Fruit structure and systematics of Monimiaceae s.s (Laurales)redbiblio.unne.edu.ar/pdf/62_265-285...

Botanical Journal of the Linnean Society

, 2007,

153

, 265–285. With 53 figures

© 2007 The Linnean Society of London,

Botanical Journal of the Linnean Society,

2007,

153

, 265–285

265

Blackwell Publishing LtdOxford, UKBOJBotanical Journal of the Linnean Society0024-4074(c) 2007 The Linnean Society of London? 2007153••265285Original Article

FRUIT STRUCTURE OF MONIMIACEAEM. S. ROMANOV Et al.

*Corresponding author. E-mail: [email protected]

Fruit structure and systematics of Monimiaceae

s.s

. (Laurales)

MIKHAIL S. ROMANOV

1

*, PETER K. ENDRESS

2

, ALEXEY V. F. CH. BOBROV

3

, ALEXANDER P. MELIKIAN

4

and ALEJANDRO PALMAROLA BEJERANO

5

1

N. V. Tzitzin Main Botanic Garden of the Russian Academy of Sciences, 127276, Botanical St., 4, Moscow, Russian Federation

2

Institute of Systematic Botany and Botanic Garden, University of Zurich, Zollikerstrasse 107, CH-8008, Zurich, Switzerland

3

Recent Deposits and Pleistocene Palaeogeography Department, Geographical Faculty, and

4

Department of Higher Plants, Biological Faculty, M. V. Lomonosov Moscow State University, 119992, Moscow, Russian Federation

5

Jardín Botánico Nacional, Universidad de la Habana, Carretera ‘El Rocio’, Km 3 1/2, Calabazar, Boyeros, C. P. 19230, Ciudad de la Habana, República de Cuba

Received March 2006; accepted for publication September 2006

Fruit structure (anatomy) was studied in 27 species of 15 genera of Monimiaceae

s.s

. Almost all have apocarpousgynoecia, with the carpels more or less surrounded by a floral cup. The fruitlets are presented on the opened floralcup, which, depending on its pre- and post-floral development, differentially contributes to the attractive part of themature fruit. Morphologically similar fruits may differ conspicuously in anatomical structure. Based on anatomicalcharacters two different fruit forms were found: drupe(let)s (with compact sclerenchymatic endocarp forming a stone:putamen) and berry(let)s (with parenchymatic endocarp, and mesocarp parenchyma containing isolated sclereidnests). Four types of drupelets differing by the endocarp structure were tentatively distinguished: (1) the

Monimia

-type has a many-cell-layered putamen of large isodiametric sclereids, interrupted on the ventral side by few radialrows of small sclereids; (2) the

Hortonia

-type has a few-cell-layered putamen of isodiametric, especially thick-walledsclereids – it may be composed of two lateral halves, i.e. with the sclerenchyma partially interrupted on the ventraland dorsal sides (but without rows of small sclereids); (3) the

Mollinedia

-type has a few-cell-layered putamen, withmore or less radially elongate sclereids with wavy cell walls; and (4) the

Hedycarya

-type has a one-cell-layered puta-men of pronouncedly radially elongate sclereids with wavy cell walls. Drupelets of some taxa with a single-cell-layered endocarp with only weakly thickened cell walls may represent a transition from drupelets to berrylets. Thefruit structure supports three major clades recognized earlier by morphological studies and by molecular phylo-genetic analyses: (1) Monimioideae (

Monimia

-type drupelets), (2) Hortonieae of Mollinedioideae (

Hortonia

-typedrupelets), and (3) the remainder of Mollinedioideae (

Hedycarya

- and

Mollinedia

-types) and berrylets. Fruitstructure also supports the close relationship of Monimiaceae and Lauraceae. © 2007 The Linnean Society ofLondon,

Botanical Journal of the Linnean Society

, 2007,

153

, 265–285.

ADDITIONAL KEYWORDS:

berry(let) – comparative carpology – drupe(let) – fruit evolution – pericarp

anatomy – phylogeny – putamen.

INTRODUCTION

The family Monimiaceae

s.s

. (exclusive of Atherosper-mataceae and Siparunaceae) is well supported as aclade in recent molecular studies, and as part of Lau-

rales (Renner, 1998, 1999; Renner & Chanderbali,2000; APG, 2003; Hilu

et al

., 2003). Earlier, Amborel-laceae and Trimeniaceae, and sometimes Chloran-thaceae, were also included in Monimiaceae

s.l

. or asseparate families in Laurales (Perkins, 1925; Money,Bailey & Swamy, 1950; Cronquist, 1981; Takhtajan,1987, 1997; Thorne, 1992; but not Thorne 2000). How-

266

M. S. ROMANOV

ET AL

.



2007,

153

, 265–285

ever, Amborellaceae and Trimeniaceae were found tobe among the basalmost angiosperms and Chloran-thaceae to be isolated and difficult to place, and thusall three families had to be excluded not only fromMonimiaceae but also from

Laurales

(e.g. Mathews &Donoghue, 1999; Qiu

et al

., 1999, 2005; Soltis, Soltis &Chase, 1999; APG, 2003). The isolated position ofAmborellaceae is also supported by floral and carpo-logical features (Endress & Igersheim, 2000; Bobrov

et al

., 2005). In molecular phylogenetic studies

Mon-imia

,

Palmeria

and

Peumus

form a clade, which is sis-ter to the other Monimiaceae

s.s

. (Renner, 1998, 1999,2002; Renner & Chanderbali, 2000). The distinctnessof this group was also recognized by morphologists(Philipson, 1993; Takhtajan, 1997); this clade is nowtreated as subfamily Monimioideae (Philipson, 1987),and the other members of the family as Mollinedio-ideae. Within Mollinedioideae,

Hortonia

is sister tothe other genera (Renner, 1998, 1999, 2002; Renner &Chanderbali, 2000). The Madagascan

Decarydendron

and

Tambourissa

form a (weakly supported) clade,which is sister to all other remaining genera (Renner,2002). The bulk of the genera, comprising the SouthAmerican and most Australasian groups, form amoderately supported clade (not including

Xymalos

,

Hedycarya

,

Levieria

or

Kibaropsis

) (Renner, 2002).The relationships of some of these groups are stillunresolved, and there is no agreement also from astructural point of view (Endress, 1980b; Philipson,1993; Bobrov

et al

., 2003b).The representatives of Monimiaceae

s.s

. are charac-terized by apocarpous gynoecia with uniovulate car-pels (Endress & Igersheim, 1997). The carpels areborne in a more or less flat or concave floral cup (Per-kins & Gilg, 1901; Perkins, 1925; Endress, 1980a, b;Endress & Lorence, 1983; Lorence, 1985; Philipson,1986, 1993; Romanov & Bobrov, 2002).

Tambourissa

species have inferior ovaries congenitally fused withthe floral cup, which results in a kind of syncarpousgynoecium (Endress, 1979, 1980b; Endress & Lorence,1983; Lorence, 1985). The upper part of the floral cupeither abscises from the base just after anthesis(rarely the cup is small from the beginning withoutabscission necessary), or it encloses the developingfruitlets and grows with them up to maturity and thensplits open with irregular valves (Endress, 1980b;Lorence, 1985). In the first case, the unabscised baseof the floral cup expands only as much as to accommo-date the growing fruitlets and is commonly inconspic-uous at fruit maturity (e.g.

Steganthera

and

Wilkiea

species), or expands slightly more (

Levieria

), or the sti-pes of the druplelets slightly enlarge (

Steganthera

,

Mollinedia

), providing some colour contrast (see fig-ures in Renner & Hausner, 1997; Cooper & Cooper,2004). In the second case, the entire floral cup takesconsiderable part in the presentation of the fruitlets

by contrasting colours (e.g.

Hennecartia

,

Monimia

,

Palmeria

and

Tambourissa

species) (Perkins & Gilg,1901; Money

et al

., 1950; Endress, 1980b; Lorence,1985; Philipson, 1986, 1993). As the outer part of thepericarp of the fruitlets of many Monimiaceae

s.s

.appears to be fleshy or pulpy and the inner zone hard,the fruitlets of the representatives of the family haveusually been referred to as drupe(let)s (Baillon, 1867–69; Perkins & Gilg, 1901; Money

et al

., 1950; Takhta-jan, 1966, 1997; Corner, 1976; Cronquist, 1981;Lorence, 1985; Philipson, 1986, 1993). However, thatsuch superficially similar fruitlets may be internallydifferent has been shown by the genus

Amborella

,which was found to be unrelated to Monimiaceae butsister to all other extant angiosperms (e.g. Qiu

et al

.,1999), and in which the seeming druplets have a hardpart that is mainly derived from the mesocarp,whereas the endocarp is thin (Bobrov

et al

., 2005).This result in

Amborella

prompted us to undertake acomparative anatomical study on the fruit structure ina broad array of Monimiaceae

s.s

. in order to elucidatethe diversity and to pursue further the systematic sig-nificance of the fruits in basal angiosperms.

MATERIAL AND METHODS

Part of the studied material (Table 1) was dry, partwas fixed in FAA and stored in ethanol (70%). Dryfruitlets were treated in Strasburger solution (glyc-erin/ethanol); they were embedded in paraffin, andtransverse (TS) and longitudinal sections (LS) at 10–20

µ

m were made with a slide microtome. The sectionswere stained with phloroglucinol and hydrochloricacid to study details of lignification of cell walls in dif-ferent topographical zones of the pericarp, and werepreserved in glycerin. Standard morphological andanatomical procedures were used (Bondartzev, 1954;Prozina, 1960; O’Brien & McCully, 1981). The liquid-fixed fruitlets were embedded in Kulzer’s Technovit7100 [2-hydroxyethyl methacrylate (HEMA)], sec-tioned at 10

µ

m with a rotary microtome (Microm HM355), stained with ruthenium red and toluidine blue,and enclosed in Histomount (following Weber & Iger-sheim, 1994). The microtome sections were studiedwith light microscopy. Fruitlet structure was alsoexamined with scanning electron microscopy (‘HITA-CHI’ S-405-A and Camscan S-2), after critical-pointdrying and sputter-coating with gold–palladium.

RESULTS

All genera of Monimiaceae

s.s

. (except

Tambourissa

)have free carpels that develop into free fruitlets. Inthese the pericarp is differentiated into three histoge-netic zones (exocarp, mesocarp and endocarp) and intothree or more histological zones.

FRUIT STRUCTURE OF MONIMIACEAE

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2007,

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, 265–285

M

ONIMIA

ROTUNDIFOLIA

The several (5–10) carpels develop into few drupelets.They remain enclosed by the floral cup. Only at matu-rity does the floral cup dehisce into 3–5 irregularvalves and the irregularly flattened drupelets areexposed (Lorence, 1985) (Fig. 50). The inner surface ofthe floral cup forms a colour contrast with the drupe-lets (red vs. orange in

Monimia ovalifolia

; D. H.Lorence, pers. comm.).

The pericarp is differentiated into four distinct his-tological zones (Fig. 5). The first zone (the exocarp)consists of the one-cell-layered epidermis of small,flattened, ellipsoidal tanniferous cells, and with a thincuticle. The second and third zones are formed by themesocarp. The second zone consists of 3–8 layers ofthin-walled parenchymatic cells, interspersed withnumerous large, spherical–ellipsoidal, thin-walledresiniferous cells. The vascular system is situated inthe inner area of the second zone, with the vascularbundles situated above the ribs of the endocarp. Thethird zone consists of 1–5 layers of small, flattened,tangentially elongate cells with unevenly insignifi-cantly thickened cell walls, the zone of hydrocytes. Thefourth zone (the endocarp), making up about three-quarters of the pericarp thickness, is composed of 13–21 layers of large, isodiametric sclereids with thick-

ened, lignified, striate, canaliculate, broadly wavy cellwalls (Fig. 29). The innermost layers of the endocarpare formed by insignificantly tangentially orientatedsclereids. In the ventral median plane of the endocarpthere are two radial rows of smaller sclereids withsomewhat less thickened walls, which appear to resultin a fainter area of the putamen (Figs 28, 50). Theperiphery of the endocarp is irregularly zigzag-shapedin TS and LS. The cuticle of the inner epidermis isinconspicuous.

P

ALMERIA

SCANDENS

The several carpels develop into (few) drupelets. Theyremain enclosed by the floral cup. Only at maturitydoes the floral cup dehisce into several irregularvalves and the irregularly flattened drupelets areexposed. The red inner surface of the floral cup dis-plays a colour contrast with the black drupelets (Coo-per & Cooper, 2004; P.K.E., pers. observ.). The fruits of

P. gracilis

are similar (Fig. 1).The pericarp is differentiated into five distinct his-

tological zones (Figs 6, 30). The first zone (the exo-carp) is formed by the one-cell-layered epidermis ofellipsoidally rectangular cells with evenly thickenedcell walls, the cell walls dark by tannins, and with a

Table 1.

Investigated species and specimens

Hedycarya angustifolia

A.Cunn., mature fruits (liquid-fixed),

P.K. Endress

, #

5033

, Australia 1980 (Z)

Hedycarya arborea

J.R.Forst. & G.Forst., mature fruits (liquid-fixed),

P.K. Endress

, #

6390

, New Zealand 1981 (Z)

Hedycarya

cf.

chrysophylla

Perkins, mature fruits (liquid-fixed),

P.K. Endress

, #

6322

, New Caledonia 1981 (Z)

Hedycarya crassifolia

Gillespie, mature fruits (dry),

A.C. Smith

, #

5149

, Fiji 1947 (LE)

Hedycarya cupulata

Baill., mature fruits (dry),

G. McPherson

, #

1783

, New Caledonia 1979 (LE)

Hedycarya dentata

G.Forst., mature fruits (dry),

M. Hombron

, s.n., New Zealand 1841 (LE)

Hedycarya dorstenioides

A.Gray, mature fruits (dry),

A.C. Smith

, #

6954

, Viti Levu 1947 (LE)

Hedycarya parvifolia

Perkins & Schltr., mature fruits (dry),

G. McPherson

, #

1621

, New Caledonia 1979 (LE)

Hennecartia omphalandra

Poiss., mature fruits (dry),

J.E. Montes

, #

9515

, Brazil 1950 (LE)

Hortonia floribunda

Wight ex Arn., mature fruits (dry),

R. Wight, # 2491, Sri Lanka 1836 (LE)Hortonia ovalifolia Wight, mature fruits (dry), L. Bernardi, # 15947, Sri Lanka 1975 (LE)Kibara coriacea Hook.f. & Thomson, mature fruits (dry), M. Ramos, # 4317, Philippines 1923 (LE)Kibaropsis caledonica (Guillaumin) Jérémie, mature fruits (liquid-fixed), P.K. Endress, # 6311, New Caledonia 1981 (Z)Levieria nitens Perkins, mature fruits (dry), H.O. Forbes, # 702, New Guinea 1885–86 (LE)Matthaea pubescens Merr. ex Perkins, mature fruits (dry), A.D.E. Elmer, # 10699, Philippines 1909 (LE)Mollinedia elliptica A.DC., mature fruits (dry), L. Riedel & B. Luschnath, # 312, Brazil 1832 (LE)Mollinedia stenophylla Perkins, mature fruits (dry), L. Riedel & B. Luschnath, # 315, Brazil 1832 (LE)Monimia rotundifolia Thouars, mature fruits (dry), L. Boivin, # 1120, La Réunion, s.d. (LE)Peumus boldus Molina, mature fruits (dry), O. Zalensky, # 15, Chile 1968 (LE)Palmeria scandens F.Muell., mature fruits (dry), P. Melville, # 3613, Queensland, Australia 1953 (LE)Steganthera ilicifolia A.C.Sm., mature fruits (liquid-fixed), P.K. Endress, # 4074, Papua New Guinea 1977 (Z)Steganthera fengeriana Perkins, mature fruits (dry), T.G. Hartley, # 9967, New Guinea 1962 (LE)Steganthera salomonensis Philipson, mature fruits (dry), P.F. Hunt, # 2415, Solomon Islands, s.d. (LE)Tambourissa comorensis Lorence, mature fruits (dry), L. Bernardi, # 11803, Comores 1967 (LE)Tambourissa tau Lorence, mature fruits (liquid-fixed), D.H. Lorence, # 2950, Mauritius 1979 (Z)Tetrasynandra laxiflora Perkins, mature fruits (dry), M.S. Clemens, s.n., Queensland, Australia 1947 (LE)Wilkiea wardellii (F.Muell.) Perkins, mature fruits (dry), F. von Mueller, s.n., Queensland, Australia, s.d. (LE)

268 M. S. ROMANOV ET AL.

© 2007 The Linnean Society of London, Botanical Journal of the Linnean Society, 2007, 153, 265–285

thick, even cuticle. The second, third and fourth zonesare formed by the mesocarp. The second zone consistsof 1–2 layers of large, spherical or ellipsoidal, thin-walled resiniferous cells. The third zone is formed by5–6 layers of large, spherical, thin-walled ethereal oilcells, interspersed with few small, thin-walled cells.The vascular system is situated in the third zone. Thefourth zone is represented by 1–2 layers of small,ellipsoidal–angular hydrocytes with unevenly thick-ened cell walls. The fifth zone (the endocarp), repre-senting up to three-quarters of the pericarp thickness,is formed by 40–55 layers of isodiametric sclereidswith heavily thickened, lignified, striate, canaliculate,somewhat wavy cell walls (Fig. 31). In the ventralmedian plane of the endocarp there are 2(−5) radialrows of radially elongate, thick-walled sclereids,which appear to result in a fainter area of theputamen. The cuticle of the inner epidermis isinconspicuous.

PEUMUS BOLDUS

The 3–5 carpels develop into 2–5 drupelets (Perkins,1925). The upper part of the floral cup abscises with a

ring-shaped abscission zone (Martínez-Laborde, 1983;Philipson, 1993). However, it is not clear whether thistakes place in the ripe fruit or earlier. At maturity thedrupelets are exposed on the inner side of the remain-ing part of the floral cup.

The pericarp is differentiated into three histologicalzones (Figs 7, 32). The first zone (the exocarp) is rep-resented by a one-cell-layered epidermis of tangen-tially elongate, rectangular tanniferous cells withunevenly thickened cell walls and with a thick, evencuticle. The second zone (the mesocarp) consists of 15–25 layers of irregularly ellipsoidal, thin-walled tannif-erous cells, interspersed with large, spherical–ellipsoi-dal, thin-walled etheral oil cells. The vascular systemis situated in the middle part of the mesocarp. Thethird zone (the endocarp), representing up to four-fifths of the pericarp thickness, consists of 15–25 lay-ers of isodiametric sclereids with heavily thickened,lignified, striate, canaliculate, somewhat wavy cellwalls (Fig. 33). In the ventral median plane of theendocarp the putamen is interrupted by an area of few(2–3) radial rows of smaller-celled sclereids (Fig. 32).The cuticle of the inner epidermis is thin andinconspicuous.

Figures 1–4. Mature fruits. Fig. 1. Palmeria gracilis Perkins. Fig. 2. Tambourissa castri-delphinii Cavaco (courtesy W.Barthlott). Fig. 3. Hedycarya arborea. Fig. 4. Wilkiea huegeliana A.DC.

FRUIT STRUCTURE OF MONIMIACEAE 269


Figures 5–10. Schematic TS of pericarp of mature fruitlets (En = endocarp; Ex = exocarp; Fc = floral cup; M = mesocarp;dark grey = resin cells; light grey = ethereal oil cells; hatched = hydrocytes; black = tanniferous cells, also cells with tanninsin cell walls). Fig. 5. Monimia rotundifolia. Fig. 6. Palmeria scandens. Fig. 7. Peumus boldus. Fig. 8. Hortonia floribunda.Fig. 9. Tambourissa comorensis. Fig. 10. Kibaropsis caledonica. Scale bars: Figs 5–9 = 0.1 mm; Fig. 10 = 0.05 mm.



Figures 11–16. Schematic TS of pericarp of mature fruitlets (En = endocarp; Ex = exocarp; M = mesocarp; darkgrey = resin cells; light grey = ethereal oil cells; hatched = hydrocytes; black = tanniferous cells, also cells with tannins incell walls). Fig. 11. Levieria nitens. Fig. 12. Hedycarya cupulata, Fig. 13. Hedycarya dorrstenioides. Fig. 14. Mollinediaelliptica. Fig. 15. Mollinedia stenophylla. Fig. 16. Hennecartia omphalandra. Scale bars: Figs 11, 12, 14, 15 = 0.05 mm;Fig. 13 = 0.1 mm; Fig. 15 = 0.03 mm.



Figures 17–21. Schematic TS of pericarp of mature fruitlets (En = endocarp; Ex = exocarp; M = mesocarp; darkgrey = resin cells; light grey = ethereal oil cells; hatched = hydrocytes; black = tanniferous cells, also cells with tannins incell walls). Fig. 17. Wilkiea wardellii. Fig. 18. Kibara coriacea. Fig. 19. Steganthera salomonensis. Fig. 20. Tetrasynandralaxiflora. Fig. 21. Matthaea pubescens. Scale bars: Fig. 17 = 0.05 mm; Figs 18–21 = 0.1 mm.



Figures 22–27. Microtome TS of pericarp of mature or submature fruitlets (fruit in Fig. 27) (stained with ruthenium redand toluidine blue) (En = endocarp; Ex = exocarp; M = mesocarp; Sc = seed coat). Fig. 22. Tambourissa tau Lorence. Fig. 23.Kibaropsis caledonica Jérémie. Fig. 24. Hedycarya angustifolia A. Cunn. Fig. 25. Hedycarya arborea. Fig. 26. Stegantherailicifolia A.C. Sm. Fig. 27. Laurus nobilis L. (Lauraceae). Scale bars: Figs 22, 24–27 = 0.2 mm; Fig. 23 = 0.1 mm.



Figures 28–33. SEM micrographs of TS (LS in Fig. 28) of pericarp (En = endocarp; Eoc = ethereal oil cell; Ex = exocarp;M = mesocarp). Figs 28, 29. Monimia rotundifolia. Fig. 28. LS, endocarp with partly torn weaker area of small sclereids(arrow) in apical part, corresponding to the area with smaller sclereids on the ventral side. Fig. 29. Endocarp. Figs 30, 31.Palmeria scandens. Fig. 30. Lateral side, pericarp. Fig. 31. Endocarp. Figs 32, 33. Peumus boldus. Fig. 32. Ventral side,endocarp with radial area of small sclereids (narrow arrow); broad arrows point to vascular bundles. Fig. 33. Close-up ofouter part of pericarp. Scale bars: Figs 28, 30, 32 = 0.3 mm; Figs 29, 31, 33 = 0.03 mm.



HORTONIA FLORIBUNDA

The several carpels develop into few fruitlets. Atmaturity the shortly stipitate drupelets are presentedon the small, reflexed floral cup. The fruitlet outline iselliptic in TS (smaller in lateral direction than inmedian direction) (Fig. 51).

The pericarp is differentiated into four distinct his-tological zones (Figs 8, 34, 35). The first zone (the exo-carp) consists of the one-cell-layered epidermis oflarge roundish–rectangular cells, with evenly thick-ened walls, the walls dark by tannins and with a thickuneven cuticle. The second and third zones are formedby the mesocarp. The second zone consists of 20–28layers of thin-walled, irregularly ellipsoidal, some-what tangentially elongate cells, interspersed withnumerous large spherical–ellipsoidal, thin-walledresiniferous cells; there are also some large resinifer-ous sclereids with thickened, lignified cell walls. Tan-niferous cells are present in the outer 3–8 cell layers,and also cells with tannins in the cell walls. The vas-cular system is situated in the middle area of the sec-ond zone. The third zone comprises 2–6 layers ofangular–ellipsoidal, tangentially elongate hydrocyteswith reticulate cell-wall thickening. The fourth zone(the endocarp) consists of 3–6 layers of large, round-ish–multiangular resiniferous sclereids of unequalsize, with exceedingly thickened, lignified, striate,canaliculate cell walls. The endocarp (putamen) is pro-truding ventrally and dorsally in the median planeforming two ridges. The inner morphological surface issimilarly protruding but appears not to reach theperiphery of the endocarp, which results in two’valves’ (Figs 34, 35, 51). The cuticle of the inner epi-dermis is thin and even.

Hortonia ovalifolia differs by the presence of morenumerous resiniferous sclereids in the second zone,only 1–2 layers of hydrocytes forming the third zone,lesser thickening of the sclereid cell walls in theendocarp, and lack of ventral and dorsal ridges in theendocarp.

TAMBOURISSA COMORENSIS

The fruit in Tambourissa is unusual because the ova-ries are inferior, immersed in the floral cup, whichresults in an unusual kind of syncarpous fruit(Endress, 1980b; Endress & Lorence, 1983; Lorence,1985). Therefore, an exocarp that surrounds each indi-vidual ’fruitlet’ is not present (Fig. 36). However, eachcarpel differentiates histological structures that func-tionally correspond to a pericarp, which then sepa-rates from the tissue of the floral cup or neighbouringcarpels. Commonly in the genus the ’fruitlets’ areorange or red, surrounded by yellow or orange parts ofthe floral cup (Lorence, 1985) (Fig. 2).

The fruit wall is differentiated into five histologicalzones of which the third and fourth are similar to amesocarp and the fifth to an endocarp (Fig. 9). Thefirst zone, the outer epidermis, is part of the unitedcomplex of carpels and floral cup. The second zone isformed by up to 100 layers of isodiametric thin-walledcells interspersed with numerous spherical thin-walled ethereal oil cells and scattered solitary orgroups of 2–13 sclereids with thickened, lignified, stri-ate, canaliculate cell walls. The sclereids differ fromeach other in their wall thickness. In places the outercell layers of the second zone divide in tangentialdirection and form a periderm composed of up to10–15 indistinct cell layers. The third zone consists of15–30 layers of small, thin-walled fusiform cells, inter-spersed with numerous large, spherical–ellipsoidal,thin-walled resiniferous and ethereal oil cells. Thevascular system is situated in the third zone. Thefourth zone is represented by the one-cell-layeredinner hypodermis, which is composed of tangentiallyelongate, ellipsoidal hydrocytes with unevenly thick-ened cell walls. The fifth zone (the endocarp) consistsof 2–4(−5) layers of large unequal sclereids, with thick-ened, lignified, striate, canaliculate, pronouncedlywavy cell walls (Fig. 37). The cuticle of the inner epi-dermis is inconspicuous.

Tambourissa tau differs by fewer secretory cells (i.e.resiniferous and ethereal oil cells) in the third zone,and more pronouncedly tangentially elongate cellswith thickened and lignified cell walls in the fourthzone (Fig. 22).

KIBAROPSIS CALEDONICA

The 40–60 carpels develop into several red drupelets,which are presented on the reflexed floral cup(Jérémie, 1977). The fruitlet outline is circular in TS.

The pericarp is differentiated into four distinct his-tological zones (Figs 10, 23). The first zone (the exo-carp) consists of the one-cell-layered epidermis ofrather small, rectangular, thin-walled tanniferouscells and with a thick, wavy cuticle. The second andthird zones (the mesocarp) consist of 55–65 cell layers.The second zone is represented by 10–12 layers of rel-atively small, thin-walled parenchymatic cells, inter-spersed with small nests of up to c. 20 sclereids withthickened, lignified, striate, canaliculate cell walls.More than half of the thin-walled cells of this zone aretanniferous. The third (and thickest) zone is composedof relatively large parenchymatic cells, interspersedwith numerous scattered spherical–ellipsoidal, thin-walled resiniferous cells. In the inner part of this zonethere are numerous ethereal oil cells and very few sol-itary scattered sclereids with thickened, lignified, stri-ate, canaliculate, cell walls. The vascular system issituated in the third zone. The fourth zone (the



endocarp) consists of 7–10 layers of large unequalsclereids, with thickened, lignified, striate, canalicu-late, somewhat wavy cell walls. Some cells are mark-edly radially elongate. The cuticle of the innerepidermis is inconspicuous.

LEVIERIA NITENS

The numerous carpels develop into numerous sessilefruitlets, which are presented at maturity on thereflexed floral cup (Philipson, 1980). The fruitlet out-line is circular in TS.

The pericarp is differentiated into four distinct his-tological zones (Figs 11, 38). The first zone (the exo-carp) consists of the one-cell-layered epidermis ofangular, somewhat tangentially elongate cells, withunevenly thickened cell walls, and with an inconspic-uous cuticle. The second and third zones are formed bythe mesocarp. The second zone is composed of 25–39layers of small, nearly ellipsoidal, thin-walled paren-chymatic cells, interspersed with numerous large,spherical–ellipsoidal thin-walled resiniferous cells.The vascular system is situated in the inner area ofthe second zone. The third zone is irregularly thick,comprising 1–4 layers of angular–ellipsoidal, tangen-tially elongate hydrocytes with reticulate cell-wallthickening. The fourth zone (the endocarp) consists ofone layer of large, radially elongated sclereids, withheavily thickened, lignified, striate, canaliculate,broadly wavy cell walls (Fig. 39). The cuticle of theinner epidermis is inconspicuous.

HEDYCARYA CUPULATA

The 9–15 carpels develop into few black drupelets,which are presented at maturity on the reflexed floralcup (Jérémie, 1978). In H. arborea the drupelets areorange (Fig. 3). The fruitlet outline is circular in TS(Fig. 53).

The pericarp is differentiated into four distinct his-tological zones (Figs 12, 40). The first zone (the exo-carp) consists of the one-cell-layered epidermis oflarge ellipsoidally rectangular cells, with unevenlythickened walls, and is covered by a very thick, evencuticle. The second and third zones are formed by themesocarp. The second zone is represented by 10–14layers of thin-walled, fusiform parenchymatic cells,interspersed with numerous large spherical–ellipsoi-dal, thin-walled resiniferous cells. The thin-walledfusiform cells are smaller in the peripheral part ofthe second zone. The vascular system is situated inthe inner area of the second zone. The third zonecomprises 2–4 layers of nearly rectangular, tangen-tially elongate hydrocytes with reticulate cell-wallthickening. The fourth zone (the endocarp) consists ofone layer of large, radially elongate sclereids, with

heavily thickened, striate, canaliculate walls. Onlythe primary cell walls are lignified. The cell walls areheavily broadly wavy, which may give the wrongimpression of the endocarp as consisting of severalcell layers. The cuticle of the inner epidermis isinconspicuous.

Hedycarya parvifolia differs in more numerous celllayers of the second and third zones. In H. angustifo-lia, H. cf. chrysophylla and H. dorstenioides the secondzone is more multilayered, but, by contrast, the thirdzone is thinner and consists of a single layer of cres-cent-shaped hydrocytes (1–2 layers in H. cf. chryso-phylla and H. crassifolia) (Figs 13, 24, 41). InH. angustifolia and H. crassifolia the cells of theendocarp are two or more times shorter (in radialdirection) than in the other studied species. InH. arborea and H. dentata only a single zone is differ-entiated in the mesocarp, corresponding to the secondzone in H. cupulata (i.e. the zone of hydrocytes isabsent); in the mesocarp scattered nests of 1–5 sclere-ids with thickened, lignified cell walls are developed(Fig. 25).

MOLLINEDIA ELLIPTICA

The 10–12 carpels develop into few sessile drupelets.After anthesis the upper part of the floral cup abscisesfrom the lower part so that the fruitlets are not cov-ered during development. At maturity they are pre-sented on the reflexed floral cup (Perkins & Gilg,1901). The fruitlet outline is circular in TS (Fig. 52).

The pericarp is differentiated into five distinct his-tological zones (Figs 14, 42). The first zone (the exo-carp) consists of the one-cell-layered epidermis oflarge rectangular palisade cells, with unevenly thick-ened cell walls and triangular lumens, and with athick, even cuticle. The second, third and fourth zonesare formed by the mesocarp. The second zone is rep-resented by a one-cell-layered hypodermis composedof square–rounded cells with insignificantly thickenedcell walls. The vascular system is situated in the innerarea of the second zone. The third zone consists of 15–25 layers of ellipsoidally flattened, thin-walled cells,interspersed with numerous large, spherical–ellipsoi-dal, thin-walled resiniferous cells. Sometimes 1–3outer cell layers of the third zone are represented byrounded–rectangular, thin-walled cells. The fourthzone comprises 1–2 layers of rather large, ellipsoidal,tangentially elongate tanniferous hydrocytes. Thefifth zone (the endocarp) consists of 2–4 layers of largeunequal sclereids, with thickened, lignified, striate,canaliculate, pronouncedly broadly wavy cell walls(Fig. 43). The cuticle of the inner epidermis is incon-spicuous.

Mollinedia stenophylla differs in the number of celllayers and number of secretory cells (i.e. resiniferous



Figures 34–39. SEM micrographs of TS of pericarp (En = endocarp; Ex = exocarp; H = hydrocytes; M = mesocarp;Rc = resin cells; Sc = seed coat). Figs 34, 35. Hortonia floribunda (narrow arrow points to slit in endocarp; broad arrowpoints to vascular bundle). Fig. 34. Dorsal side. Fig. 35. Ventral side. Figs 36, 37. Tambourissa comorensis. Fig. 36. Partof two neighbouring ‘fruitlets’. Fig. 37. Endocarp. Figs 38, 39. Levieria nitens. Fig. 38. Pericarp. Fig. 39. Endocarp. Scalebars: Figs 34, 35, 37, 38 = 0.1 mm; Fig. 36 = 0.3 mm; Fig. 39 = 0.03 mm.



and etheral oil cells) in the mesocarp, and in cell struc-ture in the endocarp (Fig. 15).

HENNECARTIA OMPHALANDRA

Of the one or two carpels commonly one develops intoa drupelet (Endress, 1980b). The drupelet(s) remain(s)enclosed by the floral cup. Only at maturity does thefloral cup dehisce into several irregular valves, andthe black drupelet is presented on the orange cup sur-face (Martínez-Laborde, 1983). The fruitlet outline iscircular in TS.

The pericarp is differentiated into three histologicalzones (Fig. 16). The first zone (the exocarp) consists ofthe one-cell-layered epidermis of large, square, tannif-erous cells with unevenly thickened cell walls, andwith a very thick, wavy cuticle, and a single-layeredhypodermis of somewhat crushed rectangular, tannif-erous cells, which appears to be derived from the epi-dermis, as suggested by radial cell rows. The secondzone (the mesocarp) comprises 23–30 layers of rela-tively large parenchymatic cells, interspersed withnumerous large spherical–ellipsoidal, thin-walledresiniferous cells. In the peripheral area the thin-walled cells are smaller The vascular system is situ-ated in the middle part of the second zone. The inner-most layer of the second zone contains some sclereidswith thickened, lignified cell walls. The third zone (theendocarp) consists of a single layer of large, radiallyelongate sclereids, with heavily thickened, lignified,striate, canaliculate cell walls. The primary cell wallsare lignified more heavily. The cell walls are pro-nouncedly wavy, which may give the wrong impressionof the endocarp as consisting of several cell layers. Thecuticle of the inner epidermis is thin.

WILKIEA WARDELLII

The several carpels develop into few stipitate drupe-lets. After anthesis the upper part of the floral cupabscises from the lower part so that the fruitlets arenot covered during development. At maturity they arepresented on the reflexed yellow remnant of the floralcup. In W. wardellii the fruitlets are red but otherwisein the genus commonly black (Cooper & Cooper, 2004)(Fig. 4). The fruitlet outline is circular in TS.

The pericarp is differentiated into four histologicalzones (Figs 17, 44). The first zone (the exocarp) con-sists of the one-layered epidermis of rectangular tan-niferous cells and with a moderately developed evencuticle. The second and third zones are formed by themesocarp. The second zone is a one-cell-layered irreg-ular hypodermis of tanniferous cells, which are rathersmall as compared with the cells of the third zone. Thethird zone consists of 23–28 layers of large, thin-walled parenchymatic cells (some of which are tannif-

erous), interspersed with numerous large, spherical,thin-walled resiniferous cells. There are numerous sol-itary sclereids or groups of up to three isodiametricsclereids with markedly (or rarely insignificantly)thickened, lignified, striate, canaliculate cell walls.The vascular system is situated in the third zone. Thefourth zone (the endocarp) is composed of a singlelayer of rectangular sclereids with U-shaped,unevenly heavily thickened lignified, striate, canalic-ulate cell walls (Fig. 45). A cuticle is not apparent onthe inner epidermis.

KIBARA CORIACEA

The c. 20 carpels develop into few sessile berrylets.After anthesis the upper part of the floral cup abscisesfrom the lower part so that the fruitlets are not cov-ered during development. At maturity they are blackand are presented on the yellow to orange reflexedremnant of the floral cup (Philipson, 1985, 1986). Thefruitlet outline is circular in TS.

The pericarp is differentiated into five distinct his-tological zones (Figs 18, 46). The first zone (the exo-carp) consists of the one-cell-layered epidermis ofellipsoidal tanniferous cells with unevenly irregularlythickened cell walls and with a thick, even cuticle. Thesecond, third and fourth zones are formed by themesocarp, consisting of 37–43 cell layers. The secondzone is represented by 13–15 layers of spherical–ellip-soidal, thin-walled cells, some of them resiniferous(especially the outermost layer), and some tannifer-ous. The third zone comprises 10–15 layers of multi-angular, thin-walled cells, interspersed with numer-ous nests of 10–30 sclereids, with heavily thickened,striate, lignified, canaliculate cell walls. The fourthzone consists of 14–17 layers of somewhat tangentiallyelongate thin-walled cells, interspersed with spheri-cal, thin-walled ethereal oil cells and some tanniferouscells. The vascular system is situated in the fourthzone. The fifth zone (the endocarp) is composed of asingle layer of medium-sized, somewhat tangentiallyelongate, thin-walled cells. The cuticle of the inner epi-dermis is inconspicuous.

STEGANTHERA SALOMONENSIS

The numerous carpels develop into several stipitateberrylets. After anthesis the upper part of the floralcup abscises from the lower part so that the fruitletsare not covered during development. At maturity theyare presented on the reflexed remnant of the floralcup. The fruitlet outline is circular in TS.

The pericarp is differentiated into three distinct his-tological zones (Figs 19, 47). The first zone (the exo-carp) consists of the one-cell-layered epidermis withunevenly thickened cell walls, and with a thin cuticle.



Figures 40–45. SEM micrographs of TS of pericarp (En = endocarp; Ex = exocarp; H = hydrocytes; M = mesocarp;Rc = resin cell; Sc = seed coat). Fig. 40. Hedycarya cupulata. Pericarp. Fig. 41. Hedycarya dorstenioides. Pericarp. Figs 42,43. Mollinedia elliptica. Fig. 42. Pericarp. Fig. 43. Endocarp. Figs 44, 45. Wilkiea wardellii. Fig. 44. Pericarp. Fig. 45. Innerpart of pericarp. Scale bars: Figs 40–42, 45 = 0.1 mm; Fig. 43 = 0.03 mm; Fig. 44 = 0.3 mm.



The second zone (the mesocarp) is formed by 30–38layers of thin-walled cells, interspersed with numer-ous solitary or nests of 2–50 sclereids with thickened,lignified, striate, canaliculate cell walls. Most cells ofthe outer layers of the mesocarp are tanniferous andthere are numerous solitary and nests of 2–15 tannif-erous cells in the mesocarp. The inner 1–3 layers of themesocarp are represented by tangentially elongate,ellipsoidal, thin-walled parenchymatic cells. The vas-cular system is situated in the second zone. The thirdzone (the endocarp) contains a single layer of thin-walled, tanniferous epidermal cells with an inconspic-uous cuticle.

Steganthera ilicifolia and S. fengeriana differ inpericarp thickness (up to 25–32 cell layers inS. ilicifolia; 50–60 cell layers in S. fengeriana)(Fig. 26).

TETRASYNANDRA LAXIFLORA

The numerous carpels develop into several stipitatedrupelets. After anthesis the upper part of the floralcup abscises from the lower part so that the fruitletsare not covered during development. At maturity theyare black and are presented on the reflexed yellow–green or yellow–orange remnant of the floral cup(Cooper & Cooper, 2004). The fruitlet outline is circu-lar in TS.

The pericarp is differentiated into five distinct his-tological zones (Fig. 20). The first zone (the exocarp)consists of the one-layered epidermis of rather small,rectangular cells with thickened outer and inner tan-gential cell walls and an even, thin cuticle. The second,third and fourth zones are formed by the mesocarp,which consists of 85–100 cell layers. The second zoneis represented by 1–2 layers of an interrupted hypo-dermis of small, somewhat ellipsoidal tanniferouscells. The third, most massive, zone is composed oflarge sclereid nests of 50–200 sclereids, which are sep-arated from each other by several layers of thin-walledcells, and scattered spherical–ellipsoidal, thin-walledresiniferous cells. The central zones of the sclereidnests are formed by sclereids with thick, lignified, stri-ate, canaliculate cell walls, from which numerousthin-walled sclereids radiate. There are also solitaryor groups of 10–20 rather large, thin-walled, tannifer-ous cells. Some sclereids are also tanniferous. The vas-cular system is situated in the third zone. The fourthzone comprises 7–13 layers of large, spherical, thin-walled resiniferous cells, interspersed with scatteredsmall, thin-walled cells. The inner 1–3 irregular layersof this zone are composed of pointed small cells. Thefifth zone (the endocarp) is composed of a single layerof medium-sized, somewhat radially elongate (pali-sade) sclereids with unevenly thickened, lignified,striate, canaliculate cell walls; the radial walls are

thickened more strongly. The cuticle of the inner epi-dermis is inconspicuous.

MATTHAEA PUBESCENS

The numerous carpels develop into numerous stipitatedrupelets (Philipson, 1986: fig. 24, for M. sancta).After anthesis the upper part of the floral cup abscisesfrom the lower part so that the fruitlets are not cov-ered during development. At maturity they are pre-sented on the reflexed remnant of the floral cup(Philipson, 1986). The fruitlet outline is roundish–quadrangular in TS.

The pericarp is differentiated into six distinct histo-logical zones (Figs 21, 48). The first zone (the exocarp)consists of the one-cell-layered epidermis of large,radially elongate, ellipsoidal, tanniferous cells ofunequal size, and is covered by a very thick cuticle.The second, third, fourth and fifth zones are formed bythe mesocarp, which consists of 20–33 cell layers. Thesecond zone is represented by 1–3 layers of inter-rupted hypodermis of ellipsoidal tanniferous cells,interspersed with large spherical–ellipsoidal, thin-walled resiniferous cells. The third zone is representedby 7–10 layers of thin-walled parenchymatic cells,interspersed with numerous solitary and nests of 2–15sclereids with insignificantly thickened, lignified, stri-ate, canaliculate cell walls. The fourth zone consists of7–21 layers of fusiform, tangentially elongate, thin-walled cells. The vascular system is situated in thefourth zone. The fifth zone is composed of a singlelayer of ellipsoidal, tangentially elongate cells withinsignificantly thickened cell walls (supposedly thezone of hydrocytes). The sixth zone (the endocarp) iscomposed of a single layer of large, markedly radiallyelongate sclereids with thickened, lignified, striate,canaliculate, broadly wavy cell walls (Fig. 49). Somecells of the endocarp are somewhat ellipsoidal and areresiniferous. The cuticle of the inner epidermis isinconspicuous.

DISCUSSION

COMPARATIVE FRUIT STRUCTURE AND RELATIONSHIPS WITHIN MONIMIACEAE S.S.

Based on the anatomical differentiation of the peri-carp, two general fruit forms were found in Monimi-aceae s.s.: apocarpous drupelets with a more or lessstrongly developed putamen formed by the lignifiedendocarp and apocarpous berrylets. In addition,endocarp differentiation allows us tentatively to dis-tinguish four different types of drupelets:

1. Monimia-type (Fig. 50). The endocarp is differenti-ated into a very massive, many-cell-layered puta-men (up to 55 layers of more or less isodiametric



Figures 46–49. SEM micrographs of TS of pericarp (En = endocarp; Ex = exocarp; M = mesocarp; Rc = resin cell;Sn = sclereid nest). Fig. 46. Kibara coriacea. Fig. 47. Steganthera salomonensis. Figs 48, 49. Matthaea pubescens. Fig. 48.Pericarp. Fig. 49. Endocarp. Scale bars: Fig. 46 = 0.1 mm; Figs 47, 48 = 0.3 mm; Fig. 49 = 0.06 mm.

Figures 50–53. Schematic TS of drupelets representing the four types here distinguished, ventral side up (endocarp grey,vascular bundles indicated). Fig. 50. Monimia-type (Monimia rotundifolia). Fig. 51. Hortonia-type (Hortonia floribunda).Fig. 52. Mollinedia-type (Mollinedia elliptica) (inset: close up of endocarp). Fig. 53. Hedycarya-type (Hedycarya dorstenio-ides) (inset: close up of endocarp). Scale bar = 1 mm.



sclereids, which forms about three-quarters of thepericarp thickness). This type was found in Mon-imia, Palmeria and Peumus.

2. Hortonia-type (Fig. 51). The endocarp is differenti-ated into a massive, many-cell-layered putamen(up to six layers of isodiametric, exceedingly thick-walled sclereids), which makes up less than one-half of the pericarp thickness. The putamen may bedifferentiated into two lateral halves, i.e. with thesclerechyma partially interrupted on the ventraland dorsal sides (but without radial rows of smallsclereids). This type was found in Hortonia.

3. Mollinedia-type (Fig. 52). The endocarp is differen-tiated into a few-cell-layered putamen (two to sev-eral layers of more or less radially elongatesclereids with wavy cell walls). It forms less thanhalf or less than one-fifth of the pericarp thickness.This type was found in Mollinedia, and to someextent in Kibaropsis (and Tambourissa).

4. Hedycarya-type (Fig. 53). The endocarp is differen-tiated into a one-cell-layered putamen of usuallypronouncedly radially elongate sclereids with wavycell walls. It forms up to half of the pericarpthickness. This type was found in Hedycarya,Hennecartia, Levieria, Matthaea, Tetrasynandraand Wilkiea.

The endocarp in Wilkiea wardellii is markedlyreduced and is represented by relatively small cellswith uneven U-shaped thickening of the cell walls. InTetrasynandra laxiflora the endocarp is also notablyweakly developed (but is still represented by rectan-gular palisade sclereids with lignified cell wall), andthere are large concentric nests of sclereids in themesocarp. The fruit of these two latter species could beviewed as transitional between drupelets and ber-rylets. The apocarpous berrylets lack sclerified (ligni-fied) cells in the endocarp (there is only a single layerof thin-walled cells) but also contain large nests ofsclereids in the middle zone of the mesocarp. They arecharacteristic of Kibara and Steganthera species (seealso Bobrov et al., 2003b).

In contrast to the Hortonia-type, in the drupelets ofthe Mollinedia-type, the endocarp cells are somewhatradially elongate and their lignified walls are wavy.This provides more intensive contact between the cellsand therefore potentially increased protection of theseeds from dispersers, such as birds. The number ofendocarp cell layers in the Mollinedia-type is aboutthe same as or more than in the Hortonia-type. Reduc-tion in the number of cell layers of the endocarp to one,but with more pronounced elongation of cells in theradial direction together with the differentiation ofconspicuously wavy cell walls may have given rise tothe Hedycarya-type of drupelets. The Hedycarya-typemay be the most advanced of all drupelets in the Mon-

imiaceae studied, and a number of variations of thesingle-cell-layered endocarp structure can be observedas to different size and form of cells and thickness ofcell walls. Fruitlets as in Kibaropsis may be viewed asintermediate between the Mollinedia-type and theHedycarya-type. If the Mollinedia-type is more ances-tral than the Hedycarya-type, the latter may havearisen twice or more: in South America and again inAustralasia, as based on molecular analyses (Renner,1998, 2002) the South American Hennecartia appearsto be related to Mollinedia, whereas the Old WorldKibaropsis is probably related to Hedycarya and Levi-eria. Tetrasynandra laxiflora (but not the other Tetra-synandra species) should probably be included inSteganthera based on floral structure (P.K.E., unpubl.data). This may be concordant with unusualendocarps: single-layered, markedly reduced scleren-chymatic endocarp in the former, and single-layeredparenchymatic endocarp in the latter. However, theseinterpretations of fruit relationships within Mol-linedioideae remain tentative as long as the phyloge-netic relationships are not clearly resolved.

Of special interest is that the distinction of threemajor clades in Monimiaceae s.s., (1) Peumus + Palm-eria + Monimia (Monimioideae), (2) Hortonia (Hor-tonieae of Mollinedioideae), and (3) the remainder ofMollinedioideae, as shown by molecular phylogeneticstudies (Renner, 1998, 1999, 2002), is also well sup-ported by the present carpological and other struc-tural data (Philipson, 1993; Romanov & Bobrov, 2002;this study). Monimioideae (clade 1) are characterizedby the Monimia-type of drupelets, Hortonieae of Mol-linedioidae (clade 2) by the Hortonia-type, and theremainder of Mollinedioideae (clade 3) by the Mol-linedia-type and Hedycarya-type or, in the extreme, byberrylets. The fruits of Hortonia also differ from theother genera of Mollinedioideae by their fruitlet shapeas seen in TS, which is elliptic (with smaller diameterin lateral than in median direction) in Hortonia andcircular in the other Mollinedioideae.

COMPARISON OF FRUITS OF MONIMIACEAE S.S. WITH THOSE OF OTHER BASAL ANGIOSPERMS

Close relationships of Monimiaceae and Lauraceaehave long been recognized (Takhtajan, 1966, 1997;Endress, 1972, 1980b; Cronquist, 1981; Philipson,1993), and were supported by molecular phylogeneticstudies (Renner, 1999; Qiu et al., 1999, 2005; Renner& Chanderbali, 2000; Soltis et al., 2000), and also bycombined molecular and morphological phylogeneticstudies (Doyle & Endress, 2000; Doyle, 2005). The car-pological data presented here also support this inter-pretation. Although in Lauraceae, in contrast toMonimiaceae s.s., the gynoecium is consistently mono-merous, and the floral cup is commonly less pro-



nounced (Kostermans, 1957; Endress, 1980b; Hyland,1989; Rohwer, 1993), the anatomical structure of somelauraceous fruits is similar with the Hedycarya-type offruitlets of Monimiaceae s.s. The most prominent char-acter of these fruit(let)s is that their endocarp isformed by a single layer of palisade sclereids withthickened, lignified walls (Melikian & Dzhalilova,2003) (Fig. 27). Thus, the two families appear to sharean apomorphic trend in fruit structure. It would be ofinterest to know more about the fruits of the ’basal’Lauraceae, Hypodaphnis and Cryptocaryeae (Rohwer& Rudolph, 2005).

Siparunaceae and Gomortegaceae are two otherfamilies of Laurales with drupe(let)s. In Gomorteg-aceae the two to three united carpels form a fruit witha thick and extremely hard stone (Heo et al., 2004). InSiparuna (Siparunaceae), the free carpels develop intodrupelets (Corner, 1976; Kimoto & Tobe, 2003). Inmost species, the floral cup of the mature fruit splitsinto irregular valves, and the drupelets are presentedon the inside of the opened floral cup, and, together,they form a colour contrast, comparable with thefruits in Monimia, Palmeria and Hennecartia. In addi-tion, the drupelets form a coloured fleshy outgrowth,which further adds to the colour contrast, and thefruitlets look like seeds with an aril (Endress, 1973;Renner & Hausner, 1997). Only in few Siparunaspecies does the floral cup never dehisce (Renner &Hausner, 2005).

In contrast to the similarities in fruit morphologyand anatomy between these four families of Laurales(particularly between Monimiaceae s.s. and Lau-raceae), fruit anatomy of these families considerablydiffers from that of basalmost angiosperms (ANITAgrade), despite superficial resemblances. In Ambo-rella, the hard part of the fruitlets is mainly formed bya massive sclerified layer of the mesocarp, whereas thesclerified endocarp is only thin (Bobrov et al., 2005). Inaddition, lignification of these sclerified cells is lackingor occurs only in late developmental stages. Fruitanatomy of Nymphaeales is poorly known. However,they do not seem to be sclerified, as maturation andseed dispersal is under water. Fleshy-fruited Aus-trobaileyales do not have sclerified layers in the peri-carp, only in the seed coat (Austrobaileyaceae,Endress, 1980c, 1983; Trimeniaceae, Endress & Samp-son, 1983; Bobrov et al., 2002; Schisandraceae, Saun-ders, 2000; Denk & Oh, 2005). The same is true forChloranthaceae (Endress, 1987), the phylogeneticposition of which is not yet settled (Doyle & Endress,2000; Qiu et al., 2005). In contrast to Laurales, inwhich the endotesta commonly appears to be sclerifiedin the seed (Kimoto & Tobe, 2001), in basalmostangiosperms either the exotesta (Nymphaeales, Aus-trobaileyales pro parte) (Corner, 1976; Melikian, inTakhtajan, 1988) or the mesotesta or both (Aus-

trobaileyales pro parte) (Melikian, in Takhtajan, 1988;P.K.E., pers. observ.) is sclerified, or the seed coat isnot sclerified (Amborella) (P.K.E., pers. observ.).

In the context of the entire basal angiosperms,drupes or drupelets appear to be rare (Endress, 1996).Fleshy fruits commonly do not form a putamen(Takhtajan, 1988; Romanov, 2004; for other Laurales,see Mohana Rao, 1986; for Magnoliales, see Endress,1983; Mohana Rao, 1983; van Setten & Koek-Noorman, 1992; Melikian, Bobrov & Romanov, 2002).Exceptions, in addition to the Laurales discussed here,are some Piperaceae (Piperales) with a thin, sclerifiedendocarp (e.g. Kanta, 1962; Palmarola Bejerano,2003), and Himantandraceae (Magnoliales), in whicheach mature carpel has a separate putamen (e.g.Endress, 1983); however, fruit development of the lat-ter has not been studied as yet.

In general, fruit anatomy and development in basalangiosperms are understudied (Endress, 1996). Thisand other studies show the promising systematicsignificance of these reproductive traits in basalangiosperms (Romanov, 2004). Not only may superfi-cially similar fruits of unrelated taxa reveal anatomi-cal differences, as discussed above, but also thereverse may be found. For example, achene-like fruit-lets of Atherospermataceae differ strongly from drupe-like fruitlets of other Laurales in their superficialappearance and mode of dispersal. Nevertheless, theanatomical structure of their pericarp is similar tothat in Monimiaceae s.s. and Lauraceae; although thepericarp is thin and dry, the endocarp is always rep-resented by one or two cell layers with thickened, lig-nified cell walls (Bobrov et al., 2003a; Bobrov, Sorokin& Romanov, 2004). Another example of apparent ana-tomical conservatism despite fruit diversity is pro-vided by the Rhamnaceae (Vikhireva, 1952). Ingeneral, it appears that there is much convergence insuperficial mature fruit structure, whereas fruitanatomy and development reveal more features ofsystematic significance (e.g. Melikian, 1996). Betterknowledge of fruit anatomy of extant plants will alsohelp to integrate more intensively fossil fruits into sys-tematic and evolutionary studies of angiosperms.

ACKNOWLEDGEMENTS

We thank David H. Lorence for providing pickledfruits of Tambourissa tau and for information on Mon-imieae. Rosemarie Siegrist is thanked for microtomesections, and Alex Bernhard for support with someillustrations. We thank Nina B. Sheremet and Alex-ander Sennikov for assistance with the collection offruit samples. Wilhelm Barthlott is thanked for Figure2. The study was supported by the Russian Founda-tion for Basic Research (grants # 05-04-49204-a and05-04-49143-a).



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