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On the occurrence of Anogramma leptophylla in Bulgaria 14TH SYMPOSIUM ON THE FLORA OF SOUTHEASTERN SERBIA AND NEIGHBORING REGIONS 26-29.06.2022, Kladovo, Serbia

On the occurrence of Anogramma leptophylla in Bulgaria
Georgi Kunev1*, Krasimir Lakovski
1Department of Botany, Faculty of Biology, Sofia University “St. Kliment Ohridski,
8 “Dragan Tzankov” Blvd., Sofia 1164, Bulgaria, e-mail: *
26-29.06.2022, Kladovo, Serbia
During the early vegetation season of 2022, we have found Anogramma leptophylla
(Pteridaceae) on the territory of Bulgaria, in two localities and about twenty
microsites. No herbarium materials of the species previously collected in Bulgaria
were found in the national indexed herbaria SO, SOM and SOA, nor any historical
records were traced back in the major floristic references on Bulgarian flora
(Ahtarov & Yordanov 1963; Assyov & Petrova 2012; Stoyanov & al.2021). Evidently,
this is the first registered find of the species in the country. With the current
presentation, we provide information on the species overall morphology, based on
collected specimens, SEM morphograps of spores and sporangia, phenology,
distribution and habitat characteristics, and provisional threatened status based on
the IUCN criteria.
Species description
Anogramma leptophylla is a fern species with unusual lifecycle. The sporophyte may live for a
few months, i.e. dies annually, while the gametophyte may stay perennial as dormant
underground tubercles. The fronds are dimorphic. First fronds that appeared during the season
(Fig. 1) are shorter, petioles up to 1-1.5 cm, lamina 2-3 cm, fan-shaped, deeply lobed, pinnae
broader, pinnules obovate at tips, mostly sterile. Secondary (fertile) fronds (Fig. 2) are taller, 3-8
(-12)cm, petioles 2-5 cm, lamina 3-7 cm, pale green, membranous, bi-or tripinnate, pinnae
narrower, pinnules obtuse-acute at tips, early in the season their margins are convolute to cover
immature sporangia (Fig. 3), sori oblong-linear, exindusiate, developed along dichotomously
brunched veins (Fig. 5). Sporangia are more or less spherical, variable in size, short stalked, 220-
310 µm in length (stalk included) (Fig. 13). Spores are brown to dark-brown, tetrahedral-
hemispherical in equatorial view, equatorial diameter is (45)-45.9-(48.1) µm (Figs. 11-12). The
data on spore morphology and measures correspond well to those presented by Vaganov & al.,
2017 for A. leptophylla from South-West Asia. Chromosome number n=26 (Rasbach & Reichstein
1990); n=29,58 (Tryon 1990). Materials from Bulgaria were not subject of chromosome count. Chronology of fieldwork with phenological observation on the species
1) The first observation of A. leptophylla was made by the first author, on 16.02.2022,on the slopes of Skalataheight,
the Struma Valley (Southern), Blagoevgrad District, on the ground, under rock ledges, and in niches, at 120 m alt. At
this particular microsite, numerous gametophytes and about 80 sporophytes were noticed. Sporophytes were mostly
juvenile, with fertile fronds just starting to emerge (Fig. 1). No sporangia were observed at that date. 2) On
25.03.2022, the observed plants were bearing not fully developed fertile fronds with immature sporangia (Figs. 2-3).
Two more microsites were located on the slopes of 'Skalata' height with not more than 10 individuals at a spot. 3) On
23.04.2022 a third trip was taken on. The observed plants were in final stage of development of their sporangia, which
were mostly matured, dark-brown or blackish and ready for spore dispersal. Several individuals were collected, from
which latter spores for SEM examinations were extracted (materials at SO 108162 and SOM 177701) (Figs 4-5; 7-13).
More sites of the species were located on the neighboring Pchelinaheight, about 3.6 km in south direction from the
first observed locality. 4) On 28.04.2022, the second author observed the species on even more sites in both locations.
With the addition of these findings, the microsites of A. leptophylla reached 20 (Fig. 14), with about 1000 individuals
overall. This shows that the species has stable populations and it is perhaps distributed on the neighboring heights,
which however have been not investigated by us. During the last two field excursions, the sterile leaves on most of the
observed individuals of the species were withered or completely dried. However, in some individuals we have
observed well-developed sporangia on the ventral side of the so-called 'sterile' fronds, although less in number
comparing with the fertile fronds of the same individuals (Fig. 10). 5) On 19.06.2022, the individuals of the species at
Pchelinaheight were completely dried with open sporangia and some spore still attached on the frond surface.
Therefore, it could be conclude that the aboveground phase of the lifecycle of A. leptophylla in Bulgarian populations
of the species completes in about 6 months - December-May.
Distribution and habitat
The species has been observed on steep, rocky slopes with inclination of about 40°.The
microsites are situated mostly at the base of tall rocks, under rock ledges, in niches or rarely in
аshallow negative topographic forms, in more or less shaded spots. Plants grow mostly from
soil or fine debris composed of sand, gravel particles and dried organic matter. Microsites
most often face West, Southwest or Northwest. The climate is of transitional Mediterranean
type, with mean annual temperature 15.2 °C, average temperature for the coldest month
(January) of 3.5°C and precipitation maximum during winter months (Climate-Data 2022). A.
leptophylla is an Atlantic-Mediterranean element, found in regions with high rainfall and
relative humidity. The Struma River and closely located hot thermal spring at Rupitelocality
provide the required level of humidity for the growth of the species at the reported sites. The
species is noncompetitive and occupies pioneer sites. It grows solitary or it is associate with
other weak competitors, mostly annuals. The species composition at the localities includes
Teesdalia coronopifolia,Viola kitaibeliana,Asterolinon linum-stellatum,Crepis sancta,
Hypochaeris glabra,Umbilicus rupestris,Fumaria officinalis,F. rostellata,Myosotis
ramosissima,Cardamine hirsuta,Galium aparine,Spergula pentandra,Vulpia ciliata,Tolpis
umbellata,Aira elegantissima,Psilurus incurvus,Micropyrum tenellum,Filago arvensis, etc.
Fig. 1 25.03.2022 25.03.2022
Fig. 2Fig. 3
Fig. 4Fig. 6Fig. 5
23.04.2022 23.04.2022
km2(2 grid squares 2x2 km), therefore the species responds against criteria B1 and B2 as aCritically Endangered and
as Endangered against criterion D. Considering the historical records (SOA 000162, Stoyanov 1921; Micevski 1985) for
the species from the closely situated Belasitsa Mt (Mt Kerkini in Greece) and the availability of adequate habitats in
the neighboring heights Byalata kashtaand Kosmatitsa(Fig.14), we propose provisional threatened status of A.
leptophylla in Bulgaria as Vulnerable.If more locations are found in following years the species than it would be better
down-listed to Nearly Threatened. (IUCN 2012). We recognized shrub encroachment as most serious threat for the
species in Bulgaria. This is especially true for the northern and northwestern slopes of the 'Skalata' height, where
Crataegus monogyna,Pyrus pyraster,P. amygdaliformis,Paliurus spina-christi,Prunus spinosa,Rubus spp. overgrow
upon significant areas. Moderate grazing of goats would stabilize this process and open up the grass-shrub coenoses
to establish suitable pioneer sites for A. leptophylla.
Conservation status and threats
A. leptophylla is a species evaluated as aLeast
Concern on European scale (Garcia Criado & al.
2017). However, it is impossible to evaluate the
status of the species at a regional scale, because not
all of the IUCN criteria could be applied at present
level of knowledge for its population trends in
Bulgaria. Currently two subpopulation with overall
20 microsites and up to 1000 individuals were
observed in the country. The ‘Extent of occurrence'
(EOO) is 0.8 km2and Area of occupancy (AOO) is 8
Fig. 7Fig. 8 Fig. 9Fig. 10
Fig. 11 Fig. 12 Fig. 13
Fig. 14
Ahtarov, B., & Yordanov, D. 1963: Pteridophyta. In: Jordanov, D. (ed.), Flora Reipublicae Popularis Bulgaricae, vol. 1, 82144.In Aedibus Academiae Scientiarum Bulgaricae, Serdicae (in Bulgarian).
Assyov, B., Petrova, A. (eds.), 2012: Conspectus of the Bulgarian vascular flora. Distribution maps and floristic elements, ed. 4. BBF, Sofia.
Garcia Criado & al.2017: European red list of lycopods and ferns.
IUCN 2012: Guidelines for Application of IUCN Red List Criteria at Regional and National Levels, Version 4.0. Gland, Switzerland and Cambridge, UK
Micevski, K., 1985: Flora of FR Macedonia. 1/1, 52. Makedonska akademija na naukite umetnostite, Skopje (in Macedonian).
Nakazato, T., & Gastony, G. J. 2003: Molecular phylogenetics of Anogramma species and related genera (Pteridaceae: Taenitidoideae). Systematic Botany, 28(3), 490-502.
Rasbach, H., & Reichstein, T. 1990: The chromosome number of Anogramma leptophylla (Adiantaceae: Pteridophyta) from Europe. Fern Gaz, 13(6), 341-348.
Stoyanov, K., Raycheva Ts. & Cheschmedzhiev I. 2021: Key to the native and foreign vascular plants in Bulgaria. Agricultural University Plovdiv Academic Press (in Bulgarian).
Stoyanov, N. 1921: Floristic materials from Mt Belasitsa. Ann. of Sofia Univ. “St. Kliment Ohridski”, (in Bulgarian).
Tryon, R. M. 1990): Pteridaceae. In: Pteridophytes and gymnosperms, 230-256. Springer, Berlin, Heidelberg.
Vaganov, A. V., Gureyeva, I. I., Kuznetsov, A. A., Shmakov, A. I., & Romanets, R. S. 2017: Data on spore morphology of Cerosora microphylla (Anogramma microphylla)(Pteridaceae). Biosystems
Diversity, 25(2), 141-144.
Zhang, L., Zhou, X. M., Lu, N. T., & Zhang, L. B. 2017: Phylogeny of the fern subfamily Pteridoideae (Pteridaceae; Pteridophyta), with the description of a new genus: Gastoniella. Molecular
Phylogenetics and Evolution, 109,59-72.
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The book contains determination keys for the vascular plants (wild and cultivated) in Bulgaria and the neighboring territories of Romania, Serbia, North Macedonia, Greece, and Turkey. The determination tables contain 6963 species (native and foreign) in 1322 genera from 310 families. (in Bulgarian)
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We used the method of scanning electron microscopy (SEM) to study the representatives of the genus Anogramma from South-West Asia and the Himalayas. To confirm the presence of Cerosora microphylla (Hook.) R.M. Tryon in China (hence, the absence of Anogramma microphylla (Hook.) Diels), we revealed the features of external morphology of spores that are not inherent in representatives of the genus Anogramma: absence of an equatorial ridge, roundish-triangular shape of the spores in the proximal-polar and distal-polar positions; absence of roller-like bulges extending upward in the form of ridges along the contour of the distal side of the spore; roller-like folds extending upward in the form of ridges both on the proximal and distal sides of the spore. In addition, one feature revealed for C. microphylla – spherical tubercles between the proximal and distal roller-like folds located along the spore equator – indicates its high species-specificity.
As the second most genera-rich fern family, Pteridaceae contain more than 1000 species contributing to ca. 10% of extant leptosporangiate fern diversity. The subfamily Pteridoideae is one of the five subfamilies often recognized. The circumscription of Pteridoideae has not been clear. A large number of species have not yet been included in any molecular analyses before. In this study, DNA sequences of six plastid loci of 154 accessions representing ca. 87 species in 14 genera of Pteridaceae subfam. Pteridoideae and four accessions representing two species in subfam. Parkerioideae and one species of subfam. Adiantoideae as outgroups were used to infer a phylogeny using maximum likelihood and maximum parsimony. Our analyses show that (1) Pteridoideae is monophyletic and the newly defined subfamily is composed of 14 genera including a newly described genus; (2) Pteridoideae is resolved into four strongly supported monophyletic clades: the Pteris clade, the Actiniopteris + Onychium clade, the JAPSTT clade, and the GAPCC clade, these being supported by not only molecular data but also morphological features and distribution information; (3) Onychium is confirmed as monophyletic and accessions of Onychium are resolved into two strongly supported clades, the O. cryptogrammoides clade and the O. siliculosum clade; and (4) Accessions of the traditionally defined Anogramma are resolved as paraphyletic in relation to Cerosora, Cosentinica, and Pityrogramma. Three species traditionally treated in Anogramma are in fact more closely related to Cerosora and Pityrogramma than they are to Anogramma. Gastoniella Li Bing Zhang & Liang Zhang, gen. nov. is described to accommodate these species and three new combinations are provided. Three currently known species of Gastoniella are distributed in the Ascension Island in South Atlantic Ocean, central Mexico, and tropical America, respectively. The new genus is distinct from Anogramma s.s. in having ultimate segments linear not obviously broadening toward the upper portion.
Anogramma is a genus of eight putative species with small annual sporophytes and potentially perennating gametophytes. Phylogenetic relationships within the genus as well as its relationships with other putatively taenitidoid genera and with traditionally cheilanthoid Cosentinia vellea have been poorly resolved and are investigated here. Maximum parsimony, maximum likelihood, and Bayesian inference analyses of rbcL sequences were used to test 1) the monophyly of Anogramma, 2) support for the proposed specific distinctness of A. guatemalensis and A. caespitosa from A. leptophylla, and 3) the asserted close (sister) relationship between Anogramma and Pityrogramma, as well as to infer the phylogenetic relationships among these genera. Results reveal that Anogramma in the traditional sense is polyphyletic. Anogramma guatemalensis and A. caespitosa nest within A. leptophylla. Pityrogramma is not sister to Anogramma as a whole but only to A. chaerophylla and A. novogaliciana. Anogramma osteniana is deeply separated from its traditional congeners and the new combination Jamesonia osteniana (Dutra) Gastony is made. Cosentinia vellea should not be subsumed within Cheilanthes but instead should be considered a taenitidoid genus closely related to A. leptophylla and A. lorentzii. Neighbor joining analysis of Amplified Fragment Length Polymorphism data sets inferred relationships among the A. leptophylla accessions, embedding A. guatemalensis and A. caespitosa in respective New World and Old World clades of A. leptophylla.
  • N Stoyanov
Stoyanov, N. 1921: Floristic materials from Mt Belasitsa. Ann. of Sofia Univ. "St. Kliment Ohridski", (in Bulgarian).