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Botanical Sciences

versión On-line ISSN 2007-4476versión impresa ISSN 2007-4298

Bot. sci vol.95 no.3 México jul./sep. 2017

http://dx.doi.org/10.17129/botsci.887 

Ecology

Polymorphism analysis in some Algerian Opuntia species using morphological and phenological UPOV descriptors

Boubakr Hadjkouider1  2  * 

Ammar Boutekrabt1 

Bahia Lallouche2 

Salim Lamine3  4 

Néjia Zoghlami5 

1 Department of Agricultural Sciences. Faculty of Nature and Life Sciences. Saad Dahlab University, Blida, Algeria.

2 Department of Agricultural Sciences, Faculty of Science, Mohamed Boudiaf University, M’sila, Algeria.

3 Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Ceredigion, UK.

4 Laboratory of Management and Valorization of Natural Resources and Quality Assurance. University of Bouira, Bouira, Algeria

5 Laboratory of Plant Molecular Physiology, Biotechnology Centre of Borj-Cédria, Hammam-lif, Tunisia.

Abstract:

Background:

In the present study, we have investigated the morphological variation in a set of five Opuntia species from the Algerian steppes using 49 UPOV descriptors.

Questions:

Which of the 49 descriptors that can be used as powerful estimators of the phenotypic diversity within Opuntia species? How is the morphological diversity patterned in Algerian Opuntia?

Species study/ Mathematical model:

Opuntia ficus-indica, Opuntia amycleae, Opuntia streptacantha, Opuntia engelmannii, Opuntia robusta. Principal Components Analysis (PCA) and Hierarchical Cluster Analysis were used.

Study site:

Four counties were studied located in the Algerian steppes. The present research was carried out during 2014.

Methods:

49 descriptors adopted by the International Union for the Protection of New Varieties of Plants (UPOV) were employed in the present research, where cladode, flower and fruit traits were used to determine the overall degree of polymorphism among 5 Opuntia species.

Results:

Principal Component Analysis and Hierarchical Cluster Analysis indicated a consistent differentiation between all studied species. The relative magnitude of the first two PCA eigenvectors showed that 8 descriptors out of 49 were identified as the most important descriptors for the classification of the species. The dendrogram performed on the calculated Euclidean distances between all species pairs allowed the identification of 3 groups, unlike the PCA that identified 4 groups. The species Opuntia ficus-indica and Opuntia amycleae were identified as very close morphologically.

Conclusions:

The present outcome represents a paramount step towards the fast selection of interesting species and for their best management and conservation.

Key words: Opuntia; diversity; multivariate analyses; clustering; UPOV

Resumen:

Antecedentes:

En el presente estudio, hemos investigado la variación morfológica en un conjunto de cinco especies de Opuntia de las estepas argelinas utilizando 49 descriptores UPOV.

Preguntas:

¿Cuáles de los 49 descriptores que pueden ser utilizados como estimadores poderosos de la diversidad fenotípica dentro de las especies de Opuntia?

¿Cómo se modela la diversidad morfológica en el Opuntia Argelina?

Especie en estudio/ Modelo matemático:

Opuntia ficus-indica, Opuntia amycleae, Opuntia streptacantha, Opuntia engelmannii, Opuntia robusta. Análisis de Componentes Principales (PCA) y un Análisis de Agrupamiento Jerárquico fueron usados

Sitio de estudio y fechas:

Se estudiaron cuatro condados situados en la estepa argelina. La presente investigación se realizó durante el año 2014.

Métodos:

En la presente investigación se utilizaron 49 descriptores adoptados por la Unión Internacional para la Protección de las Obtenciones Vegetales (UPOV), en los que se utilizaron características de cladodio, flor y fruto para determinar el grado global de polimorfismo entre 5 especies de Opuntia.

Resultados:

Se aplicó un análisis multivariado, constituido por un análisis de componentes principales (PCA) y un análisis de agrupamiento jerárquico, cuyo resultado indicó una diferenciación consistente entre las especies estudiadas. Con base en la magnitud relativa de los dos primeros eigen-vectores del PCA se seleccionaron 8 de los 49 descriptores morfológicos como los más relevantes para la clasificación de las especies siendo los que más contribuyeron a la variación morfológica detectada. Dichos descriptores pertenecen a la lista de descriptores primarios establecida por la UPOV para la caracterización de Opuntia. El dendrograma obtenido aplicando el método de Ward (1963) para el cálculo de las distancias euclídeanas entre pares de poblaciones permitió identificar tres grupos distintos, mientras que el análisis PCA diferenció cuatro grupos. Por consiguiente, las especies Opuntia ficus-indica y Opuntia amycleae fueron identificadas como especies muy cercanas filogenéticamente.

Conclusiones:

Estos resultados representan un avance crucial para la selección e identificación rápida de poblaciones de interés y una mejora para las estrategias de gestión y conservación.

Palabras clave: Opuntia; la diversidad; análisis multivariado; agrupación; UPOV

The Cactaceae are dicotyledonous angiosperms, most plentiful in the arid and semi-arid regions between 35 N and 35 S composed of about 2,260 accepted species (Taylor 1997). Among these, the genus Opuntia L. Mill. has as many as 215 species.

Opuntia has been exploited since the pre-Columbian times and is mainly present in North and South America, but has also been introduced into the Mediterranean basin, Middle-East, South Africa, India, Thailand and Australia. The species reached the Mediterranean basin during the 16th century (Barbera 1995). Nevertheless, only towards the end of the 20th century have large plantations been established, where only rough estimates of the worldwide plantation area (Zoghlami et al. 2007) are allowed due to the absence of updated statistical data from countries in which this species is cultivated.

During the last decade, cacti (Opuntia ficus-indica) They have been used for almost 500 years as a fruit crop, a defensive hedge, and, more recently, as a fodder crop and as a standing buffer feed for drought periods; they can also play a key role in erosion control and land rehabilitation, particularly in arid and semi-arid zones, and as a shelter, refuge and feed resource for wildlife (Le Houérou 1996a).

Generally, the characterization of Opuntia genus is incomplete due to few morphological characters taken into account to classify them into the genus (Rebman & Pinkava 2001); also, the inadequate descriptors have led to misclassification (Caruso et al. 2010, Majure et al. 2012), they usually lack botanical references and other data, which makes it difficult to properly document and register different varieties under the basis of a reliable classification procedure (Gallegos-Vázquez 2012). Several authors have analyzed morphological diversity in several plants (Lamine et al. 2014, Arteaga et al. 2015). In Opuntia, morphological investigations have been carried out in Brazilian (Uchoa et al. 1998), Chilean (Wang et al. 1998), Mexican (Reyes-Agüero et al. 2005, Muñoz-Urias et al. 2008, Gallegos-Vázquez et al. 2011, Gallegos-Vázquez et al. 2012, Martínez-González et al. 2015) and Moroccan genetic resources (El Finti et al. 2013).

In Algeria, several ha are cultivated with Opuntia, where Opuntia ficus-indica (L.) Mill., is an important fodder crop, mainly for sheep, during low feed availability periods following drought and dry seasons. Large plantations have recently been established in the region of Souk-Ahras (commune of Sidi Fredj), also near the region of Tebessa, for the objective of improving and rehabilitating the steppe and the marginal areas (Neffar et al. 2011). Despite the importance of Opuntia in the country, only few studies have been undertaken to characterize the nutritional value of the fruits and cladodes as important food crop and fodder (Hadj Sadok et al. 2014), and the effect of the prickly pear plantation age on soil properties and vegetation cover (Neffar et al. 2011). Thus, studies that address the amount of morphological variation are still missing for Algerian Opuntia species.

Despite its great importance, some Opuntia species are threatened with extinction due to traditional agricultural practices unsuitable for their conservation and the negligence of some species. In addition, the morphological and genetic diversity of Opuntia have not been well assessed previously. The absence of such studies in Algeria motivated us to study the morphological and phenological polymorphism of these species and to determine the most discriminatory characteristics that allow separating this genetic richness.

In this study, we aim to assess the morphological diversity in five Opuntia species with potential agro-ecological values for human consumption present in the Algerian steppes, using 49 traits collected from cladodes, flowers and fruits following the International Union for the Protection of New Varieties of Plants (UPOV) guidelines. The phenotypic diversity among and within the species has been estimated to identify the traits that contribute most to the morphologic variation and classify the genotypes using PCA and hierarchical cluster analyses.

Materials and Methods

Plant material. Five Opuntia species of the subgenus Platyopuntia (Engelm.) Kreuz, Opuntia ficus-indica, Opuntia amycleae Ten., Opuntia engelmannii Salm-Dyck ex Engelm., Opuntia streptacantha Lem., and Opuntia robusta H.L.Wendl., were prospected from the Algerian steppes in Doukkara (Tébessa), Belaiba (M’sila), Mesrane (Djelfa) and Choucha (Laghouat) districts (Figure 1). In our study, we pre-considered O. amycleae as separate sepecies from O. ficus-indica just to check the morphological similarity. However, several authors consider O. amyclaea as synonyms of O. ficus-indica, and they divided this latter species into two botanical forms: a) O. ficus-indica f. amyclaea (Ten.) Schelle, with presence of spines and b) O. ficus-indica f. inermis (Web.) (Kiesling 1999), which is spineless. In the present work we adopted a random sampling method; the sampled species were then kept at the repository of the High Commissariat for Steppes Development (HCSD) and National Institute of Forestry Research (NIFR) in Algeria (Table 1).

Figure 1 Algerian Opuntia species investigated in this study: 1: Opuntia ficus-indica; 2: Opuntia amycleae; 3: Opuntia robusta; 4: Opuntia streptacantha; 5: Opuntia engelmannii. 

Table 1 List of the five Algerian Opuntia species evaluated in this study with their agro-ecological characteristics. 

Species O. ficus-indica O. amycleae O. streptacantha O. robusta O. engelmannii
Code OFI OA OS OR OE
Mains use Fruit Fruit fruit fruit fodder
Commercial importance very high very high very high medium low
Locality Belaiba Doukkara Choucha Mesrane Mesrane
(M’sila) (Tébessa) (Laghouat) (Djelfa) (Djelfa)
Latitude 35° 36’ 35° 58’ 34° 8’ 34° 36’ 34° 36’
Longitude 05° 17’ 8° 14’ 3° 01’ 3° 03’ 3° 03’
Temp. min (C°) 13,0 10,1 9,36 9,47 9,47
Temp. Max (C°) 24,3 22,3 23,0 23,3 23,3
Precipitation (mm) 238,2 406,7 236,4 229 229
Soil type sandy/muck land muck land sandy land sandy land sandy land
Soil pH 7.69 7.52 7.53 8.55 8.55
Bioclimatic Floor semi-arid semi-arid semi-arid semi-arid semi-arid
mild winter cold winter cold winter mild winter mild winter

Species analysis per species was applied to assess morphological variation, 10 individuals were scored, and from each individual 3 cladodes, 3 flowers and 3 fruits were investigated for their differences according to the 49 UPOV morphological descriptors (Table 2).

Table 2 Morphological and phonological descriptors used for the characterization of Opuntia species from Algeria (UPOV 2006). 

Code Descriptor Abbrev. Category Note
OFI OA OS OR OE
1 Plant: growth habit PGH 1: upright; 2: spreading; 3: decumbent; 4: drooping 1 1 1 1 1
2 Plant: height PH 7: tall; 3: short; 5: medium 7 7 7 3 5
3 Cladode: length CL 5: medium; 3: short; 7: long 5 5 3 3 7
4 Cladode: width CW 5: medium; 7: broad; 3: narrow 5 5 5 7 3
5 Cladode: length/width ratio CLW 5: medium; 3: small; 7:large 5 5 3 3 7
6 Cladode: thickness CT 5:medium; 3: thin; 7: hick 5 5 3 7 3
7 Cladode: shape CS 3: elliptic; 7: obovate; 4: circular; 5: rhombic 3 3 7 4 5
8 Cladode: color CC 3: medium green; 2: light green; 5: bluish green; 1: yellow green 3 3 2 5 1
9 Cladode: color of areoles CCA 3: brown; 1: grey; 4: black 3 3 1 4 1
10 Cladode: number of spines per areole CNSA 1: none or very few; 7: many; 5: medium 1 7 7 5 7
11 Cladode: length of longest spine CLLS 5: medium; 3: short; 7: long 3 5 3 5 7
12 Spine: main color SMC 2: white; 3: yellow 2 2 2 2 3
13 Spine: number of colors SNC 2: tow; 1: one 1 2 2 2 1
14 Central spine: attitude CSA 1: erect; 5: horizontal 1 1 5 1 1
15 Central spine: Curvature (excluding base) CSC 1: absent; 9: present 1 1 9 1 1
16 Central spine: twisting CST 1: absent; 9: present 1 9 1 1 1
17 Cladode: presence of glochides CPG 1: absent or very few; 3: many; 2: few 1 3 3 2 3
18 Cladode: color of glochides CCG 2: brown; 1: yellow 2 2 1 1 1
19 Cladode: number of flowers CNF 7: many; 5: medium; 3: few 7 5 7 3 5
20 Flower: length FL 5: medium; 7: long 5 5 5 5 7
21 Flower: color of perianth FCP 2: yellow; 4: orange; 1: greenish yellow 2 2 4 1 2
22 Flower: color of style FCS 4: pink; 5: red; 2: white; 1: green 4 4 5 2 1
23 Flower: number of stigma lobes FNSL 5: medium; 7: many; 3: few 5 5 7 7 3
24 Flower: color of stigma lobe FCSL 2: green; 1: yellow 2 2 2 1 1
25 Fruit: length FRL 5: medium; 3: short 5 5 3 3 3
26 Fruit: maximum diameter FMD 5: medium; 3: broad 5 5 3 5 3
27 Fruit: ratio length/maximum diameter FLD 5: medium; 3: small 5 5 3 3 5
28 Fruit: shape FS 3: elliptic; 4: circular; 5: oblate; 2: narrow elliptic 3 3 4 5 2
29 Fruit: density of areoles FDA 7: dense; 5: medium; 3: sparse 7 7 5 3 3
30 Fruit: number of glochides FNG 3: few; 7: many; 5: medium 3 7 7 5 5
31 Fruit: color of glochides FCG 2: brown; 1: yellow 2 2 1 1 1
32 Fruit: length of stalk FLS 5: medium; 3: short; 7: long 5 5 3 3 7
33 Fruit: depression of receptacle scar FDRS 5: moderately depressed; 3: absent or slightly depressed; 5 5 5 3 7
7: strongly depressed
34 Fruit: diameter of receptacle scar FDIR 5: medium; 3: small 5 5 5 5 3
35 Fruit: thickness of peel FTP 5: medium; 3: thin; 7: thick 5 5 3 7 7
36 Fruit: weight of peel FWP 3: light; 5: medium 3 3 3 5 3
37 Fruit: weight of flesh FWF 5: medium; 7: heavy; 3: light; 9: very heavy; 1: very light 5 7 3 9 1
38 Fruit: ratio of weight of flesh/peel FWFP 5: medium; 7: large; 3: small 5 7 3 5 3
39 Fruit: evenness of color surface FECS 2: uneven; 1: even 2 2 2 1 1
40 Fruit: main color of surface FMCS 4: dark green; 8: medium red 4 4 4 8 8
41 Fruit: color of flesh FCF 3: yellow; 6: red 3 3 3 6 6
42 Fruit: firmness of flesh FFF 5: medium; 7: firm 5 5 5 7 7
43 Fruit: number of fully developed sedes FNFD 7: many; 5: medium; 3: few 7 5 3 7 3
44 Fruit: presence of abortive seeds FPAS 9: very many; 7: many; 5: medium 3: few; 9 7 5 3 1
1: absent or very few
45 Seed: size SS 5: medium; 3: small; 7: large 5 5 3 7 7
46 Time of beginning of flowering TBF 3: early; 5: medium; 7: late 3 3 5 5 7
47 Flowering habit FH 2: twice flowering; 1: once flowering 2 2 1 1 1
48 Time of harvest maturity THM 3: early; 5: medium; 7: late 3 3 5 5 7
49 Duration of harvesting period of fruit DHPF 5: medium;3: short;7: long 5 5 5 3 7

Morphological descriptors and data collection. Forty-nine major quantitative and qualitative traits, selected from the UPOV list (UPOV, 2006), comprising cladode, flower and fruit descriptors were measured and used to design a numbered-data matrix (Table 2). Ten individuals per species were evaluated for their morphological diversity across the 49 descriptors. Measurements were performed by the same two persons to avoid errors due to individual variations.

Statistical analysis based on the morphological diversity of cladode, flower and Opuntia fruits. Morphological and phenological data were analyzed by multivariate analyses and clustering using XLSTAT software (Addinsoft, http://www.xlstat.com). PCA was performed to identify species groups and to determine the axes and the characters significantly contributing to the variation. In this procedure, the similarity matrix was used to generate eigenvalues and scores for the species. The first two principal components, which accounted for the highest variation, were then used to plot two-dimensional scatter plots. Hierarchical cluster analyses (HCA) was carried out using Ward’s minimum variance method as a clustering algorithm (Williams 1976) and squared Euclidean distances as a measure of dissimilarity (Ward 1963).

Results

Principal Component Analysis (PCA). The Principal Component Analysis (PCA) showed a high level of morphological variation between the five studied Opuntia species (Table 3). The first 2 axes of the PCA accounted for 67.217 % of the total variation with the first component (PC1) explaining 38.239 % of the total variation, while PC2 accounted for 28.978.

Table 3 Definition the first two components of the PCA based on 49 UPOV morphological descriptors in five Opuntia species from Algeria. 

Principal components PC1 PC2 PC3
Eigenvalue 18.354 13.910 11.314
Variability (%) 38.239 28.978 23.570
% cumulative 38.239 67.217 90.787
Morphological descriptors* Eigenvalue
1 0.000 0.000 0.000
2 -0.127 -0.224 0.016
3 0.097 -0.128 -0.229
4 -0.113 0.217 0.100
5 0.097 -0.128 -0.229
6 -0.094 0.239 -0.061
7 0.112 -0.083 0.239
8 -0.107 0.238 0.013
9 -0.125 0.210 -0.089
10 0.127 -0.048 0.123
11 0.182 0.043 -0.018
12 0.191 0.001 0.061
13 0.030 0.081 0.191
14 0.027 -0.086 0.279
15 -0.003 -0.104 0.271
16 -0.093 -0.040 -0.064
17 0.120 -0.091 0.112
18 -0.184 -0.066 -0.161
19 -0.086 -0.218 0.052
20 0.203 -0.079 -0.116
21 -0.013 -0.192 0.204
22 -0.181 -0.107 0.146
23 -0.097 0.128 0.229
24 -0.186 -0.151 0.061
25 -0.184 -0.066 -0.161
26 -0.163 0.149 -0.127
27 -0.018 -0.131 -0.255
28 -0.062 0.197 0.185
29 -0.203 -0.119 -0.055
30 0.019 -0.055 0.182
31 -0.184 -0.066 -0.161
32 0.097 -0.128 -0.229
33 0.113 -0.217 -0.100
34 -0.203 0.079 0.116
35 0.124 0.154 -0.185
36 0.025 0.264 0.042
37 -0.126 0.212 -0.005
38 -0.157 0.076 -0.117
39 -0.186 -0.151 0.061
40 0.186 0.151 -0.061
41 0.186 0.151 -0.061
42 0.186 0.151 -0.061
43 -0.137 0.181 -0.110
44 -0.223 -0.064 -0.039
45 0.124 0.154 -0.185
46 0.229 0.001 0.043
47 -0.184 -0.066 -0.161
48 0.229 0.001 0.043
49 0.113 -0.217 -0.100

*See table 2.

Out of 49 morphological descriptors, 8 were identified as the most discriminating and useful for the classification of the Opuntia species. The contribution of all parameters to the definition of the first two PCA axes is given in Table 3. The traits that best contributed to the first component variability were the following: time of beginning of flowering (0.229), time of harvest maturity (0.229), flower length (0.203), main spine color (0.191), main color of fruit surface (0.186), color of fruit flesh (0.186), firmness of fruit flesh (0.186), length of the longest spine per cladode (0.182). On the other hand, in the second PCA component, we obtained highly and positive correlation for the descriptions cladode width (0.217), cladode thickness (0.239), cladode color (0.238), color of areoles per cladode (0.210), fruit shape (0.197), peel weight per fruit (0.264), flesh weight per fruit (0.212), and number of fully developed seeds per fruit (0.181) (Table 3, Figure 2).

Figure 2 Principal Component Analyses showing: A) the contribution of the UPOV descriptors (from 1 to 49, see Table 2) to the obtained morphological variation; B) the distinction of all studied Opuntia species. 

The projection of the species on the plot delimited by the first two PCA axes, showed the classification of the species into four distinct groups (Figure 2). The first group (a) comprises Opuntia engelmannii a second group (b) includes two species, Opuntia ficus-indica and Opuntia amycleae situated at the negative side of the plot, Opuntia robusta constituted the third group (c) and Opuntia streptacantha constituted the fourth group (d).

Cluster Analysis. To understand how the 5 Opuntia species are structured a ward-derived dendrogram was constructed based on the data yielded by the 49 morphological descriptors (Figure 3). This allowed the identification of 3 groups, unlike the PCA and phenological that identified 4 groups (Figure 3). The first cluster (C1) was constituted by three species: Opuntia robusta (OR), Opuntia ficus-indica (OFI) and Opuntia amycleae (OA). Within this group, Opuntia robusta was very different and characterized by a high number of fully developed seeds per fruit, broad thick bluish green cladodes, with black areoles, oblate fruit shape, medium peel weight and heavy fruit flesh weight (Figure 3). Opuntia ficus-indica and Opuntia amycleae were the closest as both were characterized by brown glochides, medium flower length, pink flower style, green stigma lobes, a medium ratio of length/maximum diameter of fruit, dense areoles, medium diameter of the receptacle scar.

Figure 3 Dendrogram showing relationships between five Opuntia species in Algeria using 49 morphological descriptors (G1 and G2 stand for the identified groups). 

Opuntia streptacantha formed the second cluster (C2) having an obovate cladode shape, two types of color spines, a horizontal attitude of the central spine, orange colored perianth, high number of stigma lobes and glochides.

The third group (C3) was constituted by Opuntia engelmannii (OE) that is distinguishable particularly, by late time of beginning of flowering and harvest maturity, long flower length, yellow spine color, medium red fruit surface, red fruit firm flesh, high number of long spines per areole per cladode, and large amount of many glochides (Figure 3).

Discussion

The present study revealed the morphological and phenological diversity in the five dominant species of Opuntia grown in Algerian steppes using 49 morphological descriptors.

The set of the UPOV descriptors used here allowed, for the first time, the characterization of the morphological diversity in 5 Algerian Opuntia species. The number of the descriptors was high if compared to previous studies in Cactaceae with 24 descriptors: seven describing the cladode (length, width, thickness, ratio length/width, number of areoles in the central row, number of spines per areole, length of the longest spine), three for the flower (number of flowers per cladode, length of the flower, number of stigma lobes) and 14 related to the fruit (length, maximum diameter, ratio length/maximum diameter, density of areoles, peduncle length, depression of receptacle scar, receptacle diameter, peel thickness, peel weight, pulp weight, ratio weight of peel/fruit weight, number of normal seeds, number of abortive seeds, total soluble solids (°Brix) in Gallegos-Vázquez et al. (2011), 27 descriptors from cladodes, flowers and fruits were measured in Gallegos-Vázquez et al. 2012 and 23 descriptors in Mejía et al. (2013).

According to the analysis performed, only few descriptors have shown an effective discriminating capacity. Two quantitative descriptors (length of flower and length of the longest spine per cladode,) and six qualitative descriptors (following: time of beginning of flowering, time of harvest maturity, spine main color, main color of fruit surface, color of fruit flesh, firmness of fruit flesh) have been identified as differential parameters in Opuntia ficus-indica, Opuntia amyclaea, Opuntia streptacantha, Opuntia robusta and Opuntia engelmannii (Table 3). These descriptors ranked within the primary list established by the UPOV for the characterization of Opuntia species (UPOV, 2006).

In comparison with other results, five variables were found to be significant to discriminate forty three accessions (Opuntia ficus-indica) fruit weight, peel weight, pulp weight, juice weight and peel thickness were considered as the most discriminative traits (Chalak et al. 2014), Three variables were selected as significant to discriminate twenty nine cactus pear varieties and four xoconostle varieties: peel thickness, pulp weight and to a lesser extent the diameter of the receptacle were the most discriminating of the UPOV guidelines traits (Gallegos-Vázquez et al. 2011). Moreover, spine number, margin hardness and areole distance were selected the three major variables to discriminate between three populations of Hylocereus Britton & Rose spp. (Mejía et al. 2013). In addition, ten morphological descriptors including; recepticular scar diameter, seed number, pulp weight, cladodes shape, spines, fruits number, fruits size, recepticular scar position, peel and pulp color were registered to be significant to discriminate Opuntia ficus-indica and Opuntia amyclaea (Erre & Chessa 2013).

It has been reported that phenotypic differences between populations can be linked to environmental and genetic variables (Muñoz-Urias et al. 2008). Additionally, Reyes-Agüero (2005), reported the elements of the syndrome of domestication in Opuntia and many traits are of primary interest for human utilization and have had a clear effect on domestication (Gallegos-Vázquez et al. 2012). The use of morphological descriptors comprising cladode, flower and fruit traits yielded a high number of morphotypes and allowed the discrimination of all of the studied species. In previous studies, the discrimination level was found to be as high as those reported by other studies using molecular markers for Opuntia spp (Labra et al. 2003, García-Zambrano et al. 2006, Zoghlami et al. 2007, García-Zambrano et al. 2009, Caruso et al. 2010, Majure et al. 2012, El-Banna et al. 2013, Valadez-Moctezuma et al. 2014, Ganopoulos et al. 2015, Samah et al. 2016).

Multivariate analyses based on morphological characters are continuously providing valuable information allowing the breeder to improve the species selected from specific geographical regions (Souza & Sorrells 1991). Previously, the multivariate techniques have been applied in Opuntia aiming at the morphological and the agronomic descriptions (Reyes-Agüero et al. 2005, Peña-Valdivia et al. 2008) and the industrial (Hammouch et al. 2013).

In our case, multivariate analyses have shown that the highest amount of variation was attained using fruits descriptors (Table 3). These were previously shown as the most important characters for the description of the species (Valdez-Cepeda et al. 2003, Reyes-Agüero et al. 2005, Gallegos-Vázquez et al. 2012).

Morphological descriptors were identified as powerful tools in providing meaningful data on the qualitative and the quantitative aspects in some Opuntia species. Morphological characterization is needed to provide the users with valuable information on individual accessions, relationship among traits, and the structure of collections.

In this study, we managed to provide insights on the level of polymorphism and the structuring of the diversity in five Opuntia species from the Algerian steppes using 49 UPOV morphological and phenological descriptors.

These results may contribute to the best management of the genetic diversity in Opuntia species from Algeria throughout the establishment of a core-collection sheltering representatives from interesting species that best exhibit variation, and this would be a benefit for conservation and for future breeding programs.

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Received: August 17, 2016; Accepted: March 21, 2017

* Corresponding author: Boubakr Hadjkouider, e-mail: bhadjkouider@gmail.com

All authors contributed equally during the preparation of this work.

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