239
Key words: Beteae, LM, 
palynomorphology, sculpture,  
SEM, structure, UPGMA.
Ključne besede: Beteae, svetlobni 
mikroskop, palinomorfologija, 
skulptura, vrstični elektronski 
mikroskop, struktura, UPGMA.
Corresponding author:
Daniella Ivanova
E-mail: dani@bio.bas.bg
Received: 16. 7. 2023
Accepted: 21. 2. 2024
Comparative morphometric and morphological 
study of the pollen of Beta trigyna, 
B. vulgaris and B. vulgaris subsp. maritima 
(Chenopodiaceae/Amaranthaceae sensu APG IV)
Abstract
Pollen morphology of Beta trigyna, B. vulgaris and B. vulgaris subsp. maritima, 
last of those studied for the first time, was investigated using light and scanning 
electron microscopy, based on 10 herbarium specimens. The aim of the study 
was to provide detailed data on the pollen characteristics of these taxa to identify 
similarities and differences between them. Pollen grains are pantoporate, 
spheroidal, circular in outline; small- and medium-sized. Exine sculpture 
is nanoechinate, tectum is psilate or psilate-perforate. Pore membranes are 
nanoechinate. Diagnostic relevance of the characters of pollen grains is discussed 
(pollen and pore diameters, distance between pores and between pore centres, 
nanoechini size and density, number of nanoechini on pore membranes, structure 
of columellae). UPGMA dendrograms based on palynological data support the 
differentiation of B. trigyna (section Corollinae), B. vulgaris and B. vulgaris subsp. 
maritima (section Beta). The obtained characteristics of pollen grains of Beta 
species can be used in spore-pollen analysis, especially in identifying the impact of 
human economic activity in the past.
Izvleček
S svetlobnim in vrstičnim elektronskim mikroskopom smo na 10 herbarijskih 
primerkih proučevali morfologijo peloda vrst Beta trigyna, B. vulgaris in B. vulgaris 
subsp. maritima, slednja je proučevana prvič. Namen raziskave je bil pridobiti 
natančne podatke o značilnostih peloda teh taksonov in izpostaviti podobnosti 
in razlike med njimi. Pelodna zrna so pantoporatna, sferoidna in okrogle oblike, 
majhna do srednje velika. Eksina je nanoehinatna, tektum je psilaten ari psilaten-
perforaten. Membrane por so nanoehinatne. Obravnavali smo diagnostični pomen 
lastnosti pelodnih zrn (premere peloda in por, razdaljo med porami in središči 
por, velikost in gostoto nanoehinijev na membranah por, zgradbo kolumel). 
Z Dendrogrami UPGMA na osnovi palinoloških podatkov so potrdili razlike med 
vrstami B. trigyna (section Corollinae), B. vulgaris in B. vulgaris subsp. maritima 
(section Beta). Dobljene lastnosti pelodnih zrn vrst rodu Beta lahko uporabimo 
pri analizah spor in pelodnih analizah, predvsem pri ugotavljanju vpliva človekove 
gospodarske aktivnosti v preteklosti.
Zoya M. Tsymbalyuk1, Daniella Ivanova2 & Lyudmila M. Nitsenko1
1 Department of Systematics and Floristics of Vascular Plants, M.G. Kholodny Institute of Botany, National Academy of Sciences of Ukraine, Kyiv, Ukraine.
2 Department of Plant and Fungal Diversity and Resources, Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, Sofia, Bulgaria.
DOI: 10.2478/hacq-2023-001023/2 • 2024, 239–252
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Comparative morphometric and morphological study of the pollen of Beta taxa
Introduction
Beta L. belongs to the tribe Beteae (Betoideae, Chenopodi-
aceae/Amaranthaceae sensu APG IV), and comprises 9–10 
species and an uncertain number of subspecies or varieties, 
which are mainly included in B. vulgaris L. (Iamonico, 
2019). Wild representatives of the genus are annual, 
biennial and perennial herbaceous plants occurring from 
the Atlantic coast of Europe, Macaronesia, Eastern Europe 
and the Mediterranean Region to West and South Asia 
including Eastern India and Bangladesh  (Ford-Lloyd & 
Williams, 1975; Ball & Akeroyd, 1993; Kadereit et al., 
2006; Iamonico, 2019; POWO, 2023). In the flora of 
Ukraine and Bulgaria the genus is represented by the taxa 
B. trigyna Waldst. & Kit., B. vulgaris, and B. vulgaris subsp. 
maritima (L.) Arcang. (Iljin, 1952; Jordanov & Kuzmanov, 
1966; Mosyakin & Fedoronchuk, 1999; Yena & Yevseyen-
kov, 2010). Beta vulgaris is a biennial or perennial plant; its 
native range is in the Azores, Western Europe and Eastern 
Europe, the Mediterranean Region and eastwards to In-
dia (Ford-Lloyd & Williams, 1975; POWO, 2023). This 
species is of great economic importance as a sugar crop, 
vegetable and fodder plant. Beta vulgaris is also used as 
medicinal and ornamental plant (Ford-Lloyd & Williams, 
1975; POWO, 2023). The perennial sea beat B. vulgaris 
subsp. maritima (syn.: B. maritima L.) is widespread and 
native to Macaronesia, Western and Eastern Europe, the 
Mediterranean Region, the Middle East and extends to 
India; mainly in maritime locations along the seashores, 
but inland populations also occur (Ford-Lloyd & Wil-
liams, 1975; Letschert, 1994; Stevenato et al., 2001; Bi-
ancardi et al., 2012; Richards et al., 2014; Van Dijk & 
Hautekèete, 2014). Beta vulgaris subsp. maritima has the 
Mediterranean as its centre of diversity and, most likely, 
centre of domestication (Richards et al., 2014). It is esti-
mated to be the wild progenitor of cultivated beet; it is also 
considered the most important wild source of genetic di-
versity useful in improvement of cultivated beet, especially 
sugar beet (Richards et al., 2014; Stevanato et al., 2001). 
The native range of the perennial species B. trigyna is SE 
Europe to Iran and Turkmenistan (Ford-Lloyd & Wil-
liams, 1975; Kadereit et al., 2006; POWO, 2023). 
The most comprehensive taxonomic treatment of the 
genus Beta was published by Iamonico (2019). Molecular 
phylogenetic studies of the genus were carried out by Shen 
et al. (1998), Hohmann et al. (2006), and Kadereit et al. 
(2006). Beta vulgaris and B. vulgaris subsp. maritima are 
included in the section Beta, and B. trigyna is included in 
the section Corollinae (Tranzschel) Ulbr. (Kadereit et al., 
2006; Iamonico, 2019). The first two taxa are diploids 
with 2n = 18 chromosomes; but B. trigyna is a hexaploid 
with 2n = 54 (see e.g., Queirós, 1975; Česchmedjiev, 
1976; Pastor et al., 1988; Ball & Akeroyd, 1993; Dempsey 
et al., 1994; Runemark, 1996, etc.). According to the lit-
erature, some Beta taxa are problematic and need further 
revision (Kadereit et al., 2006; Iamonico, 2019).
The palynomorphological characters are often used as 
additional diagnostic features in the taxonomy (Celenk 
et al., 2008; Albach et al., 2021; Tsymbalyuk et al., 2021, 
2022a, 2022b; El Ghazali, 2022) as well as for spore-pol-
len analysis in the paleopalynology (Monoszon, 1973; Be-
zusko et al., 2003, 2023; Tsymbalyuk et al., 2005; Lewan-
dowska et al., 2023). Many authors studied and discussed 
the pollen morphology of B. trigyna or B. vulgaris using 
light, scanning and/or transmission electron microscopy 
(Tsukada, 1967; Monoszon, 1973; Nowicke, 1975; Skvar-
la & Nowicke, 1976; Kupriyanova & Alyoshina, 1972; 
Nowicke & Skvarla, 1979; Tsymbalyuk, 2005, 2008; Ts-
ymbalyuk et al., 2005; Angelini et al. 2014). Despite the 
relatively numerous publications, the knowledge about 
the morphology of pollen grains in B. trigyna and B. vul­
garis are fragmentary because the available descriptions 
usually have only briefly addressed the pollen morphology 
or researchers have analysed a few selected pollen features. 
Palynomorphological investigation of B. trigyna, B. vul­
garis and B. vulgaris subsp. maritima taxa was carried out 
using light and scanning electron microscopy in order to 
provide detailed quantitative and qualitative data on their 
pollen characteristics to identify similarities and differ-
ences between them.
Materials and methods 
In total, pollen grains of 10 specimens belonging to 
B. trigyna, B. vulgaris and B.  vulgaris subsp. maritima 
(henceforth B. maritima) taxa were sampled in the Na-
tional Herbarium of Ukraine (KW – herbarium of the 
M.G. Kholodny Institute of Botany, National Academy 
of Sciences of Ukraine, Kyiv; the herbarium acronym is 
given according to Thiers (2023 [continuously updated]). 
The methods used in the present study have been 
described in details earlier (Tsymbalyuk et al., 2023a, 
2023b). Pollen morphology was studied using both light 
microscopy (LM) and scanning electron microscopy 
(SEM). For LM studies (Biolar ×700), the pollen was 
acetolysed following Erdtman (1952), mounted on slides 
with glycerinated gelatin, analysed, and photomicro-
graphed. Pollen morphometric features of 30 properly de-
veloped pollen grains from each specimen were measured, 
and the measurements included the following parameters: 
pollen diameter, pore diameter, distance between pores, 
exine thickness. The distance between pore centres and 
C/D value (C – pollen diameter, D – distance between 
pore centres) were calculated (McAndrews & Swanson, 
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Comparative morphometric and morphological study of the pollen of Beta taxa
1967). The number of pores was calculated by multiply-
ing the number of pores visible on the surface by two 
and adding the number of pores at the edge of the pollen 
grain. For all quantitative characters, descriptive statistics 
was applied and the range (minimum–maximum), arith-
metic mean and standard deviation were calculated using 
Microsoft Excel software. The slides were deposited in the 
Palynotheca (reference pollen collection) at the National 
Herbarium of Ukraine (Bezusko & Tsymbalyuk, 2011). 
For SEM studies (JEOL JSM-6060LA), dry and aceto-
lysed pollen grains were treated with 96%-ethanol, then the 
samples were sputter-coated with gold and investigated at 
the Centre of Electron Microscopy of the M.G. Kholodny 
Institute of Botany. The measurements of the nanoechini 
and columellae were taken on 5–8 pollen grains from each 
specimen from SEM micrographs and made using the pro-
gram AxioVision Rel.4.8.2. The numbers of nanoechini 
per unit area (4 µm²) and on pore membranes were deter-
mined. Terminology used in descriptions of pollen grains 
follows mainly the glossaries of Punt et al. (2007) and Hal-
britter et al. (2018). Abbreviations of taxon author names 
follow Brummitt & Powell (1992), with additions avail-
able from the continuously updated International Plant 
Names Index (IPNI, 2023) and from POWO (2023). 
Cluster analysis was carried out to determine the phe-
netic similarities among the investigated taxa. Thirteen 
quantitative characters were examined: pollen and pore di-
ameter, distance between pores and between pore centres, 
pore number, C/D value, and exine thickness (Table 1); 
nanoechini: height, width at the base, number/4  µm², 
number on pore membranes; columellae: height and 
thickness (Table 2). Cluster analysis was carried out using 
the unweighted pair group method with arithmetic mean 
(UPGMA). The Euclidean distance was used as a simi-
larity index in clustering analyses. PAST (PAleontologi-
cal STatistics) v. 4.08 was used for the analysis (Hammer 
et al., 2001). The variability of the characters has been 
examined by Box plots.
Taxon Pollen  
diameter
Pore  
diameter
Distance be-
tween pores
Distance between 
pore centres
Pore  
number
C/D Exine 
thickness
Beta trigyna 1 28.46±2.04
25.27–33.25
3.83±0.46
2.66–5.05
3.29±0.54
2.66–4.65
7.13±0.86
5.32–9.04
30.13±2.06
28–35
0.25±0.03
0.19–0.30
2.62±0.09
2.39–2.79
Beta trigyna 2 27.66±2.07
23.94–31.92
3.87±0.52
2.66–5.32
3.48±0.48
2.66–3.99
7.35±0.84
5.32–9.31
28.90±2.19
26–34
0.26±0.02
0.22–0.31
2.57±0.23
2.39–3.32
Beta trigyna 3 26.82±1.09
23.94–29.26
4.94±0.81
3.99–6.65
3.58±0.48
2.66–4.65
8.52±0.94
6.65–9.97
24.93±1.63
22–29
0.31±0.03
0.25–0.38
2.51±0.13
2.26–2.66
Beta trigyna G 27.64±1.91
23.94–33.25
4.21±0.80
2.66–6.65
3.45±0.51
2.66–4.65
7.67±1.07
5.32–9.97
27.98±2.97
22–35
0.27±0.04
0.19–0.38
2.57±0.17
2.26–3.32
Beta vulgaris 1 19.28±0.89
17.29–21.28
2.35±0.31
1.99–3.32
2.24±0.24
1.99–2.66
4.60±0.42
3.99–5.71
29.76±1.54
26–32
0.23±0.01
0.20–0.29
2.38±0.16
1.99–2.66
Beta vulgaris 2 22.52±2.05
18.62–26.60
3.09±0.72
1.99–4.65
2.74±0.45
2.39–3.99
5.83±1.08
4.38–8.37
26.13±2.15
23–32
0.25±0.03
0.20–0.33
2.44±0.22
1.99–2.92
Beta vulgaris 3 18.70±0.90
17.29–19.95
2.39±0.23
1.99–2.66
2.42±0.15
2.26–2.66
4.81±0.32
4.25–5.32
27.26±1.48
26–32
0.25±0.01
0.22–0.29
2.44±0.12
2.26–2.66
Beta vulgaris G 20.17±2.18
17.29–26.60
2.61±0.58
1.99–4.65
2.47±0.37
1.99–3.99
5.08±0.88
3.99–8.37
27.72±2.31
23–32
0.25±0.02
0.20–0.33
2.42±0.17
1.99–2.92
Beta maritima 1 21.13±1.34
18.62–23.94
2.79±0.40
2.39–3.99
2.76±0.36
2.39–3.99
5.55±0.65
4.78–7.44
27.07±3.25
24–32
0.26±0.03
0.22–0.36
2.34±0.22
1.99–2.66
Beta maritima 2 19.99±0.93
18.62–22.61
2.50±0.13
2.39–2.66
2.45±0.23
1.99–2.79
4.96±0.31
4.38–5.45
31.76±2.29
28–36
0.24±0.01
0.22–0.28
2.28±0.18
1.99–2.66
Beta maritima 3 18.66±1.00
17.29–19.95
2.35±0.29
1.59–2.66
2.39±0.16
1.99–2.66
4.74±0.39
3.59–5.32
28.26±2.06
25–32
0.25±0.01
0.20–0.28
1.70±0.21
1.33–1.99
Beta maritima 4 20.33±1.45
18.62–23.94
2.61±0.35
1.99–3.32
2.37±0.20
1.99–2.66
4.99±0.41
4.12–5.71
33.85±2.69
29–39
0.24±0.02
0.19–0.28
2.23±0.18
1.99–2.66
Beta maritima G 20.00±1.49
17.29–23.94
2.56±0.34
1.59–3.99
2.49±0.29
1.99–3.99
5.05±0.54
3.59–7.44
30.23±3.73
24–39
0.25±0.02
0.19–0.36
2.13±0.33
1.33–2.66
Table 1: Pollen morphometric characters (using LM): the values are presented as Mean ± Standard deviation and Range 
(minimum-maximum) (all measurements given as µm); 1, 2, 3, 4 – specimen number; G – general specimens’ measurements; 
C – pollen diameter, D – distance between pore centres.
Tabela 1: Morfološke značilnosti peloda (z uporabo LM): vrednosti predstavljajo povprečje ± standardna deviacija in rang 
(minimum-maksimum) (vse meritve so v µm); 1, 2, 3, 4 – številka primerka; G – glavne meritve primerkov; C – premer peloda, 
D – razdalja med središčem pore.
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Results
The original data on quantitative pollen characters used 
in this study are summarised in Tables 1, 2. LM and SEM 
photomicrographs of pollen grains are shown in Fig-
ures 1–4. UPGMA dendrograms showing the relationships 
of pollen grains of studied taxa are presented in Figure 5. 
Box plots illustrating the variation in pollen diameter, pore 
diameter, distance between pores and pore centres, pore 
number, and exine thickness of B. trigyna, B. vulgaris and 
B. maritima pollen grains are shown in Figure 6.
Description of pollen grains 
Beta trigyna (Figures 1a–h; 2a, b; 3a, b; 4a–c)
LM. Pollen grains monads, isopolar, spheroidal, cir-
cular in outline, slightly undulated or undulated on 
the edge; medium-sized: P (Polar axis) = E (Equatorial 
diameter) = 23.94–33.25 µm; pantoporate, with 22–35 
pores evenly distributed on the surface. Pores circular, 
2.66–6.65 µm in diameter, with distinct or indistinct 
margins. Distance between pores 2.66–4.65 µm, between 
pore centres – 5.32–9.97 µm. C/D = 0.190–0.388. Exine 
2.26–3.32 µm thick (Table 1). Sexine thicker than nex-
ine. Columellae distinct or indistinct. LO-analysis: colu-
mellae distinct, circular, densely distributed, nanoechini 
indistinct or invisible.
Figure 1: Pollen grains of Beta (LM): a–h – B. trigyna (a–d – speci-
men 2, Ukraine, e–h – specimen 3, Turkey), i–p – B. vulgaris (i, j – 
specimen 1, Ukraine, k, l – specimen 2, Ukraine, m–p – specimen 3, 
India), q–x – B. vulgaris subsp. maritima (q–t – specimen 1, France, 
u – specimen 4, Egypt, v – specimen 3, France, w, x – specimen 2, 
India). Scale bars = 10 µm. →
Slika 1: Pelodna zrna vrst rodu Beta (LM): a–h – B. trigyna (a–d – 
primerek 2, Ukrajina, e–h – primerek 3, Turčija), i–p – B. vulgaris 
(i, j – primerek 1, Ukrajina, k, l – primerek 2, Ukrajina, m–p – 
primerek 3, Indija), q–x – B. vulgaris subsp. maritima (q–t – 
primerek 1, Francija, u – primerek 4, Egipt, v – primerek 3, Francija, 
w, x – primerek 2, Indija). Merilo = 10 µm.  →
Taxon
Nanoechini (SEM) Columellae (SEM)
Height Width  
at the base
Number/4 µm² Number on  
pore membranes
Height Thickness
Beta trigyna 1 0.14±0.04
0.08–0.22
0.23±0.03
0.18–0.30
9.27±1.21
7–11
16.61±2.92
13–22
0.62±0.06
0.53–0.73
0.30±0.03
0.23–0.36
Beta trigyna 2 0.12±0.04
0.06–0.22
0.21±0.03
0.16–0.28
7.94±1.60
6–12
17.41±2.67
14–22
0.66±0.04
0.58–0.74
0.31±0.03
0.25–0.36
Beta trigyna 3 0.13±0.03
0.07–0.20
0.23±0.03
0.18–0.30
8.66±1.94
6–12
20.12±3.62
15–27
0.75±0.09
0.57–0.88
0.31±0.06
0.22–0.43
Beta trigyna G 0.13±0.04
0.06–0.22
0.22±0.03
0.16–0.30
8.48±1.69
6–12
17.91±3.34
13–27
0.71±0.10
0.53–0.88
0.31±0.05
0.22–0.43
Beta vulgaris 1 0.09±0.01
0.07–0.12
0.15±0.02
0.13–0.21
14.12±1.36
12–16
9.12±1.26
8–12
0.54±0.06
0.45–0.63
0.19±0.02
0.16–0.23
Beta vulgaris 2 0.10±0.02
0.06–0.14
0.17±0.02
0.13–0.21
11.04±1.60
9–15
13.82±2.60
8–17
0.52±0.04
0.45–0.61
0.20±0.01
0.18–0.23
Beta vulgaris 3 0.10±0.02
0.07–0.13
0.16±0.02
0.13–0.21
13.18±1.69
10–16
11.17±1.61
9–15
0.55±0.05
0.45–0.63
0.19±0.01
0.17–0.22
Beta vulgaris G 0.09±0.02
0.06–0.14
0.16±0.02
0.13–0.21
12.21±2.05
9–16
11.87±2.88
8–17
0.54±0.05
0.45–0.63
0.19±0.01
0.16–0.23
Beta maritima1 0.09±0.02
0.05–0.14
0.18±0.03
0.12–0.24
12.07±1.57
9–15
13.00±2.33
10–17
0.47±0.05
0.41–0.58
0.17±0.01
0.15–0.21
Beta maritima 2 0.09±0.02
0.05–0.15
0.17±0.03
0.11–0.24
12.39±1.58
10–15
11.40±2.48
7–16
0.42±0.04
0.35–0.53
0.20±0.02
0.16–0.25
Beta maritima 3 0.09±0.02
0.05–0.14
0.17±0.03
0.12–0.24
14.11±1.60
12–17
10.95±2.69
6–15
0.48±0.08
0.35–0.59
0.21±0.02
0.18–0.26
Beta maritima 4 0.10±0.03
0.05–0.15
0.18±0.02
0.12–0.23
12.36±1.49
9–15
9.18±1.78
6–12
0.45±0.04
0.38–0.55
0.18±0.01
0.17–0.21
Beta maritima G 0.09±0.02
0.05–0.15
0.18±0.03
0.11–0.24
12.67±1.71
9–17
10.92±2.69
6–17
0.46±0.06
0.35–0.59
0.20±0.02
0.15–0.26
Table 2: Pollen morphometric characters (using SEM): the values are presented as Mean ± Standard deviation and Range (all 
measurements given as µm); 1, 2, 3, 4 – specimen number; G – general specimens’ measurements.
Tabela 2: Morfološke značilnosti peloda (z uporabo SEM): vrednosti predstavljajo povprečje ± standardna deviacija in rang 
(minimum-maksimum) (vse meritve so v µm); 1, 2, 3, 4 – številka primerka; G – glavne meritve primerkov.
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Figure 1 
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SEM. Exine sculpture nanoechinate; nanoechini conic 
with straight sides and acute apex, 0.06–0.22 µm high, 
0.16–0.30 µm wide at base, sparsely or more densely 
distributed (6–12/4 µm²); tectum psilate-perforate in 
areas between nanoechini. Pore membranes with nanoe-
chini (in number 13–27), pores’ margin raised or sunken; 
mesoporia mainly flattened or rarely convex. Columellae 
medium-length or long, 0.57–0.88 µm long, thick, 0.22–
0.43 µm wide, densely or sparsely arranged (Table 2).
Specimens investigated: 1. Crimea, Yayla, Ai-Petri. 
Rocky slope, in a funnel. 25 July 1974. O. Dubovik (KW). 
2. Crimea, Belogorsk District, Belaya Skala village, along 
the Biyuk-Karasu River. 8 June 1978. O. Dubovik (KW). 
3. Turkey. Ex Herb. Hort. Bot. Reg. Kew. Prov. Erzurum: 
Kop Dag Pass: weed; alt. 9000 ft. 9 August 1962. Coll. 
P. Furse 3484 (KW). 
Beta vulgaris (Figures 1i–p; 2c, d; 3c, d; 4d–f )
LM. Pollen grains monads, isopolar, spheroidal, cir-
cular in outline, slightly undulated or undulated on the 
edge; small and medium-sized: P = E = 17.29–26.60 µm; 
pantoporate, with 23–32 pores evenly distributed on the 
surface. Pores circular, 1.99–4.65 µm in diameter, with 
indistinct or distinct margins. Distance between pores 
1.99–3.99 µm, between pore centres – 3.99–8.37 µm. 
C/D = 0.200–0.331. Exine 1.99–2.92 µm thick (Ta-
ble 1). Sexine thicker than nexine. Columellae indis-
tinct or invisible. LO-analysis: columellae indistinct or 
rarely distinct, circular, densely distributed, nanoechini 
 invisible. 
SEM. Exine sculpture nanoechinate; nanoechini conic 
with straight sides and acute apex, 0.06–0.14 µm high, 
0.13–0.21 µm wide at base, sparsely or more densely dis-
tributed (9–16/4 µm²); tectum psilate or psilate-perforate 
in areas between nanoechini. Pore membranes with na-
noechini (in number 8–17), pores’ margin sunken or 
raised; mesoporia mainly convex or rarely flattened. 
Columellae medium-length, 0.45–0.63 µm long, thin, 
0.16–0.23 µm wide, densely arranged (Table 2).
Specimens investigated: 1. [Ukraine] Donetsk Re-
gion, Makiivka, Novo-Kalynove village, gardens along 
the road to the mine. 30 June 1982. R.I. Burda, A.E. Kus­
kov (KW). 2. [Ukraine] Kozatske village in the Shevchen-
kiv region. Cultivated. July 1920. M. Pidoplichko (KW). 
3. [India] Delhi University Campus. 15 February 1957. 
Manahar Lal (KW).
Figure 2: Pollen grains of Beta (SEM): a, b – B. trigyna (a – specimen 1, Ukraine, dry pollen, b – specimen 3, Turkey, acetolysed pollen), 
c, d – B. vulgaris (c – specimen 1, Ukraine, dry pollen, d – specimen 3, India, dry pollen), e, f – B. vulgaris subsp. maritima (e – specimen 4, 
Egypt, dry pollen, f – specimen 4, Egypt, acetolysed pollen). Scale bars = 5 µm.
Slika 2: Pelodna zrna vrst rodu Beta (SEM): a, b – B. trigyna (a – primerek 1, Ukrajina, suh pelod, b – primerek 3, Turčija, acetoliziran pelod), 
c, d – B. vulgaris (c – primerek 1, Ukrajina, suh pelod, d – primerek 3, Indija, suh pelod), e, f – B. vulgaris subsp. maritima (e – primerek 4, Egipt, 
suh pelod, f – primerek 4, Egipt, acetoliziran pelod). Merilo = 5 µm. 
e fd
ca b
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Comparative morphometric and morphological study of the pollen of Beta taxa
Figure 3: Exine sculpture of pollen grains of Beta (SEM): a, b – B. trigyna (a – specimen 1, Ukraine, dry pollen, b – specimen 3, Turkey, acetolysed 
pollen), c, d – B. vulgaris (c – specimen 1, Ukraine, dry pollen, d – specimen 3, India, dry pollen), e, f – B. vulgaris subsp. maritima (e – specimen 
4, Egypt, dry pollen, f – specimen 2, India, dry pollen). Scale bars = 1 µm.
Slika 3: Eksina pelodnih zrn vrst rodu Beta (SEM): a, b – B. trigyna (a – primerek 1, Ukrajina, suh pelod, b – primerek 3, Turčija, acetoliziran 
pelod), c, d – B. vulgaris (c – primerek 1, Ukrajina, suh pelod, d – primerek 3, Indija, suh pelod), e, f – B. vulgaris subsp. maritima (e – primerek 4, 
Egipt, suh pelod, f – primerek 2, Indija, suh pelod). Merilo = 1 µm.
Beta maritima (= B. vulgaris subsp. maritima) (Figu-
res 1q–x; 2e, f; 3e, f; 4g–i)
LM. Pollen grains monads, isopolar, spheroidal, 
circular in outline, slightly undulated or undulated on the 
edge; small and medium-sized: P = E = 17.29–23.94 µm; 
pantoporate, with 24–39 pores evenly distributed on 
the surface. Pores circular, 1.59–3.99 µm in diameter, 
with indistinct or distinct margins. Distance between 
pores 1.99–3.99 µm, between pore centres – 3.59–
7.44 µm. C/D = 0.193–0.366. Exine 1.33–2.66 µm 
thick (Table 1). Sexine thicker than nexine. Columellae 
indistinct or invisible. LO-analysis: columellae indistinct 
or rarely distinct, circular, densely distributed, nanoechini 
invisible. 
SEM. Exine sculpture nanoechinate; nanoechini 
conic with straight sides and acute apex, 0.05–0.15 µm 
23/2 • 2024, 239–252
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Tsymbalyuk et al.
Comparative morphometric and morphological study of the pollen of Beta taxa
high, 0.11–0.24 µm wide at base, sparsely or more 
densely distributed (9–17/4µm²); tectum psilate or 
psilate-perforate in areas between nanoechini. Pore 
membranes with nanoechini (in number 6–17), pores’ 
margin sunken or raised; mesoporia mainly convex or 
rarely flattened. Columellae short and medium-length, 
0.35–0.59 µm long, thin, 0.15–0.26 µm wide, densely 
arranged (Table 2).
Specimens investigated: 1. France, Charente-Inféri-
eure [nowadays Charente-Maritime]. Pointe d’Yves, 
rocailles. 4 Juin 1929. Herbier J. Charrier (KW). 2. 
[India] Herb. Ind. Or. Hook. fil. F. Thomson. Hab. 
Punjab. Cult. Regio. hop. Coll. I.I. (KW-TURCZ: 
Turczaninow historical herbarium in Kyiv). 3. [France] 
Ajaccio – Corsica (KW-TURCZ). 4. [Egypt] prope 
Cahiram in pratis. Unio itiner. leg. Januario 1833. 
Dr. A. Wiest 77 (KW-TURCZ).
Numerical analysis of the 
palynomorphological characters
Cluster analysis of all 10 studied specimens clearly dis-
tinguished the three specimens of B.  trigyna (Table 1; 
Figure 5a). The specimens with similar larger pollen di-
ameter, pore diameter, distance between pores and pore 
centres, number of pores, C/D value and exine thickness 
belonging to B. trigyna are placed into a separate branch. 
On the other hand, B.  vulgaris and B. maritima speci-
mens with the smallest measurements of pollen grain fea-
tures are placed in another branch (Figure 5a). In general, 
the variation range in the characteristics of pollen grains 
between the different specimens of B. trigyna is small (see 
Figure 6); no significant discontinuity within species was 
observed. The samples of B.  trigyna from Ukraine had 
most similar characters. However, an exception is the 
B. trigyna specimen collected in Turkey, which had larger 
Figure 4: Pores and exine structure of pollen grains of Beta (SEM): a–c – B. trigyna (a – specimen 1, Ukraine, dry pollen, b, c – specimen 3, 
Turkey, acetolysed pollen), d–f – B. vulgaris (d – specimen 1, Ukraine, dry pollen, e, f – specimen 3, India, acetolysed pollen), g–i – B. vulgaris 
subsp. maritima (g – specimen 2, India, dry pollen, h – specimen 2, India, acetolysed pollen, i – specimen 1, France, acetolysed pollen); a, b, d, e, 
g, h – pores, c, f, i – columellae. Scale bars = 1 µm.
Slika 4: Pore in struktura eksine pelodnih zrn vrst rodu Beta (SEM): a–c – B. trigyna (a – primerek 1, Ukrajina, suh pelod, b, c – primerek 3, 
Turčija, pelod v acetonu), d–f – B. vulgaris (d – primerek 1, Ukrajina, suh pelod, e, f – primerek 3, Indija, pelod v acetonu), g–i – B. vulgaris 
subsp. maritima (g – primerek 2, India, suh pelod, h – primerek 2, Indija, pelod v acetonu, i – primerek 1, Francija, pelod v acetonu); a, b, d, e, g, 
h – pore, c, f, i – kolumele. Merilo = 1 µm.
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Tsymbalyuk et al.
Comparative morphometric and morphological study of the pollen of Beta taxa
mean pore diameter, pore centre distance, C/D value, and 
pore number, which is also confirmed by the dendrogram 
(Figure 5a). Specimens with comparable average measure-
ments of pollen grain features, belonging to B.  vulgaris 
and B. maritima, are grouped together and placed in a 
separate branch (Figure 5a).
belonging to B. vulgaris and B. maritima, are grouped to-
gether and form a separate branch (Figure 5b). 
Discussion
In general, our data are in agreement with the results of 
previous LM studies (Tsukada, 1967; Kupriyanova & 
Alyoshina, 1972; Monoszon, 1973; Angelini et al., 2014). 
Pollen diameter – The pollen size range for B.  trigyna 
was given by Kupriyanova & Alyoshina (1972) as 25.2–
27.6  µm, and by Monoszon (1973) as 25.0–30.3  µm. 
Their data are close to our pollen diameter measure-
ments, although the range in our study is slightly larger. 
The pollen sizes for B. vulgaris were given by Monoszon 
(1973) as 16.0–18.3 µm. Tsukada (1967) presented only 
the mean pollen diameter of B. vulgaris as 19.5 µm. An-
gelini et al. (2014) reported pollen grain diameters for 
B. vulgaris ssp. cicla (L.) Schübl. & G.Martens (= B. vul­
garis var. cicla L.) [19.71 (18.48–20.02) µm], B. vulgaris 
var. rubra L. [20.08 (18.48–21.56) µm], and B. vulgaris 
var. altissima Döll (= B.  vulgaris subsp. vulgaris) [20.08 
(18.48–21.56) µm]. These reports are similar to those for 
B. vulgaris and B. maritima found in the current study 
(Table 1). 
Pore diameter – Kupriyanova & Alyoshina (1972) re-
ported B. trigyna pore diameter of 2.4–3.6 µm. Monoszon 
(1973) reported B.  trigyna pollen grains that had diam-
eter of pores of 3.5–4.0 µm, and those of B.  vulgaris – 
2.8–3.8 µm, which falls in the range of our data. Angelini 
et al. (2014) reported pollen grains of B. vulgaris ssp. cicla 
(2.31–3.08 µm), B.  vulgaris var. rubra (2.31–3.39 µm), 
and B. vulgaris var. altissima (2.31–3.08 µm), in which the 
diameter of pores is comparable to those of B. vulgaris and 
B. maritima reported in the current study (Table 1). 
Distance between pores – Kupriyanova & Alyoshina 
(1972) reported B. trigyna pollen grains that had distanc-
es between pores of 3.6–4.2 µm, which is in line with 
the values obtained in this study. Angelini et al. (2014) 
reported pollen grains of B. vulgaris ssp. cicla [2.52 (2.00–
3.08) µm], B. vulgaris var. rubra [2.78 (2.31–3.08) µm], 
and B.  vulgaris var. altissima [3.08 (2.77–3.85) µm], in 
which the distances between pores are comparable to 
those of B. vulgaris and B. maritima in the present study 
(Table 1).
Distance between pore centres – Monoszon (1973) re-
ported pollen grains with 7.6–9.0 µm distances between 
centres of pores in B. trigyna, and 4.0–5.1 µm in B. vul­
garis which is consistent with our data (Table 1).
Pore number – Kupriyanova & Alyoshina (1972) re-
ported a greater number of pores on pollen of B. trigyna 
(30–40) than the values found in our study. Monoszon 
(1973) reported pollen grains of B.  trigyna with 23–29 
Figure 5: UPGMA dendrograms showing the relationships of pollen 
grains of B. trigyna, B vulgaris and B. vulgaris subsp. maritima taxa:  
a – quantitative characters (see Table 1), b – quantitative characters 
(see Table 2).
Slika 5: UPGMA dendrogrami, ki prikazujejo podobnosti peloda med 
vrstami B. trigyna, B vulgaris in B. vulgaris subsp. maritima: a – kvanti-
tativni znaki (glej Tabelo 1), b – kvantitativni znaki (glej Tabelo 2).
Pollen samples from Ukrainian B. trigyna had the most 
similar nanoechini and columellae measurements and are 
clustered into one branch (Table 2; Figure 5b). However, 
pollen grains of the Turkish B. trigyna specimen had big-
ger nanoechini number on the pore membrane. But in 
general, as seen in the UPGMA dendrogram, B. trigyna 
has distinctive pollen morphometric features (larger 
nanoechini, more nanoechini on the pore membrane, 
sparse distribution of nanoechini on the surface, longer 
and thicker columellae) and is placed in a separate cluster 
(Figure 5b). Specimens with a similar number of nanoe-
chini per unit area, number of nanoechini distributed on 
pore membrane, and comparative size of the columellae, 
Single Linkage
Euclidean distances
a
Linkage Distances
b
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Comparative morphometric and morphological study of the pollen of Beta taxa
Figure 6: Box plots of Beta pollen grains: a – pollen diameter, b – pore diameter, c – distance between pore, d – distance between pore centres,  
e – pore number, f – exine thickness; 1–3 – B. trigyna, 4–6 – B. vulgaris, 7–10 – B. vulgaris subsp. maritima.
Slika 6: Škatle z brki pelodnih zrn vrst rodu Beta: a – premer peloda, b – premer pore, c – razdalja med porami, d – razdalja med središči por,  
e – število por, f – debelina eksine; 1–3 – B. trigyna, 4–6 – B. vulgaris, 7–10 – B. vulgaris subsp. maritima.
a b
c d
e f
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Tsymbalyuk et al.
Comparative morphometric and morphological study of the pollen of Beta taxa
pores and of B.  vulgaris with up to 30 pores. Tsukada 
(1967) reported a total number of 32–40 pores per grain 
for B. vulgaris. Possibly, the observed variation is due to 
differences in pore counting approaches. Angelini et al. 
(2014) reported pollen grains of B. vulgaris ssp. cicla (44–
67), B.  vulgaris var. rubra (40–58), and B.  vulgaris var. 
altissima (35–49), which had more pores than B. vulgaris 
and B.  maritima counted in the current investigation. 
Our data showed that the C/D values are very similar in 
all taxa investigated, since the pollen grains have a similar 
or at least comparable number of pores (Table 1). 
Exine – Kupriyanova & Alyoshina (1972) reported 
pollen grains of B.  trigyna that had thinner exine (1.8–
2.4 µm) than the values recorded in this study. The exine 
of the pollen grains of B. vulgaris ssp. cicla [1.77 (1.54–
2.31) µm], B. vulgaris var. rubra [2.02 (1.54–2.77) µm], 
and B. vulgaris var. altissima [1.86 (1.54–2.31) µm], re-
ported by Angelini et al. (2014), is generally thinner than 
the exine of B. vulgaris and B. maritima measured in our 
study (Table 1). 
Exine sculpture – Tsukada (1967) presented the mean 
nanoechini number per unit area in B. vulgaris 
(12.8/4 µm²), which is consistent with our data (Table 2). 
The data obtained in the present study show that 
B.  trigyna had larger pollen grains than the other two 
taxa. Beta vulgaris and B. maritima had overlapping size 
ranges. This is also supported by the cluster analysis and 
box plots (Figures 5a, 6a). Beta trigyna had fewer pores, 
while B. vulgaris and B. maritima had bigger pore num-
bers (Figure 6e). The largest diameter of pores was ob-
served in B. trigyna, while pores with a smaller diameter 
were found in B. vulgaris and B. maritima (Figure 6b). 
Larger distances between pores and between centres of 
pores were characteristic for B. trigyna, while shorter ones 
were observed in B. vulgaris and B. maritima (Figure 6c, 
d). Beta trigyna had a thicker exine, while B. vulgaris and 
B. maritima had a thinner exine (Figure 6f ). 
Our data demonstrate the relationship between the 
pore size and the number of nanoechini on the pore mem-
brane (Tables 1, 2). The pollen grains of B. trigyna had a 
larger pore diameter and a greater number of nanoechini 
on the pore membrane (Figure 4a, b). Respectively, the 
pollen grains of B. vulgaris and B. maritima had a smaller 
pore diameter and fewer nanoechini on the membrane of 
pores (Figure 4d, e, g, h).
There are several palynomorphological characters that 
overlap. For example, pollen grains in all taxa were slight-
ly undulated or undulated on the edge, which also agrees 
with the data of Kupriyanova & Alyoshina (1972) and 
Monoszon (1973). According to the mesoporial exine 
level, pores in B. trigyna, B. vulgaris and B. maritima were 
sunken or raised. Pollen grains of all taxa had convex or 
slightly flattened mesoporia and psilate-perforate tectum 
(Figures 3, 4). Since these characters are similar in all taxa, 
their usefulness for distinguishing of the taxa is limited.
Some authors have observed a correlation between the 
ploidy level and the pollen size in members of Cheno-
podiaceae family: polyploidy may result in larger pollen 
(e.g., Bassett et al., 1983; Olvera et al., 2006). The latter 
authors noted also that the number of pores is another 
pollen character to compare with the chromosome counts 
in Chenopodiaceae (Olvera et al., 2006). In our study, 
smaller pollen grains were found in B. vulgaris and B. ma­
ritima which are diploids and possess chromosome num-
bers of 2n = 18. The largest pollen grains were found in 
the hexaploid B. trigyna with a chromosome number of 
2n = 54. The data obtained corroborate the relationship 
between the number of chromosomes and the pollen size. 
A greater number of chromosomes clearly correspond 
to an increase in the size of pollen grains. Our studies 
showed that B. trigyna pollen had a larger diameter but 
fewer pores, whereas B. vulgaris and B. maritima had a 
smaller diameter but more numerous pores. 
Bezusko et al. (2023) analysed the species composition 
of the palynofloras of Late Holocene sediments of eight 
sections located on the territory of the Left Bank of the 
modern Forest-Steppe zone of Ukraine. The obtained 
data showed that the composition of palynofloras of 
Subatlantic–3 Holocene sediments of two sections 
(Loshchyna and Lopanske) included pollen grains of 
B. vulgaris. The radiocarbon date 550±40 BP records the 
appearance of pollen grains of B. vulgaris in the palynoflora 
of the investigated deposits of the Lopanske section.
The results of the analysis of paleofloristic materials 
indicate the cultivation of B. vulgaris in the Kharkiv region 
(Bohodukhivskyi and Dergachivskyi Districts), starting 
from the second half of the Subatlantic–3 Holocene time. 
Thus, B. vulgaris had its own history of cultivation in the 
studied area.
Conclusions
The description of the pollen grains of B. maritima is pro-
vided for the first time in this study. Also, for the first 
time, a description and comparison of the exine structure 
using SEM of B. trigyna, B. vulgaris and B. maritima is 
provided. The most significant characters for the diagnosis 
of these taxa are: pollen and pore sizes, distance between 
pores and between pore centres, structure of columellae, 
nanoechini size and density, number of nanoechini on 
pore membranes, and exine thickness. The taxa B.  vul­
garis and B.  maritima are quite similar in pollen grain 
characters. Pollen grains of B. trigyna (section Corollinae) 
differ in these characters from those of B. vulgaris and 
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Comparative morphometric and morphological study of the pollen of Beta taxa
B. maritima (section Beta). The presented quantitative 
and qualitative characteristics of pollen grains and their 
photomicrographs can be used for pollen identification 
in paleopalynology for spore-pollen analysis, especially 
for identifying the impact of human economic activity in 
the past. When identifying pollen grains, it is possible to 
use a complex of features of B. vulgaris since B. maritima 
grows mainly on sea coasts. The pollen characteristics de-
scribed here may also be used in future studies aiming at 
completing the knowledge on Beteae species and Cheno-
podiaceae/Amaranthaceae in general. 
Acknowledgements
The authors express their gratitude to Natalia M. Shy-
ian, Head Curator of the National Herbarium of Ukraine 
(KW; herbarium of the M.G. Kholodny Institute of Bota-
ny, National Academy of Sciences of Ukraine). Kind help 
and cooperation of Dmytro O. Klymchuk, Head of the 
Centre of Electron Microscopy (M.G. Kholodny Institute 
of Botany, National Academy of Sciences of Ukraine), are 
greatly appreciated. This study was funded in part by the 
project of the M.G. Kholodny Institute of Botany No. 
III-96-21.476 (state registration no. 0121U100463) sup-
ported by the National Academy of Sciences of Ukraine: 
Micromorphological and palaeopalynological characteris-
tics of representatives of critical groups of asterids in the 
Flora of Ukraine (taxa of order Caryophyllales).
Zoya M. Tsymbalyuk  https://orcid.org/0000-0003-2768-0045
Daniella Ivanova  https://orcid.org/0000-0001-5286-030X
Lyudmila M. Nitsenko  https://orcid.org/0000-0003-1945-7409
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