Plant Syst Evol (2008) 275:69–91 DOI 10.1007/s00606-008-0055-6
ORIGINAL ARTICLE
Structure, development and evolution of the androecium in Adansonieae (core Bombacoideae, Malvaceae s.l.) Heidrun Janka Æ Maria von Balthazar Æ William S. Alverson Æ David A. Baum Æ Joa˜o Semir Æ Clemens Bayer
Received: 20 August 2007 / Accepted: 29 April 2008 / Published online: 25 July 2008 Ó Springer-Verlag 2008
Abstract Androecium development and vasculature were studied in nine species of the Adansonieae clade (core Bombacoideae, Malvaceae s.l.). In early androecium development either distinct pentagonal androecial ring walls or five common petal/androecium primordia are present. Ring walls give rise to five antepetalous and five alternipetalous primary androecial primordia. Common primordia divide into peripheral petal primordia and antepetalous primary androecial primordia. Antepetalous primary androecial primordia split anticlinally into ten H. Janka (&) C. Bayer Palmengarten der Stadt Frankfurt am Main, Frankfurt am Main, Germany e-mail:
[email protected] H. Janka Institute for Ecology, Evolution and Diversity, University of Frankfurt, Frankfurt am Main, Germany H. Janka Department of Botany and Molecular Evolution, Senckenberg Research Institute, Frankfurt am Main, Germany M. von Balthazar Department of Paleobotany, Swedish Museum of Natural History, 10405 Stockholm, Sweden W. S. Alverson Environmental and Conservation Programs, The Field Museum, Chicago, IL, USA D. A. Baum Department of Botany, University of Wisconsin, Madison, WI, USA J. Semir Departamento de Botaˆnica, Instituto de Biologia, Universidade Estadual de Campinas, Campinas, Sao Paulo, Brazil
primordia-halves, on which secondary androecial primordia are initiated in a centrifugal succession. Androecial lobes are formed by fusion of an alternipetalous primary androecial primordium and its two neighbouring antepetalous primary primordia-halves, a pattern that also occurs in other Malvatheca. Later, tertiary androecial primordia are formed by the subdivision of secondary androecial primordia (except in Adansonia and Ceiba). Each tertiary primordium differentiates into a two-locular androecial unit. At anthesis these two-locular androecial units are often present in pairs, corresponding to the two halves of the same secondary androecial primordium. Androecium development and vasculature imply that the alternipetalous androecial sectors have been reduced in Bombacoideae, a tendency that is shared with other subfamilies of Malvaceae. Keywords Androecium structure Androecium development Malvatheca Malvaceae Bombacoideae Adansonieae
Introduction Recent molecular phylogenetic studies have identified the well-supported evolutionary lineage Malvatheca, within the newly circumscribed Malvaceae s.l., which includes the four traditional families Bombacaceae, Malvaceae s.str., Sterculiaceae, and Tiliaceae (Alverson et al. 1998, 1999; Bayer et al. 1999; Baum et al. 2004; Nyffeler et al. 2005). The Malvatheca lineage comprises two large wellsupported clades, Bombacoideae and Malvoideae, and at least one additional smaller clade (Alverson et al. 1999; Baum et al. 1998, 2004; Bayer et al. 1999). The relationships among these lineages are, however, still largely
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unresolved (Alverson et al. 1999; Bayer et al. 1999; Baum et al. 2004; Nyffeler et al. 2005). Core Bombacoideae includes most genera of the former family Bombacaceae: 14 genera and approximately 160 species (Bayer and Kubitzki 2003). Within core Bombacoideae, the data support a subdivision into a small clade (the ‘‘Gyranthera clade’’) composed of Gyranthera, Huberodendron and Bernoullia and a larger clade (the ‘‘Adansonieae clade’’), which includes the remaining 11 genera (e.g. Adansonia, Bombax, Cavanillesia, Ceiba s.l., and Pachira s.l. (see Fig. 1). The distinction between these two subclades is consistent with their differences in floral morphology (Baum et al. 2004). Whereas members of the Gyranthera clade and other deep-branching genera of the Malvatheca clade (e.g. Ochroma, Patinoa, see von Balthazar et al. 2006) have elongated, sessile two-locular androecial units, the majority of Adansonieae have small and individually stalked twolocular structures that resemble those found in core Malvoideae (von Balthazar et al. 2004). The two-locular androecial units of Adansonieae have often been referred to as ‘‘monothecate stamens’’ (e.g. Eichler 1875/1878; Hirmer 1918; van Heel 1966; Rohweder 1972). However, until their nature is clarified, we here prefer to use the more
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neutral term ‘‘androecial units’’. Previous analyses have suggested that the stalked two-locular androecial units of core Malvoideae and Adansonieae evolved independently from elongated, sessile two-locular androecial units (Alverson et al. 1999; Baum et al. 2004; von Balthazar et al. 2006). Information on floral structure and development of the Adansonieae clade is scarce. A few studies have provided detailed descriptions of the anthetic flowers of single genera or species, often in the context of taxonomic research: e.g. Bombax (Davis and Ghosh 1970; Neubauer 1989) and Ceiba (Schumann 1890; Gibbs et al. 1988; Gibbs and Semir 2003). Likewise, most of the studies on floral structure and vasculature have focused at the generic level (Bombax: Rao 1952; Davis and Mariamma 1965; Davis 1966; Ceiba: Davis and Kundu 1965; Gibbs et al. 1988; Gibbs and Semir 2003). Among broader comparative studies such as Eichler (1875/1878), Robyns (1963) and van Heel (1966), only the study of van Heel (1966) focused on floral development and vasculature. A more comprehensive comparative study of early androecium development could greatly enhance understanding of androecium structure and evolution in the Adansonieae clade. Recent comparative structural studies have much contributed to our knowledge of androecium evolution in other groups of Malvaceae (von Balthazar and Nyffeler 2002; von Balthazar et al. 2004, 2006). A further aim of this study is to analyze the developmental origins and nature of the stalked two-locular androecial units of Adansonieae.
Materials and methods
Fig. 1 Relationships among major lineages of Bombacoideae (modified after Baum et al. 2004). The earliest branching events within Malvatheca lack clear resolution among five clades: core MalvoideaeMatisieae, core Bombacoideae, Ochroma-Patinoa, Fremontodendreae (Chiranthodendron/Fremontodendron), and Septotheca. Sequence data of matK suggests that Fremontodendreae are sister to the rest of Malvatheca. A clade comprising Gyranthera and Huberodendron is sister to the remainder of core Bombacoideae. Within Adansonieae, a Catostemma-Scleronema clade is tentatively placed as sister to the remainder of Adansonieae
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Morphological, anatomical and developmental studies were conducted from the species listed in Table 1. Flowers and floral buds were fixed in FAA or 70% ethanol and subsequently stored in 70% ethanol. For serial microtome sections, medium sized buds were embedded in Kulzer0 s Technovit (2-hydroethyl methacrylate), as described in Igersheim (1993) and Igersheim and Cichocki (1996), and sectioned. The 5–8 lm-thick sections were stained with ruthenium red and toluidine blue. All the sections were mounted in Histomount. For SEM studies, specimens were dehydrated in an ethanol series, critical-point dried, sputter-coated with gold, and studied at 5 kV in a CamScan CS2 SEM and Hitachi S570 SEM. Alcohol material and section vouchers of the taxa investigated are deposited at the Palmengarten Frankfurt am Main, Germany and the Swedish Museum of Natural History in Stockholm, Sweden. For definitions of descriptive terms, see Table 2.
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Table 1 Specimens investigated Taxa
Voucher information
Origin of sample
Adansonia digitata L.
W. H. van Heel 1964, S
Unknown
Adansonia gibbosa (A. Cunn.) Guymer ex D.A. Baum
D. A. Baum s.n., S
Madagascar
Adansonia za Baill.
D. A. Baum s.n., S
Madagascar
Bombax ceiba L.
W. H. van Heel 578, S
Unknown
Ceiba pentandra (L.) Gaertn.
W. H. van Heel 586, S
Unknown
Eriotheca sp.
L. Y. S. Aona 845, S
Unicamp, Campinas, Brazil
Pachira aquatica Aubl.
J. J. F. E. de Wilde s.n., S M. von Balthazar & J. Scho¨nenberger JS609, S
Cult. Jardin du Centre Nederlandais, Ivory Coast Cult. Tenom Agriculture Station, Borneo, Malaysia
M. von Balthazar 02–15, S
Cult. Olbrich Botanical Garden, Wisconsin, USA
s. coll., V. E. Caracas 01.01.1998, FRP 5041 M. von Balthazar & J. Scho¨nenberger JS732, S
Cult. Fairchild Tropical Garden, Florida, USA
H. Janka HJ01–04, 23.04.2001, FRP
Cult. Palmengarten Frankfurt am Main, Germany
Pachira insignis Sav. Pseudobombax ellipticum
Caracas, Venezuela
(H.B.K.) Dugand
Table 2 Definition of Descriptive Terms Term
Definition
Androecium ring wall
Continuous ring-like meristematic bulging of the floral apex from which primary androecial primordia eventually differentiate
Common petal/androecial primordium
Common primordium of petal and stamens that subsequently subdivides into a peripheral petal primordium and a more central primary androecium primordium
Androecial lobe
One of five radial bulgings of the androecium ring wall that arises in alternipetalous position and comprises one alternipetalous androecial sector and two antepetalous androecial half-sectors
Primary androecial primordium = androecial sector
One radial segment on the androecium ring wall that gives rise to secondary androecial primordia
Secondary androecial primordium
First undivided and undifferentiated structure arising from a primary androecial primordium
Tertiary androecial primordium
Undifferentiated protuberance after subdivision of a secondary androecial primordium
Androecial unit
Two-locular structure differentiating from a secondary or tertiary androecial primordium bearing either a filament or not (if sessile); the term ‘‘Andro¨cial-Einheiten’’ was already used by Rohweder (1972)
Filament tube
Congenitally fused tubular structure formed by the filaments above the corolla
Results Developmental patterns and morphological characters of the androecium in Adansonieae Young floral buds are enclosed in three epicalyx lobes (or bracts). The perianth is usually pentamerous. Sepal primordia arise in a more or less pronounced quincuncial succession. The calyx tube is considerably longer than the free portions of the sepals which are valvate. The petals in bud exceed the calyx in length (except in Adansonia and some Pachira spp.) and usually show contorted estivation. The petal bases are fused with the filament tube. At anthesis,
the androecium of most of the investigated species consists of numerous (sometimes more than 1,000) stalked, more or less reniform, two-locular androecial units. The filaments of the androecial units are fused to various degrees at their bases: they may form a filament tube and/or groups (phalanges) of a few to numerous filaments. In most studied species, androecium development starts with the formation of a more or less distinct, pentagonal androecial ring wall. Primary androecial primordia either arise as distinct primordia on the ring wall (Ceiba pentandra, Bombax ceiba, Pachira aquatica, Pseudobombax ellipticum and presumably Adansonia spp.), or as common primordia with the petals (Pachira insignis). In the later
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case the common primordia subsequently divide to form peripheral petal primordia and more central primary androecial primordia. Petals alternate with the sepals. The five antepetalous primary androecial primordia (or antepetalous androecial sectors; for definitions see ‘‘Materials and methods’’) split radially and differentiate into ten primordia-halves. The five alternipetalous primary androecial primordia (or alternipetalous androecial sectors) vary in size. Secondary androecial primordia arise on the primary androecial primordia in a centrifugal (centripetal in Adansonia gibbosa) pattern. On the antepetalous primary androecial primordia a variable number of secondary androecial primordia are initiated, between one (Ceiba pentandra) and several hundreds (Adansonia digitata). On the alternipetalous primary androecial primordia, usually a single secondary androecial primordium arises in a central position (Pachira aquatica, Eriotheca sp.) or on the tip of an androecial lobe (Pseudobombax ellipticum). Later in development, secondary androecial primordia subdivide into two tertiary androecial primordia, which later differentiate into two-locular androecial units each. However, in all studied Adansonia species and Ceiba pentandra, twolocular androecial units seem to differentiate directly from secondary androecial primordia (i.e. without further subdivision). Ovaries are 5–10-locular, syncarpous and superior with many ovules per locule. In gynoecium development, carpel primordia (in 5-carpellate gynoecia) arise opposite the petals. Adansonia gibbosa The androecium originates from a pentagonal ring wall, the corners of which alternate with the petals (Fig. 2a, b). About 40 secondary androecial primordia (already somewhat differentiated in Fig. 2a, b) develop on the rim of the ring wall. They appear to form groups of four to six secondary androecial primordia (alt as, Fig. 2a, b) in alternipetalous positions, and groups of two to four secondary androecial primordia in antepetalous positions (an as, Fig. 2a, b). The alternipetalous androecial primordia are slightly more advanced in their development than the antepetalous ones. Numerous additional secondary androecial primordia are initiated in a centripetal succession on the inner slopes of the androecial ring wall (Fig. 2a), while each peripheral secondary androecial primordium differentiates into a two-locular androecial unit (Fig. 2a, b, e). The secondary androecial primordia on the inner ring wall slopes also differentiate into androecial units in their order of initiation (Fig. 2c, d). At anthesis, numerous stomata are found in the epidermal area between filament and theca (Fig. 2f, g). Approximately 200 androecial units are present in the anthetic flower.
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Petal and androecial vascular bundles are inferred to unite into five common androecium/petal traces at the floral base. The androecial vascular bundles are arranged in a vascular ring complex at the base of the androecial tube and are surrounded by five petal vascular traces (Fig. 3a–d). More distally, androecial bundles branch off in a centripetal series, and divide again until each two-locular androecial unit is supplied by one vascular bundle (Fig. 3e–g). Adansonia za Numerous secondary androecial primordia develop on a slightly elevated pentagonal androecial ring wall in a centrifugal succession (Fig. 2h, i). The five secondary androecial primordia in the central and alternipetalous positions appear to be most advanced in their development (Fig. 2h, i). Each secondary androecial primordium differentiates into a two-locular androecial unit (Fig. 2j). At anthesis, the 100–150 androecial units have long filaments that are fused at their base to form a long filament tube. Adansonia digitata The androecial ring wall is massive when compared to the other Adansonia species studied (Fig. 2k–m). Numerous secondary androecial primordia arise centrifugally on the androecial ring wall (Fig. 2k, m). They do not form distinct groups. When the first secondary androecial primordia have differentiated into two-locular androecial units, additional androecial primordia are still being initiated at the base of the still enlarging androecial ring wall (Fig. 2m). More than 1,000 androecial units may ultimately be formed. Bombax ceiba During late stages of floral development (younger buds were not available), the filament tube with already differentiated androecial units is visible (Fig. 4a). The centralmost androecial units are further advanced in their development than the peripheral ones and indicate a centrifugal pattern of development. Each androecial unit has two elongate, convoluted pollen sacs (Fig. 4a). The peripheral androecial units are more numerous than the central ones. At anthesis, the 75–100 androecial units are elongated (Fig. 4b) and have numerous stomata in the transition area between filament and theca (Fig. 4c). At the base of the filament tube, five androecial vascular bundle pairs, corresponding to the five antepetalous androecial sectors, branch from five common androecium/petal traces (Fig. 5a, b). Additional vascular bundles are found in some of the alternipetalous androecial sectors (Fig. 5a). They join the petal/
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Fig. 2 Adansonia. Androecium development and androecium structure. All sepals removed, all petals removed except in k, l. a–g Adansonia gibbosa. a Advanced stage of androecium and gynoecium development; antepetalous (an as, encircled by white line) and alternipetalous androecial sectors (alt as) and secondary androecial primordia formed on ring wall (arrowhead); differentiation of stylar primordia, from above. b Same as a, from the side; beginning of filament tube development. c Slightly older than stage a; differentiation of secondary androecial primordia, from above. d Same as c, from the side; advanced stage of style differentiation. e Two-locular androecial units differentiated from secondary androecial primordia (encircled by white line), from the side. f Dorsal side of theca; stomata marked with arrowheads. g Close-up of f. h–j Adansonia za. h Advanced stage of androecium development and gynoecium development; androecial sectors and secondary androecial primordia formed on 5-angled ring wall; differentiation of stylar primordia, from above. Asterisks indicate developmentally most advanced
secondary androecial primordia in central and alternipetalous position. i Same as h from the side; begin of filament tube differentiation (arrowhead); advanced stage of style differentiation. j Older stage than h, filament tube growth somewhat advanced (arrowhead); differentiation of secondary androecial primordia, from the side. k–m Adansonia digitata. k Formation of secondary androecial primordia on ring wall (arrowhead); formation of carpel primordia, from above. l Same as k from the side; petals in advanced stage of development, contorted, surrounding the slightly elevated androecial ring wall. m Slightly older stage than k, differentiation of ring wall with formation of additional secondary androecial primordia; beginning of differentiation of secondary androecial primordia into androecial units, from the side. alt as Alternipetalous androecial sector; an as Antepetalous androecial sector; 2°ap secondary androecial primordium; p petal. Scale bars: a, b, e, h, i = 0.5 mm; c, d, j–m = 1 mm; f, g = 0.1 mm
androecium/gynoecium vascular complex at the floral base distinctly from the common androecium/petal traces. These alternipetalous androecial vascular bundles end distally in the filament tube without supplying
androecial units. The antepetalous vascular bundle pairs branch into a series of vascular bundles (Fig. 5c, d) and distally, after an additional subdivision, lead into the androecial units along the filament tube and fascicles
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(Fig. 5d–g). Each androecial unit is thus supplied by one vascular bundle. Ceiba pentandra After the initiation of five broad petal primordia, five alternipetalous primary androecial primordia (alt as, Fig. 6a) and five more or less antepetalous primary androecial primordia (an as, Fig. 6a) differentiate on the androecial ring wall (Fig. 6a). The latter subdivide early in development into two halves (Fig. 6a, b). Each alternipetalous primary androecial primordium fuses with two neighboring antepetalous primary androecial primordia-halves, thus forming five androecial lobes (al, Fig. 6b–d). Later, elongate secondary androecial primordia begin to develop on
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Fig. 4 Bombax ceiba. Late stages of androecium development and androecium structure. Sepals and petals removed. a Two-locular androecial units formed from tertiary androecial primordia on filament tube, from the side. b Dorsal side of androecial unit with filament attachment. c Close-up of transition area between filament and theca; some stomata marked with arrowheads. Scale bars: a, b = 1 mm, c = 0.1 mm
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the lateral margins of the androecial lobes (Fig. 6c, d). They fuse across the tip of the androecial lobe and differentiate into a convoluted androecial unit (Fig. 6e–g). Between the filament and theca, there are numerous stomata (Fig. 6h). At the flower base, five small centrally-positioned alternipetalous androecial vascular bundles branch from the common petal/androecium/gynoecium vascular traces (Fig. 7a–g). More distally, five slightly larger common petal/androecium vascular bundles branch from the common petal/androecium/gynoecium traces (Fig. 7b, c) and subdivide into a pair of lateral androecial bundles that serve the antepetalous androecial sectors and one petal bundle (Fig. 7d, e, g). Above the point of petal insertion, each central alternipetalous androecial bundle and two
Androecium structure and development in Adansonieae Fig. 5 Bombax ceiba. Transverse sections of advanced floral bud from base to top. Vasculature of epicalyx, calyx and gynoecium not shown. Petal bundles not shown in d–g. Vasculature of androecium shaded. a Level at the base of the filament tube. Five androecial vascular bundle pairs branch from five common androecium/petal traces. Additional vascular bundles are found in some of the alternipetalous androecial sectors (arrowheads). b Level just above petal insertion. c–e Level of filament insertion. f, g Level just above filament insertion. ab androecial vascular bundle; apb common androecium/petal bundle; pb petal bundle. Scale bar 1 mm
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Shortly after petal initiation (Fig. 8a, b), five primary androecial primordia appear (an as, Fig. 8b) on the adaxial side of the petals. While these antepetalous primary androecial primordia start subdividing, five additional primary
androecial primordia of variable size can be distinguished alternating with the petal primordia (alt as, Fig. 8c, d) on a now distinct ring wall. Perhaps because the five alternipetalous primary androecial primordia are somewhat smaller than the antepetalous primary androecial primordia (Fig. 8d), the antepetalous primary androecial primordia come to occupy a slightly more peripheral position than the alternipetalous primary androecial primordia (Fig. 8c). Whereas only one secondary androecial primordium develops from each alternipetalous primary androecial
Fig. 6 Ceiba pentandra. Androecium development and androecium structure. All sepals removed; petals removed in c–f. a Formation of petals, antepetalous (an as) and alternipetalous androecial sectors (alt as, arrowhead) on androecial ring wall, from above. b Same as a, from the side; beginning of differentiation of androecial lobes. c Formation of secondary androecial primordia on ring wall and further differentiation of androecial lobes (al), from above. d Same as c, from the side; petal scars shown on slightly elevated ring wall. e
Differentiation of thecae from secondary androecial primordia, from above. f Same as e, from the side; stomium marked with arrowhead. g Theca, from the side; stomium on curled up margins of theca. h Close-up of area on the dorsal side of theca (area marked in g); some of the numerous stomata indicated by arrowheads. al androecial lobe; alt as alternipetalous androecial sector; an as antepetalous androecial sector; 2°ap secondary androecial primordium; p petal. Scale bars: a–d, g, h = 0.1 mm; e, f = 1 mm
androecial bundles from the two neighboring antepetalous sectors merge into one large arch-shaped bundle that supplies each androecial lobe (Fig. 7h–k). Eriotheca sp.
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Fig. 7 Ceiba pentandra. Transverse sections of advanced floral bud from base to top. Vasculature of epicalyx and calyx not shown; vasculature of gynoecium shown only in a. Vasculature of androecium shaded. a Level of flower base below filament tube. Centrally positioned alternipetalous androecial vascular bundles branch from the common petal/androecium/gynoecium vascular traces (arrowheads). b–c Level of lower part of filament tube. Five larger common petal/androecium vascular bundles branch from the common petal/ androecium/gynoecium traces. d–e Level of middle part of filament
tube. Petal/androecium vascular bundles subdivide into a pair of lateral androecial bundles that serve the antepetalous androecial sectors and petals. f, g Level just above petal insertion. h, i Level of filament insertion. Each central alternipetalous androecial vascular bundle and two androecial bundles from the two neighbouring antepetalous sectors merge into one large arch-shaped vascular bundle that supplies each androecial lobe. j, k Level just above filament insertion. Scale bar 1 mm
primordium, numerous secondary androecial primordia arise in a centrifugal sequence on the antepetalous androecial sectors (Fig. 8e). In early stages, the five antepetalous androecial sectors appear distinctly differentiated (Fig. 8f) but in later stages they are obscured by the development of the filament tube (Fig. 8h). Each secondary androecial primordium of the ante- and alternipetalous androecial sectors subdivides into a pair of tertiary androecial primordia in a centrifugal sequence, as indicated by the slight indentations on the secondary androecial primordia in the periphery (Fig. 8e, f). Each pair of tertiary androecial primordia then differentiates into a pair of two-locular androecial units, which remain fused at their bases (Fig. 8g, h). The mature androecium is composed of paired, two-locular androecial units elevated on a filament tube (Fig. 8h). At the flower base, five central androecial vascular bundles emerge from a star-like calyx/petal/androecium/ gynoecium vascular complex (Fig. 9a, b). They alternate
with the more distally branching, arch-shaped petal/ androecium bundle complexes (Fig. 9b–d). From each arch-shaped petal/androecium bundle complex two androecial vascular bundles branch towards the center (Fig. 9c). Thus, at the base of the filament tube, there are 15 vascular bundles: 5 bundles in an alternipetalous position and five pairs in an antepetalous position (Fig. 9d). Above the point of petal insertion, the paired antepetalous androecial bundles divide into many bundles, each of which vascularizes one androecial unit (Fig. 9e–i). Each of the five alternipetalous bundles divides into two bundles that vascularize the pair of alternipetalous androecial units (Fig. 9f, g).
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Pachira aquatica Five young petals enclose an androecial ring wall (Fig. 10a). In front of each petal, one slightly subdivided
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Fig. 8 Eriotheca sp. Androecium development and androecium structure. Sepals removed; petals removed in c–h. a Pentagonal floral apex, formation of petal primordia, from above. b Slightly older as a, from the side. Arrowheads indicate five antepetalous primary androecial primordia. c Differentiation of antepetalous and alternipetalous androecial sectors; from above. d Same as c, from the side; petal scars shown on elevated ring wall. e Formation of secondary androecial primordia on antepetalous and alternipetalous androecial sectors and begin of differentiation into tertiary androecial primordia
Fig. 9 Eriotheca sp. Transverse sections of old advanced bud from base to top. Vasculature of epicalyx not shown; vasculature of calyx and gynoecium only shown in a. Vasculature of androecium shaded. a Level of flower base below filament tube. b Level of lower part of filament tube. Alternipetalous androecial vascular bundles separate from calyx/petal/androecium/ gynoecium vascular complex. c Level of lower part of filament tube. Antepetalous androecial vascular bundles branch from the petal/androecium bundle complex. d Level of middle part of filament tube. e Level just above petal insertion. Division of antepetalous androecial vascular bundles into a series of vascular bundles and subdivision of each alternipetalous androecial vascular bundle into two. f–h Level of filament insertion. i Level just above filament insertion. ab Androecial vascular bundle; apb common androecium/petal bundle; pb petal bundle. Scale bar 1 mm
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in the floral center, from above. Asterisks indicate secondary androecial primordia in alternipetalous position. f Same as e, from the side. g Pairs of androecial units formed from tertiary androecial primordia on filament tube, from above. One pair of androecial units derived from alternipetalous tertiary androecial primordia encircled by white line. h Same as g, from the side. Elongation of filament tube (arrowhead); differentiation of style. alt as Alternipetalous androecial sector; an as antepetalous androecial sector; 2°ap secondary androecial primordium; p petal. Scale bars: a–f = 0.1 mm; g, h = 1 mm
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Fig. 10 Pachira. Androecium development and androecium structure. Sepals removed; petals removed in c–e, k–m. a–g Pachira aquatica. a Differentiation of petal primordia, antepetalous (an as) and alternipetalous androecial sectors (alt as) on ring wall, from above. b Same as a, from the side. Petal differentiation in attachment to androecial ring wall. c Formation of secondary androecial primordia on antepetalous and alternipetalous androecial sectors; from above. d Same as c, from the side. Alternipetalous secondary androecial primordia visible in floral center. e Differentiation of twolocular androecial units from tertiary androecial primordia (encircled by white line), from the side. f Theca, from the side. g Pairs of twolocular androecial units, from the side (encircled by white line). h–m Pachira insignis. h Formation of common petal/androecium
primordia, from above. i Differentiation of petal primordia and antepetalous androecial sectors (an as) from common petal/androecium primordia; from above. j Slightly older stage than i; differentiation of antepetalous androecial half-sectors, from above. k Formation and differentiation of secondary androecial primordia on antepetalous androecial half-sectors and alternipetalous androecial sectors, from above. l Differentiation of tertiary androecial primordia from secondary androecial primordia, from above. m Pairs of twolocular androecial units in phalanges on antepetalous androecial halfsectors, from the side (arrowhead). alt as Alternipetalous androecial sector; an as antepetalous androecial sector; 2°ap secondary androecial primordium; p petal. Scale bars: a, b, e, h–l = 0.1 mm; c, d = 0.5 mm; f, g, m = 1 mm
primary androecial primordium may be found (Fig. 10a, b). Five additional primary androecial primordia emerge in a more central, alternipetalous position (Fig. 10a, b). Somewhat later in development, secondary androecial primordia arise centrifugally along the margins of the antepetalous half-sectors (Fig. 10c, d). The secondary androecial primordia on a given side of an antepetalous androecial sector seem to alternate with those forming on the adjacent
antepetalous androecial sector rather than the other side of the same antepetalous androecial sector (Fig. 10c, d). At the same time, one secondary androecial primordium is initiated on each of the five central alternipetalous androecial sectors (Fig. 10c, d). Then, on the antepetalous androecial half-sectors, additional secondary androecial primordia arise at the periphery. Each secondary androecial primordium subsequently splits into two tertiary androecial
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Fig. 11 Pachira aquatica. Transverse sections of advanced floral bud from base to top. Vasculature of epicalyx and gynoecium not shown; vasculature of calyx only shown in a, b. Vasculature of androecium shaded. a Level of flower base below filament tube. Alternipetalous androecial vascular bundles separate from calyx/petal/androecium/ gynoecium vascular complex (arrowheads). b Level of lower part of
filament tube. Antepetalous androecial vascular bundles branch from the petal/androecium bundle complex. c Level of middle part of filament tube. d Level just above petal insertion. e, f Level of filament insertion. g Level just above filament insertion. ab Androecial vascular bundle; pb petal bundle. Scale bar 1 mm
primordia, which then differentiate into two-locular androecial units (Fig. 10e–g). Five small alternipetalous androecial vascular bundles branch from each of the five common calyx/corolla/ androecium traces at the floral base (Fig. 11a, arrowheads). More distally, ten larger androecial vascular bundles, two per androecial sector, branch from the calyx/ corolla/androecium traces (Fig. 11b, c, d). The androecial bundles have a star-like arrangement at the base of the filament tube. The five alternipetalous vascular bundles occupy a slightly more central position than the ten antepetalous ones (Fig. 11c). More distally, each antepetalous androecial vascular bundle subdivides into a series of bundles that serve the androecial units on the antepetalous androecial sector. The five more central alternipetalous androecial bundles only subdivide once (Fig. 11e–g) and serve the alternipetalous pairs of androecial units.
asymmetrically, revealing their future direction of contortion (Fig. 10j). Secondary androecial primordia arise on the antepetalous primary androecial primordia in a centrifugal sequence (Fig. 10k). The space in the floral center is limited which may explain why the secondary androecial primordia appear to be arranged almost on top of each other. While additional secondary androecial primordia are initiated laterally and centrifugally (Fig. 10l), the first formed secondary androecial primordia each subdivide into two tertiary androecial primordia (Fig. 10l), which remain connected at their bases in later development (Fig. 10m). Each tertiary androecial primordium subsequently differentiates into a two-locular androecial unit. The androecial units are arranged in ten distinct phalanges in older developmental stages, each corresponding to one antepetalous androecial half-sector (Fig. 10m).
Pachira insignis Five common petal/androecium primordia arise on a flat to slightly concave floral apex (Fig. 10h). Each common primordium divides into a broad peripheral petal primordium and a smaller central primary androecial primordium. Later, each primary androecial primordium subdivides anticlinally into two halves, such that a pair of primary androecial primordia-halves is positioned in front of each petal primordium (Fig. 10j). The petals differentiate
Pseudobombax ellipticum Five young broad petals are visible at the periphery of a slightly elevated androecial ring wall with five androecial sectors already somewhat differentiated in alternipetalous positions (Fig. 12a). On the androecial ring wall, five alternipetalous primary androecial primordia (alt as, Fig. 12a) and five larger antepetalous primary androecial primordia arise (an as, Fig. 12a). The latter divide resulting in a pair of primary androecial primordia-halves being positioned in front of each petal (Fig. 12b). Five androecial lobes are formed, each from one alternipetalous primary
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Fig. 12 Pseudobombax ellipticum. Androecium development and androecium structure. Sepals removed; petals removed in b–f. a Formation of petal primordia, antepetalous (an as) and alternipetalous androecial sectors (alt as) on slightly elevated ring wall, from above. b Differentiation of antepetalous androecial half-sectors and alternipetalous androecial sectors on ring wall; from above. c Formation of secondary androecial primordia on antepetalous androecial half-
sectors and on the interstitial antepetalous areas; differentiation of carpel primordia; from above. d Same as c, from the side, view on the interstitial antepetalous areas opposite petal insertions. e Slightly later stage than c from above. f Differentiation of tertiary androecial primordia from secondary androecial primordia; differentiation of stylar primordia, from the side. g Theca, from the side. Scale bars: a, b = 0.1 mm; c, d = 0.5 mm; e–g = 1 mm
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Fig. 13 Pseudobombax ellipticum. Transverse sections of advanced floral bud from base to top. Vasculature of epicalyx and gynoecium not shown. Vasculature of calyx only shown in a. Vasculature of petals not shown in e–h. Androecium vasculature shaded. a Level of flower base below filament tube. Alternipetalous androecial vascular bundles separate from calyx/petal/androecium/gynoecium vascular complex (arrowheads). b, c Level of lower part of filament tube.
Arrowheads indicate alternipetalous androecial vascular bundles. d Level of middle part of filament tube. Arrowheads indicate alternipetalous androecial vascular bundles. e Level of petal insertion. f, g Level of filament insertion. ab Androecial vascular bundle; apb common androecium/petal bundle; pb petal bundle. h Level just above filament insertion. Scale bar 1 mm
androecial primordium and its two neighbouring antepetalous primary androecial primordia-halves (Fig. 12b). Secondary androecial primordia are first initiated on the innermost tip of the androecial lobes in an alternipetalous
position, followed by a centrifugal sequence of further secondary androecial primordia on the lateral margins of the androecial lobe (Fig. 12c). In an interstitial antepetalous area between the antepetalous androecial half-sectors,
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additional secondary androecial primordia arise in a centrifugal succession (Fig. 12c, d). Subsequently, the secondary androecial primordia subdivide in centrifugal sequence (Fig. 12c), giving rise to tertiary androecial primordia that each ultimately differentiate into a stalked twolocular androecial unit (Fig. 12e–g). Five androecial vascular bundles branch from five common androecium/petal traces at the flower base (Fig. 13a–c). They alternate with the remaining androecium/petal traces and distally supply the pairs of androecial units at the tip of the androecial lobes (Fig. 13g, h). After the branching of the petal vascular bundles from the common androecium/petal traces, the remaining antepetalous androecial bundles divide and each forms a horseshoeshaped androecial vascular bundle complex (Fig. 13d). The lateral parts of this vascular complex subsequently branch into rows of smaller vascular bundles, which supply the androecial units along the margins of the five androecial lobes (Fig. 13e–g). The peripheral part of the vascular complex also branches into a large number of vascular bundles, which supply the antepetalous androecial units in the interstitial antepetalous areas (Fig. 13g, h).
Discussion Developmental patterns in Adansonieae Androecial ring wall and common petal/androecium primordia Most of the taxa studied share a more or less distinct pentagonal androecial ring wall early in floral development. The ring wall usually differentiates into five larger antepetalous and five smaller alternipetalous primary androecial primordia. The size of the ring wall varies but generally species with more numerous androecial units (e.g. Adansonia digitata) produce larger ring walls. Similar ring wall development occurs in the remainder of Bombacoideae as well as Malvoideae (von Balthazar et al. 2004, 2006), but differs from ring walls of other Malvales (e.g. Cistaceae, Bixaceae) in that these acquire their final size at the time of initiation (Ronse Decraene 1988, 1989), whereas Malvoideae and Bombacoideae ring walls expand significantly after initiation. In some cases, however, as observed in Pachira insignis, common petal/androecium primordia arise, which only later split into distinct petal and primary androecial primordia. Such common petal/androecium primordia (or ‘‘stamen– petal-complexes’’) are known also from other subfamilies of Malvaceae s.l., e.g. Byttnerioideae (Jenny 1989) and Malvoideae (Duchartre 1845; Janka 2003; von Balthazar et al. 2004). Common petal/androecium primordia can be
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interpreted, in part, as reflecting delayed petal development or accelerated stamen development. The tendency for a relative delay in petal development could also explain the fact that in some Malvoideae petal primordia are only visible after the androecial primordia (Janka 2003). Ronse Decraene et al. (1993) suggested that this relative delay in inception of petals is related to the development of largesized antepetalous androecial primordia. As observed in Pachira, taxa with common petal/androecium primordia may produce similarly large numbers of androecial units as taxa with androecial ring walls. This is known also from other families, e.g. Hydrangeaceae, where taxa with common primordia may produce up to 250–300 stamens per flower, e.g. Carpenteria (Hufford 1998). Antepetalous and alternipetalous primary androecial primordia The five antepetalous primary androecial primordia each subdivide into two halves, thus one pair of primary androecial half-primordia is situated in front of each petal (e.g. Eriotheca sp., Fig. 8c; Pachira spp., Fig. 10a, j) as reported previously for Malvoideae (van Heel 1966; Sattler 1973; von Balthazar et al. 2004). In most of the species studied, five alternipetalous primary androecial primordia develop more centrally on the androecial ring wall. They tend to be smaller than the antepetalous primary androecial primordia, e.g. in Eriotheca and Pachira (Figs. 8c, d, 10a, b). In the latter, the alternipetalous primary androecial primordia are restricted to five small central areas, on each of which only one pair of twolocular androecial units develops (see also van Heel 1966). In Adansonia, however, there is variation in the size of the alternipetalous primary androecial primordia: they are large in A. gibbosa and each give rise to approximately four to six secondary androecial primordia (Fig. 2a, b) but somewhat smaller in A. za (Fig. 2h, i). A special situation is present in Ceiba pentandra where the alternipetalous androecial primordia appear to only give rise to a sterile area that becomes incorporated into the fertile tissue of the adjacent antepetalous androecial half-primordia (Fig. 6a–d). Each primary androecial primordium of Adansonieae functions as a ‘‘common’’ or ‘‘complex primordium’’ on which secondary and tertiary androecial primordia arise: their androecia are thus ‘‘complex multistaminate’’ (Ronse Decraene 1988; Ronse Decraene and Smets 1992). They differ from other multistaminate androecia where each stamen arises from its own original primordium (e.g. Leins 1975; Ronse Decraene 1988; Ronse Decraene and Smets 1992, 1995). Generally, complex multistaminate androecia have further been categorized by either developing a ring wall or distinct common primordia (Ronse Decraene and Smets 1992). However, Adansonieae present a special case
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because they combine both these features. This type of complex polystemony was also reported from Malvoideae (von Balthazar et al. 2004) and the remainder of core Bombacoideae (von Balthazar et al. 2006) but not from other subfamilies of Malvaceae s.l.
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vasculature, as for example in Bombax. A reduction or loss of the alternipetalous androecial sectors was also found in other taxa of the Malvatheca clade (Nandi 1998; von Balthazar et al. 2004, 2006). Secondary androecial primordia
Androecial lobes Early in floral ontogeny, antepetalous and alternipetalous primary androecial primordia remain associated to some degree, while distinct subdivisions take place only on the antepetalous androecial primordia, leading to two halfprimordia. Five androecial lobes, also named ‘‘staminal lobes’’ or ‘‘three-trace-lobes’’ by van Heel (1966), are formed by the association of an alternipetalous primary androecial primordium and two neighboring antepetalous primary androecial half-primordia. They thus correspond to complex structures that each encompasses one alternipetalous sector and the halves of the two neighboring antepetalous sectors. In Adansonieae, androecial lobes are most distinct in Ceiba pentandra and Pseudobombax ellipticum (Figs. 6a, b, 12b). However, the occurrence of androecial lobes is not restricted to Adansonieae; in fact, they occur in numerous members of the Malvatheca clade (von Balthazar et al. 2006). Although mature androecial lobes vary in shape across Malvatheca, there are strong commonalities in early development (von Balthazar et al. 2004, 2006). This was already noted by van Heel (1966, 1969), who suggested their homology. However, as the phylogenetic relationships among the members of Malvatheca are still largely unresolved, the possibility of a parallel evolution of androecial lobes cannot be ruled out (von Balthazar et al. 2006). Van Heel (1966) inferred that androecial lobes come to have an alternipetalous position due to a spiral growth or twist taking place early in the floral apex and that without such twisting they would be antepetalous. By examining the vascular system, he found each androecial lobe to be supplied with three synlateral vascular traces, therefore he also named them ‘‘three-trace-lobes’’. In our studies, however, we found androecial lobes to be generally positioned alternipetalously without a spiral growth or twist taking place, and with only the two marginal parts occupying a more or less antepetalous position. In accordance with van Heel (1966) we found that the androecial lobes are provided with a three-trace-vascular system, with the two lateral vascular traces supplying the antepetalous primary androecial primordia-halves and the median one supplying the alternipetalous primary androecial primordium. Generally, the median parts of the androecial lobes seem to be reduced in Adansonieae, as indicated by the initiation of a smaller number of androecial units in for example Eriotheca or Pachira (Nandi 1998) and the loss of
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Secondary androecial primordia arise on the primary androecial primordia in a centrifugal sequence in all species studied except Adansonia gibbosa, where the initiation proceeds centripetally (e.g. Fig. 12f). The number of secondary androecial primordia varies greatly between species but generally more secondary androecial primordia develop on the antepetalous than on the alternipetalous primary androecial primordia (except in A. gibbosa). In some species (e.g. Adansonia digitata, Pseudobombax ellipticum, Pachira aquatica) hundreds of secondary androecial primordia may proliferate on the antepetalous primary androecial primordia. Alternipetalous androecial sectors produce only few secondary androecial primordia and the number produced varies from a single (Eriotheca, Pachira and Pseudobombax) to six (Adansonia gibbosa) secondary androecial primordia per sector. The proliferation of secondary androecial primordia was observed to occur in an alternate pattern (e.g. in Eriotheca, Pachira), i.e. each primordium is slightly shifted from the radius of the former primordium in the centrifugal sequence. Pseudobombax ellipticum is unique among the species studied in showing initiation of secondary androecial primordia both on the margins of the androecial lobes and, later in development, on the interstitial antepetalous areas. In Pachira the concave floral apex gives the impression that the secondary androecial primordia are initiated in a centripetal succession. However, because the more centrally positioned secondary androecial primordia are more advanced in their development than the peripheral ones, we infer that initiation is centrifugal. In accordance with van Heel (1966), we noted that many secondary androecial primordia arise in positions on either side of the radius of initiation, presumably in response to the concave form of the floral apex and the space available for secondary androecial primordium development. Adansonia gibbosa, however, has truly centripetal initiation (Fig. 2a, c). Additionally, A. gibbosa differs from the other species in that neighboring secondary androecial primordia (most obviously in the peripheral alternipetalous groups) vary significantly in size and degree of differentiation (Fig. 2d). Tertiary androecial primordia Except for Adansonia and Ceiba, discussed below, secondary androecial primordia subdivide once and give rise to pairs of tertiary androecial primordia that then
Androecium structure and development in Adansonieae
differentiate into two-locular androecial units. It has been discussed whether this developmental process is best described as a de´doublement (Ronse Decraene and Smets 1993, 1996) or a partitioning (von Balthazar et al. 2004) of androecial primordia. De´doublement, in the sense of Ronse Decraene and Smets (1993, 1996), is defined as an increase in the number of stamens by a subdivision of androecial primordia during development, where the resulting structures are identical to the original structure. In contrast, partitioning involves a subdivision of structures into two equal halves. In Adansonieae, similar to Malvoideae (von Balthazar et al. 2004), the subdivision of a secondary androecial primordium and the subsequent differentiation leads to two–two-locular androecial units and not to two– four-locular androecial units. When the subdivision is incomplete, a single four-locular androecial unit may result (e.g. in Bombax ceiba). Therefore, the developmental process involving androecial primordium subdivision in Adansonieae should be described as partitioning and not de´doublement. The development and differentiation of two-locular androecial units are similar in Adansonieae and core Malvoideae (von Balthazar et al. 2004, 2006). In both cases, secondary androecial primordia arise on primary androecial primordia in a centrifugal sequence, then subdivide and give rise to pairs of tertiary androecial primordia that develop into two-locular androecial units. Given the currently accepted phylogenetic relationships it seems that Adansonieae and core Malvoideae have independently evolved a similar developmental pathway (Baum et al. 2004). Adansonia and Ceiba pursue somewhat different developmental pathways to the remainder of core Bombacoideae in that one stage of primordium subdivision is omitted. For Adansonia our data suggest two possible scenarios for the development and differentiation of twolocular androecial units. One interpretation is that the subdivision of the secondary androecial primordia into tertiary androecial primordia does not occur; instead, twolocular androecial units differentiate directly from secondary androecial primordia. The alternative scenario is that secondary androecial primordia are never formed and tertiary androecial primordia are initiated directly on the primary androecial primordia. Van Heel (1966) hypothesized that further primordium subdivisions takes place in Adansonia but at such an early stage of androecium development it cannot be observed. However, the lack of paired androecial units in Adansonia rather supports the latter hypothesis that primordium partitioning never happens in Adansonia. Ceiba is unique in Adansonieae in that no primordia subdivisions take place at all. Instead, the two antepetalous androecial half-sectors that form the marginal parts of each androecial lobe retain the undivided developmental stage of
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the secondary androecial primordia. From the latter, elongated two-locular androecial units differentiate (see below). Nature of stamens in Adansonieae In all the taxa studied except Adansonia and Ceiba, the two-locular androecial units occur in pairs and arise from the partitioning of a secondary androecial primordium. However, in some cases the partitioning of secondary androecial primordia is incomplete and results in either two monothecate, two-locular androecial units with a common filament, or fails altogether with the result of a single dithecate, four-locular androecial unit. The occurrence of both monothecate two-locular and dihecate four-locular androecial units in one flower has only rarely been reported in Adansonieae (found in: Bombax ceiba, Davis and Mariamma 1965; Davis 1966; van Heel 1966; Davis and Ghosh 1970) and in Malvoideae (Malva, Pavonia, Abutilon, Janka pers. obs. unpubl., Lagunaria, Quararibea, von Balthazar et al. 2004). The similarity of androecial units in Adansonieae and Malvoideae led to an assumption of their homology in traditional classifications (e.g. Edlin 1935; Hutchinson 1967; Takhtajan 1997). However, current phylogenetic relationships render this unlikely as core Malvoideae and core Bombacoideae appear not to be sister lineages (Baum et al. 2004). Based on this phylogenetic hypothesis, it is more parsimonious to conclude that stalked two-locular androecial units evolved independently in both lineages from ancestors with long sessile androecial units (Alverson et al. 1998; Baum et al. 2004; von Balthazar et al. 2006). Two-locular androecial units in Malvatheca have been characterized as ‘‘half stamens’’ by various authors (Eichler 1875/1878; Hirmer 1918; van Heel 1966; Rohweder 1972; von Balthazar et al. 2004). Observations of partitioning of the secondary androecial primordia in these species rules out the alternative hypothesis that the locules of a dithecate four-locular anther fuse over the apex to give rise to a single two-locular anther (Endress and Stumpf 1990). We support the interpretation of the ‘‘half stamens’’ and therefore will henceforth refer to them as ‘‘monothecate stamens’’ instead of androecial units. The androecium of Ceiba pentandra is characterized by five, stalked, two-locular androecial units, each derived from a single androecial lobe. The pollen locules develop from the elongated secondary androecial primordia on the antepetalous androecial half-primordia whereas the filament and the ‘‘connective’’ tissue derive from the alternipetalous primary androecial primordia. The production of a two-locular androecial unit in Ceiba appears to involve fusion of the two antepetalous androecial halfsectors over the top of the sterile alternipetalous androecial sector. The androecial units of Ceiba are thus complex
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structures that are not homologous to the monothecate stamens of other Adansonieae. The occurrence of ‘‘stamens’’ derived from androecial complexes in floral ontogeny, however, is also reported from two representatives of the early diverging Malvatheca, i.e. Chiranthodendron and Fremontodendron (von Balthazar et al. 2004, 2006). The resemblance of the anthetic structures of Ceiba and Fremontodendron was already noted by van Heel (1966, 1969). An important difference, however, is that the anthetic thecae of Ceiba are confluent over the apex, which is not the case in the other two genera. As reported from Ceiba pentandra, up to 15 ‘‘anthers’’ can develop instead of the usual 5 (Davis and Kundu 1965). Apparently, in those flowers the androecial sectors do not remain fused to form androecial complexes but split up to give rise to three individual monothecate anthers. A similar case is reported from C. trischistandra by Gibbs and Semir (2003). The ‘‘stamen’’ structure of Ceiba has been a subject of discussion between van Heel (1966, 1969) and Rohweder (1972). Van Heel (1966, 1969) supported the idea that the ‘‘stamens’’ of Ceiba are basically synangial and arise from a fusion of monothecate stamens that originate from antepetalous and alternipetalous androecial sectors. He thus distinguishes two different stamen types in Malvatheca: those that correspond to parts of an androecial lobe (i.e. to the alternipetalous or antepetalous androecial sectors) and those that correspond to an entire androecial lobe (as in Ceiba). He further proposed that the Ceiba androecium is derived from an ancestor with numerous monothecate stamens. Rohweder (1972) suggested that androecial primordia have ‘‘lateral meristems’’ (corresponding to the antepetalous primary androecial half-primordia) that can undergo subdivisions (e.g. in ‘‘Bombacopsis’’) to give rise to multiple (monothecate) stamens or remain undivided to produce one stamen with a single elongated theca as happens in the case of Ceiba. We concur with van Heel that ‘‘stamens’’ of Ceiba each correspond to an entire androecial lobe and that they are thus different from other taxa of Malvatheca where only parts of the androecial lobes, namely the antepetalous primary androecial half-primordia give rise to rows of secondary androecial primordia. However, we oppose his idea of a synangial stamen derived from fusion of monothecate stamens. We favor Rohweder’s idea that ‘‘lateral meristems’’ (i.e. the antepetalous primary androecial halfprimordia) have the capacity to undergo subdivisions in taxa with numerous monothecate stamens, and in some cases these structures may have prolonged activity, leading to the differentiation of elongated locules (cf. Ochroma, Quararibea, von Balthazar et al. 2004, 2006). Given that all other members of Adansonieae have stalked, monothecate stamens, an independent origin of the special ‘‘complex’’ stamens of Ceiba is most likely.
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In some species studied (Adansonia gibbosa: Fig. 2f, g; Bombax ceiba: Fig. 4c; Ceiba pentandra: Fig. 6h), numerous stomata occur on the connectives, in particular in the transition areas to the filaments. While scent production of stamens is known from many plant families, only for a few is confirmed that stomata play a role in the release of scents, for instance in Pinaceae and Fagaceae (e.g. Niinemets et al. 2002). However, as many Adansonieae flowers are strongly odoriferous, it is possible that the androecium is involved in scent production and that the scent is released by the stomata. Vasculature of the androecium The value of vasculature for revealing the nature of floral organs and for reconstructing floral evolution is controversial. It has been claimed that the vasculature evolves conservatively in comparison to morphology and may therefore be used as a tool to reconstruct androecium evolution (e.g. Saunders 1937). However, it has to be considered that vasculature also responds to basic growth and developmental processes. For example, larger organs might be intensely vascularized not because they derive from multiple fused structures but because of the way that hormone concentration gradients drive the self-organization of vascular tissue (e.g. Aloni 2001; Dengler 2001). Thus, the development of complex structures like androecial ring walls could directly lead to modifications of vascularization (e.g. in Adansonia gibbosa, Fig. 3a–d). Opponents of the ‘‘conservatism’’ theory therefore tend to assume that vascularization is a secondary process that follows primordium growth and development (e.g. Arber 1933; Cheung and Sattler 1967). Nonetheless, we believe that vasculature patterns may help to elucidate the androecium structure when interpreted in the context of developmental data. The analysis of the androecial vasculature has proven to be a useful guide in the interpretation of the androecial structure in Malvoideae and other members of Malvatheca (von Balthazar et al. 2004, 2006). In most Adansonieae, two main antepetalous androecial vascular bundles serve each antepetalous androecial sector (Fig. 14a–e). At the flower base, these bundles unite with the vascular bundle of the corresponding petal. Only in Adansonia is such a pattern difficult to discern: even in the youngest developmental stages the androecial vascular bundles are arranged in a vascular ring complex at the base of the filament tube, whose segments cannot easily be assigned to androecial sectors (Fig. 3a–g). In all the taxa studied except Adansonia and Ceiba pentandra, the lateral antepetalous androecial vascular bundles divide distally into a series of bundles that run parallel to each other before subdividing again and entering the monothecate
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Fig. 14 Diagram series of androecium vascularization of one antepetalous androecial sector and two adjacent alternipetalous androecial sectors (indicated by dotted lines). Vascularization of corolla is not shown. Petals are indicated by a semicircular symbol at the base of each diagram; monothecate stamens are indicated by the small oval structures at the top of each diagram. a Bombax ceiba. One androecial vascular bundle pair branches from a common androecium/petal trace. After branching again into a series of bundles and a further distal subdivision, each antepetalous androecial bundle vascularizes one monothecate stamen. Alternipetalous androecial vascular bundles end distally in the filament tube without supplying monothecate stamens. b Pseudobombax ellipticum. Five antepetalous androecial vascular bundles branch from a common androecium/petal trace. Additional proximal subdivisions of each bundle lead to a series of antepetalous bundles that, after a further distal subdivision, each vascularizes one monothecate stamen. Alternipetalous androecial bundles only subdivide once and supply the pairs of monothecate stamens at the tip of the androecial lobes. c Pachira aquatica. One
androecial vascular bundle pair branches from a common androecium/petal trace. More distally, each antepetalous androecial vascular bundle subdivides into a series of bundles that serve the monothecate stamens on the antepetalous androecial sector. Alternipetalous androecial bundles only subdivide once and serve the alternipetalous pairs of monothecate stamens. d Ceiba pentandra. One common petal/androecium vascular bundle subdivides into a pair of lateral androecial bundles that serves the antepetalous androecial sector and one petal bundle. Two androecial bundles from two neighboring antepetalous sectors merge with one central alternipetalous androecial bundle into one large arch-shaped bundle that supplies one androecial lobe. e Eriotheca sp. One androecial vascular bundle pair branches from a common androecium/petal trace. More distally, each antepetalous androecial vascular bundle subdivides into a series of bundles that serve the monothecate stamens on the antepetalous androecial sector. Alternipetalous androecial bundles only subdivide once and serve the alternipetalous pairs of monothecate stamens
stamens (Fig. 14a–c, e). Each monothecate stamen is then vascularized by a single androecial bundle. In addition to the antepetalous androecial vascular bundles, one vascular bundle serves each alternipetalous androecial sector. The presence of such alternipetalous androecial bundles has already been described for Bombax, Pachira and Ceiba (Wilson 1937; Davis and Kundu 1965; van Heel 1966; Gibbs and Semir 2003). At the floral base, these bundles unite with the calyx/petal/androecium bundle
complex. Distally, they run parallel with the antepetalous bundles, but, in contrast to the latter, only branch once before entering a single pair of monothecate stamens at the tip of the androecial lobe (Fig. 14a–c, e; exception: Ceiba, see below). In agreement with van Heel (1966), we found that Bombax ceiba has five alternipetalous bundles that end before reaching the distal parts of the alternipetalous androecial sectors (Figs. 5a, 14a). Our finding, however,
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contradicts Wilson (1937) who reports the existence of ten smaller, alternipetalous bundles that partly result from a subdivision of a larger petal/androecium bundle complex and partly have an independent origin from the floral base. Our results further contrast with Rao (1952), who did not report any alternipetalous androecial bundles in Bombax ceiba. The occurrence of alternipetalous bundles indicated the presence of reduced alternipetalous androecial sectors. Although the monothecate stamens of anthetic Bombax ceiba flowers have usually been interpreted as being arranged in two whorls (Robyns 1963; Davis and Mariamma 1965; Davis 1966; van Heel 1966), this inference is contradicted by the finding that all monothecate stamens are served by antepetalous vascular bundles. In Ceiba pentandra the two lateral antepetalous androecial vascular bundles of each antepetalous androecial sector do not further subdivide (Fig. 14d). Instead, the two vascular bundles of two adjacent antepetalous androecial sectors merge with the alternipetalous vascular bundle resulting in a common bundle that supplies one androecial complex. This agrees with previous reports of a three-tracesupply in each filament of C. pentandra (van Heel 1966, 1969; Davis and Kundu 1965; Gibbs et al. 1988; Gibbs and Semir 2003). Further it has been argued that the ‘‘triple nature’’ of the anthers in Ceiba is revealed in the case of C. trischistandra, where a filament may bear three monothecate anthers. Such cases of staminal fission have also been reported to occur in abnormal flowers of C. pentandra (Davis and Kundu 1965). The androecial vascular pattern found in Adansonieae consisting of two lateral vascular bundles for each antepetalous androecial sector and one vascular bundle for each alternipetalous androecial sector is very similar to that of Matisieae and the remainder of core Bombacoideae (von Balthazar et al. 2004, 2006). However, alternipetalous androecial bundles in Matisieae and the remainder of core Bombacoideae supply sterile tips of the androecial lobes while those in Adansonieae each vascularize one pair of (or a few) monothecate stamens. In core Malvoideae, alternipetalous androecial vascular bundles are absent with the exception of Gossypium where blind-ending bundles exist (von Balthazar et al. 2004). Thus, in comparison to core Bombacoideae and Matisieae, core Malvoideae have a simpler androecial vascular pattern, correlating with their simple alternipetalous androecial sectors. Androecial whorls The androecium in Adansonieae is highly variable both in the number of monothecate stamens, ranging from a handful to more than a thousand, and in their structural arrangement. Especially in species with very high numbers of monothecate stamens, it seems almost impossible to
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characterize their androecial organization in terms of androecial sectors or androecial whorls. Earlier studies suggested that the androecium of Adansonieae to be organized in either two androecial whorls (e.g. Bombax ceiba: Robyns 1963; Davis and Mariamma 1965; Davis 1966; van Heel 1966; Davis and Ghosh 1970, Neubauer 1989), Ceiba (Gibbs and Semir 2003), Pachira and Pseudobombax (Bombax) ellipticum (van Heel 1966) or only one whorl (e.g. Bombax ceiba (Rao 1952), Ceiba pentandra (Eichler 1875/1878; van Heel 1966), Eriotheca and Pseudobombax (Robyns 1963). In some cases information from floral development and floral vasculature is congruent with these findings (e.g. Pachira, Pseudobombax) but in others contradictory (e.g. Bombax ceiba, Eriotheca sp.; see Table 3 for an overview). Nonetheless, from all the data summarized in Table 3, we conclude that the androecium of Adansonieae is basically composed of two androecial whorls; but that one whorl, constituting the alternipetalous androecial sectors, is reduced in most species studied. A two-whorled androecial configuration was also inferred to apply to the remainder of core Bombacoideae (von Balthazar et al. 2006), with the notable difference that in non-Adansonieae taxa the alternipetalous androecial sectors remain sterile. Such reduction of the alternipetalous whorl is even more complete in core Malvoideae, where in most cases only the antepetalous androecial whorl is detectable (von Balthazar et al. 2004). Pollination Most Adansonieae have rather massive flowers. When borne on stiff pedicels, they are erect, but otherwise may be horizontal or pendant. Flowers are most commonly creamy or white, but may also be red (e.g. Bombax ceiba), pink (e.g. Ceiba spp.) or yellow (e.g. Adansonia spp.). Anthesis is reported as predominantly nocturnal or crepuscular and only rarely diurnal. In the first case, the flowers emit a musty, fruity, sweet or cabbage-like scent and last only a short time, sometimes only one night (van der Pijl 1936; Faegri and van der Pijl 1979; Baum 1995; Proctor et al. 1996; Gibbs and Alverson 2006 for Spirotheca). These floral characteristics indicate pollination by either bats (chiropterophily; e.g. van der Pijl 1936; Kaisila 1966; Jaeger 1974; Faegri and van der Pijl 1979; Eguiarte et al. 1987; Reddi et al. 1989; Elmqvist et al. 1992; Baum 1995; Gribel and Gibbs 2002; Lobo et al. 2005) or by nocturnal insects, especially hawkmoths (e.g. Baum 1995; MacFarlane et al. 2003). Though flower visits by nocturnal non-flying mammals have been reported (bushbabies: e.g. Coe and Isaac 1965; lemurs: Baum 1995), their role as pollinators is insignificant. Hawkmoth pollination has been documented and may play a more important role in Adansonieae than earlier assumed due to the difficulty
Androecium structure and development in Adansonieae
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Table 3 Androecium structure and organization in Adansonieae Taxa
Anthetic androecium
Androecial vasculature
Androecium development
Adansonia digitata
Numerous androecial units evenly Common petal/androecium Large numbers of secondary Number of distributed in the distal parts of vasculature arranged in a androecial primordia arise in whorls the ring-like filament tube vascular complex at base of the no discernable groups on the uncertain (Eichler 1875/1878; van Heel filament tube (van Heel 1966) androecial ring wall (van Heel 1966) 1966, this paper)
A. gibbosa; A. za
Numerous androecial units not inserted in distinct phalanges
Bombax ceiba
Five peripheral antepetalous Ten androecial bundles serve ten Numerous secondary androecial one antepetalous groups of androecial units + 15 antepetalous androecial halfprimordia arise in antepetalous + one (5 dithecate + 10 monothecate) sectors; five bundles end blind position (this paper); rudimentary alternipetalous inner androecial units in ± in the five alternipetalous one whorl whorl alternipetalous positions androecial sectors (van Heel interpreted as two androecial 1966, this paper); only whorls (Robyns 1963; Davis and antepetalous bundles (Rao Mariamma 1965; Davis 1966; 1952); ten alternipetalous van Heel 1966; Davis and Ghosh bundles (Wilson 1937) 1970; Neubauer 1989) or one All androecial units are androecial whorl (Rao 1952) vascularized by antepetalous androecial vascular system (Davis and Mariamma 1965, van Heel 1966, this paper); one whorl
Ceiba pentandra
Five alternipetalous androecial units interpreted as one androecial whorl (van Heel 1966)
Ten androecial vascular bundles Ten antepetalous androecial half- Two androecial serve ten antepeta-lous sectors + five alternipetalous whorls androecial half-sectors; five androecial sectors are formed; vascular bundles serve the five two antepetalous androecial alternipetalous androecial half-sectors and one alternisectors; two antepetalous petalous androecial sector each bundles each merge with one form an androecial unit alternipetalous bundle to form (‘‘androecial’’ complex, this one large arch-shaped bundle paper) that vascularizes one androecial unit (Davis and Kundu 1965; van Heel 1966, 1969; Gibbs et al. 1988; Gibbs and Semir 2003, this paper)
Eriotheca sp.
Numerous androecial units arranged in antepetalous phalanges interpreted as one androecial whorl (Robyns 1963)
Ten androecial vascular bundles Numerous secondary androecial serve ten antepetalous primordia arise on ten androecial half-sectors; five antepetalous androecial halfvascular bundles serve the five sectors + five on alternialternipetalous androecial petalous androecial sectors sectors (this paper); two (this paper); two whorls whorls
Pachira spp.
Numerous androecial units in ten Ten androecial vascular bundles distinct antepetalous serve ten antepetalous phalanges + five single androecial half-sectors + five androecial units in vascular bundles the five alternipetalous positions alternipetalous androecial interpreted as two androecial sectors (van Heel 1966, this whorls (Robyns 1963; van Heel paper); two whorls 1966) or only one (alternipetalous) androecial whorl (Eichler 1875/1878)
Androecial bundles arranged in a Groups of secondary androecial ring-like vascular complex at primordia arise on five the base of the filament tube antepetalous and five (A. za; this paper) alternipetalous androecial sectors thus in two whorls (this paper)
Numerous secondary androecial primordia are initiated on the ten antepetalous androecial half-sectors + five on the alternipetalous androecial sectors more centrally (van Heel 1966, this paper); two whorls
Conclusion
Two androecial whorls probable
Two androecial whorls
Two androecial whorls
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Table 3 continued Taxa
Anthetic androecium
Androecial vasculature
Pseudobombax ellipticum
Numerous androecial units in ten Ten androecial vascular bundles antepetalous phalanges + five serve ten antepetalous larger sterile androecial units on androecial half-sectors + five alternipetalous tips interpreted as vascular bundles the five two androecial whorls alternipetalous androecial (van Heel 1966) sectors (van Heel 1966, this paper); two whorls
of such studies (e.g. Baum 1995; MacFarlane et al. 2003). Adansonieae species with diurnal anthesis are reported to be pollinated by mostly bees or birds (e.g. Eguiarte et al. 1987; Oliveira et al. 1992 for Eriotheca gracilipes, E. pubescens). On the whole, however, pollination by diurnal animals seems to be the exception in Adansonieae. Adansonieae flowers primarily offer nectar, often produced in large amounts (e.g. Ceiba pentandra, Gribel et al. 1999) and/or pollen (e.g. Pseudobombax munguba, Gribel and Gibbs 2002) as floral rewards. Enhanced production and presentation of pollen in Adansonieae is basically achieved by two modifications of the androecium. The first strategy is the production of so-called brush-flowers (Proctor et al. 1996). In these flowers, stamen number is increased and stalked filaments extend the anthers beyond the perianth in such a way that a visiting animal picks up pollen on a large portion of its body surface. Such flowers occur in Adansonia, Bombax, Eriotheca, Pachira s.l., and Pseudobombax. Brush-flower morphology, however, varies within Adansonieae and also within genera. This can especially be seen in Adansonia, where species with spherical or flat brush-flowers of various sizes occur that also differ in the lengths of their filament tubes (Baum 1995; Baum et al. 1998). These morphological differences may also correspond to different pollination systems: although Adansonia digitata is a well-known bat-pollinated species, others in the genus, including A. gibbosa and A. za, are primarily pollinated by hawkmoths (Baum 1995; Baum et al. 1998). A special brush-type is found in the kapok tree, Ceiba pentandra (Proctor et al. 1996). Although the creamy-white flowers are small and have only five stamens, they are arranged in spherical fasciculate inflorescences. The ‘‘brush’’, formed by many flowers is visited by a wide range of animals: bats, marsupials, night monkeys, hawkmoths, bees, wasps and hummingbirds (Gribel et al. 1999). Similar to Adansonia, the range of floral diversity in Ceiba is large. For instance, many Ceiba species have ‘‘staminodial appendages’’ that are associated with the
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Androecium development
Conclusion
Numerous secondary androecial Two androecial primordia arise on ten whorls (the antepetalous androecial halfinner sterile) sectors and additional primordia somewhat later on the interstitial antepetalous areas. Five secondary androecial primordia arise centrally on alternipetalous androecial sectors (van Heel 1966, this paper); two whorls
filament tube and limit access to the nectar (Gibbs et al. 1988; Gibbs and Semir 2003). They are present in all moth(e.g. C. chodatii) and butterfly- (e.g. C. speciosa) pollinated species but absent or reduced in most bat-pollinated species (Gibbs and Semir 2003). Adaptations to birds have also been reported from several Adansonieae, e.g. Bombax ceiba (Neubauer 1964; Davis 1966) and Ceiba pubiflora (Gibbs and Semir 2003). They are mainly based on visual effects, such as red and yellow colors of floral parts but also different nectar components, a longer persistence of flowers and a shift towards diurnal anthesis. The second strategy to enlarge the pollen-liberating surface is found in other members of core Bombacoideae (e.g. Gyranthera) and in the closely related groups of Matisieae and Fremontodendreae, where single sessile monothecate stamens are typically very elongated and arranged in funnel- or cup-shaped flowers. Mainly bats have been reported to visit this flower type (e.g. Vogel 1969; Proctor et al. 1996). In Ochroma and Patinoa, for instance, the strongly elongated and convoluted pollen sacs cover the complete surface of the filament tube. The surface is provided with sticky mucilage, which improves the attachment of pollen to the bats’ fur. The quite robust funnel- or cup shaped flowers allow bats to cling to and partly enter them to forage on the abundant floral nectar without damaging the gynoecium (van der Pijl 1936; Jaeger 1974; Gru¨nmeier 1999). Brush-flowers with numerous stalked monothecate stamens occur in nearly all Adansonieae (excepting Spirotheca and some Ceiba spp.), in Catostemma/Scleronema and all core Malvoideae. Funnel- or cup-shaped flowers with elongated sessile monothecate stamens occur in the early branching lineages of Bombacoideae (Gyranthera/ Bernoullia/Huberodendron), in Ochroma/Patinoa, Septotheca (a lineage of unknown affiliation but most likely in Malvoideae), in Malvoideae-Matisieae and in Fremontodendreae. According to our present phylogenetic knowledge about the Malvatheca clade, bat-pollinated
Androecium structure and development in Adansonieae
flowers with elongated sessile monothecate stamens represent the ancestral condition in the clade (von Balthazar et al. 2006). The evolution of stalked monothecate stamens in brush-flowers from elongated sessile monothecate stamens by a subsequent development of ‘‘stalks’’ may have been driven by a switch from bat pollination to insect pollination (especially moths/butterflies in Adansonieae). This switch to insect pollination has presumably occurred in Malvatheca at least twice (Adansonieae + Catostemma/ Scleronema and core Malvoideae). The large number of species with brush-flowers that evolved in core Bombacoideae and core Malvoideae may indicate a species radiation in connection with the switch to insect pollination; the apparent morphological flexibility of bombacoid and malvoid brush flowers might be an important precondition for this. However, several reversals to bat and bird pollination have presumably taken place in Malvatheca, e.g. in Adansonia, moth pollination is very likely ancestral and switches to bat pollination derived (Baum et al. 1998). More detailed studies and a better phylogenetic resolution of Malvatheca are needed to shed light on the evolution of the various pollination syndromes in this clade.
Conclusions Our results show that early androecium development is overall very similar across Adansonieae. Ontogenetic patterns shared by all investigated taxa encompass the initiation of large-sized antepetalous primary androecial primordia (occasionally as common primordia with the petals) and smaller (sometimes absent) alternipetalous primary androecial primordia on a more or less distinct androecial ring wall, the subdivision of antepetalous primary androecial primordia into two half-primordia, the initiation of secondary androecial primordia on the primary androecial primordia in a centrifugal, rarely centripetal succession, the subsequent splitting of the secondary androecial primordia into tertiary primordia and the differentiation of monothecate stamens from the latter. Later ontogenetic stages vary between taxa due to different distribution and capacities of primordia-proliferating tissues which lead to different numbers and forms of anthetic structures. A nearly homogenous floral vasculature pattern was found across Adansonieae, which is similar to other Malvatheca taxa. Results from both structural and developmental studies indicate a tendency for a reduction of the alternipetalous androecial sectors in Adansonieae. This tendency is continued in other groups of Malvatheca where the alternipetalous androecial sectors do not produce any fertile organs (von Balthazar et al. 2004, 2006).
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The stalked monothecate stamens in Adansonieae result from a splitting of secondary androecial primordia and differentiation from tertiary (exceptionally secondary) androecial primordia. They are similar to the monothecate stamens in core Malvoideae, but derived independently as indicated by their phylogenetic relationship (Baum et al. 2004). An exceptional case was found in Ceiba, where the monothecate stamens are formed from ‘‘androecial complexes’’. Very similar brush flowers with large numbers of stalked monothecate stamens have evolved in core Bombacoideae and core Malvoideae independently but via similar ontogenetic pathways. Their evolution might have been driven by similar factors in pollination biology, for instance a switch from bat to insect pollination. Acknowledgments For valuable fixed plant material we would like to thank W. S. van Heel; L. Y. S. Aona; Sabah Agriculture Park, Tenom, Malaysia; Olbrich Botanic Gardens, Madison, WI, USA; Fairchild Tropical Garden, Coral Gables, FL, USA; Botanic Garden of the University of Zurich, Zurich, Switzerland and Palmengarten, Frankfurt am Main, Germany. We acknowledge the Laboratory of the Sect. Marine Evertebrates II, Senckenberg Research Institute in Frankfurt am Main and the BBPIC Laboratory of the University of Wisconsin, Madison for the use of the scanning electron microscopes. We thank Georg Zizka, Senckenberg Research Institute, Frankfurt am Main, and Matthias Jenny, Palmengarten, Frankfurt am Main for enabling access to laboratory and SEM. We are very grateful to Dieter Fiege and Marie Louise Tritz, Senckenberg Research Institute, Frankfurt am Main, for valuable aid and assistance on the SEM. For valuable comments on the manuscript we thank Ulrike Brunken. M. von Balthazar received financial support by grants from the National Science Foundation (NSF) to D. A. Baum (DEB 9876070; 0416096) and to W. S. Alverson (BSF-8800193) and by a postdoctoral fellowship from the Forschungskommission of the University of Zurich, Switzerland, and from the Swedish Research Council to E. M. Friis.
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