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165
NJB, Volume 36 (2), 165-184, Dec., 2023
TAXONOMIC SIGNIFICANCE OF THE POLLEN MORPHOLOGY OF FAMILY COMBRETACEAE
R.BR. (MYRTALES) FROM NIGERIA
1Mudasiru, O.M., 2Ayodele, A. E., 3 Rana, T.S. and 4Pandey, S.
1Department of Pure and Applied Botany, Federal University of Agriculture Abeokuta, Nigeria
2Department of Botany, University of Ibadan, Ibadan, Nigeria
3Plant Diversity, Systematics and Herbarium Division, CSIR-National Botanical Research Institute, Rana Pratap
Marg, Lucknow-226001, Uttar Pradesh, India
4, Quaternary Palynology Laboratory, Birbal Sahni Institute of Paleosciences, 53 University Road, Lucknow-
226007, Uttar Pradesh, India Correspondence: mudasiruom@funaab.edu.ng
Received 11th September, 2023; accepted 14th October, 2023
ABSTRACT
A comparative study of pollen morphological characters of 19 species of Combretaceae from
Nigeria was undertaken with a view to obtaining additional characters for adequate identification
and classification of the taxa. Pollen samples were acetolysed and investigated under light
microscope. Hierarchical cluster analysis was employed to show the similarities and affinity among
the Combretaceae species based on pollen-morphological features. All the species studied were
monads, small to medium sized, radially symmetrical, heterocolpate with three simple apertures
alternating with three composites. The exine showed various sculpturing patterns in all the taxa
studied, namely, micro-rugulate, reticulate, scabrate, striate and psilate. The pollen size ranged from
10 to 50 μm. The largest pollen size (42.68 × 38.17 μm) was recorded in C. platypterum and the
smallest one (14.75×15.05 μm) in C. sordidum. The species had prolate, sub-prolate and oblate-
spheroidal pollen shapes. The dendrogram and bi-plot revealed nested grouping of the Quisqualis
species within Combretum sub-genus Cacoucia. Palynomorphological characters of the studied
species are considered highly diagnostic at the generic and specific levels. Therefore, pollen
morphological data provide diagnostic information for differentiating Combretum platypterum and
C. racemosum, C. zenkeri, C. smeathmannii, C. sordidum, Terminalia catappa and T. mantaly,
which are morphologically similar species.
Key words: Combretaceae; heterocolpate; palynology; taxonomy, Nigeria
https://dx.doi.org/10.4314/njbot.v36i2.6
Open Access article distributed under the terms of Creative Commons License (CC BY-4.0)
INTRODUCTION
Combretaceae also known as Almond family is one of the most diversified groups of Angiosperms in the Order
Myrtales. The family includes 20 genera with over 500 species of trees, shrubs and lianas which are found across
tropical and subtropical areas of the world. The greatest genetic diversity is inAfrica and Southeast Asia and very
often in the savannah (Angiosperm Phylogeny Group, 2009). Combretum Loefl. is the largest genus in this family
with about 250 species, while Terminalia (with about 200 species) is the second largest genus (Mudasiru et al.,
2016). Several species of the Combretaceae have been reported as commercially important materials for food,
herbal medicines, furniture, cosmetics, pharmaceutical, horticultural and silvicultural purposes. Many species in
the family exhibit biological activities like anti-microbial, anti-haemorrhagic, anti-ulcer, anti-cancer activities and
are in great demand world-wide for the extraction of phytochemicals like alkaloids, flavonoids, glycoside
derivatives, pentacyclic triterpenes, tannins and other aromatic compounds (Fyhrquist, 2007).
Combretaceae was first named by Robert Brown in 1810 (Brown, 1810). He included nine genera for the
first time, namely Combretum, Cacoucia, Chuncoa, Quisqualis, Bucida, Terminalia, Conocarpus, Laguncularia
and Getonia but he did not classify them. The classification of Combretaceae has been unstable over the years
because of the different positions authors adopted for the sub-families, tribes and genera (Tan et al., 2002; Maurin
et al., 2010). The family is divided into two sub-families (Strephonematoideae Engl. et Diels and Combretoideae
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NJB, Volume 36 (2), Dec, 2023 Mudasiru, O. M. et al.
Engl. and Diels). The first one contains the single genus Strephonema Hook f. while the latter comprises most of
the genera. Combretoideae includes 19 genera (Anogeissus, Buchenavia, Bucida, Calycopteris, Calopyxis,
Combretum, Conocarpus, Dansiea, Getonia, Guiera, Gyrocarpus, Laguncularia, Lumnitzera, Meiostemon,
Pteleopsis, Quisqualis, Terminalia, Terminaliopsis and Thiloa) which are characterised by inferior ovary and seeds
with small, folded or spirally twisted cotyledons (Chen and Turland, 2007). The Combretoideae genera are not
sharply delimited and are difficult to classify based on their leaves, flowers, fruits and seeds, because of the
morphological plasticity.
The classification of the sub-family Combretoideae within the family Combretaceae has been very
ambiguous. Engler and Diels in 1899 grouped the sub-family into four tribes: Calycopterideae, Combreteae,
Laguncularieae and Terminalieae. Exell (1931) noted that the tribe Laguncularieae is a much more distinct group
than the other three tribes and that it merits a different group. Within the Combretoideae, Stace (1966) emphasised
that the tribe Laguncularieae is a very distinct one, characterised by having a pair of adnate bracteoles on the lower
receptacle, and thus he considered the other three tribes to comprise the single tribe Combreteae. Tan et al. (2002)
merged the three tribes (Combreteae, Terminalieae and Calycopterideae) into one tribe, Combreteae and retained
the Laguncularieae as a distinct tribe. Exell and Stace (1966) published the Combretaceae classification, which
was different from that of Stace (1966) in that 3 sub-tribes were recognised in the tribe Combreteae (containing
seven genera: Calopysis, Combretum, Guiera, Quisqualis and Thiloa), Pteleopsidinae (containing only Pteleopsis)
and Terminaliinae (comprising 5 genera: Terminalia, Ramatuella Kunth., Bucida Linn., Buchenavia Eichl.,
Anogeissus, Finetia Gagnep. and Conocarpus). The sub-tribe Pteleopsidinae is now inseparable from the subtribe
Terminaliinae on any single character because they are very closely related. Shared morphological characters
among Pteleopsis, Combretum and Terminalia formed the basis for the placement of Pteleopsis as a sub-tribe
(Exell and Stace, 1966). Pteleopsis possesses morphological attributes of Combretum and Terminalia and is a tree
or shrub that resembles both Combretum and Terminalia. The flowers have petals and resemble a Combretum, but
there are male flowers as well as bisexual flowers in the same inflorescence as in Terminalia. Additional revisions
on Pteleopsis by Van Vliet and Vollesen presented new evidence for merging the two sub-tribes, Terminaliinae
and Pteleopsidinae (Vollesen, 1981). As a result, the circumscription and definition of the tribes and sub-tribes of
this family are still unsettled and most local treatments have described species without reference to the affiliation
of the sub-families (Jordaan, 2003).
The family Combretaceae is a taxonomically and phylogenetically complex group. Over the past years,
many taxonomic problems remain within Combretaceae, which has never been satisfactorily classified into tribes,
sub-tribes, genera and sections. Phylogenetic relationships within Combretaceae remain one of the biggest
unresolved issues in the taxonomy of the family with most of the studies conducted on the tribe Combreteae so far
being on the temperate taxa and a few representatives of some tropical taxa. Still, these studies rarely reflect the
intricate pattern of character variation within a more robust group of tropical taxa in the family. The taxonomy of
the family Combretaceae is very complex and challenging due to the lack of sufficient taxonomical characters and
the existence of morphotypes. This family has been a subject of many academic researches both locally and
internationally. The recent treatment of Combretaceae by Maurin et al. (2010) based on molecular analysis divided
the tribe Combreteae into two sub-tribes but neither of them (Combretinae or Terminaliinae) considered
morphological and anatomical characters. The only available but rather obsolete major taxonomic treatment of the
Combretaceae in Nigeria by Hutchinson and Dalziel (1972) and Keay (1989) treated Quisqualis congeneric with
Combretum. Quisqualis species are, for instance, difficult to separate from Combretum; Ramatuella, Pteleopsis
and Termiinaliopsis are very close to Terminalia. Little is also known of the intricate pattern of character variation
within Pteleopsis and Terminalia. Pteleopsis links the two biggest genera, Combretum and Terminalia, within the
tribe Combreteae. On the inflorescence, the flowers of Pteleopsis species possess petals and resemble members of
Combretum while there are male flowers as well as bisexual flowers in the same stalk as in Terminalia. Moreover,
the Nigerian genera and species have not been studied in totality and comparatively in terms of basic research
documentation. This study was conducted to determine and evaluate the qualitative and quantitative pollen
morphological characteristics of Combretaceae with a view to improving the identification of the taxa and ascertain
the phylogenetic relationships amongst members of the family in Nigeria.
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NJB, Volume 36 (2), Dec, 2023 Taxonomic Significance of Pollen of Combretaceae
MATERIALS AND METHODS
Study area and sample collection
All the pollen grains that were used in this study were collected from different locations within Nigeria (Table 1,
Figure 1). Plant identification and authentication were done at the University of Ibadan Herbarium (UIH), Nigeria,
where voucher specimens were also deposited for future reference. All collections were made in the field. The
geo-coordinates (latitude/longitude) and elevation (altitudes) of the location for each specimen were determined
with Global Positioning System (GPS). A complete list of taxa including date of collection, site of collection,
collector’s name, voucher number, GPS coordinates and altitudes are provided in Table 1.
Preparation of pollen grains
The pollen grains of 19 species of the family Combretaceae were subjected to pollen analysis which included
acetolysis at the Palynology Unit of Quaternary Laboratory, Birbal Sahni Institute of Palaeobotany (BSIP)
Lucknow, India.
The pollen grains obtained from fresh flower buds containing anthers of the nineteen Combretaceae
species were acetolysed using the Erdtman (1966) acetolysis method, as modified by Pandey and Minkley (2018).
A mixture of acetic anhydride and concentrated sulphuric acid in the ratio of 9:1 (45 ml acetic anhydride and 5ml
concentrated tetraoxosulphate VI (H2SO4)) was used. The flowers of the taxa collected were cut using a blade and
put in 50 ml plastic centrifuge tubes clearly labelled. They were crushed with a glass rod in centrifuge tube. Three
cubic centimetre (3 cm3) of freshly prepared Acetolysis mixtures was added to the contents in the tubes. Each tube
was equipped with a glass stirring rod and the contents were stirred at regular intervals. The contents were heated
in a glass stirring rod and the contents were stirred at regular intervals. The contents were heated in a water bath
from 70oC up to boiling point for 5 minutes. The hot contents were centrifuged at 4000 rpm for 10 minutes and
then the supernatant was decanted into “acetolysis waste bottle”. Distilled water was added to the mixture in the
tubes and then shaken thoroughly, centrifuged for 5 minutes at 3,000 rpm and the residue was decanted in the tube.
This was to remove the excess acetolysis mixture. The washing with water and centrifuging were done 5 times.
Finally, the samples were prepared in 50% glycerine solution for examination under the microscope.
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NJB, Volume 36 (2), Dec, 2023 Mudasiru, O. M. et al.
Figure 1: Map of study area showing the geographical locations and distribution of the Nigerian species of
Combretaceae
Preparation of slides
After preparation, each sample was mounted on a pair of slides and a drop of DPX (Dibutylphthalate Polystyrene
Xylene) mountant was placed at the centre of the slide. The air-dried cover slip was taken upside down and placed
on the drop of the mountant at the centre of the slide. A little pressure with the finger was applied to cause a
complete spread, after which it was ready for microscopic study. All samples were studied under Olympus CH30
light microscopes with attached digital camera (3.2 MP LX) using both x40 and x100 objective lenses. A pre-
calibrated microscope with micrometre eye piece was used for observation and measurements. Pollen grains were
described based on the following characters: shape, size, exine pattern, apertural type number and character.
Qualitative characters such as types and shapes of pollen grains were assessed and recorded for each species. The
size of each pollen grain was measured based on the polar axis (PA) and equatorial diameter (ED) and the
corresponding PA/ED ratio of the pollen recorded. All measurements of the pollen, and pollen characters were
done in equatorial view and were presented in µm. The mean, range (minimum-maximum) and standard deviation
values were calculated with the aid of micrometre for all the quantitative characters such as diameter of pollen
grains, wall thickness of colpi, polar axis (P), equatorial diameter (E) of pollen grains and so on, based on twenty-
five measurements. Descriptive terminologies and slide preparations of the pollen were based on
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NJB, Volume 36 (2), Dec, 2023 Taxonomic Significance of Pollen of Combretaceae
Erdtman (1966) and Ayodele (2005) procedures. All slides were submitted to the BSIP Herbarium, Lucknow,
India and University of Ibadan Herbarium in Nigeria.
Data analysis
Both qualitative and quantitative pollen data obtained from this study were subjected to descriptive and
multivariate statistical analyses. The mean values of all the quantitative data of Combretaceae were calculated with
the range (minimum-maximum) and standard deviation. The pollen polar diameter, pollen equatorial diameter,
colpi length, exine thickness, ora width, amb, exine pattern, pollen shape class, aperture and pollen size were
scored and coded. Single linkage cluster analysis (SLCA) was performed using the Paleontological Statistical
Software (PAST, version 4.13) package (Hammer et al., 2023) and Gower Distance to determine how similar the
groups were, from which a dendrogram representing the phylogenetic relationships among the Combretaceae
species was generated following Arogundade et al. (2019). Current sub-tribal and sectional classification of the
family Combretaceae in the study were according to Alwan (1983) and APG III (2009).
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NJB, Volume 36 (2), Dec, 2023 Mudasiru, O. M. et al.
Table 1: List of Combretaceae species collected from different geographical locations in Nigeria collected for this study
GPS = Global Positioning System
S/N
Taxa
Voucher
No.
Site of Collection
Date of
Collection
Collector’s
Name
GPS Coordinates
Elevation
(m)
Latitude
Longitude
1.
Anogeissus leiocarpus (DC.)
Guill. & Perr.
22501
Okomu National Park, Edo State
06/04/2018
Mudasiru, O.M.
Ayodele A.E
N06° 20' 35.7"
E005° 21' 38.92"
66
2.
Combretum glutinosum
Perr. ex DC.
22515
Behind Central Mosque, Wikki Camp,
Yankari Game Reserve, Bauchi State
08/06/2018
Mudasiru O. M.
Ayodele A.E
N09° 49' 18.23"
E10° 19' 15.28"
424
3.
Combretum molle R.Br. ex
G.Don
22610
Kasuwa Goro Street, off Maiduguri Road, Kano
State
05/05/2018
Mudasiru O. M.
Ayodele A.E
N 11° 56' 44.7"
E008° 36' 46.87"
471
4.
C. paniculatum Vent.
22514
Holiness Estate, Idi-Omo, Off Arulogun
Road, Ibadan
26/06/2022
Mudasiru, O.M.
Ayodele A.E
N07° 30' 16.99"
E003° 57' 9.04"
244
5.
C. platypterum (Welw.) Hutch.
& Dalz.
22522
Olode-Ijaye Village, Ibadan, Oyo State
07/07/2018
Mudasiru, O.M.
Ayodele A.E
N07° 37' 52.21"
E003° 47' 51.04"
237
6.
C. racemosum P. Beauv.
22601
Obudu Cattle Ranch, Ikwette, Cross River
State
11/02/2018
Mudasiru, O.M.
N07° 24' 26.35"
E009° 23' 55.82"
746
7.
C. sordidum Exell.
22547
Off PG School Road, University of Ibadan,
Nigeria
21/07/2018
Mudasiru, O.M.
N07° 26' 49.02"
E003° 54' 5.47"
225
8.
C. smeathmannii G.Don
22462
Along Jericho GRA, Ibadan
22/07/2018
Mudasiru, O.M.
N07° 25' 37.78"
E003° 54' 7.60"
173
9.
Combretum hispidum Laws.
22546
Along Jericho Specialist Hospital, Ibadan
20/07/2018
Mudasiru, O.M.
N07° 24' 31.07"
E003° 53' 26.48"
188
10.
C. zenkeri Engl. & Diels
22510
Sabongida Ora, Owan West, Edo State
14/05/2018
Mudasiru, O.M.
Ayodele A.E
N06° 53' 34.26"
E005° 44' 40.81"
53
11.
Guiera senegalensis J.F.
Gmel.
22676
Off Gwadabawa Kasuwa, Gwadabawa Sokoto
State
14/12/2017
Mudasiru, O.M.
Ayodele A.E
N13° 22' 38.24"
E005° 13' 18.59"
262
12.
Pteleopsis habeensis Aubrev
ex Keay
22482
Opposite Museum, Yankari Game
Reserve, Bauchi
08/06/2018
Mudasiru, O.M.
Ayodele A.E
N10° 19' 15.67"
E009° 49' 18.44"
393
13.
P. suberosa Engl. & Diels
22431
Along Wawa-Babana Road, Wawa, Niger
State
19/12/2017
Mudasiru, O.M.
N09° 54' 36.43"
E004° 24' 4.79"
248
14.
Quisqualis indica Linn.
22491
Along Alabata Road, Abeokuta, Ogun
State
14/06/2018
Mudasiru, O.M.
N07° 11' 48.62"
E003° 26' 20.26"
51
15.
Q. latialata (Engl. ex Engl.
& Diels) Exell
22555
Iguelaba Village, Sapoba Forest Reserve
Community,
Orhionmwon LGA, Edo State
05/07/2018
Mudasiru, O.M.
Ayodele A.E
N06° 4' 32.44"
E005° 49' 8.94"
74
16.
Terminalia catappa Linn.
22552
Department of Botany, University of Ibadan,
Nigeria
22/07/2018
Mudasiru, O.M.
N07° 23' 53.02"
E003° 54' 55.01"
228
17.
T. glaucescens Planch. ex
Benth.
22502
Along Coulthard way, Yankari Game
Reserve, Bauchi
09/06/2018
Mudasiru, O.M.
Ayodele A.E
N09° 57' 3.96"
E10° 30' 47.23"
337
18.
T. mantaly H. Perrier
22465
NIFOR Club, Nigerian Institute for Oil Palm
Research, Benin City
05/04/2018
Mudasiru, O.M.
Ayodele A.E
N06° 33' 25.78"
E005° 37' 20.82"
53
19.
T. superba Engl. & Diels
22416
Oluwa Forest Reserve, Ondo State
22/06/2018
Mudasiru, O.M.
N06° 49' 27.01"
E004° 43' 16.43"
34
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NJB, Volume 36 (2), Dec, 2023 Taxonomic Significance of Pollen of Combretaceae
RESULTS
Descriptions of Pollen Grains
Pollen morphology of 19 species from six Combretaceae genera was investigated using the light microscopy. The
qualitative and quantitative characters obtained are listed in Table 2, while representative pollen grains are shown
in Figure 2 A-Al. Pollen grains of the species studied were monads, radially symmetrical, isopolar, small to
medium-sized and heterocolpate with three simple apertures alternating with three composite ones. The number
of subsidiary colpi and intercolpar concavities within the family were the same as the apertures and alternates with
them. Five main types of pollen grains sculpturing were recognised in the family. These include fine reticulate in
Combretum platypterum, C. racemosum, C. smeathmannii, Guiera senegalensis, Quisqualis indica; micro-
rugulate in Anogeissus leiocarpus, Pteleopsis habeensis, P. suberosa, Combretum molle, Terminalia catappa, T.
mantaly, T. superba; psilate in T. glaucescens; reticulate in Combretum paniculatum and C. hispidum; scabrate in
Quisqualis latialata and striate in Combretum sordidum, C. glutinosum and C. zenkeri. Micro-rugulate was the
common type of tectum surface ornamentation among the species, since it occured in 7 species in 4 genera (Table
2). Hexacolpate and octacolpate pollen grains were observed in this study. Octacolpate characteristic features were
only found on the polar axis of Combretum zenkeri (Figure 2 A-Al). On the same polar diameter, the amb outlines
were characteristically hexagonal in all the taxa except C. glutinosum and C. molle which were circular in shape
(Figure 2 A-C, Ae-Af). Based on pollen shape, many taxa of Combretaceae had prolate shape while a few
possessed oblate and subprolate spheroidal types (Table 2, Figure 2 A-Al). Only Quisqualis indica and Q. latialata
had oblate-spheroidal shape.
Comparative Pollen Morphology and Morphometric Analysis of the Pollen Character States
The results demonstrated that all the species studied exhibited wide inter-specific variations with respect to the
overall size of polar axes (P) and equatorial diameters (E), shape classes, the ratios of P/E, exine thickness and ora
features. The largest size of pollen (42.68 × 38.17 μm) was recorded in Combretum platypterum and the smallest
one (14.75 × 15.05 μm) in C. sordidum (table 2). The apertures of all the species had both colpi and lalongate ora
(an aperture in the inner layer of the sporoderm). The colpi length ranged from 11.83 μm in Combretum sp nov. A
to 36.22 μm in C. platypterum (Table 2). The ora width ranged from 1.2 μm in Guiera senegalensis to 7.5 μm in
C. platypterum. The minimum and maximum exine thickness were recorded as 0.84 μm in Combretum zenkeri
and 2.75 μm in Q. indica while the polar axis over equatorial diameter range from 0.87 (Q. indica) to 1.22 (P.
habeensis). The cluster and principal component analyses revealed the extent of affinity among 19 species of the
family Combretaceae (Figures 2 and 3). The cluster analysis of Combretaceae palynological data clearly separated
the species and two major clusters were found in the cladogram constructed through cluster analysis (Figure 2).
The first cluster consisted of only taxa of the genera Combretum Loefl. and Quisqualis Linn., namely Combretum
glutinosum, C. molle, C. paniculatum, C. platypterum, C. racemosum, Quisqualis indica, Q. latialata, Combretum
zenkeri, C. sordidum, C. smeathmannii, C. hispidum, while the second cluster comprised members of genera
Terminalia, Anogeissus, Pteleopsis and Guiera. T. catappa, T. glaucescens, T. superba, Terminalia mantaly,
Anogeissus leiocarpus, Pteleopsis habeensis, P. suberosa and Guiera senegalensis were found to be farther from
all other taxa in the group (Figure 3). The PCA yielded four groups and the position of each species in the PCA
showed evolutionary trend within the family Combretaceae (Figure 4). Amongst Combretum paniculatum, C.
racemosum, Quisqualis indica and Q. latialata, only Quisqualis indica and Q. latialata were identified by the PCA
as having a strong liking for one another in comparison to the other species (C. paniculatum and C. racemosum)
in the PCA. Within the species in the scatter diagram, only Q. indica and Q. latialata had tricolpate characteristic
feature and oblate-spheroidal pollen shape. The closeness of C. racemosum and C. paniculatum to Q. indica and
Q. latialata in the group is attested by the characters of pollen size (medium) and exine wall thickness (Figure 4).
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NJB, Volume 36 (2), Dec, 2023 Mudasiru, O. M. et al.
Table 2: Qualitative and quantitative pollen-grain morphological data of Combretaceae taxa
S/No.
Taxa
Polar axis
(P) (μm)
Equatorial
diameter (E) (μm)
Colpi length
(μm)
Exine
thickness
Ora
width
(μm)
P/E
Amb
Exine
pattern
Aperture
Shape class
Pollen Size
1.
Anogeissus
leiocarpus
15.0-16.3
(15.84±0.89)
14.7-15.1
(14.92±0.64)
11.7-12.5
(12.24±1.86)
1.2-1.3
(1.26±0.28)
2.5
1.06
6-lobed
Micro-
rugulate
Hexacolpate
Subprolate
Small
2.
Combretum
glutinosum
27.6-31.5
(28.25±1.25)
23.5-28.7
(26.95±0.32)
20.0-22.5
(21.43±0.76)
1.0-2.0
(1.70±0.31)
2.5
1.05
6-circular
Striate
Hexacolpate
Prolate-
spheroidal
Medium
3.
Combretum molle
25.4-27.9
(26.15±2.03)
24.2-29.5
(27.08±1.17)
21.0-24.5
(22.62±3.08)
1.0-2.0
(1.45±0.03)
2.5
1.09
6-circular
Faintly
micro-
rugulate
Hexacolpate
Subprolate
Medium
4.
C. paniculatum
22.7-28.9
(25.84±0.75)
21.5-25.1
(23.28±0.19)
20.5-24.5
(21.58±1.29)
1.5-2.5
(2.13±0.38)
2.5
1.11
6-angular
Reticula
te
Hexacolpate
Subprolate
Medium
5.
C. platypterum
40.0-45.0
(42.68±1.83)
35.5-40.2
(38.17±2.24)
35.1-37.5
(36.22±1.08)
2.5-2.8
(2.63±0.14)
7.5
1.12
6-angular
Fine
reticulate
Hexacolpate
Subprolate
Medium
6.
C. racemosum
25.1-30.5
(28.47±2.15)
22.5-27.2
(25.50±0.97)
20.5-25.3
(23.18±1.08)
2.5-2.52
(2.51±0.47)
2.5
1.12
6-angular
Fine
reticulate
Hexacolpate
Subprolate
Medium
7.
C. sordidum
14.5-15.0
(14.75±0.23)
15.0-15.2
(15.05±0.03)
11.7-12.0
(11.83±0.05)
1.2-1.3
(1.25±0.02)
1.3
0.98
6-angular
Striate
Hexacolpate
Prolate-
spheroidal
Small
8.
C. smeathmannii
26.5-31.5
(29.61±3.04)
24.8-28.1
(26.93±2.18)
20.5-23.0
(22.23±1.01)
1.0-2.0
(1.83±0.25)
1.3
1.10
6-angular
Fine
reticulate
Hexacolpate
Prolate-
spheroidal
Medium
9.
C. hispidum
17.5-20.0
(18.56±2.08)
15.0-17.5
(16.48±1.32)
15.0-16.0
(15.50±0.03)
2.5-2.6
(2.55±0.02)
2.5
1.13
6-angular
Reticulate
Hexacolpate
Subprolate
Small
10.
C. zenkeri
17.5-18.5
(17.94±2.15)
15.7-17.5
(16.88±0.76)
12.5-15.0
(13.50±0.83)
0.7-1.0
(0.84±0.03)
1.3
1.06
8-angular
Striate
Octacolpate
Prolate-
spheroidal
Small
11.
Guiera senegalensis
12.5-17.5
(16.67±1.04)
12.0-15.0
(13.81±0.96)
10.0-13.5
(12.50±2.18)
1.2-1.3
(1.25±0.03)
1.2
1.21
6-angular
Fine
reticulate
Hexacolpate
Prolate-
spheroidal
Small
12.
Pteleopsis habeensis
22.9-28.6
(24.81±1.27)
18.8-22.5
(20.35±0.92)
22.0-25.5
(23.57±4.14)
1.0-2.0
(1.50±0.22)
2.5
1.22
6-lobed
Micro-
rugulate
Hexacolpate
Subprolate
Small
13.
P. suberosa
18.5-23.5
(19.65±0.84)
15.0-17.5
(16.08±1.04)
17.5-22.5
(19.22±3.07)
1.5-2.0
(1.68±0.19)
2.5
1.14
6-lobed
Micro-
rugulate
Hexacolpate
Subprolate
Small
14.
Quisqualis indica
37.0-38.5
(37.76±2.09)
42.3-45.9
(43.38±1.05)
28.5-34.5
(31.58±1.75)
2.7-2.8
(2.75±0.02)
5
0.87
3-angular
Fine
reticulat
e
Tricolpate
Oblate-
spheroidal
Medium
15.
Q. latialata
27.0-32.7
(29.47±3.28)
22.3-27.9
(25.28±1.94)
19.5-25.5
(24.50±1.40)
2.0-2.2
(2.05±0.17)
5
1.17
3-angular
Scabrate
Tricolpate
Oblate-
spheroidal
Medium
16.
Terminalia catappa
20.0-22.5
(21.35±2.17)
20.0-20.5
(20.25±0.84)
18.7-19.5
(19.24±1.05)
2.0-2.2
(2.10±0.07)
2.5
1.05
6-lobed
Perforate
micro-
rugulate
Hexacolpate
Prolate-
spheroidal
Small
17.
T. glaucescens
20.0-21.5
(20.50±0.89)
17.0-17.5
(17.20±0.68)
17.5-18.5
(18.25±3.17)
1.2-1.3
(1.28±0.04)
2.5
1.19
6-lobed
Psilate
Hexacolpate
Prolate-
spheroidal
Small
18.
T. mantaly
16.2-17.5
(16.84±2.02)
14.5-15.0
(14.75±1.04)
14.5-15.2
(14.88±0.87)
1.2-1.3
(1.26±0.12)
2.5
1.14
6-lobed
Micro-
rugulate
Hexacolpate
Subprolate
Small
19.
T. superba
17.8-23.5
(21.93±0.86)
17.0-19.5
(18.76±0.62)
17.0-21.5
(19.57±1.65)
1.5-2.0
(1.78±0.25)
2.5
1.17
6-lobed
Perforate
micro-
rugulate
Hexacolpate
Prolate-
spheroidal
Small
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NJB, Volume 36 (2), Dec, 2023 Taxonomic Significance of Pollen of Combretaceae
Figure 2 (A-G): Photo-micrographs of pollen grains of some Combretaceae species
A: Combretum glutinosum showing colpi at equatorial view
B: Combretum glutinosum showing circular/hexagonal amb at the polar view
C: Combretum glutinosum showing striate exine pattern at equatorial view
D: Combretum paniculatum showing two colpi at equatorial view
E: Combretum paniculatum showing 6-angular amb and heterocolpate pollen at the polar
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view
F: Combretum zenkeri showing two colpi at the equatorial view
G: Combretum zenkeri showing heterocolpate pollen with 8-angular amb at the polar view
Figure 2 (H-O): Photo-micrographs of pollen grains of some Combretaceae species
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NJB, Volume 36 (2), Dec, 2023 Taxonomic Significance of Pollen of Combretaceae
H: Guiera senegalensis showing heterocolpate pollen grain at the polar view
I: Pteleopsis habeensis showing colpi at equatorial view
J: Quisqualis indica showing tricolpate pollen type with 3-aperture at the polar view
K: Quisqualis indica showing colpi at equatorial view
L: Quisqualis latialata showing tricolpate pollen grain with 3-aperture at the polar view
M: Quisqualis latialata showing colpi at equatorial view
N: Terminalia superba at equatorial view
O: Terminalia superba showing heterocolpate pollen grain at the polar view
Figure 2 (P-W): Photo-micrographs of pollen grains of some Combretaceae species
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NJB, Volume 36 (2), Dec, 2023 Mudasiru, O. M. et al.
P: Terminalia glaucescens showing colpi at equatorial view
Q: Terminalia glaucescens showing hexacolpate pollen type at the polar view
R: Terminalia mantaly at equatorial view
S: Terminalia mantaly showing hexacolpate pollen at the polar view
T: Terminalia catappa showing colpi at equatorial view
U: Terminalia catappa showing hexacolpate pollen type at the polar view
V: Anogeissus leiocarpus showing a sub-prolate pollen shape at the polar view
W: Anogeissus leiocarpus showing one aperture and ora at equatorial view
Figure 2 (X-Ad): Photo-micrographs of pollen grains of some Combretaceae species
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NJB, Volume 36 (2), Dec, 2023 Taxonomic Significance of Pollen of Combretaceae
geriaX: Combretum platypterum showing one clear aperture at equatorial view
Y: Pollen of C. platypterum showing two apertures
Z: Pollen of C. platypterum showing central aperture with distinct os
Aa: Pollen of Combretum racemosum showing two colpi
Ab: Pollen of Combretum racemosum showing a hexacolpate pollen type at the polar view
Ac: Pollen of Combretum hispidum displaying two colpi
Ad: Pollen of Combretum hispidum displaying hexacolpate pollen at the polar view
Figure 2 (Ae-Al): Photo-micrographs of pollen grains of some Combretaceae species
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NJB, Volume 36 (2), Dec, 2023 Mudasiru, O. M. et al.
Ae: Combretum molle showing colpi at equatorial view
Af: Combretum molle showing circular/hexagonal amb at the polar view
Ag: Pteleopsis suberosa displaying colpi at equatorial view
Ah & Ai: Polar view of Combretum sordidum showing hexacolpate pollen grain
Aj: Combretum sordidum showing one colpos at equatorial view
Ak: Polar view of Combretum smeathmannii displaying three colpi
Al: Pollen of Combretum smeathmannii displaying central colpos
Figure 3: Dendrogram showing affinities among the Combretaceae species in Nigeria based on the qualitative
and quantitative pollen morphological data
(Note: Numbers under branches indicate bootstrap percentages (%) derived from 1000 replicates).
Current sub-tribal (APG III, 2009) and sectional (Alwan, 1983) classifications are shown on the right side
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NJB, Volume 36 (2), Dec, 2023 Taxonomic Significance of Pollen of Combretaceae
Figure 4: Component plot (scattered diagram) for the nineteen (19) Combretaceae species based on the pollen
morphological characters
Legend:
Ale– Anogeissus leiocarpus, Cgl– Combretum glutinosum, Cmo– Combretum molle, Cpa–
Combretum paniculatum, Cpy– Combretum platypterum, Crm– Combretum racemosum, Cso– Combretum
sordidum, Csm– Combretum smeathmannii, Chi– Combretum hispidum, Cze– Combretum zenkeri., Gsl– Guiera
senegalensis; Pth– Pteleopsis habeensis, Psu– Pteleopsis suberosa, Qin– Quisqualis indica, Qla– Quisqualis
latialata, Tca– Terminalia catappa, Tgl– Terminalia glaucescens, Tmt– Terminalia mantaly, Tsu– Terminalia
superba
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NJB, Volume 36 (2), Dec, 2023 Mudasiru, O. M. et al.
DISCUSSION
Palynologically, pollen grains are most conservative plant structures and their parent genus or even species can be
recognised on the basis of morphology as each plant is unique for its pollen. Palynological features are used in
taxonomy as additional diagnostic characters, and these could be used in delineating angiospermic species. Pollen
morphology is of great application in taxa identification, delimitation and interpretation of relationships amongst
different taxonomic levels. The findings from this study revealed that Nigerian Combretaceae pollen grains are
highly heterogenous and exhibit a wide inter-specific variation with respect to the overall sizes and shape classes
(Table 2, Figure 2 A-Al). Except for some characters like amb, pollen size, colpi length as well as shape of aperture,
ora width and ratios of P/E, which are significant in the taxonomy of the genera in the family Combretaceae,
Krachai and Pornpongrungrueng (2015) used some pollen morphological features to define Thailand species in
Combretaceae. Numerous studies have shown the value of pollen morphology in the taxonomical classification of
angiosperms, and to propose relationship between taxa within families and to solve issues at the familial, sub-
familial and generic levels (El-Ghazali et al., 1998; Krachai and Pornpongrungrueng, 2015; El-Ghazali, 2016;
Ibrahim and Ayodele, 2017).
The pollen grains of the members of Combretaceae as recorded in this study are shed in monads and are
radially symmetrical, isopolar, small to medium-sized, heterocolpate with 6-8 apertures and colpus 17-36 μm in
length. Pollen grains with more colpi were found. Tricolporate grains were not observed in this study, which is in
line with findings on the general characteristics of Combretaceae pollen (El-Ghazali et al.,1998). This study also
showed that the pollen grains of the Combretaceae species are eurypalynous, far from being uniform and do not
exemplify natural groups. Combretaceae has a more advanced pollen type with colpi, isopolar and three or four
aperturate than monocolpate and non-aperturate pollen grains (primitive type). The presence of a higher number
of colpi in any group of plants has been attributed to recent evolutionary advancement in such a group of plants
(Arogundade et al., 2019). The line of advancement of pollen types in this study is from hexacolpate versus
octacolpate.
Pollen size and shape varied among the species studied. The size of pollen grains varied from small to
medium. The species of the sub-tribe Terminaliinae have only small sized-grains whereas the sub-tribe
Combretinae has small to medium sized-grains. The largest pollen size (42.68 × 38.17 μm) was recorded in
Combretum platypterum and the smallest one (14.75 × 15.05 μm) in Combretum sordidum. However, the size of
pollen grains was slightly different in Anogeissus, Combretum, Pteleopsis, Terminalia and Quisqualis species,
indicating that size variation may be used at generic level. The pollen shape in equatorial view varied among
species. Similarly, the minimum and maximum exine thickness was recorded as 0.84 μm in C. zenkeri and 2.75
μm in Q. indica, whereas the polar axis over axis of the equatorial ranged from 0.87 in Q. indica to 1.22 in P.
habeensis.
The phylogenetic relationships among the selected members of Combretaceae were presented through
cluster analysis, while more taxonomic information on classification of the Combretaceae taxa was revealed using
the PCA (Figure 4). All taxa were delineated into two clusters (Figure 3). The first cluster comprises eleven taxa,
viz: Combretum platypterum, C. sordidum, C. zenkeri, C. hispidum, Quisqualis indica, Q. latialata, C.
smeathmannii, C. paniculatum, C. racemosum, C. glutinosum and C. molle. The second cluster contains eight taxa,
namely Terminalia glaucescens, T. mantaly, T. catappa, T. superba, Anogeissus leiocarpus, Pteleopsis habeensis
and P. suberosa. Guiera senegalensis was found to be the most distant from all the other taxa in the group (Figure
4).
In the first cluster, Combretum zenkeri was grouped with C. sordidum and C. hispidum, C. racemosum with
Quisqualis indica and Q. latialata; C. smeathmannii with C. paniculatum, indicating that the members of each of
these three groups were closer to each other than they were to the members of the sub-genus Combretum (C.
glutinosum and C. molle). The closeness between Combretum zenkeri and C. sordidum was supported by their
exine pattern (striate) and pollen shape class (prolate-spheroidal). The close relationship between Quisqualis indica
and Q. latialata in the sub-genus Cacoucia group was supported by their pollen shape class (oblate-spheroidal),
type (tricolpate), size (medium), amb (6-angular) and ora width (5 μm). These similarities were inconsistent with
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NJB, Volume 36 (2), Dec, 2023 Taxonomic Significance of Pollen of Combretaceae
the findings of Akinsulire et al. (2018), who reported a remote link between Q. indica and members of Combretum
while studying macro-morphology of selected Combretaceae species. The sub-cluster of Combretum glutinosum
and C. molle was cornfirmed by their colpi length (ca. 22 μm), ora width (2.5 μm), amb (6-circular) and medium
pollen size. Thus, there is the need for further study particularly on the Combretum and Quisqualis.
In the second major cluster, three distinct sub-clusters were recorded. The first one consists of Pteleopsis
habeensis and P. suberosa. The common characteristics shared by these taxa comprise sub-prolate pollen shape,
small pollen size, amb (6-lobed) and exine sculpturing (micro-rugulate) with exine thickness (1.5-1.7 μm). In the
second sub-cluster, Terminalia catappa and T. superba were observed to be closer to each other than they were to
T. glaucescens, T. mantaly and Anogeissus leiocarpus. The close relationship between T. catappa and T. superba
was evidenced by their exine pattern perforate micro-rugulate and colpi length (19 μm). Anogeissus leiocarpus and
T. mantaly form the third sub-cluster and their close association was evidenced by exine thickness (ca. 1.26 μm),
amb (6-lobed) and prolate spheroidal pollen shape. Within the second major cluster, Terminalia glaucescens, T.
mantaly, T. catappa, T. superba, Anogeissus leiocarpus, Pteleopsis habeensis and P. suberosa were found to share
common traits with the highest bootstrap support (92%). This finding is in line with Maurin et al. (2010), who
suggested that members of the genera Pteleopsis and Anogeissus should be placed in the same sub-tribe
(Terminaliinae) based on the molecular studies. They also sugested that Pteleopsis and Anogeissus should be
placed within the genus Terminalia and that all genera of the sub-tribe Terminaliinae, should be encompassed in
an expanded circumscription of Terminalia, with the exception of Conocarpus. Results of this study confirmed
anatomical and macro-morphological data (Mudasiru, 2023). Guiera senegalensis has been reported to be
morphologically most distant from all other species examined in the cladogram. The first two component of the
Principal Component Analysis (PCA) accounted for 89% of the variation among the species studied. Based on
component 2, pollen polar diameter, pollen equatorial diameter, colpi length, exine thickness, ora width, pollen
size, amb and aperture were responsible for the variation observed among the Combretaceae species. Based on
component 2, only exine pattern and pollen shape class were accountable for the variation observed among the
species (Figure 4). The scatter plot yielded four groups and the position of each species in the PCA showed the
evolutionary trend within Combretaceae. The results of the single linkage cluster analysis and PCA as earlier
reported by Ayodele (2005) and Soladoye et al. (2010) indicate that the species in the same group are to some
extent, related morphologically, indicatng that they have similar ancestral origin with a common gene pool. This
study has shown how numerical taxonomy justifies the classification of the genus using morphological
characteristics as suggested by different authors (Ayodele, 2005; Soladoye et al., 2011; Sonibare et al., 2014).
CONCLUSION
Pollen morphology has proven to be an important tool for taxonomic identification of species within the family
Combretaceae. This study showed that Nigerian Combretaceae pollen grains are largely heterogenous. The species
can be identified based on morphometric and morphological pollen characters, particularly overall size of polar
axes (P) and equatorial diameters (E), shape classes, the ratios of P/E, exine thickness and apertural features. The
size of pollen grains was slightly different in the members of all the six genera (Anogeissus, Pteleopsis, Terminalia,
Combretum, Guiera and Quisqualis), indicating that size variation may be used at the generic level in this family.
Also, Combretaceae taxa were observed to be eurypalynous, with four shape classes, six exine sculpturing patterns
and eight aperture facets. The cluster analyses and PCA plots showed nested grouping of the Quisqualis species
within Combretum, with high bootstrap support (84%). The cluster analysis revealed congruence in the number of
main clusters resolved. Palynomorphological data have confirmed the existence of diversity and relationships
among the nineteen species of Combretaceae, in order to improve the identification of the taxa and serve as
additional source of taxonomic information for the family. The data obtained in this study not only supported the
information already known about the family Combretaceae but can also be used in combination with other
characteristics to distinguish between the various species that make up the family.
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NJB, Volume 36 (2), Dec, 2023 Mudasiru, O. M. et al.
ACKNOWLEDGEMENTS
The authors are grateful to The World Academy of Sciences (TWAS), Trieste, Italy and CSIR, New Delhi,
Government of India for joint award of Ph.D. Fellowship to Mudasiru, O.M. at CSIR-NBRI, Lucknow, India under
which this study was carried out. We thank the authorities of the University of Ibadan, Ibadan, Nigeria for
permitting Mudasiru, O.M. to take up the fellowship. Special thanks to the Prof. Saroj. K. Barik, ex-Director of
the CSIR-National Botanical Research Institute in Lucknow, Uttar Pradesh, India, for providing facilities used for
the study.
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