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Article

Pollen Variability of Alnus glutinosa (L.) Gaerth. (Betulaceae) from Southern Range Edge Populations in Northern Morocco

by
Abdelouahab Sahli
1,
Jalal Kassout
2,
Vladimiro Andrea Boselli
3,
Hassan Ennouni
1,
Soufian Chakkour
1,
Khalil Kadaoui
1,
Mhammad Houssni
1 and
Mohammed Ater
1,*
1
Bio-Agrodiversity Team, Applied Botanic Laboratory, Sciences Faculty, Abdelmalek Essaâdi University, BP 2062, P.O. Box 2121, Tétouan 93030, Morocco
2
Regional Agricultural Research Center of Marrakech, National Institute of Agricultural Research, Avenue Ennasr, P.O. Box 415, Rabat 10090, Morocco
3
Dipartimento di Geoscienze, Università degli Studi di Padova, 35131 Padova, Italy
*
Author to whom correspondence should be addressed.
Int. J. Plant Biol. 2023, 14(3), 797-810; https://0-doi-org.brum.beds.ac.uk/10.3390/ijpb14030059
Submission received: 26 July 2023 / Revised: 17 August 2023 / Accepted: 18 August 2023 / Published: 23 August 2023
(This article belongs to the Section Plant Ecology and Biodiversity)
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Abstract

:
Moroccan populations of Alnus glutinosa (L.) Gaerth. (Betulaceae) are found at the southern limit of the species’ range and are represented by tetraploid cytotypes with no available pollen data. The objective of this study was to assess the morphological and morphometric variability of the pollen, specifically focusing on pollen diameters and the number of apertures. To achieve this, we sampled 11 populations that are representative of the Moroccan distribution area of this species. We employed a hierarchical sampling design (11 populations, 10 trees per population, and from 30 to 300 pollen grains per tree, depending on the character measured) to examine different levels of variability: interpopulation, intrapopulation, and intraindividual. The results demonstrate that there is no discernible difference in the morphology or size of the pollen among the Moroccan tetraploid populations. However, we observed a high degree of intraspecific variability in pollen morphometric traits, but most of this variability is associated with the intraindividual level.

1. Introduction

Alnus glutinosa (L.) Gaerth. (Betulaceae) is a Eurasian species that ranges from western Europe to the east of Turkey and even extends to some enclaves in North Africa [1,2,3,4,5]. The morphology of Alnus pollen has been described and studied by several authors, including Erdtman [6], Blackmore et al. [7], and Leopold et al. [8]. While the variability of Alnus species’ pollen morphology and morphometric characteristics is relatively well known at the interspecific level, intraspecific variability in pollen traits is generally understudied, even in A. glutinosa.
In Morocco, A. glutinosa is a rare species with small-sized populations located in isolated habitats in the western Rif Mountains [9]. These populations are situated at the southern edge of the species’ range, an area that has been recognized as a refuge during glacial cycles [10,11]. The range of A. glutinosa has expanded and contracted with glacial cycles, leading to disproportionate genetic diversity in these populations [4,12,13]. The Moroccan black alder populations have been identified as tetraploids [4] and are considered an autopolyploid taxon [14]. Molecular markers have shown a strong distinctiveness of the Moroccan populations, with greater genetic diversity and allelic richness than the diploid populations [4]. Polyploidization is part of the evolutionary process that can lead to rapid speciation [15,16,17,18]. As a result, some researchers have proposed the creation of a new taxon of a specific rank for the Iberian and Moroccan tetraploid populations [19].
Variability in pollen morphometry and morphology is an important aspect in resolving taxonomic problems at various levels and has become an integral part of collaborative approaches in evolutionary research. Generally, pollen size exhibits extensive variation among Angiosperms, ranging from 5 µm to 250 µm [20]. This variability corresponds to how each species responds to specific pollination and fertilization environments [21]. The evolutionary consequences of inter-individual differences in pollen size depend, in part, on the relative importance of environmental and genetic controls for pollen size variation. For instance, pollen size increases with the level of ploidy at both the interspecific and intraspecific levels [22,23,24,25,26,27]. However, the relationship between pollen size and genome size is not straightforward, and their trajectories may not be linked [28,29].
Currently, there is a lack of information regarding the pollen morphology of tetraploid Moroccan populations located at the edge of the Alnus glutinosa range. Thus, the objective of this study is to fill this gap and determine whether these populations exhibit any morphometric differentiation in their pollen traits. Additionally, this study aims to investigate the variability of pollen morphometric traits at the infraspecific level at different organizational and spatial levels, including interpopulation, intrapopulation, and intraindividual levels.

2. Materials and Methods

2.1. Study Area and Sampling

Geographically, the study area is located in the Western Rif Mountains in northwest Morocco (Figure 1). The environmental conditions in this region are favorable for riparian habitats where remarkable populations of A. glutinosa are found within an altitudinal range of 500 to 1100 m and in humid bioclimates [9].
Sampling was conducted across 11 populations (Figure 1 and Appendix A) which were considered representative of the Moroccan alder forests [9]. To collect pollen grains, we sampled mature male catkins during the winter flowering period. For each population, we randomly selected 10 trees, and male catkins were collected from different parts of each tree, including the top and bottom, under different exposures to ensure homogenized samples. The sampling design allowed us to test variability at different hierarchical levels: (i) the interpopulation level (variability between different sampled populations), (ii) the intrapopulation level (variability between different trees of the same population), and (iii) the intraindividual level (variability within the same tree) (Figure 2).

2.2. Photonic Microscope Observations and Measurements

The fresh pollen was prepared for observation under a photonic microscope using the Wodehouse’s method [30], which involved mounting the pollen in glycerinated gelatin stained with basic fuchsin. Two parameters were measured for each pollen grain, the polar diameter (P) and the equatorial diameter (E), following the protocol outlined by Blackmore et al. [7]. To prevent the Cushing effect [31], which causes an increase in size due to the swelling of the pollen grains, measurements were taken in the same time interval after slide preparation. Observations and measurements were obtained using an Olympus BX43 microscope, and 30 pollen grains were analyzed for each tree. The average number of pores per pollen grain was determined by analyzing a sample of 300 pollen grains per tree. Individual pollen grains were examined under 400x magnification and photographed using a digital camera. The digital images of the pollen grains were measured via ImageJ software (https://imagej.nih.gov/ij/, accessed on 6 August 2018). Only pollen grains lying in polar view were used. The morphological description of the pollen followed the nomenclature proposed by Punt et al. [32] and Hesse et al. [33].

2.3. Scanning Electron Microscope Observations

The sample preparation protocol involved fixing the pollen sample in 2% glutaraldehyde for 24 h, followed by dehydration with increasing concentrations of ethanol (30%, 50%, 70%, 90%, and 100%) for 15 min each, repeating the process twice at each concentration. The samples were then placed on a carbon ribbon and dried in an oven at 35 °C for 12 h. Finally, the samples were coated with a 4nm layer of gold using a Leica EM AC600 high-vacuum coating device before they were observed under a Jeol JSM-7800F Schottky Field Emission Scanning Electron Microscope at a voltage of 2 kV. Both the sample preparation and observation were conducted at the Microscopy Unit of the Centralized Research Support Service (SCAI) at the University of Córdoba in Spain.

2.4. Data Analysis

The normality and homogeneity of each variance were checked prior to conducting statistical tests. The statistical analyses were performed using R software v. 4.0.5 [34] which included a one-way ANOVA with Tukey’s test for multiple comparisons, Pearson correlations, a coefficient of variation (CV %), a nested ANOVA with random effects, and variance decomposition [35,36].

3. Results

3.1. Pollen Morphology

Observations using both light and scanning electron microscopes indicate that the pollen of the Alnus glutinosa populations in Morocco is oblate in shape, as shown in Figure 3 and Figure 4. The pollen is categorized as breviaxe, with a polar diameter (P) that is smaller than the equatorial diameter (E) and an average P/E ratio of 0.73 ± 0.01 µm, as defined by Punt et al. [32]. Analyses of the variance in the P/E ratio (Table 1) reveal that there are no significant variations in the pollen grains’ shape at either the intra- or inter-population level.
The observed pollen grains’ aperture type is stephanoporate, which indicates that the pollen grains possess several pores arranged in a crown at the equatorial diameter (E), as shown in Figure 3 and Figure 4. The pores have an oval shape and are surrounded by a ring or annulus, which is formed due to detachment between the ectexin and the endexin, creating a space inside the aperture known as an atrium or vestibulum (Figure 4e). Additionally, the pollen grains have distinct arches or arcus that are formed by the thickening of the exine and connect different pores (Figure 4b,d). The exine surface of the pollen grains is scabrate (Figure 4d).

3.2. Variability of Pollen Diameters

The average size of the pollen grains observed in the studied populations of A. glutinosa is relatively small, with a polar diameter (P) of 18.75 ± 0.62 µm and an equatorial diameter (E) of 26.42 ± 0.76 µm (Table 1). The Pearson correlation test shows that the two diameters, P and E, are highly correlated (r = 0.622; p < 0.001) (Figure 5).
The range between the extreme values observed for the two pollen diameters, P and E, in the Moroccan populations of A. glutinosa appears to be relatively narrow. The minimum value for the P is observed in the Khezana population (18.08 ± 0.62 µm), and the maximum value is observed in the Amlay population (19.66 ± 0.69 µm), representing a variation of 8.4%. Similarly, for the E, the minimum value is observed in the Khezana population (24.77 ± 0.77 µm), and the maximum value is observed in the of Tifouzal population (27.37 ± 0.71 µm), representing a variation of 9.6%. However, multiple comparisons of the population means show the existence of a size gradient, with the Khezana and Amlay populations differing in the size of the P and the Khezana population differing from the Bobiyine and Tifouzal populations in the size of the E (Table 1). The one-way ANOVA (population) confirms the existence of significant interpopulation variation (Table 1).
The coefficients of variation associated with the means of the diameters show relatively limited variations, with the CV for the P ranging from 8.85% to 11.28%, and for the E, ranging from 7.18% to 13.94%. However, the one-way ANOVA (tree) shows highly significant intrapopulation variation within the 11 populations studied (Table 1).
The nested ANOVA with populations (interpopulation) and trees (intrapopulation) confirms the existence of significant variation at both levels (Table 2). The decomposition of variance shows that the hierarchical sampling design explains more than 90% of the variance (Table 2, Figure 2). Over 50% of the variance (59.2% for the P and 55.5% for the E) is expressed at the intraindividual level, i.e., the variation between pollen grains from the same tree. The intrapopulation variance, i.e., the variation between trees of the same population, is also significant, with 24.36% for the P and 31.49% for the E. Meanwhile, the interpopulation variance, i.e., the variation between trees of different populations, is very low (6.9% for the P and 3.8% for the E) and less important than the residual variance.

3.3. Variability in the Number of Apertures

Our findings demonstrate considerable variation in the number of pores present on the pollen grains, ranging from one to seven pores (Figure 6, Appendix B). However, we found no significant correlation between pore number and pollen diameter (Figure 5). The relative abundance of each type of pollen varied greatly, with pollen grains having one, two, three, or seven pores occurring relatively infrequently, accounting for less than or equal to 1% of the observed pollen. Pollen grains with four, five, or six pores were more common and were observed in all populations. Notably, pollen grains with five pores were the most dominant type, constituting approximately 80% of the observed pollen grains, while pollen grains with four or six pores accounted for around 9% of the observed pollen grains. Thus, to investigate interpopulation and intrapopulation variability, we will focus our analysis on the dominant pollen types with four, five, or six apertures (Table 3).
The ANOVA and multiple comparisons of means reveal that there are no significant variations in pollen with four or five apertures between populations. Conversely, pollen with 6 apertures exhibit significant variation according to the ANOVA (p < 0.05), and multiple comparisons of means classified the populations into three groups based on pollen frequencies with six apertures. The Tifouzal population has a high frequency (20.2%), while the populations with low frequencies (<5%), such as Bouztate, Bobiyine, Siouana, and Aïn Korra, are distinct, and other populations have intermediate frequencies. Consequently, the interpopulation variability is insignificant for pollen with four or five apertures, while it is weak for pollen with six apertures.
The intrapopulation variability (variation among trees of the same population) was assessed using coefficients of variation (CVs) (Table 3). The results indicate a small variation in pollen with five apertures, with CVs ranging from 6.36% to 19.75%. However, the variation amplitude for pollen with four or six apertures is considerably higher, ranging between 62% and 185% for the former and between 72% and 147% for the latter. Therefore, intrapopulation variability is low for the dominant five-aperture pollen type, while for the four- and six-aperture types, the variation amplitude is exceedingly high.

4. Discussion

4.1. Pollen Morphology

Our study, which involved observations using light and electron microscopy and P/E ratio measurements (Table 1, Figure 3 and Figure 4), shows that the pollen of Moroccan populations of A. glutinosa is oblate in shape, with no observed variation in the type of shape. This form is the most frequently cited in descriptions of pollen grains in Alnus glutinosa [7,33,37]. However, data from A. glutinosa populations in Turkey [38] showed a slight variation with a P/E ratio of 0.79, suggesting a form related to the suboblate type. The oblate form is also found in other Alnus species, including A. viridis, which has a P/E ratio ranging from 0.67 to 0.77 [7]. Other species in the Betulaceae family, such as Betula nana, Betula humilis, Caprinus betulus, and Corylus avellana, have a slightly different sub-oblate form [7]. Our observations also reveal that the pollen of A. glutinosa from Moroccan populations is stephanoporate, with annulus pores connected by arches and a scabrate exine (Figure 3 and Figure 4), consistent with previous studies [7,33,39]. Furthermore, our data demonstrate that the pollen morphology and stereostructure of the exine in the Moroccan populations are not different from the known descriptions of A. glutinosa. Therefore, we can conclude that the pollen of Moroccan tetraploid populations of A. glutinosa shares the same shape and exine ornamentation as that of A. glutinosa in general.

4.2. Pollen Size Variability

The size of the pollen grains in the Moroccan populations, with P = 18.75 ± 0.62 µm and E = 26.42 ± 0.76 µm, can be considered relatively small, which is a common characteristic among anemophilous species [40]. While there data are relatively available on the morphology of Alnus glutinosa pollen [7,8,33], morphometric data for comparison are scarce. The representativeness of data can be influenced by various factors inherent to the methodology used, such as the sample size, pollen grain preparation method (fresh or acetolysed), or mounting medium. For instance, May and Lacoure [41] recommend a minimum sample size of 30 pollen grains, though it is not a universal rule. Among the consulted data, those obtained from A. glutinosa populations from Turkey [38] seem to be the most suitable for establishing a comparison. They were obtained from fresh pollen using the same preparation method as Wodehouse [30] and with the same sample size. These data showed pollen grains with E = 27.86 ± 1.74 µm and P = 21.9 ± 1.34 µm, sizes comparable to those obtained in this study (Table 1), even if the P value is slightly higher. It is important to note that the Turkish populations are in the diploid range in terms of the geographical distribution of A. glutinosa cytotypes [14]. Generally, polyploidy and genome size can influence pollen grain size, as observed by Karlsdóttir et al. [42] in Betula nana (a diploid species) and Betula pubescens (a tetraploid species). While this is not a universal rule, it is common for pollen size to increase with polyploidy [43]. Therefore, one would expect pollen size to increase significantly with the ploidy level. However, in the case of the Moroccan tetraploid populations, the polyploid nature of the populations does not appear to influence the size of the pollen.
Regarding interpopulation and intrapopulation comparisons, the question of data representativeness does not arise, as the data were obtained via the same protocol. The hierarchical sampling design used in this study enabled the evaluation of the intraspecific variability in pollen diameter at different levels—interpopulation, intrapopulation, and intraindividual. The ANOVAs conducted at the interpopulation level showed a significant variation in pollen diameter (Table 1 and Table 2). The results revealed a narrow size gradient, distinguishing the populations of Khezana and Amlay via the P axis and the populations of Khezana, Bobiyine, and Tifouzal via the E axis. However, the contribution of this effect to the total variance was minimal, representing only 7% for the polar diameter and 4% for the equatorial diameter (Table 2). These results suggest that the geographical distribution of the populations does not significantly influence the pollen diameters in Moroccan populations. This can be attributed to the relatively small area occupied by the populations and the homogeneity of their habitats. The relationship between ecological factors and pollen morphometry is not clearly established and has been little studied. Some studies suggest that climatic factors may affect pollen size but over wide geographic distributions with environmental gradients. For instance, Ejsmond et al. [44] found that environments with high temperatures and evapotranspiration tend to produce fewer but larger pollen grains. However, in Cedrus atlantica, Bell et al. [45] found no significant relationship between pollen size and climate (including temperature, precipitation, and aridity). Wronska-Pilarek et al. [46] observed variations in the thickness of the exine of Convallaria majalis in different habitats but no variation in pollen diameter.
Regarding intrapopulation variations, i.e., variations between trees of the same population, the variability is highly significant and greater than that observed at the interpopulation level (Table 1 and Table 2), contributing 24.5% to the total variance for the polar diameter and 31.5% for the equatorial diameter. This level of variability is generally attributed to the heterogeneity of the habitat and/or genetic diversity. In the case of the Moroccan populations, the latter factor seems more relevant, as demonstrated by the data on the genetic diversity of these populations [4,14,47]. However, the intraindividual variability is very high and contributes significantly to the total variance, accounting for 60% for the polar diameter and 55.5% for the equatorial diameter. The preponderance of intraindividual variability suggests that the intraspecific variability observed at the level of the pollen diameter mainly corresponds to an expression of phenotypic plasticity. This indicates significant variability in the pollen diameter within the same tree (genotype). This may be explained by the irregular development of pollen grains in response to the tree’s microenvironmental heterogeneity (height and exposure, for example).

4.3. Variability in the Number of Apertures

The variability observed in the number of pollen apertures in Moroccan populations of A. glutinosa is consistent with data known for the genus Alnus and the species A. glutinosa [48]. Pollen grains of A. glutinosa are typically tri- to hexaporate, with the five-aperture type being dominant [8,49,50], which is in agreement with our results in which the pentaporate type was dominant (Figure 6). However, Shayanmehr et al. [39] have shown the dominance of tetraporate pollen in Alnus glutinosa ssp. glutinosa in Iran and pentaporate pollen in other subspecies.
The dominant pollen type, with five apertures, shows non-significant interpopulation variation and low intrapopulation variation. For the less-frequent pollen types, interpopulation variability is non-significant for the four-aperture type and weakly significant for the six-aperture type. For the latter, variability is mainly associated with a particular population (Tifouzal), without any clear factor being identified. However, at the intrapopulation level, both the four- and six-aperture types show high amplitudes of variance. The preponderance of intrapopulation variability in aperture number suggests that this may be an expression of phenotypic plasticity.
The number of apertures in pollen grains is critical for pollen viability and germination, as discussed by Edlund et al. [51]. The variation in the number of apertures is usually determined by both genetic and environmental factors [48]. The apertural type follows an ontogenic pattern during microsporogenesis [52]. However, it may be subject to various selective pressures that could explain the variability of pollen types as an adaptive response to specific environmental conditions [53]. Furthermore, local environmental factors can affect the formation of pollen grains [54]. The variability in the number of apertures observed in the Moroccan populations of Alnus glutinosa could be attributed to a possible response to the changing and stressful environment that characterizes the habitat of these populations, which is located at the southern range limit of the species. Environmental factors such as the type and duration of exposure, as well as the position and location of anthers on the tree, could influence the number of apertures.
Our findings reveal no significant correlations between the number of apertures and pollen diameters (Figure 5). Thus, it appears that variations in the aperture number are independent of pollen size. These results are consistent with those of Shayanmehr et al. [38] for the genus Alnus. However, other studies have suggested that the number of apertures is associated with pollen size [48,50,55].

5. Conclusions

The results of the study on the morphometric traits of pollen clearly demonstrate that there is no distinction between the Moroccan tetraploid populations and the diploid populations of A. glutinosa reported in the literature.
Our study also revealed significant intraspecific variability in pollen diameter and the number of apertures, with no correlation between these two characters. Most of the variability is expressed at the intrapopulation and intraindividual levels. The preponderance of intraindividual variability suggests that this is mainly due to phenotypic plasticity, which is likely an effect of the microenvironment on the development of pollen at the tree scale.

Author Contributions

Conceptualization, A.S. and M.A.; methodology, A.S. and M.A.; software, A.S., J.K. and M.A.; validation, A.S. and M.A.; formal analysis, A.S., J.K. and M.A.; investigation, A.S. and M.A.; resources, M.A.; data curation, A.S. and M.A.; writing—original draft preparation, A.S. and M.A.; writing—review and editing, A.S.; H.E., M.H., S.C., K.K., J.K., V.A.B. and M.A.; visualization, A.S., J.K. and M.A.; supervision, M.A.; project administration, A.S. and M.A. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

We thank the Microscopy Unit of the Centralized Research Support Service (SCAI) of the University of Córdoba (Spain) and the project “Improving the productivity of forest crops of high socio-economic interest in rural areas of northern Morocco (2018004)” financed by the international cooperation of the Junta de Andalucía (Spain). Likewise, the authors thank agents of the Water and Forests Department of Morocco for helpful information during fieldwork. A special thanks goes out to Abdelatif Ouahrani and Hafid Achtak for their improving the manuscript’s English.

Conflicts of Interest

The authors declare no conflict of interest.

Appendix A

Table A1. Characteristics of the sites where populations were sampled.
Table A1. Characteristics of the sites where populations were sampled.
PopulationCode PAlt-Min
(m)		Alt-Max
(m)		Latitude (°)Longitude (°)Bioclimates
Ain KorraAK240137735.16546−5.31642PH-F
AmlayAM285141235.10789−5.22525H-T
BeniIdderBN200137735.22106−5.323H-T
BoubiyineBO285141235.12983−5.23099H-T
BouztatBZ985150535.00803−5.11503H-F
KhezanaKH654156235.03445−5.14031H-F
Oued LakhmisOL7824035.28634−5.15291SH-C
SiouanaSO6459635.28816−5.46806H-T
TanghayaTN846147734.972778−5.15222H-F
TayenzaTY514160335.16082−5.25836PH-F
TifouzalTF38539035.06139−5.16553H-T
Bioclimates: PH = perhumid; H = wet; SH = subhumid. Bioclimate variants, winter: F = cool; T = temperate; C = hot. Alt-min: minimum altitude of the population; Alt-max: maximum altitude of the population.

Appendix B

Table A2. Variability in the number of apertures in the pollen of Alnus glutinosa.
Table A2. Variability in the number of apertures in the pollen of Alnus glutinosa.
PopulationsCode PP1P2P3P4P5P6P7
Ain KorraAK--1.14 ± 0.629.20 ± 4.45 a89.50 ± 4.98 a3.15 ± 1.79 ab-
AmlayAM---9.32 ± 3.72 a76.32 ± 5.29 a13.57 ± 6.08 ab0.08 ± 0.00
Ben IdderBN---9.87 ± 2.34 a80.13 ± 1.62 a10.00 ± 2.21 ab-
BobiyineBO1.23 ± 0.211.18 ± 0.251.77 ± 0.388.64 ± 1.95 a83.83 ± 3.23 a3.362 ± 0.56 a-
BouztateBZ-0.73 ± 0.012.24 ± 0.0413.16 ± 3.32 a81.16 ± 2.79 a2.71 ± 0.86 ab-
KhezanaKH---12.80 ± 6.85 a71.00 ± 4.12 a16.20 ± 4.92 ab-
Oued LakhemisOL1.42 ± 0.000.71 ± 0.010.66 ± 0.013.16 ± 3.15 a79.82 ± 5.02 a14.22 ± 5.22 ab-
SiouanaSO1.67 ± 0.161.26 ± 0.022.63 ± 0.667.64 ± 0.72 a83.60 ± 0.96 a3.20 ± 0.77 ab-
TanghayaTN---11.20 ± 4.04 a81.31 ± 3.56 a7.49 ± 2.37 ab-
TayenzaTY--1.74 ± 0.3114.66 ± 3.42 a78.32 ± 2.71 a5.29 ± 1.92 ab-
TifouzalTF0.72 ± 0.010.72 ± 0.011.65 ± 0.476.10 ± 2.39 a70.60 ± 4.59 a20.21 ± 6.04 c-
Mean 0.46 ± 0.290.42 ± 0.221.08 ± 0.469.61 ± 3.7179.33 ± 4.089.04 ± 3.980.08 ± 0.00
ANOVAinter F10, 99 ---0.04 n.s.0.27 n.s.0.01 *-
Code P = abbreviation of population’s name, P1: 1 aperture; P2: 2 apertures; P3: 3 apertures; P4: 4 apertures; P5: 5 apertures; P6: 6 apertures; P7: 7 apertures. Means are given with a confidence interval of p = 0.05. F: variance ratio of the variance. df: degree of freedom. n.s: not statistically significant. * Significant effect at p < 0.05. Values with the same suffix (a,b) are not statistically significantly different at p < 0.05 in Tukey’s HSD.

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Ijpb 14 00059 g001
Figure 1. Location of the study area and sampled populations. See Table 1 for the populations’ abbreviations.
Figure 1. Location of the study area and sampled populations. See Table 1 for the populations’ abbreviations.
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Figure 2. The hierarchical sampling design used in this study (11 populations, 10 trees per population, and 30 grains of pollen per tree).
Figure 2. The hierarchical sampling design used in this study (11 populations, 10 trees per population, and 30 grains of pollen per tree).
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Figure 3. Observation of Alnus glutinosa pollen with a light microscope. (a) Polar view of pollen grain with 5 apertures; (b) equatorial view; (c) pollen grain with 4 apertures; (d) pollen grain with 6 apertures; (e) pollen grain with 7 apertures.
Figure 3. Observation of Alnus glutinosa pollen with a light microscope. (a) Polar view of pollen grain with 5 apertures; (b) equatorial view; (c) pollen grain with 4 apertures; (d) pollen grain with 6 apertures; (e) pollen grain with 7 apertures.
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Figure 4. Observation of Alnus glutinosa pollen with a scanning electron microscope: (a) general view of the pollen; (b) pollen grain with 5 apertures; (c) pollen grain with 4 apertures; (d) annulus and arcus; (e) aperture with f1—ectoaperture; f2—endoaperture.
Figure 4. Observation of Alnus glutinosa pollen with a scanning electron microscope: (a) general view of the pollen; (b) pollen grain with 5 apertures; (c) pollen grain with 4 apertures; (d) annulus and arcus; (e) aperture with f1—ectoaperture; f2—endoaperture.
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Figure 5. Pearson’s correlations between studied pollen morphology parameters. ** p < 0.001.
Figure 5. Pearson’s correlations between studied pollen morphology parameters. ** p < 0.001.
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Figure 6. Variability in the number of Alnus glutinosa apertures. P1: 1 aperture; P2: 2 apertures; P3: 3 apertures; P4: 4 apertures; P5: 5 apertures; P6: 6 apertures; P7: 7 apertures.
Figure 6. Variability in the number of Alnus glutinosa apertures. P1: 1 aperture; P2: 2 apertures; P3: 3 apertures; P4: 4 apertures; P5: 5 apertures; P6: 6 apertures; P7: 7 apertures.
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Table 1. Variability of pollen diameters in Moroccan populations of Alnus glutinosa. Code P = abbreviation of a population’s name.
Table 1. Variability of pollen diameters in Moroccan populations of Alnus glutinosa. Code P = abbreviation of a population’s name.
Populations (P)Code PPolar Diameter (P) (µm)Equatorial Diameter (E) (µm)P/E
Mean ± CICV (%)ANOVAIntra F9290Mean ± CICV (%)ANOVAIntra F9290Mean ± CICV
(%)
Ain KorraAK19.09 ± 0.62 d,e9.1320.36 ***26.64 ± 0.73 c7.6813.83 ***0.71 ± 0.01 a4.64
AmlayAM19.66 ± 0.69 f9.7631.81 ***26.76 ± 0.69 d,e7.1810.06 ***0.73 ± 0.01 a4.54
Beni IdderBN18.26 ± 0.36 a,b9.539.22 ***26.41 ± 0.76 c,d8.0926.22 ***0.69 ± 0.01 a4.8
BobiyineBO18.95 ± 0.69 d10.1917.41 ***27.31 ± 0.71 e,f7.299.45 ***0.69 ± 0.01 a5
BouztateBZ18.16 ± 0.67 a10.3423.24 ***25.75 ± 0.69 b,c,d7.5422.62 ***0.70 ± 0.01 a4.98
KhezanaKH18.08 ± 0.62 a9.6128.25 ***24.77 ± 0.70 a7.919.47 ***0.73 ± 0.01 a4.55
Oued LakhemisOL18.69 ± 0.75 b,c,d11.2819.31 ***26.54 ± 1.32 c13.947.85 ***0.70 ± 0.01 a3.94
SiouanaSO18.45 ± 0.65 a,b,c9.884.47 ***26.30 ± 0.65 b,c,d6.8913.32 ***0.70 ± 0.01 a4.74
TanghayaTN18.80 ± 0.61 c,d911.42 ***26.17 ± 0.71 b,c,d7.679.88 ***0.72 ± 0.01 a4.63
TayenzaTY18.75 ± 0.63 b,c,d9.3612.27 ***26.60 ± 0.70 c,d7.337.88 ***0.70 ± 0.01 a4.72
TifouzalTF19.46 ± 0.62 e,f8.8513.24 ***27.37 ± 0.71 f7.288.877 ***0.71 ± 0.01 a4.68
Mean 18.75 ± 0.629.72 26.42 ± 0.768.07 0.73 ± 0.014.2
ANOVAInter F10, 3239 23.29 ***31.22 ***1.23 n.s.
CI: Confidence interval at p = 0.05; CV (%): coefficient of variation; F: ratio of variances; n.s: not statistically significant. *** p < 0.001. Values with the same suffix (a,b,c,d,e and f) are not statistically significantly different at p < 0.05 in Tukey’s HSD post-hoc tests. ANOVAInter: ANOVA between different populations. ANOVAintra: ANOVA between different trees of the same population.
Table 2. Estimated percentage variance across hierarchical levels and nested ANOVA results.
Table 2. Estimated percentage variance across hierarchical levels and nested ANOVA results.
Polar Diameter (P)Equatorial Diameter (E)
Variance Decomposition (%)
Interpopulation variance6.923.85
Intrapopulation variance24.3631.49
Intraindividual variance59.1655.53
Residual9.539.14
Nested ANOVA
Interpopulation F10,992.16 ***2.36 ***
Intrapopulation F99, 313115.31 ***11.39 ***
F: ratio of variances. Numbers in brackets are degree of freedom. *** significant at p < 0.001.
Table 3. Variability in the number of apertures in the pollen of Alnus glutinosa. P4: 4 apertures; P5: 5 apertures; P6: 6 apertures. Means are given with a confidence interval of p = 0.05.
Table 3. Variability in the number of apertures in the pollen of Alnus glutinosa. P4: 4 apertures; P5: 5 apertures; P6: 6 apertures. Means are given with a confidence interval of p = 0.05.
P4P5P6
PopulationsCode pMeanMin-MaxCV%MeanMin-MaxCV%MeanMin-MaxCV%
Ain KorraAK9.20 ± 4.45 a1.6–22.0169.2789.50 ± 4.98 a77.06–97.67.433.15 ± 1.79 ab0.76–15.26145.44
AmlayAM9.32 ± 3.72 a0–30.92122.0076.32 ± 5.29 a55.92–97.8418.4213.57 ± 6.08 ab0–42.10135.77
Ben IdderBN9.87 ± 2.34 a0 -18.97137.4180.13 ± 1.62 a81.02 -1006.3610.00 ± 2.21 ab0–14.49119.95
BobiyineBO8.64 ± 1.95 a2.94–19.0162.0383.83 ± 3.23 a76.05-93.076.603.362 ± 0.56 a0–5.1579.13
BouztateBZ13.16 ± 3.32 a5.64–30.1163.0081.16 ± 2.79 a66.94–90.6410.502.71 ± 0.86 ab0–7.3486.10
KhezanaKH12.80 ± 6.85 a0–45.34123.5071.00 ± 4.12 a54.65–98.3319.7516.20 ± 4.92 ab0–36.84138.70
Oued LakhemisOL3.16 ± 3.15 a0 -7.09179.6779.82 ± 5.02 a49.69–94.0216.2414.22 ± 5.22 ab2.58–50.30100.24
SiouanaSO7.64 ± 0.72 a0–42.85185.3983.60 ± 0.96 a46.42–97.116.863.20 ± 0.77 ab0–6.2872.17
TanghayaTN11.20 ± 4.04 a2.08–39.13100.7381.31 ± 3.56 a60.86–92.9612.007.49 ± 2.37 ab0–21.18110.93
TayenzaTY14.66 ± 3.42 a0.71–30.6669.4678.32 ± 2.71 a68.66–9410.135.29 ± 1.92 ab0–16.54147.15
TifouzalTF6.10 ± 2.39 a0–17.51131.1370.60 ± 4.59 a54.26–96.5517.5120.21 ± 6.04 c0–44.96105.26
Mean 9.61 ± 3.710–45.34114.3879.33 ± 4.0846.42–10013.719.04 ± 3.980–50.30146.97
ANOVAinter F10, 99 0.04 n.s 0.27 n.s 0.01 *
Values with the same suffix (a,b,c) are not statistically significantly different at p < 0.05 in Tukey’s HSD post-hoc tests. F: ratio of variances. *: significant effect at p < 0.05. n.s: not statistically significant. ANOVAInter: ANOVA test between different populations.
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Sahli, A.; Kassout, J.; Boselli, V.A.; Ennouni, H.; Chakkour, S.; Kadaoui, K.; Houssni, M.; Ater, M. Pollen Variability of Alnus glutinosa (L.) Gaerth. (Betulaceae) from Southern Range Edge Populations in Northern Morocco. Int. J. Plant Biol. 2023, 14, 797-810. https://0-doi-org.brum.beds.ac.uk/10.3390/ijpb14030059

AMA Style

Sahli A, Kassout J, Boselli VA, Ennouni H, Chakkour S, Kadaoui K, Houssni M, Ater M. Pollen Variability of Alnus glutinosa (L.) Gaerth. (Betulaceae) from Southern Range Edge Populations in Northern Morocco. International Journal of Plant Biology. 2023; 14(3):797-810. https://0-doi-org.brum.beds.ac.uk/10.3390/ijpb14030059

Chicago/Turabian Style

Sahli, Abdelouahab, Jalal Kassout, Vladimiro Andrea Boselli, Hassan Ennouni, Soufian Chakkour, Khalil Kadaoui, Mhammad Houssni, and Mohammed Ater. 2023. "Pollen Variability of Alnus glutinosa (L.) Gaerth. (Betulaceae) from Southern Range Edge Populations in Northern Morocco" International Journal of Plant Biology 14, no. 3: 797-810. https://0-doi-org.brum.beds.ac.uk/10.3390/ijpb14030059

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