ESSDEarth System Science DataESSDEarth Syst. Sci. Data1866-3516Copernicus PublicationsGöttingen, Germany10.5194/essd-14-3961-2022Artemisia pollen dataset for exploring the potential ecological indicators in deep timeArtemisia pollen dataset for exploring the potential ecological indicators in deep timeLuLi-LiJiaoBo-HanQinFengXieGanLuKai-QingLiJin-FengSunBinLiMinFergusonDavid K.GaoTian-Ganggaotg@ibcas.ac.cnYaoYi-Fengyaoyf@ibcas.ac.cnWangYu-Feiwangyf@ibcas.ac.cnhttps://orcid.org/0000-0002-4530-2630State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, 20 Nanxincun Xiangshan, Beijing 100093, ChinaKey Laboratory of Land Surface Pattern and Simulation, Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing 100101, ChinaDepartment of Paleontology, University of Vienna, Althanstrasse 14, Vienna 1090, AustriaUniversity of Chinese Academy of Sciences, Beijing 100049, China
Artemisia, along with Chenopodiaceae, is the dominant component growing in
the desert and dry grassland of the Northern Hemisphere. Artemisia pollen with its
high productivity, wide distribution, and easy identification is usually
regarded as an eco-indicator for assessing aridity and distinguishing
grassland from desert vegetation in terms of the pollen relative abundance ratio
of Chenopodiaceae/Artemisia (C/A). Nevertheless, divergent opinions on the degree of
aridity evaluated by Artemisia pollen have been circulating in the palynological
community for a long time. To solve the confusion, we first selected 36
species from nine clades and three outgroups of Artemisia based on the phylogenetic
framework, which attempts to cover the maximum range of pollen morphological
variation. Then, sampling, experiments, photography, and measurements were
taken using standard methods. Here, we present pollen datasets containing
4018 original pollen photographs, 9360 pollen morphological trait
measurements, information on 30 858 source plant occurrences, and
corresponding environmental factors. Hierarchical cluster analysis on pollen
morphological traits was carried out to subdivide Artemisia pollen into three types.
When plotting the three pollen types of Artemisia onto the global terrestrial biomes,
different pollen types of Artemisia were found to have different habitat ranges.
These findings change the traditional concept of Artemisia being restricted to arid
and semi-arid environments. The data framework that we designed is open and
expandable for new pollen data of Artemisia worldwide. In the future, linking pollen
morphology with habitat via these pollen datasets will create additional
knowledge that will increase the resolution of the ecological environment in
the geological past. The Artemisia pollen datasets are freely available at Zenodo
(10.5281/zenodo.6900308; Lu et al., 2022).
Introduction
The concept of global change can be considered as any consistent trend in
the environment – past, present, or projected – that affects a substantial
part of the globe. Consequently, past climates shed light on our future
(Tierney et al., 2020). When attempting to reconstruct past global change
prior to meteorological records, we need some appropriate biological or
abiotic proxies based on long-term, consistently collected data, e.g. leaf
wax biomarkers (Bhattacharya et al., 2018), tree-ring data (Moberg et al.,
2005), leaf form (Yang et al., 2015), pollen data (Mosbrugger et al., 2005;
Guiot and Cramer, 2016; Marsicek et al., 2018), atmospheric carbon dioxide
(Zachos et al., 2008; Beerling and Royer, 2011), and isotope records (Zachos
et al., 2001; Sánchez-Murillo et al., 2019). Determining a suitable
proxy to reconstruct palaeoclimate and palaeoenvironment is a great
scientific challenge (Tierney et al., 2020; McClelland et al., 2021).
The pollen of Artemisia (A), together with that of Chenopodiaceae (C) in arid and
semi-arid areas, in the form of the ratio of C/A pollen abundance, was
applied to distinguish grassland and desert vegetation types and assess the
degree of drought in the geological past (El-Moslimany, 1990; Sun et al.,
1994; Davies and Fall, 2001; Herzschuh et al., 2004; Xu et al., 2007; Zhao
et al., 2009, 2012; Zhang et al., 2010; Li et al., 2017; Ma et
al., 2017; Koutsodendris et al., 2019; Wang et al., 2020), because both
Chenopodiaceae and Artemisia are dominant elements of desert vegetation (Wu, 1980; Vrba, 1980; Tarasov et al., 1998;
Herzschuh et al., 2004; Li et al., 2010; Zhao et al., 2021), and the sum of
their pollen relative abundances in the surface soil is usually more than
50 % in arid and semi-arid areas (Sun et al., 1994; Lu et al., 2020).
Among them, the pollen of Artemisia, with its high productivity, wide spatial and
temporal distribution, easy identification, and morphological uniformity
under the light microscope (LM), is an essential component and useful
bio-indicator in pollen-based past vegetation reconstructions and
environmental assessments. Some researchers regarded Artemisia as an aridity
indicator (El-Moslimany, 1990; Yi et al., 2003a, b; Liu et
al., 2006; Cai et al., 2019; Cui et al., 2019; Chen et al., 2020; Wu et al.,
2020; Cao et al., 2021), while others suggested that the correlation between
the relative abundance of Artemisia pollen and humidity was insignificant (Weng et
al., 1993; Sun et al., 1996; Koutsodendris et al., 2019; Lu et al., 2020;
Zhao et al., 2021). Consequently, there is an urgent need to evaluate
whether different pollen types of Artemisia represent distinct habitats.
In the past, Artemisia pollen was regarded as very uniform under LM (Wodehouse, 1926;
Sing and Joshi, 1969; Ling, 1982; Wang et al., 1995). For instance,
following the description and statistics of pollen morphology of 27 species
of Artemisia in Eurasia under LM, Sing and Joshi (1969) stated that the pollen grains
of Artemisia are consistent and continuous in morphology. Later, some authors
recognized a series of pollen types (Chen, 1987; Jiang et al., 2005;
Ghahraman et al., 2007; Shan et al., 2007; Hayat et al., 2009,
2010; Hussain et al., 2019) based on a detailed survey of the pollen
micromorphology of different taxa under the scanning electron microscope
(SEM).
For example, Chen (1987) described the pollen morphology of 77 Artemisia species from
China under LM and SEM and divided these pollen grains into six types by
using pollen characters, such as the shape and size of the spinules and density of spinules and granules. Type I (sparse spinules with
granules among them), type II (dense spinules, no or few granules), type III
(sparse spinules, no granules), type IV (dense spinules, well-developed
granules), type V (small and sparse spinules, smooth tectum), and type VI
(dissimilar spinules with granules among them).
Shan et al. (2007) investigated the pollen morphology of 32 Artemisia species from
the Loess Plateau of China under LM and SEM and divided these pollen grains
into five types according to exine sculpture: type I (dense spinules with
swollen bases, small granules), type II (dense spinules, swollen bases almost
united), type III (dense spinules with swollen bases and smooth tectum), type
IV (sparse small spinules and smooth tectum), and type V (sparse spinules,
small granules).
Jiang et al. (2005) observed the pollen morphology of 57 representative
plants in seven groups of Artemisia under LM and SEM. This pollen can be divided into two
types based on exine sculpture: type I (spinules multi-ruminated with flared
bases, connecting the mostly densely arranged spinules) and type II (densely
or loosely arranged spinules without flared bases, interspace glandular or
smooth) with subtypes II-1, II-2, II-3, and II-4 based on the distribution of
the spinules.
Ghahraman et al. (2007) studied the pollen morphology of 26 species of the
33 Artemisia species in Iran under LM and SEM. Based on exine ornamentation observed
under SEM, two types of pollen grains were recognized: type I, exine surface
covered with dense acute spinules, and type II, exine surface with few
spinules.
Hayat et al. (2009, 2010) carried out a palynological study of 22
Artemisia species from Pakistan under LM and SEM. Earlier work demonstrated the
phylogenetic associations within Artemisia based on a phylogenetic analysis of nine
characters (pollen type, pollen shape, spinule arrangement, exine sculpture,
spinule base, the length of polar axis, the length of equatorial axis, exine
thickness, and colpus width) of pollen grains of Artemisia. In the latter work, eight
micromorphological characters were identified and pooled by cluster
analysis, leading to the recognition of five groups.
Hussain et al. (2019) studied the pollen morphology of 15 Artemisia species in the
Gilgit–Baltistan region of Pakistan utilizing SEM and divided these species
into four groups based on cluster analysis of seven micromorphological
characters (pollen type, pollen shape, spinule arrangement, exine sculpture,
spinule base, polar length, and equatorial width).
Phylogenetic tree of Artemisia (modified from Malik et al., 2017). The
styles of the strokes that were used to draw the branches indicate the
traditional subgeneric classification of Artemisia and the yellow spots indicate
sampled taxa.
Almost all of the above-mentioned Artemisia pollen classifications were designed to
solve taxonomic or phylogenetic problems, and only a few were concerned with
linking diverse habitats to the different pollen types in Artemisia.
Here, we attempt to (1) present abundant pollen photographs of 36 species from
nine branches and three outgroups of the genus (ca. 400 species worldwide, see
Ling, 1982; Bremer and Humphries, 1993), constrained by the phylogenetic
framework of Artemisia (Sanz et al., 2008; Malik et al., 2017); (2) describe and
measure the morphological traits of these pollen grains; (3) provide a new
classification of pollen types and their distribution worldwide, with a key
to pollen types in Artemisia; and (4) explore the diverse ecological niches of Artemisia
represented by different pollen types in order to evaluate palaeovegetation
and reconstruct palaeoenvironments.
Materials and methodsSampling strategy
The 36 pollen samples studied were selected from voucher sheets in the PE
herbarium at the Institute of Botany, Chinese Academy of Sciences
(Fig. 1 and
Table B1), covering nine main clades, i.e. subg. Tridentata, subg. Artemisia (contains Sect.
Artemisia, Sect. Abrotanum I, Sect. Abrotanum II, and Sect. Abrotanum III), subg. Pacifica, subg. Seriphidium, subg. Absinthium, and subg.
Dracunculus, constrained by the phylogenetic framework of Artemisia (Malik et al., 2017) and three
outgroups (Sanz et al., 2008), reflecting the maximum diversity or
morphological variation under LM and SEM.
Data acquisition
Pollen samples were acetolysed by the standard method (Erdtman, 1960) and
fixed in glycerine jelly. Standard procedures were followed for LM and SEM
(Chen, 1987; Wang et al., 1995). The pollen grains were photographed under
LM (Leica DM 4000) at a magnification of ×1000 and SEM (Hitachi
S-4800) at an accelerating voltage of 30 kV. The pollen terminology followed
the descriptions of Hesse et al. (2009) and Halbritter et al. (2018). The
statistical pollen morphological traits under LM (Fig. 2a and b, P: polar
length; E: equatorial width; P/E; T: exine thickness; L: pollen length; T/L)
of each species were measured using 20 pollen grains. We chose five pollen
grains under SEM for each exine ornamentation trait in each species (Fig. 2c–f, D: diameter of spinule base; H: spinule height; D/H; Gs: granule
spacing; Ss: Spinule spacing; Gs/Ss; Ps: perforation spacing) and, on
average, randomly selected four regions of each pollen grain for measuring,
yielding a total of 20 measurements. The mean value (M) and standard
deviation (SD) of the pollen grains of each species were measured and
calculated in both polar and equatorial views (Appendix A and
Table 1).
Graphical illustration of measured pollen morphological traits in
Artemisia(a, b: A. annua; c, d: A. vulgaris) and outgroups (e: Kaschagaria brachanthemoides; and f: Ajania pallasiana). Scale bar in LM and SEM overview 10 µm, and in SEM close-up 1 µm.
The scientific names of selected taxa were standardized according to Plants
of the World Online (https://powo.science.kew.org/, last access: 21 November 2021). The specimen sampling
coordinates of the corresponding taxa were obtained from the Global
Biodiversity Information Facility (GBIF, https://www.gbif.org/, last access: 9 November 2021). Only preserved specimens were filtered for GBIF
data given their well-documented geographical information and the
availability of specimens as definitive vouchers. The distribution data on
observations and cultivated collections provided by GBIF were excluded
because they may contain incorrect identification or incorrect
geo-referencing (Brummitt et al., 2021). Next, the distribution data were
standardized cleaned using R package “CoordinateCleaner” (Zizka et al.,
2019); no outliers were found.
The corresponding environmental factors including altitude and 19 climate
parameters of these coordinates were obtained from WorldClim
(https://www.worldclim.org/, last access: 15 May 2017) with a spatial resolution of 30 s
(∼1km2) in 1970–2000 by Extract MultiValues To Points
using ArcGIS 10.2 software in bilinear interpolation.
Data processing
OriginPro 2021 software was used for hierarchical cluster analysis on
Artemisia and its outgroup pollen data. The Euclidean distance was calculated after
the normalization of the original data, and the Ward method was used for
clustering. Five groups were established, and the centre point of each group
was calculated according to the sum of distances. Pollen morphological
traits for the principal component analysis (PCA) of Artemisia and its outgroups were
grouped according to the five groups of the cluster analysis. OriginPro 2021
software was used to draw group violin diagrams and boxplots respectively, to run an ANOVA to test for an overall difference between the pollen
characters of three pollen types, and to test intraspecific variability in pollen
exine ultrastructure characters among three representative species, followed
by post hoc tests (Tukey). OriginPro 2021 software was also used to draw
group violin diagrams and run a Kruskal–Wallis ANOVA to test for overall differences
between the environmental factors of the three pollen types. The images of
habitats reproduced in the text are from the websites listed in Table B1.
The global distribution data of the 36 representative species and three pollen
types were plotted on the map of terrestrial ecological regions (Olson et
al., 2001) using ArcGIS 10.2 software (Figs. 16 and 21).
Data description<italic>Artemisia</italic> pollen grains and their source plant habitats
Here, we provide detailed data on pollen morphological traits, covering 36
species from nine main clades of Artemisia and three outgroups constrained by the
phylogenetic framework (Fig. 1, Sanz et al., 2008; Malik et al., 2017) under
LM and SEM, and the habitats of their source plants (Figs. 3–14).
Statistical pollen morphological trait data of 36 sampled taxa
The mean values of 10 pollen morphological traits of 36 sampled species are
listed in Table 1, and these data distribution patterns are shown in
boxplots (Fig. 15) in the form of variation (25 %–75 %) and further
described in the form of mean value ± standard deviation (M ±SD, Appendix A).
The source plant distributions in global terrestrial biomes of 36 sampled
species are shown in Fig. 16. In Artemisia, some species have worldwide distributions,
such as A. vulgaris (Fig. 16-7), A. absinthium (Fig. 16-24), and A. campestris (Fig. 16-33); a few taxa are
limited to East Asia, such as A. roxburghiana (Fig. 16-10) and A. blepharolepis (Fig. 16-26), while
others have narrow and isolated distributions in deserts and xeric
shrublands of Central Asia, e.g. A. kurramensis (Fig. 16-13) and A. aralensis (Fig. 16-16). In
outgroups of Artemisia, Kaschagaria brachanthemoides is also confined to deserts and xeric shrublands of Central
Asia (Fig. 16-34), while Ajania pallasiana lives in forests of East Asia (Fig. 16-35).
Potential use of the <italic>Artemisia</italic> pollen datasetsThe pollen classification of <italic>Artemisia</italic>
The pollen grains of Anthemideae and Asteraceae under LM could be simply
divided into Artemisia pollen type (Figs. 3–13 and 14a, Appendix A) with indistinct and
short spinules, and Anthemis pollen type such as
Chrysanthemum indicum and Ajania pallasiana
(Fig. 14b and c, Appendix A) with
distinct and long spines on pollen exine ornamentation (Wodehouse, 1926;
Stix, 1960; Chen, 1987; Chen and Zhang, 1991; Martín et al., 2001, 2003; Sanz et al., 2008; Blackmore et al., 2009;
Vallès et al., 2011). Artemisia pollen grains are difficult to separate from
those of other related genera with Artemisia pollen type such
as Kaschgaria brachanthemoides (Fig. 14a1 and a2,
Appendix A), Elachanthemum, Ajaniopsis, Filifolium, and Neopallasia (Chen and Zhang, 1991) under LM due to their great
similarity in pollen exine ornamentation and colporate patterns (Chen, 1987;
Martín et al., 2001, 2003; Vallès et al.,
2011). Furthermore, Sing and Joshi (1969) questioned the feasibility of
recognizing pollen types under LM in the highly uniform pollen of
Artemisia. Later, SEM made it possible to subdivide the pollen of Artemisia and those of other
related genera within the Artemisia pollen type using pollen exine ultrastructure
characters (Chen, 1987; Chen and Zhang, 1991; Sun and Xu, 1997; Jiang et
al., 2005; Ghahraman et al., 2007; Shan et al., 2007; Hayat et al., 2009, 2010; Hussain et al., 2019).
Hierarchical cluster analysis (Fig. 17a) revealed that the pollen
morphological traits (P/E, H, D, D/H, Ss, Gs, Gs/Ss, and Ps) of Artemisia and its
outgroups were divided into Clade A with perforations and without granules
(Fig. 13a5 and a6, b5 and b6, c5 and c6), and Clade B with granules and without
perforations (Figs. 3–13a5 and a6, b5 and b6, c5 and c6) on the pollen exine under SEM.
Hierarchical cluster analysis, showing the dendrogram for pollen
types from Artemisia and outgroups (a), and the habitat ranges of 36 representative
species (b, Tutin et al., 1976; Zhang, 2007; Ling et al., 2011).
Principal component analysis of 36 taxa of Artemisia and its outgroups.
In addition, Clade A, as the outgroup of Artemisia, includes Anthemis type (Chrysanthemum indicum and Ajania pallasiana) with
prominent spines on pollen exine under LM, and Kaschgaria type (Kaschgaria brachanthemoides) with spinules on
pollen exine (Figs. 14a and 17a). Clade B comprises three pollen types from
three branches of Artemisia (Fig. 17a), i.e. SG type (short and wide spinule pollen
type, Clade B1), LNS type (long and narrow spinule pollen type, Clade B2-1),
and SG type (sparse granule pollen type, Clade B2-2).
Eight pollen morphological traits (P/E, H, D, D/H, Ss, Gs, Gs/Ss, and Ps)
were selected for the principal component analysis (PCA) of 36 taxa of
Artemisia and its outgroups (Fig. 18), and grouped according to the five clades of the
cluster analysis, i.e. the five pollen types (Fig. 17a). The results reveal
that Artemisia pollen morphology differs significantly from that of the outgroups,
and that three Artemisia pollen types could be distinguished.
Nine characteristics of Artemisia pollen could partially explain the differences
between these three pollen types (Fig. 19). P/E (the length of polar axis/the
length of equatorial axis) in LNS types (0.93–1.06) are significantly
different (ANOVA p<0.001) from both SWS (0.97–1.12) and SG
(0.98–1.14), so could be used to identify the LNS type. D/H (diameter of
spinule base/spinule height) in the SWS type differ significantly (ANOVA p<0.001) from both LNS and SG types. The variation range of D/H is
1.38–2.23 in the SWS type, 1.07–1.75 in the LNS type, and 0.98–1.66 in the
SG type, indicating that the SWS pollen type is distinguished by short and
wide spinules. Gs/Ss (granule spacing/spinule spacing) in the SG type was
higher than those of the SWS and LNS types (ANOVA p<0.001), which
distinguished the SG type from the other two types. Moreover, the SG type is
characterized by sparse granules with the variation range of Gs/Ss spanning
0.37–0.64, while the SWS and LNS types show much denser granules whose Gs/Ss
are mainly below 0.35.
Violin diagrams of three pollen types from Artemisia, showing the
variations (M ±SD) in nine pollen characters (P: length of polar
axis; E: length of equatorial axis; D: diameter of spinule base; H: spinule
height; Gs: granule spacing; Ss: spinule spacing; Ps: perforation spacing).
Asterisks indicate statistically significant differences (p<0.001).
Within the new Artemisia pollen classification (Fig. 17a, Key), the SWS type
represents a type of pollen with short and wide spinules (D/H>1.81) and dense granules (Figs. 17a and 19). The LNS type represents a type of
pollen with long and narrow spinules (D/H<1.38) and dense granules
(Figs. 17a and 19). The SG type is characterized by sparse granules (Gs/Ss>0.37) and small, long, and narrow spinules (Figs. 17a and 19).
Testing the pollen intraspecific variability within <italic>Artemisia</italic>
Evidence shows that the pollen morphology in Artemisia is highly uniform under LM
without discrimination (Wodehouse, 1926; Sing and Joshi, 1969; Ling, 1982;
Chen, 1987; Wang et al., 1995), which might suggest that statistical
analyses of the intraspecific morphological variation of pollen under the LM
are limited or meaningless. Right now, the SEM technique has made it
possible to subdivide Artemisia pollen into different types using pollen exine
ultrastructure characters (Chen, 1987; Chen and Zhang, 1991; Sun and Xu,
1997; Jiang et al., 2005; Ghahraman et al., 2007; Shan et al., 2007; Hayat
et al., 2009, 2010; Hussain et al., 2019).
In order to test the intraspecific variability of pollen exine
ultrastructure traits, we selected one species respectively from the three
pollen types corresponding to the three morphological clades of Artemisia pollen,
i.e. Artemisia vulgaris (SWS type), Artemisia annua (LNS type), and Artemisia maritima (SG type), and sampled five specimens of
each species (Table B2). Six pollen traits, i.e. D, H, D/H, Gs, Ss, and
Gs/Ss, were counted and analysed under SEM to test for intraspecific
variability of pollen exine ultrastructure traits.
The test showed that it was feasible to use stable D/H and Gs/Ss for pollen
type classification of Artemisia because (1) D/H and Gs/Ss were stable within species
(Fig. 20 and Table 2) for the pollen classification; and (2) D, H, Gs, and Ss were
variable as size values, e.g. these four traits were significantly different
within species in both A. vulgaris and A. annua, while D, H, and Ss were significantly
different within species in A. maritima (Fig. 20 and Table 2). There was evidence showing
that size values such as pollen exine ultrastructure size were often
variable within species due to their genetic divergence, various habitats,
and different experimental treatments (Mo et al., 1997; Zhao and Yao, 1999;
Zhang and Qian, 2011).
Boxplots of intraspecific pollen exine ultrastructure characters
from three species of Artemisia, showing the variations (M ±SD) in six pollen
characters (D: diameter of spinule base; H: spinule height; Gs: granule
spacing; Ss: spinule spacing; Ps: perforation spacing). Asterisks indicate
statistically significant differences (∗p≤0.05, ∗∗p≤0.01, ∗∗∗p<0.001).
The results of ANOVA for intraspecific variability in pollen exine
ultrastructure characters among three representative species.
Pollen exineSWS typeLNS typeSG typeultrastructure charactersArtemisia vulgarisArtemisia annuaArtemisia maritimaD (µm)significantsignificantsignificantH (µm)significantsignificantsignificantD/Hnon-significantnon-significantnon-significantGs (µm)significantsignificantsignificantSs (µm)significantsignificantsignificantGs/Ssnon-significantnon-significantnon-significantKey to three pollen types of <italic>Artemisia</italic> and two pollen types of its
outgroups
Pollen exine with perforations and without granules under SEM 2
Pollen exine with granules and without perforations under SEM 3
Distinct and long spines on pollen exine, with H>3µmAnthemis type
Indistinct and short spinules on pollen exine, with H<1µmKaschgaria type
Pollen exine with sparse granules and Gs/Ss≥0.37 under SEM SG type
Pollen exine with dense granules and Gs/Ss≤0.31 under
SEM 4
Pollen exine with D/H<1.38 under SEM LNS type
Pollen exine with D/H≥1.38 under SEM SWS type
The ecological implications of <italic>Artemisia</italic> pollen types
Plotting the distribution data of 33 species from nine main branches of
Artemisia constrained by the phylogenetic framework (Fig. 1) onto the global
terrestrial biomes (Fig. 21), we noticed that the genus is widely
distributed from forest to grassland, desert, and saline habitats (Figs. 16,
17b, and 21). Furthermore, different species of Artemisia with SWS pollen type (Fig. 21a)
and LNS type (Fig. 21b) have a rather wide distribution with severely
overlapping ranges, while those with SG type (Fig. 21c) have narrow and
isolated distributions.
The global distribution pattern of three Artemisia pollen types in terrestrial
biomes (modified from Olson et al., 2001). (a) SG type; (b) LNS type; and (c) SWS
type.
Fourteen terrestrial biomes: 01. tropical and subtropical moist broadleaf forests;
02. tropical and subtropical dry broadleaf forests; 03. tropical and
subtropical coniferous forests; 04. temperate broadleaf and mixed forests;
05. temperate coniferous forests; 06. boreal forests/taiga; 07. flooded
grasslands and savannas; 08. montane grasslands and shrublands; 09. tundra;
10: Mediterranean forests, woodlands, and shrub; 11. tropical and
subtropical grasslands, savannas, and shrublands; 12. temperate grasslands,
savannas, and shrublands; 13. deserts and xeric shrublands; 14. mangroves;
15. lakes; 16. rock and ice.
The ecological implications of Artemisia pollen types mentioned above fall into four
categories. (i) Artemisia with the SG pollen type all belong to the subg.
Seriphidium, which generally grows in dry habitats ranging from grassland desert to
desert and coastal saline–alkaline environments, with their distribution
largely limited to Eurasia and growing at low altitude (Figs. 17b, 21c, and 22).
(ii) The habitats of Artemisia with LNS pollen type have a global distribution and
occur in forest, grassland and desert, and even coastal areas (Figs. 17b,
21b, and 22), with the highest mean annual temperature (MAT). Hence, the LNS
pollen type is a generalist. (iii) Artemisia with SWS pollen type include Sect.
Artemisia, and its habitats range from forest to desert, although most of the taxa are
confined to humid environments from forest to grassland with a global
distribution and the highest mean annual precipitation (MAP, Figs. 17b, 21c,
and 22). (iv) If the SWS pollen type and the SG pollen type appear together, the
range of vegetation types could be reduced to grassland desert and desert
through niche coexistence (Fig. 17b).
Violin diagrams of three pollen types from Artemisia, showing the
variations (25 %–75 %) in MAT, MAP, and altitude. Asterisks indicate
statistically significant differences (p<0.001).
In addition, we noticed that Kaschgaria brachanthemoides as an outgroup of Artemisia lives in dry mountain
valleys or dry riverbeds of northwestern China (Toksun) and Kazakhstan, with
highly characteristic pollen (Fig. 14a), narrow habitats (Fig. 17b), and
regional distribution (Fig. 16-34), and has the potential to indicate some
specific habitats.
Data availability
Pollen datasets (Table 3) including pollen photographs under LM and SEM,
statistical data of pollen morphological traits, and their source plant
distribution for each species are available at Zenodo
(10.5281/zenodo.6900308; Lu et al., 2022).
Artemisia pollen datasets in this study.
Data typeDataData acquisitionData accessibilityformatThe phylogenetic framework of Artemisia pollen sampling..pngLiterature survey (modified from Malik et al., 2017).This articleA voucher specimen list of 36 representative species..docPollen samples were obtained from PE herbarium at the Institute of Botany, Chinese Academy of Sciences.12 illustrations of pollen grains and the habitats of their source plants..pngHabitat photos from online sources (Appendix Table B1).4018 original pollen photographs (3205 under LM, 813 under SEM)..jpgPollen samples were acetolysed by the standard method and fixed in glycerine jelly. The pollen grains were photographed under LM and SEM using standard procedures.Zenodo (https://doi.org/10.5281/zenodo.6900308; Lu et al., 2022)9360 pollen morphological trait measurements of 36 representative species..xlsxStatistical data of pollen morphological traits were measured by standard methods.1800 pollen morphological trait measurements for testing the pollen intraspecific variability within Artemisia..xlsxStatistical data of pollen morphological traits were measured by standard methods.30 858 source plant occurrence information, and corresponding environmental factors including altitude and 19 climate parameters..xlsxTheir source plant distribution coordinates were obtained from GBIF (10.15468/dl.596xd9,GBIF.org, 2021). The corresponding environmental factors of these coordinates were obtained from WorldClim (https://www.worldclim.org/, last access: 15 May 2017) with a spatial resolution of 30 s between 1970–2000.Summary
To cover the maximum range of Artemisia pollen morphological variation, we provide a
pollen dataset of 36 species from nine clades and three outgroups of Artemisia constrained by
the phylogenetic framework, containing high-quality pollen photographs under
LM and SEM, statistical data of pollen morphological traits together with
their source plant distribution, and corresponding environmental factors.
Here, we attempt to decipher the underlying causes of the long-standing
disagreement in the palynological community on the correlation between
Artemisia pollen and aridity by recognizing the different ecological implications of
Artemisia pollen types.
This dataset should work well for identifying and classifying Artemisia pollen from
Neogene and Quaternary sediments. While Artemisia pollen grains are uniform in
morphology under LM, different types can be recognized under SEM. So, the
single-grain technique for picking out fossil pollen grains and
photographing the same grains under LM and SEM should provide valuable
insights in the diversity of fossil Artemisia (Ferguson et al., 2007; Grímsson
et al., 2011, 2012; Halbritter et al., 2018).
Furthermore, those Artemisia pollen grains could then be compared with the rich
photographs from this dataset, and together with the key provided here,
possibly attributed to one of the three Artemisia pollen types, which in turn may
provide a link to the different habitat ranges.
However, the application of this dataset probably may not work well for the
Palaeogene, as (1) Artemisia might have originated in the Palaeocene, although there
is no evidence for a specific location or time interval of its origin (e.g.
Ling, 1982; Wang, 2004; Miao et al., 2011); (2) both the lack of macrofossils of
Artemisia and the strong pollen similarity between Artemisia and its closely related taxa
under LM might lead to confusion and more uncertainty in tracing the origin
of Artemisia. On the other hand, the present dataset provides a potential
morphological tool to distinguish Artemisia pollen grains from those of its related
taxa at the SEM level and may shed light on the origin of this genus in the
Palaeogene.
Moreover, these pollen photographs also have potential and the possibility
to be used for deep learning research. We are attempting to automatically
identify pollen images using pollen assemblages from the eastern Central
Asian desert as an example with deep convolutional neural network (DCNN) of
artificial intelligence. Pollen images of the many species of Artemisia provided
here, and the increasing number of intraspecific replications in the future,
will all serve for projected image identification research.
Finally and most importantly, the Artemisia pollen dataset as designed is open and
expandable for new pollen data from Artemisia worldwide in order to better serve the
global environment assessment and refined reconstruction of vegetation in
the geological past as a basis or blueprint for other overarching
statistical analyses on pollen morphology.
Pollen morphological descriptions of 36 representative species from nine clades
of Artemisia and three outgroups.
Pollen morphology of Artemisia: pollen grains oblate, spherical, or ellipsoidal;
apertures tricolporate; almost circular in equatorial view and trilobate
circular in polar view; the exine near the colpi gradually thinned; the
exine has an obvious double structure of inner and outer layers where the
outer is thicker than the inner under LM; and the exine ornamentation is psilate
(LM), spinulate, and granule (SEM).
Artemisia cana (Table 1, Figs. 3a and 15).
Pollen grains spheroidal or oblate. Almost circular in equatorial view and
trilobate circular in polar view. Apertures tricolporate. The exine near the
colpi gradually thinned. Polar length (P)=23.46±1.76µm (M ±SD), equatorial width (E)=24.50±2.13µm (M ±SD), P/E=0.96±0.04 (M ±SD), exine thickness (T)=3.91±0.36µm (M ±SD), and pollen length (L)=24.58±1.24µm (M ±SD), T/L=0.16±0.02. The exine
ornamentation is psilate (LM), spinulate (SEM). Under SEM, diameter of
spinule base (D)=0.58±0.13µm (M ±SD), spinule
height (H)=0.46±0.08µm (M ±SD), D/H=1.28±0.38 (M ±SD), granule spacing (Gs)=0.33±0.08µm (M ±SD), and spinule spacing (Ss)=1.60±0.22µm (M ±SD), Gs/Ss=0.21±0.06 (M ±SD).
Habitat: grasslands, gravel soils, mountain meadows, and stream banks; wet
mountain meadows, stream banks, and rocky areas with late-lying snows.
Artemisia tridentata (Table 1, Figs. 3b and 15).
Pollen grains prolate or spheroidal. Almost circular in equatorial view and
trilobate circular in polar view. Apertures tricolporate. The exine near the
colpi gradually thinned. P=21.36±1.54µm, E=20.69±1.85µm, P/E=1.04±0.07, T=3.55±0.41µm, L=22.35±1.90µm, T/L=0.16±0.02. The
exine ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.76±0.08µm, H=0.60±0.08µm, D/H=1.30±0.23, Gs=0.24±0.06µm, Ss=1.12±0.22µm,
Gs/Ss=0.22±0.08.
Habitat: mountains, grasslands, and meadows of western North America. Arid
and semi-arid, desert, or semi-desert areas of the growing shrub or
semi-shrub environment.
Artemisia californica (Table 1, Figs. 3c and 15).
Pollen grains prolate or spheroidal or oblate. Almost circular in equatorial
view and trilobate circular in polar view. Apertures tricolporate. The exine
near the colpi gradually thinned. P=18.94±1.30µm, E=19.13±1.43µm, P/E=0.99±0.08, T=2.70±0.16µm, L=18.85±1.12µm, T/L=0.14±0.01.
The exine ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.75±0.11µm, H=0.71±0.10µm, D/H=1.08±0.20, Gs=0.24±0.05µm, Ss=1.45±0.23µm, Gs/Ss=0.17±0.05.
Habitat: coastal scrub and dry foothills.
Artemisia indica (Table 1, Figs. 4a and 15).
Pollen grains spheroidal or oblate. Almost circular in equatorial view and
trilobate circular in polar view. Apertures tricolporate. The exine near the
colpi gradually thinned. P=23.47±1.39µm, E=23.81±0.86µm, P/E=0.99±0.06, T=3.50±0.27µm, L=23.31±0.61µm, T/L=0.15±0.01. The
exine ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.76±0.10µm, H=0.39±0.06µm, D/H=2.04±0.53, Gs=0.28±0.07µm, Ss=1.21±0.24µm,
Gs/Ss=0.24±0.07.
Habitat: roadsides, forest margins, slopes, and shrublands; low elevations to
2000 m.
Artemisia argyi (Table 1, Figs. 4b and 15).
Pollen grains prolate or spheroidal. Almost circular in equatorial view and
trilobate circular in polar view. Apertures tricolporate. The exine near the
colpi gradually thinned. P=21.80±1.00µm, E=21.67±1.27µm, P/E=1.01±0.08, T=3.55±0.40µm, L=22.24±1.13µm, T/L=0.16±0.01. The
exine ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.64±0.07µm, H=0.38±0.04µm, D/H=1.71±0.23, Gs=0.22±0.06µm, Ss=0.90±0.17µm,
Gs/Ss=0.26±0.09.
Habitat: waste places, roadsides, slopes, hills, steppes, and forest steppes;
low elevations to 1500 m.
Artemisia mongolica (Table 1, Figs. 4c and 15).
Pollen grains prolate or spheroidal. Almost circular in equatorial view and
trilobate circular in polar view. Apertures tricolporate. The exine near the
colpi gradually thinned. P=21.05±0.82µm, E=20.42±1.01µm, P/E=1.03±0.05, T=3.29±0.19µm, L=19.78±0.99µm, T/L=0.17±0.01. The
exine ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.62±0.08µm, H=0.41±0.05µm, D/H=1.54±0.25, Gs=0.19±0.06µm, Ss=0.91±0.14µm,
Gs/Ss=0.22±0.08.
Habitat: slopes, shrublands, riverbanks, lakeshores, roadsides, steppes,
forest steppes, and dry valleys; low elevations to 2000 m.
Artemisia vulgaris (Table 1, Figs. 5a and 15).
Pollen grains prolate or spheroidal. Almost circular in equatorial view and
trilobate circular in polar view. Apertures tricolporate. The exine near the
colpi gradually thinned. P=19.72±1.25µm, E=19.29±1.82µm, P/E=1.03±0.08, T=2.92±0.23µm, L=18.94±1.09µm, T/L=0.16±0.02. The
exine ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.69±0.07µm, H=0.34±0.07µm, D/H=2.13±0.52, Gs=0.29±0.07µm, Ss=1.55±0.32µm,
Gs/Ss=0.20±0.07.
Habitat: roadsides, slopes, canyons, forest margins, forest steppes, and
subalpine steppes; 1500–3800 m.
Artemisia selengensis (Table 1, Figs. 5b and 15).
Pollen grains prolate or spheroidal. Almost circular in equatorial view and
trilobate circular in polar view. Apertures tricolporate. The exine near the
colpi gradually thinned. P=20.67±1.57µm, E=19.68±1.94µm, P/E=1.06±0.09, T=3.72±0.72µm, L=20.80±2.21µm, T/L=0.18±0.03. The
exine ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.67±0.08µm, H=0.38±0.05µm, D/H=1.76±0.27, Gs=0.22±0.06µm, Ss=1.05±0.15µm,
Gs/Ss=0.22±0.07.
Habitat: riverbanks, lakeshores, humid areas, meadows, slopes, and roadsides.
Artemisia ludoviciana (Table 1, Figs. 5c and 15).
Pollen grains prolate or spheroidal. Almost circular in equatorial view and
trilobate circular in polar view. Apertures tricolporate. The exine near the
colpi gradually thinned. P=21.65±1.02µm, E=20.82±1.10µm, P/E=1.04±0.08, T=3.71±0.28µm, L=20.94±1.13µm, T/L=0.18±0.01. The
exine ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.70±0.08µm, H=0.37±0.04µm, D/H=1.94±0.31, Gs=0.20±0.05µm, Ss=1.23±0.13µm,
Gs/Ss=0.16±0.04.
Habitat: disturbed roadsides, open meadows, and rocky slopes.
Artemisia roxburghiana (Table 1, Figs. 6a and 15).
Pollen grains prolate or spheroidal. Almost circular in equatorial view and
trilobate circular in polar view. Apertures tricolporate. The exine near the
colpi gradually thinned. P=23.88±2.04µm, E=23.69±2.00µm, P/E=1.01±0.06, T=3.78±0.39µm, L=21.81±1.05µm, T/L=0.17±0.02. The
exine ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.76±0.07µm, H=0.39±0.06µm, D/H=1.96±0.37, Gs=0.28±0.11µm, Ss=0.79±0.11µm,
Gs/Ss=0.36±0.14.
Habitat: roadsides, slopes, dry canyons, grasslands, waste areas, and terraces;
700–3900 m.
Artemisia rutifolia (Table 1, Figs. 6b and 15).
Pollen grains spheroidal or oblate. Almost circular in equatorial view and
trilobate circular in polar view. Apertures tricolporate. The exine near the
colpi gradually thinned. P=22.22±1.10µm, E=22.70±1.37µm, P/E=0.98±0.05, T=3.53±0.37µm, L=24.93±1.05µm, T/L=0.14±0.01. The
exine ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.31±0.04µm, H=0.26±0.04µm, D/H=1.20±0.18, Gs=0.21±0.05µm, Ss=1.27±0.19µm,
Gs/Ss=0.17±0.04.
Habitat: hills, dry river valleys, basins, steppes, semideserts, and stony
desert; 1300–5000 m.
Artemisia chinensis (Table 1, Figs. 6c and 15).
Pollen grains spheroidal or oblate. Almost circular in equatorial view and
trilobate circular in polar view. Apertures tricolporate. The exine near the
colpi gradually thinned. P=21.53±1.95µm, E=22.75±2.00µm, P/E=0.95±0.05, T=2.97±0.40µm, L=23.71±2.30µm, T/L=0.13±0.01. The
exine ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.70±0.05µm, H=0.55±0.07µm, D/H=1.29±0.19, Gs=0.27±0.07µm, Ss=0.91±0.17µm,
Gs/Ss=0.31±0.09.
Habitat: littoral plants found on raised coral outcrops.
Artemisia kurramensis (Table 1, Figs. 7a and 15).
Pollen grains spheroidal. Almost circular in equatorial view and trilobate
circular in polar view. Apertures tricolporate. The exine near the colpi
gradually thinned. P=19.71±1.28µm, E=19.35±1.02µm, P/E=1.02±0.05, T=3.30±0.38µm, L=19.44±0.92µm, T/L=0.17±0.02. The exine
ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.38±0.04µm, H=0.27±0.03µm, D/H=1.41±0.21, Gs=0.23±0.07µm, Ss=1.25±0.21µm,
Gs/Ss=0.19±0.06.
Habitat: foothills, mountain slopes, dry graveyards, and field borders with
sparse vegetation on gravelly, fine to coarse sandy-clay soils.
Artemisia compactum (Table 1, Figs. 7b and 15).
Pollen grains spheroidal. Almost circular in equatorial view and trilobate
circular in polar view. Apertures tricolporate. The exine near the colpi
gradually thinned. P=22.33±1.81µm, E=21.97±1.23µm, P/E=1.02±0.06, T=2.97±0.43µm, L=21.67±0.87µm, T/L=0.14±0.02. The exine
ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.41±0.07µm, H=0.28±0.03µm, D/H=1.50±0.33, Gs=0.51±0.12µm, Ss=0.92±0.12µm,
Gs/Ss=0.56±0.12.
Habitat: rocky slopes and semi-deserts, from low elevations to sub-alpine
areas.
Artemisia maritima (Table 1, Figs. 7c and 15).
Pollen grains prolate. Almost circular in equatorial view and trilobate
circular in polar view. Apertures tricolporate. The exine near the colpi
gradually thinned. P=26.24±1.61µm, E=23.09±1.43µm, P/E=1.14±0.06, T=3.54±0.44µm, L=24.42±1.51µm, T/L=0.14±0.02. The exine
ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.28±0.04µm, H=0.23±0.06µm, D/H=1.30±0.34, Gs=0.53±0.12µm, Ss=1.08±0.12µm,
Gs/Ss=0.50±0.13.
Habitat: saltmarsh, dry and calcareous hillsides, seashores, and dry saline
or alkaline soils.
Artemisia aralensis (Table 1, Figs. 8a and 15).
Pollen grains prolate or spheroidal. Almost circular in equatorial view and
trilobate circular in polar view. Apertures tricolporate. The exine near the
colpi gradually thinned. P=22.32±1.72µm, E=21.91±1.63µm, P/E=1.02±0.06, T=3.16±0.36µm, L=22.76±1.45µm, T/L=0.14±0.01. The
exine ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.25±0.04µm, H=0.22±0.04µm, D/H=1.16±0.28, Gs=0.50±0.13µm, Ss=1.09±0.18µm,
Gs/Ss=0.46±0.14.
Habitat: clayey, sandy loam, and solonetzic soils.
Artemisia annua (Table 1, Figs. 8b and 15).
Pollen grains prolate or spheroidal. Almost circular in equatorial view and
trilobate circular in polar view. Apertures tricolporate. The exine near the
colpi gradually thinned. P=19.71±0.84µm, E=19.45±1.32µm, P/E=1.02±0.07, T=3.45±0.25µm, L=19.20±0.92µm, T/L=0.18±0.01. The
exine ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.45±0.06µm, H=0.39±0.05µm, D/H=1.18±0.25, Gs=0.27±0.08µm, Ss=1.29±0.16µm,
Gs/Ss=0.21±0.08.
Habitat: hills, waysides, wastelands, outer forest margins, steppes, forest
steppes, dry flood lands, terraces, semidesert steppes, rocky slopes,
roadsides, and saline soils; 2000–3700 m.
Artemisia freyniana (Table 1, Figs. 8c and 15).
Pollen grains prolate. Almost circular in equatorial view and trilobate
circular in polar view. Apertures tricolporate. The exine near the colpi
gradually thinned. P=23.39±1.21µm, E=21.30±1.07µm, P/E=1.10±0.04, T=3.17±0.26µm, L=21.29±0.95µm, T/L=0.15±0.01. The exine
ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.56±0.05µm, H=0.40±0.06µm, D/H=1.40±0.15, Gs=0.20±0.05µm, Ss=1.15±0.15µm,
Gs/Ss=0.18±0.05.
Habitat: steppes, slopes, dry river valleys, riverbanks, and outer forest
margins.
Artemisia stechmanniana (Table 1, Figs. 9a and 15).
Pollen grains prolate or spheroidal. Almost circular in equatorial view and
trilobate circular in polar view. Apertures tricolporate. The exine near the
colpi gradually thinned. P=26.31±1.48µm, E=25.16±1.22µm, P/E=1.05±0.07, T=3.97±0.60µm, L=23.45±1.38µm, T/L=0.17±0.02. The
exine ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.37±0.05µm, H=0.35±0.05µm, D/H=1.07±0.25, Gs=0.19±0.04µm, Ss=1.40±0.24µm,
Gs/Ss=0.14±0.04.
Habitat: hillsides, roadsides, shrubland, and forest-steppe areas, and often
becoming the dominant species or main associated species of plant
communities in some areas of mountainous sunny slopes.
Artemisia pontica (Table 1, Figs. 9b and 15).
Pollen grains prolate or spheroidal. Almost circular in equatorial view and
trilobate circular in polar view. Apertures tricolporate. The exine near the
colpi gradually thinned. P=20.64±1.54µm, E=19.62±1.59µm, P/E=1.05±0.07, T=3.01±0.39µm, L=19.75±0.84µm, T/L=0.15±0.02. The
exine ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.60±0.11µm, H=0.37±0.06µm, D/H=1.63±0.37, Gs=0.17±0.04µm, Ss=1.32±0.27µm,
Gs/Ss=0.13±0.04.
Habitat: rocky slopes, dry valleys, steppes, and hills; low to middle
elevations.
Artemisia frigida (Table 1, Figs. 9c and 15).
Pollen grains prolate or spheroidal. Almost circular in equatorial view and
trilobate circular in polar view. Apertures tricolporate. The exine near the
colpi gradually thinned. P=25.11±1.75µm, E=24.90±1.48µm, P/E=1.01±0.07, T=4.61±0.74µm, L=24.83±1.27µm, T/L=0.19±0.02. The
exine ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.46±0.08µm, H=0.32±0.04µm, D/H=1.44±0.26, Gs=0.31±0.08µm, Ss=1.30±0.18µm,
Gs/Ss=0.24±0.06.
Habitat: steppes, sub-alpine meadows, dry hillsides, stable dunes, and dry waste
areas; 1000–4000 m.
Artemisia rupestris (Table 1, Figs. 10a and 15).
Pollen grains prolate or spheroidal. Almost circular in equatorial view and
trilobate circular in polar view. Apertures tricolporate. The exine near the
colpi gradually thinned. P=24.45±1.41µm, E=22.92±1.40µm, P/E=1.07±0.08, T=3.18±0.40µm, L=21.96±1.15µm, T/L=0.14±0.02. The
exine ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.55±0.05µm, H=0.33±0.04µm, D/H=1.68±0.28, Gs=0.25±0.07µm, Ss=0.91±0.11µm,
Gs/Ss=0.28±0.09.
Habitat: dry hills, desert or semidesert steppes, grassy marshlands, dry
river valleys, riverbeds, scrub, and forest margins.
Artemisia sericea (Table 1, Figs. 10b and 15).
Pollen grains spheroidal or oblate. Almost circular in equatorial view and
trilobate circular in polar view. Apertures tricolporate. The exine near the
colpi gradually thinned. P=26.31±1.31µm, E=27.90±1.67µm, P/E=0.94±0.03, T=3.75±0.32µm, L=26.89±2.12µm, T/L=0.14±0.01. The
exine ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.89±0.09µm, H=0.54±0.10µm, D/H=1.71±0.36, Gs=0.28±0.07µm, Ss=1.74±0.31µm,
Gs/Ss=0.16±0.05.
Habitat: forest margins, hills, steppes, canyons, and waste areas.
Artemisia absinthium (Table 1, Figs. 10c and 15).
Pollen grains prolate. Almost circular in equatorial view and trilobate
circular in polar view. Apertures tricolporate. The exine near the colpi
gradually thinned. P=22.79±1.22µm, E=20.84±1.11µm, P/E=1.09±0.05, T=3.39±0.31µm, L=19.92±1.74µm, T/L=0.17±0.01. The exine
ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.59±0.05µm, H=0.40±0.06µm, D/H=1.52±0.25, Gs=0.18±0.04µm, Ss=1.11±0.15µm,
Gs/Ss=0.16±0.04.
Habitat: hillsides, steppes, scrub, forest margins, and often in locally moist
situations; 1100–1500 m.
Artemisia abrotanum (Table 1, Figs. 11a and 15).
Pollen grains prolate or spheroidal. Almost circular in equatorial view and
trilobate circular in polar view. Apertures tricolporate. The exine near the
colpi gradually thinned. P=24.47±1.56µm, E=23.73±1.65µm, P/E=1.03±0.07, T=3.15±0.28µm, L=18.82±0.81µm, T/L=0.17±0.01. The
exine ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.72±0.10µm, H=0.51±0.05µm, D/H=1.44±0.25, Gs=0.22±0.04µm, Ss=1.41±0.19µm,
Gs/Ss=0.16±0.04.
Habitat: the wasteland of western, southern, central, and southern Europe.
Artemisia blepharolepis (Table 1, Figs. 11b and 15).
Pollen grains spheroidal. Almost circular in equatorial view and trilobate
circular in polar view. Apertures tricolporate. The exine near the colpi
gradually thinned. P=18.96±0.98µm, E=19.26±0.99µm, P/E=0.99±0.05, T=3.15±0.28µm, L=18.82±0.81µm, T/L=0.17±0.01. The exine
ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.69±0.09µm, H=0.44±0.07µm, D/H=1.64±0.44, Gs=0.37±0.18µm, Ss=1.68±0.20µm,
Gs/Ss=0.23±0.14.
Habitat: low-altitude areas of dry slopes, grasslands, steppes, waste areas,
roadsides, and dunes near riverbanks.
Artemisia norvegica (Table 1, Figs. 11c and 15).
Pollen grains prolate. Almost circular in equatorial view and trilobate
circular in polar view. Apertures tricolporate. The exine near the colpi
gradually thinned. P=24.51±1.40µm, E=22.11±1.05µm, P/E=1.11±0.06, T=3.48±0.39µm, L=22.61±1.31µm, T/L=0.15±0.01. The exine
ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.67±0.08µm, H=0.43±0.11µm, D/H=1.66±0.51, Gs=0.19±0.03µm, Ss=1.56±0.24µm,
Gs/Ss=0.12±0.03.
Habitat: bare stony ground, Racomitrium heath, bouldery crests of
solifluction terraces, and sometimes hollows between rocks.
Artemisia tanacetifolia (Table 1, Figs. 12a and 15).
Pollen grains prolate or spheroidal. Almost circular in equatorial view and
trilobate circular in polar view. Apertures tricolporate. The exine near the
colpi gradually thinned. P=28.38±0.90µm, E=27.75±1.70µm, P/E=1.03±0.06, T=3.46±0.47µm, L=27.63±1.06µm, T/L=0.13±0.02. The
exine ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.71±0.06µm, H=0.32±0.04µm, D/H=2.23±0.40, Gs=0.30±0.07µm, Ss=1.08±0.16µm,
Gs/Ss=0.29±0.07.
Habitat: middle and low-altitude areas of forest grasslands, grasslands,
meadows, forest edges, open forests, salty grasslands, grass slopes, and
brushwood.
Artemisia tournefortiana (Table 1, Figs. 12b and 15).
Pollen grains prolate or spheroidal. Almost circular in equatorial view and
trilobate circular in polar view. Apertures tricolporate. The exine near the
colpi gradually thinned. P=20.76±0.98µm, E=20.43±0.83µm, P/E=1.02±0.06, T=3.33±0.19µm, L=20.03±0.79µm, T/L=0.17±0.01. The
exine ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.73±0.06µm, H=0.42±0.07µm, D/H=1.81±0.33, Gs=0.26±0.07µm, Ss=1.25±0.20µm,
Gs/Ss=0.22±0.08.
Habitat: widely distributed on hills, terraces, dry flood lands, waste
fields, steppes, open forests, and semi-marshlands.
Artemisia dracunculus (Table 1, Figs. 12c and 15).
Pollen grains spheroidal. Almost circular in equatorial view and trilobate
circular in polar view. Apertures tricolporate. The exine near the colpi
gradually thinned. P=22.89±1.24µm, E=22.87±1.32µm, P/E=1.00±0.05, T=2.82±0.52µm, L=21.91±1.35µm, T/L=0.13±0.03. The exine
ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.68±0.05µm, H=0.45±0.07µm, D/H=1.56±0.31, Gs=0.31±0.10µm, Ss=0.92±0.15µm,
Gs/Ss=0.34±0.11.
Habitat: dry slopes, steppes, semidesert steppes, forest steppes, forest
margins, waste areas, roadsides, terraces, subalpine meadows, meadow
steppes, dry river valleys, rocky slopes, and saline–alkaline soils; 500–3800 m.
Artemisia japonica (Table 1, Figs. 13a and 15).
Pollen grains spheroidal or oblate. Almost circular in equatorial view and
trilobate circular in polar view. Apertures tricolporate. The exine near the
colpi gradually thinned. P=20.18±1.28µm, E=21.23±1.26µm, P/E=0.95±0.05, T=4.24±0.49µm, L=21.02±1.14µm, T/L=0.20±0.02. The
exine ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.57±0.05µm, H=0.32±0.05µm, D/H=1.80±0.24, Gs=0.26±0.05µm, Ss=1.26±0.16µm,
Gs/Ss=0.21±0.04.
Habitat: forest margins, waste areas, shrublands, hills, slopes, and roadsides.
Low elevations to 3300 m.
Artemisia capillaris (Table 1, Figs. 13b and 15).
Pollen grains spheroidal or oblate. Almost circular in equatorial view and
trilobate circular in polar view. Apertures tricolporate. The exine near the
colpi gradually thinned. P=19.53±1.09µm, E=19.64±1.62µm, P/E=1.00±0.08, T=3.54±0.34µm, L=19.18±0.97µm, T/L=0.18±0.01. The
exine ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.51±0.06µm, H=0.36±0.04µm, D/H=1.44±0.30, Gs=0.26±0.04µm, Ss=1.27±0.16µm,
Gs/Ss=0.21±0.05.
Habitat: humid slopes, hills, terraces, roadsides, and riverbanks; 100–2700 m.
Artemisia campestris (Table 1, Figs. 13c and 15).
Pollen grains prolate or spheroidal. Almost circular in equatorial view and
trilobate circular in polar view. Apertures tricolporate. The exine near the
colpi gradually thinned. P=21.69±0.85µm, E=21.26±0.89µm, P/E=1.02±0.07, T=3.68±0.33µm, L=21.21±0.89µm, T/L=0.17±0.02. The
exine ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.57±0.09µm, H=0.38±0.05µm, D/H=1.53±0.23, Gs=0.41±0.09µm, Ss=1.23±0.19µm,
Gs/Ss=0.34±0.08.
Habitat: steppes, waste areas, rocky slopes, and dune margins; 300–3100 m.
Kaschgaria brachanthemoides (Table 1, Figs. 14a and 15).
Pollen grains prolate or spheroidal. Almost circular in equatorial view and
trilobate circular in polar view. Apertures tricolporate. The exine near the
colpi gradually thinned. P=23.26±1.44µm, E=22.09±1.18µm, P/E=1.06±0.08, T=3.93±0.44µm, L=21.01±1.28µm, T/L=0.19±0.02. The
exine ornamentation is psilate (LM), spinulate (SEM). Under SEM, D=0.55±0.07µm, H=0.44±0.05µm, D/H=1.25±0.20, Gs=0µm, Ss=1.75±0.20µm, Gs/Ss=0,
perforations spacing (Ps)=0.47±0.14µm.
Habitat: dry mountain valleys, and old dry riverbeds; 1000–1500 m.
Ajania pallasiana (Table 1, Figs. 14b and 15).
Pollen grains spheroidal. Almost circular in equatorial view and trilobate
circular in polar view. Apertures tricolporate. The exine near the colpi
gradually thinned. P=35.16±2.68µm, E=35.92±3.31µm, P/E=0.98±0.03, T=10.23±0.85µm, L=38.31±2.06µm, T/L=0.27±0.03µm. The exine
ornamentation spinose. Under SEM, D=4.41±0.35µm, H=3.47±0.38µm, D/H=1.29±0.21, Gs=0µm, Ss=7.84±1.25µm, Gs/Ss=0, Ps=0.39±0.12µm.
Habitat: thickets and mountain slopes; 200–2900 m.
Chrysanthemum indicum (Table 1, Figs. 14c and 15).
Pollen grains prolate or spheroidal or oblate. Almost circular in equatorial
view and trilobate circular in polar view. Apertures tricolporate. The exine
near the colpi gradually thinned. P=33.54±1.71µm, E=34.42±2.46µm, P/E=0.98±0.08, T=8.65±0.89µm, L=34.82±1.65µm, T/L=0.25±0.02.
The exine ornamentation spinose. Under SEM, D=2.94±0.33µm,
H=3.59±0.29µm, D/H=0.82±0.10, Gs=0µm, Ss=7.11±0.76µm, Gs/Ss=0, Ps=0.37±0.13µm.
Habitat: grasslands on mountain slopes, thickets, wet places by rivers,
fields, roadsides, saline places by seashores, and under shrubs; 100–2900 m.
List of the voucher specimen in PE Herbarium, Institute of Botany, Chinese Academy of Sciences.
Note: in the absence of habitat photographs of two species, habitat
photographs of species with which they have close phylogenetic relationships
and similar habitats were used in this study instead, i.e. the habitat
photograph of Kaschagaria komarovii was used instead of Kaschagaria brachanthemoides, and the habitat photograph of Artemisia taurica for Artemisia kurramensis. * Last access: 19 August 2022
Note: in the absence of habitat photographs of two species, habitat
photographs of species with which they have close phylogenetic relationships
and similar habitats were used in this study instead, i.e. the habitat
photograph of Kaschagaria komarovii was used instead of Kaschagaria brachanthemoides, and the habitat photograph of Artemisia taurica for Artemisia kurramensis. * Last access: 19 August 2022
List of the voucher specimens in PE Herbarium, Institute of
Botany, Chinese Academy of Sciences. Sample no. 0 was the specimen for
cluster analysis. Sample nos. 1–4 were used in testing intraspecific
variability in pollen exine ultrastructure characters among three
representative species.
SampleSWS type LNS type SG type no.Artemisia vulgarisArtemisia annuaArtemisia maritimaSpecimen barcodesColl. no.Specimen barcodesColl. no.Specimen no.Coll. no.0PE 01669703P.Frost-Olsen 1833PE 01197344Wen-Hong Jin-Tian, Kai-Yong Lang, Ge Yang 328no. 1338063s.n.1PE 0053241775-1521PE 00420433Xue-Zhong Lang328no. 209452G. Belloteau 25 September 19122PE 00492025K.M.Liou L.6601PE 00420647T.N.Liou & C.Wang 731no. 209446s.n.3PE 00492038P.C.Hoch, Jia-Rui Chen 86077PE 00420660Da-Shun Wang 856s.n.Hanelt Schultze-Motel 4464PE 00492029Hong-Bin Cui, You-Run Lin, Zhen-Dai Xia 80-290PE 00420664Lei,C.I. 858s.n.O. Nordstedt 9 October 1901Author contributions
YFW, YFY, and TGG conceived the ideas; LLL, BHJ, KQL, and
BS collected the literature; LLL extracted and compiled the data, LLL, FQ,
and BHJ made the statistical analysis; GX and ML collected pictures; LLL,
KQL, and BS drew the figures and tables; LLL, YFW, YFY, JFL, FQ, and GX
wrote the first draft of this article; DKF corrected the various versions
of the article; and all authors contributed substantially to revisions.
Competing interests
The contact author has declared that none of the authors has any competing interests.
Disclaimer
Publisher's note: Copernicus Publications remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Acknowledgements
We thank Jian Yang, Institute of Botany, Chinese
Academy of Sciences, for his kind help in drafting graphics. We appreciate
Chen Chen from Institute of Botany, Chinese Academy of Sciences, Ji-Ye Zheng
from No. 1 Middle School of Jiyang Shandong, Jia-Hao Shen from Institute
of Botany, Jiangsu Province and Chinese Academy of Sciences (Nanjing
Botanical Garden Mem. Sun Yat-Sen), and from Almaty, Kazakhstan, for their enthusiastic assistance in
providing habitat photographs.
Financial support
This research was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (grant no. XDB26000000), National Natural Science Foundation of China (grant nos. 31970233, 32070240, 31870179, 31570204, 42077416, 32000174 and 42077423), the Chinese Academy of Sciences President’s International Fellowship Initiative (grant no. 2018VBA0016), the Sino-Africa Joint Research Center (grant no. SAJC201614), Key Project at Central Government Level: the ability establishment of sustainable use for valuable Chinese medicine resources (grant no. 2060302), National Plant Specimen Resource Bank (grant no. E0117G1001), and the International Partnership Program of Chinese Academy of Sciences (grant no. 151853KYSB20190027).
Review statement
This paper was edited by Alessio Rovere and reviewed by Angela Bruch and one anonymous referee.
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