448 S.AfrJ.Bot., 1992,58(6): 448 - 455 Fruit polymorphism in ephemeral species of Namaqualand. I. Anatomical differences between polymorphic diaspores of two Dimorphotheca species

Karen Beneke,* Irmgard von Teichman,t Margaretha W. van Rooyen * and G.K. Theron* "Grassland Research Centre, Private Bag X05, Lynn East, 0039 Republic of South Africa tMargaretha Mes Institute for Seed Research, Department of Botany, University of Pretoria, Pretoria, 0002 Republic of South Africa *Department of Botany, University of Pretoria, Pretoria, 0002 Republic of South Africa

Received 25 November 1991; revised 20 June 1992

Differences in germination behaviour between different diaspore types of Dimorphotheca sinuata DC. and Dimorphotheca polyptera DC. induced the morphological study of the above-mentioned species. The study reveals that the difference between the diaspore types lies in the structure of the pericarp. Pericarp characteristics such as presence of mucilage, tanniniferous substances and cuticles as well as extensive sclerenchymatous zones, are associated with those diaspore types with the poorest germination. Fruit polymorphism represents a survival strategy in these species from the arid Namaqualand.

Verskille in ontkiemingsgedrag tussen die verskillende diaspoortipes van Dimorphotheca sinuata DC. en Dimorphotheca po/yptera DC. het aanleiding gegee tot die moriologiese ondersoek van die verskillende diaspoortipes. Die studie het getoon dat die belangrikste verskille tussen die diaspoortipes in die perikarp­ struktuur voorkom. Perikarpkenmerke soos aanwesigheid van slym, tannienagtige stowwe en kutikulas sowel as goed-ontwikkelde sklerenchiemstreke is geassosieer met diaspoortipes wat die swakste ontkiem het. Vrugpolimorfisme verteenwoordig 'n oorlewingstrategie in hierdie spesies van die dorre Namakwaland.

Keywords: Arid environment, Asteraceae, Dimorphotheca sinuata, Dimorphotheca polyptera, Namaqualand.

*To whom correspondence should be addressed.

Introduction Namaqualand. This arid region in South Africa has a The Asteraceae (Compositae) is a large, cosmopolitan minimum and maximum rainfall of 43.8 mm and 996.9 mm, family of about 900 - 950 genera and 17 000 - 20 000 respectively, with an average annual rainfall of 162 mm species (Dyer 1975; Bailey & Bailey 1978). Fruit polymor­ falling mainly in winter, and an average annual temperature phism is a typical feature of many members of this family of 17.7°C measured at Okiep (Weather Bureau 1988). (Bachmann et al. 1984). Disc achenes, borne in the centre of Climatic conditions may vary greatly from one year to the capitulum, are produced by the disc florets and in many another and plants growing under different environmental instances can easily be distinguished from the ray achenes, conditions differ in their appearance, for example, inflores­ produced by the ray florets, on the margin of the capitulum. cence colour and size, plant size and achene colour and size, The details of this phenomenon differ greatly between while the ratio of the diaspore types which are produced species. The distinguishing characteristics may be achene depends on environmental conditions during maturation. size, shape, colour, structure of the fruit wall, presence or There may thus be structural differences within the same structure of the pappus and physiological features (Bach­ species between fruit morphs collected in different years and mann et al. 1984). Polymorphism greatly enhances the abil­ at different localities. ity of a species to survive in highly variable environments This study forms part of a project investigating the eco­ (Stebbins 1974). logical significance of polymorphism in four polymorphic Different seed morphs usually differ in germination species of Namaqualand (see Beneke et al. 1992a-f). Being behaviour (Beneke et al. 1992b) and competitive perform­ primarily an anatomical study, the reader is referred to ance (Beneke et al. 1992e). Venable and Levin (1985) found Reese (1989) for a complete and updated review of previous that the behaviour exhibited by the two diaspore types is the studies concerning pericarp and/or seed coat anatomy of the result of basic structural differences between the two types. Asteraceae. The term diaspore is preferred in this study Pericarp structure or anatomy may be, in part, responsible since the achene is seen as an ecological dispersal unit. for the different germination responses of ray and disc dia­ spores. The pericarp may influence germination by physical­ Materials and Methods ly impeding germination, blocking diffusion of gasses, pre­ Achenes were collected in the Goegap Nature Reserve. The venting the imbibition of water or containing chemicals that reserve is situated approximately 12 km east of Springbok, inhibit germination (Tanowitz et al. 1987). The main between 17°55' and 18°08' East and 29°34' and 29°43' purpose of this paper is to examine the anatomical differ­ South. ences between the fruit morphs and to trace the structural Transverse sections of disc and ray diaspores of Dimor­ adaptations which have evolved in order to explain the photheca sinuata and D. polyptera DC. were examined with functional importance of polymorphism in two species from a light microscope. S.Afr.J.Bot., 1992,58(6) 449

To improve the infiltration, one third of the achene was embryo. The cell walls are thickened and mainly composed removed. Transverse sections were cut from the central of mannose. The embryo has two well-developed cotyle­ portion of the mature achene. The material was fixed in dons, a hypocotyl, an epicotyl and a minute radicle. Nutrient 2.5% glutaraldehyde in a 0.1 mol dm-3 buffer, consisting of reserves, comprising mainly fats and proteins, are stored in Na2HP04 and NaH2P04 (Coetzee & Van der Merwe 1985). the endosperm remnants, the epidermis and thin-walled To fix the tannins, 0.5% caffeine was added to the fixative parenchyma of the cotyledons. Globoid crystals occur only (Mueller & Greenwood 1978). The material was dehydrated in the protein bodies of the embryo parenchyma cells. in 2-methoxyethanol, ethanol, n-propanol and n-butanol (Feder & O'Brien 1968), at room temperature and infiltrated Discussion with a monomer mixture consisting of 94% (v/v) hydroxy­ Asteraceae fruits are achenes, the seed develops from an ethyl methacrylate (commercially available - 94% HEMA anatropous, unitegmic, tenuinucellate ovule, the inner purified in our laboratory to remove most of the methacrylic acid); 5% (v/v) polyethylene glycol 200 and 0.6% (w/v) epidennis of the integument often being differentiated into benzoyl peroxide. Embedding was done in fresh monomer an endothelium (Netolitzky 1926; Comer 1976; Pandey & mixture at 60°C for 24 h. Sections, 2 - 4 J.Lm thick, were Singh 1982). In the case of D. sinuata, the percentage cut on a Porter Blum MT-l ultramicrotome. The 'Periodic germination is higher in the disc diaspore than in the ray Acid-Schiff Reaction' (PAS) was used (Feder & O'Brien diaspore (Beneke et at. 1992b). The anatomical difference 1968). Sections were counterstained for about 3 min in between the disc and ray diaspores of D. sinuata lies in the 0.05% toluidine blue a in a benzoate buffer, pH 4.4 structure of the pericarp. (Sidman et at. 1961). Other sections were treated as follows: The epidennis, hypodermis and cells with lignified walls (i) To test for cutin, a saturated solution of Sudan black B in of the ray diaspore are filled with tanniniferous substances 70% ethanol for 10 min was used. The sections were mount­ which may inhibit the germination of the diaspores, serve as ed in liquefied glycerine jelly. (ii) Staining for proteins in a protective screen against excessive insolation or as a amido black lOB was done according to Bullock el at. chemical protection of the seed. The sclerenchymatous zone (1980). (iii) Crystals were observed in unstained sections in the pericarp of the ray diaspore is lignified to a greater under crossed polarizing filters. extent than that of the disc diaspore, thus fonning a stronger mechanical layer. Results The pericarp anatomy of the ray diaspore described here The shape of the diaspores is described using the termi­ is more or less in accordance with that described by Reese nology proposed by the Systematics Association Committee (1989). Reese (1989) described the exocarp of D. sinuala as for Descriptive Biological Terminology (1962). being papil-like. However, the exocarp structure of the disc In all the following descriptions the position of the diaspore, as well as its general shape (Figure 2C), differs vascular bundles in the pericarp and seed coat in relation to from the description of D. sinuata by Reese (1989). We the cotyledons is described according to Bruhl (1984) in certainly agree with Reese (1989) in the interpretation of the Short et at. (1989). 'The terms lateral, medial and oblique pericarp, i.e. that the outer and inner epidennis of the ovary are used to indicate these relations. In fruit with lateral wall develop to fonn the exocarp s. str. and endocarp s. Sir., vascular bundles the bundles occur in the plane of the upper respectively. Therefore, the mesocarp s. str. comprises all surface of the cotyledons. In fruit with medial vascular the cell layers lying between these two epidennallayers. bundles the bundles are opposite the lower surface of the The external morphology as well as the pericarp structure cotyledons. If the position is intennediate between lateral of D. sinuata fruit from Namaqualand are very similar to and medial then the bundles are considered to be oblique' that of D. sinuata fruit from Lucknow (India), described by (Figure 1). Pandey & Singh (1978). The mucilaginous epidennis of the ray diaspore may con­ Dimorphotheca sinuata tribute towards keeping the diaspore moist for a longer A comparison between the shape and anatomy of the disc period, thus ensuring successful germination. Fahn (1990) and ray diaspores of D. SinIlLlta is shown in Table 1. stressed the importance of mucilage in the epidennal cell Remains of the endospenn of both the disc and ray dia­ walls of leaves and seeds as an adaptive strategy in the spores consist of one layer of cells. According to Grau and water economy of xerophytes. According to Roth (1977), Hopf (1985), in all tribes of the Asteraceae an endospenn of mucilaginous cells are characteristic of the achene of many one to three cell layers, consisting of living cells rich in taxa within the Asteraceae. proteins and fatty oils but without starch, envelops the In the Asteraceae the exotesta shows great anatomical diversity, including lignification, a palisade-like structure and cells with a linea tucida (Netolitzky 1926; Comer 1976; Grau 1980; Reese 1989). On the other hand the inner epi­ dermis (or endotesta) is also differentiated as a mechanical layer in many mature seeds. Gerdts (1905) showed that the obliteration of the central layers of the seed coat proceeds A B c from the inner layers centrifugally, while the inner epi­ Figure 1 The position of the vascular bundles in the pericarp in dermis of the seed coat may be persistent as, for example, in relation to the cotyledons. A, lateral; B, medial; C, oblique (Bruhl species of Buphthatmum. The seed coat of both the disc and (1984) in Short et al. 1989). ray diaspores of D. sinuata is weakly developed, since the 450 S.-Afr.Tydskr.Plantk., 1992, 58(6)

Table 1 An anatomical comparison between the two diaspore types of Dimorphotheca sinuata

Characteristic Disc diaspore Ray diaspore

1. Shape obovate, winged obtriangular, unwinged no ridges peri carp ridges (Figures 2A&B) (Figures 2D&E) 2. Pericarp (a) Epidennis thin-walled, rectangular or large, pappilate cells transversely elongated cells tanniniferous substances outer and inner tangential cell walls mucilaginous thickened (Figure 2F) (Figure 2C) (b) Hypodermis thin-walled parenchyma thin-walled parenchyma ::': 3 cell layers ::': 2 cell layers (Figure 2C) tanniniferous substances (Figure 2F) (c )Sclerenchymatous zone (i) outer thickened and lignified thickened and lignified tanniniferous substances (ii) inner weak! y lignified cells brachysclereids sclereids fibres fibres (Figure 2F) (Figure 2C) (d) Endocarp Squashed parenchyma Squashed parenchyma (Figure 2C) (Figure 2F) (e) Vascular bundles 2 bundles 3 major bundles, slightly oblique 2 oblique, 1 lateral (Figure 2B) Several minor bundles (Figure 2E) 3. Air space Continous, between pericarp Continuous, between pericarp and seed and seed 4. Seed coat (a) Outer epidermis thin, lignified cell walls thin, lignified, collapsed thin cuticle cell walls inner tangential cell walls lignified thin cuticle (Figure 2C) (Figure 2F) (b) Inner epidermis Distinct cuticle Inner tangential cell walls slightly thickened thin cuticle (c) Vascular bundles 2 bundles 2 bundles slightly oblique lateral (Figure 2B) (Figure 2E)

pericarp has taken over the main protective function. Reese the endospenn is reported. (1989) reported no secondary strengthening (i .e. thickening In all species examined, proteins and fats are stored in the or lignification) of the outer epidennis in the seed coat of D. embryo parenchyma and endospenn remnants. These results sinuata. Both the outer and the inner epidermis of the seed comply with those of Netolitzky (1926) and Roth (1977) coat are covered by a cuticle. who seldom found starch in the seeds of the Asteraceae. In Dimorphotheca sinuata and all other Compositae dia­ Proteins and fats are high energy nutrient reserves, which spores investigated, the seeds are exalbuminous, since only provide the genninating embryo and young seedling with endosperm remnants are present. sufficient energy to establish and survive in an unpredictable Netolitzky (1926) also reported that only one or two cell environment. The embryo in all fruit types has very similar layers of the endosperm persist, the cell walls being compact protein bodies. These are characterized by the presence of and capable of swelling. The latter might explain the promi­ numerous small globoid crystals embedded in the proteina­ nent appearance of the endosperm cell walls in the seeds ceous matrix and the absence of protein crystalloids. This studied presently. Comer (1976) mentioned that the initial supports the findings of Buttrose and Lott (1978), who endosperm development in the Asteraceae is cellular or found these globoid crystals to be phytin-rich, and consider­ nuclear and that the endosperm may be persistent or not in ed this type of protein body possibly being characteristic of the mature seed. In more recent, ontogenetic studies, e.g. by the family. Pandey and Singh (1982), the persistence of two layers of The ray diaspores represent a 'cautious' or low-risk S.AfrJ.Bot., 1992, 58(6) 451

D

B

Figure 2 The two diaspore types of Dimorphotheca sinuata. A, The external morphology of the disc diaspore; B, transverse section of the disc diaspore; C, detail of the pericarp and embryo of the disc diaspore; D, the external morphology of the ray diaspore; E, transverse section of the ray diaspore; and F, detail of the pericarp of the ray diaspore. as, air space; cot, cotyledons; endot, endotesta; es, endosperm; exo, exocarp; exot, exotesta; isz, inner sclerenchymatous zone; osz, outer scIerenchymatous zone; phI, parenchymatous hypodermal layers; pvb, pericarp vascular bundle; svb, seed vascular bundle; large arrow shows the well-developed cuticle, and the small black arrow the less-developed cuticle. Scale bars in A: 1.0 mm, C: 40 j.Lm, D: 1.1 mm, and F: 100 j.Lm. strategy, in which the pericarp structure delays germination Dimorphotheca polyptera and spreads the dormant period over a longer time to avoid A comparison between the shape and anatomy of the disc, disastrous conditions. Disc achenes with their weaker winged-ray and unwinged-ray diaspores of D. polyptera is developed pericarp are capable of high rates of germination shown in Table 2. under favourable conditions (Venable & Levin 1985). The endosperm remnants as well as the nutrient reserves 452 S.-Afr.Tyds1cr.Plantk., 1992,58(6)

Table 2 An anatomical comparison between the three diaspore types of Dimorphothecapo/yptera

Characteristic Disc diaspore Winged-ray diaspore Unwinged-ray diaspore

1. Shape obovate o btriangular obtriangular 2 wings 3 wings unwinged (Figures 3A&B) (Figures 3D&E) (Figures 4A&B) 2. Pericarp (a) Epidennis flattened or compressed protuberances protuberances (Figure 3C) papillate outer tangential cell walls outer tangential cell walls are mucilaginous are mucilaginous transversely elongated cells (Figure 3F) thin cuticle tarminiferous su bstances (Figure 4C) (b) Hypodermis parenchymatous thickened and lignified thickened and lignified (Figure 3C) part of sclerenchymatous zone tarminiferous su bstances (Figure 3F) (Figure 4C) (c) Sclerenchymatous zone (i) outer slightly thickened thickened and lignified lignified, radially elongated cells and lignified tanniniferous substances macrosclereids with pitted (Figure 3C) (Figure 3F) cell walls (Figure 4C) (ii) inner sclereids :!: 3 layers of fibres :!: 6 layers of fibres (Figure 3C) (Figure 3C) (Figure 4C) (d) Endocarp squashed parenchyma squashed parenchyma squashed parenchyma (Figure 3C) (Figure 3C) (e) Vascular bundles 2 major bundles, oblique 3 major bundles, 10 bundles varying in size 2 minor bundles 2 oblique, 1 lateral (Figure 4B) (Figure 3B) several minor bundles (Figure 3E) 3. Air space between pericarp and seed continuous, between outer in the centre of protuberances near vascular bundles epidermis and hypodermis of epidermis of pericarp (Figure 3B) of pericarp (Figure 4B) continuous, between peri carp and seed (Figures 3B&C) 4. Seed coat (a) Outer epidennis compressed cells compressed cells compressed cells outer tangential cell walls outer tangential cell walls cell walls slightly thickened thickened and lignified thickened and lignified and lignified thin cuticle thin cuticle (b) Inner epidennis Remnants of lignified inner tangential cell walls inner tangential cell walls inner tangential cell walls thickened and lignified thickened well-developed cuticle cuticle well-developed cuticle (c) Vascular bundles 2 bundles, lateral 2 bundles, lateral 2 bundles, lateral (Figure 3B) (Figure 3E) (Figure 4B)

in the cotyledons are similar to those described for D. has a high percentage germination and differs from the un­ sinuala. winged-ray diaspores in the following respects: (i) absence of tannin-like substances in the epidermis and hypodermis; Discussion (ii) absence of both the above-mentioned cuticles, and (iii) a Comparing the anatomy of these three diaspore types of D. rather narrow sclerenchymatous cylinder. The winged-ray poiyplera might explain the differences in germination diaspore is an intermediate form with regard to germination behaviour (Beneke el ai. 1992b). Factors possibly contrib­ as well as anatomical features. uting towards the poor germination of the unwinged-ray diaspore are the following: (i) presence of tannin-like sub­ Conclusions stances in the mucilaginous outer epidermis (exocarp) and The main differences between the diaspore types of both D. the hypodermis; (ii) a cuticle on this exocarp and a well­ sinuala and D. poiyplera are found in the pericarp, and to a developed cuticle on the inner surface of the inner epidermis lesser extent in the seed coat structure. A mucilaginous outer of the seed coat; and (iii) a very thick sclerenchymatous epidermis (exocarp), the extent of thickening and lignifica­ cylinder in the pericarp. On the other hand, the disc diaspore tion, the abundance of tanniniferous substances, the de- S.Afr.J.Bot., 1992, 58(6) 453

Figure 3 Two of the diaspore types of Dirnorphotheca polyptera. A, the external morphology of the disc diaspore; B, transverse section of the disc diaspore; C, detail of the pericarp and embryo of the disc diaspore; D, the external morphology of the winged-ray diaspore; E, transverse section of the winged-ray diaspore; F, detail of the pericarp and seed coat shown in E. Except for the following, the abbre­ viations are as in Figure 2: ph, parenchymatous hypodermis; pro, protuberances, and sh, sclerenchymatous hypodermis. Scale bars in A: 1.1 mm, C: 30 /-Lm, D: 1.1 mm and F: 50 /-Lm. velopment of the sclerenchymatous zone, as well as the disc diaspores, which show a high germination percentage number and thickness of the cuticles, influence the germina­ (Beneke et al. 1992b) under favourable conditions, are tion percentages of the different diaspores and may also responsible for the relative abundance and the range exten­ have some physiological implications. Polymorphism in the sion of the species, on the other hand the ray diaspores, with two Dimorphotheca species from Namaqualand is important delayed germination, protect the species against unpredict­ since it provides a two-way strategy: on the one hand the able, disastrous conditions. 454 S.-Afr.Tydskr.Plantk., 1992, 58(6)

Unit of the University of Pretoria, for the use of their A facilities.

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