 9 4 388 397 http://dx.doi.org/10.1111/j.1469-1795.2006.00045.x 10.1111/j.1469-1795.2006.00045.x Gorbunov P. Kosterin O. 2007 The butterflies (Hesperioidea and Papilionoidea) of North Asia (Asian part of Russia) in nature Rodina & Fodio Moscow 408 Kaitila J. P. Nupponen K. Kullberg J. Laasonen E. M. 2010 Butterflies and moths Rassi P. Hyvärinen E. Juslén A. Mannerkoski I. The 2010 Red List of Finnish Species Ympäristöministeriö & Suomen ympäristökeskus Helsinki 685 978-952-11-3806-5 Konvicka M Cizek O Filipova L Fric Z Benes J Krupka M Zamecnik J Dockalova Z 2005 For whom the bells toll: Demography of the last population of the butterfly Euphydryas maturna in the Czech Republic. Biologia 60 551 557 Korshunov Y. P. Gorbunov P. Y. 1995 Butterflies of the Asian part of Russia. A handbook University Press Ekaterinburg 202 Russian Kuussaari M. van Nouhuys S. Hellmann J. Singer M. C. 2004 Larval Biology of Checkerspots Ehrlich P. R. Hanski I. On the Wings of Checkerspots: A Model System for Population Biology Oxford University Press New York 408 978-0-19-515827-4 Levente Á. 2005 Biomonitoring of the butterfly fauna in the Drava region (Lepidoptera: Diurna) Natura Somogyiensis 7 63 73 Nieminen Marko Suomi Johanna Nouhuys Saskya Van Sauri Pauliina Riekkola Marja-Liisa 2003 Effect of iridoid glycoside content on oviposition host plant choice and parasitism in a specialist herbivore Journal of Chemical Ecology 29 4 823 844 http://dx.doi.org/10.1023/a:1022923514534 10.1023/a:1022923514534 Rákosy L. Pecsenye K. Mihali C. Tóth A. Varga Z. 2012 Taxonomic review of Euphydryas maturna (Linnaeus, 1758) (Lepidoptera, Nymphalidae) with description of a new subspecies from Dobrogea (Romania) and notes on conservation biology Acta Zoologica Academiae Scientiarum Hungaricae 58 145 161 Tuzov V. K. Bogdanov P. V. Churkin S. V. Dantchenko A. V. Devyatkin A. L. Murzin V. S. Samodurov G. D. Zhdanko A. B. 2000 Guide to the butterflies of Russia and adjacent territories (Lepidoptera, Rhopalocera). Volume 2: Libytheidae, Danaidae, Nymphalidae, Riodinidae, Lycaenidae Pensoft Sofia & Moscow 581 Wahlberg N. 1998 The life history and ecology of Euphydryas maturna (Nymphalidae: Melitaeini) in Finland Nota lepidopterologica 1998 154 169 Wahlberg Niklas 2001 The Phylogenetics And Biochemistry Of Host-Plant Specialization In Melitaeine Butterflies (Lepidoptera: Nymphalidae) Evolution 55 3 522 537 http://dx.doi.org/10.1111/j.0014-3820.2001.tb00786.x 10.1111/j.0014-3820.2001.tb00786.x

Larval web of Euphydryas maturna on Melampyrum sylvaticum in Sipoo, S Finland (November 2nd, 2014).

Clear-cut edge habitat of Euphydryas maturna. Clear-cut edges typically remain suitable for breeding for some years only until they become overgrown by tall grasses and tree seedlings.

Euphydryas maturna habitat in a commercial, thinned spruce-dominated forest. Such habitats are probably suitable after thinning for several years.

Euphydryas maturna habitat in a commercial, thinned pine-dominated forest with ca. 30-year old trees, and in a clear-cut edge. This kind of forest habitat is probably suitable after thinning for several years, but longer than spruce-dominated forests (Fig. 3). Also, edge habitats in these relatively dry habitats overgrow somewhat slower than in moister edges (Fig. 2).

Powerline habitat of Euphydryas maturna. Vegetation under powerlines is kept open continuously, so powerline habitats may function both as breeding places and dispersal corridors.

Records of host plants used for oviposition by Euphydryas maturna females and/or for feeding by pre-diapause larvae.

Species Locations References
Fagus sylvatica Europe Dolek et al. 2013
Fraxinus angustifolia Carpathian Basin and SE Europe, Hungary Dolek et al. 2013, Rákosy et al. 2012
Fraxinus excelsior Austria, Czech Republic, Germany, Hungary, Italy, Russia, Sweden Dolek et al. 2013, Eliasson 1991, Freese et al. 2006, Konvicka et al. 2005, Levente 2005, Rákosy et al. 2012, Tuzov et al. 2000
Fraxinus ornus Carpathian Basin and SE Europe Dolek et al. 2013, Rákosy et al. 2012
Ligustrum vulgare Czech Republic, Germany, Hungary Dolek et al. 2013, Freese et al. 2006, Konvicka et al. 2005, Rákosy et al. 2012
Lonicera Russia Tuzov et al. 2000
Melampyrum sylvaticum Finland This study
Melampyrum pratense Finland Wahlberg 1998
Plantago lanceolata Komi Republic Gorbunov and Kosterin 2007
Populus alba Russia Tuzov et al. 2000
Populus tremula Europe, Russia Dolek et al. 2013, Tuzov et al. 2000
Salix caprea / Salix Europe, Russia Dolek et al. 2013, Tuzov et al. 2000
Spiraea Russia Tuzov et al. 2000
Syringa vulgaris Russia, Sweden Dolek et al. 2013, Eliasson and Shaw 2003, Tuzov et al. 2000
Veronica longifolia Finland, Komi Republic, Krasnoyarsk area, Omsk area, Novosibirsk Province Gorbunov and Kosterin 2007, Wahlberg 1998
Viburnum opulus Finland, Germany, Sweden Dolek et al. 2013, Eliasson 1991, Wahlberg 1998
Viola arvensis Komi Republic Gorbunov and Kosterin 2007
Viola canina Komi Republic Gorbunov and Kosterin 2007