1. Introduction

The Hyrcanian forests stretch as a green continuous arc from the Talish in Azerbaijan Republic, cover the northern slopes of the Alborz Mountains along three Iranian Provinces (Gilan, Mazandaran and Golestan) and end in Golestan National Park (GNP) (Fig. 1). There are some isolated outliers of the Hyrcanian forests in North Khorassan Province (Jowzak area) and East Azarbaijan Province in the Arasbaran Protected Area (APA) (Akhani et al., 2010 and references therein). The area is climatically and topographically very heterogeneous, with a unique flora and vegetation (Frey and Probst, 1986; Akhani et al., 2010). These forests have a surface area of about 1.9 mio ha in Iran and 0.1 mio ha in Azerbaijan (Anonymous, 2010). Although large parts of the mesic areas are covered by lowland and montane forests and wetlands, there are also transitional habitats in nearby areas produced by the presence of arid and semi-arid Irano-Turanian flora and the high elevations of the Alborz Mountains. The diversity of transition zones between forests and adjacent Irano-Turanian vegetation is extremely high. For example, a total of 1362 species has been documented in GNP, which is almost 19% of the entire Iranian flora (Akhani, 1998, 2005).

The Hyrcanian forests contain Arcto-Tertiary relict elements, which are of high phytogeographical interest. However, the intensification of human activity in this threatened forest zone has made conservation a major priority. Accordingly, in 2019, the Hyrcanian forests were designated a UNESCO World Heritage property (https://whc.unesco.org/en/list/1584).

In our first review paper we provided an overview of the flora, climate, major vegetation units, phytogeography, palaeoecology and conservation status of the Hyrcanian forests (Akhani et al., 2010). In this paper, an annotated critical checklist of endemic and near endemic species is provided, with plant chorology, conservation status and habitats. To evaluate phytogeographical status and threat categories, distribution maps are provided for all taxa. Further, we try to answer the following questions: (i) Is the Hyrcanian forest zone an autochthonous floristic province under the Euro-Siberian (boreal) region? (ii) Which species are endangered and require specific protection measures, and which taxa are Data Deficient based on IUCN threat categories?

2. Material and methods 2.1. Sources for taxonomic evaluation, literature and herbarium data

We searched for any floristic records from the northern provinces of Iran (Gilan, Mazandaran and Golestan), GNP, and the APA. The main sources of our data include 181 volumes of Flora Iranica (Rechinger, 1963–2015), 143 volumes of Flora of Iran (Research Institute of Forests and Rangeland: Assadi et al., 1992–2016), floristic records of the APA (Assadi, 1987, 1988; Hamzeh'ee et al., 2010) and GNP (Akhani, 1998), and our own collections and field studies over the entire Hyrcanian forests over the last three decades.

We constructed a second database consisting of only endemic and near endemic species. Complete information, including location data, elevational range and any ecological information, have been added to the data base. The chorology data were expanded from reliably identified herbarium specimens held in the following herbaria: 1) Herbarium of Halophytes and C₄ Plant Research Laboratory (Hb. Akhani, School of Biology, University of Tehran); 2) Herbarium of Iranian Research Institute of Plant Protection (IRAN); 3) Herbarium of Research Institute of Forests and Rangelands (TARI) and 4) Herbarium of Botanical Garden and Botanical Museum of Berlin (B). Access to the Central Herbarium of University of Tehran (TUH) was not possible except for one specimen. For some critical taxa we checked either type specimens in mentioned herbaria or received photos from the herbarium of the Conservatoire botanique de la Ville de Genève (G), and through JSTOR, as well as some photos of specimens from Komarov Botanical Institute (LE).

All literature and herbarium data were georeferenced and converted into coordinates. Our access to reliable records outside of Iran, in particular the Caucasus, was limited. Therefore, we used point maps available in the monumental work, Flora Caucasus (Flora Kavkaza) (Grossheim, 1939, 1940, 1950, 1952, 1962, 1967), converting the points into coordinates. With the same method, we have extracted the point data of some arboreal species from Browicz's chorology of trees and shrubs in SW Asia (Browicz, 1982, 1983, 1984, 1986, 1988, 1991, 1992, 1994, 1996; Browicz and Zieliński, 1984). In total 5408 records (1272 herbarium data and 4136 literature records) have been used to generate distribution data and calculate the frequency of species. Records in the literature and specimens that we have been able to see in the herbarium are considered here as “seen plant”.

Nomenclature of plant families follows APG IV (Byng et al., 2016) and the nomenclature of taxa is mainly based on Flora Iranica (Rechinger, 1963-2015). However, in many outdated volumes we tried to use the latest taxonomic updates. In some cases, we have checked the identity of species using type specimens in herbaria or from their photos. In recent years several new species have been described from the study area mostly by our Iranian colleagues, which may require verification. Despite our efforts to see the types of these taxa, we were unable to check and ensure some of them because of restrictions we confronted with curators/staff. Therefore, these species are in the list of doubtful or excluded species. Voucher specimens were given for many species we studied. Specimens have been deposited in herbaria as indicated in Appendix 1; otherwise, they have been stored in the herbarium of Halophytes and C₄ Plants Laboratory, School of Biology, University of Tehran (Herbarium H. Akhani).

2.2. Criteria to include species as endemic or near endemic

Endemic taxa are attributed to those species that exclusively occur in mesic parts of the Hyrcanian forests. Near endemic taxa are species found in the Hyrcanian area as well as in the transitional zones between the Hyrcanian area and the Irano-Turanian region, and/or species distributed through the Hyrcanian area and that have expanded further in the Caucasus and Euxinian areas. Phytogeographic assessment of species occurring in transitional habitats with the neighboring Irano-Turanian flora is problematic. The South Caspian forests on the northern slopes of the Alborz Mountains connect with the Irano-Turanian vegetation on the southern slopes of these mountains, above the timberline and many rain shadow valleys in the northern slopes (Fig. 1). It is controversial to say whether a species growing in transition zone is a dry-adapted Hyrcanian species or a mesic-adapted Irano-Turanian species. In such cases we apply the following measures:

Those species growing in cliffs surrounded by forests and scrubs or occurring in coastal area with a distribution pattern within the Hyrcanian zone are accepted in our list as Hyrcanian species.

2)The endemic species of the Sefidrud Massif (Fig. 1), known in our paper as Manjil-Rudbar pattern, are included in the list of Hyrcanian plants, despite the fact that these species are xerophytes growing in a rain shadow Mediterranean semi-arid climate.

Species growing in moist transitional habitats such as meadows are considered Hyrcanian/Alborz transition species.

2.3. Distribution maps

All geographical coordinates were imported into DMAP (Morton, 2001) and distribution maps were generated for almost all taxa. The richness map of all species has been calculated using coincidence option for 30’ x 30’ grids. According to the inspection of 254 distribution maps and our own knowledge of the area, eight distribution patterns were defined for the Hyrcanian endemic and near endemic species. These patterns were determined based on the distribution range of each species along the study area. To identify the borders of each pattern, we generated multispecies maps of species that show similar distribution ranges.

2.4. Conservation status

The conservation status of all species has been assessed using IUCN criteria (IUCN, 2019). In some cases, we have only one old type collection. We preferred to classify such taxa as “Data Deficient” (DD) rather than considering them extinct.

We have presented two assessments for each species. In the first step we applied the assessment obtained by GeoCAT (a browser-based tool), which used the extent of occurrence (EOO) and the area of occupancy (AOO) according to criterion B of the IUCN Red List categories (http://geocat.kew.org; Moat, 2007; Bachman et al., 2011; Memariani et al., 2016; Pahlevani et al., 2020). The obtained categories have either been accepted or improved further, based on own field knowledge and field observations that support other IUCN criteria, i.e., A, C and D criteria (IUCN, 2019). The number of records gained from herbaria and literature provides useful information for evaluation of threat categories.

2.5. Habitat data

The Caspian forests and its transitional zones display high habitat heterogeneity (Akhani et al., 2010). The habitat types used in this paper are mostly based on our own field studies and available data in the literature. Our own extensive studies in GNP provide habitat information for a large number of species (Akhani, 1998).

3. Results and discussion

The number of genera and species (including subspecific taxa) of all plant families recorded from three Iranian northern provinces, Talish of Azerbaijan Republic, and two protected areas (GNP and APA) (Fig. 1) is provided in Table S1. A list of all endemic and near endemic taxa of the Hyrcanian area is provided in Appendix 1, with data on distribution, elevation range, number of records, chorotype, life form, threat category, habitat type, references, and one selected voucher specimen. Additional notes on the taxonomy of specific taxa are given in Appendix 2. A photographic selection of 37 representative endemic Hyrcanian species is depicted in Fig. 2, Fig. 3, Fig. 4. Distribution patterns of the Hyrcanian endemics and near endemics are shown in Fig. 5 and the percentage of these taxa within each distribution pattern is given in Fig. 6. The percentage of life forms of the Hyrcanian endemic and near endemic taxa is illustrated in Fig. 7. The numbers and percentages of these endemic and near endemic taxa in each threat category are summarized in Table 1. A richness map of all Hyrcanian endemics and near endemics is provided in Fig. 8. The distribution map of 254 Hyrcanian endemic and near endemic species is presented in Supplemental materials: Maps 1–254.

3.1. Alborz Mountains: Diversity hot spot in SW Asia

The total number of species recorded from three provinces (Gilan, Mazandaran and Golestan) and adjacent areas, including the APA and Talish, shows that 3855 vascular plant taxa (species and subspecies) belonging to 135 families and 893 genera are known from the area (Supplemental file 1: Table S1). There are only 55 species of Pteridophytes (ferns and fern allies) belonging to 15 families and 25 genera, and 10 species of Gymnosperms belonging to three families and five genera. In addition to 91 families, 681 genera and 3125 Dicot taxa and 23 families, 178 genera and 659 species of Monocots, these areas also contain basal Angiosperms, e.g., two species and two genera of Nymphaeales (Nymphaeaceae), and two species and one genus of Magnoliids (Aristolochiaceae); two species of Ceratophyllaceae, which is a sister family of Eudicots (Supplemental file 1: Table S1). The presence of at least 3855 species, which corresponds 52.8% of the total Iranian flora, in only three provinces of the northern Iran covering just 3.5% of the country's surface area is of great conservation importance. These provinces include the whole northern slopes of the Alborz Mountains and fragments of the southern slopes and parts of the Khorassan-Kopet Dagh Mountains (Fig. 1). This figure would increase if the whole Alborz area, i.e., the montane zones of Ardabil, Zanjan, Qazvin, Alborz, Tehran and Semnan provinces, is included. The presence of at least 1623 species in the area of Tehran and its vicinity to central Alborz is evidence of a hot spot center in the Irano-Turanian area. This is related to the complex lithological and elevational diversity, as well as the palaeoecological history of the area (Akhani et al., 2010, 2013) (Figs. 5G and 8).

Our floristic data support the hypothesis that the Alborz Mountains are an important diversity center in the Holarctic. The Irano-Turanian flora predominate the southern slopes and above timberline in the northern slopes and the Euro-Siberian flora dominate the northern slopes with higher precipitation. Parts of the deep valleys, such as Manjil-Rudbar Massif, are characterized by a Mediterranean climate and vegetation. The climatic diversity, presence of many high peaks and rich mountains ridges result in a tremendous heterogeneity for the growth of a wide spectrum of mesophytes, chasmophytes, oreophytes, psammophytes, halophytes, xerophytes, alpine and nival plants (Klein, 1994; Noroozi et al., 2008; Akhani et al., 2010, 2013; Noroozi and Akhani, 2013).

3.2. Hyrcanian forests: A regional center of diversity

In total, 256 endemic and near endemic taxa belonging to 50 families and 152 genera of flowering plants have been identified in the Caspian forests (Appendix 1; Fig. 2, Fig. 3, Fig. 4). This is less than the ca. 280 species which we have previously noted in our previous paper (Akhani et al., 2010). The reason for this is that we have excluded several taxa with doubtful taxonomic status and endemic taxa that require re-evaluation. As 11 species of our list are indeed Euxino-Hyrcanian species, we can accept 245 species belonging to endemic and near endemic species of the Hyrcanian area and nearby Alborz Mountains. By excluding an additional 62 species of the Alborz-Hyrcanian pattern, only 183 species remain as exclusive endemic species of the Hyrcanian forests.

The largest families of the Hyrcanian endemic and near endemic species are Asteraceae (13.3%), Apiaceae (7.8%), Rosaceae (7%) and Lamiaceae (5.8%), comprising one third of these taxa. The most species-rich genera among the Hyrcanian endemics and near endemics are Alchemilla L. (with nine species), Cousinia Cass., Dianthus L., and Veronica L. (each with seven species), and Astragalus L. and Leutea Pimenov (each with six species). The life form spectra (Fig. 7) show noticeable number of phanerophytes within the Hyrcanian endemic taxa. However, hemicryptophytes, with 140 species (54.7%), and geophytes, with 45 species (17.6%), are the most species-rich life forms in the area. The chamaephytes include only 12 species (4.7%), albeit, 10 further species (3.9%) could not well be classified as chamaephyte or hemicryptophyte.

There is consensus between most authors considering Hyrcanian forests as an autochthonous phytogeographical entity with a particular palaeoecological history, and particular flora and vegetation. However, its chorological position has fluctuated between province, subprovince and district. Zohary (1973) considered the area a district of the Pontic province belonging to the Euro-Siberian region. Takhtajan (1986) classified the area as the Hyrcanian province in the Irano-Turanian region. Frey et al. (1999) categorized the area as the Hyrcanian subprovince of the Euxino-Caucasian-Hyrcanian province, and Hedge and Wendelbo (1978) justified its position as the Hyrcanian subprovince of the Euro-Siberian region, supporting their view by the absence of Abies Mill., Picea A. Dietr., Pinus L. and Rhododendron L. in the area. The data in our paper confirms a regional center of diversity equivalent to a floristic province by the presence of 256 endemics and near endemics. The area is not only rich in isolated relicts but also harbors several vicariants with Euxinian and or northern and western Euro-Siberian areas, which probably evolved through allopatric speciation. All three important, widely distributed arboreal Hyrcanian species in the genera Ilex L., Buxus L. and Hedera L. have sister or related species in the Euxinian forests: Ilex spinigera (Loes.) Loes. (its Euxinian sister is Ilex colchica Pojark.) (Manen et al., 2010), Buxus hyrcana Pojark. (its Euxinian sister is B. colchica Pojark.) (Van Laere et al., 2011), Hedera pastuchovii Woron. ex Grossh. (its close affinity is H. colchica (K.Koch) K.Koch) (Vargas et al., 1999; Green et al., 2011).

The presence of 256 endemics and near endemics in a small area of forest zone, the presence of many relict species and a dozen of vicariant species with ecologically sister areas are justification for a floristic province. The Khorassan-Kopet Dagh floristic province located at the easternmost part of the Hyrcanian area is known with 356 endemics (Memariani et al., 2016).

There is some evidence that the Hyrcanian forests played a role in donating species to the Irano-Turanian region. The genus Leutea (Apiaceae) is an exclusively endemic genus in the Hyrcanian and Irano-Turanian region. Species of the arid parts of the Irano-Turanian are characterized by their cylindrical leaves (Pimenov, 1987). Discovery of a broad-leaved species (Leutea laseroides Akhani = Laser rechingeri Akhani) (Supplemental file 2: Map 53) in the moist cliffs of the eastern parts of the Hyrcanian forests, which is phylogenetically sister to the cylindrical-leaved species, is evidence of its ancestral state (Akhani, 1996, 1998; Valiejo-Roman et al., 2006). Both Rubiaceous species Phuopsis stylosa (Trin.) Hook. f (an endemic Hyrcanian genus, Fig. 4E, Supplemental file 2: Map 236). and Crucianella platyphylla Ehrend. & Schönb.-Tem (Supplemental file 2: Map 230). show plesiomorphic features (Schönbeck-Temesy and Ehrendorfer, 1989; Ehrendorfer and Schönbeck-Temesy, 2005). Alyssopsis Boiss. is also an isolated non-arboreal Hyrcanian endemic genus that phylogenetic studies show has an affinity with the Irano-Turanian genera Dielsiocharis O.E.Schulz and Calymmatium O.E.Schulz (Warwick et al., 2010; Toro-Nunez et al., 2015).

3.3. Distribution patterns and endemism

According to the distribution maps of 254 taxa (Supplemental file 2: Maps 1-254), eight geographical distribution patterns have been identified for the Hyrcanian endemic and near endemic species (Fig. 5).

1)Omni-Hyrcanian pattern (OH, Fig. 5A)

This is the second largest group of species, including 61 species belonging to 34 families and 51 genera. The core range of most species lies in a continuous belt on the South Caspian forests. However, some more widespread species occur in proper surrounding areas such as isolated forests in the APA, East Caucasus up to South Dagestan, the Jowzak forest (in North Khorassan Province in the eastern part of the Hyrcanian area) and even mesic valleys in Turkmenistan. Some prominent arboreal examples of this group are the Tertiary relict elements such as Parrotia persica (DC.) C.A. Mey. (Fig. 3F; Supplemental file 2: Map 150), Quercus castaneifolia C.A. Mey. (Fig. 3G; Supplemental file 2: Map 147), Alnus subcordata C.A. Mey. (Supplemental file 2: Map 98), Acer velutinum Boiss. (Fig. 4G; Supplemental file 2: Map 239), Pyrus boissieriana Buhse (Fig. 4C and D; Supplemental file 2: Map 216), Frangula grandifolia (Fisch. & C.A. Mey.) Grubov (Supplemental file 2: Map 204) and Ilex spinigera (Fig. 2H; Supplemental file 2: Map 60). Many herbaceous species are associated with forest zones and their distribution ranges perfectly overlap with arboreal species. Examples are Digitalis nervosa Steud. & Hochst. ex Benth. (Fig. 3N; Supplemental file 2: Map 180), Primula heterochroma Stapf (Fig. 4A; Supplemental file 2: Map 196), Scutellaria tournefortii Benth. (Fig. 3I; Supplemental file 2: Map 163), Alyssopsis mollis (Jacq.) O.E. Schulz (Supplemental file 2: Map 108), Echium amoenum Fisch. & C.A. Mey. (Fig. 2L; Supplemental file 2: Map 100), and Centaurea hyrcanica Bornm. (Fig. 2J; Supplemental file 2: Map 68).

2)West Hyrcanian pattern (WH, Fig. 5B)

This group includes 39 species belonging to 21 families and 31 genera. They usually occur from the central Mazandaran westwards to the Talish forests on the border of Iran and Azerbaijan. This area matches with the “temperate oceanic” bioclimate (Djamali et al., 2011) and is the most humid part of the Hyrcanian zone, where the annual precipitation may reach or even exceed 2000 mm in some parts. Epimedium pinnatum Fisch. (Fig. 2K; Supplemental file 2: Map 97), Pyrus grossheimii Fedor. (Supplemental file 2: Map 217), P. stylosa (Fig. 4E; Supplemental file 2: Map 236), Scrophularia rostrata Boiss. & Buhse (Supplemental file 2: Map 246) and Potentilla petraea Willd. ex Schlecht (Supplemental file 2: Map 215). are the most prominent species representing the West Hyrcanian pattern.

3)Manjil-Rudbar pattern (MR, Fig. 5C)

Sefidrud Massif is a special area in the Hyrcanian lowlands, in which the climate is very dry and forms an island-like sub-desert in the moist zone of Iran. The low elevation and the strong winds create a rain shadow in this valley, forming sand dunes in parts of the area. The bioclimate of this zone is Mediterranean Xeric Oceanic (MXO) (Djamali et al., 2011). A total of 17 species belonging to 11 families and 16 genera are known to be endemic in this small area, including Cousinia erinacea Jaub. & Spach (Supplemental file 2: Map 76), Cousinia hypochionea Bornm. (Supplemental file 2: Map 78), Salvia oligophylla Auch. ex Benth. (Supplemental file 2: Map 158), Atraphaxis aucheri Jaub. & Spach (Supplemental file 2: Map 189) and Asperula sherardioides (Boiss.) Jaub. & Spach (Supplemental file 2: Map 226). A new undescribed species of Heliotropium is also known from this area (Supplemental file 2: Map 102). Most species of this pattern are either very rare, known only from type locality, e.g., Scorzonera persica Boiss. & Buhse (Supplemental file 2: Map 91), or are endangered species such as Aristolochia hyrcana Davis & M.S. Khan (Fig. 2A; Supplemental file 2: Map 1).

4)Central Hyrcanian pattern (CH, Fig. 5D)

This pattern includes 15 species belonging to 11 families and 15 genera, with a center of distribution in forest zone of Mazandaran Province. Most species occur in scrubs and cliff habitats. Satureja isophylla Rech. f. (Supplemental file 2: Map 161) and Galium wendelboi Ehrend. & Schönb.-Tem. (Supplemental file 2: Map 235) are found in cliff habitats. Ophrys kojurensis Gölz (Supplemental file 2: Map 29), Hypericum fursei N. Robson (Supplemental file 2: Map 151), Pyrus mazanderanica Schönbeck-Temesy (Supplemental file 2: Map 219), Spiraea sheikhii Zare (Supplemental file 2: Map 222), and Astragalus lacus-valashtii Maassoumi, Podlech & Jalili (Supplemental file 2: Map 137) are examples of scrub habitats and Acer iranicum M. Mohtashamian & A. Rastegar/Acer mazandaranicum Amini, Zare & Assadi (Supplemental file 2: Map 238) a tree species of the forest zone.

5)Central and East Hyrcanian pattern (CEH, Fig. 5E)

Species in this group occur from the central Hyrcanian forests and extend their range into the eastern parts up to Khorassan-Kopet Dagh area in some cases. This pattern includes 18 species belonging to 15 families and 18 genera. Except a few species such as Epipactis rechingeri Renz (Supplemental file 2: Map 26) and Heracleum gorganicum Rech. f. (Supplemental file 2: Map 48), which grow in shady forests, most other species, e.g., Berberis orthobotrys Bienert ex C.K. Schneider (Supplemental file 2: Map 96), Campanula lourica Boiss. (Fig. 3A; Supplemental file 2: Map 114), Alcea gorganica (Rech. f., Aell. & Esfand.) Zohary (Supplemental file 2: Map 169), Verbascum sublobatum Murb. (Supplemental file 2: Map 251) and Colutea buhsei (Boiss.) Shap. (Supplemental file 2: Map 142) are elements of cliffs, meadows and scrubs.

6)East Hyrcanian pattern (EH, Fig. 5F)

The range of the 33 species (belonging to 14 families and 29 genera) in this group is located from 52°E longitude to the easternmost extensions of the Hyrcanian forests. They usually occupy open scrubs and rocky outcrops, and grasslands adjacent to the forests. Some species of this group are taxonomically and phylogenetically very isolated, such as Leutea laseroides (Supplemental file 2: Map 53), Johrenia golestanica Rech. f. (Supplemental file 2: Map 50), Centaurea golestanica Akhani & Wagenitz (Supplemental file 2: Map 67), Crucianella platyphylla (Supplemental file 2: Map 230) and Corydalis chionophila Czernjak. (Supplemental file 2: Map 177). Sometimes it is very difficult to distinguish these species from the surrounding phytochoria, in particular that of the Khorassan-Kopet Dagh Province of the Irano-Turanian region. According to Memariani et al. (2016) some species of this pattern have been categorized in the checklist of Khorassan-Kopet Dagh Province. GNP and Jahan Nama Protected Area are two important protected areas of Iran, in which many East Hyrcanian endemics occur (Akhani, 1998; Jafari and Akhani, 2008).

7)Alborz-Hyrcanian pattern (AH, Fig. 5G)

Several mesophytic Irano-Turanian elements co-occur with the Hyrcanian species in the northern slopes of the Alborz Mountains, usually in deforested areas and rocky outcrops, or at the marginal and transitional parts in the timberline and nearby grasslands. One may consider these species, which constitute the largest group of endemics, as “xerophytic Hyrcanian” species or “mesophytic Irano-Turanian” elements, with 62 species, belonging to 21 families and 43 genera. In some cases, the range of some species extends to Talish in the west and Khorassan-Kopet Dagh Mountains in the east. Some prominent examples of the Alborz-Hyrcanian pattern are Phleum iranicum Bornm. & Gauba (Supplemental file 2: Map 35), Seseli elbursense Pimenov & Kljuykov (Supplemental file 2: Map 58), Dolichorrhiza persica (Boiss.) B. Nord. (Supplemental file 2: Map 84), Eritrichium gracillimum Rech. f. (Supplemental file 2: Map 101), Nepeta pogonosperma Jamzad & Assadi (Supplemental file 2: Map 156), Veronica paederotae Boiss. (Supplemental file 2: Map 186), Dionysia aretioides (Lehm.) Boiss. (Supplemental file 2: Map 195), Paraquilegia caespitosa (Boiss. & Hohen.) Drumm. & Hutch. (Supplemental file 2: Map 201), and Galium aucheri Boiss. (Supplemental file 2: Map 231).

8)Euxino-Hyrcanian pattern (XH, Fig. 5H)

We have not included all Euxino-Hyrcanian species in this paper. The 11 selected species belong to 11 families and 11 genera. These species show an inconsistent pattern, ranging from the Euxinian species with some localities in the Hyrcanian forests [Erythronium caucasicum Woron. (Supplemental file 2: Map 20) and Polygonatum glaberrimum C. Koch (Supplemental file 2: Map 14)] or the Hyrcanian species with some localities in the Euxinian or Caucasus area [Froriepia subpinnata (Ledeb.) Baill. (Supplemental file 2: Map 47)], or widespread species occurring in both areas [Anemone caucasica Willd. ex Rupr. (Fig. 4B; Supplemental file 2: Map 198), Orchis adenocheila Czerniak. (Supplemental file 2: Map 31), Hesperis hyrcana Bornm. & Gauba (Fig. 2M; Supplemental file 2: Map 109), Teucrium hyrcanicum L. (Supplemental file 2: Map 166) and Lonicera iberica M. Bieb. (Fig. 3B; Supplemental file 2: Map 116)].

Comparison of the species richness of different distribution patterns (Fig. 6) indicates that the Alborz-Hyrcanian (Fig. 5G) and Omni-Hyrcanian (Fig. 5A) patterns are the richest in the area.

In the Caspian forests the richness of endemics in lowlands and sub-montane zones is low whereas it increases remarkably in montane forests and above timberline towards the limits of the area (Hedge and Wendelbo, 1978) (Fig. 9). This is a known phenomenon in Iran, explained by the geographical isolation in higher elevations (Noroozi et al., 2016). According to the results, the elevational distribution of Hyrcanian endemics and near endemics ranges between sea level in the Caspian lowlands and 4200 m in the alpine areas (Appendix 1). The largest numbers of Hyrcanian endemics and near endemics are found at elevations between 500 and 3000 m. Notably, many endemic and near endemic species, such as Poa masenderana Freyn & Sint. (75–2600 m), Centaurea hyrcanica (50–2810 m), C. zuvandica (Sosn.) Sosn. (0–3000 m), Crepis willemetioides Boiss. (50–2900 m), Echium amoenum (60–3000 m), Rhynchocorys maxima C. Richter (-26–2750 m), Polygala platyptera Bornm. & Gauba (0–2500 m) and Scrophularia rostrata (50–3010 m), have wide elevational distribution ranges in this area. The main reason for this extensive range is likely owed to favorable ecological conditions, including convenient temperature and humidity, from low to high elevations. Annual species become quite rare at high elevations (Mahdavi et al., 2013). These species are not common as endemics or near endemics in the Hyrcanian forests and mostly grow in the lowlands.

3.4. Hyrcanian forests: Irano-Turanian or Euro-Siberian?

Although the majority of phytogeographers have classified the Hyrcanian forests under the circumboreal or Euro-Siberian region (Zohary, 1973; Browicz, 1989; White and Léonard, 1991; Frey et al., 1999), a few, however, prefer to consider the area a mesophytic variant of the Irano-Turanian region (Takhtajan, 1986; Manafzadeh et al., 2017) or Sub-Mediterranean subregion (Meusel et al., 1965). The arguments in favour of the Euro-Siberian enclaves mostly refer to large number of arboreal species which are either circumboreal species such as Carpinus betulus L., Sorbus torminalis (L.) Crantz, Fraxinus excelsior L., Acer campestre L. and Berberis vulgaris L. (Browicz, 1989) or species having close affinity with some widely distributed boreal taxa belonging to Carpinus L., Quercus L., Fagus L., Castanea Mill., Acer L., Evonymus L., Zelkova Spach, and many more. The majority of Orchids and Pteridophytes growing in Iran are restricted to the Hyrcanian area as boreal or Euro-Siberian elements (Renz, 1978; Khoshravesh et al., 2009). Many Tertiary relict Hyrcanian endemic trees such as Parrotia persica (Fig. 3F; Supplemental file 2: Map 150), Quercus castaneifolia (Fig. 3G; Supplemental file 2: Map 147) and Acer velutinum (Fig. 4G; Supplemental file 2: Map 239) survived glaciations as refugees. The fossils of several species or their close affinities have been identified in Europe [(Bernasso in south France (Leroy and Roiron, 1996), the Mesovian Interglacial of Poland (Binka et al., 2003), and Willershausen in Germany (Ferguson and Knobloch, 1998)]. Twenty-nine of the species in Willershausen near Göttingen grow in the Hyrcanian forest zone and 16 further species are almost identical (Probst, 1981).

Parrotia C.A. Mey., which was long considered a monotypic genus, has a sibling Chinese species (P. subaequalis (Hung T. Chang) R.M. Hao & H.T. Wei) known from a few populations in Eastern China in Jiangsu, Anhui and Zhejiang provinces (Li and Del Tredici, 2008). Despite very long distances (6500 km), the two regions share many woody plant genera, including Acer, Albizzia Durazz., Buxus, Castanea, Carpinus, Diospyros L., Fagus, Pterocarya Kunth, Quercus, Sorbus L., Taxus L., Zelkova and Hedera (Valcárcel et al., 2017).

From vegetation point of view, none of the syntaxa of the Hyrcanian forest correspond with Irano-Turanian region. All four classes recently known from the area (Alnetea glutinosae Br.-Bl. et Tx. ex Westhoff et al., 1946, Alno glutinosae-Populetea albae P. Fukarek et Fabijanić 1968, Carpino-Fagetea sylvaticae Jakucs ex Passarge 1968, and Quercetea pubescentis Doing-Kraft ex Scamoni et Passarge 1959) are indeed Euro-Siberian higher syntaxa (Mucina et al., 2016; Gholizadeh et al., 2020).

The chorological analysis of the flora of Golestan National Park, the easternmost end of the Hyrcanian forests with the mixture of deciduous forests in the west and Irano-Turanian Juniper woodlands, Artemisia L. and montane steppes in southern, eastern and northern parts of the area shows that 15% of the species are Euro-Siberian plants (Akhani, 1998). The distribution of the Euro-Siberian species shows that 40% of the species are Omni-Euro-Siberian, 30% are Euxino-Hyrcanian sharing species and 30% are Hyrcanian endemics. Despite its easternmost location, many Euro-Siberian species dominate the mesic parts of the area and some interesting cases have been found as new records from that area, such as Carex pseudocyperus L., Hordelymus europaeus (L.) Harz and Alopecurus aequalis Sobol. (Akhani and Scholz, 1998; Akhani, 1999).

The Irano-Turanian region is characterized by its drought-adapted flora, which evolved under a particular climate differentiated from the Euro-Siberian region by continentality, winter temperature, and precipitation seasonality (Djamali et al., 2012). The climate of the Hyrcanian area has a characteristic temperate feature in the distribution of precipitation over the year, a very short dry period, and high air humidity (Akhani et al., 2010). However, the area deviates from the northern temperate forests by having an average minimum of temperatures in the coldest month above the freezing point. This provides not only support for growing thermophilous trees [such as deciduous species belonging to Parrotia, Pterocarya and Zelkova, and evergreen Buxus, Hedera and Ilex (Iversen, 1944)] but also the development of C₄ grasslands in open areas (Akhani and Ziegler, 2002). The main argument that supports excluding the Hyrcanian forests from the Irano-Turanian region is the age difference of their endemics. The Irano-Turanian region harbors many neoendemics, with large numbers of recently radiated lineages adapted to the arid conditions, mostly diversified after orogenic activities since the Oligocene (Manafzadeh et al., 2014). But the endemics of the Hyrcanian area are either paleoendemics that remained as refugees in the area or evolved from common ancestors of widely distributed temperate elements due to geographical vicariance (Tralau, 1963).

The Irano-Turanian elements in the Hyrcanian zones only occur in the marginal habitats of the forests, rain shadow areas, rocky outcrops, above the timberline and sometimes also in the deforested parts. None of the typical Irano-Turanian species and genera are associated with the forests. Therefore, considering Hyrcanian forests as Irano-Turanian is not justified.

3.5. Hyrcanian area with highly threatened species

The endemic and near endemic species of the Hyrcanian forests area have been evaluated using the IUCN Red List categories and criteria. We did not accept preliminary evaluations for several species suggested by Jamzad and Jalili (1999) or Naqinezhad et al. (2015), because of the poor methodological approach of these studies. Our checklist includes 30 taxa (11.7%) as Critically Endangered (CR), 52 taxa (20.3%) as Endangered (EN), 30 taxa (11.7%) as Vulnerable (VU), 25 taxa (9.8%) as Near Threatened (NT), 81 taxa (31.6%) as Least Concern (LC) and 38 taxa (14.8%) are Data Deficient (DD), lacking reliable data to be evaluated (Table 1). Assessment of 44% of the Hyrcanian endemic and near endemic species as threatened is alarming for national and international community. The distribution of different threatened categories among eight known distribution patterns clearly shows that except for the “Omni-Hyrcanian”, “Central and East Hyrcanian” and “Euxino-Hyrcanian” patterns, all other patterns harbor a considerable number of Critically Endangered, Endangered and Vulnerable species (Fig. 10). The Caspian forests are among the most highly threatened ecosystems in Iran. Some of the main factors responsible for threatening populations of indigenous species include urbanization and industrialization, clearing land areas for agricultural purposes, livestock overgrazing, road and dam construction, firing, intensive mining, disposal of waste, and pollution (Akhani et al., 2010).

Several threatened species of the Hyrcanian area, including Aristolochia hyrcana (Fig. 2A; Supplemental file 2: Map 1), Hyacinthella persica (Boiss. & Buhse) Chouard (Supplemental file 2: Map 10), Heliotropium sp. nov. (Supplemental file 2: Map 102), Nonea longiflora Wettst. ex Stapf (Supplemental file 2: Map 106), Scabiosa schimperiana Boiss. & Buhse (Supplemental file 2: Map 117) and Atraphaxis aucheri (Supplemental file 2: Map 189), grow in special habitats around Sefidrud valley (MR pattern, Fig. 5C). The area has been heavily damaged by a variety of land use activities such as road and dam construction along with development of agricultural activities (olive plantations). Other species, such as Crocus almehensis Brickell & Mathew (Supplemental file 2: Map 17), Ophrys kojurensis (Supplemental file 2: Map 29), Eriocycla ghafooriana Akhani (Supplemental file 2: Map 46), Leutea laseroides (Supplemental file 2: Map 53), Centaurea golestanica (Supplemental file 2: Map 67), Plantago podlechii Akhani (Supplemental file 2: Map 181) and Saxifraga ramsarica Jamzad (Supplemental file 2: Map 242), are very local endemics with distributions restricted to small areas in the Hyrcanian zone. Additional endemics have suffered from habitat loss in coastal areas, as well as lowland and montane forests, e.g., Daucus littoralis Smith subsp. hyrcanicus Rech. f. (Supplemental file 2: Map 44), Typha caspica Pobed. (Supplemental file 2: Map 39), Dianthus hyrcanicus Rech. f. (Supplemental file 2: Map 120), Polygala platyptera (Supplemental file 2: Map 188), Scrophularia megalantha Rech. f (Supplemental file 2: Map 245). and Veronica francispetae M.A. Fischer (Supplemental file 2: Map 183).

The Data Deficient category should be applied only in cases of unresolved taxonomy or uncertain locality information (Callmander et al., 2005). Many Hyrcanian endemics and near endemics designated as DD in the checklist (Appendix 1), including Tulipa harazensis Rech. f., Bunium scabrellum Korov., Crepis alfredi Bornm., Campanula ghilanensis Pall., Hypericum fursei, Phlomis ghilanensis C. Koch and Delphinium syncarpum Freyn, have incomplete locality information and other taxa require updated taxonomic assessments.

4. Conclusion

The Hyrcanian forests, a UNESCO World Heritage region, harbor highly valuable relicts of Tertiary elements. The area is suffering from many degrading factors threatening the unique ecosystems that contains many rare and endangered species both in the mesic parts of the forests and surrounding highlands. Our studies support the hypothesis that the Hyrcanian forests are a regional center of endemism within the boreal (Euro-Siberian) floristic region. Implementation of protection measures to stop reduction of forest area and reduce destructive factors should be combined with documentation of the status of individual species, identification of unknown populations, census of rare species and in situ and ex situ programs to ensure the survival of rare, endemic and threatened species.

Author contribution

H.A. conceived of the research idea, A.Gh. collected and provided the data, tables and maps. The tables were critically reviewed by H.A., who wrote the manuscript jointly with A.Gh.

Declaration of competing interest

The authors declare no conflict of interests.

Acknowledgments

The herbarium curators of the Plant Pests and Diseases Research Institute (IRAN), the Research Institute of Forests and Rangeland (TARI) and Botanical Garden and Botanical Museum of Berlin (B) are appreciated for allowing us to study available material in those herbaria. We are grateful to Targol Chatrenoor for preparing some photos of herbarium specimens from Komarov Botanical Institute (LE). We appreciate Alireza Noormohammadi for providing the photograph of Lilium ledebourii and Mahmood Shakiba for finding Gentiana grossheimii in Jahan Nama Protected Area.

Appendix A Supplementary data

The following are the Supplementary data to this article: https://doi.org/10.1016/j.pld.2021.07.005.