Clausing Et Al 2000

7/28/2019 Clausing Et Al 2000

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BolankdJ ournul oJ / h Linnean Sociplv (20OO), I.?.?: 303-326. With G figuresdoi:l0.lOOS/lmjl.1999.0340,available online at http://www.idealibrary.rom on I h

Correlations among h i t raits and evdifferent h i t swithin MelastomataceaGUDRUN CLAUSING'*, KARSTEN MEYER' ANDSUSANNE S. RENNER''nstitut$r Spezielh Botanik, Universitat Main


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304 G. CLAUSING ETA.Characters and their states . . . . . . . . . . .Multivariate analyses . . . . . . . . . . . . .Discussion . . . . . . . . . . . . . . . . . .Structural heterogeneityof berries and capsules . . . . .

Dissochaeteae/Sonerileaecomplex . . . . . . . .Fruit evolution in M elastomataceae, especially in theFruit variation at the intrageneric level: the case of MelastomaFruit types as phylogenetic indicatorsFruit character plasticity and dispersal ecology. . . . . . . .. . . . .Acknowledgements . . . . . . . . . . . . . . .References . . . . . . . . . . . . . . . . . .

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INTRODUCTIONFruit types such as capsule, nut, drupe, samara and berry havregarded as evolutionarily conservative (Stebbins, 1974; Spjut, 1

older classification systems accorded fruit type a high taxonomicmolecular phylogenetic studies are showing that fruits often are unof natural alliances and that their use in higher-level classifiartificial groups (Apiaceae: Plunkett, Soltis& Soltis (1996); Lam& Olmstead (1997); Myrtaceae: Johnson & Briggs (1984); Ran(1995); Rhamnaceae: Richardson& Medan (pers. corn., SeptRohrer, Robertson & Phipps (1991), Morgan, Soltis & Roberfragaceae: Soltis, Soltis&Bothel (1990)). n Rubiaceae, for examevolution on a molecular phylogenetic tree suggests that fleshy f12 times independently within that family (Bremer& ErikssoAndreasen & Olsson, 1995). Moreover, molecular data are sevolution may be rapid when morphogenetic genes of major effeccan cause dramatic morphological differences (cf. Kadereit, 199The striking homoplasy of fruit types may have two causes. from strong directional selection on fruit characters; the latter aand directly correlated with the dispersal agent. For example, fleare associated with dissemination by animals. Second, fruit charmore homoplastic than they really are becauseof incorrect homThis is a problem particularly in large tropical families, suchMelastomataceae, where detailed morphological and anatomica


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FRUIT TRAITS IN MEIASTOMATACEAEThese examples from close relatives of the Melastomataceae (Co

1996) suggest that phylogenetic investigations, followed by critihomology assessments, are needed if fruit characters are to be usanalyses of this family. Tribal classificationsofMelastomataceae (DNaudin, 1851; Triana, 1871; Cogniaux, 1891; Renner, 1993) hon fruit types, both as diagnostic characters as well as supposed ph(Renner, 1993). Based on outgroup comparison, Renner consideplesiomorphic for the family and fleshy fruits from inferior oembedded in pulp (her true berries) as apomorphic. Because shplasticityof fruit characters, especially the different origins of flemodes of dehiscence, she used only one fruit character in her anpresence and absence of true berries, suggesting that further critifruit attributes was needed (Renner, 1993: 529).The present study examines the fruit anatomy and morphologMelastomataceae, representing the mainly palaeotropical AstronieKibessieae, Melastomeae, and Sonerileae, and a few neotropiclastomeae, Miconieae, and Bertolonieae (for tribal classificationmethods). Our major goal was to investigate whether the teberry as traditionally applied in these groups describe structurphenotypes. To this end we performed multivariate analyses of 3morphological characters to identifjr states that might correlate wi(or a lack thereof). We also investigated the pattern of plasticityat different hierarchical levels and within monophyletic groupmolecular sequence data, and tried to relate it to ecological dete

MATERIAL AND METHODSFruits of 85 species of Melastomataceae, representing 31 gene

were investigated (see Appendix in which we follow the classif(1993); we recognize Bertolonieae and Dissochaeteaesemu Cognon molecular phylogenetic results (Clausing, 1999; Clausing &although the circumscription of these tribes at present is unclear)alcohol samples (70 spp.) collected in South-east Asia, Madag


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306 G . CLAUSINC ETAL.TABLE. Characters and their states; see tex t for definitionsof problematic statelisted here atid scored for all species, the 31 shown in T ables 2-6 were includanalysesTissuePlarentaEndorarp

Mesorarp

Hypanthium

Fusrd tissues

Character Persistenre ahscnt (0)Rrsistrnce alxcnt (0)L ignification ahsent (0).Cell pattern mosaic-like ( I )Ditto undulate ( I )Dittn elongate ( I )Ditto elongate-undulate'~hickness thin (0)Sclerrid presenre absent (0)Few sclereids present ( I )Intermediate numher of sclereids prrsent ( I )Many sclereids present ( I )Sclercid distribution scattered ( I )Ditto rlustered ( I )Ditto in a ring (I )Calcium oxalate presencc ahsent (0)Sti irrh granule presence allsent (0)Thickness thin (0)Srlereid presence ahsent (0)Few sclereids present ( I )Intermediate number of srlereids present ( I )M any srlereids presrnt ( I )Srlereid distribution scattered ( I )Ditto clustered ( I )Ditto in a ring ( I )Calcium oxalatr presence absent (0)Starch granule presence ahsent (0)Size of inner epidermis rells relative to groundtissue rells larger ( I )Ditto same s ize ( I )Ditto smaller (1)Outer epidermis cell surfare smooth ( I )Thickness thin (0)Sclerrid presence absent (0)Few srlereids present ( I )Intermediate numher of sclrreids present ( I )M any sclereids present ( I )Sclereid distribution scattered ( I )Ditto clustered ( I )Diito i n a ring (1)Calcium oxalate presence absent (0)


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FRUIT 'I'MITS IN MELAST'0MATAC:FAETABLE. Standardized canonical coefficients of a discriminanalysis that included 81 spccies and nine fruit charactValues indicate the contribution of each variable to the nonical axis separating dehiscent and indehiscent fruitsCharacter and state CanPlacenta persistence (0, I )Endocarp persistence(0, I)Outer epidermis cells smooth ( I , 0)Fused tissues (0, I )Ovary/ hypanthium fusion complete ( I , 0)Ovary/hypanthium fusion partial ( I , 0)Exocarp distinctness at maturity (0, I )Ovary longer than hypanthium ( I , 0)Ovary as longas hypanthium ( I , 0)

-0.210.750.470.16-0.78-0.440.000.340.42

(Results: Characters and their states). Of the 52 characters scored,from multivariate analysis because breaking-up of multistate chcoding resulted in the statistical redundancy of seven characharacters were excluded because not all characters applied tobeen observed in all species. For example, characters referring to fbe scored in species with free ovaries. T he multivariate matrixand species comprised 4212cells, and empty cells due to such canalysis. Of the excluded characters, five dealt with endocarp ligpattern, and nine with types of sclereid distribution in the mesoor fused tissues.T o determine which characters were associated with dehiscenwe first performed a discriminant analysis that included nine chall species (Table 2) and pooled display fruits (i.e. fruits that dehisplacentas) with dehiscent fruits. Blakea paucgora, Centradenia ghomoeandra, and Sonerila malgaritacea were excluded from this analacked values for some characters. In a second discriminant ana60 species for which the relevant data were available, placenta present), was added as a character, and fruits were categorized as


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308 C.CLAUSING ET AL . h u . Standardized canonical coefficients of a discriminant anaincluded 81 species and nine fruit characters, and for which frseparated into the four categories indehiscent-fleshy, dehiscendehiscent-dry, and dehiscent-fleshy (=display fruits). High valueshigh contributions of the respective character to the canonical axis sdchiscent-fleshy fruits from indehiscent or dehiscent-dry fruits. Thuhypanthium fusion and fleshy placentas explain much of the between fruit types, while placenta persistence per Je does nodifferences between fruit typesCharartrr and state CanSquared canonical rorrelation KPlacenta fleshy (0, I )Placenta persistence (0, I )F,nclocarp persistence (0, 1)Fused tissues (0, 1)Ovary/hypanthium fusion complete ( I , 0)Ovary/hypanthium fusion partial ( I , 0)Exocarp distinrtness at maturity (0 , I )Ovary longer than hypanthium ( I , 0)Ovary as long as hypanthium ( I , 0)

0.540.000.400.25-0.83-0.170.270.03

0.83

0.17

-04

--0-0

TABLE. Standardized canonical coefficients of a discriminant analys28species with fused tissues and 14 fruit characters. Values indicate the the characters to the canonical axis separating dehiscent and indehisceendocarp persistence and abundant calcium oxalate in the fused tissues in fused tissues most clearly separate dehiscent from indehiscen haracter and statePlacenta prrsistence (0, I )Endocarp pemistencr (0, I )Hypmthium outer rpidrrmis cells smooth ( I , 0)Fused tissues thick (0, I )Ovary/hypanthium fusion complete ( I , 0)Ovary/hypanthium fusion partial ( I , 0)Exocarp distinctnessat maturity (0, 1)Ovary longrr than hypanthium ( I , 0)Ovary as long as hypdnihium ( I , 0)Sclereid prrsencc in fused tissues (0, I )


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FRUIT TRAIlS IN MEIASI'OMATACEAE


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310 G.CIAUSING ET ALseeds are embedded. The general shape of melastome fruits varicampanulate or urceolate (Fig. l), with some capsules being Sarcopyrams nepalensk) or cubic (e.g. Phyllagathis dispar). In DionyDichaetanthera, half of the ovary is exposed due to a short cup-shaphypanthium.Melastome fruits develop from epigynous or perigynous flowwall thus consistsof twoparts of different morphological origin. Tfrom the ovary and consists of endo-, meso-, and exocarp. [IThexocarp are used in the strict sense (Cave, 1869)) referring onlyouter cell-layer of the ovary, respectively]. The outer fruit walhypanthium and includes inner and outer hypanthium epidermground tissue. The most important differences in the anatomy othe extent of fusion of ovary and hypanthium, presence or absenand the location and degree of lignification (the importance of thalso evident in all statistical analyses; see Results: Multivariate anais predominantly axillary, but some genera have basal-axillaplacentas located on the ovary wall between the septs. Mesocartissues comprise several layers of parenchymatous cells that are the epidermal cells.An inner hypanthium epidermis and an exoparts of the fruit where ovary and hypanthium are not fused. Inpockets that house the stamens in bud stage, these are locatedand hypanthium tissue (Fig. 4E). They appear as compressed laepidermis. The epidermis on the inside of the pockets eventuaexocarp and that on the outside continues nto the inner epidermisEnations or hairs may be found on both epidermises and on theuni- or multiseriate hairs, glandular hairs or scales are common onfruits, although some fruits are entirely glabrous, e.g. those of Me

Characters and their statesSee Table 1.Placentation. Placentation is predominantly axillary. In Kibessie4F), the placentas are located on the ovary wall between the lo


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Figure 2. Placenta shapes. A, fleshy; B, stalked; C, club-shaped; D,V- or T -s


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312 G. CIAUSING E74Ldistribution of sclereids, which are elongate and/or branched walls. We recorded the presence or absence of sclereids and threeabundance, namely few sclereids (c0.4 per one degree and cell labundance (0.5-0.8per one degree and cell layer), and many scledegree and cell layer). Sclereids may be scattered throughout thin small groups, or form closed rings, but these patterns were nstatistical analyses. Further mesocarp characters concerned the poxalate crystals (found in most species) and starch granules (founPlethiandra).Hypanthium. The hypanthium ground tissue is very similar to thaLike the mesocarp, it is characterized by a varying density asclereids and calcium oxalate crystals, with sclereid and crystal abbeing higher than in the mesocarp. Definition of classes of abuthe mesocarp. In two instances, Arthmstemma ciliaturn and Blasubepidermal cell layers are lignified. Another hypanthium chasome statistical analyses was the size of the inner hypanthium epidto those of the exocarp. We distinguished two states, viz. whethinner hypanthium epidermis are smaller (the commonest conditthose of the exocarp. Different from exocarp cells, cells of the epidermis remain unlignified. The outer hypanthium epidermis ceconvex or papillose (coding, see Table 1).Fused tissues. Where ovary and hypanthium are fused, their tdistinguishable, resulting in the category fused tissues for which twere recorded as for the mesocarp and hypanthium. T he fuhypanthium can be complete or partial, with much plasticity evespecially in Medinilla and Melastoma. Difficulties in determining tharise from the stamen pockets, which extend downwards into ovary and hypanthium are adnate and which appear as compcross-sections (Fig.4E).We scored ovaries as free if no septs connhypanthium.Exocaq. Four exocarp characters were included in the statisticalwhether the exocarp was distinct in mature fruits, whether it was the size of its cells was relative to those of the mesocarp.


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AFRUIT TRAITS INMELASTOMATACFAE

B


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314 C.CLAUSING ETAL.If fleshiness of the placenta was included in the data set and

in the four categories indehiscent-fleshy (soft berries), dehiscindehiscent-dry (dry berries), and dehiscent-fleshy (display fruit), difound three axes of which the first twowere most significant(WF =4.8, df = 24,168, RO. 0001; n=60 species). The first axis pdehiscent-fleshy(=display) fruits from indehiscent-fleshy and ind( RO. 0001,p=54%). It was associated positively with a fleshpersistent endocarp. It was negatively associated with ovary/h(Table 3). The second canonical axis separated dehiscent-dry fruitthe three other types (RO.001, p=50%) and was positively persistent endocarp and negatively with fusion of hypanthium anDiscriminant analysis of 28species with a fused ovary and hypcharacters, again separated dehiscent and indehiscent fruits, with 5in the data set accounted for by dehiscence, but only marginal siof the small sample size (Wilk's lambda=0.44, F = 1.4, df = 13,1the analyses based on larger sample sizes, dehiscence was positivapersistent endocarp and negatively withapersistent placenta anhypanthium fusion (Table4). Weaker correlations existed betwethe presence of calcium oxalate crystals and sclereids. The 25 cfor the 52 species lacking fused tissues easily discriminated dehiscefruits, with 83% of the variance attributable to mode of dehiscenc0.17, F = 5.6, df= 24,27, RO. 0001). The highest correlationdehiscence and the presence of sclereids in the mesocarp, followendocarp (Table5).Principal component analysis based on nine characters revealedaxis that accounted for 40% of the total variation present in thone end of the axis have fruits with a complete fusion of ovarytissues, while fruits at the other end have distinct exocarps and ohypanthium fusion (Table6).

DISCUSSIONThe general picture that emerges from the five multivariatesmall number of characters, addressing the persistence and fu


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FRU IT TRA ITS IN MELASTOMATACEAE TABLE.Standardized canonical coefficients ofa discriminant analysis that iwithout fused tissues and25fruit characters. Values indicate the contributionto the canonical axis separating dehiscent and indehiscent fruits. Characterseparate dehiscent from indehiscent fruits are sclereids in the mesocarp asistence. Sclereid presence vs presence in low or intermediate numbers mtributions to the separation of fruit types because ofO / 1coding (cfCharacter and statePlacenta persistence (0, I )Endocarp persistence (0, I )Hypanthium outer epidermis cells smooth (1, 0)Hypanthium thick (0, I )Ovary/hypanthium fusion complete (1, 0)Ovary/hypanthium fusion partial (1, 0)Exocarp distinctness at maturity (0, I )Ovary longer than hypanthium (1, 0)Ovary as long as hypanthium (1, 0)Sclereid presence in hypanthium (0, 1)Hypanthium with few sclereids (1, 0)Hypanthium with an intermediate number of sclereids ( I , 0)Calcium oxalate presence in hypanthium (0, I )Starch granule presence in hypanthium (0, 1)Inner epidermis cells larger than hypanthium cells ( I , 0)Inner epidermis cellsof samesize as hypanthium cells ( I , 0)Mesocarp thick (0, 1)Sclereid presence in mesocarp (0, 1)Mesocarp with few sclereids (I , 0)Mesocarp with an intermediate number of sclereids (1, 0)Calcium oxalate presence in mesocarp (0, I )Starch granule presence in mesocarp (0, I )Exocarp lignification(0, 1)Exocarp cells larger than mesocarp cells ( I , 0)Exocarp cells of same size as mesocarp cells ( I , 0)

TABLE. Relative contributions of nine fruit characters in a principanalysis of fruits from81 species.As in Tables2-5, values indicate theof each character to the canonical axi s separating dehiscent and indThus, presence or absence of fused tissues, exocarp distinctness n matovary/hypanthium fusion contribute most strongly to the canonical adehiscent and indehiscent fruitsCharacter and state


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316 G.CLAUSINC ETAL.sample, which contains many species with dry or woody berrExamples of soft berries with fleshy placentas areLorga spmceanaasmithii (Miconieae), and Medinilla amplectern, and Pachycentria glaucSoft berries are characterized by the absence of lignified tissuesclereids in the fruit walls, and often by an early-degrading endocare characterized by a persistent endocarp as seen in DissochaetaJ niS, in which mesocarp and hypanthium ground tissues are not fthe thick ground tissue contains a dense ring of sclereids. Some msuch as those of Bellucia aequiloba, also have a dense ring of scleretissue, but their ovary and hypanthium are completely fusedendocarp. In al speciesof the neotropical genusBlaha investighypanthium are fused and heavily sclerified, and in B. mtundijileven lignified.As shown by these examples, berries in Blakeeae, Dissochaeteare so variable in structure that they cannot be considered a sinpresence or absence of which can be coded in binary fashion a(1993).Capsules. Roughly half the species sampled had dehiscent fruitscapsules in Melastomataceae are very heterogenous, but less orepresented in our sample, which lacks representatives of Microlicie(all of which have capsules) and includes only one Bertolonieparticularly diverse capsules (see illustrations n Baumgratz, 1983-8dehiscence sassociated withapersistent endocarp and unfused or ohypanthium and ovary tissues. Exceptions are some species of SFigs lC, 4D) and ptentandra (Kibessieae; Figs lF, 4F). Pternandintermediates between berries and capsules, with variation in fruit species. In some, the fruit walls consist of fused hypanthium andare strikingly hard due to an abundance of sclereids scattered ofruit wall. Such fruits were referred to as capsulae baccatae by DIn Sonerila, capsules may have a more or less completely fusedovary, their tissues being indistinguishable (Fig. 4D). If anything, is lignified, and the capsules then resemble the woody berries sochaeteae.In other lineages, capsule lignification is also highly variable.example, comprise capsules with lignified endocarp, exocarp,


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FRUIT TRAITS IN MELASTOMATACMEh i t sunordered

Soft berryDy berryWoody berryFleshy capsule0V capsule

m rupeEquivocal

RhynchantheraMicroliciaLavoisieraRhexiaArthrostemmaMonochaetumDissotisTibouchinaPteroplepisMelastomaOsbeckiaDichaetantheraCentradeniaNepseraAciotosDiplectriaMedinillaCalvoaAmphiblemmaDriesseniaBlastusPhyllagathisBlakea-olenaMonolenaBertoloniantrazygiaMaietalbcocaLeandraClidemiaG m fenriedaMerianinAdelobotrysBellucia-stroniaAstroniaPternandmPternandraMouririMouririMemecylonMemecylonOliniaPenaeaRhynchocalyxAlzateaCrypteroniaMyrtusEugeniaLudwigiu

Figure 5. Fruit evolution in Melastomataceae and Memecylaceae as trace


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318 G.CLAUSINC ETAL.


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FRUIT TRAITS IN MELASTOMATACEAEThe present study included fruits from 15 genera and man

aochaeteae/Sonerileae (Appendix), and their anatomy and mgreatly. For example, woodinessh some dissochaetcan hi ts isification of the hypanthium ground tissue and/or the mesocabracteata; Fig. 4E), while in others, such as Dissochaetaafik or D.is due to a closed ring of sclereids in the hypanthium ground tisof these woody berries is very different from that of soft berriDissochaeteae (compareDissochaeta bracteata, Fig. 4E, andMedinillaAnother example of the plasticity of fruits in this alliance is proand its sister group Catanthera. The former has a thick-walled cwith four regular longitudinal cracks (Clawing, pers. obs.), whileberries. Both genera are root-climbers and form a well-suppogroup-Sonerileae sequencedsofar (Amphiblemma, Blastus, Calvoa,Driesseappear nested within Dissochaeteae (Fig. 5). Capsules in these glignified endocarp and sometimes also a lignified exocarp, but aglandul&ra the hypanthiumis fleshy and there is no lignificationsimilar to those of some Dissochaeteae, suchasMedinilla serpens.

Fruit variation at the intrageneric level: the case@MelastAnother example of fruit variation among closely related spec

ndhF sequences (Meyer, 1999; Renner&Meyer, submitted) s prova member of the pantropical Melastomeae (including Rhexieaebe monophyletic (Fig.5).Melastoma species have a persistent endolignified or parenchymatous (Fig. 4A). The exocarp and the innehypanthium are always distinct so that mesocarp and hypanthcan be distinguished. The fusion of ovary and hypanthium rangeto up to 3/4 fused. Mesocarp and hypanthium vary in numberdistribution of sclereids and calcium oxalate crystals. Often, tsubexocarpal, or subepidermal layers are stuffed with calcium oxFigure 6 shows three fruit types that have evolved within this g(Meyer, in press). The commonest fruit type is represented by Me(Fig. 6C), with irregularly transversal splitting of woody frui


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320 C.CLAWING LTAL.complete drying out of the placenta at maturity so that the seedligdied endocarp from where they are released through the poresis parenchymatous with ten lignified nerves that persist when thseeds, a striking parallelism to the capsules of Oxyspora exbaAstronia smihciilia. Capsules of A. smlaciifolia also have a persistenis not lignified. Their star-like dehiscence results from the irregulthe fruit wall (which consists of the fused ovary and hypanthtriangular parts of the wall persistingas a dome-shaped frame. Chave a heavily lignified and persistent endocarp andahypanthiuvascular bundles. The seeds are released loculicidally through fivin the endocarp.

Fruit gpes as phylogaetic indicatorsBerries may evolved three times (Fig. 5) within the family,

examples from other families listed in the introduction, the usupposed synapomorphy of Blakeeae, Dissochaeteae, and Miconiresulted in the unnatural grouping of a large number of palaeotropigenera that do not form a monophyletic clade. Erroneous hommay have partly resulted from a lack of detailed studies of fruianatomy. In Melastomataceae, as in other Myrtales, fruit chavariable even at the intrageneric level (as evidenced by Melastomrarely be reliable indicators of monophyletic groups. This docarefully coded fruit-anatomical characters should not be includeanalysis of the family. Indeed, in some other families, fruit chafound to be non-homoplastic even at higher hierarchical levels. Thshowed that fruit-anatomical traits are valuable for recognizing gein Oleaceae. A phylogenetic study of Cornus based on cpDNA morphological data also found the two major clades to be cpresence of iridoid glucosides and fruit colour (Xianget al., 1996):the blue-fruited, the other the red-fruited dogwoods, as posmorphological grounds by Eyde (1985). Also in Eythrina, a phcpDNA restriction site and morphological data indicates that exocand texture are phylogenetically informative (Bruneau, 1996),


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FRUIT TRAITS IN MELASTOMATACMEbirds may be less abundant (Stiles&Rosselli, 1993). Alternativemay undergo selection for increased fleshiness of their exocarp aentering more closed forest habitats. Stiles and Rosselli found thathe pattern of species richness of small mashers, such as manaconforms closely to the distribution patterns of berry-fruited mconieae and Blakeeae). These birds, like Miconieae and Blakeeain wet forests at middle elevations. Similar relationships may exisalthough thereareno detailed studies of fruit handling and dispersmelastomes by birds. Species of Medinilla and other soft-beroccurring in montane forests (700-2000 m) at Mt. Kinabalu Natidepend on small to medium-sized birds living in flocks and on sdispersal of their seeds (Clausing, 1999).Another selective factor may be habit. In melastomes, an strongly associated with baccate fruits adapted to bird dispersathe neotropics,85% of epiphytic melastomes produce berries (Re300 of the 350 Dissochaeteae known are facultativeor obligate e1999), and thus, a combination of similar growth forms (nameand habitats (tropical forests) may have promoted independentadapted berries in Dissochaeteae and Miconieae. Once juicy befurther adaptive shifts became possible. While most Miconieaeblue berries, a few have much larger yellow ones adapted for dmonkeys (Renner, 1989), and this may then have selected for hberries as seen in Bellucia.

Little is known about the biophysical detailsof capsule funct(butseeWeber, 1987; Stone&Weber, 1988; Cellinese, 1997, on rin Sonerileae). However, wind tunnel experiments in other groupcapsule morphology can influence the shape of seed shadowKadereit, 1991).This suggests that parallelisms in capsule morphosuch as the sclerified vascular bundles that function in capsule oOvspora e e a , and Melastoma pellegrinianum, may reflect similar sin terms of seed dispersal in these species habitats. Capsularundergo selection for increased fleshiness of their pericarp anentering more closed forest habitats.Together, our results indicate that berries and capsules evowithin Melastomataceae, with anatomical evidence supporting


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322 G. CIAUSING ETdL .for preparing microtome sections. Financial support for this projDeutsche Forschungsgemeinschaft (grantRE/603/2- 1 to S.S. Rand collecting of fruit samples was conducted with kind permissioEkonomi Unit, Kuala Lumpur, and Sabah Parks, Kota Kinabalsupport came from Kinabalu Park, Sabah, the Sabah ForestSandakan, the Institute of Biodiversity and Environmental CoUniversiti Malaysia, Sarawak, the Department of Botanyof the Nof Hanoi, and the Department of Biology of Prince of SongkhYai, Thailand.

REFERENCESBaumgratz J FA. 1983-1985 [1988]. Morfologia dos frutos e sementes de MelaArchivos do J ardim Botanic0 do Rio de J aneim 27: 113-1 55.Blattner F, K adereit J W 1991. Patterns of seed dispersal in two species of

natural conditions. Flora 185: 55-64.Boissieu MH de. 1912. Une MClastomacCe asiatique dun genre africain. Bullede F rance5 9 33C332.Br emer ByAndreasen K , Ol sson D. 1995. Subfamilial and tribal relationsbased on rbc L sequence data. Annals ofthe Missouri Botanical Garden 82: 383-Br emer By Eriksson 0. 1992. Evolution of fruit characters and dispersal famly Rubiaceae. BiologicalJournal ofthe Linnean So&o 47: 7S95.Bruneau A. 1996. Phylogenetic and biogeographical patterns in Erythrina (Legas inferred from morphological and chloroplast DNA characters. Systematic Candolle deAP. 1828. Melastomaceae. Rudmmus 3: 99-202.Cave C. 1869. Structure et dkveloppement du fruit.Annales des Sciences NaturelleCellinese N. 1997. Notes on the systematics and biogeography of the SoClausingG. 1999. Die Systematikder Dissochaeteae und ihre Stellung nnerhalbClausingG,Renner SS.(inpress).Molecular phylogeneticsof MelastomataceCogniaux CA . 1891. Melastomaceae. In: De Candolle A, De CandolleC, eConti E, L itt A, Sytsma I ( J . 1996. Circumscription of Myrtales and theirEydeRH. 1985. The case for monkey-mediated evolution in big-bracted dogwGraham SA, Crisci J V, Hoch PC. 1993. Cladistic analysis of Lythrace

123- 190.(Melastomataceae)with special focus on fruit characters. Tivpical BiodivernoPh.D. dissertation, ohannes Gutenberg-Universitat, Mainz.implications for character evolution.American Journal ofBotany.emgamarum vol7. Paris: G . Masson, 1-1256rosids: evidence from rbcL sequence data. American Journal ofBotany 83: 221-


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Clausing Et Al 2000

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