Utility of island populations in reintroduction programs—
relationships between Arabian gazelles (Gazella arabica)
from the Farasan Archipelago and endangered mainland
populations
—Online Supplementary Material—
HANNES LERP, MARTIN PLATH, TORSTEN WRONSKI, EVA VERENA BÄRMANN,
ANNA MALCZYK, REVINA-ROSA RESCH, BRUNO STREIT, and MARKUS
PFENNINGER
Additional Methods
Inference of population genetic structure
As STRUCTURE results are sensitive to the violation of HWE, which was observed within our
data set, results must be interpreted with caution. To secure that our conclusions were not
affected by this, we also used the software GENETIX v4.05.2 (Belkhir et al. 2004) to calculate
a multidimensional factorial correspondence analysis (FCA). The software groups individuals
on multiple factorial axes based on shared alleles only and uses no a priori assumptions of
group membership or a particular population genetic model (Belkhir et al. 2004).
Additional Results and Discussion
Null alleles within the data set
We used the software FreeNP (Chapuis & Estoup 2007) to estimate the frequencies of null
alleles per population and locus (Table S6). We detected a relatively high rate of nonamplifying alleles within our data set (0.00-0.37). However, using Micro-checker 2.2.3 (Van
Oosterhout et al. 2004) we found no signs of large allele dropout in any group, indicating that
null alleles were probably caused by genuine low amplification success of certain alleles rather
than non-amplification of the larger allele in case of heterozygous loci.
In general, genotyping errors seem to be correlated with low DNA quality, because
errors often occurred in several loci of the same sample. Since we included only those samples
with sufficiently high DNA quality (137 of 238 samples were included in the final data set)—
i.e., those with less than 30% missing data—average error rates per locus were low (0–11%;
Table S3).
A possible reason for high null allele frequency estimates might be cross-species
amplification. Although most microsatellite markers (except RM088) were successfully
amplified in other antelope species before and all remaining loci except MCM38 were even
successfully amplified in the genus Gazella (Table S3), they were originally developed for
cattle (Bos taurus) or sheep (Ovis aries). Some alleles in Gazella might comprise mutations in
the primer regions leading to low amplification success. In case of deletions or insertions in the
flanking regions allele lengths might differ by only a single base pair, which might go
undetected due to binning with even-sized alleles, finally causing apparent heterozygote
deficiency. Indeed, after carefully re-evaluating our raw data we found some evidence for rare
alleles showing a pattern of one-base-pair length variation (especially in MCM38 and
OarFCB). However, counting those alleles separately had no effect on deviation from HWE
(i.e., heterozygote deficiency; data not shown), nor were estimates of null alleles lower (Table
S6).
As we used the ‘recessive allele option’ in STRUCTURE and accounted for null alleles
when calculating FST-values and given that the factorial correspondence analysis corroborated
the STRUCTURE results (see below), we are confident that the conclusions we have drawn
from our analyses are biologically meaningful and provide insights that will be of great use for
the conservation of G. arabica.
Genetic structure between mainland and island populations
The factorial correspondence analysis conducted with GENETIX retrieved three canonical axes
explaining 80.76% of the total variance (Fig. S3). The first axis (explaining 36.14% of the
variance) separated the majority of gazelles from Farasan Islands from mainland animals (Fig.
S3a)—corroborating the STRUCTURE analysis at K = 2 (Fig. 3c in the main text), while the
second axis separated the mainland groups South-West and North from East (Fig. S3b),
corroborating the STRUCTURE analysis at K = 7 (Fig. S2). The third axis separated the groups
South-West and North (Fig. S3c)—a result that could not be inferred with STRUCTURE.
However, these results are in line with the pattern inferred from pairwise FST-values (Table 2 in
the main text).
Genetic assignment of confiscated animals from the Akhoba Market in Jizan
Another aim of this study was to identify the origin of illegally traded gazelles. Although
strictly forbidden by international and national laws (Child & Grainger 1990) trading of
wildlife is common in the Middle East (e.g., Bachmann 2010; Stanton 2009). Gazelles are
traditionally held as pets (e.g., G. subgutturosa, Kingswood & Blank 1996; G. dorcas, Mallon
& Kingswood 2001) or bred in private collections (IUCN/SSC Antelope Specialist Group
2008). Living gazelles designated to be traded at Akhoba Market in Jizan (Saudi Arabia) were
repeatedly confiscated by customs and brought to the King Khalid Wildlife Research Centre. In
order to infer their origin and to obtain insights into the patterns of illegal gazelle trading, we
tested the confiscated specimens against the microsatellite reference data base derived from the
entire distribution range of G. arabica.
The analyses conducted with STRUCTURE and GENETIX revealed that several
gazelles confiscated at Akhoba Market originated from the Protected Area of the Farasan
Islands (Fig. 3c in the main text). Other animals clustered more distantly from Farasan and
mainland gazelles (Fig. S3). At K ≥ 4, seven individuals were assigned to a separate cluster
(i.e., estimated group membership was Q > 0.75), with no equivalent found in the sampled
mainland animals (Fig. S2). Furthermore, we found four specimens assigned to both the
separate and the Farasan cluster, suggesting admixed origin (Q = 0.3–0.5). In STRUCTURE
runs for K = 7, three individuals were assigned to a genetic cluster that occurs mainly in SouthWest Arabia (Fig. S2).
Assignment of illegally traded animals to specific mainland population was not possible
because little genetic structure was found among mainland groups (see below). Nevertheless,
some animals confiscated at the Akhoba Market could be clearly assigned to the distinct
Farasan cluster and were most likely caught on the archipelago. This implies that illegal
capture of live gazelles is existent, violating Saudi Arabian and international law (Child &
Grainger 1990). Living gazelles are regularly confiscated by rangers on Farasan Islands,
reflecting the strong demand for pet gazelles. Gazelles are chased until exhaustion using
motorcycles and then captured alive (Supplementary Video 1). Local hunters, as well as
tourists from as far away as Tabuk (northern Saudi Arabia), are said to hunt on Farasan Islands
or purchase fresh game meat (T. Wronski, pers. comm. with rangers from Saudi Wildlife
Authority). Hence, one of Saudi Arabia’s most iconic species has been lost from most of its
former range and now appears to be targeted at yet another site—the last remaining stronghold
of the species in the Kingdom.
Other confiscated animals were assigned to a genetic cluster (at K ≥ 4) that was not
represented elsewhere in our data-set. Therefore, the origin of those animals could be only
speculated upon. Since Jizan is close to the Yemen border, one likely explanation would be that
animals were caught in Yemen (Fig. 1 in the main text). The situation for gazelles in Yemen is
unclear (Mallon & Al-Safadi 2001) and included samples obtained from Yemen were collected
close to the Saudi border. Although gazelles in Yemen are thought to be rare, small populations
may still exist (Mallon & Al-Safadi 2001) and live capture in those populations is also highly
likely. Trading and catching of wildlife is very common in Yemen and appears to
opportunistically increase the income of the involved people (Stanton 2009). It is easily
conceivable that a certain variety of wildlife (including gazelles) is regularly smuggled across
the border into Saudi Arabia to achieve higher prices.
Gazella arabica on the Arabian Peninsula
No deep genetic structuring between mainland groups of gazelles could be observed and
pairwise FST-values were ≤ 0.076. We conclude that the observed fragmentation of extant
population (Mallon & Kingswood 2001) is a recent phenomenon, as isolation had only minor
effects on allele distributions. As discussed earlier, the high deviations from HWE especially
observable in the mainland groups may partly reflect the negative effects of population
fragmentation, i.e., a lack of gene flow even between adjacent populations that were pooled
into one mainland group. Besides hunting, habitat loss through agricultural development,
fencing of pasture, overgrazing by domestic livestock, and the construction of roads and
settlements increased dramatically over the past 30 years and were the main reasons for the
steep decline of Arabian gazelles on the mainland (IUCN/SSC Antelope Specialist Group
2008; Alwelaie 1989).
Results from our isolation-with-migration approach were consistent with a scenario of
recent population fragmentation, since we inferred a more than 50-fold larger number of
gazelles to have lived only a few centuries ago. However, results of historic abundance
estimates, inferred from present genetic diversity, should be treated with caution, since they
rely on a model with simplified assumptions (Palsbøll et al. 2013). Nevertheless, only a short
time span was inferred for the estimations of θ and µ, and it remains doubtless that gazelle
populations (especially on the mainland of the Arabian Peninsula) underwent a severe decline
during the past few centuries (IUCN/SSC Antelope Specialist Group 2008).
The inferred inbreeding coefficients were high, but comparable to other endangered
ungulates, e.g., Ethiopian walia ibex (Capra walie; Gebremedhin et al. 2009) or European
bison (Bison bonasus; Daleszczyk & Bunevich 2009). Deviations from Hardy-Weinberg
equilibrium were detected in all groups of mainland gazelles but were particular pronounced in
the South-West group. Here, specimens were sampled from different, isolated subpopulations
that sometimes harbor less than ten individuals (e.g., Asir Mountains; Boug et al. 2012). For
future management decisions, these signs of population fragmentation should be taken into
account to prevent further loss of genetic diversity.
In order to preserve Arabian gazelles on the mainland different approaches have been
forwarded in recent decades (Greth et al. 1996), and priority needs to be given to in situ
conservation of wild, indigenous populations and their natural habitats. In addition, several
captive populations have been established in governmental and private breeding centers in
most countries of the species’ natural range (e.g., King Khalid Wildlife Research Centre, Saudi
Arabia; Al Wabra Wildlife Preservation, Qatar; Al Ain Wildlife Park, Al Ain, UAE; Breeding
Center for Endangered Arabian Wildlife, Sharjah, UAE; Al Areen Wildlife Sanctuary,
Bahrain), and conservationist do their best to aid wild populations through several reintroduction projects. However, conservation prospects on the Arabian mainland will remain
fruitless for the next couple of decades, unless law enforcement is ensured and uncontrolled
habitat consumption is terminated (Alwelaie 1989). Should this combination of captive
breeding and in situ conservation of native populations fail to preserve remnant gazelle
populations, future management plans will have to rely on island populations like that on the
Farasan Islands to maintain intra-specific variation in Arabian gazelles.
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Supplementary Tables
Table S1 Phenotypic differences between G. arabica occurring on Farasan Island and the
mainland based on Thouless and Al-Basri (1991).
Trait
Body weight
Body length
Horn size in females
Horn size in males
Horn shape in males
Horn tip to tip
Tooth-row
Skull
Palate
Brain case
Legs
Coat colour
Leg colour
Flank strip
a
in relation to body length
Farasan Island gazelles
small
large
short, deformed or absent
not relatively shorter
straight
wide
curved
small
short and broad
narrow
relatively shorta
dark seal-grey
sandy-brown
well developed
Mainland gazelles
large
large
normally developed
not relatively larger
lyrate
narrow
straight
large
long and narrow
broad
relatively longa
dark grey-ochre – light fawn
dark grey-ochre – light fawn
often absent or weak
Table S2 List of specimens (wild, captive or confiscated) of G. arabica included in the population genetic analyses, origin, their collectors,
sample types and group the specimens were designated.
Southern Arava Valley
Al Bad’ (N 28°30’, E 35°00’)
BirMarshan (N 28°50’ E 34°51’)
HarratUwayrid (N 26°50’, E 37°45’)
Jordan
Wadi Al Safa, Dubai
between Muscat and Sur, Oman
Wadi Al Safa Wildlife Centre
Wadi Tarj (N19°28’, E42°21’)
Maqhshush (N18°38’, E41°22’)
Al Hayla (N18°17’, E41°49’)
Yemen (Amran)
National Wildlife Research Center
Tabalah (N20°05’, E42°04’)
Sharawrah
Al Wabra Wildlife Preservation
Wild/ captive/
confiscated
wild
wild
wild
wild
wild
wild
wild
captive
wild
wild
wild
wild
captive
wild
wild
captive
Farasan Islands (N16°40’, E42°09’)
wild
Akhoba Market Jizan, unknown provenance
confiscated
Origin (coord.)
a
TAUM – Tel Aviv University Natural History Collection
Collector (number of samples)
R. King, R. Hammond, D. Blank, TAUMa (8)
M. Sandouka (1)
T. Wacher (1)
K. Alageel (1)
O. Mohammed (1)
D. O’Donovan (2)
M. Al Jahdhami (5)
I. Nader, D. O’Donovan (7)
T. Wronski (6)
T. Wacher
T. Wacher (2)
P. Vercamen (1)
P. Mésochina
T. Wacher, R. Hammond (1)
T. Wacher
D. Williamson (3)
T.Wacher, O. Mohammed , M. Sandouka, H. Tatwany, S.
Ostrowski,T. Wronski (66)
S. Mubarak, S. Anajarriya (23)
Sample type
Group
tissue, DNA
tissue
tissue
tissue
tissue
tissue
tissue
tissue, hairs
tissue
feces
hairs
hairs
tissue, blood
hairs
hairs
blood, hairs
tissue, blood,
hairs
tissue, blood
North
North
North
North
North
East
East
East
South-West
South-West
South-West
South-West
South-West
South-West
South-West
South-West
Farasan
Islands
Jizan
Table S3 Microsatellite loci used in this study, original and antelope reference, used dye-label, number of multiplex reaction in which markers
were amplified and amplification error rates.
Locus
BM302
BM415
CSSM043
TEXAN19
BM4505
SR-CRSP6
MCM38
INRA40
OarFCB304
RM088
TEXAN6
Original reference
Bishop et al. 1994
Bishop et al. 1994
Moore et al. 1994
Burns et al. 1995a
Bishop et al. 1994
Bhebhe et al. 1994
Hulme et al. 1994
Vaiman et al. 1994
Buchanan & Crawford 1993
Kossarek et al. 1995
Burns et al. 1995b
Antelope reference
Gazella dorcas (Beja-Pereira et al. 2004)
G. dorcas (Beja-Pereira et al. 2004)
G. cuvieri, G. dorcas (Ruiz-Lópes et al. 2009)
G. spekei (Engel et al. 1996)
G. dorcas (Beja-Pereira et al. 2004)
G. dorcas (Beja-Pereira et al. 2004)
Aepyceros melampus (Lorenzen & Siegismund 2004)
G. dorcas (Beja-Pereira et al., 2004)
G. cuvieri, G. dorcas (Ruiz-Lópes et al. 2009)
this study
G. spekei (Engel et al. 1996)
Label
CY5
DY-751
CY5
IRD700
IRD700
IRD700
CY5
DY-751
CY5
CY5
IRD700
Multiplex No.
1
1
1
1
2
2
2
2
3
3
3
Amplification Error Rate [%]
2.91
1.02
8.82
3.77
6.45
4.04
11.32
0.00
7.00
9.52
8.65
Table S4 Estimated null allele frequencies for the 11 microsatellite loci inferred from the STRUCTURE analyses for different numbers of
genetically distinct clusters (K). Cluster 1 always correspond to the cluster exclusively present on the Farasan Archipelago
Locus
BM302
BM415
CSSM043
TEXAN19
BM4505
SR-CRSP6
MCM38
INRA40
OarFCB304
RM088
TEXAN6
Clusters
K=2
1
2
0.143 0.212
0.029 0.115
0.128 0.273
0.018 0.079
0.174 0.145
0.011 0.117
0.037 0.109
0.099 0.155
0.030 0.119
0.042 0.140
0.053 0.128
K=3
1
0.148
0.025
0.125
0.020
0.167
0.011
0.022
0.105
0.026
0.037
0.052
2
0.213
0.120
0.261
0.101
0.147
0.120
0.122
0.164
0.121
0.106
0.146
3
0.095
0.057
0.293
0.011
0.041
0.033
0.015
0.039
0.026
0.100
0.017
K=4
1
0.148
0.024
0.127
0.017
0.164
0.012
0.017
0.101
0.021
0.032
0.051
2
0.221
0.124
0.244
0.078
0.130
0.139
0.102
0.123
0.092
0.096
0.128
3
0.182
0.094
0.292
0.115
0.170
0.062
0.134
0.226
0.158
0.123
0.151
4
0.087
0.038
0.198
0.007
0.032
0.034
0.010
0.019
0.014
0.051
0.012
K=5
1
0.140
0.020
0.119
0.016
0.158
0.008
0.010
0.103
0.020
0.033
0.054
2
0.197
0.099
0.187
0.044
0.121
0.162
0.056
0.095
0.076
0.074
0.102
3
0.156
0.082
0.280
0.108
0.117
0.045
0.072
0.218
0.134
0.136
0.094
4
0.222
0.155
0.301
0.067
0.211
0.123
0.149
0.109
0.099
0.070
0.176
5
0.081
0.025
0.124
0.007
0.030
0.023
0.008
0.017
0.012
0.040
0.013
Table S5 Axis loadings for the first five principle components (eigenvalue > 1) in the
principle component analysis on skull morphometry. Abbreviations are as in Fig. S1.
Variable
WP
LL
OD
WB
DSF
LF
LP
L F+P1
L F+P2
DH
HD1
HD2
HBD
LTR
LPR
HL1
LN
WM
WBA
WBP
WC
WPP
OHB
OHO
DOC
BW
BL
IB
HTD
MWH
IPD
ZW
WAO
Component 1
0.725
0.919
0.766
0.871
0.814
0.841
0.594
0.910
0.885
-0.436
0.916
0.903
0.195
0.767
0.761
0.855
0.662
0.580
0.766
0.884
0.311
0.925
0.824
0.933
0.893
0.682
0.840
0.642
0.583
0.853
0.602
0.901
0.922
Component 2
0.022
0.185
0.184
0.299
0.291
0.052
0.210
0.081
0.069
0.810
-0.204
-0.322
0.780
0.133
0.013
-0.277
0.184
-0.026
-0.181
0.181
0.342
0.205
-0.332
-0.078
-0.096
-0.065
0.210
-0.322
-0.364
-0.245
-0.042
0.087
0.137
Component 3
0.358
-0.062
0.070
0.006
0.007
-0.214
-0.004
-0.138
-0.166
0.021
-0.136
-0.136
-0.378
-0.211
-0.246
-0.189
0.326
0.468
-0.096
0.191
0.075
0.057
-0.165
0.010
0.117
-0.319
-0.009
0.361
-0.066
-0.269
0.423
0.166
0.271
Component 4
-0.130
-0.020
0.170
-0.167
-0.205
0.013
-0.211
-0.099
-0.061
0.059
0.077
0.068
-0.210
0.051
0.230
0.112
-0.050
-0.079
-0.387
-0.049
0.688
-0.018
0.019
-0.047
-0.073
0.370
0.101
-0.200
0.080
-0.074
0.503
0.068
-0.068
Component 5
-0.327
-0.058
-0.263
0.127
0.177
0.235
0.475
0.206
0.262
-0.025
0.062
0.039
-0.054
-0.352
0.009
0.043
-0.433
0.282
-0.185
-0.074
0.159
-0.047
-0.203
-0.063
-0.138
-0.152
-0.058
0.151
-0.013
0.133
0.219
-0.130
0.088
Table S6 Estimate of null allele frequencies of the original data (Nulli) and including alleles with single base pair mutations (Nullm) a using the
EM algorithm (Dempster et al. 1977) using the software FreeNA (Chapuis & Estoup 2007) and percentage of missing data per population and
locus.
Locus
BM302
BM415
CSSM043
TEXAN19
BM4505
SR-CRSP6
MCM38
INRA40
OarFCB304
RM088
TEXAN6
Nulli
0.21
0.00
0.05
0.06
0.19
0.11
0.30
0.07
0.16
0.25
0.12
North (N = 12)
% missing
Nullm
data
0.21
0.0
0.00
0.0
0.07
16.7
0.06
0.0
0.19
25.0
0.11
8.3
0.30
0.0
0.14
25.0
0.16
8.3
0.25
0.0
0.12
0.0
Nulli
0.00
0.03
0.22
0.00
0.06
0.06
0.00
0.16
0.15
0.00
0.19
Nullm
0.00
0.03
0.22
0.00
0.06
0.06
0.00
0.16
0.15
0.00
0.19
East (N = 14)
% missing
data
0.0
7.1
0.0
0.0
0.0
7.1
0.0
42.9
0.0
0.0
0.0
Nulli
0.27
0.17
0.37
0.14
0.22
0.14
0.08
0.19
0.11
0.11
0.09
South-West (N = 22)
% missing
Nullm
data
0.27
0.0
0.17
9.1
0.37
4.5
0.14
0.0
0.22
9.1
0.11
18.2
0.10
9.0
0.19
22.7
0.12
4.5
0.11
0.0
0.09
4.5
Farasan Islands (N = 66)
% missing
Nulli Nullm
data
0.21
0.21
9.1
0.12
0.12
10.6
0.23
0.23
3.0
0.11
0.11
1.5
0.19
0.19
16.7
0.04
0.04
3.0
0.18
0.21
3.0
0.10
0.10
24.2
0.07
0.07
4.5
0.05
0.05
1.5
0.14
0.14
0.0
Akhoba Market Jizan (N = 23)
% missing
Nulli
Nullm
data
0.00
0.00
0.0
0.01
0.01
0.0
0.20
0.20
8.7
0.00
0.00
0.0
0.06
0.06
0.0
0.04
0.04
0.0
0.00
0.00
0.0
0.07
0.07
8.7
0.04
0.05
0.0
0.19
0.19
0.0
0.00
0.00
0.0
Supplementary Figures
Figure S1 Skulls measurements taken for morphological analyses. Figure modified
from Bärmann et al. (2013).
Figure S2 Percentage population assignments to inferred genetic clusters with K
ranging from 3 to 7. Animals were sorted by Q values of the genetic cluster endemic
to the Farasan Islands (red) for each population separately.
Figure S3 Factor correspondence analysis of allele frequencies. The first three axes
are shown explaining 80.8% of variance within the data set. Symbols are equivalent to
Fig. 1. (A) First two axes explaining 61.1% of the total variance; (B) first and third
axes (55.8%), and (C) second and third axes (44.6%).