Trees

https://doi.org/10.1007/s00468-022-02367-0

ORIGINAL ARTICLE

Assessing argan tree (Argania spinosa (L.) skeels) ex‑situ collections

as a complementary tool to in‑situ conservation and crop introduction
in the Mediterranean basin
Yalbeiry Labarca‑Rojas1,3 · J. Esteban Hernández‑Bermejo1,2,3 · Francisca Herrera‑Molina1,2,3 ·
Marta Hernández‑Clemente1 · José L. Quero1

Received: 2 February 2022 / Accepted: 10 November 2022

© The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2022

Key message The argan ex-situ collections help its crop breeding and conservation in the Mediterranean basin,
specifically in the southern Iberian Peninsula, where climatic refuges and new cultivation areas could be established.
Abstract A. spinosa (L.) Skeels, hereafter argan, is a tree species naturally distributed in Morocco and Algeria, introduced
mainly for productive purposes in countries, such as Tunisia, Israel, and Spain. This promising species has a more extensive
potential cultivation and use due to its economic prospects in human food and cosmetics. These reasons and its great aridity
adaptation have raised the strategic value of argan and its ex-situ collections, compared to other more sensitive to climate
change crops. From this perspective, this study aims to evaluate the genetic diversity of an ex-situ, 10-year-old collection on
more than 600 specimens raised in southern Iberian Peninsula, and to promote its cultivation in the most suitable regions
for its introduction throughout the Mediterranean basin. To this end, the genetic and morphological diversity of a subset of
selected specimens was compared, and six MaxENT models were trained using 96 occurrence points in both wild and cul-
tivated localities (ex-situ collections), together with six bioclimatic variables in a current timeframe and under two climate
change scenarios (optimist and pessimist). Surprisingly, this Iberian collection’s genetic diversity was highly representative of
the wild population’s diversity in their natural range. Given this representativeness, these cultivars could be a complementary
conservation tool as well as a starting point for domestication, breeding, and cultivation programs in a wide environmental
range in these territories. The natural distribution of argan will be considerably reduced and shift towards northern habitats
by 2050 and 2080, where climatic refuges and new cultivation areas could be established.

Keywords Argan tree · Argania spinosa · Climate change · Ex-situ conservation · Genetic diversity · Suitability models

Introduction UNESCO and protected by Moroccan legislation. Even, the

United Nations proclaimed May 10 as International Argan
The argan tree is a species native to south-western Morocco Tree Day (Charrouf and Guillaume 2009; Sinsin et al. 2020).
and western Algeria. It is the main component of the Argan- Therefore, their management, which is particularly commit-
eraie, a forest formation declared a Biosphere Reserve by ted to their conservation, must adopt an ecosystemic per-
spective in these territories, compatible with their use as
an ancestral natural resource. However, beyond its natural
Communicated by J. Carlson.
range, the species has also been introduced over the centu-
* Yalbeiry Labarca‑Rojas ries, in countries such as Tunisia, Israel, Iran, Libya, Mau-
[email protected] ritania, and Spain (Louhaichi et al. 2011; Louati et al. 2019;
1 Martínez-Gómez et al. 2018, 2020; Mezghenni et al. 2014;
Forestry Engineering Department, School of Agricultural
and Forestry Engineering (ETSIAM), University of Cordoba, Nerd et al. 1994), and more recently in others, such as Aus-
Rabanales University Campus, Cordoba, Spain tralia, the United States, Kuwait, and Mexico (Habibah et al.
2
Andalusian Plant Germplasm Bank (BGVA), Junta de 2007; Nouaim and Chaussod 1993), generally seeking to
Andalucía, avda. Linneo s/n, Cordoba, Spain cultivate and exploit it. The situation is different in each of
3
Red CultIVA–CYTED (www.cyted.org/es/cultiva), Cordoba, these countries. This introduction, almost always carried out
Spain for productive purposes, has been able to generate processes

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of selection and genetic breeding, so that these germplasm Yatrib et al. 2015, 2017). Most of these studies were mainly
collections could represent an alternative for ex-situ con- aimed at assessing the amount and partitioning of genetic
servation, especially in the case of old introductions and diversity among natural argan populations to understand to
specimens kept in botanical gardens and arboreta. what extent genetic patterns are linked to geographic dis-
This species, adapted to different habitats (littoral, sub- tributions and to establish what measures should be taken
littoral, mountainous, and desert), inhabits a wide variety in the future for the conservation of this important species
of vegetal formations and landscapes together with other based on its genetic structure. Mouhaddab et al. (2015, 2016,
species, depending upon locality and ecological conditions, 2017) have even identified core collections to preserve the
such as Quercus ilex subsp. rotundifolia, Pistacia lentiscus, total genetic diversity.
Olea marocanna, Ziziphus lotus, Periploca laevigata, Tetra- The remarkable genetic and phenotypic diversity
clinis articulata, Juniperus phoenicea, Whitania frutescens, observed in Argania spinosa has generally been related to
Genista tricuspidata, Globularia alypum, Rhus tripartita, the diversity of habitats in which it occurs (Charco 1999;
G. ifniense, Ziziphus lotus, Lavandula dentata, Ephedra Díaz-Barradas et al. 2010; Msanda et al. 2005, 2021; Quézel
nebrodensis, or even Buxus balearica (Barbero et al. 1981; et al. 1994). This polymorphism could explain to a large
Msanda et al. 2005). It is also altitude-independent, as it extent why the species is able to occur in a relatively wide
occupies from the coastal areas up to 1800 m where pen- range of habitats, sometimes taking advantage of Atlan-
etrates the valleys forming oueds (wadis) that rise from the tic advection fogs in the coastal regions of SW Morocco
High Atlas and the Anti-Atlas Mountains. (Labarca-Rojas et al. 2022) and sometimes occupying the
A very singular case of the presence and persistence bottoms of drainage rills, reaching higher altitude moun-
of these ancient crops in the territories occupied by Al- tain environments with higher precipitation, relieved by
Andalus, an ancient region comprising the southern and orographic fogs on the southern slopes of the western High
eastern two-thirds of the Iberian Peninsula and over which Atlas and the northern slopes of the Anti-Atlas, or even liv-
Muslim domination extended for centuries, is sufficiently ing close to the Mediterranean in Beni-Snassen mountains in
documented (Carabaza Bravo et al. 2004; García Sánchez the Eastern Rif. These different ecosystems show a floristic
et al. 2021). Specifically, texts from the Middle Ages on composition of relative diversity, loaded with endemisms,
agronomy, botany, and pharmacognosy suggest its cultiva- made up of Mediterranean floristic components (with Olea
tion and oil production [Ibn Ŷulŷul (10th c.), Abū l-Jayr: europea, Pistacia atlantica, P. lentiscus, Buxus balearica,
(12th c.), and Ibn al-Bayṭār (13th c.) in García Sánchez et al. Quercus ilex, Tetraclinis articulata, or Juniperus commu-
2021]. Even in these days, 800 years later, there are still nis), Macaronesian (Kleinia, Aeonium, Euphorbia and Asty-
scattered trees in some localities in the provinces of Murcia damia species, even Dracaena ajgal, and some fern such
and Alicante and some cultivated trees in different gardens as Davallia canariensis), or Afrotropical (Acacia spp.).
(Crespo et al. 2007; Martínez-Gómez et al. 2019; Rivera All these communities are considered by phytosociology
Núñez et al. 1997). school (Barbéro et al. 1981; Quézel et al. 1994) as Mediter-
From an agronomical point of view, argan has high eco- ranean and sclerophyllous plant communities, included in
nomic prospects due to its applications in the cosmetic and the order Acacio-Arganietalia. In them, the argan tree is in
human food industries. If we add this to its great aridity direct competition with a few tree species (such as Tetra-
adaptation, we are faced with a complementary or alter- clinis articulata, Acacia gummifera, Pistacia atlantica, P.
native crop for warm and low-rainfall areas, where other lentiscus, Ceratonia siliqua—probably an archaeophyte—or
woody crops, such as olive, pistachio, and almond trees, even Buxus balearica or Quercus ilex at the limits of its eco-
may already be in decline because of the progressive climate logical range). It may also compete with some thorny shrubs
change in circum-Mediterranean, North African, and Mid- with intricate branching, with oleoid-to-microbuxoid leaves
dle East countries. However, the techniques of domestica- (the same range of variation as the argan tree), such as Olea
tion, propagation, and cultivation of argan have not yet been europea, Ziziphus lotus, Lycium sp., and Genista spp. Peri-
effectively resolved, and the area of exploitation is almost ploca angustifolia). However, it probably does not compete
exclusively limited to its natural range. with other physiognomically very different species, such as
On the other hand, in-situ conservation measures may crassulents of Macaronesian, nor with the Mediterranean
be insufficient to reverse the regression of argan natural small shrubs of Teucrium, Sideritis, Thymus, Lavandula, or
communities (Sinsin et al. 2020). The genetic diversity Globularia.
in these habitats has been extensively studied for decades In this ecosystem framework, the argan tree has “open”
with different molecular techniques (Ait Aabd et al. 2015; ecological niches in which it can compete, undergoing
Bani-Aameur and Benlahbil 2004; El Bahloul et al. 2014; El favorable physiognomies with respect to some of its com-
Mousadik and Petit 1996; Louati et al. 2019; Majourhat et al. petitors. For this reason, Argan probably has very different
2008; Mouhaddab et al. 2015, 2016, 2017; Msanda 1993; growth habit and branching forms, very different levels of

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spinescence, polymorphic leaves (from oleoid to microbux- (1) to evaluate the molecular and morphological diversity
oid), fruit types and production, phenology, and pollination of existing ex-situ argan collections in the S of the Iberian
systems (ambophily). In this scenario, we must also con- Peninsula in comparison with that already evaluated in their
sider, as a complementary justification for its polymorphism, natural distribution; (2) to draw the most successful areas
the hypothesis that argan has developed an “i” strategy for argan cultivation in the Mediterranean basin (and nearby
(diversity cenotic strategy described by Blandin et al. 1976), archipelagos) using probabilistic models; (3) to identify the
as well as other species in Mediterranean ecosystems, as a most effective areas for future argan cultivation, in the same
form of adaptation of the late Tertiary flora to Quaternary Mediterranean geography and under two foreseeable sce-
mediterraneanization. This strategy promotes infraspecific narios of climate change (2050 and 2080).
variability, compensating the “s” diversity deficit (strategy
of occupying ecological niches with species of different
taxonomic nature). Materials and methods
Whatever the reason for the outstanding polymorphism
of this species, it is clear that any attempt at cultivation or Natural range of argan
reintroduction in other regions should play on a sufficiently
representative genetic diversity. The identification of locali- Argan naturally occurs in Mediterranean Africa, extending
ties and small ex-situ collections of argan, especially if they over 1,076,000 ha (Lefhaili and Amhajar 2020) in south-
comprise enough genetic diversity, makes feasible to create western Morocco and 96 940 ha in south-western Algeria
suitability models that may expand its potential distribution (Tindouf) (Benaouf et al. 2015; Kechebar et al. 2013). In this
for cultivation. These ex-situ collections may facilitate argan work, we have therefore studied argan’s natural distribution
domestication and cultivation and be an alternative way of extended to the rest of the Mediterranean Basin, between
conservation facing the future risks that wild populations 15° N and 50° N latitude and 20° W and 50° E longitude as
may have. study area. We selected this study area, considering how cli-
Taking into account the above considerations, the main mate change trends affect this area and that the argan forma-
objective of this study was directed towards the evaluation tions are ecologically Mediterranean (infra-Mediterranean
of ex-situ collections as a complementary tool to in-situ bioclimatic ground, in Acacio-Arganetalia formations of
conservation and to search for possible climatic refugia, Quercetea ilicis for sigmatist phytosociology).
developing for this purpose three more specific objectives:

Table 1  Ex-situ localities (experimental crops and ancient trees) of Argania spinosa in the Mediterranean basin
Status Country Locality Plantation year Latitude (º) Longitude (º) References

Experimental crops Algeria Adrar-ville 2003 27.88 − 0.28 Benaouf et al. (2015), Kechairi and Ben-
Experimental crops Algeria Bechar 2003 31.63 − 2.22 mahioul (2019)
Experimental crops Algeria Timimoun 2003 29.25 0.24
Experimental crops Algeria Tindouf-ville 2003 27.67 − 8.11
Experimental crops Israel Ktura and Ramat 1994 29.97 35.07 Nerd et al. (1994)
Experimental crops Tunisia Gabés Early sixties 33.51 10.15 Hanana et al. (2018), Louati et al. (2019)
Experimental crops Tunisia Nabeul 35.82 10.57
Experimental crops Tunisia Sfax 35.07 10.18
Experimental crops Tunisia Tunis 36.84 10.19
Experimental crops Spain Aguilar de la Frontera 2013 37.48 − 4.73
Experimental crops Spain Santomera No data 38.11 − 1.04 López González (2001), Martínez-Gómez
Ancient trees Spain Agaete – 28.10 − 15.70 et al. (2018, 2020), Ruiz de la Torre
(2006)
Ancient trees Spain Alicante – 38.39 − 0.46
Ancient trees Spain Alicante – 38.37 − 0.50
Ancient trees Spain Alicante – 38.36 − 0.51
Ancient trees Spain Jijona – 38.49 − 0.48
Ancient trees Spain Molina de Segura – 38.06 -1.17
Ancient trees Spain Orihuela – 37.90 − 0.76
Ancient trees Spain Tenerife – 28.15 − 16.52

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or old specimens of argan trees are preserved, and they are

also made up of a very small number of individuals. There-
fore, a stratified sampling design was carried out to ensure
the presence of the different physiognomic and morphologi-
cal characters observed in this single locality of Aguilar de
la Frontera with around 600 specimens. A total of 210 speci-
mens located along the transects defined in the field were
carefully examined. Ten descriptors were defined to explain
the phenotypic variability present (D: level of development;
F: physiognomy shoot angle; R: branching; Fx: phyllotaxis;
FH: leaf shape; CH: leaf color; NF: fruit quantity; CF: fruit
color; MF: fruit maturity; FF: fruit shape). Therefore, 10% of
the specimens examined (n = 21) were chosen as representa-
tive of the different combinations of characters found. The
rule of 20 individuals per locality was maintained.

Morphological diversity

Morphological diversity has been studied by different

authors who have evaluated the germplasm of this species
from an agronomic perspective and identified different mor-
photypes for both the fruit and the morphologic aspect of the
tree. In this study, we selected six morphological and four
Fig. 1  Landscape view of the experimental crop collection with about
600 trees located in the municipality of Aguilar de la Frontera (Anda- fruit characters (Fig. 2).
lusia, Spain) A cluster analysis was performed to obtain a first approxi-
mation of differentiable morphotypes in the germplasm col-
lection under cultivation chosen in this study. This method
Experimental crop collections: a case study in south clustered the individuals according to their similarity in
Spain terms of the different types of modalities within the ten
selected qualitative categories. The result of the clustering
Beyond its natural area, there are localities around the Medi- is shown in the dendrogram obtained by applying the Jac-
terranean basin where argan cultivation has been tested for card similarity index. The multiple correspondence analysis
productive and reforestation purposes. Such are the cases (MCA) function of the FactoMineR package (Kassambara
of some cities in Algeria, Tunisia, Israel, and Spain where 2017) was used to recognize the traits associated with each
argan is located in small experimental cultivations, com- group and individual.
mercial nurseries, botanical gardens, and scattered old speci-
mens (Table 1). There are other documented records of indi- Molecular diversity
viduals introduced in Libya (Hammer et al. 1988; Louhaichi
et al. 2011). The genetic diversity of these ex-situ localities Simple Sequence Repeat (SSR or microsatellite) markers
has not yet been evaluated, except for a minor experimental are ideal for genetic studies of population structure (Day-
crop in Spain (Bnikkou et al. 2021). Therefore, in this work, anandan et al. 1998). Due to their co-dominance and high
we have attempted to assess diversity for what may be the reproducibility, these markers are far enhanced to the com-
argan collection with the largest number of specimens in monly used Random Amplified Polymorphic DNA (RAPD),
Spain, located in the municipality of Aguilar de la Frontera Inter-Simple Sequence Repeats (ISSR), and Amplified Frag-
(Andalusia, Spain) with about 600 trees under cultivation, ment Length Polymorphism (AFLP) (Pakhrou et al. 2016).
planted by seeds in 2013 and transplanted in 2015 (Fig. 1). SSR markers previously used by El Bahloul et al. (2014),
Sample size’s selection was based on the criteria used Majourhat et al. (2008), Mouhaddab et al. (2017), and Yatrib
in the consulted genetic diversity studies (El Bahloul et al. et al. (2017) were used to assess the genetic diversity of this
2014; Majourhat et al. 2008; Mouhaddab et al. 2017; Yatrib argan crop collection in south Spain. Additionally, we tried
et al. 2017), around 20 individuals per locality. In these to correlate some morphological characters and the molecu-
cases, the aim was to compare natural populations consisting lar identity of the individuals, based on its high polymor-
of hundreds or thousands of individuals. However, there are phism. This correlation would provide a tool for predicting
not so many localities in the Iberian Peninsula where adults

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Fig. 2  Flowchart summarizing the methodology used in this study. 1Multiple correspondence analysis. 2Simple sequence repeats

the performance (e.g., productivity) in the crop of the dif- 2–2.5 µl of amplified product mixed with 6 µl of formamide
ferent cultivated specimens. and 0.15 µl of ROX 400 size standard and denatured 2 min
Accordingly, a pre-selection was made of the 15 prim- at 95 °C were loaded.
ers with the highest polymorphism information content The genetic diversity was estimated by the number of
(PIC), which had shown good discrimination of loci, and alleles (Na) per locus SSRs and farther genetic informa-
heterozygosity when analyzing diversity between individuals tion of the codominant SSR markers was determined by the
and populations of argan (ASMS01, ASMS20, ASMS2012- effective number of alleles (Ne), observed heterozygosity
04, ASMS2012-34, ASMS2012-37, MH07, MH04, MH06, (Ho), and expected heterozygosity (He) (Kloosterman et al.
ME11, MH20, MH08, ME05, MH12, MH17, and MH22), 1993) calculated applying the GenAlEx package (Peakall
of which six showed amplification capacity in the 21 argan and Smouse 2012).
samples studied.
DNA was extracted from 20 mg of leaf sample previ- Suitability models and climate change scenarios
ously sprayed with liquid nitrogen, using the QIAGEN Mini
Kit plant Dneasy. Quantification was done by absorbance The five bioclimatic variables that better explain the cur-
spectrophotometry at a wavelength of 260 nm using a Nan- rent argan distribution area according to Labarca-Rojas et al.
oDrop-Lite spectrophotometer, for which a 1/10 dilution of (2022) were obtained from the WorldClim data portal (Fick
the extracted DNA samples dissolved in 200 µl of TE had and Hijmans 2017). It contains information about Mean
to be performed. Diurnal Range Temperature (Tmdr), Min Temperature of
The PCR program consisted of an initial step of 6 min at Coldest Month (Tncm), Temperature Annual Range (Tmar),
94ºC followed by 35 cycles of 30 s at 94 °C, 30 s at 55 °C for and Precipitation of Driest Month and Quarter (Pmdm,
PCR I, and 57 °C for PCR II, and 30 s at 72 °C, and a final Pmdq), and Elevation from 1960 to 1990. In addition, the
extension step of 20 min at 72 °C. PCRs were performed global gridded of pH soil information at 0–5 cm depth was
at the Central Service for Research Support (SCAI) of the included to the dataset (Hengl et al. 2017). All of them with
University of Cordoba with the Biometra T3 Thermocycler a spatial resolution of 30 s (~ 1 ­km2).
and the HorsePower-Taq DNA Polymerase Kit (Canvax). To test whether the introduction of ex-situ localities wid-
Genetic analysis was performed by capillary electropho- ens the range of argan distribution, two current suitability
resis with Genetic Analyzer ABI3130 XL (Applied Biosys- models were estimated: the first one using only in-situ locali-
tems) and GeneMapper v 4.0 analysis software; for which ties and the other combining in-situ and ex-situ localities

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Table 2  Characterization of 6 Locus Bp Na Ne He Ho X2

SSR loci with 18 individuals of
A. spinosa ASMS01 141–175 14 10.62 0.91 1.00 NS
ASMS20 202–220 9 3.16 0.68 0.67 NS
ASMS2012-04 303–315 4 2.41 0.59 0.50 NS
ASMS2012-34 197–247 12 8.42 0.88 0.83 NS
MH22 191–209 6 5.49 0.82 0.44 *
ASMS2012-37 191–219 10 7.28 0.86 0.78 NS
Total – 55 – – –
Mean – 9.17 6.23 0.79 0.70
SE – 1.52 1.29 0.05 0.09

Bp allele size range, Na number of alleles, Ne effective number of alleles, He expected heterozygosity, Ho
observed heterozygosity, X2 Chi-square tests for Hardy−Weinberg equilibrium, NS no significant differ-
ence. *Significant (P < 0.05) between He and Ho according to X2 test.

(Fig. 2). These combined localities were used to calculate Given the diversity of ecosystems in which the argan is
the future geographical distribution based on the Hadley found, all sites considered natural have been used (see sup-
Centre Global Environment Model (v. 2). Four models porting data). On the other hand, to reinforce the suitability
were obtained in two different periods 2050 (mean values models, sites from other countries, such as Algeria, Tunisia,
from 2041 to 2060) and 2080 (the mean values from 2061 to Israel, and Spain, in which the species has been successfully
2080) applying two scenarios of the Intergovernmental Panel introduced outside its natural range have been added. These
on Climate Change (IPCC): Representative Concentration ex-situ localities with known coordinates are summarized
Pathway (RCP) 4.5 and 8.5 (Fig. 2). The four scenarios were in Table 1.
predicted using the MaxEnt algorithm that represents the In total, 87 occurrence points from both in-situ and ex-situ
distribution of the species by the probability function P over localities were used to train the models. The obtained output
a set X of locations in the studied area. predicts the suitability of the argan fulfilling all the asso-
ciated bioclimatic limits and maintaining the distribution

Table 3  Morphological categories used to group 21 argan specimens from an experimental crop collection in Andalusia (Spain)
ID D F R Fx FH CH NF CF MF FF

1 High Upright-patent Medium Fasciculate Buxoid Green Abundant Yellow Medium Piriform
2 High Upright-patent High Fasciculate Oleoid Light green Scarce Yellow Full Piriform
3 High Upright-patent Medium Fasciculate Buxoid Green Abundant Yellow Full Apiculate
4 Medium Decumbent Low Fasciculate Oleoid Green Scarce Yellow–red Full Rounded
5 High Upright-patent Medium Fasciculate Oleoid Green Abundant Yellow Medium Fusiform
6 High Upright-patent High Fasciculate Buxoid Green Abundant Yellow Full Rounded
7 High Decumbent Medium Solitary Myrtoid Green Scarce Yellow Full Apiculate
8 Medium Decumbent Medium Fasciculate Buxoid Green Scarce Brown Full Apiculate
9 Medium Decumbent High Fasciculate Oleoid Green Abundant Yellow Full Apiculate
10 Medium Patent Medium Fasciculate Oleoid Green Abundant Yellow–red Full Apiculate
11 Low Decumbent Medium Solitary MicroBuxoid Dark green – – – –
12 Medium Patent Medium Fasciculate Oleoid Green Abundant Yellow Full Oval
13 Medium Patent Medium Fasciculate Oleoid Green Scarce Yellow Low Fusiform
14 High Decumbent High Fasciculate MicroBuxoid Dark green – – – –
15 High Decumbent High Fasciculate Buxoid Green Abundant Yellow Low Fusiform
16 Medium Decumbent Medium Solitary MicroBuxoid Green – – – –
17 High Patent High Fasciculate Oleoid Light green – – – –
18 High Patent High Solitary Buxoid Green Scarce Yellow Full Oval
19 Medium Decumbent Medium Solitary Buxoid Dark green Scarce Yellow Full Apiculate
20 Low Patent Medium Solitary Rounded Dark green – – – –
21 Medium Patent Medium Fasciculate Oleoid Green Scarce Amarillo Full Piriform

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to its maximum entropy. The lowest suitability areas are

symbolized by 0, while 1 symbolizes areas with maximum
suitability (Pratumchart et al. 2019; Sharma et al. 2018).
The ROC curve (receiver of characteristics) graphically rep-
resents the discriminative capacity of the model from all
possible cut-off points and how adjusted this distribution is
expressed by the value of the area under the curve (AUC)
(poor 0.75 < AUC > 0.95 excellent) (Kogo et al. 2019).

Results

Molecular diversity

These results reveal the genetic diversity of 18 individuals

out of 21. Three individuals, 9, 15, and 20, did not amplify
with any of the primers used. A total of 55 alleles were
detected among 18 A. spinosa trees (Table 2). The num-
ber of alleles per locus (Na) varied from 4 (ASMS2012-
04) to 14 (ASMS01), with an average of 9.17. While, the
effective number of alleles per locus (Ne) ranges from 2.41
(ASMS2012-04) to 10.623 (ASMS01).
No significant differences were observed between Ho
and He for five loci, indicating that the sample is close to
Hardy–Weinberg equilibrium. Nevertheless, locus MH22
shows a He higher than Ho, indicating a slight lack of hete-
rozygosity. This might be due to the presence of null alleles.

Morphological diversity Fig. 3  Dendrogram of qualitative characteristics among 21 collected

trees of A. spinosa based on Jaccard similarity coefficient and ward
method
Table 3 shows the results of the characteristics taken for each
individual studied in the experimental farm.
D level of development, F physiognomy shoot angle, R group includes individuals with low branching, few oval
branching, Fx phyllotaxis, FH leaf shape, CH leaf color, NF fruits, and full maturity.
fruit quantity, CF fruit color, MF fruit maturity, FF fruit Specifically, three models of argan trees have been dis-
shape tinguished: model I: well-developed trees, with erect-patent
The cluster analysis establishes, as shown in the dendro- branching, fasciculate leaves, and buxoid or oleoid shape,
gram (Fig. 3), the distribution of the 21 individuals ana- light green color, with abundant fruiting and yellow pyri-
lyzed through qualitative characters, identifying three large form or fusiform fruit during maturity (see Fig. 4); model II:
groups: a morphotype I that gathers in the center of the more or less well-developed trees, with patent or somewhat
dendrogram the seven most productive individuals (Fig. 4), decumbent branching, with leaves in fasciculate arrange-
a morphotype II on the bottom with nine individuals of ment, myrtoid in shape and green color, medium or scarce
medium fruiting (Fig. 5), and the morphotype III on the top fructification with round or oval fruits of reddish or brown-
of the dendrogram with the five sterile individuals (Fig. 6). ish color (see Fig. 5), and model III: poorly developed trees
The MCA method was applied to group the 21 sampled with patent or decumbent branches, solitary, alternate leaves,
specimens by similar morphological characters (Fig. 7). This microbuxoid shape, and intense green color, without fruits
algorithm differentiates three different groups. The non-pro- (see Fig. 6). Morphotype I could be probably very close to
ductive group includes individuals with no fruit, low devel- the ideotype desired by any farmer.
opment, microbuxoid leaves, and dark green color. The sec-
ond group includes individuals with erect-patent branches, Suitability model and climate change scenarios
large development, abundant fruit, pyriform or fusiform in
shape, and less-intense green color of the leaves. The third The current geographical distribution of argan was mod-
eled in Maxent. Analysis of the AUC values of the training

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Fig. 4  Seven individuals of the Morphotype I model: well-developed trees, with erect-patent branching, fasciculate leaves, and buxoid or oleoid
shape, light green color, with abundant fruiting and yellow pyriform or fusiform fruit during maturity

and test data indicated acceptable values of 0.95 and 0.94, Discussion
respectively. These results explain the excellent discrimi-
nation ability of the model. The Jackknife test reveals that The level of genetic representativeness achieved with the
both variables Mean Diurnal Range Temperature (Tmdr) management of 21 individuals from the south Iberian crop
and Min Temperature of Coldest Month (Tncm) had the collection is enough to compensate for possible diversity
highest contribution in the model. Although, the remaining losses in wild populations in North Africa, as shown in
bioclimatic variables used were considered necessary in the Table 2; Fig. 10. The ratio between effective and detected
model (Fig. 8). alleles indicates a better distribution of allele frequency
As can be seen in the current scenario, suitability extends among our sampled individuals compared with the results
to locations where argan could be successful beyond its obtained by El Bahloul et al. (2014), Yatrib et al. (2017),
natural range. Table 4; Fig. 9 show the extent of the area and Mouhaddab et al. (2017) with a sample size of 150, 240,
estimated by the MaxEnt algorithm in six different mod- and 480 individuals, respectively. Figure 10 shows how the
els; combining current climate conditions with only in-situ rise in effectiveness decreases with increasing sample size,
locations (Fig. 9a) and with in-situ and ex-situ locations especially with ASMS2012-34 and ASMS2012-37 loci. It is
(Fig. 9b), two IPCC scenarios were used to calculate the relevant to mention that Mouhaddab et al. (2017) calculated
remaining four models, the most optimistic (RCP 4.5) by a core collection integrated by 92 individuals, increasing the
2050 (Fig. 9c), and 2080 (Fig. 9d), and the pessimistic one number of effective alleles from 14.55 to 19.60.
(RCP 8.5) during the same periods 2050 (Fig. 9e), and 2080 Results from Mouhaddab et al. (2017) show the possi-
(Fig. 9f), this time using all locations. bility to establish a core collection of only 13 individuals
A large part of the study area does not have the most using ISSR techniques and 96 using SSR. With only two
suitable conditions for argan occupation (more than 80%). SSR markers (ASMS01 and ASM2012-34), they obtained
The IPCC scenarios for 2050 and 2080 shift the area of a mean Ne = 20.81 with a sample of 480 trees, while using
distribution and/or cultivation towards the N, with a large the same markers in the crop collection, we have obtained
part of the current area of its wild populations in Morocco a mean Ne = 9.52, i.e., 45.75% of the total diversity of the
disappearing and refuges and new areas of cultivation 24 natural localities of argan in Morocco, so the number of
appearing on the N side of the Mediterranean Basin (Iberian, alleles detected is highly significant. likewise, our sample
Italic, and Balkan Peninsulas and the Tyrrhenian Islands). has a mean Na = 9.80, which exceeds those results obtained

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Trees

Fig. 5  Nine individuals of the of the Morphotype II model: more and green color, medium or scarce fructification with round or oval
or less well-developed trees, with patent or somewhat decumbent fruits of reddish or brownish color
branching, with leaves in fasciculate arrangement, myrtoid in shape

by (Bnikkou et al. 2021), who got a mean Na = 6.80 and the genetic diversity detected is very representative, because
4.60, respectively, when evaluating a Spanish locality (Ali- the allelic distribution has high effectiveness, and the level
cante) and a Moroccan one (Essaouira). of heterozygosity is very close to the expected one. Only
This genetic study has made it possible to identify indi- one of the six markers deviated significantly from HWE
viduals with higher heterozygosity; we have observed that (Ho < He), and the same pattern was observed in (El Bahloul
the individuals 1, 5, 6, 13, 16, and 17 have the highest het- et al. 2014). The opposite is true for other species such as
erozygosity across loci (H > 0.83) and individual 3 has the Pistacia vera and Olea europaea which have presented loci
lowest values (H = 0.33). This information may be interest- with significant deviation from HWE when assessing their
ing for the improvement of the species. It can be stated that

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 Trees

Fig. 6  Five individuals of the

of the Morphotype III model:
poorly developed trees with
patent or decumbent branches,
solitary, alternate leaves, micro-
buxoid shape, and intense green
color, without fruits

Fig. 7  Biplot of the 21 sampled

argan ex-situ collection grouped
applying the Multiple Cor-
respondence Analysis (MCA)
method

genetic structure using SSR markers (Choulak et al. 2019; In this assessment, it has been considered essential to
Gomes et al. 2009). ensure the management of a sufficiently representative

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Trees

Fig. 8  Jackknife test of the

importance of individual
climatic and environmental
variables (blue bars) in the
development of the MaxEnt
model relative to all climatic
and environmental variables
(red bar). Mean diurnal range
temperature (Tmdr) and min
temperature of coldest month
(Tncm) had the highest contri-
bution in the model

Fig. 9  Suitability areas of A. spinosa in the Mediterranean basin. 8.5 (e, f). Suitability class range: 0 means not suitable (white color),
Current geographical distribution using in-situ (a) and in-situ + ex- 0–0.25 means not very suitable (blue color), 0.25–0.50 means mod-
situ (b) collections. Potential geographical distribution by 2050 and erately suitable (yellow color), 0.50–0.75 means suitable (orange
2080 according to the climate scenarios RCP 4.5 (c, d) and RCP color), and 0.75–1 means highly suitable (red color)

genetic diversity in the collections and cultivation trials On the other hand, it has not been possible to establish
carried out. a correlation between molecular and morphological diver-
sity, since the markers used have been employed in various

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 Trees

Table 4  Current suitability areas of A. spinosa in the Mediterranean basin and its potential distribution area in 2050 and 2080 in the IPCC sce-
narios RCP 4.5 and RCP 8.5
Range Class Current RCP 4.5 RCP 8.5
2050 2080 2050 2080
2 2 2 2
Km % Km % Km % Km % Km2 %

0 Not suitable 17 864 337 72 19 567 786 79 20 182 163 82 19 148 483 78 20 021 218 81
0.00–0.25 Not very suitable 4 508 312 18 3 137 074 13 2 816 728 11 3 471 106 14 3 057 667 12
0.25–0.50 Moderately suitable 1 252 317 5 1 158 390 5 1 006 092 4 1 301 601 5 1 008 325 4
0.50–0.75 Suitable 612 113 2 585 496 2 485 431 2 545 071 2 399 521 2
0.75–1 Highly suitable 408 108 2 187 537 1 145 869 1 170 022 1 149 552 1
Total (km2) 24 645 187 100 24 636 283 100 24 636 283 100 24 636 283 100 24 636 283 100
RCP Representative concentration pathway

studies of similarity between populations in all localities of also others that have now disappeared, on the SW Atlantic
the argan natural habitats. Similarly, Majourhat et al. (2008) coast, where the historical record shows that it was also suc-
were also unable to correlate fruit types with genotype when cessfully cultivated (Herrera, 1513, ed. 1818; García Novo
comparing the results obtained with RAPD and SSR tech- et al. 2007).
niques, observing in their results that accessions of different
morphotypes had, in some cases, more genetic similarity
than accessions with the same morphotype. Conclusion
Our results confirm the high degree of argan polymor-
phism at both genetic and morphological levels as shown The historical presence and introduction of the argan tree
in (Mouhaddab et al. 2017; Zahidi et al. 2014). This high in diverse regions of the Mediterranean basin allow us to
diversity is justified not only by the habitat heterogeneity consider these ex-situ materials as a complementary tool for
(Msanda et al. 2021), but also probably by the development the conservation of the genetic diversity of this species. This
of an “i” diversity cenotic strategy (Blandin et al. 1976), a tool supports the implementation of domestication, improve-
typical adaptation strategy for species that appear dominant ment, and cultivation programs in a very wide range of envi-
in ecosystems with low “s” diversity. Such is the case of the ronmental variables in these territories.
Arganeraie ecosystem where the lack of species capable of The genetic diversity of the argan cultivated collection
occupying the different ecological niches allows argan to studied in the south of the Iberian Peninsula is highly repre-
conserve and express a high genetic diversity, thus achieving sentative of the total diversity estimated for the wild popula-
better resilience at the ecosystem level. tions of Morocco and can therefore be considered as a col-
Despite ongoing reforestation programs and because of lection of ex-situ diversity. Furthermore, as a core collection,
changing climatic conditions, the argan natural area occu- it can be used for the selection of propagation and cultivation
pancy continues to decrease each year (Sinsin et al. 2020). materials for productive purposes. Within these 600 speci-
This trend is evident in the climate scenarios modeled in this mens, three different morphotypes have been identified with
study, with a clear decrease in the most suitable area. Simi- distinguishable characters in terms of growth habit, branch-
larly, experiences in more southerly latitudes demonstrate ing, size, shape, and color of leaves and fruits.
the successful introduction of argan to northern Morocco The suitability models generated from the native distribu-
and Algeria (Benaouf et al. 2015; Kechairi and Benmahioul tion localities of the argan tree demonstrate the possibilities
2020), thus corroborating the observed shift of the most of its cultivation in a coastal area of variable width along the
suitable conditions for this species to thrive towards higher circum-Mediterranean areas, especially in the Iberian and
latitudes (Fig. 9). Therefore, the introduction of new ex-situ North African regions. By extending the occurrence data
localities increases the potential area of distribution of argan with ex-situ localities where it is successfully cultivated or
in the Mediterranean basin, extending the range of action conserved, its ecological range is increased and the possibil-
with a higher probability of cultivation in countries, such as ity of cultivation over larger areas is demonstrated.
Tunisia, northern Algeria, Libya, Egypt, Israel, Portugal, and Under foreseeable climate scenarios according to IPCC
Spain (Fig. 9). In the Iberian Peninsula, the model not only models (RCP4.5 and RCP8.5), the distribution and/or culti-
incorporates localities on the SE Mediterranean coast where vation area of the argan tree shifts towards the N, disappear-
argan specimens have been preserved (Crespo et al. 2007; ing a large part of the current area of its wild populations in
Martínez-Gómez et al. 2019; Rivera Núñez et al. 1997), but Morocco, and refuges and new cultivation areas appear on

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Trees

Fig. 10  Comparison of the number of detected and effective alleles for each locus with other studies. N = 38 (Majourhat et al. 2008). N = 150 (El
Bahloul et al. 2014). N = 240 (Yatrib et al. 2017). N = 480 (Mouhaddab et al. 2017)

the N side of the Mediterranean basin (Iberian and Balkan Data availability The data that support the findings of this study are
Peninsulas and islands such as Sicily and Sardinia). openly available in figshare repository at https://​doi.​org/​10.​6084/​m9.​
figsh​are.​18680​201.

Author contribution statements Study conception and Declarations

design were performed by JEH-B. Material preparation, and
data collection were performed by YL-R, EH-B, F-H, and Competing interests The authors have no relevant financial or non-
MH-C. Methodology, Investigation, analysis, and first draft financial interests to disclose.
written were performed by YL-R and EH-B. Review and
editing were performed by JLQ. Supervision was performed
by EH-B and JLQ. All authors read and approved the final References
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