ArticlePDF Available

Abstract and Figures

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).
Content may be subject to copyright.
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
Publisher’s Note: MDPI stays neutral
with regard to jurisdictional claims in
published maps and institutional affil-
iations.
Copyright: © 2022 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
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
References
1.
Bongers, F.; Groenendijk, P.; Bekele, T.; Birhane, E.; Damtew, A.; Decuyper, M.; Eshete, A.; Gezahgne, A.; Girma, A.;
Khamis, M.A.; et al. Frankincense in peril. Nat. Sustain. 2019,2, 602–610. [CrossRef]
2.
Madˇera, P.; Paschová, Z.; Ansorgová, A.; Vrškový, B.; Lvonˇcík, S.; Habrová, H. Volatile compounds in oleo-gum resin of Socotran
species of Burseraceae. Acta Univ. Agric. Silvic. Mendel. Brun. 2017,65, 73–90. [CrossRef]
3.
Ogbazghi, W. The Distribution and Regeneration of Boswellia papyrifera (Del.) Hochst. in Eritrea. Ph.D. Thesis, Wageningen
University, Wageningen, The Netherlands, 2001; p. 131.
4.
Ogbazghi, W.; Bongers, F.; Rijkers, T.; Wessel, M. Population structure and morphology of the frankincense tree Boswellia papyrifera
along an altitude gradient in Eritrea. J. Drylands 2006,1, 85–94.
5.
Gebrehiwot, K.; Muys, F.B.; Haile, M.; Mitloehner, R. Introducing Boswellia papyrifera (Del.) Hochst. and its non-timber forest
product, frankincense. Int. For. Rev. 2003,5, 348–353. [CrossRef]
6.
Negussie, A.; Aerts, R.; Gebrehiwot, K.; Muys, B. Seedling mortality causes recruitment limitation of Boswellia papyrifera in
northern Ethiopia. J. Arid Environ. 2008,72, 378–383. [CrossRef]
7.
Sabo, P.; Ouédraogo, A.; Salako, K.V.; GlèlèKakaï, R. Land use impacts on Boswellia dalzielii Hutch., an African frankincense tree
in Burkina Faso. Bois Forêts Trop. 2021,349, 51–63. [CrossRef]
8.
Attorre, F.; Taleb, N.; De Sanctis, M.; Farcomeni, A.; Guillet, A.; Vitale, M. Developing conservation strategies for endemic tree
species when faced with time and data constraints: Boswellia spp. on Socotra (Yemen). Biodivers. Conserv.
2011
,20, 1483–1499.
[CrossRef]
9.
Lvonˇcík, S.; Vahalík, P.; Bongers, F.; Peijenburg, J.; Hušková, K.; Van Rensburg, J.J.; Hamdiah, S.; Madˇera, P. Development of
Boswellia elongata Balf. F., population in Homhil protected area, Soqotra. Rend. Lincei Sci. Fis. Nat. 2020,31, 747–759. [CrossRef]
10. Thulin, M. The Genus Boswellia (Burseraceae): The Frankincense Trees; Acta Universitatis Upsaliensis: Uppsala, Sweden, 2020.
11. Miller, A.G.; Morris, M. Ethnoflora of the Soqotra Archipelago; Royal Botanic Garden Edinburgh: Edinburgh, UK, 2004.
12. Lvonˇcík, S.; ˇ
Repka, R. Boswellia socotrana: One or two taxa? Novon 2020,28, 17–23. [CrossRef]
13.
Madˇera, P.; Volaˇrík, D.; Patoˇcka, Z.; Kalivodová, H.; Divín, J.; Rejžek, M.; Vybíral, J.; Lvonˇcík, S.; Jeník, D.; Hanáˇcek, P.; et al.
Sustainable land use management needed to conserve the dragon
´
s blood tree of Socotra Island, a vulnerable endemic umbrella
species. Sustainability 2019,11, 3557. [CrossRef]
14.
Swartout, B.T.; Solowey, E. Increasing Boswellia sacra seeds’ germination viability and genetic variability utilizing various methods.
Net J. Agric. Sci. 2018,6, 29–34. [CrossRef]
15. Eslamieh, J. Creating “Perfect” Boswellia. Cactus Succul. J. 2010,82, 126–131. [CrossRef]
16.
Eshete, A.; Teketay, D.; Lemenih, M.; Bongers, F. Effects of resin tapping and tree size on the purity, germination and storage
behavior of Boswellia papyrifera (Del.) Hochst. seeds from Metema District, northwestern Ethiopia. For. Ecol. Manag.
2012
,269,
31–36. [CrossRef]
17.
Ouédraogo, A.; Thiombiano, A. Regeneration pattern of four threatened tree species in Sudanian savannas of Burkina Faso.
Agrofor. Syst. 2012,86, 35–48. [CrossRef]
18.
Rijkers, T.; Ogbazghi, W.; Wessel, M.; Bongers, F. The effect of tapping for frankincense on sexual reproduction in
Boswellia papyrifera.J. Appl. Ecol. 2006,43, 1188–1195. [CrossRef]
19.
Gebre Medhin, T.G.; Negash, L. The Effect of Different Pre-Sowing Seed Treatments on the Germination of Boswellia papyrifera, a Key
Dryland Tree; Final Report; Ethiopian Society of Soil Science: Addis Ababa, Ethiopia, 1999.
20.
Adam, A.A.; El Tayeb, A.M. A comparative study of natural regeneration of B. papyrifera and other tree species in Jebel Marra
Darfur; Sudan. Res. J. Agric. Biol. Sci. 2008,4, 94–102.
21.
Savithramma, N.; Ankanna, S.; Bhumi, G. Effect of nanoparticles on seed germination and seedling growth of Boswellia ovalifoliolata
an endemic and endangered medicinal tree taxon. Nano Vis. 2020,2, 2.
22.
De Souza, A.C.; de Oliveira, L.M.; Souza, G.F.; Schmidt, S.S.; Liesch, P.P. Causes of low seed quality in Ilex paraguariensis A. St. Hil.
samples (Aquifoliaceae). Floresta Ambient. 2020,27, e20170960. [CrossRef]
23.
Wang, K.S. Relationship between empty seed and genetic factors in European beech (Fagus sylvatica L.). Silva Fenn.
2003
,37,
419–428. [CrossRef]
24.
Fuentes, M.; Shupp, E.W. Empty seeds reduce seed predation by birds in Juniperus osteosperma.Evol. Ecol.
1998
,12, 823–827.
[CrossRef]
25.
Raju, A.J.S.; Lakshmi, P.V.; Ramana, K.V. Entomophily, ornithophily and anemochory in the highly self-incompatible
Boswellia ovalifoliolata
Bal. & Henry (Burseraceae), an endemic and endangered medicinal tree species. J. Threat. Taxa
2012
,4,
2673–2684. [CrossRef]
26.
Sunnichan, V.G.; Mohan Ran, H.Y.; Shivanna, K.R. Reproductive biology of Boswellia serrata, the source of salai guggul, an
important gum-resin. Bot. J. Linn. Soc. 2005,147, 73–82. [CrossRef]
27.
García, C.; Vasconcelos, R. The beauty and the beast: Endemic mutualistic interactions promote community-based conservation
on Socotra Island (Yemen). J. Nat. Conserv. 2017,35, 20–23. [CrossRef]
28.
Scholte, P.; De Geest, P. The climate of Socotra Island (Yemen). A first-time assessment of the timing of the monsoon wind reversal
and its influence on precipitation and vegetation patterns. J. Arid Environ. 2010,74, 1507–1515. [CrossRef]
Plants 2022,11, 1418 21 of 21
29.
Kalivodová, H.; Culek, M.; ˇ
Cermák, M.; Madˇera, P.; Habrová, H. Potential importance of Socotra dragon’s blood tree cloud forests
and woodlands for capturing horizontal precipitation. Rend. Lincei Sci. Fis. Nat. 2020,31, 607–621. [CrossRef]
30.
Abiyu, A.; Bongers, F.; Eshete, A.; Gebrehiwot, K.; Kindu, M.; Lemenih, M.; Moges, Y.; Ogbazghi, W.; Sterck, F.J. Incense
woodlands in Ethiopia and Eritrea: Regeneration problems and restoration possibilities. In Degraded Forests in Eastern Africa;
Routledge: Abingdon, UK, 2010; pp. 144–163.
31.
Bantihun, A.; Tesema, T. Regeneration status of Acacia polyacantha and Boswellia papyrifera species in Shimelegir Forest, Jawi
District, Ethiopia. J. Nat. Sci. Res. 2018,8, 27–36. [CrossRef]
32.
Groenendijk, P.; Eshete, A.; Sterck, F.J.; Zuidema, P.A.; Bongers, F. Limitations to sustainable frankincense production: Blocked
regeneration, high adult mortality and declining populations. J. Appl. Ecol. 2012,49, 164–173. [CrossRef]
33.
Teshome, M.; Eshete, A.; Bongers, F. Uniquely regenerating frankincense tree populations in western Ethiopia. For. Ecol. Manag.
2017,389, 127–135. [CrossRef]
34.
Tolera, M.; Sass-Klaassen, U.; Eshete, A.; Bongers, F.; Sterck, F.J. Frankincense tree recruitment failed over the past half century.
For. Ecol. Manag. 2013,304, 65–72. [CrossRef]
35.
Adam, A.A.; Osman, A.A. Sprouting capacity of Boswellia papyrifera (Del.) Hochst in Jebel Mrarra Area, Darfur; Sudan: Effect of
stump diameter and height. Res. J. Agric. Biol. Sci. 2008,4, 51–57.
36.
Abiyu, A.; Dejene, T.; Eshete, A.; Sisay, K. Vegetative propagation of Boswellia papyrifera: Time of collection and propagule size
affect survival and establishment. J. Arid Environ. 2016,133, 122–124. [CrossRef]
37.
Haile, G.; Gebrehiwot, K.; Lemenih, M.; Bongers, F. Time of collection and cutting sizes affect vegetative propagation of
Boswellia papyrifera (Del.) Hochst through leafless branch cuttings. J. Arid Environ. 2011,75, 873–877. [CrossRef]
38.
Lvonˇcík, S.; Madˇera, P.; Volaˇrík, D.; Vrškový, B.; Habrová, H. First proposal of seed regions for frankincense trees (Boswellia spp.)
on Socotra Island. J. Landsc. Ecol. 2013,6, 35–45. [CrossRef]
39.
Niebler, J.; Eslamieh, J.; Buettner, A. Frankincense revisited, part II: Volatiles in rare Boswellia species and hybrids. Chem. Biodivers.
2016,13, 630–643. [CrossRef]
40.
International Seed Testing Association (ISTA). International Rules for Seed Testing; International Seed Testing Association: Bassers-
dorf, Switzerland, 2020; Chapter 5; pp. 21–52.
41.
Czabator, F.J. Germination value: An index combining speed and completeness of pine seed germination. For. Sci.
1962
,8,
386–396.
42.
Attorre, F.; Van Damme, K. Twenty years of biodiversity research and nature conservation in the Socotra Archipelago (Yemen).
Rend. Lincei Sci. Fis. Nat. 2020,31, 563–569. [CrossRef]
43.
Madˇera, P.; Van Damme, K. Socotra Archipelago (Yemen). In The Encyclopedia of Conservation; Elsevier: Amsterdam,
The Netherlands
,
2020; ISBN 9780124095489. [CrossRef]
... Several factors play a role in their global decline, mainly intensity of grazing and the olibanum trade (Bongers et al., 2019). There is a general lack of natural regeneration in Boswellia because of human and climate impacts, which is also the case in Socotra (Attorre et al., 2011;Lvončík et al., 2013, even though the biological capacity for regeneration (through seed germination) is present (Hamdiah et al., 2022). ...
... The lack of regeneration in Socotran Boswellia has been shown to have no direct biological cause, because in nearly all species, a good proportion of the seeds germinate easily (Hamdiah et al., 2022). After germination however, these vulnerable seedlings have to survive in a hostile environment challenged by low water availability and herbivores in the form of goats. ...
... Individual protection of naturally occurring seedlings during the rainy season is another applied measure, which is more demanding for maintenance but will not limit movement of livestock through rangeland and pastures. Chances for natural regeneration in the absence of grazing pressure are realistic, as seed production and germination rates are high for all species (Hamdiah et al., 2022). Therefore, in exclosures, seedlings are expected to survive after rain to grow and eventually produce offspring (Habrová & Pavliš, 2017;Maděra, Habrová, et al., 2019). ...
Article
Full-text available
Societal Impact Statement Conserving frankincense trees (Boswellia) is crucial for both ecological and socio‐economic reasons. Surveying these trees in the field and using remote sensing unmanned aerial vehicles in the Socotra Archipelago, we found that Socotran frankincense trees are threatened by forest fragmentation, overgrazing, and increasingly frequent extreme climate events. A better understanding of the distribution and the threats of these important insular species will improve the conservation policy of the local authorities and benefit local communities in the Socotra Archipelago. At the same time, this work serves as a good practice example to guide conservation efforts for other culturally important threatened tree species around the world, therefore helping to sustain local livelihoods, fostering ecological resilience, and supporting socio‐economic stability. Summary Globally, frankincense trees (Burseraceae: Boswellia) are increasingly under threat because of habitat deterioration, climate impacts, and the olibanum trade. Despite harboring nearly half of the species in the genus, up‐to‐date insights are lacking for the insular endemic frankincense trees of the Socotra Archipelago UNESCO (United Nations Educational, Scientific and Cultural Organization) World Heritage Site (Yemen). We combined georeferencing of individual trees in the field with remote sensing applying unmanned aerial vehicles (UAVs) to evaluate Boswellia distribution and (sub)population sizes in the entire Socotra Archipelago. We counted 17,253 trees across all 11 taxa and we surveyed almost 55% directly in the field, collecting individual information on threats and health indicators. We estimate that the current total population sizes of the relatively common Socotran Boswellia taxa (Boswellia elongata, Boswellia popoviana, and Boswellia ameero) consist of a few thousand mature individuals with fragmented distribution of which a large proportion occurs in highly disjunct relictual stands, while the more range‐restricted species survive only through a few hundred (Boswellia nana and Boswellia samhaensis) to fewer than a hundred trees (Boswellia scopulorum). Our field data show that the Socotran frankincense trees are threatened by fragmentation and overgrazing resulting in a lack of natural regeneration, in combination with effects of extreme climate events (e.g., higher frequency and intensity of cyclones and prolonged drought) and potential future infrastructure developments; the species are less impacted by resin collection. We provide recommendations to strategize urgent protection of the declining Socotran frankincense trees, and we update their conservation status, resulting in an endangered status for seven and a critically endangered status for four taxa.
... Natural regeneration and seedling establishment in Boswellia is better in the absence of grazing in different areas of the world (Gebrehiwot et al. 2003;Ogbazghi et al. 2006;Negussie et al. 2008;Bongers et al. 2019) and protecting woodland areas from livestock pressure has a high conservation potential in Socotra (Habrová, Pavliš 2017 (Hamdiah et al. 2022). Therefore, there is a potential for natural regeneration, guided through conservation efforts. ...
... The reasons for decline could also be partly biological. However, all Boswellia species in Socotra produce a healthy proportion of viable seeds (Hamdiah et al. 2022). This result demonstrated that there is, at least, good potential for natural regeneration in some species and/or localities of Boswellia stands (Hamdiah et al. 2022). ...
... However, all Boswellia species in Socotra produce a healthy proportion of viable seeds (Hamdiah et al. 2022). This result demonstrated that there is, at least, good potential for natural regeneration in some species and/or localities of Boswellia stands (Hamdiah et al. 2022). Nevertheless, there is also a large proportion of unfertilised seeds, which may indicate the presence of a problem with pollination or another biological/ecological factor (Raju et al. 2012). ...
... . Topics in this Special Issue. Overview of topics and articles related to them: seed quality [1,2], physical and biological factors [3,4], seed pre-treatment [5][6][7][8], management [9,10], salt and drought stress [11,12], and seed technology [13]. ...
... Hamdiah et al. [2] were interested in the biological characteristics of the seeds of nine endemic taxa Boswellia (Burseraceae) tree species from Socotra Island (Yemen). They tested seed germination rates in controlled experiments for two subsequent years. ...
Article
Full-text available
Plants have evolved various strategies allowing them to be successful in heterogeneous habitats, including the number and size of the seeds they produce, mechanisms for their dispersal, seed dormancy, seed vigor, seed germination, etc [...]
... The family Burseraceae stands out as having the highest rate of endemism among the plants in the Socotra Archipelago, with at least 15 taxa present in the genera Boswellia (11 taxa, all endemic) and Commiphora (5 species, 4 endemic) (Miller and Morris, 2004;Brown and Mies, 2013;Thulin, 2020). Although there have been several studies on the taxonomy, distribution, conservation and biology of the Socotran Boswellia (Miller and Morris, 2004;Attorre et al., 2011;Lvončík et al., 2013Lvončík et al., , 2020Thulin, 2020;Hamdiah et al., 2022), comparably little is known about the archipelago's endemic Commiphora species. ...
... Another issue is the lack of natural regeneration from seeds, due to the grazing pressure which leads the goats to eat whatever plants they encounter in particular small seedlings, except for those situated in inaccessible areas or in a protected location (e.g., rocky slopes, surrounded by stones), as seen for Boswellia spp. (Lvončík et al., 2020;Hamdiah et al., 2022) or Dracaena cinnabari (Habrová and Pavlis, 2017;Maděra et al., 2019a). Ultimately, an indirect effect of overgrazing is land degradation and soil erosion. ...
Article
Full-text available
The Socotra Archipelago (Yemen) is an interesting biodiversity hotspot, with a significant proportion of endemic species that have evolved to survive in an arid subtropical environment, inscribed as a World Heritage Site by UNESCO. The terrestrial ecosystems of Socotra face several threats, including climate change, overgrazing and soil degradation. Socotra Island has four endemic species of the genus Commiphora (Burseraceae). Little is known about their local distribution and ecology, yet these trees could be useful indicator species. Our study focuses on the distribution and niche characterisation of the four endemic Commiphora species of Socotra and how climate change may affect them. The aim is to improve insights into their habitats and to provide an essential basis for future local management plans and ecological restoration. We compared the current distribution with the forecasted potential distribution under a CMIP6 (Coupled Model Intercomparison Project) climate scenario, allowing us to define target conservation areas and assess potential local extinction risks. To achieve this, we collected distribution data in the field throughout Socotra Island, covering the current distribution ranges of the four species. To assess the potential distribution of these species, we applied three models (GAM, MaxEnt, RandomForest) using bioclimatic, topographic and soil variables. Forecasts under a climate change scenario were made using bioclimatic variables from the CMCC-CESM2 climate model for two different socioeconomic pathways. The distribution of three endemic Socotran Commiphora is mainly correlated to clay content in the soil and winter precipitation, while C. socotrana is affected by seasonal precipitation and temperature. Under different potential future climate scenarios, the distribution of C. ornifolia is predicted to remain stable or increase, while C. parvifolia distribution could increase, yet C. planifrons and C. socotrana are predicted to undergo a strong reduction of suitable areas and an upward shift in the mountains. Our results highlight that it is essential to conserve the unique terrestrial ecosystems in Socotra and to preserve these endemic trees which have a wide range of ecosystem services. Updates on the predicted extinction risk assessment are fundamental to understand conservation priorities and strategize future actions to ensure the persistence of Socotran myrrh trees and other endangered endemic tree taxa on the island.
... Additionally, the low germination rate of N. jamban seeds may be a contributing factor to its endangerment in natural habitat, a phenomenon observed commonly in rare and endemic species such as Betula humilis (Bona et al. 2022), Manglietia crassipes (Wang et al. 2021), and Boswellia spp. (Hamdiah et al. 2022). The percentage of pitchers developing shoots at ten months after culture. ...
Article
Full-text available
The study to optimize in vitro propagation of the Indonesian native and critically endangered species, Nepenthes jamban, in order to support the ex-situ conservation efforts has been done. Using Murashige and Skoog (MS) as a basal media, disinfected seeds of N. jamban were germinated on five types of germination media, viz. ¼ MS, ½ MS, MS, ¼ MS+benzyl adenine (BA)+Biotin and MS+BA+Biotin. Afterwards, in vitro shoots with 6-7 leaves were inoculated on growing media, i.e., ¼ MS, ¼ MS 60 (3:1) (MS modification with a higher concentration of nitrogen), and ¼ MS+naphtalene acetic acid (NAA)+BA. The results showed that the germination of N. jamban seeds was slow, indicated by the percentage of germination being less than 20% after 6 months of being planted on germination media. The highest percentage of germination was after the 6th month and the greatest pitcher development at the 10th month were obtained on ¼ MS medium. Furthermore, shoot growth and pitchers development consistently increased for 12 months in ¼ MS 60 (3:1) medium while other media resulted in a decrease in pitcher formation. It seemed that low concentrations of nutrient in the medium proved to be more effective to induce in vitro seed germination and enhance shoot growth which was also supported by higher nitrogen (nitrate) concentration in the medium. This study provides information that supports ex situ conservation action of native and critically endangered Nepenthes species from Indonesia.
... The stem bark is used for the management of venereal diseases, fever, leprosy, rheumatism, ulcers, pain, inflammation, gastrointestinal disorders, malaria, toothaches, sores, abscesses, mental disorders, yellow fever, asthma, wounds, and dysentery (Burkhil 2004). Despite these combined uses, unfortunately, all members of the genus Boswellia are globally endangered as a result of overexploitation and overgrazing by livestock (Hamdiah et al. 2022), fire, land conversion for agriculture, improper or excessive harvesting of resin, and attacks by insects (Johnson et al. 2023). This species is threatened in Nigeria by overharvesting, agricultural expansion, excessive grazing, and climate change. ...
Preprint
Full-text available
Nigeria is one of the most floristic rich countries on the continent of Africa due to the variation in climate, which favors the growth of several species. Sadly, its biodiversity is one of the most threatened in the world, mainly due to deforestation and various unsustainable land use patterns, which are human activities. However, these anthropogenic activities are more prevalent in Nigeria's northern savanna zone (NSZ). In this study, we present the first regional conservation assessments and red listing of tree species in the northern savanna zone (NSZ) of Nigeria according to the International Union for Conservation of Nature (IUCN) criteria and categories. We recorded 31 tree species as the most utilized in the region. For the assessments, we provided the fundamental taxonomic information of each species, their local names, and their uses. This study provided the extent of occurrence, area of occupancy, population size and trend, description of habitats, and ecological requirements and discussion of the threats affecting each species and their habitats. We further inform conservation actions and research activities needed to ensure the future of the tree species and their sustainable uses. Overall, approximately 97% of the taxa were evaluated as threatened (41% as endangered, 31% as critically endangered, 24% as vulnerable, and 4% as least concerned). Therefore, we recommend the adoption of the risk status of the species to develop sound conservation strategies and measures for the management of flora in this inundated region.
... The stem bark is used for the management of venereal diseases, fever, leprosy, rheumatism, ulcers, pain, in ammation, gastrointestinal disorders, malaria, toothaches, sores, abscesses, mental disorders, yellow fever, asthma, wounds, and dysentery (Burkhil 2004). Despite these culminated uses, unfortunately, all members of the genus Boswellia are globally endangered as a result of overexploitation and overgrazing by livestock(Hamdiah et al. 2022), re, land conversion for agriculture, improper or excessive harvesting of resin, and attacks by insects(Johnson et al. 2023). This species is threatened in Nigeria by overharvesting, agriculture expansion, excessive grazing, and climate change. ...
Preprint
Full-text available
Nigeria is one of the most floristic rich countries on the continent of Africa due to the variation in climate, which favors the growth of several species. Sadly, its biodiversity is one of the most threatened in the world mainly due to deforestation and various forms of unsustainable land use patterns, which are human activities. However, these anthropogenic activities are more prevalent in Nigeria's northern savanna zone (NSZ). In this study, we present the first regional Conservation assessments and Red Listing of tree species of the Northern Savanna Zone (NSZ) of Nigeria according to the International Union for Conservation of Nature (IUCN) criteria and categories. We recorded 31 tree species as the most utilized in the region in the region. For the assessments, we provided the fundamental taxonomic information of each species, their local names, and uses. This study provided the extent of occurrence, area of occupancy, population size and trend, a description of habitats, ecological requirements; discussion of the threats affecting each species and their habitats. We further also inform conservation actions and research activities needed to ensure the future of the tree species and their sustainable uses. Overall, about 97% of the taxa were evaluated as threatened (41% as Endangered, 31% as critically endangered, 24% as Vulnerable, and 4% as Least Concerned). Based on this, we recommend the adoption of the risk status of the species to develop sound conservation strategies and measures for the management of flora in this inundated region
... Germination of seeds was marked as the radicle reached 1/2 of the seed length by following the method of Xiao et al. [23], and observation was ended on the 7th day of the germination experiment. The rest of the parameters, including seedling biomass, seed germination energy (GE), germination rate (GR), mean germination time (MGT), and germination index (GI), were measured with Equations (1)-(6) as follows [24]: ...
Article
Full-text available
Nitrogen, despite being essential for the growth of plants, can pose serious threats to the ecological environment when applied excessively as fertilizers. The application of nanomaterials has a catalytic effect on crop growth and a restorative effect on the environment. However, their effect on mitigating ammonium stress in crops is poorly understood. In the present study, the roles of nanoparticles of magnesium oxide (nMgO) and hydroxyapatite (nHA) with different application rates (0, 10, 100, 500, and 1000 mg L−1) on seed germination and seedling growth in water spinach (Ipomoea aquatica Forssk.) and Hami melon (Cucumis melo L.) were investigated, and the ammonium stress mitigating capacity of nanoparticles with the optimal application rate on the two crops was analyzed. The results showed that the application of nMgO and nHA at an optimal rate of 100 mg L−1 significantly promoted seed germination of water spinach, followed by the increase of germination potential, seed germination rate, and germination index, while alleviating the inhibitory effect of NH4+ stress in water spinach. As for the Hami melon, nHA reduced the ammonium stress on seedlings by promoting antioxidant enzyme activity, while nMgO was found to be involved in reducing the root growth of Hami melon seedlings. This study provided a reference on how to select the appropriate type and optimize the application method of nanomaterials that will be used in agriculture in the future.
Article
With the waves of evolution in genomics and genomics technology, the 21st century has experienced a surge in human and pathogen genome sequencing both at the clinical and public health care levels. These latest efforts have led to what is commonly referred to as "precision public health," which is a multidisciplinary field that incorporates genomics, artificial intelligence (AI), and big data to help predict the healthcare outcomes of an individual and improve the general population's health. To individualize healthcare at the clinical and public health levels, research efforts have seen the emergence and utilization of technology in the management of healthcare. Despite precision public health being ascribed as a highly promising tool that could help provide solutions to many public health problems in developed societies, how this turns out in developing nations is yet to be established. This study applied an analytical cross-sectional study design and aimed at assessing challenges and enablers of PPH in Nigeria using genomic surveillance with an objective of understanding the challenges, establishing the influence of data integration methods on the attainment of PPH, the influence of health equity on the attainment of PPH and identifying the influence of health policies. The empirical literature review and cross-sectional study design were used with SPSS 23, and the visualization of data was done using the Microsoft Excel 2019 software. The study findings illustrated that more than 52% of the respondents have heard about precision public health, with 56.4% of the respondents disagreeing with the equitable distribution of technological infrastructure to support data management. A high proportion of the respondents agree that the government can implement PPH in Nigeria. However, a slightly higher proportion of the respondents (46.2%) disagreed on the role of the private sector in establishing PPH across private health facilities and the need for political goodwill to support the implementation of PPH in Nigeria. In conclusion, PPH can help improve disease prevention strategies, treatment, and control efforts if appropriately implemented, and the study recommends a need for African studies to aggregate, analyze, visualize, and make available high quality for PPH to be more effective than traditional public health.
Article
Full-text available
Boswellia dalzielii Hutch., an African frankincense tree, is a socio-economically important aromatic and medicinal tree. It is currently threatened by uncontrolled exploitation, and therefore requires action to ensure its sustainable management. This study assessed the population structure and regeneration of its natural stands across three land use types in Burkina Faso: woodlands, fallows and farmlands. Sixty, fifty and fifty 50 m × 20 m plots were established respectively in woodlands, fallows and farmlands. All the plots were surveyed for adult tree (dbh ≥ 5 cm) density, dbh, total height and health conditions. Data on regeneration density (dbh < 5 cm), source (generative, stem shoots, suckers), total height and collar diameter were also collected. The results show similar total tree heights (7.0 m-9.0 m) but significantly (p < 0.05) smaller tree dbh in woodlands (mean ± SD: 20.5 ± 0.49 cm) and fallows (29.3 ± 0.64 cm) than in farmlands (32.8 ± 0.15 cm). Adult tree density (trees/ha) was 1.3 and 2.7 times higher in woodlands (82.37 ± 6.57) than in fallows (62.00 ± 3.98) and farmlands (30.02 ± 1.63), respectively. The density of regeneration in woodlands was 28 and 6 times higher than in fallows and farmlands, respectively. The majority (> 50%) of regenerating plants were suckers and no seedling regeneration was found in farmlands. The distribution of trees in diameter classes was J-shaped in woodlands, bell-shaped in farmlands and positive asymmetric in fallows, indicating recruitment bottlenecks. We found that 80.18% of individuals encountered were unhealthy. Intensive debarking and cutting were the main threats to the species and no conservation strategy was in place in the study region. We suggest measures to reduce intensive debarking and cutting, which should contribute to better management of the species.
Article
Full-text available
The topical collection ‘Twenty years of biodiversity research and nature conservation in the Socotra Archipelago’, in short ‘Socotra biodiversity research and nature conservation’ was conceived at the 18th Friends of Socotra annual meeting and Socotra conference which took place at the Orto Botanico di Palermo, Palermo, Italy, 26–29 September, 2019. In total, 13 research papers are included in the collection, which covers a selection of the latest scientific progress on the fauna and flora of the terrestrial and aquatic environments of the Socotra Archipelago UNESCO World Heritage Site (Yemen). Topics include conservation, taxonomy, ecology, biology and biogeography. The focus is mainly on biodiversity conservation and aimed at identifying current challenges, trends and processes that may impact on local ecosystems and livelihoods, based on analysis of data collected over the last decades. With this collection, we wish to emphasise the importance of taking into account science-based conservation approaches in future strategic steps towards safeguarding the ecosystems of Socotra.
Article
Full-text available
This study sought to determine the possible causes of the low seed quality of I. paraguariensis A. St. Hil. Seeds from six samples collected at different sites were classified as empty, decayed, herbivorous and full. Viability was assessed by tetrazolium test in seeds filled with a visualized embryo. High amounts of empty and deteriorated seeds (54% to 93%) were verified in four of the evaluated samples, and insect attack was observed in two samples. The viability of visualized embryo-filled seeds was 83% to 100%. Low quality generally results from the presence of empty and deteriorated seeds, as well as dormancy.
Article
Full-text available
The harvest of plant parts and exudates from wild populations contributes to the income, food security and livelihoods of many millions of people worldwide. Frankincense, an aromatic resin sourced from natural populations of Boswellia trees and shrubs, has been cherished by world societies for centuries. Boswellia populations are threatened by over-exploitation and ecosystem degradation, jeopardizing future resin production. Here, we reveal evidence of population collapse of B. papyrifera—now the main source of frankincense—throughout its geographic range. Using inventories of 23 populations consisting of 21,786 trees, growth-ring data from 202 trees and demographic models on the basis of 7,246 trees, we find that over 75% of studied populations lack small trees, natural regeneration has been absent for decades, and projected frankincense production will be halved in 20 yr. These changes are caused by increased human population pressure on Boswellia woodlands through cattle grazing, frequent burns and reckless tapping. A literature review showed that other Boswellia species experience similar threats. Populations can be restored by establishing cattle exclosures and fire-breaks, and by planting trees and tapping trees more carefully. Concerted conservation and restoration efforts are urgently needed to secure the long-term availability of this iconic product.
Article
Full-text available
Unsustainable overgrazing is one of the most important threats to the endemic and endangered population of dragon's blood tree (Dracaena cinnabari) on Socotra Island (Republic of Yemen). However, there is a lack of information about the exact population size and its conservation status. We estimated the population size of D. cinnabari using remote sensing data. The age structure was inferred using a relationship between crown projection area and the number of branch sections. The conservation importance of each sub-population was assessed using a specially developed index. Finally, the future population development (extinction time) was predicted using population matrices. The total population size estimated consists of 80,134 individuals with sub-populations varying from 14 to 32,196 individuals, with an extinction time ranging from 31 to 564 years. Community forestry controlled by a local certification system is suggested as a sustainable land management approach providing traditional and new benefits and enabling the reforestation of endemic tree species on Socotra Island.
Chapter
The Socotra Archipelago contains islands of high conservation importance. Since 2003, the Socotra Archipelago is a UNESCO Man and Biosphere Reserve and since 2008 it was officially listed as a UNESCO Natural World Heritage Site. In addition, the Socotra Archipelago contains currently the only Ramsar Site of Yemen (Detwah Lagoon), and it has been declared as one of 200 WWF Global Ecoregions for its unique terrestrial ecosystems (xeric shrublands), the status indicated as critical/endangered by WWF. Even the freshwater ecosystems that harbor several endemics have been given a special status, as Socotra is recognized as one of the globally outstanding Freshwater Ecoregions of the World. Socotra is also part of the Horn of Africa Biodiversity Hotspot as recognized by Conservation International, and listed as a Centre of Plant Diversity by Plantlife International, ranked among the richest yet most threatened biodiversity areas on the Planet. The Archipelago was declared as its own Ecologically or Biologically Significant Marine Area (EBSA) at the Convention of Biological Diversity (CBD) meeting in 2016, and the same year as an Endemic Bird Area by BirdLife International, which listed several Important Bird Areas (IBAs) for the Archipelago. A number of endemic plants and vertebrates from Socotra have been included in the IUCN Red List, but updates are needed and very few of the many endemic invertebrates have been listed. However, the biodiversity of Socotra is increasingly affected by impacts that affect ecosystems globally, such as unsustainable resource use and global warming which are now visible in the islands. We discuss the main threats and list some general conservation needs in the Socotra Archipelago.
Article
We assessed seven decades of change in the largest known population of the endangered endemic Boswellia elongata Balf. F. (Burseraceae) on Socotra Island (Yemen). To quantify the population change we evaluated tree number and locations on digitized images from various sources in the period 1956–2017 and combined this with direct field measurements of the population between 2011 and 2017. Our study reveals that the Homhil Nature Sanctuary B. elongata population shows a continuous decline since 1956. The steady but slow natural decline was strongly accelerated by two catastrophic cyclones in November 2015, when 38% of the trees were directly destroyed by strong winds. During the following 2 years 29% of the remaining trees died additionally. The remaining population has a bell-shaped size distribution; most trees are around 40 cm in diameter (range 18 to 70 cm). Tree ring analysis of 11 dead trees with a diameter of 29 to 44 cm without bark, resulted in estimated tree ages between 80 and 101 years. We estimate that similar-sized trees showing strong signs of senescence have a maximum age of a little over 100 years. The age structure of the Homhil population is, therefore, unbalanced with large sized trees prevailing. Natural regeneration is absent for decades. Viable seeds are available and have been shown to germinate, but the development of seedlings into saplings is a bottleneck. If the decline continues at the current rate, only 30 trees will remain there in 2036. Protection, planting and awareness activities are needed to keep this unique frankincense tree in Homhil Nature Sanctuary.
Article
The importance of populations of the Socotra dragon’s blood trees (Dracaena cinnabari Balf.f., 1882) for horizontal precipitation capture was estimated for the first time. Dragon’s blood trees (Asparagaceae) inhabit semiarid cloud forests with low levels of rainfall that strongly depend on additional moisture from fog and clouds. Our estimation was based on a detailed description of the aboveground biomass structure of stands of the dragon’s blood trees on Socotra Island. The aboveground biomass was described using non-destructive methods. An example of a well-preserved forest was measured in terms of the basic biometric characteristics of each tree, and the trees were divided into three classes based on crown projections. For each class, we took detailed measurements of one representative tree. All measured and counted growth characteristics were converted to the stand level. The tree population at the whole island level was investigated using remotely sensed data. The estimation of horizontal precipitation was performed using detailed and precise evaluation of the available climate data in half-hour intervals over the period of June 2009 and June 2010 and the ambulatory direct measurements (12.6.2009–26.6.2009). The mean annual horizontal precipitation below the crown of the dragon’s blood tree was estimated to be 792 mm in the highest (951–1545 m a.s.l.), 373 mm in the middle (601–950 m a.s.l.) and 46 mm in the lowest (180–600 m a.s.l.) altitudinal zones. Our model showed that the horizontal precipitation exceeded 40% of the total annual precipitation. The decline in the dragon’s blood tree forest could therefore cause the loss of additional water from the island’s hydrological cycle.
Article
There are seven endemic species of Boswellia Roxb. ex Colebr. on Socotra Island, Yemen. Boswellia socotrana Balf. f. is a culturally, economically, and ecologically important species on the island. The name Odina aspleniifolia Balf. f. has been considered as a synonym, but there are morphological differences between the two taxa sufficient to justify their distinction at subspecific rank. Therefore, O. aspleniifolia is transferred to Boswellia as B. socotrana subsp. aspleniifolia (Balf. f.) Lvončik. A lectotype is designated for O. aspleniifolia. The distribution and ecology of both subspecies are discussed, as is their conservation status.