INTRODUCTION
Family Boraginaceae Juss. is one of the widely distributed families. It has about one hundred genera and more than two thousand species distributed allover the world (Heywood, 1978). Members of the family have great variations in their morphological characters. They are trees, shrubs or lianas, annuals or perennials lacking essential oils. They are also inhabit different habitats, mountains, wadyes or even disturbed habitats. Stems and leaves of the Boraginaceae characterized by the presence of hairs on their surfaces which may be glandular or eglandular (Metcalf and Chalk, 1979). The density of these hairs may be varied in the different habitats. Few taxa have glabrous leaves and this encouraged Hutchinson (1948) to isolate them in another new family Ehretiaceae. Family Boraginaceae had drawn the attention of many taxonomists since long time ago. Hallier (1912), Bessey (1915, Brand (1921), Lawrence (1963), Chopra (1971), Khalifa and Hamed (1982), Al-Nowaihi et al. (1987), Taia and Shiha (1999) are ones from those who gave great attention to the systematics of the family. According to the ovary, entire or lobed, genera of the Boraginaceae has been divided into four subfamilies. These subfamilies have been faced with many taxonomic opinions since long time ago. Svensson (1925), Pal (1963) and Di Fulvio (1978) transfer the three subfamilies Heliotropoideae (Schrad.) Arn., Cordioideae (R.Br.) Lindl. And Ehretioideae (Mart. Ex Lindl.) Arn. and gathered them in a separate family Heliotropiaceae. This conclusion has been supported by Hilger (1989), Ferguson (1999) and Diane et al. (2002) on the basis of both fruit and flower development as well as molecular analysis data. The taxonomic status of the family according to different systems of classifications are listed in Table 1, while the main divisions of the family and their characters (Heywood, 1978) as well as the genera studied are listed in Table 2.
This study concerns with the variations in hair characters and density within 66 species distributed over 20 genus collected mainly from deferent habitats in Saudi Arabia. The aims of the study are to investigate how much these characters can affect the delimitation of the taxa and to determine whether they can reinforce the generic boundaries and clarify the evolutionary line between the taxa or not. The study based on both light and scanning electron microscopes, as well as vegetative examinations.
MATERIALS AND METHODS
Materials of the studied taxa and their locations are listed in Table
3. Leaves of the 66 species are collected either from field trips or from
herbarium specimens allocated at the ministry of agriculture and water resources
herbarium in El-Riyadh city. At least five specimens, from each species examined
by the stereomicroscope firstly, before subjecting to softening. Chosen parts
of the leaves were boiled softly in 10% nitric acid until the epidermises could
be removed. Then both the abaxial and adaxial ones were examined by light microscope.
Dry leaves from most of the taxa studied were mounted onto clean stubs and coated
with gold and examined by JEOL T-20 scanning electron microscope allocated at
Alexandria University.
| Table 1: |
Systematic position of family Boraginaceae in the different
systems of classification |
|
|
| Table 2: |
Taxonomic division of family Boraginaceae (Heywood, 1998) |
|
|
| Table 3: |
Studied taxa and their distribution in Saudi Arabia |
|
|
| species not recorded in the flora of Saudi Arabia (Migahid,
1996), **Species not recorded in the flora of Saudi Arabia (Migahid, 1996)
but recorded by Zohary (1957) |
Terminology used here are that of Al-Shammary and Gornall (1994).
RESULTS
The results obtained are summarized in Table 4 and illustrated
in Fig. 1-56. From Table
4 we can notice that the genera Ehretia (Fig. 54),
Paracaryum boissieri and P.intermedium (Fig. 56)
are the only ones with glabrous leaves while the rest of the genera are either
hairy or even woolly with deferent hair lengths. No variations in the density
of hairs have been noticed between both the abaxial and adaxial surfaces. Few
species only which are sparsely hairy, Arnebia linearifolia, A. tetrastigma
(Fig. 41 and 42), Cordia abyssinica
(Fig. 55), C. africana (Fig. 52),
C. myxa (Fig. 24), Echium horridum (Fig.
20), Lappula sinaica (Fig. 43), Trichodesma
africana (Fig. 9) and T. ehrenbergii (Fig.
39). Few species have adpressed hairs, Echiochilon sp. (Fig.
15 and 16), Gastrcotyle hispida (Fig.
46), Heliotopium crispum (Fig. 30), H. kotschi
(Fig. 31), H. lasiocarpum (Fig. 45),
H. lignosum, H. ramosissimum (Fig. 19),
H. ramiflorum (Fig. 13), H. strigosum (Fig.
47), Lapula sinaica (Fig. 43) and Ogastemma
pusillum (Fig. 18). Most of the species have distributed
hairs allover the lamina except Arnebia tetrastigma (Fig.
42), Brandella erythraea (Fig. 22), Cordia
africana (Fig. 52), C. myxa (Fig.
24), C. ovalis (Fig. 53), Heliotropium curassavicum
(Fig. 49) and Ogastema pusillum (Fig.
18) in which the hairs are restricted to the midrib area only. The types
of hairs are mostly either unicellular pointed or multi-cellular pointed ones,
branched hairs founded with multi-cellular ones in Microparacaryum intermedium
only (Fig. 48).
| Table 4: |
Characters investigated in the studied taxa |
|
1-Hair presency: 1 = Absent, 2 = Present; 2-Hair density:
1 = Glabrous, 2 = Hairy, 3 = Densely hairy, 4 = Woolly, 5 = Sparse,
3-Hair direction: 1 = Glabrous, 2 = Pressed on the leaf surface, 3 = Erect;
4-Hair location 1 = Glabrous, 2 = Restricted to the midrib,
3 = Throughout the lamina; 5-Hair type: 1 = Absent, 2 = Multi-cellular
pointed, 3 = Both, branched and pointed, 4 = Unicellular pointed;
6-Basal stalk cell(s): 1 = Glabrous, 2 = One enlarged cell, 3 = Many-celled,
one layer, 4 = Many-celled, two layers 5 = Absent;
7-Hair wall: 1 = Glabrous, 2 = Granulate, 3 = Echinate, 4 = Scaly 5 =
Smooth; 8-Figure number
|
|
|
| Fig. 1: |
Anchusa milleri Willd |
|
| Fig. 2: |
Arnebia decumbens (Vent.) Coss & Karl. |
|
| Fig. 3: |
Arnebia hispidissima (Lehm.)DC. |
|
| Fig. 4: |
Echium plantagineum Del. |
|
| Fig. 5: |
Echium longifolium Del. |
|
| Fig. 6: |
Paracaryum regulosum L. |
|
| Fig. 7: |
Paracaryum regulosum L. |
|
| Fig. 8: |
Alkana orientalis (L.) Boiss. |
|
| Fig. 9: |
Trichodesma africanum (L.) R.Br. |
|
| Fig. 10: |
Paracynoglossum bottae DC. |
|
| Fig. 11: |
Heterocaryum subsessile Varke |
|
| Fig. 12: |
Lappula spinocarpos (Forssk.) Asch.ex Ktze. |
|
| Fig. 13: |
Heliotropium ramiflorum Del. |
|
| Fig. 14: |
Heliotropium supinum L. |
|
| Fig. 15: |
Echiochilon kotschyi Bunge. |
|
| Fig. 16: |
Echiochilon propersicum Burm.F. |
|
| Fig. 17: |
Molkiopsis ciliata (Forssk.) Johnst. |
|
| Fig. 18: |
Ogastemma pusillum Boiss. |
|
| Fig. 19: |
Heliotropium ramosissimum (Lehm.) Siebu ex DC. |
|
| Fig. 20: |
Echium horridum Batt. |
|
| Fig. 21: |
Buglossoides arvensis (L.) I.M.Johson |
|
| Fig. 22: |
Brandella erythraea L. |
|
| Fig. 23: |
Arnebia asperrima L. |
|
| Fig. 25: |
Heliotropium pterocarpum Hochst. |
|
| Fig. 26: |
Heliotropium caleareum Forssk.* |
|
| Fig. 27: |
Heliotropium arbainense Fres. |
|
| Fig. 28: |
Helioltropium cinerascens Steud. |
|
| Fig. 29: |
Heliotropium battae |
|
| Fig. 30: |
Heliotropium crispum L. |
|
| Fig. 31: |
Heliotropium kotschyi (Bunge) Gurke |
|
| Fig. 32: |
Heliotropium bacciferum Forssk. |
|
| Fig. 33: |
Heliotropium Longiflorum (A.DC.) Steud et Hochst. |
|
| Fig. 34: |
Heliotropium europaeum L. |
|
| Fig. 35: |
Heliotropium pallens Del. |
|
| Fig. 36: |
Heliotropium hirsutissimum Grauer |
|
| Fig. 37: |
Echium sericeum L. |
|
| Fig. 38: |
Buglossoides tenuiflora L. |
|
| Fig. 39: |
Trichodesma ehrenbergii Schweinf. |
|
| Fig. 40: |
Cordia gharaf Forssk. Ehrln.ex Asch. |
|
| Fig. 41: |
Arnebia linearifolia DC. |
|
| Fig. 42: |
Arnebia tetrastigma Forssk. |
|
| Fig. 43: |
Lappula sinaica (DC) Aschirs Schweif. |
|
| Fig. 44: |
Heliotropium digynum (Forssk.) Asch. |
|
| Fig. 45: |
Heliotropium lasiocarpum L. |
|
| Fig. 46: |
Gastrocotyle hispida (Forssk.)Bunge |
|
| Fig. 47: |
Heliotropium strigosum Willd. |
|
| Fig. 48: |
Microparacaryum intermedium Boiss. |
|
| Fig. 49: |
Heliotropium curassavicum Steud.* |
|
| Fig. 50: |
Trichodesma pauciflorum Bak. |
|
| Fig. 51: |
Trichodesma trichodesmioides Boiss. |
|
| Fig. 52: |
Cordia africana L. |
|
| Fig. 53: |
Cordia ovalis L. |
|
| Fig. 54: |
Ehretia abyssinica R.Br.* |
|
| Fig. 55: |
Cordia abyssinica R.Br. |
|
| Fig. 56: |
Paracaryum intermedium (Forssk.)Lipsky |
The presence of basal cell(s), considered most important in delimiting the
taxa as most of the taxa have many, rosette-like, basal cells which are either
one row or in many rows. Few taxa have either one enlarged basal cell (Fig.
22, 25, 26, 32-35,
38 and 39) or the hairs are without any
differentiated basal cell. Hair walls are mostly covered with scales while echinate
hair walls are present in Arnebia asperma (Fig. 23),
A. hispidissima (Fig. 3), Cordia myxa (Fig.
24), Heliotropium pterocarpum (Fig. 25), H.
ramiflorum (Fig. 13), H. strigosum (Fig.
47) and Microparacaryum intermedium (Fig. 43).
Meanwhile few taxa have granulate or even smooth hair wall. Most of the taxa
studied have either needle-shaped or granulated wax deposits on their surfaces
and for that, we considerate as s common character in the family.
The characters studied are clustered in a similarity index dendrogram (Fig.
57) in order to evaluate them and to know the most correlated ones. From
this dendrogram we found that all the studied characters are grouped in two
categories. The first category comprise hair presence (1), hair location (4)
and both of them are closely relay on hair direction (3). These three characters
are tied together at similarity 95. The second group comprises hair type (5)
and basal cell (6) in one branch and hair density (2) and hair wall (7) in another
branch and all these four characters gathered at similarity index of 84. These
two categories met together at similarity index of 74.
All the taxa studied are clustered together in another dendrogram (Fig.
58) to examine the most correlated species according to hair characters.
From the resulted dendrogram, we found that all the taxa are divided into four
groups at similarity index of 84. The most evaluated characters in grouping
the taxa are hair presency (char.1), hair density (char. 2), basal cell(s) (char.
6) and hair wall (char. 7), respectively.
Group 1: This group characterizes by having glabrous leaves and has
the following species: Ehretia obtusifolia, Ehretia abyssinica,
Paracaryum boissieri and Paracaryum intermedium.
|
| Fig. 57: |
Dendrogram showing the similarity between the studied characters |
Group 2: This group characterizes by having densely hairy or even hairy leaves. The hairs are either without basal cell or with basal cells in one or two raws. This group is subdivided into two subgroups as follows:
Subgroup 2a: This subgroup has densely hairy leaves, with many-celled, one raw basal cells. The hairs have smooth walls. It includes Echium plantagineum, Alkana orientales, Anchusa aegyptiaca, Heliotropium supinum, Molkiopsis ciliata, Echium angustifolium, Heliotropium cinerascens, Heliotropium bacciferum, Heliotropium ramiflorum, Echiochilon propersicum, Echiochilon kotschi, Arnebia asperima, Arnebia hispidissima and Arenabia decumbens.
Subgroup 2b: This subgroup characterizes by having hairy or densely hairy leaves with either many-celled, two layered basal cells or without basal cells at all. The hairs have scaly walls. It is subdivided again into two categories the first (2b 1) has densely hairy leaves with many-celled, two layered basal cells and includes the following species: Echium hordium, Anchusa hispida, Anchusa milleri, Anchusa undulata, Echium rauwolfia, Lappula spinocarpus, hormuzakia aggregata, Paracaryum regulosum, Paracynoglossum bottae, Echium longifolium and Heterocaryum subsessile.
Subgroup (2b 2): has hairy leaves without distinct basal cell and includes the species Trichodesma africanum, Trichodesma ehrenbergii, Lappula sinaica, Arnebia linearifolia and Cordia abyssinica.
Group 3: has sparsely hairy leaves, with the hairs restricted around the midrib only. The hairs without distinct basal cell and have scaly walls. This group has the species Cordia africana, Arnebia tetrastigma, Cordia myxa, Buglossoides arvensis, Cordia gharaf, Brandella erythraea and Cordia ovalis.
Group 4: This group characterizes by having densely hairy or even woolly
leaves, with or without basal cells and either scaly, granulate or smooth walls.
It is subdivided into two subgroups as follows:
Subgroup 4a: With many-celled, one layered basal cells and either granulate or scaly walls. It gathers most of the Heliotropium species as follows: Heliotropium kotschi, H. strigosum, H. crispum, H. lignosum, H. caleareum, H. arabainense, H. battae, H. hirsutissimum, H. kassasi, H. pallens, H. europaeum and H. longiflorum.
|
| Fig. 58: |
Dendrogram showing the similarity between the studied taxa |
|
| Fig. 59: |
Diagram shows the line of evolution within the Boraginaceae.
According to hair characters |
Subgroup 4b: Without basal cell and the hairs have smooth walls. It gathers the rest of the Heliotropium species with another taxa as follows: Gastrocotyle hispida, Heliotropium hirsutissimum, Ogastema pusillum, Heliotropium lasiocarpum, Heliotropium ramosissimum, Buglossoides tenuiflora, Heliotropium pterocarpum, Echium sericeum, Trichodesma pauciflorum, Microparacaruym intermedium, Trichodesma zylanicum, Heliotropium digynum and Trichodesma trichodesmoides.
DISCUSSION
From the results obtained, we can notice that hair characters support the isolation of the genus Ehretia as proposed by Hutchinson (1948), as the species studied of this genus have glabrous leaves. Genera within the Boraginaceae are mostly hairy or even woolly, except Paracaryum which show close affinity to the genus Ehretia and met together in group 1. Group 3 has seven species, four of Cordia, one of Brandella and the other two species are of Arnebia and Buglossoides. This group gathers, mainly, species of subfamily Cordioideae with the exception of the latest two species. Meanwhile, group 4a has most of the Heliotropium species. This means that hair characters of the Heliotropium species have close affinity to each other and do not support the isolation of the three subfamilies Ehretioideae, Heliotropoideae and Cordioideae from the Boraginaceae and gather them in a single family as proposed by Svenson (1925), Pal (1963), Di Fulvio (1978), Hilger (1989), Ferguson (1999) and Diane et al. (2002). Meanwhile this data show that species of the genus Heliotropium can be isolated as a unique group. Group 4b collect the rest of the Heliotropium species with other species of subfamily Boraginoideae. Group 2, in spite of being divided into three categories, it does not differentiate between the Boraginoideae species as all the three categories have species from the five tribes. These mean that taxa within family Boraginaceae do not show any sharp variations in their hair characters, except those with glabrous leaves, Ehretioideae.
Endress (2004) mentioned that glabrous plants are more primitive than hairy
ones and within the hairy plants the simple, unicellular hairs considered less
advanced than the multi-cellular or branched hairs. According to our data, we
can postulate a line of evolution within the studied genera according to hair
characters. Thus, we can put group 1, with glabrous plants, in one end of the
line while the other end will be group 4a which characterize by densely hairy
or even woolly leaves, with multi-cellular hairs and multi-cellular and one-layered
basal cells and granulate or scaly hair walls. Accordingly, species separated
in family Ehretiaceae can be considered the less advanced ones while those within
subfamily Boraginoideae are the more advanced species (Fig. 59).
Within the Boraginoideae there are levels of evolution within the genera as
well. This conclusion, partly, coordinate with that obtained by Taia and Shiha
(1999) on the basis of pollen characters as they considered species of the Boraginoideae
the more advanced ones within the family. Meanwhile the data obtained supports
the taxomonic position of the family in a separate order. Boraginals as proposed
by Takhtajan (1974) and Dahlgren (1989) classifications (Table
1).