Distribution of Carex pallidula ( Cyperaceae ) in Europe

Carex pallidula is a European species which is often overlooked because it is similar in appearance to C. digitata. So far, this species has been recorded from ten European countries. During herbarium studies in 2014 and 2015, the occurrence of C. pallidula was confirmed for another six European countries (Albania, Austria, Greece, Romania, Serbia, and Switzerland), providing a new insight into its distribution. A list of new localities of C. pallidula and a distribution map for Europe are provided. A key for determining some taxa within the section Clandestinae is presented. Finnish material of the supposed hybrid of C. digitata and C. pallidula is considered to be young specimens of C. digitata.

Carex pallidula Harmaja is similar to C. digitata and the differences are rather subtle [4,7].In general appearance, C. pallidula is more upright and taller than C. digitata and the inflorescences are usually longer than the leaves, in contrast to C. digitata.Besides, specimens of C. pallidula are a bit paler in color because the female glumes are pale brown, rather than reddish-brown as in C. digitata.Similarly, the lowest bract sheath is usually paler and more greenish than that of C. digitata, which is always reddish-purple.However, the most reliable features are the size and form of the utricles (e.g., [7,11,12]).Holub [11] gives drawings of the utricles of both species, in which the differences are obvious (see also the photograph in Harmaja [7]).According to Holub [11], Carex pallidula has smaller utricles, 2.9-3.6 mm long, which are more shining and have a very short, blunt beak, while C. digitata's utricles are longer, 3.4-4.2mm, more hairy and with a longer, tapering beak.Harmaja [7] gives slightly bigger sizes of the utricles:  and C. rhizina [6,[12][13][14].Although the taxa within the section Clandestinae are rather similar in appearance, they have been demonstrated to be an artificial group.The section is polyphyletic despite the fact that all the species look alike (P.Jiménez-Mejías, personal communication, 2016).There are only a few hybrids known within this section.The one which is relatively most common is C. ×dufftii Hausskn.(C.digitata × C. ornithopoda), known from North(-East) and Central Europe [14].The hybrid C. digitata × C. rhizina has been recorded for Norway [15], whereas C. digitata × C. pallidula has been reported from Finland [7].
Carex pallidula is a temperate-European species with a disjunctive range [16].It occurs in Northern Europe [4,5,7,17] and in some central and southeastern parts of Europe, from the highlands in the south of Poland to the northern part of the Balkan Peninsula [4,7,11,18,19].Jiménez-Mejías and Luceño [20] reported a similar distribution pattern for this species, but the map shows the Caucasus by mistake.They erroneously merged C. pallidula with C. pamirica var.dichroa (Malyschev) T. V. Egorova [20].According to Koopman [14], Carex pallidula is currently known from the following nine countries worldwide: Norway, Sweden, Finland, Russia, Poland, the Czech Republic, Slovakia, Slovenia, and Montenegro.Additionally, it is also known from Bulgaria [21] .

Material and methods
The available material of C. digitata, C. ornithopoda subsp.ornithopoda, C. ornithopoda subsp.ornithopodioides, C. rhizina, and C. pallidula in the herbaria of Berlin (B), Vienna (W) and Wrocław (WRSL) was studied in 2014 and 2015, as these species are sometimes confused with one another.Besides, material of the first author's private herbarium and of C. pallidula collected during fieldwork in the Czech Republic in 2014, deposited in the Herbarium of Szczecin University (SZUB), was taken into account.We have also examined the material of C. digitata × C. pallidula on loan from the Herbarium of the Finnish Museum of Natural History (H; Appendix S1 and Appendix S2).Abbreviations of herbaria follow Index Herbariorum [22].

Results
Carex pallidula was detected in the following six European countries: Albania, Austria, Greece, Romania, Serbia, and Switzerland, where its occurrence was unknown until now.All the material was originally labeled as C. digitata (Appendix S1).Carex pallidula was identified only in the herbarium material from Berlin (B) and Vienna (W).A search through the material in Wrocław (WRSL) did not reveal any sheets with C. pallidula, although this species is mentioned for central-southern Poland [18,19].
The oldest collections of C. pallidula, newly reported in this paper, are from NE Greece (near Nomós Dráma, Rodopi), SE Serbia (Pirot), SW Romania (near Herkulesbad), and E Switzerland (Molinis, E of Chur, Graubünden).In each of these countries, only one locality for this species was found.Two recent collections, from 2007 and 2010, have been made in northern Albania.Eleven new localities of C. pallidula were recorded from Austria and these are scattered throughout the country: three in Lower Austria and Vienna (E Austria), four in Upper Austria and Salzburg (N Austria), two in Vorarlberg (W Austria), one in Carinthia, and one in Styria (S Austria; Appendix S1, Fig. 1).
The hybrid C. digitata × C. pallidula has hitherto been recorded from a few locations in Finland.Harmaja [7] was the first who identified this hybrid.Although Harmaja wrote "HH" on p. 151 indicating that his material was deposited in H, the staff from the Herbarium of the Finnish Museum of Natural History could not find any specimens of Carex deposited by Harmaja in their collections.However, we were able to study some other material of this supposed hybrid from H comprising eleven gatherings (Appendix S2).After the name of four collections the finders added a question mark and one more with "cf.", obviously not being sure of their determination, which is understandable, taking into account the striking similarity of the putative parents.The other collections from H have more or less normally developed utricles and nuts, which are identical in shape and size to C. digitata.Besides, the anthers were normally developed in all the collections which were examined.All examined collections of the presumed hybrid, in our opinion, represent the same taxon and comprise young material of C. digitata, rather than the supposed hybrid.

Discussion
A valid description of Carex pallidula has been published in 2005, and in the scarce literature it has been reported until now from ten countries worldwide, all in Europe [14].It is strikingly similar to the well-known C. digitata.The characters mentioned in literature are not always as clear-cut as supposed; however, the most reliable features are the size and shape of the utricles [4,7,11] (Fig. 1).Carex digitata and C. pallidula are very similar in appearance, which may suggest a close affinity, but the hybrid of both species has not been yet detected with certainty.The supposed hybrid material seen from Finland is here regarded as young material of C. digitata.Carex pallidula is often confused with C. digitata, therefore, the hybrid of these two species may exist but may not be recognized.Tyler's studies [23] show that gene flow between C. pallidula and C. digitata appears to be very limited.Also Harmaja [4,7] pointed out that hybrids between this species are not common.
Carex pallidula is often regarded as a more northern species, probably because it was first found in Scandinavia [7,9].Fig. 2 makes clear that it has a much wider range in Europe, from Scandinavia to the Balkan Peninsula.Obviously it is often overlooked and/or misidentified for C. digitata, as Holub [11] already made clear with his search through Czech and Slovakian herbaria.In the Czech Republic, C. pallidula does not seem to be very rare.During the fieldwork by the first two authors in 2014, this species proves to be rather common in Bohemia (CZ).In fact the precise geographical distribution of C. pallidula has not been delineated yet [10].Based on literature, the locations in Scandinavia [4,9,10], Russia [17], Poland [18,19], the Czech Republic, Slovakia [11], Slovenia, and Montenegro [10] have been identified.However, the new data presented here indicate that in Central and Southern Europe, the species is more common than suggested by previous research (e.g., [9][10][11]18,19].The eleven findings in Austria show that the species seems to be less rare in this country.However, the fact we could find only one, old, collection for four other new countries, Greece, Romania, Serbia, and Switzerland, reflects only the historical distribution of the species.The occurrence of C. pallidula in these countries is still questionable.Carex pallidula was also mentioned by Valev and Kitanov [21] in Flora Bulgaria, but it was missing in Koopman [14].The first author of this article collected material of this species in 2013 in SW Bulgaria, on Gocev Vrah, Slavyanka (Appendix S1).
We checked all the German material in Berlin, but C. pallidula did not show up for this country.It also seems to be absent in Hungary (A.Mesterházy, personal communication, 2015).However, as it occurs in the neighboring countries (Austria, the Czech Republic, Poland, and Switzerland), the presence of this species in Germany and Hungary should be expected.To get a more complete picture of the distribution of C. pallidula in Europe other searches in Central and Eastern European herbaria and/or intensive fieldwork are needed and these may reveal C. pallidula for these two countries.Its occurrence in nearby Asia, e.g., on the Caucasus, should not be ruled out [20].

Fig. 2
Fig. 2 Distribution of Carex pallidula Harmaja in Europe, according to herbarium vouchers and literature.The outlined areas indicate dense populations.Black circles -single, isolated locations known from the literature.Triangles -new locations based on herbarium material.White circles -single locations (where only one old collection for each country was found in the studied herbarium material).