Closing bodies in the capsular fruits of Ruschioideae ( Aizoaceae ) — a review

Capsular fruits of the Mesembryanthema' are uniquely diverse and have been used to establish groupings within the tribe Ruschieae. The function, structure and development of the closing bodies of the Ruschioideae are reviewed from existing lit­ erature and are supplemented by personal observations, providing a framework for future research aimed at resolving critical issues regarding the structure and taxonomic implications of the closing bodies of the Ruschioideae. The number of species per taxon, distribution and presence or absence of covering membranes and closing bodies within the Mesembryanthema are tabulated. INTRODUCTION c les sometimes close the locule entrance to a certain In the past, the structure of the capsular fruits was considered critical in the systematics o f the Mesem­ bryanthema (Herre 1971; Hartmann 1988, 1991, 1993, 2001; Smith et al. 1998). In particular, it is the internal structure of the capsular fruits that yields most o f the variable characters. However, with the publication of molecular data by Klak et al. (2003, 2007) it was found that the groupings proposed by Hartmann were not sup­ ported by molecular data. In many Mesembryanthema the locules are covered by roof-like lids known as covering membranes, leaving only a narrow distal opening through which seeds can be dis­ persed. This entrance is frequently closed to some degree and the blockage has an immensely important role in the dissemination biology of the Mesembryanthema as it results in the complete or partial occlusion of the locule. Seeds are consequently locked in and cannot simply be washed out by raindrops as in other species that lack such blocking devices. This structure results in the seeds being forced out, jet-like, through the gaps between the covering membranes (Parolin 2006). The distal closing devices are generally very diverse in their structure, but two main types are distinguished. By far the most striking are the closing bodies, which are prominent and often hemispherical structures formed on the fruit wall near the upper end of the placentas (Figure 1A). The second type of closing device (Figure IB), in the form of bulges, ledges and rodlets (Hartmann 1991), occurs on the lower surface of the covering membrane near the distal end. In a number of species, none of these closing devices are present, but dense bundles of funi* National Parks Board. Singapore Botanic Gardens. 1 Cluny Road. Singapore 259569; e-mail: Hubert KURZWEILfanparks.gov.sg. ** National Herbarium, South African National Biodiversity Institute, 0001 Pretoria; e-mail: Burgoyne@sanbi.org. I Research Fellow, Department of Environmental Sciences. University of South Africa. PO. Box 392. 0003 UNISA Pretoria. MS. received: 2007-04-20. ‘ The subfamilies Mesembryanthemoideae and Ruschioideae together are termed Mesembryanthema (Hartmann 1991) and represent a group without taxonomic rank. extent (Figure 1C; Lampranthus Group. Hartmann 1988, 1991; some Drosanthemum species, Hartmann & Bruckmann 2000; Hereroa, Dehn 1992). In some Mesembry­ anthema, the free upper ends o f the placentas contribute to the occlusion o f the locules (Dehn 1992). In this paper we are dealing only with the first type. Closing bodies are normally easily visible with the naked eye, particularly the larger ones, which can be up to 2 mm in diameter. In an open capsule they are very con­ spicuous as they are mostly pale and often have a shiny surface, thus contrasting with the dark brown remainder o f the capsule. Owing to their prominent appearance, these bodies were already discovered in the early days of botanical exploration of the arid regions o f south­ ern Africa. The generic name o f the genus Disphyma N.E.Br. is derived from the closing bodies (two-lobed in this case). Much has been said about the function, structure and development of the closing bodies of the Ruschioideae (Berger 1908; Huber 1924; Lockyer 1932; Schwantes 1952, 1957; Volk 1960; Ihlenfeldt 1960. 1971; Haas 1976; Hartmann 1988. 1991, 1993; Hartmann & Golling 1993; Kurzweil 2005). Comments on the closing bodies of indi­ vidual species are also found in numerous floristic and taxo­ nomic publications, but most o f these are merely descrip­ tions of their shape, size and colour. Detailed investigations and comparisons of these prominent capsule features are rare in literature (Poppendieck 1976; Hartmann 1988), and a number of problems exist, calling for further stud­ ies. While the overall appearance of the closing bodies was often used as a diagnostic feature of certain genera and spe­ cies, there is as yet no clear and well-documented compara­ tive survey of these bodies. Furthermore, information on fruit characters in general is scattered throughout the taxo­ nomic literature and is often not easily accessible (language barrier, some journals not easily obtainable). The present paper aims to review the existing literature on the closing bodies of Mesembryanthema and is supplemented by per­ sonal observation. It is hoped that this review will provide the starting point for future research aimed at resolving critical issues regarding the structure and taxonomic impli­ cations of the closing bodies of the Ruschioideae. 108 Bothalia 39,1 (2009) THE CLOSING BODIES AND THEIR STRUCTURE Closing bodies are mostly round and often hemispher­ ical protrusions positioned on the fruit wall below the distal ends o f the covering membranes at the upper end o f the placentas (Figure 1 A). Their size ranges from less than 1 mm to 2 mm in diameter. The closing bodies are FIGURE 1.—A, Ruschia lineolata, Burgovne 9848: closing bodies formed on fruit wall near upper end of placentas; B, Ruschia sp.. Burgoyne 8102; closing ledges formed on lower surface of distal end of covering membranes; C. Lampranthus watermeyeri, Bur­ goyne 7562 or Smicrostigma viride, Stey n 384: dense bundles of funicles close locules. CB, closing bodies; CL, closing ledges; CM, covering membranes; F, funicles; VR, valve rims. Scale bars: A, 4 mm or 3 mm; B. C, 5 mm. firmly united with the placentas, the upper ends of the latter often running in a pronounced groove. The larger closing bodies often touch the covering membranes and thus close the locule completely, and in many cases also reach partly under the latter. Small or tiny closing bodies are sometimes rather deeply positioned inside the locule (for example in some genera o f the Eberlanzia Group). Prominent closing bodies have only been reported in subfamily Ruschioideae, and then only in genera that have complete or nearly complete covering membranes in their capsular fruit (although closing bodies do not occur in all o f the genera with covering membranes). The term ‘closing bodies’ was originally coined by Steinbrinck (1883). Later Huber (1924) considered these structures as formations of the placentas and con­ sequently termed them ‘Plazentarhócker’ (= placental tubercles). This term was subsequently adopted by many textbooks and taxonomic treatments. Ihlenfeldt (1960) on the other hand, interpreted these formations as a prod­ uct o f the endocarp and suggested reverting to the origi­ nal term ‘closing bodies’. After a detailed examination of the closing bodies of Pleiospilos N.E.Br., Hartmann & Liede (1986: 458) also rejected Huber’s controversial term ‘tubercle’ as completely inadequate. The shape of the closing bodies o f the Ruschioideae is very diverse. Particularly elaborate closing bodies are found in Hartmann’s (1993) Leipoldtia Group. They are normally rather large and consist of a ‘head’ borne on a distinct stalk. Anatomically, the central part is made up o f large, spongy cells covered by several cell layers of sclerenchymatic tissue. Smaller rodlet-shaped closing bodies are found in the Ruschia type of fruit (Hartmann 1988) and have a similar anatomy. Comparatively small, hook-shaped closing bodies are found in the Titanopsis type of fruit, and they consist of sclerenchymatic cells only (Hartmann 1988: 327). The closing bodies of the Mitrophyllum type of fruit are not prominent hemispher­ ical bodies, but appear as broad ridges or bosses where the placentas and expanding keels meet (Poppendieck 1976; Ihlenfeldt & Struck 1987). Their epidermis is only moderately thick-walled and an extensive spongy tis­ sue is present. In some genera referred to this fruit type, broad, spongy closing bodies have the shape of ledges and have also been termed as such (Hartmann 1991); the closing ledge of Dorotheanthus Schwantes has been referred to as ‘Verschlusswall’ (= closing sill) (Ihlen­ feldt & Struck 1987). Hartmann (1988) suggested that these aforementioned types of closing bodies are not all


INTRODUCTION
c les som etim es close the locule entrance to a certain In the past, the structure o f the capsular fruits was considered critical in the systematics o f the M esem bryanthema (Herre 1971;Hartmann 1988Hartmann , 1991Hartmann , 1993Hartmann , 2001;;Smith et al. 1998).In particular, it is the internal structure o f the capsular fruits that yields most o f the variable characters.However, with the publication o f molecular data by Klak et al. (2003,2007) it was found that the groupings proposed by Hartmann were not sup ported by molecular data.
In many Mesembryanthema the locules are covered by roof-like lids known as covering membranes, leaving only a narrow distal opening through which seeds can be dis persed.This entrance is frequently closed to some degree and the blockage has an immensely important role in the dissemination biology of the Mesembryanthema as it results in the complete or partial occlusion o f the locule.Seeds are consequently locked in and cannot simply be washed out by raindrops as in other species that lack such blocking devices.This structure results in the seeds being forced out, jet-like, through the gaps between the covering membranes (Parolin 2006).
The distal closing devices are generally very diverse in their structure, but two main types are distinguished.By far the most striking are the closing bodies, which are prominent and often hemispherical structures formed on the fruit wall near the upper end o f the placentas (Figure 1A).The second type o f closing device (Figure IB), in the form o f bulges, ledges and rodlets (Hartmann 1991), occurs on the lower surface o f the covering membrane near the distal end.In a number o f species, none o f these closing devices are present, but dense bundles o f funi-extent (Figure 1C; Lampranthus Group. Hartmann 1988, 1991; some Drosanthemum species, Hartmann & Bruckmann 2000; Hereroa, Dehn 1992).In some M esembry anthema, the free upper ends o f the placentas contribute to the occlusion o f the locules (Dehn 1992).
In this paper we are dealing only with the first type.Closing bodies are normally easily visible with the naked eye, particularly the larger ones, which can be up to 2 mm in diameter.In an open capsule they are very con spicuous as they are mostly pale and often have a shiny surface, thus contrasting with the dark brown remainder o f the capsule.Owing to their prominent appearance, these bodies were already discovered in the early days o f botanical exploration o f the arid regions o f south ern Africa.The generic name o f the genus Disphyma N.E.Br. is derived from the closing bodies (two-lobed in this case).
Much has been said about the function, structure and development of the closing bodies of the Ruschioideae (Berger 1908;Huber 1924;Lockyer 1932;Schwantes 1952Schwantes , 1957;;Volk 1960;Ihlenfeldt 1960Ihlenfeldt . 1971;;Haas 1976;Hartmann 1988Hartmann . 1991Hartmann , 1993;;Hartmann & Golling 1993;Kurzweil 2005).Comments on the closing bodies o f indi vidual species are also found in numerous floristic and taxo nomic publications, but most o f these are merely descrip tions of their shape, size and colour.Detailed investigations and comparisons of these prominent capsule features are rare in literature (Poppendieck 1976;Hartmann 1988), and a number of problems exist, calling for further stud ies.While the overall appearance of the closing bodies was often used as a diagnostic feature of certain genera and spe cies, there is as yet no clear and well-documented compara tive survey of these bodies.Furthermore, information on fruit characters in general is scattered throughout the taxo nomic literature and is often not easily accessible (language barrier, some journals not easily obtainable).The present paper aims to review the existing literature on the closing bodies of Mesembryanthema and is supplemented by per sonal observation.It is hoped that this review will provide the starting point for future research aimed at resolving critical issues regarding the structure and taxonomic impli cations of the closing bodies of the Ruschioideae.

THE CLOSING BODIES AND THEIR STRUCTURE
Closing bodies are mostly round and often hemispher ical protrusions positioned on the fruit wall below the distal ends o f the covering membranes at the upper end o f the placentas (Figure 1 A).Their size ranges from less than 1 mm to 2 mm in diameter.firmly united with the placentas, the upper ends o f the latter often running in a pronounced groove.The larger closing bodies often touch the covering membranes and thus close the locule completely, and in many cases also reach partly under the latter.Small or tiny closing bodies are sometimes rather deeply positioned inside the locule (for example in some genera o f the Eberlanzia Group).
Prominent closing bodies have only been reported in subfamily Ruschioideae, and then only in genera that have complete or nearly complete covering membranes in their capsular fruit (although closing bodies do not occur in all o f the genera with covering membranes).
The term 'closing bodies' was originally coined by Steinbrinck (1883).Later Huber (1924) considered these structures as formations o f the placentas and con sequently termed them 'Plazentarhócker' (= placental tubercles).This term was subsequently adopted by many textbooks and taxonomic treatments.Ihlenfeldt (1960) on the other hand, interpreted these formations as a prod uct o f the endocarp and suggested reverting to the origi nal term 'closing bodies'.After a detailed examination o f the closing bodies o f Pleiospilos N.E.Br., Hartmann & Liede (1986: 458) also rejected H uber's controversial term 'tubercle' as completely inadequate.
The shape o f the closing bodies o f the Ruschioideae is very diverse.Particularly elaborate closing bodies are found in Hartmann's (1993) Leipoldtia Group.They are normally rather large and consist o f a 'head' borne on a distinct stalk.Anatomically, the central part is made up o f large, spongy cells covered by several cell layers of sclerenchymatic tissue.Smaller rodlet-shaped closing bodies are found in the Ruschia type o f fruit (Hartmann 1988) and have a similar anatomy.Comparatively small, hook-shaped closing bodies are found in the Titanopsis type o f fruit, and they consist o f sclerenchymatic cells only (Hartmann 1988: 327).The closing bodies of the Mitrophyllum type o f fruit are not prominent hemispher ical bodies, but appear as broad ridges or bosses where the placentas and expanding keels meet (Poppendieck 1976;Ihlenfeldt & Struck 1987).Their epidermis is only moderately thick-walled and an extensive spongy tis sue is present.In some genera referred to this fruit type, broad, spongy closing bodies have the shape of ledges and have also been termed as such (Hartmann 1991); the closing ledge of Dorotheanthus Schwantes has been referred to as 'Verschlusswall' (= closing sill) (Ihlen feldt & Struck 1987).Hartmann (1988) suggested that these aforementioned types of closing bodies are not all homologous.
According to their ontogenetic derivation, most o f the closing bodies o f the Ruschioideae are endocarpal structures.A few other species possess small placen tal closing bodies, which have a different texture and anatomy (Hartmann 1988).This emerged originally from a careful study o f the closing bodies o f Pleios pilos (Hartmann & Liede 1986) where the following were observed: 1, endocarpal closing bodies are often large, although small and insignificant endocarpal bod ies have also been reported occasionally, e.g.Tanquana H.E.K. Hartmann & Liede (1986).Endocarpal closing bodies comprise an epidermis o f sclerenchymatic cells over a body o f isodiametric cells with equally thick walls, the central part o f the closing body comprising either parenchym atic or sclerenchym atic cells.Thus they differ m arkedly from the cells o f the placentas which have unthickened walls throughout.The deriva tion o f these prom inent closing bodies from endocarpal tissue has also been found by Kurzweil (2005); 2, pla cental closing bodies are rare in the M esem bryanthem a and contribute only a little to the occlusion o f the locule.Exam ples include Malephora N.E.Br., Pleiospilos nelii Schwantes, P. simulans (M arloth) N.E.Br.and P. bolusii (Hook.f.) N.E.Br.(Hartm ann & Liede 1986).
They are made up o f cells with only weakly thickened or unthickened walls, although the cell walls o f the epi dermis can be strongly thickened.In Drosanthemum Schwantes, the endocarp may form a little protrusion, lifting the closing body slightly (Hartmann & Bruckmann 2000: 81).
The genera Disphyma and Rhombophyllum (Schwantes) Schwantes have two-lobed closing bodies.The situation in a few other genera is somewhat reminiscent o f this condi tion as the closing bodies and their stalks have a more or less deep groove (although this is often largely obscured by the placentas).It is suggested that this partial or complete two-lobed condition is a reflection o f the origin from two carpel margins (Kurzweil 2005).
While in most genera the closing bodies are constant in their size and can therefore be used as diagnostic char acters, some intraspecific variation was found in Mitrophyllum Schwantes (Poppendieck 1976), Dorotheanthus subgen.Dorotheanthus (Ihlenfeldt & Struck 1987) and Disphyma (Chinnock 1996).The shape o f the closing bodies o f Odontophorus marlothii N.E.Br.varies even within the same capsule (Hartmann 1976).

DISTRIBUTION OF CLOSING BODIES IN THE RUSCHIOIDEAE
Only the subgroups o f subfamily Ruschioideae are treated here, as closing bodies do not occur in subfamily Mesembryanthemoideae (Figure 2A).The following is a brief review o f detailed investigations o f the closing bodies o f individual genera in the literature.Comparative descriptions and discussions o f these structures can also be found in Hartmann (1983Hartmann ( , 1988) ) and Dehn (1992).Overall descriptions o f shape, size, colour and consist ency o f closing bodies are found throughout taxonomic and floristic literature and are not listed here.2C).Sometimes they have comparatively insignificant closing bodies (Hartmann 1988(Hartmann , 1991)), developed as swellings, spongy sills or ridges but not as large, hemispherical structures as in other M esembryanthema genera.These closing bodies have a broad base, which is typical o f the Mitrophyllum type o f fruit to which the Dorotheantheae are referred (Hartmann 1988).Ihlenfeldt (1960) and Ihlenfeldt & Struck (1987) also described these ridge-like closing bodies (referred to as 'V erschlussw air = closing sill), which are found in some species o f the genus Dorotheanthus.They are best devel oped in D. bellidiformis (Burman) N.E.Br.subsp.bellidiformis.Generally, the ridge-like closing bodies o f this group are interpreted as a product o f the endocarp and not the placenta (Ihlenfeldt 1960: 49).In the genus Dor otheanthus, the occurrence o f the seven different capsule types defined on the basis o f features o f the covering membranes and closing bodies is geographically corre lated, and species with capsules that have pronounced closing bodies are more frequent in the southern parts of the distribution area (Ihlenfeldt & Struck 1987).

Tribe R uschiae Ihlenf., Schwantes & Straka
This group comprises most o f the Ruschioideae, cur rently including nearly 1 600 species.An enormous diversity in the capsular fruit structure is found in this group.

Mitrophyllum Group
The capsules have mostly been referred to the Mitro phyllum type o f fruit (Figure 3  In Disphyma the closing bodies are deeply two-lobed (Chinnock 1996).However, in D. papillatum Chinnock the closing bodies are variable in size and range from well developed to vestigial, and D. australe (Aiton) J.M.Black lacks closing bodies altogether.An abnormal population o f this species with variously shaped fin ger-like outgrowths at the entrance o f the locules was reported by Chinnock (1996).Glottiphyllum has large  (2003), informal groups after Hartmann (1991Hartmann ( , 1993Hartmann ( , 1998a)).Approximate numbers of species follow Hartmann (1993) (Hartmann & Gólling 1993).The closing bodies of various species in the genus Mitrophyllum are variable in the extent o f their formation even within the same popu lation (Poppendieck 1976).They are generally apparent as swellings or swollen ridges in a position where the placentas and the expanding sheets meet.Anatomically, they are made up o f isodiametric cells with strongly thickened walls.The epidermis in their proximal part consists o f similar cells but the cells in the distal part are elongate (when seen in a longitudinal section) and have weakly thickened walls, thus resembling the cells o f the adjacent expanding tissue.

Delosperma Group
The capsules o f this group (Figure 3B) are rather diverse, and the different genera were referred to the Delosperma N.E.Br., Drosanthemum and Lampranthus N.E.Br.types o f fruit (Hartmann 1988).Seed pockets occur occasionally.Expanding keels are usually distinct from the expanding sheets and the valves have mostly broad wings.Covering membranes are present or absent.Closing bodies are almost always absent, but the genus Malephora often has knobs on the distal end o f the pla centas which act as closing bodies (Hartmann 1988: 56); these placental closing bodies may also be bilobed.Small and often bilobed endocarpal closing bodies are found in some species o f the genus Drosanthemum, and most species o f this genus have placental closing bodies (Hartmann & Bruckmann 2000).

Stomatium Group
The capsules can mostly be referred to the Delo sperma and Drosanthemum types o f fruit o f Hartmann (1988).Covering membranes are present or absent, and valve wings are broad to reduced or absent.Seed pock ets derived from basal false septa are found in Stomatium Schwantes (Figure 3C).Closing bodies are normally absent in the group but small, obscure ones are found in Orthopterum L. Bolus. Herre (1971) stated that distinct bifid closing bodies were also found in Chasmatophyllum maninum L.Bolus, whereas they were absent in the rest o f this genus.We examined the notes accompanying the protologue made by Bolus (1927), where she stated that capsules o f C.  Hartmann (1988) placed Faucaria Schwantes and Orthopterum in this group, but for an alternative view, which is followed below, see Groen & Van der Maesen (1999).

Faucaria Group
This group corresponds to the section established by Schwantes (1952) and reinstated by Groen & Van der Maesen (1999) and comprises only two genera {Fau caria and Orthopterum) as their capsules are unique (Figure 3D).When the capsules are viewed after wet ting, one gets the impression that they are empty, as locules are hidden by lamellae curving over the top of the locules.The capsules are 5( 6)-locular and are deep, the valves with fissures between them.Conventional covering membranes and closing bodies are absent and expanding keels end in an awn.The deep locules com bined with curved lamellae are highly effective in retain ing seeds during periods o f low rainfall.Capsules can become detached after ripening by being pushed out by the enlarging leaf pair produced the following season and may roll away, but are never found more than a few centimetres from the parent plants (Groen & Van der Maesen 1999).Particularly prominent valve wings are found in Faucaria where they are borne erect when the capsule is open.When dry, these valve wings fold back into thin grooves.Orthopterum has similar fruits with their septa separated into two parts, the upper part arch ing on top o f the capsule.

Titanopsis Group
The capsules o f this group (Figure 3F), mostly referred to Hartmann's (1988)  The genus Ihlenfeldtia was established to include two species previously included in Cheiridopsis (Hart mann 1992).This genus is characterized by its distinct fruit morphology, with mostly 10 locules, thin, straight, complete covering membranes, and valve wings that are broad at the base.Endocarpal closing bodies are present and are illustrated by line drawings in Hartmann's publi cation.Anatomically, they comprise a translucent layer of vertical cells on top o f a sclerenchymatic body.The small genus Tanquana was separated from Pleiospilos as it differs in several characters including its fruit structure (Hartmann & Liede 1986).Capsules were shown to be generally less robust than those o f Pleiospilos, having thinner valves and covering membranes.Important dis tinguishing features were found in the structure of the closing bodies, which are small and o f endocarpal ori gin.

Dracophilus Group
Fruits o f this group (Figure 3E) mostly belong to the Delosperma type o f capsule (Hartmann 1988).Covering membranes are mostly reduced to form a narrow rim, and valve wings are usually prominent.Closing bodies are generally absent.

Bergeranthus Group
This group has fruits that are close to the Mitrophyl lum type o f Hartmann (1988) but generally have stout and firm covering membranes (Figure 4A).The valve wings are mostly reduced to narrow organs and are often awn-like; occasionally they are absent altogether.Clos ing bodies are present or absent.
The spongy closing bodies o f Bergeranthus Schwantes are rather large plates (Schwantes 1952: 16;Hartmann 1993: 61).In Cerochlamys N.E.Br., the small closing bodies are o f placental origin and they are frequently over arched by a translucent layer o f tissue that is derived from the expanding sheets (Hartmann 1998b: 52).The placental closing bodies o f Hereroa (Schwantes) Din ter & Schwantes are tiny (Hartmann 1993: 61).In this genus the locule entrance is often closed by long funicles (Dehn 1992: 135).Small and frequently deeply set closing bodies are found in Machairophyllum Schwantes where they may be irregular in shape (Kurzweil & Ches selet 2003).Rhomhophyllum species have large, flat or rounded and bipartite closing bodies (Schwantes 1952: 15-17;Hartmann 1993: 61).

Lampranthus Group
Most genera o f this group have capsules o f the Lam pranthus type (Figure 4B;Hartmann 1988).While hygrochastic capsules are the norm, Carpobrotus N.E.Br.species differ by being the only genus within the tribe Ruschieae to have indehiscent fleshy berries (Figure 5A).Locules have rigid covering membranes with addi tional closing devices at the distal end.Together with sterile funicles, these closing devices on the underside o f the covering membranes are largely responsible for clos ing the entrance to the locule.Valve wings are present or absent.Prominent closing bodies have only been reported in the genus Enarganthe N.E.Br.(Herre 1971) but are absent in all other genera.

Ruschia Group
This is a large group with fruits mostly o f the Ruschia type (Figure 4C;Hartmann 1988).Fruits normally remain on the plants (occasionally up to several years) and release the seeds after dehiscence, but tumble fruits are found in Khadia N.E.Br.and rarely also in Ruschia Schwantes.The frequently deep locules have firm, complete covering membranes with additional clos ing devices at the distal end.Expanding keels are often widely diverging and valve wings are mostly absent or reduced.Closing bodies are small or medium-sized and hook-or rodlet-shaped.They are comparatively large in Acrodon N.E.Br.(Burgoyne 1998), a genus with a capsule structure that is somewhat reminiscent o f the Leipoldtia type o f fruit according to Hartmann (1988).
An endocarpal closing body that is largely covered by the placenta was reported in Ebracteola montis-moltkei (Dinter) Dinter & Schwantes (Hartmann 1996: 39) are partly covered by some outgrowth o f the expanding sheets.Dehn (1992) showed that the endocarpal clos ing bodies o f Ruschia are comprised mainly o f irregu lar, thin-walled cells, and are covered by 3-6 layers of prosenchymatic and moderately thick-walled cells plus a one-layered sclerenchymatic epidermis, which corre sponds well with the observations o f Hartmann & Liede (1986).Based on structure, six types o f closing bodies were distinguished by Hartmann & Liede (1986) in the study o f Ruschia and related genera.

Leipoldtia Group
Most genera of this group were referred to the Leipold tia type of fruit (Figure 5B;Hartmann 1988), characterized by: 1, persistent, ± concave, complete covering membranes that frequently have additional closing devices in the form of bosses or ledges; 2, mostly large and distinctly stalked closing bodies; 3, broad (rarely reduced) valve wings.
Capsules normally remain on the plant but tumble fruits are known in Fenestraria N.E.Br.and Cephalophyllum N.E.Br.This is the only group of Mesembryanthema in which the closing bodies are consistently present as prominent structures.They are also large in most genera-comparatively small closing bodies are found only in Fenestraria (Hartmann 1982), Jordaaniella H.E.K. Hartmann (Hartmann 1984) and Cylindrophyllum Schwantes (Herre 1971).Their surface is often rugose (Hartmann 1991: 124).The texture of the closing bodies o f this group is corky, with sclerenchymatic outer lay ers.Most genera o f this group have been taxonomically revised by H.E.K. Hartmann (several papers, see below; sometimes with co-workers), with detailed comments on many plant features including the closing bodies.
As part of a detailed study of the genus Antimima N.E.Br.emend Dehn, Dehn (1988)  Friedrich was shown by Hartmann & Rust (1994).The shape and surface of the closing bodies of Odontophorus marlothii was found to be variable within one population and even within the same capsule, and can therefore not be used as a diagnostic feature (Hartmann 1976).The genus Pleiospilos was examined in detail by Hartmann & Liede  (1986).It was shown that the five species of P. subgenus Punctillaria have large endocarpal closing bodies that close the locule entrance almost completely and are entirely made up of sclerenchymatic cells.The epidermis cells are elongate (vertically arranged), whereas the cells of subja-cent layers are isodiametric.The three species of P. subge nus Pleiospilos have small placental closing bodies com prising isodiametric cells with unthickened walls although their epidermis cells can have slightly thickened walls.
In our opinion, Antimima and Cylindrophyllum do not belong in the Leipoldtia Group.Antimima is better placed within the Ruschia Group and Cylindrophyllum belongs in the Bergeranthus Group.

Eberlanzia Group
This small informal group was established by Hart mann (1998a).In Eberlanzia Schwantes (Figure 5C) and Amphibolia L.Bolus, the fruit structure is similar to that o f Ruschia except for the broad valve wings.Closing

FUNCTIONAL ASPECTS
Seed dispersal in the Mesembryanthemaceae is defined as ombrohydrochorous, i.e. triggered by rain drops.The covering membranes, which prevent the sim ple washing-out o f the seeds, always comprise two parts that are arranged roof-like but are never ftised on top.It has been shown that the association o f flexible covering membranes and prominent closing bodies results in an increased water pressure in the locule after a direct hit by a rain drop (Parolin 2006), and consequently the seeds are expelled jet-like, following a bending o f the cover ing membranes (Berger 1908;Lockyer 1932;Schwantes 1952).Lockyer (1932) showed that this complete occlu sion o f the locule actually promoted dissemination in space, as jet-like expelled seeds fell further from the par ent plant than merely washed-out seeds would.The same mechanism also protracts dispersal in time, i.e. results in slow or delayed release o f the seeds (Ihlenfeldt 1971), and this is obviously ecologically advantageous in the arid habitat o f the Mesembryanthemaceae.The role o f the small closing bodies o f some species that close the distal entrance o f the covering membranes only partly is not fully understood as yet, e.g.Tanquana (Hartmann 1983: 37;Hartmann & Liede 1986: 461).Those species that lack prominent closing bodies altogether often have other devices to achieve the occlusion o f the locules, such as protrusions from the covering membranes in the form o f ledges, sills, bulges or rodlets, by sterile funicles or by free ends o f placentas.This seems to suggest that the occlusion o f the locules is favoured by natural selection but is achieved by different means.Capsule types that have only very incomplete or no covering membranes are clearly less efficient with regard to their seed dispersal (e.g.Ihlenfeldt & Struck 1987).These species also tend to be found in areas o f higher rainfall (e.g.Delosperma), where it is not critical if seed is dis seminated in one rainfall event if this is closely followed by more rain.
From an evolutionary point o f view, certain adaptive pressures on dispersal mechanisms can influence the size and shape o f the closing bodies, as they are obvi ously correlated with the dispersal syndrome.This was illustrated by Hartmann (1988: 329) in the example o f Fenestrariathis species is dispersed as tumble fruits, and therefore only small closing bodies have evolved in its capsules.

TAXONOMIC SIGNIFICANCE
In view o f our incomplete knowledge o f the closing bodies o f the Mesembryanthemaceae, it is premature to make firm proposals regarding the taxonomic signifi cance o f their structure.Owing to the variation observed in some genera and the only sporadic occurrence o f these bodies, it is unlikely that extensive studies will eventu ally yield taxonomically significant features.While the structure o f the closing bodies does not permit a new classification, some correlations to fruit types can be observed (Hartmann 1988: 327).Nevertheless, the struc ture and size o f the closing bodies can mostly be used as diagnostic features o f individual species and genera, and partly also o f larger informal groups (Hartmann 1991(Hartmann , 1993)).
The arrangement o f the subfamilies and tribes follows the classification o f Klak et at.(2003).The large sub family Ruschioideae is divided in four groups (clades), two o f these representing the tribes Apatesieae and Dorotheantheae (corresponding to the Apatesia and Cleretum Groups o f Hartmann 1993).They form a monophyletic, well-supported group, supported by molecular data (Klak et al. 2003).The remaining two clades fall within the tribe Ruschieae in which few DNA sequence changes have been observed (Klak et a l 2003).Hart mann (1988) has proposed 10 groups for the species in the tribe Ruschiae.
A;Hartmann 1988).Cov ering membranes are mostly complete but are sometimes reduced, and the surface o f expanding keels are extended to form flat expanding sheets.Closing bodies are some times present, and are mostly developed as spongy sills or ridges and have a broad base.They are rather variable in the extent o f their formation but are rarely very large (Glottiphyllum (Haw.)N.E.Br.).Valve wings are mostly broad, though sometimes very narrow or absent.
maninum were not yet available and a drawing o f the portion o f a capsule o f C. musculinum (Haw.)Dinter & Schwantes was given, showing bifid closing bodies.Both Bolus and Herre made an error in citing bifid clos ing bodies for Chasmatophyllum maninum.Examination by the authors o f many recently collected specimens o f C. musculinum has shown no bifid closing bodies.
described the clos ing bodies and illustrated them by means of line drawings and SEM micrographs.The large closing bodies are shortstalked and of endocarpal origin.Hartmann (1977) revised the genus Argyroderma and examined the late development of the closing bodies of A. congregatum L.Bolus.It was shown that the cells of the closing bodies still have unthick ened walls at the time of anthesis and become thickened only later.The structure and position of the closing bodies of the genus Cephalophyllum was described by Hartmann (1978).According to Hartmann & Dehn (1987), species ot Cheiridopsis have large closing bodies in the mature fruits, which often partly reach under the distal parts of the cover ing membranes and close their entrance entirely.No taxo nomic correlation of the different types of closing bodies was found.An informative SEM micrograph of the stalked closing body of Leipoldtia schultzei (Schlechter & Diels) bodies in the group are small or large, sometimes deeply set in the locule.Fruits breaking up into nutlets are found in Stoeberia Dinter & Schwantes where the anemochoric seeds are also unusual.SEM illustrations o f closing bod ies o f Amphibolia laevis (Aiton) H.E.K.Hartmann were shown by Hartmann & Dehn (1989).

TABLE 1 .
-Distribution of closing bodies in the Mesembryanthemaceae.Subfamilies and tribes after Klak et al.