S.Afr.J. Bot., 1989,55(3): 321-331 321 What is primitive in Mesembryanthemaceae? An analysis of evolutionary polarity of character states

V. Bittrich* and M. Struck Institut fUr Allgemeine Botanik und Botanischer Garten der Universitat Hamburg, Ohnhorststr. 18, D-2000 Hamburg 52, West Germany

Accepted 16 November 1988

Characters of the family Mesembryanthemaceae are investigated with respect to their state (primitive or derived) within this family. Out-group comparison with the closely related family Aizoaceae s.str. (excl. Mesembryanthemaceae) is used mainly, along with some other criteria. A tabulated survey of the characters discussed is provided. By combination of all characters considered as primitive, a morphotype (,hypothetical ancestor') of the Mesembryanthemaceae can be constructed. It is shown that no extant taxon possesses all features of this morphotype, but that all have acquired a number of derived characters. The possibility of the meronectary being a further synapomorphy of the family is discussed. A new synapomorphy for the subfamily Mesembryanthemoideae, namely the absence of expanding sheets on the valves of the hygrochastic capsule, is provided. The fundamental splitting of the Mesembryanthemaceae in two monophyletic subfamilies (Mesembryanthemoideae and Ruschioideae) is further supported by the results.

Kenmerke van die familie Mesembryanthemaceae word, met betrekking tot hul toestand (primitief of afgelei) binne die familie, ondersoek. Buitegroep-vergelyking met die naverwante familie Aizoaceae s. str. (wat die Mesembryanthemaceae uitsluit) word hoofsaaklik, saam met ander kriteriums gebruik. 'n Getabuleerde oorsig van die kenmerke onder bespreking, word voorsien. Deur middel van 'n kombinasie van al die kenmerke wat as primitief beskou word, kan 'n morfotipe (hipotetiese voorouer) van die Mesembryanthemaceae gekonstrueer word. Daar word aangetoon dat geen lewende takson oor al die kenmerke van die morfotipe beskik nie, maar dat almal 'n aantal afgeleide kenmerke ontwikkel het. Die moontlikheid van meronektarie as 'n verdere sinapomorfiese kenmerk van die familie word bespreek. 'n Nuwe sinapomorfie van die subfamilie Mesembryanthemoideae, naamlik die afwesigheid van die uitspreidende plate van die higrochastiese kapsule, word voorsien. Die fundamentele verdeling van die Mesembryanthemaceae in twee monofiletiese subfamilies (Mesembryanthemoideae en Ruschioideae) word verder deur die resultate ondersteun.

Keywords: Aizoaceae, character states, Mesembryanthemaceae, morphotype, synapomorphies

*To whom correspondence should be addressed

Introduction Aizoon L., differ least from the Mesembryanthemaceae The Mesembryanthemaceae (130 genera with about and show the smallest patristic distance. This led Dinter 1 000 species), a family belonging to the Caryophyllales (1935) erroneously to regard Aizoanthemum as a 'trans­ (Centrospermae) are native to the deserts and semi­ itional taxon' between Aizoaceae s.stt. (excl. Mesem­ deserts of southern Africa. They form a natural mono­ bryanthemaceae) and Mesembryanthemaceae. phyletic group comprising two subfamilies Mesembryan­ The most important synapomorphy of the entire Aizo­ themoideae (= Aptenioideae) and Ruschioideae (incl. aceae S.str. is the epidermal bladder-cell idioblasts Caryotophoroideae and Hymenogynoideae; Bittrich (much enlarged cells with water-storing function). 1986; Bittrich & Hartmann 1988). As discussed Further evolution into homogeneous, more xeromorphic elsewhere (Bittrich 1986; Bittrich & Hartmann 1988) epidermis-types is well documented (e.g. Ihlenfeldt & these subfamilies are closely related to the Aizooideae, Hartmann 1982). Other possible synapomorphies such Sesuvioideae and Tetragonioideae. All five subfamilies as perigynous flowers, and hygrochastic capsules are form a monophyletic group and could be combined discussed elsewhere (see Bittrich 1986; Bittrich & under the name Aizoaceae S.str. (s.str. = excl. Mollugin­ Hartmann 1988). aceae). The composition of the Aizoaceae S.str. is shown The Mesembryanthemaceae are defined by the follow­ in Table 1. We would like to emphasize, however, that it ing synapomorphies: (petaloid) staminodes, the absence is of major importance to characterize monophyletic of a superior ovary, and possibly the well-formed valve groups, whereas their ranking remains open to some wings of the fruit (see below). The Aizoaceae S.str. subjectivity (unless the classification is strictly (excl. Mesembryanthemaceae) are characterized by the c1adistical). For methodological reasons, in the follow­ chromosome base number x=8 (7) (Mesembryanthema­ ing, the Mesembryanthemaceae and Aizoaceae S.str. ceae x=9) and the tepals, which are petaloid on the inner (excl. Mesembryanthemaceae) will be treated as (upper) side. These characters could be regarded as separate families (see Table 1). synapomorphies (Bittrich & Hartmann 1988), but the Undoubtedly, the genera of the Aizooideae, espec­ relationship between the subfamilies is not satisfactorily ially the genera Aizoanthemum Dinter ex Friedrich and settled (see below). All Aizoaceae S.str. produce 322 S.-Afr.Tydskr. Plantk., 1989,55(3)

Table 1 Composition of the Aizoaceae s.str. (for further discussion see Bittrich & Hartmann 1988)

Aizoaceae S.str. (= excl. Molluginaceae)

Aptenioideae = Mesembryanthemoideae Mesembryanthemaceae Ruschioideae ] Aizooideae Aizoaceae S.str. (excl. Tetragonioideae Mesembryanthemaceae) Sesuvioideae J

betalains as flower pigments (as do most centrospermous primitive. families). Muller (1909) already found differences in the As regards the relationship of the three subfamilies of type of calcium oxalate crystals: within the Mesembry­ the Aizoaceae s.str. (excl. Mesembryanthemaceae) two anthemaceae, raphid bundles occur, whereas druses are hypotheses should be considered. Either all three sub­ found within the Aizoaceae S.str. (excl. Mesem­ families form a single monophyletic group as suggested bryanthemaceae). As the question of the closest relative by the synapomorphies mentioned above (Bittrich 1986; of these families within the Centrosperms (i .e. the sister Bittrich & Hartmann 1988), or a monophyletic group group) is still not settled (contra Rodman et al. 1984; consisting of Aizooideae and Tetragonioideae (Hof­ Levin 1985; Bittrich & Hartmann 1988) one cannot yet mann 1973; Bittrich in press) represents the sister group decide which of these crystal types has to be considered of the Mesembryanthemaceae as suggested by the capsule type and the epicuticula of the seed coat (see below). In this case the Sesuvioideae would be the sister Tetragonioideae Sesuvioideae Aizooideae Mesembryanthemaceae group of the rest of the Aizoaceae S.str. (see Figure 1). This problem as well as the relationship within the monophyletic group Aizooideae/Tetragonioideae will be discussed at length elsewhere (Bittrich in press). So far, the question of primitive characters of the Mesembryanthemaceae has only rarely been discussed (Ihlenfeldt 1960; Bittrich 1986 for Mesembryanthe­ moideae). Therefore, this paper intends to amplify the knowledge in this field, which is essential for a further analysis of the phylogeny of this family. New results are included. A A number of characters will be examined with respect to their evolutionary polarity. Based on that survey, a list of the characters with their putative primitive (ancestral) and advanced (derived) states is given. By the combination of the primitive features the morpho­ type (sometimes called 'hypothetical ancestor', Nelson 1972; for discussion of terms see Hull 1979) of the Mesembryanthemaceae can be constructed. Tetragonioideae Sesuvioideae Aizooideae Mesembryanthemaceae Materials and Methods The basis of the present investigations is comprehensive data extracted from the available literature and other sources as well as from our studies of herbarium speci­ mens and living plants from the collection of the Mesem­ bryanthemaceae study group in Hamburg (West Germany) under the direction of Prof. H-D. Ihlenfeldt. Methods and criteria to determine primitive character

B states have been discussed extensively in a number of recent publications (e.g. Crisci & Stuessy 1980; Humphries & Funk 1984; Stevens 1980; Wiley 1980). Figure 1 Possible sister-group relationships in Aizoaceae For this determination, 'the out-group criterion is the S.str. inc\. Mesembryanthemaceae. A. Mesembryanthemaceae main criterion used by phylogeneticists' as Wiley (1980) are the sister-group to the rest of the Aizoaceae S.str. B. put it. The application of this criterion has been Mesembryanthemaceae and Aizooideaeffetragonioideae are thoroughly examined (e.g. Donoghue & Cantino 1984; sister-groups. Maddison et al. 1984; Wiley 1981). The most useful out- S.Afr.J. Bot., 1989, 55(3) 323

group for character comparison and evaluation is the suggests that herbaceous growth forms are primitive sister-group of the taxon under investigation. As within this family. Furthermore: most of the taxa mentioned above, the sister-group of the Mesembryan­ showing several other primitive characters within both themaceae is not defined unequivocally. Therefore, in subfamilies of Mesembryanthemaceae (Mesembryanthe­ cases with different character states in the two possible mum L., Cleretum, Dorotheanthus) are more or less sister-groups, an out-group comparison necessarily must herbaceous. Hence, the application of the criterion of lead to uncertain results. When an out-group character correlation gives further evidence for the comparison cannot be applied, additional criteria to primitiveness of herbaceous growth forms within the determine phylogenetic polarity may be employed. Mesembryanthemaceae. Their application, advantages, and drawbacks have been discussed thoroughly by Crisci & Stuessy (1980) and Epidermis Stevens (1980). A criterion of major importance is the Bladder-cell idioblasts concept of correlation, which was commonly employed by many workers (see Crisci & Stuessy 1980; Stevens An epidermis with water-storing bladder-cell idioblasts , 1980) and is also applied in the present investigation. is the synapomorphy of the entire Aizoaceae S.str. The criterion suggests that primitive states are correlated (Bittrich 1986; Bittrich & Hartmann 1988). Hence, this with some probability, so that they can be found more epidermis type is the primitive state within the Mesem­ probably in taxa showing other primitive features (as bryanthemaceae. The epidermis has been modified deduced from different criteria) than in those showing a phylogenetically in two different ways (Ihlenfeldt & greater number of advanced features. This presupposes Hartmann 1982; Jurgens 1985). In the first line, the that the primitive taxa belong to different early branches bladder-cell idioblasts are more and more reduced and of the group under investigation. The argument is even finally lost completely (Ihlenfeldt & Hartmann 1982; stronger if a character is functionally correlated with Ihlenfeldt & Jurgens 1982). In the second line, the outer another character with resolved evolutionary polarity cell walls of the idioblasts are progressively thickened, (see under Gynoecium: number of ovules and fruit often forming a 'second surface' [functionally inter­ type). Taxa found in the present study to show several preted as decrease of transpiration (Jurgens 1986) or as primitive features and therefore considered to be useful an exoskeleton (Ihlenfeldt 1985)]. They thus finally lose for the correlation criterion in Ruschioideae are their function as a recyclable water storage. The primarily Cleretum N.E. Br. and Delosperma N.E. Br., primitive state within the Mesembryanthemaceae is and to a lesser degree Dorotheanthus Schwantes. bladder-cell idioblasts with more or less thin outer cell walls (Jurgens 1986), which also occur in the Aizoaceae Results and Discussion S.str. (excl. Mesembryanthemaceae) (out-group Vegetative characters criterion) . Growth form Ihlenfeldt (1960) considers shrubs as primitive within the Stomata Mesembryanthemaceae, as woody growth forms are The Mesembryanthemaceae show three types of generally regarded to be most primitive in the Angio­ stomata: anomocytic, anisocytic, and paracytic. All sperms. However, it is not unlikely that within the three types may occur together (1), or anisocytic and Centrosperms, as 'in the monocots, woody forms have paracytic may be combined (2), or the paracytic type arisen secondarily (Cronquist 1981). This view is may occur alone (3) (Dupont 1968b). Within Aizoaceae supported by the widespread occurrence of anomalous S.str. (excl. Mesembryanthemaceae) only the first condi­ secondary thickening and of ferulic acid in un lignified tion is known. This is also true for the species with the cell walls (Hartley & Harris 1981) within the order primitive epidermal bladder-cell idiobiasts within the (Kubitzki pers. comm.; ferulic acid is a preliminary stage Mesembryanthemaceae. Not only an out-group compar­ in lignin synthesis, which may be accumulated in the ison with the Aizoaceae S.str. (excl. Mesembryanthe­ absence of lignification: this feature probably originated maceae) but also the correlation with the bladder-cell in ancestral herbaceous Centrosperms and is retained in idioblasts provide evidence for the primitiveness of the the modern groups). Both characters are also found in combined occurrence of all three types of stomata. The some monocots, though these show a different type of same arguments hold for the conclusion that non-sunken anomalous secondary thickening. Within the Aizoaceae stomata are more primitive than sunken ones. For the S.str. (excl . Mesembryanthemaceae) not only woody same reasons, parallelly adjusted stomata and those that shrublets but also herbaceous plants occur. Therefore, are transversely oriented to the long axis of an organ an out-group comparison with the Aizoaceae S.str. (excl . (Ihlenfeldt & Bittrich 1985; Butterfass 1987) are Mesembryanthemaceae) does not provide a definite advanced states. result for the polarity of this character in Mesembryan­ themaceae. Molluginaceae and Caryophyllaceae (con­ Leaves sidered as early branches within the Centrosperms) are Within the Mesembryanthemaceae, all transitions from nearly lacking shrubby growth forms. An out-group flat, weakly succulent to cylindrical, highly succulent comparison with these closely related families (which are leaves occur. Leaves with a higher succulence require a not necessarily the sister group) of the Aizoaceae S.str. higher level of organization with considerable changes in 324 S.-Afr. Tydskr. Plantk., 1989,55(3)

their construction: as shown by JUrgens (1986) the estab­ Their occurrence in both Mesembryanthemoideae and lishment of a central water-storing tissue with increasing Ruschioideae is regarded as a parallelism. succulence (in Mesembryanthemaceae and other families) is often connected with the reduction or Root modification of a primitive epidermal water-storing In several genera of the Mesembryanthemaceae tissue (in case of the Mesembryanthemaceae the markedly thickened storage roots are developed (e.g. bladder-cell idioblasts, see above). In Aizoaceae s.str. Phyllobolus N.E. Br., Fenestraria N.E. Br., Tricho­ either flat, weakly succulent or cylindrical, more diadema Schwantes, Herrea Schwantes). In the Aizo­ succulent leaves can be found. Therefore, the out-group aceae s.str. (excl. Mesembryanthemaceae) such a comparison is not easily applicable. The genera Aizoon specialization is wanting, except in Gunniopsis glabra and Aizoanthemum, however, which show the smallest (Luehm. ex Ewart) C. Gardner. As thickened storage patristic distance to the Mesembryanthemaceae, possess roots represent a higher level of organization and as they flat, slightly succulent leaves exclusively. Therefore, flat, are almost lacking in the Aizoaceae s.str. (excl . Mesem­ slightly succulent leaves (with primitive epidermal bryanthemaceae), roots without special storage function bladder-cell idioblasts, see above) are considered are supposed to be primitive within the Mesem­ bryanthemaceae. primitive within the Mesembryanthemaceae.

Seedlings Stem Generally, within the Mesembryanthemaceae the Anomalous secondary thickening weakly or markedly succulent cotyledons are broadly Anomalous secondary thickening is a widespread feature connate at the base and fully expanded. In the sister­ of the Centrosperms, even within the Caryophyllaceae group Aizoaceae s.str. (excl . Mesembryanthemaceae) and Molluginaceae (which are considered as early the mostly weakly succulent cotyledons are expanded at branches in the order because they still possess an tho­ most at an acute angle (Dupont 1968a). It is impossible cyanins, see Rodman et al. 1984). It is lacking only in the to ascertain which type of seedling is primitive in the probably derived families Portulacaceae, Didiereaceae, entire Aizoaceae s.str., as the question of the closest and Basellaceae. This provides evidence for the relative is still unsettled (see above). primitiveness of this feature within the Centrosperms As higher succulence requires a higher level of organi­ (contra Ehrendorfer 1976b). Anomalous secondary zation, and in Aizoaceae s.str. (excl. Mesembry­ thickening also occurs in a number of genera of the anthemaceae) nearly always weakly succulent cotyle­ Aizoaceae s.str. (excl. Mesembryanthemaceae) and in dons are found, the latter are considered primitive both subfamilies of the Mesembryanthemaceae. It also within Mesembryanthemaceae. occurs in at least some annual species, e.g. Mesembry­ anthemum clavatum L. Bolus and Synaptophyllum juttae Inflorescence N.E. Br. Gibson (1978) states that in Aizoaceae, normal Within the entire Aizoaceae s.str. (with the exception of secondary xylem is produced in inner wood, before Tetragonioideae) dichasial monotelic cymes are anomalies occur. Normal secondary thickening has, as common (e.g. Hofmann 1973; Troll & Weberling ]981). yet, exclusively been observed in Mesembryanthema­ Such inflorescences (closed thyrses) are also typical of ceae only in pedicels (above and below the bracts) (e.g. the anthocyanin-families Molluginaceae and Caryophyl­ Hartmann 1978). To answer the question of the polarity laceae which are considered as early branches of the of normal and anomalous secondary thickening in Centrosperms (Rodman et al. 1984). Therefore, it seems pedicels, further investigations are required. On the likely that this type is primitive within the order. basis of an out-group comparison, anomalous secondary A reduction of the cymes to lateral or terminal single thickening in stems and roots is considered primitive for flowers takes place in various groups of the Aizoaceae the Mesembryanthemaceae. s.str. (excl. Mesembryanthemaceae ) (e.g. Plinthus Fenzl emend. Verdoorn) and Mesembryanthemaceae (e.g. Cortex Brownanthus Schwantes, Conophytum N.E. Br., Psilo­ Apart from the typical leaf succulence, some Mesembry­ caulon N.E. Br.). In these cases some less-reduced anthemaceae occasionally show the development of a cymes may sometimes be found at the basal parts of the more or less succulent cortical tissue (e.g. Brownanthus stems (see Bittrich 1986 for Mesembryanthemoideae). Schwantes, Psilocaulon N.E. Br., Monilaria (Schwantes) The vegetative part is always monopodial (Troll & Schwantes, Ruschia Schwantes spp.). Within the Weberling 1981). With respect to the leaves within the Mesembryanthemoideae all but some advanced species inflorescences, a leafy (frondose) and a bracteose type show cortical bundles as well, whereas in Ruschioideae, can be distinguished in Mesembryanthemaceae (Bittrich these have only been found in some species of the & Hartmann 1988). Furthermore, bracteose inflores­ advanced genus Ruschia Schwantes (Bittrich 1986). In cences are found in the Sesuvioideae, but leafy ones in the Aizoaceae s.str. (excl. Mesembryanthemaceae) stem most Aizooideae (Hofmann 1973), except e.g. in succulence as well as cortical bundles are absent. Based Galenia africana L., and Gunniopsis tenuifolia Chinnock, on an out-group comparison it can be concluded that which are doubtless derived in this subfamily. An out­ both characters are derived in Mesembryanthemaceae. group comparison only shows a result if the Aizooideael S.Afr.1. Bot., 1989,55(3) 325

Tetragonioideae are considered as the sister group of the Androecium Mesembryanthemaceae (Figure 1b). In this case leafy The possession of (petaloid) staminodes presents the inflorescences would be primitive. With the application most important synapomorphy for the members of the of a tendency statement (Crisci & Stuessy 1980) that the Mesembryanthemaceae. In view of the absence of less-specialized character is regarded as primitive, one staminodes within Aizoaceae s.str. (excl. Mesembry­ gets the same result. anthemaceae) the polarity of the different details of this character complex cannot be evaluated by an out-group Generative organs comparison with the Aizoaceae s.str. Flower According to Ihlenfeldt (1960) three basic andr­ Description oecium-types can be distinguished: The flower of the Mesembryanthemaceae consists of a Type 1: Various transitional stages occur between the green perigon (,calyx'), which doubtless can be homolo­ inner fertile stamens and outer petaloid stam­ gized with the perigon of the Aizoaceae s.str. (excl. inodes. Mesembryanthemaceae). The numerous members of the Type 2: Beside the fertile stamens two types of stamin­ androecium originate by centrifugal dedoublement. The odes may be distinguished by their morphology outer members are always petaloid staminodes and partly by their colour. (,petals'). In several species, different types of stamin­ Type 3: The fertile stamens are clearly distinct from the odes may occur between the 'petals' and the fertile petaloid staminodes and other types of stamin­ members of the androecium (stamens). Below the base odes are absent. of the inner stamens a nectary is usually differentiated. Ihlenfeldt (1960) argues that type 1 - as the least­ In Mesembryanthemoideae the flower is mostly weakly specialized condition - may be considered primitive and perigynous (gynoecium half-inferior, rarely inferior), clearly shows the origin of the petaloid staminodes. but it is epigynous in Ruschioideae. The styles are Furthermore, Ihlenfeldt (1960) assumes that type 3 is usually free from the base. The placentation is axile more advanced than type 2, the latter being considered a (Mesembryanthemoideae) or basal to parietal (Rusch­ transitional stage in the above series. However, an origin ioideae) . Normally, numerous ovules are produced in of type 3 directly from type 1 is equally justifiable. In each carpel, rarely only one or two. adaptation to their pollinators, the inner staminodes, especially in type 2, show considerable modifications in Position of floral organs in respect to the ovary shape and arrangement (see Vogel 1954) . Within the Aizoaceae s.str. (excl. Mesembryan­ Unicellular hairs at the base of the stamens and themaceae) the flower is perigynous. An out-group sometimes the staminodes are frequent in the Ruschioi­ comparison indicates, therefore, that the weakly deae but are absent in Mesembryanthemoideae and perigynous flowers as present in the Mesembryan­ Aizoaceae s.str. (excl. Mesembryanthemaceae), with themoideae have to be considered primitive in Mesem­ the rare exception of Gunniopsis calva Chinnock. An bryanthemaceae. Possibly the perigynous condition is a out-group comparison indicates, therefore, that the synapomorphy for the entire Aizoaceae s.str. (see primitive state is filaments without hairs at the base in Bittrich & Hartmann 1988). the Mesembryanthemaceae. In most species of the Mesembryanthemoideae, the Perigon members of the androecium are basally connate for In the entire Aizoaceae s.str. the perigon usually consists some millimeters, thus forming a short tube. This feature mostly of five (rarely of four) tepals with a quincuncial is also found in a few highly derived genera of the aestivation (Hofmann 1973), only in Ruschioideae up to Ruschioideae (e.g. Conophytum N.E. Br. and Frithia eight tepals may occur. Ihlenfeldt (1960) concludes that N.E. Br.), and is certainly due to parallel evolution. the presence of five tepa Is - a number most common in Furthermore, such a staminal tube is lacking in the the Mesembryanthemaceae - is the primitive state in Aizoaceae s.str. (excl. Mesembryanthemaceae) and this family, for in perigons with four tepals these are nearly all Ruschioideae (for exceptions see above). mostly not arranged in an exactly opposite position. Hence, within the Mesembryanthemaceae, free stamens However, Wilke (1913) already showed that four and and staminodes are considered primitive (Bittrich 1986). five tepals may occur on the same plant, a condition which can also be found within Aizoaceae s.str. (excl. Nectaries Mesem bryanthemaceae). Within the Mesembryanthemaceae, the nectaries are In Mesembryanthemoideae (except Aptenia N.E. Br. always located shortly below the insertion of the spp.) and a number of species of Aizoaceae s.str. (excl. stamens. Shell-shaped to tubular (koilomorphic) and Mesembryanthemaceae), the tepal bases may form a crest-shaped (lophomorphic) nectary forms can be short tube. In Ruschioideae the tepals are free from the distinguished. In the first case four or five nectaries base (in a few cases a hypanthium may be formed, e.g. occur in each flower, in the latter case a circular nectary Argyroderma N .E. Br., which sometimes has been (holonectary) or several distinct crests (meronectary) referred to as a 'calyx-tube', Hartmann 1978). Up to may occur (Rappa 1912). now there exists no evidence to confirm the phylogenetic Zandonella (1972, 1977) states that within the Centro­ state of either condition. sperms, nectaries are derivatives of the receptacle in 326 S.-Afr.Tydskr. Plantk., 1989, 55(3)

close contact with the androecium and always are anthemaceae is half-inferior or inferior. The number of located at the base of the stamens. locules (= number of carpels) varies between three and The Aizoaceae S.str. (excl. Mesembryanthemaceae) more than twenty, each locule usually contains possess a circular, flat or slightly convex, smooth nectary numerous ovules, rarely one or two. The placentation is which merges with the bases of the stamens. In Mesem­ axile or, after ontogenetic displacement, basal to parietal bryanthemoideae four or five nectar-pits are formed (Payer 1857; Eichler 1878; Buxbaum 1951). The latter (koilomorphic meronectary). The nectariferous tissue is type has also been named pseudo-parietal (e.g. Straka localized at their outer sides. Nearly all Ruschioideae 1955) in order to delimit this type terminologically from form either five to several nectaries or one annular parietal placentation in paracarpous ovaries. nectary, both being mostly conspicuously convex and In Aizooideae and Sesuvioideae the septate ovary is tuberculate. Only Glottiphyllum N .E. Br. lacks a nectary nearly superior. Furthermore, a superior ovary is gener­ (Rappa 1912). In the flowers of the subtribe ally looked upon as primitive in comparison to an Dorotheanthinae (Schwantes) emend. Ihlenfeldt & inferior ovary (tendency statement). Therefore it can be Struck (Ruschioideae) five flat nectaries are usually concluded that the nearly superior ovary is primitive in present [in some populations of Dorotheanthus the entire Aizoaceae S.str. Accordingly, the absence of a bellidiformis (L.f.) N.E. Br. a flat, circular nectary has nearly superior ovary can be regarded as a synapo­ been observed, Struck 1985]. In this subtribe the morphy of the Mesembryanthemaceae, and the half­ nectaries are never tuberculate. inferior ovary of the Mesembryanthemoideae can be An out-group comparison of Mesembryanthemaceae considered more primitive than the completely inferior with Aizoaceae S.str. (excl. Mesembryanthemaceae) ovary of the Ruschioideae (criterion of character suggests that a flat, i.e. not or only slightly convex, non­ association, see Crisci & Stuessy 1980). The similar tuberculate nectary is pnmltlve in the family. position of the ovary in Tetragonioideae and Mesembry­ Accordingly, both shell-shaped as well as crest-shaped, anthemoideae is interpreted as a parallelism (see tuberculate nectaries are derived conditions. Hofmann 1973; Bittrich & Hartmann 1988). The question of the polarity of the characters holo­ In Aizoaceae S.str. (excl. Mesembryanthemaceae) the and meronectary remains problematical. Only holonec­ ovary is mostly four- to five-locular, but lower (in all taries have been found in the Aizoaceae S.str. (excl. three subfamilies) and higher numbers of locules (up to Mesembryanthemaceae) and all other centrospermous ten in Aizooideae and Tetragonioideae) occur. Hence, families (Zandonella 1977) up to now. However, in an out-group comparison gives no definite result. Within Mesembryanthemoideae only meronectaries occur. In the Mesembryanthemaceae a reduction in the number of those genera of Ruschioideae belonging to early carpels is always correlated with advanced characters. branches of the subfamily and showing several primitive For instance, in the derived genera Caryotophora characters (e.g. Cleretum N.E. Br., Delosperma N.E. Leistner (Ruschioideae) and Pseudobrownanthus Ihlenf. Br., Dorotheanthus Schwantes, character correlation see & Bittrich (Mesembryanthemoideae) the reduction of above) meronectaries are the common condition. This the carpels to three is combined with the development of suggests the primitiveness of meronectaries for the indehiscent fruits with only a few seeds (Leistner 1958; Ruschioideae. This view is supported by an out-group Ihlenfeldt & Bittrich 1985). An increase in the number comparison with the sister group Mesembryanthemoi­ of carpels only took place in Ruschioideae (within deae. Therefore, a meronectary is probably the primitive Mesembryanthemoideae six and five carpels on the same condition within the entire Mesembryanthemaceae. plant have been observed in exceptional cases). It occurs Furthermore, as in all other Centrosperms only holo­ in all nine fruit types of Ruschioideae as described by nectaries 'have been found, yet the meronectary should Hartmann (1988) . Those genera of this subfamily, be considered a further synapomorphy for the Mesem­ however, which possess several primitive characters bryanthemaceae (out-group comparison). (e.g. Cleretum, Delosperma, and Dorotheanthus; Zandonella (1977) argues that in connection with the character correlation, see above) show five (four) increasing fusion of the receptacle and ovary during the carpels. Thus, these numbers of carpels are interpreted change of position from superior to (half-)inferior the as primitive in Mesembryanthemaceae. previously annular nectaries were interrupted in the The axile placentation as present in Mesembryan­ vicinity of the septa. Furthermore, the distribution of the themoideae is doubtless primitive, as it is characteristic nectary types within Ruschioideae - flat and smooth in for the Aizoaceae S.str. (excl. Mesembryanthemaceae) the Dorotheanthinae, convex and tuberculate in all and, moreover, must be regarded as primitive for the other genera known so far - leads to the assumption of Centrosperms in general. In the Mesembryanthemoi­ an early phylogenetic separation of the Dorothe­ deae as well as in Aizoaceae S.str. (excl. Mesembry­ anthinae. If this view cannot be confirmed, the crest­ anthemaceae) the placenta is shifted into the upper shaped, tuberculate nectary has to be considered a central parts of the locules during ontogeny. synapomorphy for the entire Ruschioideae. In either In Mesembryanthemaceae, normally numerous ovules case further evidence is desirable. are produced in each carpel. A decrease in ovule number generally is correlated with the development of Gynoecium indehiscent fruits [e.g. Hymenogyne Haw. , Ruschian­ The completely septate gynoecium of the Mesembry- themum Friedrich (Ruschioideae), Pseudobrownanthus S.Afr.l. Bot., 1989,55(3) 327

(Mesembryanthemoideae)]. The latter are to be inter­ connected with the shifting of the placenta into a parietal preted as derived in comparison to the hygrochastic position (Bittrich 1986; Hartmann 1988). Within Aizooi­ capsules common in Mesembryanthemaceae (see Fruit). deae the expanding keels of the hygrochastic capsules Consequently, numerous ovules per locule are the are identical in morphology and anatomy to those of the putative primitive condition. Mesembryanthemoideae. But in contrast to Hartmann (1988) we found an expanding sheet in the hygrochastic Pollen fruits of the Aizooideae as well. The basic type of the Centrospermae is a tricolpate, Based on an out-group comparison, the condition of punctate, (micro) spinulose pollen (Nowicke & Skvarla expanding keels extending centrally to the column is 1979) . This type is also very common in the entire Aizo­ regarded as primitive in Mesembryanthemaceae. For the aceae S.str. and without doubt represents the primitive same reason, the presence of expanding sheets must be condition. considered primitive in the Mesembryanthemaceae as well. Therefore, the absence of the expanding sheets in Fruit Mesembryanthemoideae must now be regarded as Loculicidal capsules are most common in the Caryophyl­ another synapomorphy of this subfamily. Furthermore, laceae and Molluginaceae (Hofmann 1973), which are it is deduced here that the formation of the expanding considered as early branches in the Caryophyllales, and tissue as described by Schwantes (1952) in his Delo­ thus presumably primitive in this order. The loculicidal, sperma-type and Micropterum-type (Micropterum hygrochastic capsule (first described by Steinbrinck Schwantes is a younger synonym of Cleretum N.E. Br.) 1883) is the most common fruit type within the is primitive in Ruschioideae. In contrast to this conclu­ Mesembryanthemaceae. In the Aizoaceae S.str. (excl. sion Hartmann (1988) considers the position of the Mesembryanthemaceae) loculicidal capsules (in expanding keels in fruits of her Delosperma-type (which Aizooideae), indehiscent fruits (in Tetragonioideae) and is defined by more and partly different characters than circumscissile capsules (in Sesuvioideae) can be found. Schwantes' Delosperma-type!) as a result of a secondary The extraordinary similarity in the morphology and development in evolution. Furthermore, the formation anatomy of the hygrochastic capsules in Aizooideae of the expanding tissue in the capsule of Cleretum is (Aizoanthemum, Aizoon, Gunniopsis Pax, Galenia and interpreted by Hartmann (1988) as a derivation from the Plinthus) and Mesembryanthemaceae provides strong typical form of her Mitrophyllum-type, among which the evidence for the homology of the fruit-types within the capsule of Cleretum is included. entire Aizoaceae S.str. and thus for a monophyletic The covering membranes, which are common within origin. Consequently, the hygrochastic capsules must be Ruschioideae, are absent in Mesembryanthemoideae regarded as primitive in the Mesembryanthemaceae (out-group comparison) (Bittrich 1986; Bittrich & and Aizoaceae S.str. (excl. Mesembryanthemaceae), and Hartmann 1988). therefore considered derived (Bittrich & Hartmann In Mesembryanthemaceae the expanding tissue caus­ 1988). The widespread occurrence of (at least seam-like) ing the opening of the fruit originates from the endocarp, covering membranes within the Ruschioideae, even in particularly from the epidermis of the septa (Mesembry­ taxa with several other primitive characters (correlation anthemoideae, Rappa & Camarrone 1954) and/or from criterion, e.g. Cleretum N.E. Br. , Delosperma N.E. the ovary roof (Ruschioideae; Huber 1924; Guttenberg Br.), is considered as an indication for its synapo­ 1926; Ihlenfeldt 1960). In mature capsules more or less morphous status in this subfamily. Their development distinct ridges may be formed (expanding keels) as well presupposes the shortening and shifting of the expanding as shallower tissue (hygroscopic skin , Lockyer 1932; keels as described by Ihlenfeldt (1960), Bittrich (1986) more suitably defined by Hartmann 1988 as expanding and Hartmann (1988). sheets). A detailed survey of the fruit characters is given In an extensive discussion of mainly functional and by Hartmann (1988) . adaptive aspects, Hartmann (1988) comes to a similar In Mesembryanthemoideae the expanding tissue is conclusion for the putative primitive fruit of the formed by two expanding keels of exclusively septal Ruschioideae. She states that an expanding sheet, a origin (septate expanding keels, Hartmann 1988) exten­ basal expanding keel and a ridge continuing the keel in ding parallel to each other from the tip of each valve to central valvar position over the valve are probably the central column in open capsules. Within Rusch­ characteristic for this fruit , and moreover, that covering ioideae the expanding tissue is restricted to the valves membranes derived from central valvar endocarp were and a small portion of the septa in the open capsules likely present in primitive Ruschioid capsules as well. (Hartmann 1988). In most cases it is composed of The so-called valve wings, which ontogenetically expanding keels (valvar expanding keels, Hartmann develop from false septa in the locules (Ihlenfeldt 1960), 1988) and expanding sheets. Both expanding tissues join were thought of as a special feature of the Mesembryan­ more or less seamlessly. The expanding keels are prob­ themaceae. Bittrich (1986), however, showed that even ably always developed from septal tissue, but the expan­ in Aizoanthemum membrumconnectens Dinter ex ding sheets are derived from the ovary roof. The shifting Friedrich (Aizooideae), short false septa and narrow of the expanding tissue is possibly caused by the valve wings occur. These findings, as well as the ubiquity ontogenetic displacement of endocarpic tissues, which is of this feature in the Mesembryanthemaceae, especially 328 S.-Afr.Tydskr. Plantk., 1989, 55(3)

Table 2 Character states of the Mesembryanthemaceae. The state of each character is listed (0 = primitive; 1 = advanced). The respective method or criterion to determine the polarity of characters (Crisci & Stuessy 1980) is indicated. The synapomorphies of either subfamily are mentioned (M = Mesembryanthemoideae; R = Ruschioideae), parentheses are given in case of some uncertainty

Character Mode State Method/Criterion

Growth form Herbaceous 0 Out-group comparison; Woody 1 character correlation Leaf Flat, weakly succulent 0 Tendency statement ± roundish , succulent 1 Epidermis Bladder-cell idioblasts 0 Out-group comparison Homogeneous Stomata Anomocyt. + anisocyt. Out-group comparison ; + paracyt. 0 character correlation Anisocyt. + paracyt. Paracyt. 1 Not sunken 0 Out-group comparison; Sunken character correlation Secondary Anomalous secondary thickening thickening 0 Out-group comparison in stems Normal secondary and roots thickening only 1 Stem succulence Absent 0 Out-group comparison Present 1 Cortical Absent 0 Out-group comparison bundles Present 1M Root No conspicuous thickening 0 Out-group comparison; Conspicuous thickening 1 tendency statement Cotyledons Weakly succulent 0 Character correlation; Succulent tendency statement I n florescence Dichasial, monotelic partial florescences 0 Out-group comparison Single flowers 1 Frondose leaves 0 Tendency statement Bracteate leaves 1 Flower Weakly perigynous 0 Out-group comparison Epigynous 1 R Perigon 5(4) tepals 0 Out-group comparison; More than 5 tepals 1 character correlation Androecium Androecium-type 1 0 Tendency statement Androecium-type 2 Androecium-type 3 1 Staminal Absent 0 Out-group comparison tube Present 1M Filaments Glabrous 0 Out-group comparison Basally hairy 1 R Nectary Flat 0 Out-group comparison Crest-shaped 1 (R) Shell-shaped to tubular 1M Composed (meronectary) 0 Out-group comparison; Annular (holonectary) 1 character correlation Gynoecium Half-inferior 0 Character association (Completely) inferior 1 R 5 carpels 0 Character correlation Carpels less or more 1 Placentation Axile 0 Out-group comparison Parietal lR S.Afr.l.Bot., 1989,55(3) 329

Table 2 Continued

Character Mode State Method/Criterion

Ovules per Numerous 0 Character correlation locule Few Pollen Tricolpate, punctate, (micro) spinulose 0 Out-group comparison Other types I Fruit Hygrochastic capsule 0 Out-group comparison Other types Expanding Keels and surface Out-group comparison tissue combined 0 Expanding keels only 1M Expanding surface only 1 Expanding Extending to column 0 Out-group comparison keels ± restricted to valves IR Valve wings Present 0 Out-group comparison; Absent 1 character correlation Covering Absent 0 Out-group comparison membranes Present 1 (R) Seed Testa Black or brown , sculptured 0 Out-group comparison; Colourless, smooth criterion based on developmental processes Epicuticular Present 0 Out-group comparison layer Absent

in all taxa showing several other pnmltlve characters heterochronic change, namely a paedomorphosis. This (correlation criterion), suggests the primitiveness of this view appears to be more convincing than the postulation character within the Mesembryanthemaceae. Further of a multiple evolution of testa sculpturing, deposition of evidence is given by the fact that in ovaries of species tannins, and epicuticula either in the Aizoaceae s.str. lacking valve wings short false septa can be detected (excl. Mesembryanthemaceae) or in both subfamilies of (Ihlenfeldt 1960; Haas 1976; Bittrich 1986; criterion of the Mesembryanthemaceae. Therefore, sculptured seeds vestigial organs, Crisci & Stuessy 1980). As the valve with an epicuticular fine sculpture, and a tanniniferous wings in Aizoaceae s.str. (exc\ . Mesembryanthema­ testa are considered primitive in Mesembryan­ ceae), if present at all are very narrow, the well­ themaceae. developed valve wings of the Mesembryanthemaceae should be considered as a possible synapomorphous Chromosome number character of the family. All Mesembryanthemaceae share the chromosome base number x = 9, which is considered primitive within the Seeds Centrosperms in general by Raven (1975) and Ehren­ Generally, the seeds of the Mesembryanthemaceae may dorfer (1976a). Accordingly, the chromosome base be arranged in two groups. In one, the seeds are brown number x = 8 (rarely x = 7) of the Aizoaceae s.str. (exc\. or black, due to the deposition of tannins into the testa, Mesembryanthemaceae) would be a derived character with conspicuous sculpturing of the exotesta, and an and therefore a synapomorphy of the Aizooideae, epicuticular rodlet layer (Woodcock 1930; Ehler & Sesuvioideae, and Tetragonioideae (Bittrich 1986; Barthlott 1978). In the other group, the seeds are Bittrich & Hartmann 1988). However, further counts, smooth, more or less colourless and without epicuticular particularly in Molluginaceae, are needed to substantiate micro-sculptures. The seeds of the latter group are this assumption. usually smaller than those of the first. Testa sculpturings and deposition of tannins similar to that found in the General Conclusions seeds of the first group are also known in other centro­ The synopsis of those characters of Mesembryan­ spermous families, but the epicuticular layer seems to be themaceae that are regarded as primitive in this survey unique to the Aizooideae and the Mesembryan­ can be employed to construct a basic morphotype themaceae. As the sculpturing of the testa, the (,hypothetical ancestor', see above) of the family. The deposition of tannins, and the formation of the respective characters are compiled in Table 2. It must be epicuticula take place only in late ontogenetic stages, the stressed that the adjective 'primitive' only refers to the second seed type may be interpreted as a result of a basal branches of the Mesembryanthemaceae. These 330 S.-Afr.Tydskr. Plantk. , 1989, 55(3)

primitive characters must not be adopted uncritically in CRISCI, l .V. & STUESSY , T.F. 1980. Determining primitive the evaluation of the characters of any derived group, as character states for phylogenetic reconstruction. Syst. Bot. the possibility of character reversals has to be taken into 5: 112- 135. consideration. CRONQUIST, A. 1981. An integrated system of classification The synapomorphies of both subfamilies as indicated of flowering plants. Columbia University Press, New York. DINTER, K. 1935 . Aizoanthemum membrumconnectens Dtr. in Table 2 provide strong evidence for a monophyletic n. gen. Kakteenkunde 2: 27- 28. origin of Ruschioideae and Mesembryanthemoideae, DONOGHUE, M.l. & CANTINO, P.O. 1984. The logic and respectively. None of the extant taxa of the Mesembry­ limitations of the outgroup substitution approach to anthemaceae can be regarded as the ancestor of the rest cladistic analysis. Syst. Bot. 9: 192-202. of the family. DUPONT, S. 1968a. Revision des characteres des epidermes The main distribution area of the Mesembryanthema­ et des plantules chez les Mesembryanthemacees . Ph.D. ceae is located in southern Africa. In addition to this, thesis , Univ. of Toulouse. few species of both subfamilies occur in northern Africa DUPONT, S. 1968b. Epidermes et plantules des and the Middle East (Mesembryanthemoideae) or East Mesembryanthemacees. Systematique. Evol. Bull. Soc. Hist. Nat. Toulouse 104: 7-64. Africa and the Arabian Peninsula (Ruschioideae). All EHLER, N. & BARTHLOIT, W. 1978. Die epicuticulare these taxa show the same subfamilial synapomorphies as Skulptur der Testa-Zellwande einiger Mesembryan­ their southern relatives and no evidence for an 'own' themaceae. Bot. lahrb. Syst. 99: 329-340. evolutionary development above species level could be EHRENDORFER, F. 1976a. Chromosome numbers and detected. From the present character analysis as well as differentiation of centrospermous famil ies. Pl. Syst. Eval. geographical data, no conclusion can be drawn with 126: 27- 30. respect to the early history of radiation of the Mesem­ EHRENDORFER, F. 1976b. Closing remarks: systematics bryanthemaceae. and evolution of centrospermous families. Pl. Syst. Eval. Furthermore, the basic morphotype of the Mesembry­ 126: 99- 105. EICHLER, A.W. 1878. B1iithendiagramme. 2. Teil. Wilhelm anthemaceae may serve as a reference for the evaluation Engelmann Verlag, Leipzig. of characters within the Aizoaceae s.str. (excl. Mesem­ GIBSON, A .C. 1978. Rayless secondary xylem of bryanthemaceae), along with an out-group comparison Halophytum. Bull. Torr. Bot. Club 105 : 39-44. with the sister-group Mesembryanthemaceae. Due to GUITENBERG, H. VON 1926. Die Bewegungsgewebe. In: insufficient character analysis the phylogenetic relation­ Handbuch der Pflanzenanatomie, ed. Linsbauer, K. , 1. ships within the Aizoaceae s.str. (excl. Mesem­ Abteilung, 2. Teil Histologie, Band 5, Gebriider branthemaceae), however, are still not well resolved. Borntraeger, Berlin. Therefore, a satisfactory out-group comparison is not yet HAAS, R. 1976. Morphologische, anatomische und possible, as out-group comparisons should be based on entwicklungsgeschichtliche Untersuchungen an B1iiten und monophyletic, non-paraphyletic in-groups (Wiley 1980). Friichten hochsukkulenter Mesembryanthcmaceen­ Gattungen. Diss. Botanicae 33, Verlag l. Cramer, Vaduz. HARTLEY, R.D. & HARRIS, P.l. 1981. Phenolic Acknowledgements constituents of the cell walls of dicotyledons. Biochem. Syst. The basic practical work, mainly on Mesembryanthe­ Ecol. 9: 189- 203 . maceae, has been supported financially by the Deutsche HARTMANN, H . 1978. Monographie der Gattung Forschungsgemeinschaft, to which we are much Argyroderma N.E. Br. (Mesembryanthemaceae Fenzl). indebted. We also wish to thank Prof. Dr H .-D. Mitt. [nst. Allg. Bot. Hamburg 15 : 121- 235. Ihlenfeldt, Dr H.E.K. 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