Micromorphological Traits of Balcanic Micromeria and Closely Related Clinopodium Species (Lamiaceae)
by
, , , ,
Dario Kremer
1, 
Edith Stabentheiner
2,
Faruk Bogunić
3,
Dalibor Ballian
3,4,
Eleni Eleftheriadou
5,
Danijela Stešević
6,
Vlado Matevski
7,
Vladimir Ranđelović
8,
Daniella Ivanova
9,
Mirko Ruščić
10 and
Valerija Dunkić
10,*
1
Faculty of Pharmacy and Biochemistry, University of Zagreb, A. Kovačića 1, 10000 Zagreb, Croatia
2
Institute of Biology, Karl-Franzens University, Schubertstrasse 51, 8010 Graz, Austria
3
Faculty of Forestry, University of Sarajevo, Zagrebačka 20, 71000 Sarajevo, Bosnia and Herzegovina
4
Slovenian Forestry Institute, Večna Pot 2, 1000 Ljubljana, Slovenia
5
School of Forestry and Natural Environment, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece
6
Faculty of Natural Sciences and Mathematics, University of Montenegro, Džordža Vašingtona bb, 81 000 Podgorica, Montenegro
7
Faculty of Natural Sciences and Mathematics, Ss. Cyril and Methodius University, Gazi Baba bb, 1000 Skopje, North Macedonia
8
Faculty of Sciences and Mathematics, University of Niš, Višegradska 33, 18000 Niš, Serbia
9
Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, Acad. Georgi Bonchev Str., bl. 23, 1113 Sofia, Bulgaria
10
Faculty of Science, University of Split, Ruđera Boškovića 33, 21000 Split, Croatia
*
Author to whom correspondence should be addressed.
Plants 2021, 10(8), 1666; https://doi.org/10.3390/plants10081666
Submission received: 28 July 2021
/
Revised: 9 August 2021
/
Accepted: 10 August 2021
/
Published: 13 August 2021
(This article belongs to the Special Issue Morphology, Anatomy and Secondary Metabolites of Mediterranean Plants)
Abstract
:A study of the trichomes types and distribution and pollen morphology was carried out in nine Micromeria taxa (M. cristata ssp. cristata, M. cristata ssp. kosaninii, M. croatica, M. graeca ssp. graeca, M. graeca ssp. fruticulosa, M. juliana, M. kerneri, M. longipedunculata and M. microphylla) and five closely related Clinopodium species (C. dalmaticum, C. frivaldszkyanum, C. pulegium, C. serpyllifolium and C. thymifolium) from the Lamiaceae family of the Balkan Peninsula. By scanning electron microscope, non-glandular trichomes, peltate and capitate trichomes were observed on the calyx, leaves and stem of the studied species. Two subtypes of capitate trichomes were observed in Micromeria species: subtype 1 (consisting of a basal epidermal cell and an elliptically shaped head cell) and subtype 2 (consisting of a basal epidermal cell, two to three stalk cells and a round head cell). In Clinopodium species, three types of capitate trichomes were observed: subtype 1, subtype 3 (consisting of a basal epidermal cell, a short peduncle cell, and a single round head cell), and subtype 4 (consisting of a basal epidermal cell, a stalk cell, and an elongated head cell). These results support the recent transfer of Micromeria species from the section Pseudomelissa to the genus Clinopodium.
1. Introduction
The family Lamiaceae is one of the largest families among the eudicots, consisting of more than 240 genera and more than 7200 species [1]. Many of species belonging to this family are aromatic and medicinal plants due to the presence of glandular trichomes that produce essential oil. One of the plant groups in this family is the genus Micromeria Benth. and closely related species from the genus Clinopodium L. The genus Micromeria belongs to subtribe Menthinae and tribe Mentheae (subfam. Nepetoideae). According to Briquet [2], Killick [3] and Greuter et al. [4], it is considered part of the indistinctly defined “Satureja” complex. However, this opinion is slowly being abandoned today. According to Bentham [5], Micromeria species form a separate genus and this opinion prevails today [6,7]. The genus Micromeria includes 54 [8] to 70/20 [9] perennial herbs, subshrubs and shrubs, rarely annual herbs. According to Bräuchler et al. [8,10], the range of Micromeria species extends from India and China to the Macaronesian Archipelago and from the Mediterranean to South Africa and Madagascar. Bräuchler et al. [10] showed that the genus Micromeria is polyphyletic and that a revision of this genus is necessary. In accordance with this opinion, Bräuchler et al. [11] transferred the taxa included to the section Pseudomelissa from the genus Micromeria to the genus Clinopodium.
Micromeria species are more or less aromatic plants with opposite leaves and thyrsoid or sometimes racemelike, dense or loose, spikelike inflorescences. The leaf blade is entire or with a few indistinct teeth, often with a thickened and revolute margin. The petiole is distinct, short or minute. The calyx is tubular in the lower part and five-lobed in the upper part, almost actinomorphic to distinctly two-lipped, mostly hairy in the mouth. The upper lip is three-lobed; the lower lip is two-lobed, divided to the base and their lobes are mostly narrower and longer than those of the upper lip. The teeth are ciliate or not. The corolla is strongly two-lipped, with a straight tube. The upper lip is emarginated; the lower lip is three-lobed with middle lobe broader than lateral [8,10,12]. Clinopodium species are also aromatic plants with opposite leaves and flowers arranged in opposite, axillary, dense, many-flowered cymes. The calyx is tubular with a curved tube and more or less two-lipped in the upper part, hairy in the mouth. The teeth are almost never ciliate. The corolla is two-lipped, with straight tube. The upper lip is entire or emarginated, while the lower lip is three-lobed with middle lobe wider than lateral [8,10].
The type and distribution of secretory and non-secretory trichomes play an important role in taxonomic study. The study of trichomes in Micromeria and Clinopodium species has been reviewed by several authors [13,14,15,16,17,18,19]. Palynology also provides valuable taxonomic data and information on the origin and evolution of species [20]. The pollen of Micromeria and Clinopodium species has also been studied by several authors [15,16,21,22,23,24].
This study represents a continuation of our investigations of Balkan Micromeria and Clinopodium species. Instead of studying additional species individually, we included all available Micromeria and Clinopodium species from Balkan Peninsula in this paper. Of the genus Clinopodium, only species transferred from Micromeria sect. Pseudomelissa were included in this study. So, the aim of this study is to gain insight into the micromorphological traits of Micromeria species as well as the closely related Clinopodium species recently transferred from the Micromeria sect. Pseudomelissa. The main objective is to determine whether micromorphological traits support the transfer of species from section Pseudomelissa to the genus Clinopodium.
2. Results and Discussion
2.1. Trichomes
The non-glandular and glandular trichomes were observed in the studied Micromeria and Clinopodium species. Non-glandular (NG) trichomes have been observed on the leaves, calyces, and stem of both genera. These trichomes are unbranched, uniseriate, bi-cellular to multicellular and most often bent on different sides. They could be called attenuated trichomes because they gradually taper from base to tip [25]. The length of the NG trichomes is highly variable and ranges from very short trichomes, especially on the adaxial leaf surface, to very long hairs on the calyx and stem (Figure 1 and Figure 2). The surface of these trichomes is warty (Figure 1). The main function of NG trichomes is to protect the plant from water loss. The same type of NG trichomes is present in both Micromeria and Clinopodium species.
The occurrence and frequency of NG trichomes on the adaxial and abaxial sides of the leaf, the outer side of the calyx and the stem are shown in Table 1 and Table 2. All Micromeria species studied have a more or less abundant coverage of NG trichomes on the adaxial and abaxial leaf surface (Figure 1). A certain exception is M. longipedunculata, in which the upper and lower leaf surfaces are less hairy. The adaxial and abaxial leaf surfaces and stem of M. graeca ssp. fruticulosa and the stem of M. cristata have the highest number of long NG trichomes forming an abundant covering.
In general, Micromeria species have a denser indumentum of attenuated trichomes on leaves than Clinopodium species. Clinopodium serpyllifolium is an exception as it has the densest NG trichomes cover of all Micromeria and Clinopodium species examined (Figure 2). Studies by Firat et al. [22] also showed very dense indumentum on the leaves and stem of Clinopodium serpyllifolium ssp. sirnakense. The frequency of NG trichomes on the calyx of Clinopodium species is similar to this coverage of NG trichomes in Micromeria species. A slightly lower frequency of NG trichomes was observed on the calyx of C. frivaldszkyanum and C. pulegium, and on the stem of C. frivaldszkyanum. The presence of NG trichomes has been previously well documented in Micromeria [13,15,16] and Clinopodium [13,14,17,18] species, as well as in other Lamiaceae [13,14,26].
Glandular trichomes were observed on all plant parts of the Micromeria and Clinopodium species examined. These trichomes can be further divided into two main subtypes, namely, peltate and capitate trichomes. Peltate trichomes consist of a basal cell, a very short unicellular stalk and a multicellular head with a large subcuticular space (Figure 1). These trichomes are also known from some other Lamiaceae species [13,26,27,28,29,30,31,32]. The distribution and frequency of peltate trichomes on the studied plant parts are shown in Table 1 and Table 2. Although peltate trichomes are present on all plant parts studied, they are more abundant on the abaxial leaf surface and on the calyx. They are completely absent on the adaxial side of the leaf in M. croatica and M. longipedunculata (Table 1). Peltate trichomes were previously reported in Micromeria fruticosa [13], Micromeria myrtifolia Boiss. et Hohen. [33], M. croatica [15], M. kerneri, M. juliana [16] and M. longipedunculata [34]. Husain et al. [14] showed the presence of peltate trichomes on the leaves of Clinopodium serpyllifolium, C. dalmaticum and C. thymifolium. Peltate trichomes were also detected in micrographs of C. thymifolium leaves presented by Marin et al. [35]. Mladenova et al. [19] observed these trichomes in the leaves of C. frivaldszkyanum, although they did not describe them as peltate.
The capitate trichomes can be further divided into several subtypes. Subtype 1 (C1) capitate trichomes consist of a basal epidermal cell and an elliptically shaped head cell with a larger subcuticular space. C1 trichomes are not erect but can be described as adherent to the surface (Figure 1). This type was observed on both the abaxial and adaxial sides of the leaves, on the stem and on the outer side of the calyx. They are present in all Micromeria and Clinopodium species studied (Table 1 and Table 2). These trichomes were described in detail in Micromeria croatica by Kremer et al. [15].
C1 trichomes have also been observed in M. kerneri and M. juliana [16]. Although Husain et al. [14] did not mention C1 trichomes in M. longipedunculata, unclear SEM micrographs probably show just the C1 type of trichomes. On the other hand, SEM micrographs of M. fruticosa presented by Werker et al. [13] did not show C1 trichomes. According to drawings made by Koca [33], it seems that C1 trichomes are also present in Micromeria myrtifolia. C1 trichomes were also observed in Clinopodium dalmaticum, C. pulegium, C. serpyllifolium and C. thymifolium [17].
Hanlidou et al. [36] described trichomes comparable to C1 trichomes in Calamintha menthifolia Host as short and usually curved trichomes. These trichomes are regularly present in all studied Micromeria and Clinopodium species, but they cannot be considered specific only to these two genera. In addition, the SEM micrographs presented by Werker et al. [13] show C1 trichomes in Majorana syriaca (L.) Rafin., Satureja thymbra L., and Thymus capitatus (L.) Hoffmanns. et Link. However, it is evident that C1 trichomes are not as common as peltate trichomes in Lamiaceae species.
Subtype 2 capitate trichomes (C2) are composed of a basal epidermal cell, two to three stalk cells and a rounded head cell with subcuticular space (Figure 1). C2 trichomes are upright while the height of these trichomes varies from short trichomes, mainly on the abaxial side of the leaf, to quite long trichomes on the calyx and stem. However, they are often absent on the adaxial leaf side. C2 trichomes are observed only in Micromeria species studied.
So far, these trichomes have been observed in Micromeria fruticosa [13], M. myrtifolia [34], M. croatica [15], M. kerneri, M. juliana [16], and M. longipedunculata [34]. These trichomes are more common than C1 trichomes in Lamiaceae species and trichomes comparable to C2 trichomes have also been described in Salvia L. [30] and Satureja L. [37,38,39] species.
Subtype 3 capitate trichomes (C3) are also erect and consist of a basal epidermal cell, a relatively short stalk cell, and a single roundish cell head with subcuticular space. Although C3 trichomes were observed in all investigated Clinopodium species, they were almost absent in C. frivaldszkyanum, C. pulegium and C. thymifolium (Table 2). Marin et al. [35] did not mention C3 trichomes, but they are visible in the presented SEM micrographs of C. thymifolium leaves. They are also present in the micrographs of Satureja montana L., S. subspicata Vis. and S. kitaibelii Wierzb. ex Heuff. presented by Dunkić et al. [38] and Dodoš et al. [39].
The capitate trichomes of subtype 4 (C4) are upright and consist of a basal epidermal cell, a stalk cell and an elongated head cell. In these trichomes, the head cell is as narrow as the stalk cells, and only slightly enlarged above, with a subcuticular space. They resemble a finger (Figure 2). Although C4 trichomes are present in all Clinopodium species studied, they are relatively rare trichomes (Table 2). The presence of C4 trichomes was previously observed in Clinopodium dalmaticum, C. pulegium, C. serpyllifolium and C. thymifolium by Dunkić et al. [17]. These trichomes are also visible in SEM micrographs of leaves of Micromeria fruticosa and Clinopodium thymifolium presented by Werker et al. [13] and Marin et al. [35], respectively. C4 trichomes are visible in SEM micrographs of Calamintha menthifolia, and in micrographs of Satureja montana and S. subspicata presented by Hanlidou et al. [36] and Dunkić et al. [38], respectively. Unclear micrographs presented by Al-Zubaidy et al. [40] probably show just C4 trichomes in Clinopodium vulgare L. ssp. vulgare and C. vulgare ssp. arundanum Boiss. In addition, they can be observed in SEM micrographs of Majorana syriaca, Salvia fruticosa Mill., S. officinalis L. [13], and S. divinorum Epling et Játiva [30]. Although data from the literature [13] suggest that C4 trichomes may sometimes be present in Micromeria species, our results show that they are characteristic for Clinopodium species.
The results presented here show that NG trichomes, peltate trichomes and capitate trichomes of subtype 1 are present in both Micromeria and Clinopodium taxa. On the other hand, the capitate trichomes of subtype 2 are present only in studied Micromeria taxa, while subtypes 3 and 4 are present only in Clinopodium taxa. Since the investigated taxa of the genus Clinopodium belong to the former Micromeria sect. Pseudomelissa, it can be concluded that micromorphological traits also support the recent transfer of Micromeria sect. Pseudomelissa to the genus Clinopodium.
2.2. Pollen
The pollen of all Micromeria and Clinopodium species examined is single (monad pollen) and isopolar with an elliptical equatorial outline (Figure 3 and Figure 4).
The polar view shows a circular shape with visible ends of apertures. The pollen has six apertures (hexacolpate pollen) located in the equatorial pollen belt (zonocolpate pollen). The apertures are long and rather narrow, widest in the middle and gradually narrowing towards the poles. The margins of the apertures are clear and sharp, while the ends are narrow and pointed. The membranes are ornamented. The apocolpium is relatively small, while the mesocolpium is quite large. The pollen exine is semitectate with medium reticulate ornamentation. The reticulum meshes are unequal (heterobrochate reticulum type) with more or less smooth surfaces of muri. Only the pollen exine of M. cristata ssp. cristata and M. cristata ssp. kosaninii show uneven surfaces of the muri (Figure 3). The lumina vary in size and are narrower or about the same width as the muri, rarely wider than muri as in M. croatica (Figure 3). The shape of the lumina is irregular with obtuse angles. So far, the pollen of Micromeria marginata, M. croatica, M. longipedunculata, and M. imbricata (Forssk.) C. Chr. have been described in detail [15,21,23]. In general, there is no visible difference in pollen shape between the Micromeria and Clinopodium species studied.
The size of pollen grains according to polar and equatorial axis is shown in Table 3. According to Erdtman [20], the pollen of M. cristata ssp. kosaninii, M. longipedunculata, M. microphylla, and C. thymifolium belong to the small pollen, while the pollen of the other investigated species belong to the medium pollen. Micromeria longipedunculata and M. microphylla have the smallest pollen (according to the length of the longer axis, 21.10 and 21.80 µm, respectively). On the other hand, M. graeca ssp. graeca and M. graeca ssp. fruticulosa have the largest pollen (by the longer axis, 34.65 and 33.86 µm, respectively). The size of pollen grains of M. croatica in this study was similar to the results of Kremer et al. [15], who studied the pollen of this species from another locality. Comparable results were also obtained for the pollen of M. juliana, M. kerneri, and M. longipedunculata [16,34]. Micromeria marginata has middle-large pollen with a polar axis of 26.6 μm and an equatorial diameter of 35.2 μm [21]. According to Doaigey et al. [23], the pollen of Micromeria imbricata has a length of 34.57 and 31.33 µm (polar and equatorial axis, respectively). The smallest pollen among the investigated Clinopodium species was in C. thymifolium (23.52 µm), while the largest pollen (according to longer axis 32.47 µm) was in C. dalmaticum. The measure of polar length of Clinopodium foliosum pollen ranges from 20.45–28.6 μm and for C. menthifolium from 25.7–31.4 μm [24]. On the other hand, the equatorial width is 20.46–28.57 μm for C. foliosum and 20.9–31.43 μm for C. menthifolium [24].
The results of the ANOVA show the significant difference between most of the studied taxa in terms of pollen size (Table 4 and Table 5). Although there is a significant difference between most of Micromeria and Clinopodium taxa, this difference is not clear. There is a significant difference between the closely related taxa M. cristata ssp. cristata and M. cristata ssp. kosaninii in terms of equatorial diameter. However, there is a significant difference between the closely related taxa M. graeca ssp. graeca and M. graeca ssp. fruticulosa according to the polar axis. There is no significant difference between M. croatica and M. pseudocroatica, which are one species according to Bräuchler et al. [8]. On the other hand, there is a significant difference between C. dalmaticum from Orjen Mt (Montenegro) and C. dalmaticum from Mesta River Valley (Bulgaria) for both polar and equatorial axes.
3. Materials and Methods
3.1. Plant Material
The survey included, depending on the point of view [8,9,12,41,42,43,44,45], nine to ten Micromeria taxa from the Balkan Peninsula (Table 6, Figure 5, Figure 6 and Figure 7): M. cristata (Hampe) Griseb. ssp. cristata, M. cristata ssp. kosaninii (Šilić) Bräuchler et Govaerts (syn. M. kosaninii Šilić), M. croatica (Pers.) Schott (including M. pseudocroatica Šilić), M. graeca (L.) Benth. ex Rchb. ssp. graeca, M. graeca ssp. fruticulosa (Bertol.) Guinea (syn. M. fruticulosa (Bertol.) Šilić), M. juliana (L.) Benth. ex Rchb., M. kerneri Murb., M. longipedunculata Bräuchler, (syn. M. parviflora Rchb.), and M. microphylla (d’Urv.) Benth. In addition, five to six, depending on point of view [8,12,19,41,42,43,44,45,46], taxa recently transferred from the genus Micromeria to the genus Clinopodium were studied, namely Clinopodium dalmaticum (Benth.) Bräuchler et Heubl (syn. Micromeria dalmatica Benth.) including M. bulgarica (Velen.) Vandas, C. frivaldszkyanum (Degen) Bräuchler et Heubl (syn. M. frivaldszkyana (Degen) Velen.), C. pulegium (Rochel) Bräuchler (syn. M. pulegium (Rochel) Benth.), C. serpyllifolium (M. Bieb.) Kuntze (syn. M. albanica (Griseb. ex K. Malý) Šilić), and C. thymifolium (Scop.) Kuntze (syn. M. thymifolia (Scop.) Fritch.). Each locality was described with GPS coordinates and elevation. Voucher specimens of the plant material were deposited in the Herbarium “Fran Kušan” (HFK-HR), Faculty of Pharmacy and Biochemistry, University of Zagreb, Croatia (Table 6 and Table 7).
Samples of the stems, leaves, and flowers of ten plants per population were fixed in FAA (formalin/96% ethanol/acetic acid/water: 5/70/5/20). After three days the samples were transferred from the fixation medium to 70% (v/v) ethanol and stored in the refrigerator until analysis.
The samples for scanning electron microscopic (SEM) investigation were transferred from 70% (v/v) ethanol to 70% (v/v) acetone. Then, the samples were dehydrated from 70% (v/v) to 90% (v/v), and 100% (v/v) acetone. The dehydrated samples were subjected to critical point drying using CO2 as the drying medium (CPD030; Bal-tec, Balzers, Liechtenstein). The samples were then sputter coated with gold (Sputter Coater, Agar Scientific Ltd., Essex, UK) and examined under the scanning electron microscope XL30 ESEM (FEI) with an acceleration voltages of 20 kV in high vacuum mode. The presence and abundance of the different trichome types was qualitatively assessed (− missing, ± rare, + present, ++ abundant, +++ extremely abundant). Pollen was collected from the anthers of several flowers per plant after critical point drying. A total of pollen from ten plants per population studied was mixed and examined under a scanning electron microscope. The length of 30 pollen grains per population was measured. Pollen size is expressed as the length of the longest axis according to Erdman [20]. Common terminology was used in describing trichomes and pollen [25,47].
3.2. Statistical Analysis
Descriptive statistics: minimum (Min), maximum (Max), mean, standard deviation (Stdev) and coefficient of variation (CV) for length and diameter of pollen grains were calculated. Polar end equatorial axis lengths of pollen grains were subjected to One-way Analysis of Variance (ANOVA). Differences between taxa were tested with Tukey’s HSD post hoc tests [48].
4. Conclusions
Non-glandular trichomes, peltate trichomes, and four subtypes of capitate trichomes were observed on the aerial parts of the Micromeria and Clinopodium taxa examined. The NG trichomes, peltate trichomes and capitate trichomes of subtype 1 (bent trichomes consisting of a basal epidermal cell and an elliptically shaped head cell) were observed in both Micromeria and Clinopodium taxa. Capitate trichomes of subtype 2 (erect trichomes consisting of a basal epidermal cell, two to three stalk cells and a rounded head cell) were observed only in Micromeria taxa, while capitate trichomes of subtype 3 (upright trichomes consisting of a basal epidermal cell, a relatively short stalk cell and a rounded celled head) and subtype 4 (upright trichomes consisting of a basal epidermal cell, a stalk cell, and a narrow and elongated head cell) were observed only in Clinopodium taxa. Such a distribution of capitate trichomes subtypes in Micromeria and Clinopodium taxa shows that, on the basis of micromorphological traits, it is possible to distinguish taxa from the former Pseudomelissa section from other Micromeria taxa. In this way, micromorphological traits support the recent transfer of Micromeria species from the section Pseudomelissa to the genus Clinopodium.
On the other hand, the pollen studies have shown that there are no significant differences between pollen of the Micromeria and Clinopodium taxa.
Author Contributions
Conceptualization, D.K., V.D.; Methodology, E.S.; Formal Analysis, D.K., E.S.; Investigation, D.K., E.S., F.B., D.B., E.E., D.S., V.M., V.R., D.I., M.R.; Data Curation, D.K., E.S.; Writing—Original Draft Preparation, D.K., F.B.; Writing—Review and Editing, D.K., V.D., D.B.; Visualization, D.K., F.B.; Supervision, V.D. All authors have read and agreed to the published version of the manuscript.
Funding
This research received no external funding.
Institutional Review Board Statement
Not applicable.
Informed Consent Statement
Not applicable.
Conflicts of Interest
The authors declare no conflict of interest.
References
- Harley, R.M.; Atkins, S.; Budantsev, A.L.; Cantino, P.D.; Conn, B.J.; Grayer, R.; Harley, M.M.; De Kok, R.P.J.; Krestovskaja, T.; Morales, R. Labiatae. In The Families and Genera of Vascular Plants, 1st ed.; Kubitzki, K., Ed.; Springer: Berlin, Germany, 2004; Volume 4, pp. 167–282. [Google Scholar]
- Briquet, J. Labiatae. In Die Naturlichen Pflanzenfamilien; Engler, A., Prantl, K., Eds.; Wilhelm Engelmann: Leipzig, Germany, 1895–1897; Volume 4, pp. 183–380. [Google Scholar]
- Killick, D.J.B. South African species of Satureia. Bothalia 1961, 7, 435–437. [Google Scholar] [CrossRef] [Green Version]
- Greuter, W.; Burdet, H.M.; Long, D. Satureja. In Med-Checklist; Conservatoire et Jardin Botaniques de la ville de Genève: Geneva, Switzerland, 1986; Volume 3, pp. 323–341. [Google Scholar]
- Bentham, G. Labiatae. In Prodromus Systematis Universalis Regni Vegetabilis; Candolle, A.P., Ed.; Treuttel et Würtz: Paris, France, 1848; Volume 12, pp. 212–226. [Google Scholar]
- Doroszenko, A. Taxonomic Studies on the Satureja Complex (Labiatae). Ph.D. Thesis, Edinburgh University, Edinburgh, UK, 1986. [Google Scholar]
- Valverde, R.M. Sinopsis y distribución del género Micromeria Bentham. Bot. Complut. 1993, 18, 157–168. [Google Scholar]
- Bräuchler, C.; Ryding, O.; Heubl, G. The genus Micromeria (Lamiaceae), a synoptical update. Willdenowia 2008, 38, 363–410. [Google Scholar] [CrossRef] [Green Version]
- Erhardt, W.; Götz, E.; Bödeker, N.; Seybold, S. Zander–Handwörterbuch der Pflanzennamen, 19th ed.; Eugen Ulmer GmbH und Co.: Stuttgart, Germany, 2014; p. 576. [Google Scholar]
- Bräuchler, C.; Meimberg, H.; Abele, T.; Heubl, G. Polyphyly of the genus Micromeria (Lamiaceae)—Evidence from cpDNA sequence data. Taxon 2005, 54, 639–650. [Google Scholar] [CrossRef]
- Bräuchler, C.; Meimberg, H.; Heubl, G. New names in old world Clinopodium—The transfer of the species of Micromeria sect. Pseudomelissa to Clinopodium. Taxon 2006, 55, 977–981. [Google Scholar] [CrossRef]
- Chater, A.O.; Guinea, E. Micromeria Benth. In Flora Europaea; Tutin, T.G., Heywood, V.H., Burges, N.A., Moore, D.M., Valentine, D.H., Walters, S.M., Webb, D.A., Eds.; Cambridge University Press: Cambridge, UK, 1972; Volume 3, pp. 167–170. [Google Scholar]
- Werker, E.; Ravid, U.; Putievsky, E. Structure of glandular hairs and identification of the main components of their secreted material in some species of the Labiatae. Isr. J. Bot. 1985, 34, 31–45. [Google Scholar] [CrossRef]
- Husain, S.Z.; Marin, P.D.; Šilić, Č.; Qaser, M.; Petković, B. A micromorphological studies of some representative genera in the tribe Saturejeae. Bot. J. Linn. Soc. 1990, 103, 59–80. [Google Scholar] [CrossRef]
- Kremer, D.; Stabentheiner, E.; Dunkić, V.; Müller, I.D.; Vujić, L.; Kosalec, I.; Ballian, D.; Bogunić, F.; Bezić, N. Micromorphological and chemotaxonomical Traits of Micromeria croatica (Pers.) Schott. Chem. Biodivers. 2012, 9, 755–768. [Google Scholar] [CrossRef]
- Kremer, D.; Dunkić, V.; Ruščić, M.; Matevski, V.; Ballian, D.; Bogunić, F.; Eleftheriadou, E.; Stešević, D.; Kosalec, I.; Bezić, N.; et al. Micromorphological traits and essential oil contents of Micromeria kerneri Murb. and M. juliana (L.) Benth. (Lamiaceae). Phytochemistry 2014, 98, 128–136. [Google Scholar] [CrossRef] [PubMed]
- Dunkić, V.; Kremer, D.; Grubešić, R.J.; Rodríguez, J.V.; Ballian, D.; Bogunić, F.; Stešević, D.; Kosalec, I.; Bezić, N.; Stabentheiner, E. Micromorphological and phytochemical traits of four Clinopodium L. species (Lamiaceae). S. Afr. J. Bot. 2017, 111, 232–241. [Google Scholar] [CrossRef]
- Kaya, A. Morphological characteristics of Clinopodium acinos and Clinopodium suaveolens (Lamiaceae) growing in Turkey. J. Res. Pharm. 2019, 23, 62–68. [Google Scholar] [CrossRef] [Green Version]
- Mladenova, T.R.; Stoyanov, P.S.; Michova-Nankova, I.K.; Mladenov, R.D.; Boyadzhiev, D.T.; Bivolarska, A.V.; Todorov, K.T. Comparative leaf epidermis analyses of Micromeria frivaldszkyana (Degen) Velen. and Clinopodium vulgare L. (Lamiaceae) from Bulgarka Nature Park, Bulgaria. Ecol. Balk. 2019, 11, 133–140. [Google Scholar]
- Erdtman, G. Handbook of Palynology; Scandinavian Univ. Books: Munksgaard, Denmark, 1969. [Google Scholar]
- Moon, H.-K.; Vinckier, S.; Smets, E.; Huysmans, S. Palynological evolutionary trends within the tribe Menthae with special emphasis on subtribe Menthinae (Nepetoideae: Lamiaceae). Plant Syst. Evol. 2008, 275, 93–108. [Google Scholar] [CrossRef] [Green Version]
- Firat, M.; Akçiçek, E.; Kaya, A. Clinopodium serpyllifolium subsp. sirnakense (Lamiaceae), a new taxon from south-eastern Anatolia, Turke. Phytotaxa 2015, 201, 131–139. [Google Scholar] [CrossRef]
- Doaigey, A.R.; El-Zaidy, M.; Alfarhan, A.; Milagy, A.E.-S.; Jacob, T. Pollen morphology of certain species of the family Lamiaceae in Saudi Arabia. Saudi J. Biol. Sci. 2018, 25, 354–360. [Google Scholar] [CrossRef]
- Padure, I.; Simic, S. Pollen and nutlet surface micromorphology of Clinopodium foliosum and C. menthifolium (Lamiaceae) from Istria. Joannea Botanik 2019, 16, 83–89. [Google Scholar]
- Payne, W.W. A glossary of plant hair terminology. Brittonia 1978, 30, 239–255. [Google Scholar] [CrossRef]
- Giuliani, C.; Bini, L.M. Insight into the structure and chemistry of glandular trichomes of Labiatae, with the emphasis on subfamily Lamioideae. Plant Syst. Evol. 2008, 276, 199–208. [Google Scholar] [CrossRef]
- Werker, E. Trichome Diversity and Development. In Advances in Botanical Research Incorporating Advances in Plant Pathology, 1st ed.; Hallahand, D.L., Gray, J., Callow, J.A., Eds.; Academic Press: London, UK, 2000; Volume 31, pp. 1–35. [Google Scholar]
- Corsi, G.; Bottega, S. Glandular hairs of Salvia officinalis: New data on morphology, localization and histochemistry in relation to function. Ann. Bot. 1999, 84, 657–664. [Google Scholar] [CrossRef] [Green Version]
- Jia, P.; Liu, H.; Gao, T.; Xin, H. Glandular Trichomes and Essential Oil of Thymus quinquecostatus. Sci. World J. 2013, 3, 387952. [Google Scholar] [CrossRef] [Green Version]
- Kowalczuk, A.P.; Raman, V.; Galal, A.M.; Khan, I.A.; Siebert, D.J.; Zjawiony, J.K. Vegetative anatomy and micromorphology of Salvia divinorum (Lamiaceae). J. Nat. Med. 2014, 68, 63–73. [Google Scholar] [CrossRef]
- Stojičić, D.; Tošić, S.; Slavkovska, V.; Zlatković, B.; Budimir, S.; Janošević, D.; Uzelac, B. Glandular trichomes and essential oil characteristics of in vitro propagated Micromeria pulegium (Rochel) Benth. (Lamiaceae). Planta 2016, 244, 393–404. [Google Scholar] [CrossRef]
- Tozin, L.R.S.; Rodrigues, T.M. Morphology and histochemistry of glandular trichomes in Hyptis villosa Pohl ex Benth. (Lamiaceae) and differential labeling of cytoskeletal elements. Acta Bot. Brasilica 2017, 31, 330–343. [Google Scholar] [CrossRef] [Green Version]
- Koca, F. Morphological and anatomical properties of Micromeria myrtifolia Boiss. et Hohen. Acta Pharm. Sci. 2002, 44, 235–242. [Google Scholar]
- Kremer, D.; Dunkić, V.; Stešević, D.; Kosalec, I.; Ballian, D.; Bogunić, F.; Bezić, N.; Stabentheiner, E. Micromorphological traits and essential oil of Micromeria longipedunculata Bräuchler (Lamiaceae). Cent. Eur. J. Biol. 2014, 9, 559–568. [Google Scholar] [CrossRef] [Green Version]
- Marin, M.; Jasnić, N.; Ascensão, L. Histochemical, micromorphology and ultrastructural investigation in glandular trichomes of Micromeria thymifolia. Bot. Serb. 2013, 37, 49–53. [Google Scholar]
- Hanlidou, E.; Kokkini, S.; Bosabalidis, A.M.; Bessiere, J.-M. Glandular trichomes and essential oil constituents of Calamintha menthifolia (Lamiaceae). Plant Syst. Evol. 1991, 177, 17–26. [Google Scholar] [CrossRef]
- Sonboli, A.; Fakhari, A.; Kanani, M.R.; Yousefzadi, M. Antimicrobial activity, essential oil composition and micromorphology of trichomes of Satureja laxiflora C. Koch from Iran. Z. Naturforsch C 2004, 59, 777–781. [Google Scholar] [CrossRef]
- Dunkić, V.; Kremer, D.; Müller, I.D.; Stabentheiner, E.; Kuzmić, S.; Grubešić, R.J.; Vujić, L.; Kosalec, I.; Randić, M.; Srečec, S.; et al. Chemotaxonomic and micromorphological traits of Satureja montana L. and S. subspicata Vis. (Lamiaceae). Chem. Biodivers. 2012, 9, 2825–2842. [Google Scholar] [CrossRef]
- Dodoš, T.; Janković, S.; Marin, P.D.; Rajčević, N. Essential oil composition and micromorphological traits of Satureja montana L., S. subspicata Bartel ex Vis., and S. kitaibelii Wierzb. ex Heuff. plant organs. Plants 2021, 10, 511. [Google Scholar] [CrossRef]
- Al-Zubaidy, A.M.A.; Hassan, K.I.; Jabbari, B.S. A comparative anatomical study of the genera Clinopodium L., Hymenocrater Fish. & Mey. and Melissa L. (Lamiaceae) in Kurdistan Region of Iraq. Diyala J. Pure Sci. 2015, 11, 30–43. [Google Scholar]
- Diklić, N. Micromeria Bentham. In Flora SR Srbije; Josifović, M., Ed.; Academie Serbe des Sciences et des Arts: Belgrade, Serbia, 1974; Volume 6, pp. 458–462. [Google Scholar]
- Šilić, Č. Monography of genuses Satureja L., Calamintha Miller, Micromeria Bentham, Acinos Miller and Clinopodium L. in flora of Yugoslavia; Zemaljski muzej BiH: Sarajevo, Bosnia and Herzegovina, 1979; pp. 172–262. [Google Scholar]
- Ančev, M. Micromeria Benth. In Flora Reipublicae Popularis Bulgaricae; Velčev, V., Ed.; Academiae Scientiarum Bulgaricae, Serdicae: Sofia, Bulgaria, 1989; Volume 9, pp. 356–362. [Google Scholar]
- Melnikov, D.G. New sections of the genus Clinopodium L. (Lamiaceae) and their synopsis. Turczaninowia 2015, 18, 103–112. [Google Scholar] [CrossRef] [Green Version]
- Nikolić, T. Flora Croatica; Alfa: Zagreb, Croatia, 2019; Volume 4, pp. 408–409. [Google Scholar]
- Matevski, V. Clinopodium albanicum (Griseb. ex K. Malý) Melnikov new species for the flora of the Republic of Macedonia. Contrib. Sect. Nat. Math. Biotech. Sci. 2018, 39, 123–128. [Google Scholar] [CrossRef]
- Punt, W.; Hoen, P.P.; Blackmore, S.; Nilsson, S.; Le Thomas, A. Glossary of pollen and spore terminology. Rev. Palaeobot. Palynol. 2007, 143, 1–81. [Google Scholar] [CrossRef]
- Hill, T.; Lewicki, P. Statistics Methods and Applications; Stat Soft Inc.: Tulsa, OK, USA, 2006. [Google Scholar]
Figure 1.
SEM micrographs with different types and distribution of trichomes in Micromeria cristata ssp. cristata (Mc), M. cristata ssp. kosaninii (McK), M. croatica (Mcr) including M. pseudocroatica (McrP), M. graeca ssp. graeca (Mg), M. graeca ssp. fruticulosa (MgF), M. juliana (Mj), M. kerneri (Mk), M. microphylla (Mm), and M. longipedunculata (Ml). Non-glandular trichomes (NG), peltate trichome (P), Subtype 1 capitate trichomes (C1) and Subtype 2 capitate trichomes (C2) on the adaxial (1) and abaxial (2) leaf surface, on the calyx (3) and stem (4).
Figure 1.
SEM micrographs with different types and distribution of trichomes in Micromeria cristata ssp. cristata (Mc), M. cristata ssp. kosaninii (McK), M. croatica (Mcr) including M. pseudocroatica (McrP), M. graeca ssp. graeca (Mg), M. graeca ssp. fruticulosa (MgF), M. juliana (Mj), M. kerneri (Mk), M. microphylla (Mm), and M. longipedunculata (Ml). Non-glandular trichomes (NG), peltate trichome (P), Subtype 1 capitate trichomes (C1) and Subtype 2 capitate trichomes (C2) on the adaxial (1) and abaxial (2) leaf surface, on the calyx (3) and stem (4).
Figure 2.
SEM micrographs with different types and distribution of trichomes in Clinopodium dalmaticum (Cd) including Micromeria bulgarica (CdB), C. frivaldszkyanum (Cf), C. pulegium (Cp), C. serpyllifolium (Cs), and C. thymifolium (Ct). Peltate trichome (P), Subtype 1 capitate trichomes (C1), Subtype 3 capitate trichomes (C3) and Subtype 4 capitate trichomes (C4) on the adaxial (1) and abaxial (2) leaf surface, calyx (3), and stem (4).
Figure 2.
SEM micrographs with different types and distribution of trichomes in Clinopodium dalmaticum (Cd) including Micromeria bulgarica (CdB), C. frivaldszkyanum (Cf), C. pulegium (Cp), C. serpyllifolium (Cs), and C. thymifolium (Ct). Peltate trichome (P), Subtype 1 capitate trichomes (C1), Subtype 3 capitate trichomes (C3) and Subtype 4 capitate trichomes (C4) on the adaxial (1) and abaxial (2) leaf surface, calyx (3), and stem (4).
Figure 3.
SEM micrographs of pollen grains and exine surface after critical point drying in Micromeria cristata ssp. cristata (Mc), M. cristata ssp. kosaninii (McK), M. croatica (Mcr) including M. pseudocroatica (McrP), M. graeca ssp. graeca (Mg), M. graeca ssp. fruticulosa (MgF), M. juliana (Mj), M. kerneri (Mk), M. microphylla (Mm), and M. longipedunculata (Ml).
Figure 3.
SEM micrographs of pollen grains and exine surface after critical point drying in Micromeria cristata ssp. cristata (Mc), M. cristata ssp. kosaninii (McK), M. croatica (Mcr) including M. pseudocroatica (McrP), M. graeca ssp. graeca (Mg), M. graeca ssp. fruticulosa (MgF), M. juliana (Mj), M. kerneri (Mk), M. microphylla (Mm), and M. longipedunculata (Ml).
Figure 4.
SEM micrographs of pollen grains and exine surface after critical point drying in Clinopodium dalmaticum (Cd) including Micromeria bulgarica (CdB), C. frivaldszkyanum (Cf), C. pulegium (Cp), C. serpyllifolium (Cs), and C. thymifolium (Ct).
Figure 4.
SEM micrographs of pollen grains and exine surface after critical point drying in Clinopodium dalmaticum (Cd) including Micromeria bulgarica (CdB), C. frivaldszkyanum (Cf), C. pulegium (Cp), C. serpyllifolium (Cs), and C. thymifolium (Ct).
Figure 5.
Collection sites of studied Micromeria and Clinopodium taxa: M. cristata ssp. cristata (Mc), M. cristata ssp. kosaninii (McK), M. croatica (Mcr) including M. pseudocroatica (McrP), M. graeca ssp. graeca (Mg), M. graeca ssp. fruticulosa (MgF), M. juliana (Mj), M. kerneri (Mk), M. microphylla (Mm), M. longipedunculata (Ml), C. dalmaticum (Cd) including M. bulgarica (CdB), C. frivaldszkyanum (Cf), C. pulegium (Cp), C. serpyllifolium (Cs), and C. thymifolium (Ct).
Figure 5.
Collection sites of studied Micromeria and Clinopodium taxa: M. cristata ssp. cristata (Mc), M. cristata ssp. kosaninii (McK), M. croatica (Mcr) including M. pseudocroatica (McrP), M. graeca ssp. graeca (Mg), M. graeca ssp. fruticulosa (MgF), M. juliana (Mj), M. kerneri (Mk), M. microphylla (Mm), M. longipedunculata (Ml), C. dalmaticum (Cd) including M. bulgarica (CdB), C. frivaldszkyanum (Cf), C. pulegium (Cp), C. serpyllifolium (Cs), and C. thymifolium (Ct).
Figure 6.
Photographs of Micromeria cristata ssp. cristata (Mc), M. cristata ssp. kosaninii (McK), M. croatica (Mcr) including M. pseudocroatica (McrP), M. graeca ssp. graeca (Mg), M. graeca ssp. fruticulosa (MgF), M. juliana (Mj), M. kerneri (Mk), M. longipedunculata (Ml) and M. microphylla (Mm).
Figure 6.
Photographs of Micromeria cristata ssp. cristata (Mc), M. cristata ssp. kosaninii (McK), M. croatica (Mcr) including M. pseudocroatica (McrP), M. graeca ssp. graeca (Mg), M. graeca ssp. fruticulosa (MgF), M. juliana (Mj), M. kerneri (Mk), M. longipedunculata (Ml) and M. microphylla (Mm).
Figure 7.
Photographs of Clinopodium dalmaticum (Cd) including Micromeria bulgarica (CdB), C. frivaldszkyanum (Cf), C. thymifolium (Ct), C. pulegium (Cp) and C. serpyllifolium (Cs).
Figure 7.
Photographs of Clinopodium dalmaticum (Cd) including Micromeria bulgarica (CdB), C. frivaldszkyanum (Cf), C. thymifolium (Ct), C. pulegium (Cp) and C. serpyllifolium (Cs).
Table 1.
Occurrence and frequency of trichomes on aerial parts of Micromeria taxa.
| Taxon/ | Trichomes | Leaf | Calyx | Stem | |
|---|---|---|---|---|---|
| Locality | Adaxial | Abaxial | |||
| M. cristata | NG | + | +/++ | ++ | + |
| ssp. cristata | peltate | + | + | ++ | + |
| Humsko | capitate C1 | +/++ | + | + | + |
| Brdo | capitate C2 | − | ±/+ | + | + |
| M. cristata | NG | + | +/++ | ++ | ++ |
| ssp. cristata | peltate | + | + | + | + |
| Vitosha Mt | capitate C1 | + | + | + | + |
| capitate C2 | − | ±/+ | + | ± | |
| M. cristata | NG | + | +/++ | ++ | +/++ |
| ssp. cristata | peltate | +/++ | + | +/++ | + |
| Pirin Mt | capitate C1 | + | + | + | + |
| capitate C2 | − | + | ± | ± | |
| M. cristata | NG | +/++ | +/++ | +/++ | + |
| ssp. cristata | peltate | + | + | + | + |
| Demir | capitate C1 | ±/+ | + | −/± | + |
| Kapija | capitate C2 | −/± | +/++ | +/++ | ±/+ |
| M. cristata | NG | +/++ | + | ++ | + |
| ssp. cristata | peltate | + | + | + | + |
| Nomos | capitate C1 | ±/+ | + | + | + |
| Serron | capitate C2 | − | + | + | +/++ |
| M. cristata | NG | + | +/++ | ++ | +/++ |
| ssp. cristata | peltate | + | + | + | ±/+ |
| Paikon Mt | capitate C1 | + | +/++ | + | + |
| capitate C2 | − | +/++ | + | +/++ | |
| M. cristata | NG | ++ | ++ | ++ | +/++ |
| ssp. kosaninii | peltate | +/++ | + | + | + |
| Pletvar | capitate C1 | ±/+ | ±/+ | + | + |
| capitate C2 | ±/+ | +/++ | ±/+/++ | + | |
| M. croatica | NG | + | + | + | + |
| Rossijev | peltate | − | +/++ | + | + |
| kuk | capitate C1 | − | ±/+ | ± | − |
| capitate C2 | ±/++ | ++ | ++ | − | |
| M. croatica | NG | + | + | ++ | + |
| Stupačinovo | peltate | − | + | −/± | + |
| capitate C1 | − | +/++ | + | ± | |
| capitate C2 | − | ±/++ | ± | +/++ | |
| M. croatica | NG | + | + | ++ | + |
| Dubočani | peltate | − | ++ | +/++ | + |
| capitate C1 | − | ±/++ | +/++ | ± | |
| capitate C2 | −/++ | ±/++ | ±/+ | +/++ | |
| M. croatica | NG | + | + | + | + |
| (syn. M. | peltate | − | ++ | + | + |
| pseudocroatica) | capitate C1 | ± | +/++ | + | + |
| Pijavičino | capitate C2 | ± | ++ | ++ | +/++ |
| M. croatica | NG | + | + | + | + |
| (syn. M. | peltate | − | ++ | + | + |
| pseudocroatica) | capitate C1 | ± | +/++ | + | + |
| Prapratno | capitate C2 | ± | ++ | ++ | +/++ |
| M. graeca | NG | ++ | ++ | +/++ | +/++ |
| ssp. graeca | peltate | + | + | + | + |
| Malo | capitate C1 | ± | ++ | ++ | + |
| zlo polje | capitate C2 | ± | + | ++ | + |
| M. graeca | NG | ++ | ++ | +/++ | +/++ |
| ssp. graeca | peltate | + | ++ | + | + |
| Komiža | capitate C1 | ± | ++ | + | + |
| capitate C2 | ± | + | ++ | ± | |
| M. graeca | NG | ++ | + | +/++ | ++ |
| ssp. fruticulosa | peltate | ±/++ | + | + | + |
| Sušac | capitate C1 | ± | + | + | + |
| capitate C2 | ± | + | + | + | |
| M. juliana | NG | + | + | ++ | +/++ |
| Grude | peltate | + | + | + | + |
| capitate C1 | ± | + | + | ±/+ | |
| capitate C2 | − | + | + | + | |
| M. juliana | NG | + | + | ++ | + |
| Cijevna | peltate | + | + | + | + |
| capitate C1 | + | ± | ++ | + | |
| capitate C2 | − | ++ | ++ | + | |
| M. juliana | NG | ++ | ++ | ++ | ++ |
| Rajec Reka | peltate | + | + | + | + |
| capitate C1 | ± | + | + | + | |
| capitate C2 | − | + | + | + | |
| M. juliana | NG | + | +/++ | +/++ | +/++ |
| Cholomon Mt | peltate | + | + | ±/+ | + |
| capitate C1 | + | + | + | + | |
| capitate C2 | − | ±/+ | ± | + | |
| M. kerneri | NG | +/++ | + | ++ | +/++ |
| Zavratnica | peltate | + | + | +/++ | + |
| bay | capitate C1 | ± | + | ± | + |
| capitate C2 | − | + | ++ | + | |
| M. kerneri | NG | +/++ | + | ++ | + |
| Mostar | peltate | ± | + | + | + |
| capitate C1 | ± | + | ±/+ | ± | |
| capitate C2 | − | ± | ++ | − | |
| M. | NG | + | + | + | +/++ |
| longipedunculata | peltate | − | + | + | ± |
| Jazina | capitate C1 | ± | +/++ | + | + |
| capitate C2 | − | + | + | ± | |
| M. | NG | + | + | + | + |
| longipedunculata | peltate | − | + | + | ± |
| Krivošije Mt | capitate C1 | ± | +/++ | + | + |
| capitate C2 | − | + | + | ±/+ | |
| M. microphylla | NG | + | + | ++ | + |
| Svetac Island | peltate | + | + | + | + |
| capitate C1 | −/±/+ | ±/+ | ± | ±/+ | |
| capitate C2 | − | + | +/++ | + | |
Note: NG = non-glandular trichomes; trichomes frequency: −, trichomes completely missing; ±, trichomes are present in small numbers; +, trichomes are moderately present; ++, trichomes are present in large numbers.
Table 2.
Occurrence and frequency of trichomes on aerial parts of Clinopodium taxa.
| Taxon/ | Trichomes | Leaf | Calyx | Stem | |
|---|---|---|---|---|---|
| Locality | Adaxial | Abaxial | |||
| C. dalmaticum | NG | + | +/++ | + | +/++ |
| Orjen | peltate | + | +/+ | + | + |
| capitate C1 | + | ±/+ | ±/+ | +/++ | |
| capitate C3 | ± | ++ | +/++ | − | |
| capitate C4 | − | ± | ± | ± | |
| C. dalmaticum | NG | + | +/++ | +/++ | + |
| (syn. M. bulgarica) | peltate | ± | + | +/++ | + |
| Mesta | capitate C1 | + | +/++ | ±/+/++ | ++ |
| River | capitate C3 | − | −/± | ±/+ | ± |
| Valley | capitate C4 | − | − | ±/+ | −/± |
| C. dalmaticum | NG | + | + | +/++ | + |
| (syn. M. bulgarica) | peltate | ± | ++ | +/++ | + |
| Vlahina Mt | capitate C1 | + | +/++ | + | ++ |
| capitate C3 | − | − | − | − | |
| capitate C4 | − | − | −/± | −/± | |
| C. frivaldszkyanum | NG | ± | ± | + | −/+ |
| Malusha peak | peltate | ±/+ | + | +/++ | −/+ |
| capitate C1 | + | ++ | + | + | |
| capitate C3 | − | − | − | − | |
| capitate C4 | − | −/± | + | − | |
| C. frivaldszkyanum | NG | ± | ±/+ | + | + |
| Vikanata Skala | peltate | ± | + | + | + |
| Nature | capitate C1 | + | + | + | + |
| Monument | capitate C3 | − | − | −/± | − |
| capitate C4 | − | − | + | − | |
| C. pulegium | NG | ± | + | + | + |
| Međeđa | peltate | + | ++ | ++ | + |
| capitate C1 | ± | +/++ | +/++ | + | |
| capitate C3 | − | − | − | − | |
| capitate C4 | − | − | ± | − | |
| C. serpyllifolium | NG | +++ | +++ | ++ | ++ |
| Prizren | peltate | + | + | + | + |
| capitate C1 | + | ++ | ++ | +/++ | |
| capitate C3 | − | ± | ± | ± | |
| capitate C4 | − | ± | ± | − | |
| C. thymifolium | NG | ± | + | + | + |
| Učka Mt | peltate | + | +/++ | +/++ | + |
| capitate C1 | +/++ | +/++ | +/++ | +/++ | |
| capitate C3 | − | − | ± | − | |
| capitate C4 | − | − | ± | − | |
| C. thymifolium | NG | + | + | + | +/++ |
| Dokozina | peltate | + | +/++ | +/++ | + |
| plan | capitate C1 | + | ++ | ++ | + |
| capitate C3 | − | − | − | − | |
| capitate C4 | − | − | − | − | |
| C. thymifolium | NG | + | + | + | + |
| Šušanj | peltate | + | ++ | +/++ | + |
| capitate C1 | + | ++ | +/++ | + | |
| capitate C3 | − | − | − | − | |
| capitate C4 | − | − | ± | − | |
| C. thymifolium | NG | + | + | + | + |
| Blidinje | peltate | + | +/++ | +/++ | + |
| capitate C1 | + | ++ | +/++ | + | |
| capitate C3 | ± | − | − | − | |
| capitate C4 | − | − | − | − | |
| C. thymifolium | NG | ± | + | + | ±/+ |
| Manastir | peltate | + | +/++ | +/++ | + |
| Morače | capitate C1 | +/++ | ++ | ++ | +/++ |
| capitate C3 | − | − | − | − | |
| capitate C4 | − | − | ± | − | |
Note: NG = non-glandular trichomes; trichomes frequency: −, trichomes completely missing; ±, trichomes are present in small numbers; +, trichomes are moderately present; ++, trichomes are present in large numbers; +++, trichomes completely cover the surface.
Table 3.
Descriptive statistics for length of Micromeria and Clinopodium pollen grain according to polar (P) and equatorial (E) axis. Mean, Stdev, Min, and Max are in µm; CV is in %.
Table 3.
Descriptive statistics for length of Micromeria and Clinopodium pollen grain according to polar (P) and equatorial (E) axis. Mean, Stdev, Min, and Max are in µm; CV is in %.
| Taxon | Polar Axis (P) | Equatorial Axis (E) | Pollen Size | P/E Ratio | |
|---|---|---|---|---|---|
| M. cristata ssp. cristata | Mean | 21.65 | 25.90 | Medium | 0.84 |
| Stdev | 1.10 | 2.28 | |||
| Min | 19.40 | 21.30 | |||
| Max | 23.60 | 28.60 | |||
| CV | 5.08 | 8.80 | |||
| M. cristata ssp. kosaninii | Mean | 21.00 | 22.94 | Small | 0.92 |
| Stdev | 0.91 | 1.10 | |||
| Min | 19.00 | 21.30 | |||
| Max | 22.70 | 25.00 | |||
| CV | 4.33 | 4.80 | |||
| M. croatica | Mean | 25.97 | 28.22 | Medium | 0.92 |
| Stdev | 1.86 | 1.93 | |||
| Min | 23.90 | 25.70 | |||
| Max | 30.50 | 32.40 | |||
| CV | 7.16 | 6.84 | |||
| M. croatica (syn. M. pseudocroatica) | Mean | 26.35 | 29.65 | Medium | 0.89 |
| Stdev | 2.38 | 2.80 | |||
| Min | 22.10 | 25.40 | |||
| Max | 30.00 | 23.90 | |||
| CV | 9.03 | 9.44 | |||
| M. graeca ssp. graeca | Mean | 28.65 | 34.65 | Medium | 0.83 |
| Stdev | 2.42 | 2.69 | |||
| Min | 24.60 | 31.20 | |||
| Max | 33.00 | 44.00 | |||
| CV | 8.45 | 7.76 | |||
| M. graeca ssp. fruticulosa | Mean | 26.73 | 33.86 | Medium | 0.79 |
| Stdev | 3.16 | 2.74 | |||
| Min | 22.40 | 28.10 | |||
| Max | 35.20 | 38.00 | |||
| CV | 11.82 | 8.09 | |||
| M. juliana | Mean | 23.37 | 27.10 | Medium | 0.86 |
| Stdev | 1.21 | 1.29 | |||
| Min | 21.30 | 25.10 | |||
| Max | 26.30 | 29.40 | |||
| CV | 5.18 | 4.76 | |||
| M. kerneri | Mean | 23.92 | 27.92 | Medium | 0.86 |
| Stdev | 1.40 | 1.02 | |||
| Min | 21.90 | 26.50 | |||
| Max | 26.20 | 29.90 | |||
| CV | 5.85 | 3.65 | |||
| M. longipedunculata | Mean | 18.18 | 21.10 | Small | 0.86 |
| Stdev | 0.74 | 1.67 | |||
| Min | 17.10 | 18.30 | |||
| Max | 19.40 | 25.50 | |||
| CV | 4.07 | 7.91 | |||
| M. microphylla | Mean | 18.65 | 21.80 | Small | 0.86 |
| Stdev | 1.18 | 0.90 | |||
| Min | 16.60 | 20.30 | |||
| Max | 20.80 | 23.60 | |||
| CV | 6.32 | 4.13 | |||
| C. dalmaticum | Mean | 26.67 | 32.47 | Medium | 0.82 |
| Stdev | 1.52 | 3.28 | |||
| Min | 24.40 | 27.50 | |||
| Max | 29.20 | 37.90 | |||
| CV | 5.70 | 10.10 | |||
| C. dalmaticum (syn. M. bulgarica) | Mean | 21.37 | 25.95 | Medium | 0.82 |
| Stdev | 2.82 | 1.35 | |||
| Min | 15.70 | 23.40 | |||
| Max | 24.10 | 27.30 | |||
| CV | 13.20 | 5.20 | |||
| C. frivaldszkyanum | Mean | 25.46 | 28.36 | Medium | 0.90 |
| Stdev | 1.23 | 0.99 | |||
| Min | 24.00 | 26.30 | |||
| Max | 28.50 | 29.40 | |||
| CV | 4.83 | 3.49 | |||
| C. pulegium | Mean | 26.87 | 28.90 | Medium | 0.93 |
| Stdev | 2.54 | 3.00 | |||
| Min | 25.00 | 26.10 | |||
| Max | 21.00 | 33.60 | |||
| CV | 9.45 | 10.38 | |||
| C. serpyllifolium | Mean | 22.27 | 26.21 | Medium | 0.85 |
| Stdev | 3.10 | 2.07 | |||
| Min | 12.60 | 22.60 | |||
| Max | 26.30 | 29.60 | |||
| CV | 13.92 | 7.89 | |||
| C. thymifolium | Mean | 22.15 | 23.52 | Small | 0.94 |
| Stdev | 1.21 | 1.17 | |||
| Min | 19.70 | 21.50 | |||
| Max | 24.60 | 25.90 | |||
| CV | 5.46 | 4.97 |
Table 4.
Results of Tukey HSD post hoc test at the 0.05 level for the polar length of studied Micromeria and Clinopodium taxa. Presence of asterisk (*) indicates significance at p ≤ 0.05.
Table 4.
Results of Tukey HSD post hoc test at the 0.05 level for the polar length of studied Micromeria and Clinopodium taxa. Presence of asterisk (*) indicates significance at p ≤ 0.05.
| Taxon | Mc4 | McK | Mcr2 | McrP1 | Mg1 | MgF |
|---|---|---|---|---|---|---|
| McK | 0.996467 | |||||
| Mcr2 | 0.000029 * | 0.000029 * | ||||
| McrP1 | 0.000029 * | 0.000029 * | 0.999995 | |||
| Mg1 | 0.000029 * | 0.000029 * | 0.000041 * | 0.000605 * | ||
| MgF | 0.000029 * | 0.000029 * | 0.981839 | 0.999995 | 0.013724 * | |
| Mj1 | 0.054533 | 0.000335 * | 0.000059 * | 0.000030 * | 0.000029 * | 0.000029 * |
| Mk1 | 0. 000813 * | 0.000030 * | 0.005354 * | 0.000199 * | 0.000029 * | 0.000032 * |
| Ml1 | 0.000029 * | 0.000032 * | 0.000029 * | 0.000029 * | 0.000029 * | 0.000029 * |
| Mm | 0.000030 * | 0.000389 * | 0.000029 * | 0.000029 * | 0.000029 * | 0.000029 * |
| Cd | 0.000029 * | 0.000029 * | 0.992281 | 1.000000 | 0.008540 * | 1.000000 |
| CdB1 | 1.000000 | 0.999997 | 0.000029 * | 0.000029 * | 0.000029 * | 0.000029 * |
| Cf1 | 0.000029 * | 0.000029 * | 0.999806 * | 0.930688 | 0.000029 * | 0.464403 |
| Cp | 0.000029 * | 0.000029 * | 0.919882 * | 0.999711 | 0.037175 * | 1.000000 |
| Cs | 0.998023 | 0.469331 | 0.000029 | 0.000029 * | 0.000029 * | 0.000029 * |
| Ct4 | 0.999848 | 0.649443 | 0.000029 | 0.000029 * | 0.000029 * | 0.000029 * |
| Taxon | Mj1 | Mk | Ml1 | Mm | Cd | |
| Mk1 | 0.999474 | |||||
| Ml1 | 0.000029 * | 0.000029 * | ||||
| Mm | 0.000029 * | 0.000029 * | 0.999931 | |||
| Cd | 0.000029 * | 0.000035 * | 0.000029 * | 0.000029 * | ||
| CdB1 | 0.007514 * | 0.000077 * | 0.000029 * | 0.000037 * | 0.000029 * | |
| Cf1 | 0.003785 * | 0.151169 | 0.000029 * | 0.000029 * | 0.559547 | |
| Cp | 0.000029 * | 0.000030 * | 0.000029 * | 0.000029 * | 1.000000 | |
| Cs | 0.711451 | 0.081441 | 0.000029 * | 0.000029 * | 0.000029 * | |
| Ct4 | 0.534318 | 0.038831 * | 0.000029 * | 0.000029 * | 0.000029 * | |
| Taxon | Cd | CdB1 | Cf1 | Cp | Cs | |
| CdB1 | 0.000029 * | |||||
| Cf1 | 0.559547 | 0.000029 * | ||||
| Cp | 1.000000 | 0.000029 * | 0.272970 | |||
| Cs | 0.000029 * | 0.924334 | 0.000029 * | 0.000029 * | ||
| Ct4 | 0.000029 * | 0.977758 | 0.000029 * | 0.000029 * | 1.000000 | |
Table 5.
Results of Tukey HSD post hoc test at the 0.05 level for the equatorial diameter of pollen grain of studied Micromeria and Clinopodium taxa. Presence of asterisk (*) indicates significance at p ≤ 0.05.
Table 5.
Results of Tukey HSD post hoc test at the 0.05 level for the equatorial diameter of pollen grain of studied Micromeria and Clinopodium taxa. Presence of asterisk (*) indicates significance at p ≤ 0.05.
| Taxon | Mc4 | McK | Mcr2 | McrP1 | Mg1 | MgF |
|---|---|---|---|---|---|---|
| McK | 0.000032 * | |||||
| Mcr2 | 0.001274 * | 0.000029 | ||||
| McrP1 | 0.000029 * | 0.000029 * | 0.324744 | |||
| Mg1 | 0.000029 * | 0.000029 * | 0.000029 * | 0.000029 * | ||
| MgF | 0.000029 * | 0.000029 * | 0.000029 * | 0.000029 * | 0.983544 | |
| Mj1 | 0.638719 | 0.000029 * | 0.763081 | 0.000190 * | 0.000029 * | 0.000029 * |
| Mk1 | 0.012601 * | 0.000029 * | 1.000000 | 0.080933 | 0.000029 * | 0.000029 * |
| Ml1 | 0.000029 * | 0.044219 * | 0.000029 * | 0.000029 * | 0.000029 * | 0.000029 * |
| Mm | 0.000029 * | 0.725134 | 0.000029 * | 0.000029 * | 0.000029 * | 0.000029 * |
| Cd | 0.000029 * | 0.000029 * | 0.000029 * | 0.000039 * | 0.003949 | 0.379663 |
| CdB1 | 1.000000 | 0.000031 * | 0.001974 * | 0.000029 | 0.000029 * | 0.000029 * |
| Cf1 | 0.000381 * | 0.000029 * | 1.000000 | 0.518758 | 0.000029 * | 0.000029 * |
| Cp | 0.000031 * | 0.000029 * | 0.996257 | 0.990120 | 0.000029 * | 0.000029 * |
| Cs | 1.000000 | 0.000029 * | 0.014167 * | 0.000029 * | 0.000029 * | 0.000029 * |
| Ct4 | 0.000793 * | 0.999419 | 0.000029 * | 0.000029 * | 0.000029 * | 0.000029 * |
| Taxon | Mj1 | Mk | Ml1 | Mm | Cd | |
| Mk1 | 0.977496 | |||||
| Ml1 | 0.000029 * | 0.000029 * | ||||
| Mm | 0.000029 * | 0.000029 * | 0.995845 | |||
| Cd | 0.000029 * | 0.000029 * | 0.000029* | 0.000029 * | ||
| CdB1 | 0.711996 | 0.018248 * | 0.000029 * | 0.000029 * | 0.000029 * | |
| Cf1 | 0.566977 | 0.999982 | 0.000029 * | 0.000029 * | 0.000029 * | |
| Cp | 0.055158 | 0.897260 | 0.000029 * | 0.000029 * | 0.000029 * | |
| Cs | 0.950327 | 0.090359 | 0.000029 * | 0.000029 * | 0.000029 * | |
| Ct4 | 0.000029 * | 0.000029 * | 0.000581 * | 0.083981 | 0.000029 * | |
| Taxon | Cd | CdB1 | Cf1 | Cp | Cs | |
| CdB1 | 0.000029 * | |||||
| Cf1 | 0.000029 * | 0.000598 * | ||||
| Cp | 0.000029 * | 0.000032 * | 0.999755 | |||
| Cs | 0.000029 * | 1.000000 | 0.004970 * | 0.000068 * | ||
| Ct4 | 0.000029 * | 0.000505 * | 0.000029 * | 0.000029 * | 0.000068 * | |
Table 6.
Details on origin and collection data of investigated Micromeria (M.) and Clinopodium (C.) taxa.
Table 6.
Details on origin and collection data of investigated Micromeria (M.) and Clinopodium (C.) taxa.
| Taxa—According to | Collecting Site | Voucher no. | |
|---|---|---|---|
| Bräuchler et al., 2008 (Code) | Balkan Literature | ||
| M. cristata ssp. cristata (Mc1) | M. cristata | Humsko brdo Mt (Serbia) | HFK-HR-51126 |
| M. cristata ssp. cristata (Mc2) | M. cristata | Vitosha Mt (Bulgaria) | HFK-HR-51132 |
| M. cristata ssp. cristata (Mc3) | M. cristata | Pirin Mt (Bulgaria) | HFK-HR-51133 |
| M. cristata ssp. cristata (Mc4) | M. cristata | Demir Kapija (N. Macedonia) * | HFK-HR-51141 |
| M. cristata ssp. cristata (Mc5) | M. cristata | Nomos Serron (Greece) | HFK-HR-51145 |
| M. cristata ssp. cristata (Mc6) | M. cristata | Paikon Mt (Greece) | HFK-HR-51146 |
| M. cristata ssp. kosaninii (McK) | M. kosaninii | Pletvar (N. Macedonia) * | HFK-HR-51142 |
| M. croatica (Mcr1) | M. croatica | Rossijev kuk (Croatia) | HFK-HR-51016 |
| M. croatica (Mcr2) | M. croatica | Stupačinovo (Croatia) * | HFK-HR-51017 |
| M. croatica (Mcr3) | M. croatica | Dubočani (BIH) | HFK-HR-51020 |
| M. croatica (McrP1) | M. pseudocroatica | Pijavičino (Croatia) * | HFK-HR-51032 |
| M. croatica (McrP2) | M. pseudocroatica | Prapratno (Croatia) | HFK-HR-51033 |
| M. graeca ssp. graeca (Mg1) | M. graeca | Malo zlo polje (Croatia) * | HFK-HR-51036 |
| M. graeca ssp. graeca (Mg2) | M. graeca | Komiža (Croatia) | HFK-HR-51037 |
| M. graeca ssp. fruticulosa (MgF) | M. fruticulosa | Sušac Island (Croatia) * | HFK-HR-51038 |
| M. juliana (Mj1) | M. juliana | Grude (BIH) * | HFK-HR-51043 |
| M. juliana (Mj2) | M. juliana | Cijevna Canyon (Montenegro) | HFK-HR-51045 |
| M. juliana (Mj3) | M. juliana | Rajec Reka (N. Macedonia) | HFK-HR-51168 |
| M. juliana (Mj4) | M. juliana | Cholomon Mt (Greece) | HFK-HR-51147 |
| M. kerneri (Mk1) | M. kerneri | Zavratnica (Croatia) * | HFK-HR-51018 |
| M. kerneri (Mk2) | M. kerneri | Mostar (BIH) | HFK-HR-51044 |
| M. longipedunculata (Ml1) | M. parviflora | Jazina (BIH) * | HFK-HR-51046 |
| M. longipedunculata (Ml2) | M. parviflora | Krivošije Mt (Montenegro) | HFK-HR-51047 |
| M. microphylla (Mm) | M. microphylla | Svetac Island (Croatia) * | HFK-HR-51039 |
| C. dalmaticum (Cd) | M. dalmatica | Orjen Mt (Montenegro) * | HFK-HR-51051 |
| C. dalmaticum (CdB1) | M. bulgarica | Mesta River Valley (Bulgaria) * | HFK-HR-51134 |
| C. dalmaticum (CdB2) | M. bulgarica | Vlahina Mt (Bulgaria) | HFK-HR-51135 |
| C. frivaldszkyanum (Cf1) | M. frivaldszkyana | Malusha peak (Bulgaria) * | HFK-HR-51136 |
| C. frivaldszkyanum (Cf2) | M. frivaldszkyana | Vikanata Skala Nature Monument (Bulgaria) | HFK-HR-51137 |
| C. pulegium (Cp) | M. pulegium | Međeđa (BIH) * | HFK-HR-51050 |
| C. serpyllifolium (Cs) | M. albanica | Prizren (Kosovo) * | HFK-HR-51074 |
| C. thymifolium (Ct1) | M. thymifolia | Učka Mt (Croatia) | HFK-HR-51077 |
| C. thymifolium (Ct2) | M. thymifolia | Dokozina plan (Croatia) | HFK-HR-51082 |
| C. thymifolium (Ct3) | M. thymifolia | Šušanj (Croatia) | HFK-HR-51081 |
| C. thymifolium (Ct4) | M. thymifolia | Blidinje (BIH) * | HFK-HR-51042 |
| C. thymifolium (Ct5) | M. thymifolia | Manastir Morača (Montenegro) | HFK-HR-51053 |
Note: BIH = Bosnia and Herzegovina; N. = North; * = site of pollen collecting.
Table 7.
Details on collection data of investigated Micromeria (M.) and Clinopodium (C.) taxa.
| Taxa–According to | Latitude | Longitude | Altitude a.s.l. (m) | |
|---|---|---|---|---|
| Bräuchler et al., 2008 (Code) | Balkan Literature | |||
| M. cristata (Mc1) | M. cristata | 43°22′45.0″ | 21°53′50.1″ | 387 |
| M. cristata (Mc2) | M. cristata | 42°29′33.4″ | 23°11′43.1″ | 980 |
| M. cristata (Mc3) | M. cristata | 41°46′11.4″ | 23°25′19.1″ | 1970 |
| M. cristata (Mc4) | M. cristata | 41°24′18.1″ | 22°15′47.0″ | 111 |
| M. cristata (Mc5) | M. cristata | 41°15′10.3″ | 23°24′49.8″ | 190 |
| M. cristata (Mc6) | M. cristata | 40°57′21.2″ | 22°20′02.0″ | 1650 |
| M. cristata ssp. kosaninii (McK) | M. kosaninii | 41°22′09.0″ | 21°39′06.1″ | 1020 |
| M. croatica (Mcr1) | M. croatica | 44°45′51.1″ | 4°59′17.1″ | 1641 |
| M. croatica (Mcr2) | M. croatica | 44°32′37.5″ | 15°10′04.7″ | 1058 |
| M. croatica (Mcr3) | M. croatica | 43°35′10.1″ | 18°04′44.0″ | 715 |
| M. croatica (McrP1) | M. pseudocroatica | 42°56′58.8″ | 17°22′02.1″ | 436 |
| M. croatica (McrP2) | M. pseudocroatica | 42°49′28.1″ | 17°39′57.9′ | 167 |
| M. graeca (Mg1) | M. graeca | 43°03′43.3′‘ | 16°12′55.9″ | 137 |
| M. graeca (Mg2) | M. graeca | 43°02′17.4″ | 16°05′49.5″ | 43 |
| M. graeca ssp. fruticulosa (MgF) | M. fruticulosa | 43°02′13.4″ | 16°05′50.5″ | 10 |
| M. juliana (Mj1) | M. juliana | 43°23′18.5″ | 17°23′27.8″ | 495 |
| M. juliana (Mj2) | M. juliana | 42°25′44.6″ | 19°28′53.5″ | 157 |
| M. juliana (Mj3) | M. juliana | 41°26′12.2″ | 21°52′06.4″ | 199 |
| M. juliana (Mj4) | M. juliana | 40°27′30.0″ | 23°31′04.6″ | 1100 |
| M. kerneri (Mk1) | M. kerneri | 44°42′02.2″ | 14°54′45.6″ | 161 |
| M. kerneri (Mk2) | M. kerneri | 43°20′27.7″ | 17°48′53.2″ | 61 |
| M. longipedunculata (Ml1) | M. parviflora | 42°42′11.7″ | 18°30′37.1″ | 347 |
| M. longipedunculata (Ml2) | M. parviflora | 42°32′51.8″ | 18°42′41.1″ | 624 |
| M. microphylla (Mm) | M. microphylla | 43°01′07.8″ | 15°45′08.2″ | 28 |
| C. dalmaticum (Cd) | M. dalmatica | 42°33′45.1″ | 18°37′36.6″ | 1074 |
| C. dalmaticum (CdB1) | M. bulgarica | 41°40′46.6″ | 23°43′29.7″ | 580 |
| C. dalmaticum (CdB2) | M. bulgarica | 41°50′30.6″ | 22°59′27.8″ | 1140 |
| C. frivaldszkyanum (Cf1) | M. frivaldszkyana | 42°45′01.0″ | 25°16′53.7′ | 1311 |
| C. frivaldszkyanum (Cf2) | M. frivaldszkyana | 42°45′57.6″ | 25°30′08.1″ | 1040 |
| C. pulegium (Cp) | M. pulegium | 43°44′01.2″ | 19°17′07.3″ | 563 |
| C. serpyllifolium (Cs) | M. albanica | 42°12′01.6″ | 20°45′57.7″ | 376 |
| C. thymifolium (Ct1) | M. thymifolia | 45°17′08.1″ | 14°12′02.4″ | 1189 |
| C. thymifolium (Ct2) | M. thymifolia | 44°39′04.3″ | 15°02′39.1″ | 1441 |
| C. thymifolium (Ct3) | M. thymifolia | 44°31′33.8″ | 15°06′45.1″ | 604 |
| C. thymifolium (Ct4) | M. thymifolia | 43°31′07.8″ | 17°23′09.8″ | 1195 |
| C. thymifolium (Ct5) | M. thymifolia | 42°45′50.9″ | 19°23′34.6″ | 301 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
MDPI and ACS Style
Kremer, D.; Stabentheiner, E.; Bogunić, F.; Ballian, D.; Eleftheriadou, E.; Stešević, D.; Matevski, V.; Ranđelović, V.; Ivanova, D.; Ruščić, M.; et al. Micromorphological Traits of Balcanic Micromeria and Closely Related Clinopodium Species (Lamiaceae). Plants 2021, 10, 1666. https://doi.org/10.3390/plants10081666
AMA Style
Kremer D, Stabentheiner E, Bogunić F, Ballian D, Eleftheriadou E, Stešević D, Matevski V, Ranđelović V, Ivanova D, Ruščić M, et al. Micromorphological Traits of Balcanic Micromeria and Closely Related Clinopodium Species (Lamiaceae). Plants. 2021; 10(8):1666. https://doi.org/10.3390/plants10081666
Chicago/Turabian StyleKremer, Dario, Edith Stabentheiner, Faruk Bogunić, Dalibor Ballian, Eleni Eleftheriadou, Danijela Stešević, Vlado Matevski, Vladimir Ranđelović, Daniella Ivanova, Mirko Ruščić, and et al. 2021. "Micromorphological Traits of Balcanic Micromeria and Closely Related Clinopodium Species (Lamiaceae)" Plants 10, no. 8: 1666. https://doi.org/10.3390/plants10081666
Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.
