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Citation: Hamdiah, S.; Karas, L.;
Houšková, K.; Van Damme, K.;
Attorre, F.; Vahalík, P.; Habrová, H.;
Lvonˇcík, S.; Eler, K.; Madˇera, P. Seed
Viability and Potential Germination
Rate of Nine Endemic Boswellia Taxa
(Burseraceae) from Socotra Island
(Yemen). Plants 2022,11, 1418.
https://doi.org/10.3390/
plants11111418
Academic Editors: Božena Šeráand
František Hniliˇcka
Received: 2 May 2022
Accepted: 25 May 2022
Published: 26 May 2022
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plants
Article
Seed Viability and Potential Germination Rate of Nine Endemic
Boswellia Taxa (Burseraceae) from Socotra Island (Yemen)
Salem Hamdiah 1,2, Lukáš Karas 1, * , Kateˇrina Houšková3, Kay Van Damme 1,4 , Fabio Attorre 5,
Petr Vahalík6, Hana Habrová1, Samuel Lvonˇcík1, Klemen Eler 2and Petr Madˇera 1
1Department of Forest Botany, Dendrology and Geobiocoenology, Faculty of Forestry and Wood Technology,
Mendel University in Brno, Zemˇed ˇelská3, 613 00 Brno, Czech Republic; balagahar@gmail.com (S.H.);
kay.vandamme@ugent.be (K.V.D.); hana.habrova@mendelu.cz (H.H.); samuel.lvoncik@mendelu.cz (S.L.);
petr.madera@mendelu.cz (P.M.)
2Biotechnical Faculty, University of Ljubljana, Jamnikarjeva 101, 1000 Ljubljana, Slovenia;
klemen.eler@bf.uni-lj.si
3Department of Silviculture, Faculty of Forestry and Wood Technology, Mendel University in Brno,
Zemˇed ˇelská3, 613 00 Brno, Czech Republic; katerina.houskova@mendelu.cz
4Centre for Academic Heritage and Archives & Ghent University Botanical Garden, Ghent University, K.L.
Ledeganckstraat 35, 9000 Ghent, Belgium
5Department of Environmental Biology, Sapienza-University of Rome, Piazzale Aldo Moro 5,
00185 Rome, Italy; fabio.attorre@uniroma1.it
6Department of Forest Management and Geoinformatics, Faculty of Forestry and Wood Technology,
Mendel University in Brno, Zemˇed ˇelská3, 613 00 Brno, Czech Republic; petr.vahalik@mendelu.cz
*Correspondence: lukas.karas@mendelu.cz
Abstract:
The endemic Boswellia species (Burseraceae) on Socotra Island (Yemen) are of great local
significance due to their various local ethnobotanical uses. However, despite the fact that these trees
are endangered, little is known about their biology. We tested seed germination rates in controlled
experiments (trials of 21 days) for two subsequent years and for nine endemic taxa of Boswellia
occurring on Socotra Island. For this, seeds were collected island-wide from a wide range of localities
and for several populations per species. We observed differences in germination among Boswellia
species, among species and localities and among both years, which indicates that the development
of seeds is strongly affected by external ecological factors. Although we noted a large variation in
seed germination (relatively high in Boswellia socotrana), and half of the species showed relatively low
mean daily germination, our study indicated that all endangered endemic Frankincense Tree taxa of
Socotra harbor the potential for in situ conservation through recruitment, given that known impacts
can be reduced in local replantation areas (e.g., grazing).
Keywords: Boswellia; endangered species; Frankincense; propagation; Soqotra
1. Introduction
All Frankincense tree taxa, or members of the genus Boswellia (Burseraceae), are glob-
ally endangered, being harvested intensively for their oleo-gum resin [
1
]. The unsustainable
use of olibanum or frankincense leads to the overexploitation of Boswellia populations on
a global scale [
1
,
2
]. In addition, Boswellia trees are endangered because of overgrazing by
livestock, which is considered an important negative factor influencing natural regener-
ation [
1
,
3
]. This is particularly problematic in arid regions, where the majority of these
trees reside. For example, in Eritrea, human-induced factors such as land clearing for
agriculture, overgrazing and overtapping of resin are threatening Boswellia papyrifera (Del.)
Hochst populations [
4
]. Boswellia papyrifera in central and eastern Africa is declining at an
alarming rate, as natural populations are facing degradation due to agricultural expansion,
overgrazing, fires, poor incense harvesting practices, shifting cultivation, termites and other
infestations; urgent conservation measures are required to save the species [
5
]. Similar
Plants 2022,11, 1418. https://doi.org/10.3390/plants11111418 https://www.mdpi.com/journal/plants
Plants 2022,11, 1418 2 of 21
factors are affecting other species in Africa and the Arabian Peninsula [
6
,
7
]. In general,
based on extensive research throughout the geographic range of the five most economically
important Boswellia species, Bongers et al. [
1
] concluded that Boswellia populations are glob-
ally threatened by over-exploitation and ecosystem degradation, jeopardizing future resin
production. These changes are caused globally by increased human population pressure
on Boswellia woodlands mainly through livestock grazing and unsustainable tapping.
As a result of mainly human impacts, frankincense tree populations are declining
rapidly in the wild. However, studies about population decline and the relationships
with potential causes are relatively few. The most comprehensive study revealed evidence
of the population collapse of B. papyrifera throughout its geographic range in Africa [
1
].
Using inventories of 23 populations consisting of 21,786 trees, growth-ring data from
202 trees
and demographic models based on 7246 trees, the latter authors found that over
75% of the studied populations lacked young trees, and natural regeneration had been
absent for decades; therefore, the projected frankincense production could be halved in
20 years [
1
]. Additionally, a population structure analysis of B. papyrifera in Eritrea made
by Ogbazghi et al. [
4
] shows that there seems to be an overall absence of juvenile trees.
Natural regeneration was found only in two areas in which trees were not tapped for resin
and that were inaccessible to livestock. On Socotra Island (Yemen), Boswellia population
studies are nearly lacking, with two exceptions. Attorre et al. [
8
] evaluated all Boswellia
species known at that time on Socotra Island and found natural regeneration in only two
cliff-rooted species (Boswellia popoviana and B. dioscoridis). Lvonˇcík et al. [
9
] concentrated on
the evaluation of the long-term development of the largest population of Boswellia elongata
in Homhil Nature Sanctuary, also showing an overall lack of juvenile trees and a strong
effect of global climate change, in this case, unusually strong cyclones.
Socotra Archipelago (Yemen), situated in the northwestern Indian Ocean, has the
highest diversity of Burseraceae species in the world [
10
]. Eleven taxa of Boswellia can
be found there, all of them are endemic, and five species of Commiphora, four of which
are endemic [
10
–
12
]. Frankincense trees in Socotra have numerous environmental, socio-
economic, traditional medicine and potentially industrial benefits as the ethnobotanical
knowledge indicate [
10
,
11
] which, besides grazing, all add to the increased vulnerability
and human use of these species. Finally, global climate change contributes in both direct and
indirect ways to a rapid population decline of frankincense trees on Socotra Island [
9
] and
is estimated to have an impact on Boswellia globally [
1
]. Therefore, renewed efforts should
be made to improve our knowledge of particularly range-restricted insular populations
of endangered Boswellia such as those on Socotra Island, in order to strategize aimed
future conservation actions. A better understanding of the biology of these species can be a
powerful tool in local long-term conservation. As a comparative example in Socotra, studies
on the biology of the endemic Socotran Dragon’s Blood Tree
Dracaena cinnabari Balf. f.
, are
useful tools to understand the potential and limitations in conservation activities for the
entire group of Dragon Trees in the world [13].
Scientific studies on the biology, including seed germination ability of Boswellia species
from Socotra Island, as a basis of natural regeneration, and the potential intrinsic factors
for the decline, are missing. In other Frankincense tree taxa, relatively low germination
rates were recorded. Swartout and Solowey [
14
] mentioned significantly low germination
viability for Boswellia sacra Flueck. (4–16%) in Israel, and significantly low germination
rates (up to 8%) in this species were also recorded by Eslamieh [
15
]. The viability of
seeds of Boswellia papyrifera in Ethiopia was estimated at ca. 49% to 59% [
16
]. Higher
germination rates were found in the latter study in untapped trees, thus tapping (i.e.,
manual extraction of resin through administering wounds to the tree) may negatively
affect seed viability. Rijkeers et al. [
17
] published similar results in Boswellia papyrifera
in Ethiopia, where untapped trees produced three times as many healthy, and properly
filled germinable seeds as tapped trees. Germination success was highest in stands with
untapped trees (>80%) and lowest with those for tapped trees (<16%). Experiments that
have included treatments for breaking seed dormancy were carried out for African Boswellia
Plants 2022,11, 1418 3 of 21
species [
16
–
19
]. Such experiments are key to future replantation of these endangered tree
species for conservation efforts, and to assess the effects of human impacts on tree biology.
The general lack of natural regeneration of in situ populations of Boswellia [
1
] could
be caused by both extrinsic (e.g., grazing, climate change) and intrinsic factors (e.g., floral
biology, physiology). Our focus in this study is on assessing the influence of intrinsic
biological factors related to generative reproduction (seed germination), in the function of
future conservation of these endangered species. The main question of the current study
is to establish whether seed germination, as a major intrinsic factor, is a limiting factor
for the natural regeneration of Boswellia species on Socotra Island. Thus, we assessed the
germination rates and germination energy of seeds of nine Boswellia taxa (Boswellia ameero
Balf. f., Boswellia bullata Thulin, Boswellia dioscoridis,Boswellia elongata,Boswellia nana Hepper,
Boswellia popoviana,Boswellia scopulorum Thulin, Boswellia socotrana subsp. aspleniifolia (Engl.)
Lvonˇcík, and Boswellia socotrana Balf. f. subsp. socotrana) occurring on Socotra Island
through seed germination trials under controlled conditions, taking into account potential
variation of germination between different years and different populations.
2. Results
2.1. Inter-Locality Variabilities of Different Boswellia Taxa in 2020 and 2021
The highest proportion of germinated and fresh seeds (ca. 90%) and the lowest
proportion of empty seeds (up to 1%) was observed in B. socotrana in both subspecies and
tested sites in 2020 (subsp. socotrana BSSA 20 from Ayhaft and subsp. aspleniifolia BSAS from
Shata Qalansiyah; Figure 1). The other tested Boswellia species showed a lower proportion
of germinated and fresh seeds (up to 40%) and a higher proportion of empty seeds (above
40%). Eight out of eleven localities had more than 50% empty seeds in the 2020 seed sets.
The lowest proportion of germinated and fresh seeds (up to 5%) was found in B. bullata
BBT from Taida’ah and B. elongata BEM from Makalihim, no germinated or fresh seeds
were found for B. elongata BEDB from Diburak and B. popoviana BPK from Klisan; the seeds
of these species were mostly empty. Most samples from 2020 had 10% or less of dead seeds
or seeds damaged by insects (Figure 1); only seeds of B. bullata BBT from Taida’ah and
B. elongata BEH from Homhil contained ca. 30% of dead or insect infected seeds.
Figure 1.
Seed category proportions of the seven Boswellia taxa collected from 12 localities (Socotra
Island) in 2020 (for abbreviations, see Table 1).
Plants 2022,11, 1418 4 of 21
Table 1.
List of codes, (sub)species, locality names, coordinates, altitude, and date of collection of the
9 Boswellia taxa from Socotra Island (Yemen) assessed in this study.
Species Locality Sp. Code Coordinates Altitude Date of Collection
Boswellia ameero
(BA)
Ayhaft BAA 12.594013 N
53.988233 E 424 18 May 2021
Danagahan BADN 12.585567 N
54.052267 E 629 2 June 2020,
27 May 2021
Dixam BADX 12.517885 N
53.930242 E 928 17 May 2021
Firmihin BAF 12.481588 N
54.010128 E 617 17 May 2021
Qatariyah BAQ 12.351153 N
53.708817 E 860 1 June 2021
Boswellia bullata
(BB)
Hazahaz BBH 12.657705 N
53.440213 E 476 24 May 2021
Shoab rock
(green flowers) BBSG 12.62341 N
53.403162 E 1 7 May 2021
Shoab
(red flower) BBSR 12.61131 N
53.401565 E 1 7 May 2021
Taida’ah
(Ditwah mountain)
BBT 12.697685 N
53.514572 E 215 20 June 2020,
15 May 2021
Boswellia dioscoridis
(BD)
Wadi Diasraha BDDA 12.419418 N
54.144430 E 67 26 May 2021
Wadi Difa’araha BDDF 12.423367 N
54.123345 E 78 26 May 2021
Wadi Digasfa BDDG 12.455117 N
54.146743 E 167 26 May 2021
Halah
(Hoq cave) BDH 12.591258 N
54.360668 E 70 27 May 2021
Sheebhan BDS 12.473968 N
54.004037 E 572 20 May 2020,
17 May 2021
Boswellia elongata
(BE)
Diburak BEDB 12.523304 N
54.277032 E 360 7 June 2020,
3 June 2021
Dishal BEDS 12.527823 N
51.177206 E 282 26 May 2020,
2 June 2021
Homhil BEH 12.576047 N
54.286267 E 335 1 June 2020,
10 June 2021
Makalihim BEM 12.505041 N
54.168744 E 169 28 May 2020,
2 June 2021
Shabarah BES 12.524795 N
53.885643 E 441 4 July 2021
Boswellia nana (BN) Hamadarah
(Homhil) BNH 12.593068 N
54.303272 E 616 19 May 2021
Plants 2022,11, 1418 5 of 21
Table 1. Cont.
Species Locality Sp. Code Coordinates Altitude Date of Collection
Boswellia popoviana
(BP)
Bedgofahar BPB 12.657987 N
54.166502 E 178 30 May 2021
Sheebhan
(Didrafarantan) BPD 12.471406 N
54.004312 E 570 5 June 2021
Firmihin BPF 12.482612 N
54.009487 E 608 17 May 2021
Klisan BPK 12.473802 N
54.335207 E 270 19 June 2020,
10 June 2021
Momi Falang BPV 12.460495 N
54.364178 E 304 19 June 2020,
10 June 2021
Boswelliascopulorum
(BS) Bedgofahar BSB 12.656790 N
54.139097 E 149 20 May 2021
Boswellia
socotrana subsp.
aspleniifolia (BSA)
Raidah (Taida’ah) BSAB 12.6832650 N
53.5772433 E 346 6 June 2021
Dinawtat BSAN 12.655353 N
53.683472 E 34 16 May 2021
Shata Qalansiyah BSAS 12.629508 N
53.592948 E 128 28 May 2020,
17 May 2021
Taida’ah
(Ditwah mountain)
BSATD 12.699898 N
53.515875 E 288 15 May 2021
Tarabah BSATR 12.579373 N
53.924450 E 128 9 June 2021
Boswellia
socotrana subsp.
socotrana (BSS)
Ayhaft BSSA 12.596872 N
53.989797 E 242 20 May 2020,
23 June 2021
Hamadarah
(Homhil) BSSH 12.591187 N
54.301247 E 466 12 June 2021
Zarkan (Asmin) BSSZ 12.595920 N
54.151198 E 408 15 June 2021
In 2021, the highest proportion of germinated and fresh seeds was observed in
B. socotrana subsp. socotrana,B. socotrana subsp. aspleniifolia and B. dioscorodis reaching
70–80% (Figure 2), for both subspecies of B. socotrana values were lower than in 2020.
For
B. socotrana
subsp. aspleniifolia, the high proportion of these seeds were similar at
all tested localities (no statistical differences in germination rate, see Figure 3) but for
B. socotrana subsp. socotrana (BSSZ), seeds only from Zarkan reached the highest value
and seeds from Ayhaft (BSSA) and Homhil (BSSH) reached up to 40% of germinated and
fresh seeds (statistical difference in germination rate, see Figure 3). Seeds of B. bullata
contained ca. 35–50% germinated and fresh seeds at all localities, seeds of other species
reached a similar proportion of these seeds only at one locality, i.e., B. ameero (BADN)
from Danagahan,
B. elongata
(BEH) from Homhil, B. nana (BNH) from Hamadarah and
B. popoviana (BPD) from Sheebhan; the seeds from other localities contained the minimal
proportion of these seeds (usually up to 15%) and showed significantly lower germination
rate. Seeds of B. elongata,B. scopulorum and B. popoviana at most localities were empty, and
those of B. ameero,B. bullata and B. dioscoridis at most localities were dead or damaged
by insects.
Plants 2022,11, 1418 6 of 21
Figure 2.
Seed categories proportion of all nine taxa of Boswellia collected from different localities on
Socotra Island in 2021 (for abbreviations, see Table 1).
Figure 3.
Seed germination rate of all nine taxa of Boswellia from different localities in 2021 on
Socotra Island (a, b, c—Indexes denoting localities with significantly separate germination rates
within individual taxon, the same index associates the seed without statistically significant difference
in germination rate).
For the samples of 2021, Boswellia socotrana subsp. aspleniifolia reached the relatively
highest germination rate of full seeds (ca. 70–90%) in all localities (Figure 4). B. dioscoridis,
B. elongata,B. popoviana and B. socotrana subsp. socotrana showed a high germination rate
of full seeds (ca. 70–95%) as well, but not in all localities (Figure 4). B. dioscoridis reached
the highest values (ca. 90%) at Wadi Difa’araha (BDDF), statistically significantly lower
values (ca. 70–80%) at Wadi Diasraha (BDDA) and Wadi Difgasfa (BDDG) and the lowest
values (ca. 10–30%) at Halah (BDH) and Sheebhan (BDS). B. elongata reached the highest
Plants 2022,11, 1418 7 of 21
values (ca. 70–95%) at Homhil (BEH) and Shabarah (BES) and statistically significantly
lower values (usually up to 50%) at Diburak (BEDB), Dishal (BEDS) and Makalihim (BEM).
B. popoviana reached the highest values (ca. 85%) at Sheebhan (BPD) and Firmihin (BPF)
and statistically significantly lower values (usually up to 50%) at Momi Falang (BPV) that
did not differ from the zero germination rate of full seeds at Bedgofahar (BPB) and Klisan
(BPK). B. socotrana subsp. socotrana reached the highest values (ca. 85%) at Zarkan (BSSZ)
and statistically significantly lower values (ca. 50%) at Ayhaft (BSSA) and Homhil (BSSH).
B. scopulorum from Bedgofahar (BSB) showed a high (ca. 80%) germination rate of full seeds
too, but with high variability (from 22% to 100%). B. ameero did not reach such high values
of germination rate of full seeds (maximum of ca. 65% at Qatariyah (BAQ), lower values
of ca. 45% at Danagahan (BADN) and the lowest values up to ca. 20% at Ayhaft (BAA),
Dixam (BADX) and Firmihin (BAF)). B. bullata has an average germination rate of full seeds
(usually 40–60%) without significant differences between localities.
Figure 4.
Seed germination rate of full seeds of all nine taxa of Boswellia from Socotra Island from
different localities in 2021 (a, b, c—Indexes denoting localities with significantly separate germination
rates within individual taxon, the same index associates the seed without statistically significant
difference in germination rate of full seeds).
In 2021, Boswellia socotrana subsp. aspleniifolia seeds germinated relatively fast in all
localities in comparison to other taxa (highest germination energy; Figure 5). There were no
statistically significant differences in the germination energy of these seeds; within 4 days
from the start of the germination test, most of the full seeds (65–85%) germinated. B. nana
as well as B. elongata and B.socotrana subsp. socotrana also had a similar seed germination
energy (above 50% on average), but not in all localities. Other species germinated more
slowly, with less than 50% of full seeds germinating within 4 days of the start of the
germination test. The lowest germination energy (up to 5%) was recorded in some localities
for B. ameero (from Ayhaft BAA and Firmihin BAF), B. dioscoridis (from Wadi Diasraha
BDDA, Wadi Difa’araha BDDF, Wadi Difgasfa BDDG and Halah BDH), B. elongata (from
Diburak BEDB) and B. popoviana (from Bedgofahar BPB, Sheebhan BPD and Klisan BPK).
Plants 2022,11, 1418 8 of 21
Figure 5.
Seed germination energy of full seeds of all nine taxa of Boswellia from different localities
in 2021 (a, b, c—Indexes denoting localities with significantly separate germination rates within
individual taxon, the same index associates the seed without statistically significant difference in
germination energy of full seeds).
2.2. Average Inter-Annual and Inter-Species Variability of Germination Rates
Most of the species showed a similar germination rate between the two sampled years,
but only three taxa (Boswellia bullata,B. socotrana subsp. aspleniifolia and B. socotrana subsp.
socotrana at BBT, BSAS and BSSA) showed significant differences (Figure 6). B. socotrana
subsp. aspleniifolia (BSAS) and B. socotrana subsp. socotrana (BSSA) showed relatively higher
germination rates in 2020, B. bullata (BBT) in 2021.
Figure 6.
Inter-annual variability of seed germination rate of tested Boswellia species (a, b, c, d, e, f, g,
h, i—Indexes denoting localities with significantly separate germination rates within individual taxon,
the same index associates the seed without statistically significant difference in germination rate).
Plants 2022,11, 1418 9 of 21
When comparing the other species’ average germination rates, except B. socotrana,
other Boswellia species show a relatively low germination rate, in half of the cases lower than
10%. It was usually due to the high proportion of empty seeds (see Figure 6vs. Figure 7).
In some cases, germination rates were 0% (BEDB, BPK).
Figure 7.
Inter-annual variability of germination rate of full seeds of tested Boswellia species (a, b,
c, d, e, f, g, h, i—Indexes denoting localities with significantly separate germination rates within
individual taxon, the same index associates the seed without statistically significant difference in
germination energy of full seeds).
2.3. Peak Value Indices
Seeds of all of the Socotran species started germinating in the first week of the germi-
nation test (Figures 8and 9). Both subspecies of B. socotrana started germinating during the
first day of the test and B. popoviana, and B. scopulorum started germinating at the end of
the first week. B. ameero,B. bullata,B. elongata,B. nana,B. socotrana subsp. aspleniifolia and
B.socotrana subsp. socotrana germinated fast and reached peak values in the first week of
the test, while the remaining species (B. dioscoridis,B. popoviana and B. scopulorum) in the
second week. In 2020 and 2021, seeds of B. socotrana of both subspecies germinated the
fastest (in 2021 closely followed by B. nana). All of the species finished germinating in the
first or second week of the germination test, there were almost no germinating seeds found
in the third week.
Plants 2022,11, 1418 10 of 21
Figure 8. Peak value indexes of seeds of different Boswellia taxa from Socotra sampled in 2020.
Figure 9. Peak value indexes of seeds of different Boswellia taxa from Socotra sampled in 2021.
3. Discussion
3.1. Factors Affecting Germination of Boswellia Seeds
On average, we found germinated seeds in nine Socotran Boswellia taxa under con-
trolled conditions. The observed germination rate among species and localities varied
highly (B. ameero 0–70%, B. bullata 0–65%, B. dioscoridis 5–90%, B. elongata 0–45%,
B. nana
30–70%
,B. popoviana 0–65%, B. scopulorum 5–25%, B. socotrana subsp. aspleniifolia 25–94%,
Plants 2022,11, 1418 11 of 21
and B. socotrana subsp. socotrana 5–92%, for further details see Appendix A,
Tables A1 and A2
).
We did not have seeds of two species (B. hesperia sp. prov. and B. samhaensis Thulin and
Scholte) occurring on the Socotra Archipelago available for the experiment. In 2022, after
our visit to Samha Island, we found one fruiting tree of B. samhaensis and collected a limited
number of seeds. A fast preliminary experiment of 20 seeds showed that after three days
six seeds germinated, and on the fourth day, another one germinated as well. Therefore,
B. samhaensis
also has germinable seeds with a preliminary germination rate of 35%. There
are only a few studies focusing on germination trials with seeds of Boswellia species, but
generally, most of them report relatively low germination rates. Well known for a low ger-
mination rate is Boswellia sacra, varying between 4 and 16% [
14
,
15
]. The germination rate of
Boswellia papyrifera was found to range from 4 to 7% under different treatments [
20
]. Higher
germination rates were published by Eshete et al. [
16
] (40–72%) and by Rijkers et al. [
18
]
(14–94%), but in both cases, the germination rate was counted from filled (full, viable) seeds.
Similarly, Savithramma et al. [
21
] mentioned a 70% germination rate for Boswellia ovalifoliata
N.P.Balakr. The last investigated species was Boswellia dalzielii Hutch. [
17
], associated with
a germination rate in the field experiment (seeds were sown without any pre-treatment to
the pots in the nursery) between 30 to 35%.
Tapping was found to be an important factor in decreasing the number of viable seeds
and their germination rate [
16
,
18
]. Only naturally oozed resin is collected on Socotra Island,
mostly without tapping [
11
]. Therefore, tapping is perhaps not the most important factor
affecting the Boswellia trees’ vitality on Socotra and therefore may at this point not affect
seed germination potential. Nevertheless, we did not systematically assess the tapping of
the mother trees in our trials, as we focused on general seed germination in the first step.
Nonetheless, a high percentage of empty seeds was found across almost half of the
taxa we included in our study (Boswellia elongata,B. nana,B. scopulorum and B. popoviana).
Similar to our results, Rijkers et al. [
18
], Adam and El Tayeb [
20
] mentioned high percentages
of empty seeds for B. papyrifera too. Additionally, Swartout and Solowey [
14
] reported
only 4–17% of viable seeds of Boswellia sacra were detected by sink test. The high ratio
of empty seeds could be caused by some external factors such as insufficient humidity
or low soil nutrient content during fruit development. Climatic factors as a reason for
low seed quality are mentioned by de Souza et al. [
22
]. Another explanation for a high
proportion of empty seeds could be in hybridogenic origin within the evolution of these
island species. Additionally, self-fertilization is mentioned as the main cause of empty
seeds in Fagus sylvatica L. [
23
]. Fuentes and Shupp [
24
] demonstrated that empty seeds
may reduce predation of full seeds of Juniperus osteosperma (Torr.) Little in Utah by seed-
eating birds, therefore, a high ratio of empty Boswellia seeds on Socotra could also be a
natural phenomenon.
Floral biology of two Boswellia species (B. ovalifoliata and B. serrata Roxb. Ex Colebr.)
was investigated in detail by Raju et al. [
25
] and Sunnichan et al. [
26
], respectively. Strictly
self-incompatible flowers were documented for both the above-mentioned species. With
high probability, this will be the case for Boswellia species on Socotra as well. In populations
with low tree density where individual specimens are far apart (which is often the case of
Boswellia species on Socotra), most flowers could be self-pollinated and thus the fruit set is
very low. Under open pollination, the fruit set was only about 10% of Boswellia serrata [
26
].
Unfortunately, we have not investigated this phenomenon on Socotra yet.
On the other hand, there is high importance on insects in the pollination of Boswellia
species. Raju et al. [
25
] and Sunnichan et al. [
26
] report mainly bees as the principal
pollinator insect. Sunbirds can serve as pollinators as well, but floral characteristics suggest
that entomophily is the main mode [
25
]. The wind is not a vector for the spreading of
pollen grains [
26
]. Raju et al. [
25
] found garden lizards to be predators of pollinating
insects in Boswellia ovalifoliata, which can affect the pollination rate of this tree species. On
Socotra, García and Vasconcelos [
27
] found a few species of geckos that may pollinate the
dragon’s blood tree (Dracaena cinnabari), therefore, similarly they may serve as pollinators
for Boswellia species.
Plants 2022,11, 1418 12 of 21
Not many seeds were infested with insects in the Socotran Boswellia species (3% in
2020, 2% in 2021), which contradicts the figures for Boswellia papyrifera varying from 15.8 to
16.6% [
16
], 19.0–24.5% [
18
] to 55.7% [
20
]. Other predators of buds and flowers are possible,
such as weevil or the palm squirrel, predating on fruits of other Boswellia [25].
We found high variability in germination rate between the years in three taxa (BBT,
BSAS, BSSA) and also among different localities of the same Boswellia species on Socotra.
This may indicate considerable sensitivity to the above-mentioned factors and there may be
other factors that are not yet identified, affecting seed development. Over all these potential
(yet undefined) factors, our results suggest that the problem of missing regeneration of
Boswellia species on Socotra Island is not caused by internal biological factors related to
generative reproduction. Although the germination rate is zero in one year, it is sufficient
in another, with the exception of BEDB and BPK. We can conclude that individual trees
of the different Boswellia taxa on Socotra are producing a sufficient amount of germinable
seeds. Therefore, the problem of missing sapling recruitment is probably connected with
external ecological factors acting on the growth of the seedlings after their germination.
3.2. Phenology of Fruit Ripening
We observed that the time of Boswellia capsules ripening on Socotra begins in the
first half of May (B. bullata) and continues until the end second half of June (B. popoviana).
However, there is a strong variability among the localities of individual species. None of
the species were observed to ripen outside of May–June, with the exception of B. dioscoridis,
which seems to ripen gradually during the whole year (Table 1).
The fruit ripening in Boswellia on Socotra (May–June) is potentially connected with
the first rainfalls at the beginning of the summer monsoon, and subsequently, the winged
seeds [
25
] are spread by strong summer winds [
28
]. However, it seems that most seeds
fall in the proximity of the parental tree, a few meters to tens of meters [
9
]. The first
natural seedlings appear in September with last summer monsoon rainfalls and their
growth is supported by showers within the winter monsoon from October to December [
9
].
Additionally, high air humidity and horizontal precipitation in July and August [
29
] can
substantially contribute to the survival of young seedlings. Similarly, B. ovalifoliata seed
germination is connected with the first rainfalls [25].
3.3. Natural Regeneration
A relatively high recorded seed germination energy shows an excellent adaptation of
seeds to the harsh dry environment with sporadic precipitation. The seeds are prepared
to germinate immediately after the first rains at the beginning of the short rainy season.
Similarly, other experiments have shown that seeds of Boswellia papyrifera start germinating
around the fifth day after trial establishment [
18
,
20
]. In general, Boswellia seeds have short
dormancy, after one year of storage, the germination rate may drop to half [
16
]. Swartout
and Solowey [
14
] even report a lack of dormancy in Boswellia species which means that
seeds of Boswellia species do not actually need pre-sowing treatment; the best solution
is to soak them in cold water to germinate [
20
], as they likely cannot be stored at room
temperatures indefinitely.
Although natural regeneration occurs in most Boswellia species on Socotra, the re-
cruitment is missing, especially in ground-rooting species [
8
]. Their populations are thus
gradually aging as Lvonˇcík et al. [
9
] convincingly documented in the case study from
Homhil (Socotra) for the B. elongata population. Similar population structure and develop-
ment are documented across the entire area of Boswellia global distribution [
1
]. Missing or
poor natural regeneration resulting in an unbalanced age structure of Boswellia populations
is mentioned by many authors, for instance, for B. papyrifera in Sudan [
20
], in Eritrea [
3
,
4
,
30
]
and in Ethiopia [
6
,
31
,
32
]. The healthy, regenerating populations of B. papyrifera in Ethiopia
are unique [
33
]. Tolera et al. [
34
], investigating the population age structure of B. papyrifera,
stated that the current populations in Ethiopia lack successful recruitment since 1955. This
is in agreement with findings made by Lvonˇcík et al. [9] for B. elongata on Socotra Island.
Plants 2022,11, 1418 13 of 21
All the above-mentioned authors listed several factors to explain the missing young
age classes of trees in Boswellia populations, more often intensive resin harvesting leading
to extensive stem injuries and to decreasing of trees vitality that can be thereafter more
easily affected by insect and fungal diseases; frequent human-induced fires; changes in
land-use followed by land degradation or over-grazing. However, the fact that the success
rate of seedling recruitment is highly limited due to water stress and nutrient-poor soils,
must also be taken into account [25].
On the other hand, some authors mention the aspect of inaccessibility in species
growing in rocky habitats (rock-dwellers). Ouédraogo and Thiombiano [
17
] proved this
fact for B. dalzielii in Burkina Faso or Attorre et al. [
8
] for B. popoviana on Socotra Island.
They attribute the success in natural regeneration to the inaccessible terrain for goats and
to the remoteness of localities from inhabited areas.
An alternative way of regeneration could be vegetative propagation, as an adaptation
to specific stress conditions such as wildfires or drought. Recruitment by root suckers is
more common than sexual reproduction in Boswellia dalzielii [
17
]. Adam and Osman [
35
]
proved the ability of Boswellia papyrifera stumps to create sprouts in high percentages which
allow tree regeneration by coppicing. Propagation by cuttings with a high percentage of
rooting was reported by Abiyu et al. [
36
] and Haile et al. [
37
], which may help overcome
the population recruitment bottleneck of the Boswellia species [
37
] if properly managed and
assisted to enhance the genetic diversity, including the directed propagation of hybrids
and hybridogenic species that appear very often on Socotra [
15
,
38
,
39
] due to common
occurrence of ten different species’ distinct characteristics.
4. Materials and Methods
4.1. Seed Collection and Preparation
We covered a significant area on Socotra Island with the aim to collect seeds of all
known Boswellia species from different environments. The collection was carried out from
April to June in two subsequent years (2020–2021), the first from May to June 2020 including
12 localities, the second end of April until the end of June 2021 covering 35 localities ranging
between 1 and 932 m asl (Table 1, Figure 10). We aimed to collect seeds from five different
localities for each Boswellia species (not possible for all species). Each species at a specific
locality was assigned a code (Table 1) that is used in the graphs in the results. Seed collection
and germination tests were part of the project “Conservation of the endangered endemic
Boswellia trees on Socotra Island (Yemen)”, the project has written permission from the
Environmental Protection Authority, Hadibo, Socotra (EPA), and EPA is a partner of the
project and informed about the project activities.
Fruits were collected from at least ten adult trees per species, chosen randomly within
each locality. Ripe fruits, recognized by capsules being reddish, black, or brown (not green),
were collected directly from the trees and transported in separate recipients per species
and locality using labeled cotton bags. The fruits were air-dried for two–three days, then
the seeds were removed from the dried capsules manually and separated. The separated
seeds were stored in labeled envelopes in the local Boswellia seed bank on Socotra (storage
temperatures uncontrolled, ranging between 28
◦
C and 39
◦
C). The seeds were used for
seed germination laboratory trials within three to maximally six months of collection.
Plants 2022,11, 1418 14 of 21
Figure 10.
Map of the study area (Socotra Island, Yemen) showing the locations where seeds of
Boswellia species were collected.
4.2. Trials
A seed germination test was conducted for a random sample of 500 (in 2020) and
100 seeds
(in 2021; due to lower amounts) from all collected species and localities. Seeds of
each sample were divided into five replicates and germinated in Petri dishes. Conditions
for the tests were according to the conditions for seed germination of most of the woody
plants according to International Rules for Seed Testing [
40
] as follows: the dark phase
for 16 h at 20
◦
C and the illuminated phase for 8 h at 30
◦
C. The trial was observed daily
for 21 days straight during which germinated seeds were counted. A seed was deemed
germinated when the radicle was at least as long as the size of the seed (Figure 11). All
seed germination tests were carried out in Socotra. After each observation, seeds were
transferred to a separate container daily to avoid double counting in the next day. After the
end of the experiment, ungerminated seeds were cut and sorted into four classes: fresh,
empty, dead, or damaged by insects, defined as follows:
•
fresh—the tissue inside was solid, light or greenish, assuming start of germination in a
longer time than the length of the germination trial;
•
empty—without any tissue inside or remnants of tissue that filled less than half the
internal space of the seed;
•
dead—the tissue inside was soft, brownish and filled more than half the internal space
of the seed;
•
damaged by insects—seeds containing insects at different stages of development or an
insect exit hole was visible in the seed coat.
Germination tests started at the beginning of October 2020 on seven Boswellia taxa
endemic to Socotra Island from 12 localities collected in 2020; the next germination tests
were conducted in September 2021 on 34 different seed sets belonging to nine taxa from the
island, collected in 2021 (see all species and localities in Table 1).
Plants 2022,11, 1418 15 of 21
Figure 11.
Petri dish with seeds of Boswellia socotrana subsp. aspleniifolia, some of them already
developed radicle longer than the seeds, i.e., they are deemed as germinated.
4.3. Data Evaluation
The following parameters were selected for data processing and evaluation which are
described below.
Germination rate (in %) was defined as the number of germinated seeds at the end of
the experiment (after 21 days) out of the total number of seeds (including all seeds, full and
empty) [41].
Germination rate of full seeds (in %) was defined as the number of germinated seeds
at the end of the experiment (after 21 days) out of all full seeds. Full seeds are defined
here as all seeds (germinated, fresh, dead, damaged by insect) that were determined as
non-empty at the end of the germination test.
Germination energy (in %) was defined as the number of germinated seeds determined
on day 4 after setting up the germination test from the total number of seeds [
42
,
43
]
(including all seeds, full and empty).
Germination energy of full seeds (in %) was defined as the number of germinated
seeds on day 4 after setting up the germination test from all full seeds.
Mean daily germination—Czabator [
41
] presented a peak value as a maximum quo-
tient derived by dividing the number of germinants accumulated per day by the corre-
sponding number of days, which is the mean daily germination of the most vigorous
components of the seed lot. All values (not only peaks) are shown in the results (graphs).
Mean daily germination and percentages of germinated, fresh, dead, empty, and
insect-damaged seeds were processed in MS Excel for the creation of graphs. We used
Statistica 12.0 for data analysis and creation of the statistical graphs; one-way ANOVA was
conducted to assess intra-locality variability (i.e., variability among localities of one species
in the same year) of the data of the germination rate, the germination rate of full seeds and
the germination energy of full seeds. Box plots show mean values, standard deviations and
Plants 2022,11, 1418 16 of 21
95% confidence intervals. For inter-annual and inter-species variability, two-way ANOVA
was used for the data of the germination rate and the germination rate of full seeds. Mean
values are shown in graphs and the vertical bars represent 95% confidence intervals. When
a significant difference was observed, mean separation was performed using Fisher’s least
significant difference (LSD) test. All statistical tests were performed at a significance level
of p< 0.05.
5. Conclusions
Our results are relevant to the conservation of the endangered Boswellia species in
Socotra, as they indicate a realistic potential for seed germination for all species and for
most localities. Potential human-mediated factors affecting significant differences between
the years, between localities, or between species, are currently not examined in detail.
However, there are initial indications that some species (e.g., Boswellia socotrana) show more
potential for natural regeneration (under the conditions applied here, and without taking
into account grazing impacts) than others. Mean daily germination remains relatively low
for more than half of the species. Low germination rates in certain species or certain areas
should be examined in more detail to understand the potential (human or other) impacts
on their biology.
However, general factors impacting the Socotran terrestrial ecosystems are well un-
derstood, such as overgrazing and climate change impacts through recent cyclone ef-
fects [
13
,
42
,
43
]. In situ conservation and local seed germination in local nurseries on
Socotra combined with replantation in nature (protected from browsing and replanted
within the same area to avoid population mixing) are realistic additional strategies for
improving natural protection and natural regeneration. As most Frankincense tree species
in Socotra serve a variety of ecosystem services, among which their many ethnobotanical
uses [
11
], more than one strategy for replantation is useful, besides protection of the natural
terrestrial habitats, which are under various pressures. The current study on seed germina-
tion is a step towards strategizing as it improves the understanding of the future chances
of success of local conservation endeavors.
Author Contributions: Conceptualization, S.H., P.M., K.V.D. and F.A.; methodology, L.K., K.H. and
P.M.; formal analysis, L.K. and K.H.; investigation, S.H. and L.K.; resources, S.H. and K.H.; data
curation, L.K., K.H. and K.E.; writing original draft preparation, S.H., P.M., L.K. and K.H.; writing
review and editing, K.H., P.M., K.V.D., F.A., H.H., S.L. and K.E.; visualization, L.K., K.H. and P.V.;
supervision, P.M., K.V.D. and F.A.; project administration, P.M.; funding acquisition, P.M., K.V.D. and
F.A. All authors have read and agreed to the published version of the manuscript.
Funding: This research was funded by the Franklinia Foundation (2020–2023) “Conservation of the
endangered endemic Boswellia trees on Socotra Island (Yemen), grant number 2020-03”.
Data Availability Statement: Data used in this article are available from the authors.
Acknowledgments:
We would like to gratefully acknowledge the financial support of the Franklina
Foundation. Additionally, we want to express many thanks to the Environmental Protection Authority
(Hadibo, Socotra) for its permission and cooperation to implement our research. We are also grateful
to our friends Mohammed Amer, Mohammed Shanaihan, Salem Keebany and Mohammed Kaseem
for their help in this study.
Conflicts of Interest: The authors declare no conflict of interest.
Plants 2022,11, 1418 17 of 21
Appendix A
Table A1. Mean values from germination tests in 2020 (±standard deviation).
Boswellia Species Sp. Code Locality Germination
Rate (%)
Germination Rate
of Full Seeds (%)
Germination
Energy (%)
Germination Energy
of Full Seeds (%) Fresh (%) Dead (%) Empty (%) Insect (%)
B. ameero BADN Danagahan 38 ±7.13 85 ±7.13 12 ±5.34 27 ±11.05 0 ±0 1 ±2.4 55 ±9.42 6 ±2.64
B. bullata BBT Taida’ah
(Ditwah
mountain) 1±2 3 ±5.71 0 ±0 0 ±0 0 ±0 28 ±4 71 ±4.9 0 ±0
B. dioscoridis BDS Sheebhan 17 ±4.12 67 ±8.25 0 ±0 0 ±0 0 ±0 8 ±2.61 75 ±6.97 1 ±1.2
B. elongata BEDB Diburak 0 ±0 0 ±0 0 ±0 0 ±0 0 ±0 1 ±1.02 98 ±1.47 0 ±0.49
B. elongata BEDS Dishal 10 ±3.03 70 ±8 9 ±3.66 63 ±15.22 0 ±0 2 ±1.17 86 ±2.9 2 ±0.98
B. elongata BEH Homhil 26 ±3.41 44 ±3.44 25 ±2.93 43 ±4.07 0 ±0 17 ±1.74 41 ±8.23 16 ±5.19
B. elongata BEM Makalihim 4 ±1.62 25 ±7.47 2 ±1.02 19 ±9.15 0 ±0 9 ±2.73 86 ±3.9 1 ±1.55
B. popoviana BPK Klisan 0 ±0 0 ±0 0 ±0.4 2 ±4.44 0 ±0 4 ±2.5 93 ±2.61 3 ±1.85
B. popoviana BPV Momi Falang 6 ±1.02 32 ±4.59 1 ±1.17 6 ±5.57 6 ±1.02 6 ±1.94 80 ±2.15 2 ±0.75
B. socotrana subsp.
aspleniifolia BSAS Shata
Qalansiyah 89 ±3.85 89 ±4.01 81 ±3.61 82 ±3.87 0 ±0 10 ±3.6 0 ±0.49 0 ±0.49
B. socotrana subsp.
socotrana BSSA Ayhaft 90 ±2.32 90 ±2.17 85 ±3.06 85 ±3.18 0 ±0 7 ±2.73 1 ±0.8 2 ±0.98
Plants 2022,11, 1418 18 of 21
Table A2. Mean values from germination tests in 2021 (±standard deviation).
Boswellia Species Sp. Code Locality Germination
Rate (%)
Germination Rate
of Full Seeds (%)
Germination
Energy (%)
Germination Energy
of Full Seeds (%) Fresh (%) Dead (%) Empty (%) Insect (%)
B. ameero BAA Ayhaft 3 ±4 3 ±4.19 2 ±2.45 2 ±2.52 0 ±0 88 ±8.72 2 ±2.45 7 ±5.1
B. ameero BADN Danagahan 42 ±14.35 44 ±15.76 18 ±13.64 19 ±14.61 1 ±2 51 ±15.62 5 ±4.47 1 ±2
B. ameero BADX Dixam 14 ±8.6 14 ±9.15 12 ±6.78 12 ±7.26 0 ±0 71 ±13.19 2 ±2.45 13 ±5.1
B. ameero BAF Firmihin 5 ±4.47 5 ±4.73 0 ±0 0 ±0 0 ±0 88 ±7.48 4 ±4.9 3 ±4
B. ameero BAQ Qatariyah 60 ±7.07 65 ±6 7 ±8.72 8 ±9.54 2 ±2.45 28 ±4 8 ±4 2 ±2.45
B. bullata BBH Hazahaz 45 ±11.4 49 ±11.73 24 ±10.2 26 ±9.31 0 ±0 47 ±9.8 8 ±6.78 0 ±0
B. bullata BBSG Shoab rock
(green flowers) 50 ±8.94 61 ±10.47 33 ±6.78 40 ±5.44 0 ±0 32 ±9.27 18 ±6.78 0 ±0
B. bullata BBSR Shoab
(red flower) 36 ±4.9 37 ±6.71 18 ±6.78 19 ±7.87 0 ±0 61 ±8.6 3 ±4 0 ±0
B. bullata BBT Taida’ah
(Ditwah
mountain) 51 ±10.2 54 ±10.58 6 ±5.83 6 ±5.81 0 ±0 41 ±10.68 6 ±5.83 2 ±2.45
B. dioscoridis BDDA Wadi Diasraha 50 ±4.47 69 ±8.17 0 ±0 0 ±0 1 ±2 22 ±8.12 27 ±9.27 0 ±0
B. dioscoridis BDDF Wadi
Difa’araha 80 ±9.49 90 ±10 0 ±0 0 ±0 3 ±2.45 5 ±6.32 11 ±8.6 1 ±2
B. dioscoridis BDDG Wadi Digasfa 70 ±7.07 76 ±7.21 1 ±2 1 ±2 0 ±0 22 ±7.48 8 ±6.78 0 ±0
B. dioscoridis BDH Halah
(Hoq cave) 13 ±5.1 13 ±4.93 3 ±2.45 3 ±2.55 0 ±0 83 ±2.45 4 ±3.74 0 ±0
B. dioscoridis BDS Sheebhan 20 ±8.94 20 ±8.77 6 ±4.9 6 ±4.89 0 ±0 78 ±6.78 2 ±2.45 0 ±0
B. elongata BEDB Diburak 0 ±0 0 ±0 0 ±0 0 ±0 0 ±0 1 ±2 99 ±2 0 ±0
B. elongata BEDS Dishal 2 ±4 20 ±40 1 ±2 10 ±20 0 ±0 0 ±0 98 ±4 0 ±0
B. elongata BEH Homhil 36 ±11.14 76 ±17.3 36 ±11.14 76 ±17.3 0 ±0 10 ±5.48 54 ±6.63 0 ±0
B. elongata BEM Makalihim 2 ±2.45 12 ±14.53 2 ±2.45 12 ±14.53 0 ±0 8 ±2.45 87 ±5.1 3 ±2.45
B. elongata BES Shabarah 15 ±7.07 94 ±11.43 11 ±8 55 ±32.3 0 ±0 2 ±4 83 ±10.3 0 ±0
B. nana BNH Hamadarah
(Homhil) 47 ±17.2 71 ±16.19 40 ±11.4 61 ±9.83 0 ±0 16 ±7.35 36 ±9.7 1 ±2
Plants 2022,11, 1418 19 of 21
Table A2. Cont.
Boswellia Species Sp. Code Locality Germination
Rate (%)
Germination Rate
of Full Seeds (%)
Germination
Energy (%)
Germination Energy
of Full Seeds (%) Fresh (%) Dead (%) Empty (%) Insect (%)
B. popoviana BPB Bedgofahar 0 ±0 0 ±0 0 ±0 0 ±0 0 ±0 0 ±0 100 ±0 0 ±0
B. popoviana BPD Sheebhan
(Didrafarantan) 55 ±8.94 85 ±3.23 0 ±0 0 ±0 0 ±0 10 ±3.16 35 ±11.4 0 ±0
B. popoviana BPF Firmihin 29 ±4.9 84 ±12.19 3 ±2.45 9 ±7.84 0 ±0 6 ±4.9 65 ±6.32 0 ±0
B. popoviana BPK Klisan 0 ±0 0 ±0 0 ±0 0 ±0 0 ±0 0 ±0 100 ±0 0 ±0
B. popoviana BPV Momi Falang 1 ±2 20 ±40 1 ±2 20 ±40 0 ±0 5 ±4.47 94 ±3.74 0 ±0
B. scopulorum BSB Bedgofahar 12 ±6.78 80 ±26.67 0 ±0 0 ±0 0 ±0 3 ±4 85 ±5.48 0 ±0
B. socotrana subsp.
aspleniifolia BSAB Raidah
(Taida’ah) 64 ±13.56 91 ±8.27 59 ±12.41 84 ±9.39 0 ±0 6 ±5.83 30 ±11.4 0 ±0
B. socotrana subsp.
aspleniifolia BSAN Dinawtat 72 ±12.88 77 ±12.6 70 ±12.25 75 ±11.27 6 ±3.74 15 ±8.37 7 ±4 0 ±0
B. socotrana subsp.
aspleniifolia BSAS Shata
Qalansiyah 56 ±19.85 68 ±19.77 53 ±17.49 64 ±17.17 0 ±0 25 ±13.04 19 ±11.58 0 ±0
B. socotrana subsp.
aspleniifolia BSATD Taida’ah
(Ditwah
mountain) 67 ±9.27 86 ±5.35 64 ±11.58 82 ±9.15 2 ±2.45 9 ±3.74 22 ±6 0 ±0
B. socotrana subsp.
aspleniifolia BSATR Tarabah 70 ±15.17 78 ±14.9 69 ±17.15 77 ±17.29 1 ±2 18 ±11.66 11 ±7.35 0 ±0
B. socotrana subsp.
socotrana BSSA Ayhaft 16 ±10.2 45 ±24.19 16 ±10.2 45 ±24.19 2 ±2.45 10 ±11.4 65 ±10.49 7 ±6.78
B. socotrana subsp.
socotrana BSSH Hamadarah
(Homhil) 32 ±10.3 54 ±15.43 25 ±10 43 ±15.47 5 ±6.32 8 ±5.1 40 ±11.83 15 ±7.07
B. socotrana subsp.
socotrana BSSZ Zarkan
(Asmin) 82 ±5.1 83 ±6.69 76 ±3.74 77 ±4.86 0 ±0 15 ±6.32 1 ±2 2 ±2.45
Plants 2022,11, 1418 20 of 21
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