Biodiv. Res. Conserv. 50: 25-32, 2018 BR C www.brc.amu.edu.pl DOI 10.2478/biorc-2018-0005 Submitted 06.05.2018, Accepted 30.06.2018 Numerical taxonomic study of the genus Crotalaria L. (Crotalarieae, Fabaceae) in Nigeria Samaila Samaila Yaradua*1,2, Dhafer Ahmed Alzahrani2 & Abubakar Bello1 Center for Biodiversity and Conservation, Department of Biology, Umaru Musa Yar’adua University, P.M.B. 2218, Katsina, Nigeria Department of Biological Sciences, Faculty of Science, King Abdulaziz University, Jeddah, Saudi Arabia 1 2 Abstract. Numerical taxonomic study of the genus Crotalaria L. in Nigeria was conducted to identify and differentiate some of the species of the genus Crotalaria using numerical taxonomy based on quantitative and qualitative characters. Field work was conducted, where different species were collected and analyzed using multivariate analysis. The results showed that all the collected species are distinct at Euclidian distance of 0.41 in the cluster analysis with Cophenetic correlation (r)=0.964. The ordination analysis based on the results of the PCA, separated the specimens into 7 groups corresponding to the result of cluster analysis. The first two components of the PCA account for 81.5%. The length of petiole, width of leaflet and length of fruit contributed more to showing delimitation among the species. Key words: Crotalaria, multivariate analysis, Nigeria, numerical taxonomy 1. Introduction Crotalaria L. is one of the largest genera of Fabaceae consisting of ca. 700 species (Le Roux et al. 2013). It is the largest genus of vascular plants in tropical Africa (Polhill 1982). The genus common name is “rattlepod” or “rattlebox” and it is derived from the fact that the seeds become loose in the pod as they mature, and make a rattling sound when the pod is shaken. Representatives of Crotalaria differ in habit that ranges from small shrubs to herbs and may be annual or perennial. They are easily recognised by their yellow, whitish to purplish or bluish coloured flowers. The leaves are simple or one to three foliate, alternate, lanceolate to obovate. The genus can also be recognised by a combination of the following five diagnostic characters: rostrate keel, 5+5 highly dimorphic anther arrangement (five long, basifixed anthers alternating with five short, dorsifixed ones), trichomes present on the style, inflated fruit, and macrocyclic pyrrolizidine alkaloids (Baker 1914; Polhill 1968; Van Wyk 2005) Crotalaria is almost cosmopolitan in distribution across tropical and subtropical regions of the world (Lewis et al. 2005), with it centre of diversity in Africa and Madagascar (ca. 543 species) (Polhill 1968, 1982; Le Roux et al. 2013) and a secondary center in India (ca. 92 species) (Ansari 2008; Sibichen & Nampy 2007). The genus is also widely distributed across the southern hemisphere, extending into Asia and North America. There are ca. 51 species of Crotalaria in West Africa (Hutchinson et al. 1958) commonly distributed in tropical and sub-tropical regions. Some of the species within the genus are widely used in agriculture, production of commercial products while some have medicinal and nutritional value (Polhill 1982; Van Wyk 2005; Pandey et al. 2010). Morphometric analysis involves the multivariate analysis of a set of quantitative and qualitative morphological characters of individual specimens of the taxa of interest (sometimes referred to as operational taxonomic units, or OTUs). This is often used to determine whether closely related species have discrete or overlapping morphologies, which may be important in the taxonomic revision of a group. It is also used to ascertain the useful characters that can be used in classifying taxa of interest. Morphometrics attempts to classify organisms based on morphological similarity. It can be used to describe ©Adam Mickiewicz University in Poznań (Poland), Department of Plant Taxonomy. All rights reserved. VARIABILITY, TAXONOMY AND PHYLOGENY * corresponding author (e-mail: dryaradua@gmail.com) 26 Samaila Samaila Yaradua et al. Numerical taxonomic study of the genus Crotalaria L. (Crotalarieae, Fabaceae) in Nigeria the pattern of similarities among taxa by ordination or cluster analysis (James & McCulloch 1990). Several angiosperm taxa have been reclassified using numerical taxonomy (El-Gazzar 2008). Hussaini and Iwo (1992) worked extensively on Crotalaria and reported the genus phenological information which is based on conventional taxonomic methods. The aim of this study is to identify and differentiate some of the species of the genus Crotalaria in Nigeria. Table 1. List of studied species within the genus Crotalaria S/No Name of taxon Collector Number Locality 1. 2. 3. 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 C. macrocalyx C. macrocalyx C. senegalensis C. senegalensis C. senegalensis C. senegalensis C. senegalensis C. senegalensis C. senegalensis C. senegalensis C. senegalensis C. senegalensis C. atrorubens C. atrorubens C. atrorubens C. atrorubens C. atrorubens C. atrorubens C. atrorubens C. atrorubens C. atrorubens C. atrorubens C. goreensis C. goreensis C. goreensis C. goreensis C. goreensis C. goreensis C. retusa C. pallida C. pallida C. pallida C. pallida C. pallida C. pallida C. pallida C. pallida C. pallida C. pallida C. pallida var. obovata C. pallida var. obovata C. pallida var. obovata C. pallida var. obovata C. pallida var. obovata C. pallida var. obovata C. pallida var. obovata C. pallida var. obovata C. pallida var. obovata C. pallida var. obovata Yaradua Muhammad Yaradua Yaradua Yaradua Yaradua Yaradua Yaradua Yaradua Yaradua Yaradua Yaradua Yaradua Yaradua Yaradua Yaradua Yaradua Yaradua Yaradua Yaradua Yaradua Yaradua Mustapha Yaradua Mustapha Yaradua Yaradua Yaradua Yaradua and Bello Yaradua Yaradua and Bello Yaradua and Bello Yaradua and Bello Yaradua and Bello Yaradua and Bello Bello Bello Bello Yaradua Yaradua and Bello Yaradua and Bello Bello Yaradua and Bello Yaradua Yaradua and Bello Yaradua and Bello Yaradua and Bello Yaradua and Bello Yaradua and Bello SSY1 MM1 SSY2 SSY3 SSY4 SSY5 SSY6 SSY7 SSY8 SSY9 SSY10 SSY11 SSY12 SSY13 SSY14 SSY15 SSY16 SSY17 SSY18 SSY19 SSY20 SSY21 SSY22 SSY23 SSY24 SSY25 SSY26 SSY27 Bello395 SSY28 Bello396 Bello397 Bello398 Bello399 Bello340 Bello341 Bello342 Bello343 SSY28 Bello344 Bello345 Bello346 Bello347 SSY29 Bello348 Bello349 Bello350 Bello351 Bello352 Jibia Jibia Kaita Kaita Kaita Mashi Mashi Mashi Mani Mani Daura Daura Sandamu Sandamu Kaita Kaita Kaita Mashi Mashi Jibia Jibia Jibia Mani Jibia Jibia Jibia Jibia Jibia Kaita Jibia Jibia Daura Daura Daura Daura Mani Mani Jibia Kaita Kaita Kaita Kaita Kaita Kaita Jibia Jibia Daura Daura Daura Biodiv. Res. Conserv. 50: 25-32, 2018 2. Materials and methods 2.1. Taxon sampling Specimens were collected in the field to study their vegetative and floral morphology. The specimens were pressed carefully, to not affect their vegetative and floral characters. Morphological measurements of the characters were made immediately. In addition, some dried specimens from the herbarium of Umaru Musa Yaradua University, Katsina (herbarium acronym) were used in the study. The total numbers of 49 individuals representing 7 species were found and used in the morphometric analyses. The details of the taxa included in the analysis are given in Table 1. 2.2. Morphological characters A character set, consisting of 21 characters for morphometric analysis of Crotalaria, was adapted from the character set used previously by Le Roux et al. (2013) and Britto et al. (2011) with some slight modifications. Out of the 21 characters, 15 were quantitative and 6 were qualitative (Table 2). 2.3. Multivariate analysis Multivariate analyses were carried out by cluster analysis (CA), principal components analysis (PCA) and Jaccards similarity coefficient using PAST 3 program (version 3.05) to determine the morphological similarity among the species and the characters that contribute to the variation of the taxa. 2.4. Cluster analysis Cluster analysis is a multivariate data mining technique, whose goal is to group objects based on a set of user selected characteristics. The cluster analysis groups individuals that are very similar in one cluster and shows similarities and differences among and within the clusters by building similarity matrix between the studied individuals. Individuals in the same cluster will be recognized as belonging to the same species. The cophenetic correlation coefficient between the distance matrix and the tree matrix was calculated to examine how well the cluster analysis fits the distance matrix (Sokal & Rohlf 1997; Rohlf 1998). 2.5. Principal Component Analysis (PCA) PCA is an accepted method to study multivariate character correlation. Its purpose is to study linearly correlated variables (Hotelling 1933, 1936). PCA enables the distinguishing of groups as well as identification of Table 2. List of quantitative and qualitative characters and their characteristics used in morphometric analysis S/No Character 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 Number of leaflet (Nl) Length of petiole (Lp) Length of leaflet (Ll) Width of leaflet (Wl) Length of fruit (Lf) Length of seed (Ls) Length of pedicel (Lpd) Number of flowers per axis Length of calyx (Lc) Number of seeds (Ns) Length of standard petal (Lsp) Width of standard petal (Wsp) Length of wing petal (Lwp) Width of wing petal (Wwp) Length of keel petal (Lkp) 16 17 18 19 Habit (H) Life form (lf) Presence of hair on stem(Ph) Shape of leaflet (Sl) 20 21 Inflorescence position (Ip) Pod size (Ps) States Quantitative characters mm mm mm mm mm mm mm mm mm mm mm mm Qualitative characters Herb (0), small shrub (1) Annual (0), Perennial (1) Presence (0), Absent (1) Lanceolate (0), Spatulate (1), Elliptic (2), Cuneate (3), Obovate (4) Terminal (0) Axial (1) Slightly exceeding calyx (0), far exceeding calyx (1) 27 28 Samaila Samaila Yaradua et al. Numerical taxonomic study of the genus Crotalaria L. (Crotalarieae, Fabaceae) in Nigeria Fig. 1. Unweighted Pair Group Method with Arithmetic mean (UPGMA) phenogram resulting from cluster analysis. Cophenetic correlation (r)=0.964 the relative contribution of size dependent and size-independent variation to species discrimination (Humphries et al. 1981). Therefore, it will show those characters that are useful in showing delimitation among the species. The Jaccards similarity coefficient was calculated to found the morphological similarity among the species. All the 21 morphological characters, including both quantitative and qualitative traits, for all the 49 specimens were used for the analysis and each individual specimen was considered as an operational taxonomic unit (OUT). In all the analysis, the data were first log10 transformed for the standardization of the data matrix. 3. Results 3.1. Cluster analysis The result of the cluster analysis separates the data set into seven clusters (at Euclidian distance of 0.41; Fig. 1), and the cophenetic correlation coefficient value of r=0.964 indicates a perfect match between the triangular distance matrix and the phenogram (Sneath & Sokal 1973; Rohfl 1998). The groups were recognized as distinct taxa at different taxonomic hierarchies, if all their OTUs did not mix between clusters. All the a priori groups formed distinct clusters with the exception of G (C. pallida var. pallida) and H (C. pallida var. obovata) Table 3. Similarity matrix based on Jaccard’s coefficient C. macrocalyx C. atrorubens C. senegalensis C. goreensis C. retusa C. barkae C. pallida C. pallida var. obovata C. macrocalyx C. atrorubens C. senegalensis C. goreensis C. retusa C. barkae C. pallida C. pallida var. obovata 1 0.933333 1 1 1 0.933333 1 0.933333 1 0.933333 0.933333 0.933333 0.866667 0.933333 1 0.933333 1 1 1 0.933333 1 1 0.933333 1 1 1 0.933333 1 1 0.933333 1 1 1 0.933333 1 0.933333 0.866667 0.933333 0.933333 0.933333 1 0.933333 1 0.933333 1 1 1 0.933333 1 1 0.933333 1 1 1 0.933333 1 1 0.933333 1 1 1 0.933333 1 1 Biodiv. Res. Conserv. 50: 25-32, 2018 Fig. 2. Plot of the first two principal component analyses (PCA) obtained from the analysis of the morphological data set for specimens of the studied species within the genus Crotalaria. The first and second PCA axes explain 72.3% and 9.2% of the total variation among all the taxa, respectively Explanations: A – Crotalaria macrocalyx, B – C. atrorubens, C – C. senegalensis, D – C. goreensis, E – C. retusa, F – C. barkae, G – C. pallida var. pallida, H – C. pallida var. obovata whose specimens intermixed and formed a large cluster (cluster VII).This is because they are the same species, and H is a variety of G. Result of the cluster analysis showed the relationship among the studied seven species. Two major clusters (A and B) were found in the UPGMA dendogram with sub-clusters within them. C. macrocalyx and C. atrorubes were clustered together in one sub-cluster. This showed that they are closely similar. This sub-cluster was connected with C. barkae forming a large cluster B. In cluster A, C. senegalensis was grouped with C. goreensis in a sub-cluster, which indicates that the two species share some similarities.This sub-cluster toghether with a sub-cluster contaning C. pallida and C. pallida var. obovata and a sub-cluster of C. retusa formed the large cluster A. The grouping indicates that members of each group are more similar to each other than to the members of other groups. The results of the Jaccard’s similarity coefficient varied between 0.867 and 0.993,indicating closer relationships among the species (Table 3). 3.2. Ordination The ordination analysis based on the result of PCA separated 49 specimens into 7 groups corresponding largely to those obtained in the cluster analysis (Fig. 2). Principal component 1 accounted for 72.3% of the variation, while principal component 2 accounted for 9.2% of the variation (Fig. 1). The loading of the PC 1 and 2 is presented in Table 4. The character mostly correlated with the first PCA axis (r>0.50) is the length of petiole – 0.77, while the character correlated with the second PCA axis (r>0.50) is the number of flowers per axis – 0.87. The result of the PCA showed that the majority of the clusters in the ordination plot, corresponds largely to those obtained by cluster analysis. The length of petiole, width of leaflet and length of fruit contributed more to showing delimitation among the species (Fig. 3). The priori groups identified in cluster analysis (Euclidian distance 0.41, Fig. 1) were supported by the ordination analysis. 3.3. Taxonomic description and revision Crotalaria macrocalyx Benth. London Journal of Botany 2: 572 (1843) Type: Heudelot M. 205 (P, holotype) Herb, annual; leaves 3-foliate, lanceolate, petiole length 3-5 mm, leaflet length 42-45 mm, leaflet width 8-10 mm, inflorescence terminal with 6-8 flowers, calyx length 9-11mm, standard petal length 6-8 mm, standard petal width 8-10 mm, wing petal length 9-11 mm, wing 29 30 Samaila Samaila Yaradua et al. Numerical taxonomic study of the genus Crotalaria L. (Crotalarieae, Fabaceae) in Nigeria Fig. 3. PCA loading of the characters shows the PCA loading of the contribution of each character to similarities among the species. The length of petiole and length of leaflet have higher loading in the result petal width 5-7 mm, fruit length 6-8 mm, pods slightly exceeding calyx, seed length 2-3 mm, hairs present on stem. Crotalaria atrorubens Benth. London Journal of Botany 2:572 (1843) Type (Isotype) Shrub, annual, leaves 3-foliate; spatulate, leaflet length 30-33 mm, leaflet width 6-8 mm, petiole length 4-6 mm, inflorescence terminal with 7-8 flowers, calyx length 10-12 mm, standard petal length 8-10 mm, standard petal width 8-10 mm, wing petal length 7-9 mm, Table 4. Loadings of the first and second components of the principal components analysis Axis Eigenvalue % variance 1 0.3524410 72.337 2 0.0450442 09.2451 3 0.0368382 07.5608 4 0.0254375 05.2209 5 0.0179612 03.6864 6 0.0048452 00.99445 7 0.0012719 00.26105 8 0.0011449 00.23499 9 0.0007317 00.15018 10 0.0005689 00.11676 11 0.0003361 00.068992 12 0.0002474 00.050785 13 0.0001870 00.03839 14 0.0001280 00.026278 15 4.00E-050 00.0082159 wing petal width 5mm, fruit length 8-10 mm, pods slightly exceeding calyx, seed number 9-11, seed length 1-2 mm, pedicel length 2-4 mm, hairs present on the stem. Crotalaria senegalensis (Pers.) Bacle ex DC. Prodromus Systematis Naturalis Regni Vegetabilis 2: 133 (1825) Type: Adanson 24 (MPU, isotype). Shrub, annual, leaves 3- foliate; elliptic, leaflet length 33-35 mm, leaflet width 10-12 mm, petiole length 20-22 mm, inflorescence terminal or axial with many flowers, calyx length 3-5 mm, standard petal length 1012 mm, standard petal width 7-9 mm, wing petal length 5-7 mm, wing petal width 5-7 mm, fruit length 9-11 mm, pods far exceeding calyx, number of seed 10, seed length 1-2 mm, length of pedicel 3 mm, hairs present on stem. Crotalaria goreensis Guill. & Perr. Florae Senegambiae Tentamen 1: 165 (1832) Type: Leprieur & Perrottet number (P, protologue) Shrub, annual, leaves 3-foliate; elliptic, leaflet length 40-42 mm, leaflet width 17-19 mm, petiole length 40-42 mm, inflorescence terminal or axial with many flowers, calyx length 6-8 mm, standard petal length 8-10 mm, standard petal width 10-12 mm, wing petal length 12-14 mm, wing petal width 7-9 mm, fruit length 15-17 mm, pods far exceeding calyx, seed number 1012, seed length 3-5 mm, pedicel length 3-5 mm, hairs present on the stem. Crotalaria barkae Schweinf Bull. Herb. Boissier 4 (App.2): 226 (1896) Shrub, annual, leaves 3-foliate; elliptic, leaflet length 30-32 mm, leaflet width 13-15 mm, petiole length 30- Biodiv. Res. Conserv. 50: 25-32, 2018 32 mm, inflorescence terminal with 1-3 flower, calyx length 4-6 mm, standard petal length 8-10 mm, standard petal width 7-9 mm, wing petal length 6-8 mm, wing petal width 3-5 mm, fruit length 16-18 mm, pods size far exceeding calyx, seed number 10-12, seed length 2-4 mm, pedicel length 3-5.5 mm, hairs present on the stem. Crotalaria pallida var. obovate (G. Don) Polhill Kew Bull, 22: 265 (1968) Type: Polhill number (BM, holotype) Shrub, annual, leaves 3-foliate; obovate, leaflet length 40-42 mm, leaflet width 23-25 mm, petiole length 38-40 mm, inflorescence terminal or axial with many flowers, calyx length 4-6 mm, standard petal length 7-9 mm, standard petal width 6-8 mm, wing petal length 7-9 mm, wing petal width 57 mm, fruit length 20-22 mm, pods far exceeding calyx, number of seed 12, seed length 1-2 mm, pedicel length 1-3 mm, hairs present on the stem 2 mm, length of pedicel 2 mm, hair presence. Crotalaria pallida Aiton Hortus Kewensis 3:20-21 (1789) Type: James Bruce s.n (BM, holotype) Shrub, annual, leaves 3-foliate; elliptic, leaflet length 40-42 mm, leaflet width 23-25 mm, petiole length 3840 mm, inflorescence terminal or axial with many flowers, calyx length 4-6 mm, standard petal length 7-9 mm, standard petal width 6-8 mm, wing petal length 7-9 mm, wing petal width 57 mm, fruit length 20-22 mm, pods far exceeding calyx, number of seed 12, seed length 1-2 mm, pedicel length 1-3 mm, hair present on the stem 2 mm, length of pedicel 2 mm, hair presence. Crotalaria retusa L. Species Plantarum 2:715 (1753) Type: Herman 84 (BM, lectotype) Shrub, perennial, leaves simple, cuneate, leaflet length 50-52 mm, leaflet width 12-14 mm, length of petiole 3-5 mm, inflorescence terminal with many flowers, calyx length 8-10 mm, standard petal length 12-14 mm, standard petal width 9-11 mm, wing petal length 12-14 mm, wing petal width 5-7 mm, fruit length 33-35 mm, pods far exceeding calyx, seed number 1416, seed length 2-4 mm, pedicel length 6-8 mm, hair absent. 4. Discussion The following representatives of Crotalaria were found during field work and included in this study: C. senegalensis, C. goreensis, C. retusa, C. pallida, C. macrocalyx, C. pallida var. obovata, C. atrorubens and C. barkae. Odewo et al. (2015) in their study on ecological distribution of the genus Crotalaria in Nigeria reported only two species from Katsina – C. naragutensis and C. ononoides. However, C. ononoidesis has not been found in this study; a species morphologically resembling Crotalaria naragutensis, i.e., Crotalaria pallida and 7 other species were reported from Katsina. Chromosome counts and cytomorphological studies of Crotalaria from Northern Nigeria conducted by Adelanwa et al. (2014) reported nine species. C. ononoides reported by Odewo et al. (2015) was wrongly identified. The specimens were not C. ononoides, because morphometric analysis showed that morphological features of these specimens did not match the type specimen of C. ononoides. For example, the leaf shape of the species in question is spatulate, while that of C. ononoides is lanceolate to elliptic or obovate. The species 3-foliate leaves are unequal in size, while that of C. ononoides are equal in size. The length of the fruit is 8 mm, while for C. ononoides is 12mm. The discussed species was correctly identified as C. atrorubens. Britto et al. (2011) reported that phenetics proves its robustness in identifying species similarity, instead of relying on few vegetative characters, which creates a great confusion in identifying species. One of accepted infrageneric classification systems of the genus Crotalaria was based on morphometrics (Bisby 1973; Bisby & Polhill 1973). Morphological characters, both vegetative and generative, were used for constructing classifications (Agyeno et al. 2014a). Similarly, Jayeola (2001) reported the efficiency of utilizing vegetative and floral parts in numerical evaluation of similarities among taxa. Agyeno et al. (2014b) reported that morphology of leaf, habit and life span played a very important role in delimiting members of the genus Crotalaria due to their discontinuity or discreteness. Findings of this study agreed with his findings, because leaf morphology is the character that showed a great variation among the sampled species in this study. The study of Raj et al. (2011) also highlighted that qualitative characters, such as habit and leaf type, and quantitative characters, such as the pod length, seed number and petiole length, are phylogenetically important. Findings of this study also prove that morphological characters are effective in showing similarities among the species within the studied genus. This study considered some characters, such as petiole length, which were not reported earlier, and these characters were found to be effective in morphometric analysis of the genus. 31 32 Samaila Samaila Yaradua et al. Numerical taxonomic study of the genus Crotalaria L. (Crotalarieae, Fabaceae) in Nigeria References adelanwa m. a., hussaini s. w. a., Falusi o. a. & awulu e. a. 2014. Chromosome counts and cytomorphological studies of nine species of Crotalaria (Linn) from Northern Nigeria. International Journal of Biological Research 6(1): 95-102. agyeno o. e. & azzuwut P. A 2014a. 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