Startseite A comparative analysis of dendrometric, macromorphological, and micromorphological characteristics of Pistacia atlantica subsp. atlantica and Pistacia terebinthus in the middle Atlas region of Morocco
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A comparative analysis of dendrometric, macromorphological, and micromorphological characteristics of Pistacia atlantica subsp. atlantica and Pistacia terebinthus in the middle Atlas region of Morocco

  • Mohammed Bassouya EMAIL logo , Mohamed Chedadi , Jawhari Fatima Zahra , Mohammed Kara EMAIL logo , Amine Assouguem , Riaz Ullah , Mohamed A. Ibrahim , Ahmed Bari , Hafize Fidan , Lafraxo Soufyane , Abdellatif Alami und Amina Bari
Veröffentlicht/Copyright: 17. September 2024
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Abstract

The genus Pistacia, with its species having notable ecological, economic, and medicinal implications, demonstrates remarkable environmental adaptability. The central objective of the study is to analyze interspecific variations between Pistacia atlantica subsp. atlantica and Pistacia terebinthus across three distinct bioclimatic zones in the Middle Atlas region of Morocco. The methodology includes collecting dendrometric measurements and conducting macromorphological examinations on these two taxa, with a detailed analysis of 27 qualitative and quantitative variables. A micro-morphological analysis of leaves, using scanning electron microscopy (SEM), is employed to explore specific features such as size and stomatal density, as well as qualitative aspects like epidermal cell shape and trichomes. Dendrometric measurements have revealed that the canopy surface and the number of trunks per tree can serve as distinctive features between the two species. Regarding the sex ratio of Pistacia atlantica subsp. atlantica, 59% of the examined trees are males, primarily associated with the jujube tree in arid zones and the dwarf palm in humid areas. In contrast, female Pistacia terebinthus exhibit a similar percentage, predominantly associated with oak groves and cade juniper in their distribution areas. Principal component analysis of biometric measurements emphasized a significant disparity between the two species, representing 60.25% of the total variance. The use of SEM unveiled new features facilitating the identification of the two species. By leveraging the macromorphological and micromorphological variability of pistachio trees, we can qualify those best suited to diverse bioclimates. In this regard, we suggest incorporating them into reforestation and rehabilitation programs aimed at restoring our declining ecosystems.

Keywords: Pistacia atlantica subsp. atlantica ; Pistacia terebintus ; morphology; stomatal density; scanning electron microscopy

1 Introduction

The Mediterranean flora in general, and the Moroccan flora in particular, is now much better understood than it was 20 years ago. Systematic research, whether of a traditional or modern (molecular) nature, has refined our knowledge of various taxa (families, genera, or species) [1]. Our research delves into the present condition of iconic Moroccan ecosystems, with a specific focus on two members of the Anacardiaceae: PA (Pistacia atlantica subsp. atlantica) and PT (Pistacia terebinthus).

With around ten species of pistachio trees, some of them share similar physical characteristics, posing challenges in accurate identification when observed in their natural habitats. This challenge is particularly evident for the PA and PT, given their morphological resemblances. Overcoming this potential confusion and ensuring precise identification necessitates a comprehensive study of these species [2].

The genus Pistacia comprises ten species characterized by alternate, pinnate-compound leaves [3]. Also, from a taxonomic perspective, establishing the limits of Anacardiaceae has been challenging; that is to say, not long ago, Anacardiaceae and Bursuaceae were grouped under the family Terebinthaceae [4]. According to Zohary [5], PA has been classified into four distinct eco-geographical varieties: cabulica, latifolia, kurdica, and finally, atlantica, originating from the Maghreb region [6], while Álvarez et al. [7] have elevated the first three varieties to the status of subspecies; moreover, other authors considered some of them as separate species [8–11].

However, it is worth noting that the classification proposed by Rechinger [12] was not accepted by Iranian botanists [13]. PA is naturally found from the Mediterranean basin to Central Asia. It is a dominant tree in its natural spaces and plays a significant economic role in these regions. The leaves are imparipinnate with 5–9 lanceolate leaflets, measuring 26–70 mm in length and 8–22 mm in width. The petioles are winged and are extra-axillary, ranging from 7 to 15 cm in length [14].

PT is a shrub or small tree and typically range in height from 2 to 6 m, occasionally reaching up to 12 m. Their deciduous leaves, either impari- or paripinnate, measure between 10 and 19 cm in length and 6–19 cm in width, eventually becoming leathery. Petioles are usually rounded, rarely flattened, and the rachis lacks winged extensions. Leaflets, numbering from 3 to 11, are typically 3.5–8 cm long and 1–3.1 cm wide, with an average ratio of about 2.7:1. They are arranged opposite to subopposite and vary from ovate to narrowly ovate, often with a pointed tip and a fine pubescence or smooth surface. The terminal leaflet, if present, tends to be smaller than the lateral ones, measuring between 1 and 6 cm long and 5 and 20 mm wide. Staminate panicles, reaching up to 8 cm long, feature diffuse branching and large bracts with long white trichomes. Pistillate panicles, up to 15–23 cm long, become more robust in fruit and may have a slightly hairy or smooth surface. Initially reddish, the drupes eventually ripen to a blue color, completing the characteristic features of these plants [15].

PT is native to Eastern Mediterranean countries, where it is commonly found on rocky sites with open vegetation. It avoids the driest and coldest locations [16].

Morphological characterization of a plant represents a critical and significant trait as it encompasses growth and developmental profile while also playing a role in formulating conservation strategies. When distinguishing between taxa or for taxonomy purposes, it is essential to consider the various levels and degrees of intraspecific and interspecific variations [17].

Indeed, these two taxa are characterized by their intraspecific diversity, broad geographic distributions, and therapeutic uses by different ethnic groups in Asia and North Africa [18].

On the other hand, our comparison also encompasses the phytodermic and stomatal characteristics of the two taxa under study to explore potential variations between them. It should be pointed out that the morphology, distribution, and behavior of stomata exhibit responsiveness to a diverse range of signals, ranging from intracellular signaling to global climate changes [19].

Precise identification of the two taxa is essential for establishing a combined strategy for conservation and improvement. Indeed, species identification involves three distinct types of characterization: morphological, biochemical, and molecular. In this study, we specifically focused on the first type, directing our attention to macromorphological and micromorphological characterization, which form the fundamental basis for species classification.

2 Materials and methods

2.1 Sampling area

Trees of PA and PT used in this study were sampled from three regions (Figure 1) located in different bioclimatic zones of the Middle Atlas in Morocco (Table 1). It is important to emphasize that the populations of PA and PT are scattered or isolated. Therefore, we sampled our trees at various locations in the same study area based on the presence of both species. Regarding PT, we noticed that this taxon is distributed in humid areas, with a few isolated individuals found in the early stages of the semi-arid climate, particularly in our Amghas zone. In other words, as aridity increases, PT disappears regardless of altitude.

Figure 1 Map of the study area and sampling stations (ARC-GIS program).
Figure 1

Map of the study area and sampling stations (ARC-GIS program).

Table 1

Summary of the main climatic characteristics of the studied stations [23–25]

Study areas Latitude Longitude Altitude Substrate type Bioclimatic stage
Ait Naamane Pistacia atlantica Desf. 33°41'56.1″N 5°21'23.2″W 1,023 Shallow red soil resting on Lias limestones and dolomites Sub-humid, ranging from cool to cold
Pistacia Terebinthus L. 33°41'50.9″N 5°21'25.1″W 1,020
Lac Afourgagh Pistacia atlantica Desf. 33°36'45.9″N 4°53'02.6″W 1,449 Shallow red soil resting on a carbonate series, typically dolomitic Semi-arid with cool winters
Pistacia Terebinthus L. 33°36'57.7″N 4°52'57.1″W 1,425
Amghas Pistacia atlantica Desf. 33°68'63.9″N 5°37'01.1″W 1,043 Schistose-sandstone and quartzitic deposits Semi-arid with a temperate winter
Pistacia Terebinthus L. 33°37'12.5″N 5°25'45.2″W 1,047

3 Dendrometric characteristics of trees

Due to the uneven distribution of trees, an initial visual count was conducted on each slope of every station. Subsequently, various parameters were assessed, including plant sex, circumference, height, canopy, associated flora, number of trunks, and tree vigor. The selection of trees was made randomly and based on the presence of the two studied taxa. We chose only trees that had reached a flowering stage in order to know the sex of each tree (Table 2).

Table 2

Dendrometric characteristics measured for trees in distinct populations

Circumference PA (cm) Height PA (cm) Surface of canopy PA (cm) Circumference PT (cm) Height PT (cm) Surface of canopy PT (cm)
Amghas 204.5a ± 75.3 (92–335); 36.82 823.4b ± 414.1 (131–1,550); 50.30 3,821c ± 1,298 (1,620–6,468); 33.98 72d ± 23.75 (50–105); 32.98 573.3e ± 65.55 (505–670); 11.43 2,010f** ± 393.2 (16.33–2,575); 19.57
Ait naamane 299.3a ± 113.9 (60–365); 38.07 1399b ± 398.5 (710–1,860); 28.5 3,719c ± 1,068 (2,010–5,401); 28.71 158.5d ± 79.36 (60–340); 50.06 936.9e ± 207.3 (705–1,420); 22.13 3,042f** ± 840.8 (2,010–5,401); 27.64
Afourgagh 258.9a ± 95.16 (102–380); 36.75 1234b ± 486.4 (720–2,270); 39.4 5,483c* ± 1,390 (3,580–7,850); 25.35 191.4d ± 108.2 (70–312); 56.5 1,181e ± 155.5 (955–1,365); 13.16 4,816f*** ± 1,965 (3,203–8,236); 40.8

Letters a–f represent the correlation coefficient of variables measured with the station, according to Tukey’s multiple comparisons test (p < 0.05). Values identified by the same letter show no significant difference. *p < 0.05; **p < 0.01; ***p < 0.001. Mean Avg; Standard deviation: SD; Range: Min-Max; CV: coefficient of variation (%); PA: Atlas pistachio; PT: Terebinth pistachio.

Height was measured using a geometric principle based on the Bucher’s cross, while circumference was measured with a tape measured at 1.30 m from the ground [20].

Although the exact calculation of the crown area is theoretically impossible [21], it can be approximated by utilizing directly measurable values such as the crown height and diameter using the following formula:

S = [ π ( d 1 ⋅ d 2 ) ] / 4 ,

where S represents the crown area at the ground level in square meters, d1 is the ground diameter of the north–south crown, and d2 is the east–west crown diameter at the ground level [22].

Statistical analysis of data: to assess the consistency or disparity of the collected dendrometric parameters, various statistical indicators were utilized. The standard deviation (σ) and coefficient of variation (CV) were calculated among these parameters, providing insights into the dispersion and distribution of individuals around the mean. Furthermore, a two-factor analysis of variance was applied, accompanied by the use of Tukey’s test for both variance analysis and mean comparison.

4 Morphological analysis

4.1 Sampling of the plant material

Due to the scattered distribution of individuals of the studied species, sample collection was carried out subjectively by selecting the most accessible subjects in the field. Consequently, 30 trees were measured in each of the three study stations. Given the deciduous nature of PA, periodic field trips were conducted throughout the year 2022 to collect leaves, inflorescences, and fruits at different stages of development. Morphological characteristics were chosen as the main analysis parameters, as they are frequently used by taxonomists to differentiate between taxa. These characteristics provide crucial information about the variability of adaptations and are essential for a better understanding of natural population differentiation, as indicated in ref. [22].

4.2 Measured parameters

The reference samples for each institution were sorted at the Herbarium of the Dher el Mehrez Faculty of Science, specifically the “LBEAS” laboratory (Figure 2).

Figure 2 Plant material used and certain measurement techniques: (a) Tree of Pistacia terebinthus. L (PT); (b) inflorescence of PT; (c) leaf diameter measurements using a caliper; (d) tree of Pistacia atlantica subsp. atlantica (PA); (e) Herbarium; and (f) dendrometric measurements.
Figure 2

Plant material used and certain measurement techniques: (a) Tree of Pistacia terebinthus. L (PT); (b) inflorescence of PT; (c) leaf diameter measurements using a caliper; (d) tree of Pistacia atlantica subsp. atlantica (PA); (e) Herbarium; and (f) dendrometric measurements.

At each location, a random selection of 20 trees was made. Subsequently, each plant was sampled, including 20 leaves and 20 fruits. The leaves and fruits were naturally dried and stored in the laboratory. Biometric and morphological measurements were conducted following the method described by the descriptors of the pistachio tree [26].

In total, 27 morphological characteristics were measured, consisting of 13 qualitative traits and 14 quantitative traits. The qualitative traits are represented in Table 3, while the quantitative traits are presented in Table 4.

Table 3

Character encoding of qualitative morphological traits

Character Code Value
Size of the terminal leaflet SiTL 1; resembling the basal leaflets 2; greater in size than the basal leaflets3; lesser in size than the basal leaflets
Shape of the terminal leaflet ShTL 1; lanceolate widened 2; elliptical 3; oval 4; round oval 5; rounded 99; other terminal leaflet apex shape
Shape of terminal leaflet apex ShTLa 1; pointed or tapering 2; sharp tip 3;slightly sharp tip 4;rounded 5;Indented 6; other shapes
Shape of terminal leaflet base ShTLb 1; attenuate 2; rounded 3; truncate 4; inclined 99; other
Margin of terminal leaflet MTL 1; flat 2; wavy
Shape of the petiole ShP 1; flattened 2; rounded 3; rounded with a straight upper surface
Leaf color LC 1; light green 2; green 3; deep green
Unduly from the central leaf vein UCLV 1; glabrous 2; sparsely pubescent
Shape of flowering buds ShFB 1; broad oval 2; narrow oval 3; conical
Color of the flowering buds CFB 1; burnished 2; Blonde 3; brown 4; Russet
Abundance of inflorescence AIn 3; sparse 5; moderate 7; dense
Shape of the fruit ShFr 1; round (l/w < 1.5) 2; ovoid (1.5 < l/w < 1.8) 3; elongated (l/w > 1.8) 4; narrowed cordiform 5; cordiform
Apex of the shell AS 1; flattened 2; rounded 3; symmetrical treble
4; asymmetrical treble
Cell shape Csh 1; irregular 2; isodiametric 3; polygonal
Type of stomata Ts 1; anomocytic 2; actinocytic 3; paracytic
Type of trichome Tt 1; Absent 2; glandular 3; uncinate/hooked
Table 4

Characteristics of the quantitative traits measured for the leaves, inflorescences, and fruits of the three populations

Characteristics Avg ± SD; Extent
Ait Naamane «Area: 1» Lac Afourgagh «Area: 2» Amghas «Area: 3»
PA PT PA PT PA PT
Leaf length (cm) 15.81 ± 2.16a (11.8–19.8) 15.27 ± 2.79a (10.8–19.8) 11.15 ± 1.98a (8.3–15.6) 12.05 ± 3.49a (5.5–19) 13.22 ± 2.84a (7.2–17.1) 14.19 ± 3.18a (8.7–19.9)
Leaf width (cm) 11.71 ± 1.54a (9.6–15.4) 12.44 ± 3.06a (7.33–17.71) 8.46 ± 1.78a** (5.4–11) 10.6 ± 2.39 b** (7.1–15.2) 11.79 ± 2.58a*** (6.2–15.3) 11.81 ± 1.91 b*** (8.9–15.9)
Number of leaflets 10.95 ± 2.04a*** (6–13) 8.5 ± 1.43b*** (6–11) 8.15 ± 2.13a (4–11) 8.75 ± 1.95a (5–12) 6.6 ± 1.60a (3–9) 7.15 ± 1.79a (3–11)
Length of the terminal leaflet (cm) 4.35 ± 2.02a (0–6.7) 4.57 ± 2.08a (0–8.09) 3.16 ± 1.50a (0–4.5) 3.45 ± 1.21a (1.1–6) 4.23 ± 2.49a (0–7.4) 3.39 ± 2.53a (0–8.5)
Width of the terminal leaflet (cm) 0.935 ± 0.45a*** (0–1.4) 1.69 ± 0.83b*** (0–3.07) 1.07 ± 0.50a** (0–1.5) 1.69 ± 0.63b** (0.5–2.9) 1.38 ± 0.80a (0–2.3) 1.75 ± 1.29a (0–4.5)
Length/width ratio 4.109 ± 2.09a** (0–8) 2.52 ± 1.0b** (0–3.92) 2.52 ± 1.14a (0–3.5) 2.09 ± 0.37a (1.5–3.0) 2.49 ± 1.34a* (0–3.82) 1.55 ± 1.08b* (0–3.25)
Fruit length (mm) 7.99 ± 0.89a*** (6.2–9.6) 4.34 ± 0.42b*** (3.8–5.2) 7.68 ± 1.06a*** (5.9–9.2) 6.04 ± 0.55b*** (4.9–7.2) 7.9 ± 0.62a*** (6.4–9) 6.64 ± 0.35b*** (5.8–7.2)
Fruit width (mm) 5.63 ± 0.88a*** (4.1–6.8) 3.32 ± 0.25b*** (3–3.9) 6.04 ± 0.8a*** (4.8–7.8) 4.9 ± 0.66b*** (3.4–6.1) 6.05 ± 0.66a* (5.2–7.9) 5.67 ± 0.37b* (5.1–6.4)
Fruit thickness (mm) 5.545 ± 0.84a*** (4.1–6.7) 2.12 ± 2.89b*** (1.5–2.7) 5.90 ± 0.86a*** (5–7.6) 4.84 ± 0.60b*** (3.7–6) 4.33 ± 0.39a*** (3.7–5.2) 5.41 ± 0.40b*** (5–6.4)
Inflorescence rachis length (cm) 4.79 ± 1.93a*** (1.3–7.6) 8.83 ± 0.1b*** (6.8–10.8) 10.90 ± 1.21a*** (9–14.2) 13.26 ± 2.59b*** (8.7–17.2) 12.4 ± 2.06a* (8.5–15.8) 14.64 ± 4.32b* (7.5–23.1)
Number of primary lateral inflorescence 15.1 ± 0.45a (14–16) 16.65 ± 3.91a (7–24) 16.20 ± 2.75a*** (12–21) 12.3 ± 2.83b*** (7–18) 15.6 ± 3.05a (10–21) 14.2 ± 3.40a (8–20)
Almonds length (mm) 5.3 ± 0.3a (4.8–5.8) 5.453 ± 0.60a (4.2–6.7) 5.36 ± 0.27a*** (4.9–.5.8) 4.43 ± 0.76b*** (2.9–5.5) 5.19 ± 0.39a (4.2–5.8) 5.03 ± 0.35a (4.4–5.8)
Almonds width (mm) 5.0 ± 0.32a (4–5.3) 4.94 ± 0.52a (4.3–6.2) 5.06 ± 0.40a (4.1–5.8) 4.04 ± 0.98b*** (1.8–5.2) 4.33 ± 0.37a (3.5–5) 4.29 ± 0.30a (3.8–4.8)
Almonds thickness (mm) 4.88 ± 0.34a (4–5.3) 4.97 ± 0.45a (4.4–6.2) 4.13 ± 0.31a (3.4–4.6) 4 ± 0.91a (1.9–5.1) 3.89 ± 0.22a* (3.4–4.2) 3.66 ± 0.31b* (3.1–4.1)

Mean: Avg; Standard deviation: SD; Range: Min–Max; values marked with the same letters (a;b) are not significantly different. *p < 0.05; **p < 0.01; ***p < 0.001.

5 Micromorphological characteristics of leaflets

5.1 Observations under a photon microscope

For optical microscopy, observations were conducted on epidermal impressions obtained using the epidermal sampling method. The technique involves applying a sufficiently thick layer of transparent nail polish to both sides of a fresh leaf. Once the nail polish has completely dried in ambient air, the peel of the nail polish, reproducing the topography of the leaf, is gently removed with tweezers and spread onto a slide previously moistened with a drop of water. Observations were made at magnifications of ×10 and ×40. The slides are stored in the Laboratory of Biotechnology, Environment, Agriculture, and Health at Sidi Mohamed Ben Abdellah University.

5.2 Scanning electron microscopy (SEM) observations

The sample preparation method for SEM observation depends on the information sought, including the topography, microstructure, nature of the sample, and its presentation form, such as biological samples or powders [27].

The epidermal surfaces of the leaves were examined using a scanning electron microscope. Three specimens were taken from each site, each comprising a 5 mm2 section of the dry leaf surface (abaxial and adaxial surfaces). SEM images were digitally recorded at various levels of magnification with a JSM-IT500HR at the Regional University Interface Center (CURI) of Sidi Mohamed Ben Abdellah University in Fès. Observations and measurements focused on ten qualitative and quantitative characteristics of trichomes and stomata. Qualitative features included the shape of the epidermal cells, stomatal shape, stomatal complex type, and trichome type. Quantitative features encompassed stomatal density on the upper and lower surfaces, as well as the length and width of stomata.

6 Results

6.1 Dendrometric characteristics

6.1.1 Quantitative measurements

Comparison of the conformation of samples from PA and PT trees. Sixty trees were studied in three selected zones, with 20 trees per zone.

According to our dendrometric measurements summarized in Table 3, a significant phenotypic difference was observed in the field between PA and PT, specifically in terms of canopy surface and the number of trunks per tree. For each species, there was no significant difference in the tree height and circumference between the three zones. Indeed, the results for height, circumference, and canopy surface were consistently higher (1,399 cm, 299.3 cm, 5,483 cm2) for PA than for PT in all three zones.

For PA, 59% of the examined trees were male, and the identical percentage was noted for female trees of PT (Figure 3). It is crucial to underscore that no instances of hermaphroditism were detected in any of the populations under study.

Figure 3 Number of male and female individuals in the three zones; PA: Pistacia atlantica Desf and PT: Pistacia terebinthus.
Figure 3

Number of male and female individuals in the three zones; PA: Pistacia atlantica Desf and PT: Pistacia terebinthus.

6.2 Qualitative measurements

As regards the tree trunks of the two taxa studied, we found that PA trees are mainly individualized, with rare cases of two trunks (Figure 4).

Figure 4 PA1: individualized trunk in PA; PT1: branching trunk in PT; PA2: ripe fruits of PA; and PT2: ripe fruits of PT.
Figure 4

PA1: individualized trunk in PA; PT1: branching trunk in PT; PA2: ripe fruits of PA; and PT2: ripe fruits of PT.

With regard to the vegetation associated with PA, the analysis highlights the presence mainly of Ziziphus lotus L. (Family: Rhamnaceae) at Amghas, as well as Chamaerops humilis L. (Arecaceae) and Quercus ilex L. (Fagaceae) at Afourgagh and Ait Naamane. PT, on the other hand, is mainly accompanied by Quercus ilex L. (Fagaceae), Pistacia lentiscus L. (Anacardiaceae), and Juniperus oxycedrus L. (Cupressaceae) in the three zones studied.

Regarding tree vigor, 50% of the trees of both species showed low vigor, while only 20% of the specimens represented vigorous trees (Figure 5). In terms of trunk, all measured PT trees have branching (not-individualized) trunks, ranging from 2 to 7 stems in some cases.

Figure 5 Number of plants according to vigor.
Figure 5

Number of plants according to vigor.

7 Morphological traits of leaves, inflorescence, and fruits

7.1 Inter-species variability

The leaves of PA observed in different locations showed an average length of 13.39 ± 2.32 cm, varying from a minimum of 7.2 ± 2.84 cm to a maximum of 19.8 ± 2.16 cm. Leaf width was between 5.4 ± 1.78 cm and 15.4 ± 1.54 cm, with an average width of 10.65 ± 1.96 cm.

For leaves of PT, length ranged from 5.5 ± 3.49 cm to 19.9 ± 3.18 cm, with an average length of 13.83 ± 3.15 cm. The calculated width had an average variation of 11.61 ± 2.45 cm, ranging from a minimum of 7.1 ± 2.39 cm to a maximum of 17.71 ± 3.06 cm (Table 4).

With regard to leaf morphology, both species are mainly characterized by an odd-pinnate arrangement of their leaflets. In the case of PA, the average number of leaflets was 8.56 ± 1.92. The most frequently observed number of leaflets was 7, representing 21.6% of the cases. In contrast, PT had an average of 8.13 ± 1.72 leaflets per leaf. The number of leaflets most frequently encountered was 7, with a frequency of 31.6% (Figure 6).

Figure 6 Frequencies of the number of terminal leaflets.
Figure 6

Frequencies of the number of terminal leaflets.

The comparison of the ratios between the length and width of the terminal leaflet in the PA and the PT within three distinct stations reveals significant differences. The average length/width ratio for PA was 3.03 + 1.32, which was significantly higher than that of the PT estimated to be 2.05 + 0.82. The analysis of the dimensions of the fruits (Figure 4) reveals a marked distinction between PA and PT. The seeds of PA had higher values, with an average of 7.99 ± 0.89 for the length, while width and thickness were 6.05 ± 0.66 and 5.90 ± 0.86, respectively. For PT, the average width, length, and thickness were 6.64 ± 0.35, 5.67 ± 0.37, and 5.41 ± 0.40, respectively (Figure 7).

Figure 7 Fruit size measurements.
Figure 7

Fruit size measurements.

The length, width, and thickness of the almond of PA generally were greater than those of PT. The analysis of the dimensions of the almonds reveals a marked distinction between the two species examined. For PA, the length, width, and thickness of the almond were 5.283 ± 0.96, 4.79 ± 0.363, and 4.3 ± 0.29, respectively; and for PT, they were 4.996 ± 0.57, 4.42 ± 0.6, and 4.2 ± 0.556, respectively (Figure 8).

Figure 8 Almond size measurements.
Figure 8

Almond size measurements.

Morphometric analysis also revealed a significant difference in the length of the inflorescence rachis between the PT and PA. Indeed, the length of the rachis of the inflorescence is greater in PT than in PA. Also, PA has a higher number of primary lateral inflorescential branches compared to PT (Table 4).

8 Inter-population variability

8.1 Principal component analysis (PCA)

The 14 quantitative morphological characters of specimens from various populations of PA and PT were subjected to PCA. The main emphasis of the interpretation of the results was placed on the first two axes, namely axis 1 and axis 2. The information provided by these two selected axes represents 60.25% of the total variance (Figure 9). To identify the variables responsible for the variations along the selected axes, we used the correlation between the variables and the factors (Table 5). Only the first two factors (axes) present variables with factor weights ≥0.6. It is obvious that most of the measured variables are strongly negatively correlated with axis 1 and axis 2. However, the width of the terminal leaflet is negatively correlated with axis 2, while the length of the inflorescence rachis is positively correlated with axis 2. On the other hand, the parameters of the fruits are strongly correlated with axis 1. It is clearly observable that the populations of PA and PT are distinguishable, which indicates morphological differences in the characteristics of the leaves, flowers, and fruits. The traits (variables) responsible for this distinction are those that have high correlations with the axes concerned (≥0.6).

Figure 9 Correlation circle and individual projection onto factors 1 and 2.
Figure 9

Correlation circle and individual projection onto factors 1 and 2.

Table 5

Correlations between variables and factors: correlations ≥ 0.6 are in bold

F1 F2 F3 F4 F5
Leaf length −0.484 −0.608 −0.507 −0.361 −0.091
Leaf width −0.706 −0.170 −0.394 −0.448 −0.341
Number of leaflets 0.025 −0.834 0.264 −0.270 0.400
Length of the terminal leaflet −0.639 −0.221 0.609 −0.371 −0.186
Width of the terminal leaflet −0.736 0.654 −0.085 −0.072 0.138
Length/width ratio 0.112 −0.733 0.574 −0.345 0.010
Fruit length 0.905 −0.098 −0.042 −0.278 −0.303
Fruit width 0.915 0.211 −0.109 −0.260 −0.198
Fruit thickness 0.888 0.108 −0.009 −0.335 0.297
Inflorescence rachis length −0.017 0.999 −0.030 −0.007 0.027
Number of primary lateral inflorescence −0.334 0.011 0.859 0.383 0.060
Almond length 0.019 −0.557 −0.540 0.576 −0.256
Almond width 0.192 −0.770 −0.222 0.557 0.105
Almond thickness −0.263 −0.030 −0.825 −0.233 0.442

9 Inter-specific variability of qualitative morphological parameters

9.1 Leaf parameters

The size of the terminal leaflet exhibits significant variations. In PA, 73.3% of the terminal leaflets resemble those of basal leaflets, whereas in PT, this proportion is 48.3%. Furthermore, 73.3% of the terminal leaflets in PA have an elongated lanceolate form, whereas in PT, it is 71.67% and they have an oval rounded shape. Concerning the apex of the leaflets, 83.3% of the acuminated forms are observed in PA, while 56.66% of the mucronulate forms are noted in PT (Table 6).

Table 6

Frequencies (%) for qualitative traits measured in different populations of Pistacia atlantica Desf and Pistacia terebinthus L.

Provenance species Amghas Afourgagh Ait Naamane
Pistacia atlantica Desf Pistacia terebinthus L. Pistacia atlantica Desf Pistacia terebinthus L. Pistacia atlantica Desf Pistacia terebinthus L.
Size of the terminal leaflet (STL) 0 0 0 15 0 20 25
1 100 0 60 75 60 10
2 0 15 25 25 10 5
3 0 85 0 0 10 60
Shape of the terminal leaflet (ShTL) 0 0 0 15 0 20 25
1 100 0 75 0 45 10
2 0 0 10 0 30 15
4 0 80 0 85 0 50
5 0 20 0 15 0 0
Shape of the terminal leaflet apex (ShTLa) 0 0 0 15 0 20 25
1 100 25 70 25 80 25
2 0 0 15 0 0 5
3 0 75 0 75 0 20
4 0 0 0 0 0 30
Shape of the terminal leaflet base (ShTLb) 0 0 0 15 0 20 25
1 100 0 85 85 80 75
2 0 0 0 15 0 0
3 0 0 0 0 0 0
4 0 100 0 0 0 0
Margin of the terminal leaflet (MTL) 0 0 0 15 0 20 25
1 100 100 85 100 70 75
2 0 0 0 0 10 0
Shape of the petiole (ShP) 0 0 0 15 0 0 0
1 0 100 0 80 15 100
2 20 0 10 0 40 0
3 80 0 75 20 45 0
Leaf color (LC) 0 0 0 15 0 0 0
1 5 5 0 0 5 15
2 70 95 25 10 75 85
3 25 0 70 90 20 0
Unduly from the central leaf vein (UCLV) 1 100 100 100 80 100 100
2 0 0 0 20 0 0
Shape of the flowering buds (ShFB) 1 0 85 10 85 100 100
2 100 15 90 15 0 0
Color of the flowering buds (CFB) 1 100 60 25 100 65 100
2 0 40 0 0 0 0
4 0 0 75 0 35 0
Abundance of inflorescence (AIn) 3 0 0 0 85 15 55
5 100 30 85 15 55 45
7 0 70 15 0 30 0
Shape of the fruit (ShFr) 1 100 100 100 85 100 15
2 0 0 0 15 0 85
Apex of the shell (AS) 1 0 100 65 10 10 85
2 100 0 35 90 90 15

Also, the shape of the basal leaflets differs between the two species. In PA, 88.3% of the basal leaflets are attenuated, whereas in PT, this proportion is 53.3%, with 33% adopting an oblique form. Regarding the edge of terminal leaflets, it is flat in PA (85%) and PT (91.66%).

The petiole exhibits differences. In PA, the petiole is rounded and straight on the upper surface (66.6%), while in PT, it is flattened (93.3%). The leaf color varies, being green and dark green in PA (48 and 38.3%, respectively) and similarly in PT (60 and 30%, respectively). However, the color difference was observed in November, the time when the leaves are about to fall. Young leaves of PA are pale when young, while those of PT are reddish. The central leaf veins are glabrous at 100% for both species (Table 6).

9.2 Flower and fruit parameters

In PA, the flower buds have a narrowed oval form, while in PT, 90% have an enlarged oval shape. The flower color is reddish-brown in 63.3% of PA and 86.66% of PT. Inflorescence abundance varies, with 80% moderately abundant inflorescences in PA and 46.67% sparsely abundant in PT. The fruit shape of both species is round (l/w < 1.5) at 100% for PA and 66.67% for PT. The apex of fruits is rounded in PA (75%) and flattened in PT (65%) (Table 6).

10 Comparative analysis of micromorphological characters

10.1 Quantitative characteristics measured for stomata

According to Table 7, it is observed that stomatal density values in PA range from 150 to 440 stomata per mm² on the abaxial side, with an average of 280.03 stomata per mm². Conversely, on the adaxial side of the leaf, where the number of stomata is lower, the variation ranges between 5 and 85 stomata per mm², with an average of 28.03 stomata per mm².

Table 7

Stomatal density in different study areas

Characteristics Stomatal density of PA on the abaxial side Stomatal density of PA on the adaxial side Stomatal density of PT on the abaxial side Stomatal density of PT on the adaxial
Afourgagh 265.6ac** ± 43.76; 215–340 (16.48) 19.22ac*** ± 12.25; 5–41 (63.7) 290.6ad*** ± 20.22; 265–315 (6.96) 42.89a*** ± 20.23; 17–74 (47.16)
Amghas 221.8b** ± 43.64; 150–275 (19.68) 8.222b*** ± 3.42; 5–15 (41.59) 186.4be*** ± 25.75; 144–214 (13.81) 84.78bc ± 15.03; 60–102 (17.73)
Ait Naamane 358.7bd ± 51.85; 285–440 (14.46) 56.67bd ± 20.62; 20–85 (36.38) 409.2cf*** ± 48.24; 340–480 (11.79) 121.4ac ± 32.61; 74–165 (26.85)

Mean: Avg; Standard deviation: SD; Range: Min–Max; CV: coefficient of variation (%); values marked with the same letters are not significantly different. *p < 0.05; **p < 0.01; ***p < 0.001.

For PT, stomatal density values vary between 144 and 480 stomata per mm² on the abaxial side, with an average of 295.4 stomata per mm². On the adaxial side of the leaf, the number of stomata varies between 17 and 165 stomata per mm², with an average of 83.02 stomata per mm². It is noteworthy that stomatal density also varies based on the origin of the leaves of the two species, with the highest recorded values in Ait Naamane, followed by Afourgagh, and finally, Amghas.

The measurements of the stomatal size on the adaxial and abaxial sides of the leaves of PA and PT revealed significant variations. In the Afourgagh area, the stomata for PT had an average length of 27.56 µm on the abaxial side and 22.34 µm on the adaxial side. The average width was 19.43 µm on the abaxial side and 10.48 µm on the adaxial side. In Amghas, the stomata of PA has an average length of 22.06 µm on the abaxial side and 18.94 µm on the adaxial side, with average widths of 8.607 and 8.863 µm, respectively. Ait Naamane PA had smaller stomata, with an average length of 14.47 µm on the abaxial side and 12.68 µm on the adaxial side. The average widths were 9.584 and 8.724 µm, respectively.

For PT, in Afrougagh, the average length of the stomata was 16.86 µm on the abaxial side and 21.46 µm on the adaxial side. The average widths were 8.343 and 12.32 µm, respectively, in Amghas, the stomata of PT had an average length of 10.53 µm on the abaxial side and 9.184 µm on the adaxial side, with average widths of 7.942 and 7.634 µm, respectively.

Ait Naamane PT had stomata with an average length of 11.77 µm on the abaxial side and 11 µm on the adaxial side, with average widths of 7.52 and 7.64 µm, respectively. These results highlight the variability in the stomatal size between different zones and the two Pistacia species studied (Table 8).

Table 8

Size of stomata in the abaxial and adaxial sides

Ait Naamane Afourgagh Amghas
Pistacia atlantica Desf Length of stomata on Abaxial side (µm) 21.31a** ± 3.14;17. 4–26.35 (14.74) 27.33b** ± 3.73; 20.66–34.14 (13.65) 21.11ad** ± 5.12; 13.1–28.71 (24.25)
Adaxial face (µm) 22.24a ± 2.85; 18.56–27 (12.81) 23.08a ± 4.45; 16.6–2976 (19.27) 19.05a ± 5.4; 10.2–2.47 (28.36)
Width of stomata on Abaxial side (µm) 11.66a*** ± 3.77; 5.89–16.4 (32.36) 19.71bc*** ± 2.64; 15.21–24.55 (13.38) 9.011ad ± 5.22; 2–19.1 (57.89)
Adaxial face (µm) 11.37a ± 2.02; 9.56–15.52 (17.72) 11.21a ± 3.59; 7.02–17.8 (32.04) 8.89a ± 3.66; 5.17–12.41 (26.6)
Pistacia terebinthus L. Length of stomata on Abaxial side (µm) 15.87ac*** ± 2.88; 11.66–19.15 (18.16) 15.9ad ± 2.92; 10.49–20.66 (18.36) 23.82be*** ± 2.76; 17.85–28.33 (11.59)
Adaxial face (µm) 26.42a* ± 3.1; 20.8–30.74 (11.74) 21.81b* ± 4.04; 16.84–29.52 (18.54) 25.06a ± 2.71; 20.7–29.09 (10.8)
Width of stomata on Abaxial side (µm) 7.12a ± 1.66; 4.7–9.26 (23.33) 8.15ab*** ± 2.57; 4.18–12.47 (31.56) 17.4ac*** ± 2.22; 14.94–21.34 (12.79)
Adaxial face (µm) 16.5a* ± 3.63; 12.23–22.66 (22.02) 12.62b ± 2.32; 8.77–16.62 (18.37) 12.85b ± 2.72; 9.46–17.72 (21.2)

Mean: Avg; Standard deviation: SD; Range: Min–Max; CV: coefficient of variation (%); values marked with the same letter are not significantly different. *p < 0.05; **p < 0.01; ***p < 0.001.

10.2 Types of trichomes

Figure 9 shows the two main types of trichomes observed in all examined leaves, namely glandular and uncinate. Trichomes are primarily present either on the abaxial or adaxial surfaces, with some cases showing the presence on both surfaces, while in other cases, they are absent. In the present study, trichomes were found on both surfaces of PA leaves in the three study zones: Amghas, Afourgagh, and Ait Naamane. Meanwhile, in PT, trichomes were absent in all samples tested from the three leaf sources. Qualitative results regarding trichomes are presented in Table 9.

Table 9

Qualitative variables measured for stomata and trichomes

Provenance species Amghas Afourgagh Ait Naamane
Pistacia atlantica Desf Pistacia terebinthus L. Pistacia atlantica Desf Pistacia terebinthus L. Pistacia atlantica Desf Pistacia terebinthus L.
Cell shape 1 100 100 100 90 100 100
2 0 0 0 0 0 0
3 0 0 0 10 0 0
Type of stomata 1 90 90 70 100 80 100
2 0 10 20 0 0 0
3 10 0 10 0 20 0
Type of trichome 1 20 100 0 100 30 100
2 70 0 20 0 20 0
3 10 0 80 0 50 0

Three distinct categories of stomata have been identified in all examined leaves, including anomocytic, paracytic, and actinocytic stomata. More than 90% of the leaves exhibited anomocytic stomata, and sometimes a single epidermis had two or more types of stomata (Figure 10). Additionally, in both species, stomata are primarily located on the abaxial surface of the leaves, although they are occasionally present on both surfaces (Table 9).

Figure 10 (a) Stomata on the abaxial surface of PA; (b) stomata of the abaxial surface of PT; (c) micrographs of stomata on the abaxial surface of PA; (d) micrographs of stomata on the adaxial surface of PA; (e) size of stomata on the abaxial surface of PA; (f) size of stomata on the adaxial surface of PA; (g) micrographs of stomata on the abaxial surface of PT; (h) Micrographs of stomata of the adaxial surface of PT; (i) size of stomata on the abaxial surface of PT. (j) size of stomata on the adaxial surface of PT. (k) form of the epidermis of PA; (l) main leaf veins of PA; and (m) and (n): ciliated and glandular trichomes of PA.
Figure 10 (a) Stomata on the abaxial surface of PA; (b) stomata of the abaxial surface of PT; (c) micrographs of stomata on the abaxial surface of PA; (d) micrographs of stomata on the adaxial surface of PA; (e) size of stomata on the abaxial surface of PA; (f) size of stomata on the adaxial surface of PA; (g) micrographs of stomata on the abaxial surface of PT; (h) Micrographs of stomata of the adaxial surface of PT; (i) size of stomata on the abaxial surface of PT. (j) size of stomata on the adaxial surface of PT. (k) form of the epidermis of PA; (l) main leaf veins of PA; and (m) and (n): ciliated and glandular trichomes of PA.
Figure 10

(a) Stomata on the abaxial surface of PA; (b) stomata of the abaxial surface of PT; (c) micrographs of stomata on the abaxial surface of PA; (d) micrographs of stomata on the adaxial surface of PA; (e) size of stomata on the abaxial surface of PA; (f) size of stomata on the adaxial surface of PA; (g) micrographs of stomata on the abaxial surface of PT; (h) Micrographs of stomata of the adaxial surface of PT; (i) size of stomata on the abaxial surface of PT. (j) size of stomata on the adaxial surface of PT. (k) form of the epidermis of PA; (l) main leaf veins of PA; and (m) and (n): ciliated and glandular trichomes of PA.

11 Discussion

11.1 Dendrometric characteristics

In this study, most dendrometric parameters of the pistachio tree are not influenced by different zones, and the same observations were made concerning acacia and were endorsed by studies conducted by Fonton et al. [28]. However, statistical analysis revealed two discriminant features for identifying PA and PT. First, the canopy of PA covers a larger area than that of PT in the three study zones. El Zerey-Belaskri et al. [29] showed that PA trees are characterized by dense foliage compared to other species of the Pistacia, confirming our findings regarding the canopy area. Second, the PT tree has a multi-trunk arboreal stem starting at less than 50 cm from the ground. On the other hand, the PA tree has a well-individualized stem, whether for young shoots or older subjects. This observation was confirmed by Quezel and Santa [30]. The trunk of the PA tree is primarily singular, although in rare cases, it may branch out from the base. On the other hand, similar studies conducted in the literature [2,30] showed that PA trees are robust and vigorous, reaching heights of 15–20 m; however, intermediate trees are also observed. The trunks of adult trees can exceed 1 m in diameter and 6 ms in circumference, with a striated dark gray bark.

Our dendrometric results are partially inconsistent with those of Aloui [31]. He showed that the climatic effect is significant on the tree circumference and canopy diameter but is not a significant factor in tree height.

Regarding the sex ratio, our results align with the study of Mabberley [32]. Flowers are generally unisexual in Anacardiaceae, and the genus Pistacia is distinguished by its dioecious reproductive system. Some exceptional cases of sexual types have been reported in the literature; Ozbek and Ayfer [33] observed two hermaphrodite trees in Turkey.

11.2 Morphological traits of leaves, inflorescence, and fruits

Among the distinctive features, several are used in the classification of species in the Pistacia genus, including the size of the terminal leaflet, the number of pairs of leaflets, the shape of the apex of the terminal leaflet, the presence of leaflet wings on the rachis, and finally, the shape of the fruit [5,8].

The description provided in previous studies [5,8,13,34] suggests that the leaves of P. atlantica possess leaflets with finely winged rachis [35]. The rachis is broadly winged, with wings extending along its entire length [13]. Regarding the terminal leaflet, it is stated to be as large as the basal leaflets [34]. In our study, the size of the terminal leaflet varies, and the shape of the apex can be acute or acuminate, contrary to the obtuse shape reported by Zohary [5].

Regarding our observations on inflorescences, the parameters we studied did not uncover any distinctive characteristics. However, during the sampling process, we noticed that some male PA produced flower buds starting in January. Based on our sample set and the studies conducted by Yaaqobi et al. [36] on the flowering and germination of PA seeds, we considered these cases to be exceptional occurrences. On the other hand, flowering is early in trees PA and late in PT and this phenomenon is more pronounced in areas where aridity decreases. It is also crucial to emphasize that flowering occurs before vegetative development, with a tendency for males to flower before females. This observation aligns with Delph [37], demonstrating that males invest more resources in flowering early in the season before leaf production. Thus, resources allocated to the development of vegetative growth, including photosynthetic tissues (leaves), may be limited or unstable [38].

On the other hand, in the mountains of the Bulgarian Rhodopes, some monoecious plants of PT were found [39]. Some trees were entirely monoecious, while others had only staminate flowers or bore only pistillate inflorescences. To assess the stability of the monoecious type, a study was conducted to investigate the morpho-anatomical development of floral buds and the floral biology of the aforementioned genotypes of PT. The study of monoecious plants of PT in the Mediterranean region is important for the opportunity it provides to increase the biodiversity of agroforestry systems, for rootstock platforms, and for obtaining new interspecific hybrids as potential rootstocks [40].

The statistical analyses indicate significant variations both in terms of size and shape of the seeds between the two species in the three stations studied. This observation has been validated within the subspecies of the PA. Indeed, Behboodi [13] described the leaves and fruits of the PA tree found in Iran. The drupes are slightly broader than long in P. atlantica subsp. mutica; they are globular, with equal length and width in P. atlantica subsp. cabulica; and they are depressed globular, measuring 5–8 mm × 8–10 mm in P. atlantica subsp. kurdica. Previous studies conducted on the fruits partially align with our findings. Indeed, the fruit is a syncarpous drupe, morphologically variable, characterized by a thin and oleaginous exocarp [5,6,29]. It is small in size (≤0.8/0.7 cm) [29], with large and oval drupes that turn from red to dark green when mature (August to September). Its single seed is oval and yellow. Previous results report an average of 37 fruits per infructescence in adult individuals [41].

The measurements taken on the size of the fruits and almonds of PT and PA trees reveal a significant issue of empty seed formation, estimated to be 77%. This result has been explained in previous studies [42,43]; the authors suggest that the production of fruits with non-viable seeds can be triggered by specific conditions affecting a plant during the pollination period or during the process of fertilization and early fruit growth [44].

12 Micromorphological characteristics

Stomata represent the primary mechanism by which higher plants adapt to their constantly changing environment [45]. Homeostasis, a fundamental biological property of living organisms, requires the regulation of the internal environment while interacting with the surroundings [46]. Adaptive homeostatic ranges are significantly broader in plants than in animals [47], but the overall conservation of homeostasis remains equally crucial in both kingdoms.

The results obtained from measurements of qualitative and quantitative characteristics of stomata and trichomes agree with some studies but differ from others. Statistical analyses reveal significant differences for the measured variables among the studied species. According to the statistical results, the most discriminating stomatal characteristics recorded during this study are size and stomatal density.

Examining the data, the density is higher in the abaxial epidermis, and it appears that increased aridity is associated with a decrease in the number of stomata. This trend is observed on both the adaxial and abaxial surfaces, and similar results were reported by Gindel [48] in studies conducted in Israel. PT exhibits a higher stomatal density than PA. Additionally, PT develops stomata of smaller size than PA. The few stomata on the adaxial surface are primarily located near the main and secondary veins of the leaflet. These observations support the earlier findings of Doghbage et al. [49].

Our conclusions are inconsistent with the phytodermological study of Pistacia atlantica subsp. atlantica and Pistacia lentiscus conducted by Smail-Saadoun [50]. This study demonstrated that the adaptation of these two species to water scarcity involves a complete absence of stomata on the upper surface of the leaves and the presence of paracytic mesoperigenous stomata on the lower surface of the leaf.

About 90% of the samples exhibit anomocytic forms, and in rare cases, actinocytic and paracytic stomata are observed in both species (Figure 10a and b). Most epidermal cells have an irregular shape, except for 10% of the cells in PT from the Afourgagh area, which have a polygonal shape. Furthermore, the guard cells were not aligned at the same level as the adjacent epidermal cells, and the subsidiary cells did not clearly surround the guard cells. Our results are in agreement with those of Al-Saghir et al. [51] and contradict the findings of the study conducted by Lin et al. [3], which reported that all pistachio species (P. atlantica, P. exicana, P. chinensis, P. integrrima, P. khinjuk, P. texana, P. vera, and P. weinmannifolia) had actinocytic stomata.

According to Al-Saghir [52], amphistomy is considered the primitive characteristic in Pistacia species, with occurrence on a single surface (hypostomy or epistomy) seen as an evolution. P. vera is identified as the most primitive species, while P. terebinthus is considered more recent. In our study, PA exhibits almost the same stomatal density on the abaxial surface compared to PT in Afourgagh and Amghas, but it is lower on the adaxial surface, where stomata are localized along the main and secondary veins in all three studied zones. The researchers [10] suggest that stomatal loss in Pistacia species could be an adaptation to climate changes. This adaptation is also supported by morphological features, as more evolved species have smaller elongated leaflets with pointed tips, facilitating water drainage from the leaves.

The outcome of Simon [53] considered that the regulation of evaporation at the stomatal level can occur either through their sunken position or by the presence of thick edges that protect the pore [53]. Mucilage deposited on stomatal pores could also contribute to reducing evaporation. Wax deposits would serve a similar function, especially in species with low hair coverage.

The information regarding the presence or absence of trichomes on Pistacia leaves is contradictory. Al-Saghir et al. [51] reported the presence of trichomes in all Pistacia species, while other authors indicated that Pistacia leaves are devoid of hairs [3]. The results of the present study reveal the absence of trichomes on the leaflets of PT. Many immature leaves lose their trichomes as the leaf blade opens and expands [54] showed that trichomes produce essential oils that appear to play a protective role against herbivores and pathogens.

13 Conclusions

This study has unveiled crucial aspects for the identification of two species within the Pistacia genus, examining dendrometric, macromorphological, and micromorphological characteristics. Parameters such as canopy surface and trunk count have been identified as distinctive indicators between these two species. Additionally, features including leaf and terminal leaflet dimensions, as well as the size and shape of the terminal leaflet, fruit and almond size, stomatal size and density, and the shape of epidermal stomata and trichomes, were recognized as the most discriminating. Given the broad distribution of these species in North Africa, particularly PA subjected to diverse climatic conditions, it is crucial to conserve these resources and utilize them optimally. This holds particular significance within the context of research and development projects, especially those aimed at restoring heavily degraded forest environments in the Middle Atlas region of Morocco. Furthermore, the potential presence of genetic variability underscores the need to delve deeper into research in this area, considering the comparison of populations from different geographical regions through the use of molecular markers.

Acknowledgments

The authors extend their appreciation to the Researchers Supporting Project (RSP2024R171), King Saud University, Riyadh, Saudi Arabia for financial support.

  1. Funding information: The authors extend their appreciation to the Researchers Supporting Project (RSP2024R171), King Saud University, Riyadh, Saudi Arabia for financial support.

  2. Author contributions: M.B., M.C., J.F.Z., and Am.B. – conceptualization; M.B., M.C., A.Al ., and J.F.Z.– formal analysis; M.B., M.K., A.As., and J.F.Z. – investigation; M.B., M.C., R.U., L.S., and Am.B. – writing – original draft; M.B., M.K., Ah.B., and H.F. – software; M.B., M.K., A.As., M.A.I., and H.F. –writing – review and editing; and A.Al. and Am.B. – supervision. All authors have read and agreed to the published version of the manuscript.

  3. Conflict of interest: Authors state no conflict of interest.

  4. Data availability statement: The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Received: 2024-04-17
Revised: 2024-06-28
Accepted: 2024-07-08
Published Online: 2024-09-17

© 2024 the author(s), published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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  208. Retraction
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https://doi.org/10.1515/biol-2022-0941
Schlagwörter für diesen Artikel
Pistacia atlantica subsp. atlantica; Pistacia terebintus; morphology; stomatal density; scanning electron microscopy
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Artikel in diesem Heft

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  4. PEGylated porcine–human recombinant uricase: A novel fusion protein with improved efficacy and safety for the treatment of hyperuricemia and renal complications
  5. Research progress on ocular complications caused by type 2 diabetes mellitus and the function of tears and blepharons
  6. The role and mechanism of esketamine in preventing and treating remifentanil-induced hyperalgesia based on the NMDA receptor–CaMKII pathway
  7. Brucella infection combined with Nocardia infection: A case report and literature review
  8. Detection of serum interleukin-18 level and neutrophil/lymphocyte ratio in patients with antineutrophil cytoplasmic antibody-associated vasculitis and its clinical significance
  9. Ang-1, Ang-2, and Tie2 are diagnostic biomarkers for Henoch-Schönlein purpura and pediatric-onset systemic lupus erythematous
  10. PTTG1 induces pancreatic cancer cell proliferation and promotes aerobic glycolysis by regulating c-myc
  11. Role of serum B-cell-activating factor and interleukin-17 as biomarkers in the classification of interstitial pneumonia with autoimmune features
  12. Effectiveness and safety of a mumps containing vaccine in preventing laboratory-confirmed mumps cases from 2002 to 2017: A meta-analysis
  13. Low levels of sex hormone-binding globulin predict an increased breast cancer risk and its underlying molecular mechanisms
  14. A case of Trousseau syndrome: Screening, detection and complication
  15. Application of the integrated airway humidification device enhances the humidification effect of the rabbit tracheotomy model
  16. Preparation of Cu2+/TA/HAP composite coating with anti-bacterial and osteogenic potential on 3D-printed porous Ti alloy scaffolds for orthopedic applications
  17. Aquaporin-8 promotes human dermal fibroblasts to counteract hydrogen peroxide-induced oxidative damage: A novel target for management of skin aging
  18. Current research and evidence gaps on placental development in iron deficiency anemia
  19. Single-nucleotide polymorphism rs2910829 in PDE4D is related to stroke susceptibility in Chinese populations: The results of a meta-analysis
  20. Pheochromocytoma-induced myocardial infarction: A case report
  21. Kaempferol regulates apoptosis and migration of neural stem cells to attenuate cerebral infarction by O‐GlcNAcylation of β-catenin
  22. Sirtuin 5 regulates acute myeloid leukemia cell viability and apoptosis by succinylation modification of glycine decarboxylase
  23. Apigenin 7-glucoside impedes hypoxia-induced malignant phenotypes of cervical cancer cells in a p16-dependent manner
  24. KAT2A changes the function of endometrial stromal cells via regulating the succinylation of ENO1
  25. Current state of research on copper complexes in the treatment of breast cancer
  26. Exploring antioxidant strategies in the pathogenesis of ALS
  27. Helicobacter pylori causes gastric dysbacteriosis in chronic gastritis patients
  28. IL-33/soluble ST2 axis is associated with radiation-induced cardiac injury
  29. The predictive value of serum NLR, SII, and OPNI for lymph node metastasis in breast cancer patients with internal mammary lymph nodes after thoracoscopic surgery
  30. Carrying SNP rs17506395 (T > G) in TP63 gene and CCR5Δ32 mutation associated with the occurrence of breast cancer in Burkina Faso
  31. P2X7 receptor: A receptor closely linked with sepsis-associated encephalopathy
  32. Probiotics for inflammatory bowel disease: Is there sufficient evidence?
  33. Identification of KDM4C as a gene conferring drug resistance in multiple myeloma
  34. Microbial perspective on the skin–gut axis and atopic dermatitis
  35. Thymosin α1 combined with XELOX improves immune function and reduces serum tumor markers in colorectal cancer patients after radical surgery
  36. Highly specific vaginal microbiome signature for gynecological cancers
  37. Sample size estimation for AQP4-IgG seropositive optic neuritis: Retinal damage detection by optical coherence tomography
  38. The effects of SDF-1 combined application with VEGF on femoral distraction osteogenesis in rats
  39. Fabrication and characterization of gold nanoparticles using alginate: In vitro and in vivo assessment of its administration effects with swimming exercise on diabetic rats
  40. Mitigating digestive disorders: Action mechanisms of Mediterranean herbal active compounds
  41. Distribution of CYP2D6 and CYP2C19 gene polymorphisms in Han and Uygur populations with breast cancer in Xinjiang, China
  42. VSP-2 attenuates secretion of inflammatory cytokines induced by LPS in BV2 cells by mediating the PPARγ/NF-κB signaling pathway
  43. Factors influencing spontaneous hypothermia after emergency trauma and the construction of a predictive model
  44. Long-term administration of morphine specifically alters the level of protein expression in different brain regions and affects the redox state
  45. Application of metagenomic next-generation sequencing technology in the etiological diagnosis of peritoneal dialysis-associated peritonitis
  46. Clinical diagnosis, prevention, and treatment of neurodyspepsia syndrome using intelligent medicine
  47. Case report: Successful bronchoscopic interventional treatment of endobronchial leiomyomas
  48. Preliminary investigation into the genetic etiology of short stature in children through whole exon sequencing of the core family
  49. Cystic adenomyoma of the uterus: Case report and literature review
  50. Mesoporous silica nanoparticles as a drug delivery mechanism
  51. Dynamic changes in autophagy activity in different degrees of pulmonary fibrosis in mice
  52. Vitamin D deficiency and inflammatory markers in type 2 diabetes: Big data insights
  53. Lactate-induced IGF1R protein lactylation promotes proliferation and metabolic reprogramming of lung cancer cells
  54. Meta-analysis on the efficacy of allogeneic hematopoietic stem cell transplantation to treat malignant lymphoma
  55. Mitochondrial DNA drives neuroinflammation through the cGAS-IFN signaling pathway in the spinal cord of neuropathic pain mice
  56. Application value of artificial intelligence algorithm-based magnetic resonance multi-sequence imaging in staging diagnosis of cervical cancer
  57. Embedded monitoring system and teaching of artificial intelligence online drug component recognition
  58. Investigation into the association of FNDC1 and ADAMTS12 gene expression with plumage coloration in Muscovy ducks
  59. Yak meat content in feed and its impact on the growth of rats
  60. A rare case of Richter transformation with breast involvement: A case report and literature review
  61. First report of Nocardia wallacei infection in an immunocompetent patient in Zhejiang province
  62. Rhodococcus equi and Brucella pulmonary mass in immunocompetent: A case report and literature review
  63. Downregulation of RIP3 ameliorates the left ventricular mechanics and function after myocardial infarction via modulating NF-κB/NLRP3 pathway
  64. Evaluation of the role of some non-enzymatic antioxidants among Iraqi patients with non-alcoholic fatty liver disease
  65. The role of Phafin proteins in cell signaling pathways and diseases
  66. Ten-year anemia as initial manifestation of Castleman disease in the abdominal cavity: A case report
  67. Coexistence of hereditary spherocytosis with SPTB P.Trp1150 gene variant and Gilbert syndrome: A case report and literature review
  68. Utilization of convolutional neural networks to analyze microscopic images for high-throughput screening of mesenchymal stem cells
  69. Exploratory evaluation supported by experimental and modeling approaches of Inula viscosa root extract as a potent corrosion inhibitor for mild steel in a 1 M HCl solution
  70. Imaging manifestations of ductal adenoma of the breast: A case report
  71. Gut microbiota and sleep: Interaction mechanisms and therapeutic prospects
  72. Isomangiferin promotes the migration and osteogenic differentiation of rat bone marrow mesenchymal stem cells
  73. Prognostic value and microenvironmental crosstalk of exosome-related signatures in human epidermal growth factor receptor 2 positive breast cancer
  74. Circular RNAs as potential biomarkers for male severe sepsis
  75. Knockdown of Stanniocalcin-1 inhibits growth and glycolysis in oral squamous cell carcinoma cells
  76. The expression and biological role of complement C1s in esophageal squamous cell carcinoma
  77. A novel GNAS mutation in pseudohypoparathyroidism type 1a with articular flexion deformity: A case report
  78. Predictive value of serum magnesium levels for prognosis in patients with non-small cell lung cancer undergoing EGFR-TKI therapy
  79. HSPB1 alleviates acute-on-chronic liver failure via the P53/Bax pathway
  80. IgG4-related disease complicated by PLA2R-associated membranous nephropathy: A case report
  81. Baculovirus-mediated endostatin and angiostatin activation of autophagy through the AMPK/AKT/mTOR pathway inhibits angiogenesis in hepatocellular carcinoma
  82. Metformin mitigates osteoarthritis progression by modulating the PI3K/AKT/mTOR signaling pathway and enhancing chondrocyte autophagy
  83. Evaluation of the activity of antimicrobial peptides against bacterial vaginosis
  84. Atypical presentation of γ/δ mycosis fungoides with an unusual phenotype and SOCS1 mutation
  85. Analysis of the microecological mechanism of diabetic kidney disease based on the theory of “gut–kidney axis”: A systematic review
  86. Omega-3 fatty acids prevent gestational diabetes mellitus via modulation of lipid metabolism
  87. Refractory hypertension complicated with Turner syndrome: A case report
  88. Interaction of ncRNAs and the PI3K/AKT/mTOR pathway: Implications for osteosarcoma
  89. Association of low attenuation area scores with pulmonary function and clinical prognosis in patients with chronic obstructive pulmonary disease
  90. Long non-coding RNAs in bone formation: Key regulators and therapeutic prospects
  91. The deubiquitinating enzyme USP35 regulates the stability of NRF2 protein
  92. Neutrophil-to-lymphocyte ratio and platelet-to-lymphocyte ratio as potential diagnostic markers for rebleeding in patients with esophagogastric variceal bleeding
  93. G protein-coupled receptor 1 participating in the mechanism of mediating gestational diabetes mellitus by phosphorylating the AKT pathway
  94. LL37-mtDNA regulates viability, apoptosis, inflammation, and autophagy in lipopolysaccharide-treated RLE-6TN cells by targeting Hsp90aa1
  95. The analgesic effect of paeoniflorin: A focused review
  96. Chemical composition’s effect on Solanum nigrum Linn.’s antioxidant capacity and erythrocyte protection: Bioactive components and molecular docking analysis
  97. Knockdown of HCK promotes HREC cell viability and inner blood–retinal barrier integrity by regulating the AMPK signaling pathway
  98. The role of rapamycin in the PINK1/Parkin signaling pathway in mitophagy in podocytes
  99. Laryngeal non-Hodgkin lymphoma: Report of four cases and review of the literature
  100. Clinical value of macrogenome next-generation sequencing on infections
  101. Overview of dendritic cells and related pathways in autoimmune uveitis
  102. TAK-242 alleviates diabetic cardiomyopathy via inhibiting pyroptosis and TLR4/CaMKII/NLRP3 pathway
  103. Hypomethylation in promoters of PGC-1α involved in exercise-driven skeletal muscular alterations in old age
  104. Profile and antimicrobial susceptibility patterns of bacteria isolated from effluents of Kolladiba and Debark hospitals
  105. The expression and clinical significance of syncytin-1 in serum exosomes of hepatocellular carcinoma patients
  106. A histomorphometric study to evaluate the therapeutic effects of biosynthesized silver nanoparticles on the kidneys infected with Plasmodium chabaudi
  107. PGRMC1 and PAQR4 are promising molecular targets for a rare subtype of ovarian cancer
  108. Analysis of MDA, SOD, TAOC, MNCV, SNCV, and TSS scores in patients with diabetes peripheral neuropathy
  109. SLIT3 deficiency promotes non-small cell lung cancer progression by modulating UBE2C/WNT signaling
  110. The relationship between TMCO1 and CALR in the pathological characteristics of prostate cancer and its effect on the metastasis of prostate cancer cells
  111. Heterogeneous nuclear ribonucleoprotein K is a potential target for enhancing the chemosensitivity of nasopharyngeal carcinoma
  112. PHB2 alleviates retinal pigment epithelium cell fibrosis by suppressing the AGE–RAGE pathway
  113. Anti-γ-aminobutyric acid-B receptor autoimmune encephalitis with syncope as the initial symptom: Case report and literature review
  114. Comparative analysis of chloroplast genome of Lonicera japonica cv. Damaohua
  115. Human umbilical cord mesenchymal stem cells regulate glutathione metabolism depending on the ERK–Nrf2–HO-1 signal pathway to repair phosphoramide mustard-induced ovarian cancer cells
  116. Electroacupuncture on GB acupoints improves osteoporosis via the estradiol–PI3K–Akt signaling pathway
  117. Renalase protects against podocyte injury by inhibiting oxidative stress and apoptosis in diabetic nephropathy
  118. Review: Dicranostigma leptopodum: A peculiar plant of Papaveraceae
  119. Combination effect of flavonoids attenuates lung cancer cell proliferation by inhibiting the STAT3 and FAK signaling pathway
  120. Renal microangiopathy and immune complex glomerulonephritis induced by anti-tumour agents: A case report
  121. Correlation analysis of AVPR1a and AVPR2 with abnormal water and sodium and potassium metabolism in rats
  122. Gastrointestinal health anti-diarrheal mixture relieves spleen deficiency-induced diarrhea through regulating gut microbiota
  123. Myriad factors and pathways influencing tumor radiotherapy resistance
  124. Exploring the effects of culture conditions on Yapsin (YPS) gene expression in Nakaseomyces glabratus
  125. Screening of prognostic core genes based on cell–cell interaction in the peripheral blood of patients with sepsis
  126. Coagulation factor II thrombin receptor as a promising biomarker in breast cancer management
  127. Ileocecal mucinous carcinoma misdiagnosed as incarcerated hernia: A case report
  128. Methyltransferase like 13 promotes malignant behaviors of bladder cancer cells through targeting PI3K/ATK signaling pathway
  129. The debate between electricity and heat, efficacy and safety of irreversible electroporation and radiofrequency ablation in the treatment of liver cancer: A meta-analysis
  130. ZAG promotes colorectal cancer cell proliferation and epithelial–mesenchymal transition by promoting lipid synthesis
  131. Baicalein inhibits NLRP3 inflammasome activation and mitigates placental inflammation and oxidative stress in gestational diabetes mellitus
  132. Impact of SWCNT-conjugated senna leaf extract on breast cancer cells: A potential apoptotic therapeutic strategy
  133. MFAP5 inhibits the malignant progression of endometrial cancer cells in vitro
  134. Major ozonated autohemotherapy promoted functional recovery following spinal cord injury in adult rats via the inhibition of oxidative stress and inflammation
  135. Axodendritic targeting of TAU and MAP2 and microtubule polarization in iPSC-derived versus SH-SY5Y-derived human neurons
  136. Differential expression of phosphoinositide 3-kinase/protein kinase B and Toll-like receptor/nuclear factor kappa B signaling pathways in experimental obesity Wistar rat model
  137. The therapeutic potential of targeting Oncostatin M and the interleukin-6 family in retinal diseases: A comprehensive review
  138. BA inhibits LPS-stimulated inflammatory response and apoptosis in human middle ear epithelial cells by regulating the Nf-Kb/Iκbα axis
  139. Role of circRMRP and circRPL27 in chronic obstructive pulmonary disease
  140. Investigating the role of hyperexpressed HCN1 in inducing myocardial infarction through activation of the NF-κB signaling pathway
  141. Characterization of phenolic compounds and evaluation of anti-diabetic potential in Cannabis sativa L. seeds: In vivo, in vitro, and in silico studies
  142. Quantitative immunohistochemistry analysis of breast Ki67 based on artificial intelligence
  143. Ecology and Environmental Science
  144. Screening of different growth conditions of Bacillus subtilis isolated from membrane-less microbial fuel cell toward antimicrobial activity profiling
  145. Degradation of a mixture of 13 polycyclic aromatic hydrocarbons by commercial effective microorganisms
  146. Evaluation of the impact of two citrus plants on the variation of Panonychus citri (Acari: Tetranychidae) and beneficial phytoseiid mites
  147. Prediction of present and future distribution areas of Juniperus drupacea Labill and determination of ethnobotany properties in Antalya Province, Türkiye
  148. Population genetics of Todarodes pacificus (Cephalopoda: Ommastrephidae) in the northwest Pacific Ocean via GBS sequencing
  149. A comparative analysis of dendrometric, macromorphological, and micromorphological characteristics of Pistacia atlantica subsp. atlantica and Pistacia terebinthus in the middle Atlas region of Morocco
  150. Macrofungal sporocarp community in the lichen Scots pine forests
  151. Assessing the proximate compositions of indigenous forage species in Yemen’s pastoral rangelands
  152. Food Science
  153. Gut microbiota changes associated with low-carbohydrate diet intervention for obesity
  154. Reexamination of Aspergillus cristatus phylogeny in dark tea: Characteristics of the mitochondrial genome
  155. Differences in the flavonoid composition of the leaves, fruits, and branches of mulberry are distinguished based on a plant metabolomics approach
  156. Investigating the impact of wet rendering (solventless method) on PUFA-rich oil from catfish (Clarias magur) viscera
  157. Non-linear associations between cardiovascular metabolic indices and metabolic-associated fatty liver disease: A cross-sectional study in the US population (2017–2020)
  158. Knockdown of USP7 alleviates atherosclerosis in ApoE-deficient mice by regulating EZH2 expression
  159. Utility of dairy microbiome as a tool for authentication and traceability
  160. Agriculture
  161. Enhancing faba bean (Vicia faba L.) productivity through establishing the area-specific fertilizer rate recommendation in southwest Ethiopia
  162. Impact of novel herbicide based on synthetic auxins and ALS inhibitor on weed control
  163. Perspectives of pteridophytes microbiome for bioremediation in agricultural applications
  164. Fertilizer application parameters for drip-irrigated peanut based on the fertilizer effect function established from a “3414” field trial
  165. Improving the productivity and profitability of maize (Zea mays L.) using optimum blended inorganic fertilization
  166. Application of leaf multispectral analyzer in comparison to hyperspectral device to assess the diversity of spectral reflectance indices in wheat genotypes
  167. Animal Sciences
  168. Knockdown of ANP32E inhibits colorectal cancer cell growth and glycolysis by regulating the AKT/mTOR pathway
  169. Development of a detection chip for major pathogenic drug-resistant genes and drug targets in bovine respiratory system diseases
  170. Exploration of the genetic influence of MYOT and MB genes on the plumage coloration of Muscovy ducks
  171. Transcriptome analysis of adipose tissue in grazing cattle: Identifying key regulators of fat metabolism
  172. Comparison of nutritional value of the wild and cultivated spiny loaches at three growth stages
  173. Transcriptomic analysis of liver immune response in Chinese spiny frog (Quasipaa spinosa) infected with Proteus mirabilis
  174. Disruption of BCAA degradation is a critical characteristic of diabetic cardiomyopathy revealed by integrated transcriptome and metabolome analysis
  175. Plant Sciences
  176. Effect of long-term in-row branch covering on soil microorganisms in pear orchards
  177. Photosynthetic physiological characteristics, growth performance, and element concentrations reveal the calcicole–calcifuge behaviors of three Camellia species
  178. Transcriptome analysis reveals the mechanism of NaHCO3 promoting tobacco leaf maturation
  179. Bioinformatics, expression analysis, and functional verification of allene oxide synthase gene HvnAOS1 and HvnAOS2 in qingke
  180. Water, nitrogen, and phosphorus coupling improves gray jujube fruit quality and yield
  181. Improving grape fruit quality through soil conditioner: Insights from RNA-seq analysis of Cabernet Sauvignon roots
  182. Role of Embinin in the reabsorption of nucleus pulposus in lumbar disc herniation: Promotion of nucleus pulposus neovascularization and apoptosis of nucleus pulposus cells
  183. Revealing the effects of amino acid, organic acid, and phytohormones on the germination of tomato seeds under salinity stress
  184. Combined effects of nitrogen fertilizer and biochar on the growth, yield, and quality of pepper
  185. Comprehensive phytochemical and toxicological analysis of Chenopodium ambrosioides (L.) fractions
  186. Impact of “3414” fertilization on the yield and quality of greenhouse tomatoes
  187. Exploring the coupling mode of water and fertilizer for improving growth, fruit quality, and yield of the pear in the arid region
  188. Metagenomic analysis of endophytic bacteria in seed potato (Solanum tuberosum)
  189. Antibacterial, antifungal, and phytochemical properties of Salsola kali ethanolic extract
  190. Exploring the hepatoprotective properties of citronellol: In vitro and in silico studies on ethanol-induced damage in HepG2 cells
  191. Enhanced osmotic dehydration of watermelon rind using honey–sucrose solutions: A study on pre-treatment efficacy and mass transfer kinetics
  192. Effects of exogenous 2,4-epibrassinolide on photosynthetic traits of 53 cowpea varieties under NaCl stress
  193. Comparative transcriptome analysis of maize (Zea mays L.) seedlings in response to copper stress
  194. An optimization method for measuring the stomata in cassava (Manihot esculenta Crantz) under multiple abiotic stresses
  195. Fosinopril inhibits Ang II-induced VSMC proliferation, phenotype transformation, migration, and oxidative stress through the TGF-β1/Smad signaling pathway
  196. Antioxidant and antimicrobial activities of Salsola imbricata methanolic extract and its phytochemical characterization
  197. Bioengineering and Biotechnology
  198. Absorbable calcium and phosphorus bioactive membranes promote bone marrow mesenchymal stem cells osteogenic differentiation for bone regeneration
  199. New advances in protein engineering for industrial applications: Key takeaways
  200. An overview of the production and use of Bacillus thuringiensis toxin
  201. Research progress of nanoparticles in diagnosis and treatment of hepatocellular carcinoma
  202. Bioelectrochemical biosensors for water quality assessment and wastewater monitoring
  203. PEI/MMNs@LNA-542 nanoparticles alleviate ICU-acquired weakness through targeted autophagy inhibition and mitochondrial protection
  204. Unleashing of cytotoxic effects of thymoquinone-bovine serum albumin nanoparticles on A549 lung cancer cells
  205. Erratum
  206. Erratum to “Investigating the association between dietary patterns and glycemic control among children and adolescents with T1DM”
  207. Erratum to “Activation of hypermethylated P2RY1 mitigates gastric cancer by promoting apoptosis and inhibiting proliferation”
  208. Retraction
  209. Retraction to “MiR-223-3p regulates cell viability, migration, invasion, and apoptosis of non-small cell lung cancer cells by targeting RHOB”
  210. Retraction to “A data mining technique for detecting malignant mesothelioma cancer using multiple regression analysis”
  211. Special Issue on Advances in Neurodegenerative Disease Research and Treatment
  212. Transplantation of human neural stem cell prevents symptomatic motor behavior disability in a rat model of Parkinson’s disease
  213. Special Issue on Multi-omics
  214. Inflammasome complex genes with clinical relevance suggest potential as therapeutic targets for anti-tumor drugs in clear cell renal cell carcinoma
  215. Gastroesophageal varices in primary biliary cholangitis with anti-centromere antibody positivity: Early onset?
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Heruntergeladen am 20.9.2025 von https://www.degruyterbrill.com/document/doi/10.1515/biol-2022-0941/html?lang=de
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