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Reassessing the Generic Status of Petalolophus (Annonaceae): Evidence for the Evolution of a Distinct Sapromyophilous Lineage within Pseuduvaria



The genus Petalolophus (Annonaceae) consists of only one species, P. megalopus, which is characterised by the possession of elaborate perianth wings that extend abaxially from the midrib of the inner petals. Recently published molecular phylogenetic data suggest that Petalolophus is congeneric with Pseuduvaria. Morphological and anatomical characteristics of both genera are critically re-examined and shown to support this conclusion: Petalolophus shares numerous characteristics in common with Pseuduvaria (particularly species from New Guinea) and it is only the autapomorphic possession of extended perianth wings that currently distinguish Petalolophus from Pseuduvaria. Petalolophus megalopus is accordingly formally transferred to Pseuduvaria. Field observations reveal that the flowers of Pseuduvaria megalopus are visited by flies; it is likely that pollination is sapromyophilous, and that the inner petal wings attract flies by mimicking carrion.
Systematic Botany (2005), 30(3): pp. 494–502
qCopyright 2005 by the American Society of Plant Taxonomists
Reassessing the Generic Status of Petalolophus (Annonaceae): Evidence for
the Evolution of a Distinct Sapromyophilous Lineage within Pseuduvaria
C. F. S
B. M
J. A. K
M. K. S
Department of Ecology & Biodiversity, The University of Hong Kong, Pokfulam Road, Hong Kong, China;
Nationaal Herbarium Nederland, Universiteit Leiden branch, P.O. Box 9514, 2300 RA Leiden, The Netherlands;
Papua New Guinea National Forest Authority, Papua New Guinea Forest Research Institute, Lae 411,
Morobe Province, Papua New Guinea
Author for Correspondence (
Communicating Editor: Thomas A. Ranker
.The genus Petalolophus (Annonaceae) consists of only one species, P. megalopus, which is characterised by the
possession of elaborate perianth wings that extend abaxially from the midrib of the inner petals. Recently published mo-
lecular phylogenetic data suggest that Petalolophus is congeneric with Pseuduvaria. Morphological and anatomical character-
istics of both genera are critically re-examined and shown to support this conclusion: Petalolophus shares numerous charac-
teristics in common with Pseuduvaria (particularly species from New Guinea) and it is only the autapomorphic possession
of extended perianth wings that currently distinguish Petalolophus from Pseuduvaria.Petalolophus megalopus is accordingly
formally transferred to Pseuduvaria. Field observations reveal that the flowers of Pseuduvaria megalopus are visited by flies; it
is likely that pollination is sapromyophilous, and that the inner petal wings attract flies by mimicking carrion.
The genus Petalolophus K. Schum. (Annonaceae) con-
sists of a single species, Pe. megalopus K. Schum. (Figs.
1–3), which is endemic to tropical lowland forests in
Papua New Guinea (Schumann and Lauterbach 1905).
As with most Annonaceae, the flowers have a whorl
of three sepals, and two whorls of three petals each.
The inner petals are connivent over the reproductive
organs, and are unique in the family in possessing
large, outwardly projecting ‘‘wings’’ that extend abax-
ially from the midrib (Figs. 1A–D, 2B).
This strikingly distinct floral morphology led to the
recognition and continued acceptance of Petalolophus as
a separate genus in various classification schemes (e.g.,
Hutchinson 1923, 1964; Fries 1959; Heusden 1992; Set-
ten and Koek-Noorman 1992; Keßler 1993, 1995). Con-
tradictory ideas relating to the taxonomic affinities of
Petalolophus have arisen due to differing interpretations
of floral structure. Hutchinson (1923, 1964) erroneously
interpreted Petalolophus flowers as having only three
petals, and accordingly grouped it with other annon-
aceous genera with a reduced number of petals (Table
1). Most classifications have generally associated Petal-
olophus with other genera that have mitriform inner
petals, such as Orophea Blume, Mitrephora Hook.f.&
Thomson, and Pseuduvaria Miq. (Table 1), irrespective
of whether the classifications were based on floral data
(Fries 1959; Heusden 1992; Keßler 1993, 1995), pollen
data (Walker 1971) or fruit and seed data (Setten and
Koek-Noorman 1992).
None of these studies specifically addressed the
phylogenetic relationships of Petalolophus.Molsetal.
(2004), however, recently investigated the phylogenetic
relationships within the tribe Miliuseae (sensu Keßler
1993) and related genera (including Pe. megalopus), us-
ing rbcL and trnL-trnF plastid DNA sequence data. This
study showed that Pe. megalopus was located within a
clade of four Pseuduvaria species, viz.: Ps. ‘‘brachyantha’’
Y. C. F. Su & R. M. K. Saunders (ined.), Ps. ‘‘coriacea’’
Y. C. F. Su & R. M. K. Saunders (ined.), Ps. rugosa
(Blume) Merr., and Ps. pamattonis (Miq.) Y. C. F. Su &
R. M. K. Saunders. Within this Pseuduvaria clade, Pe-
talolophus formed a comparatively robust clade with Ps.
brachyantha and Ps. coriacea (74% maximum parsimony
bootstrap support, 100% Bayesian posterior probabil-
ity), suggesting that Petalolophus and Pseuduvaria are
likely to be congeneric.
The genus Pseuduvaria was initially proposed by Mi-
quel (1858), and is currently recognised as comprising
51 species (Su 2002), although several of these species
still await formal publication. Pseuduvaria is widely dis-
tributed in Southeast Asia, extending from Myanmar
to northern Australia, and has a center of diversity in
New Guinea, where there are 19 species (Su 2002). The
genus is characterized by its small, axillary, and gen-
erally unisexual flowers, with outer petals that are
usually shorter than the inner, and with inner petals
that are apically connivent, forming a mitriform dome
over the reproductive organs.
The primary objective of this study is to critically
examine the morphology, anatomy and ultrastructure
of Pe. megalopus to determine whether the species
should be reclassified as a species of Pseuduvaria. Cor-
responding data on Pseuduvaria have been extracted
from the monographic revision recently completed by
Su (2002). The occurrence and distribution of calcium
oxalate crystals are investigated because they have
been shown to be diagnostically important in distin-
guishing Pseuduvaria from other annonaceous genera
.1. Pseuduvaria (5Petalolophus)megalopus. A. Flowering branch. B. Flower with proximal inner petal removed. C. Clawed
inner petal (adaxial), with extended undulating wing. D. Enlargement of base of (C). E. Isolated stamen. F. Fruit. (A, W. Takeuchi
& D. Ama 15599; B–E, W. Takeuchi & D. Ama 16666;F,W. Takeuchi & D. Ama 15682). Scale bars: A, C 52 cm; B 55 mm; D 5
4 mm; E 51 mm; F 53 mm. Drawing by J. H. van Os.
.2. Pseuduvaria (5Petalolophus)megalopus. A. Habit, showing pendent fruit (arrowed) and flowers, with long pedicel and
peduncle. B. Flower and immature fruit (lower left). (A, W. Takeuchi & D. Ama 17070;B,W. Takeuchi & D. Ama 16666).
. 3. Distribution of Pseuduvaria (5Petalolophus)megalo-
pus in New Guinea.
1. Previously suggested relationships between Petalolophus and other genera. Nomenclature follows Keßler (1993).
Based on
flower characters.
Based on fruit and seed characters.
Additional, doubtfully associated genera: Anomianthus,Fissistigma,Mitrella,Neo-
Reference Taxon/informal group Genera included
Hutchinson (1923)
Tribe Unoneae, subtribe Xylopi-
ineae, series Tripetalae
Dasymaschalon, Dennettia, Eburopetalum (5Anax-
agorea), Enantia (5Annickia), Petalolophus,
Thonnera (5Uvariopsis)
Fries (1959)
‘‘Orophea group’’ Atopostema, Exellia, Goniothalamus, Mitrephora,
Oreomitra, Orophea, Petalolophus, Phaeanthus,
Platymitra, Popowia, Pseuduvaria, Richella, Schef-
feromitra, Trivalvaria
Hutchinson (1964)
Tribe Unoneae, subtribe Xylopi-
ineae, ‘‘group C’’
Anaxagorea, Dasymaschalon, Dennettia, Enantia (5
Annickia), Petalolophus, Thonnera (5Uvariopsis)
Heusden (1992)
‘‘Mitrephora group’’ Fitzalania, Mezzettiopsis (5Orophea), Mitrephora,
Oreomitra, Orophea, Petalolophus, Platymitra, Po-
powia, Pseuduvaria
Setten and Koek-Noorman
‘‘Group 9’’ Mitrephora, Monocarpia, Petalolophus, Piptostigma,
Platymitra, Polyceratocarpus, Pseuduvaria
Keßler (1993, 1995)
‘‘Pseuduvaria group’’ Friesodielsia, Goniothalamus, Melodorum, Mitrepho-
ra, Oreomitra, Petalolophus, Pseuduvaria, Richel-
la, Schefferomitra
(Jovet-Ast 1942). Functional and evolutionary interpre-
tations of the elaborate inner petal wings are also dis-
cussed, following extensive field observations.
Calcium oxalate leaf crystals were examined by boiling herbar-
ium leaf specimens (Millar NGF 13801) in water for 15 mins and
bleaching (1:2 chlorox:water) overnight, and then peeling the ad-
axial and abaxial epidermal layers using fine forceps. Acid solu-
bility tests, with 2% hydrochloric acid and 5% glacial acetic acid
(Macnish et al. 2003), were used to tentatively determine crystal
chemical composition.
Stamen and pollen structure were studied with scanning elec-
tron microscopy (SEM) using herbarium specimens (Hartley 11333
and Takeuchi & Ama 16235). Pollen was gently shaken from de-
hiscing anthers onto adhesive conducting carbon tabs on specimen
stubs. All stub preparations were then sputter-coated with a mix-
ture of gold and palladium, and viewed using a Leica Cambridge
Stereoscan 440 SEM at 12 kV.
The herbarium specimens of Pe. megalopus examined are listed
in Appendix 1. Comparative morphological data on Pseuduvaria
species were abstracted from the recent taxonomic revision by Su
(2002). Field observations on the floral biology of Pe. megalopus
were made using naturally occurring populations in Morobe Prov-
ince, Papua New Guinea.
Comparative data on selected morphological char-
acters of Petalolophus and Pseuduvaria are presented in
Table 2. Three species of Pseuduvaria from New Guinea
(Ps. dolichonema (Diels) J. Sinclair, Ps. nova-guineensis J.
Sinclair, and Ps. sessilifolia J. Sinclair) are emphasised,
as they bear a particularly strong resemblance to Pe.
Habit. Petalolophus megalopus is a monocaul or spar-
ingly branched treelet to ca. 4 m, whereas Pseuduvaria
species are variably treelets to medium-sized trees,
ranging from less than 1 m (Ps. costata (Scheff.) J. Sin-
clair, from New Guinea) up to 40 m (Ps. rugosa, from
western Malesia).
Leaf Structure. Petalolophus megalopus leaves are es-
sentially sessile; in contrast, most Pseuduvaria species
have leaves that are petiolate, although two New Guin-
ea species, Ps. sessilifolia and a new, currently unde-
scribed species, are epetiolate.
Crystals are found in both the ad- and abaxial leaf
epidermal layers of both Petalolophus megalopus and all
species of Pseuduvaria. The crystals completely dis-
solved in 2% hydrochloric acid but only partially dis-
solved when pretreated with 5% acetic acid, suggest-
ing that they are composed of calcium oxalate (Mac-
nish et al. 2003). The adaxial foliar epidermis in Pe.
megalopus possesses druse crystals (Fig. 4A), whereas
the crystals in the abaxial epidermis are rhombic (Fig.
4B). Druse crystals are the predominant type in Pseu-
duvaria, although various other shapes also occur, in-
cluding book-shaped, rectangular, rhombic, and
square crystals.
2. Comparison of important morphological characteristics of Petalolophus megalopus and Pseuduvaria species.
character Pe. megalopus Ps. dolichonema Ps. nova-guineensis Ps. sessilifolia Other Pseuduvaria spp.
Petiole length 6absent 4–6 mm 2–6 mm 6absent Generally 2–10(–15) mm
Leaf crystals
Druse ? Druse Druse Variable, but predominantly
Leaf crystals
Rhombic ? Rhombic Rhombic Variable, but predominantly
Rachide length ,5mm ,5mm ,5mm ,5 mm Short (most species) to 35
mm (Ps. filipes)
Flowering pe-
duncle length
100–165(–270) mm ca. 200 mm 50–100 mm 44–92 mm Short (most species) to 35
mm (Ps. aurantiaca and Ps.
Flowering pedi-
cel length
(50–)65–95 mm ca. 27 mm 14–42 mm (2–)4–9 mm Short (most species) to ca. 60
mm (e.g., Ps. multiovulata)
Floral sex Androdioecious Dioecious? Hermaphro-
Dioecious Monoecious or dioecious, oc-
casionally androdioecious
or hermaphroditic
Inner petal wing Present Absent Absent Absent Absent
Inner petal
Absent Absent Present Absent Present or absent
Stamen number 60 (bisexual),
90 (staminate)
ca. 42 ca. 90 31–42 16–153
Carpel number ca. 15 ? ca. 5 ca. 5 (1–)2–30
Pollen exine Scabrate ? Rugulate Psilate Variably rugulate, verrucate,
scabrate or psilate
Monocarp stipe
Absent ? 1.5–7 mm Absent Absent, or up to 10(–20) mm
As with all Annonaceae, the leaves of both Petalolo-
phus and Pseuduvaria are hypostomatic with paracytic
stomata (Fig. 4B). The stomata are somewhat sunken
below the epidermal layer in Petalolophus, a feature that
is also observed in several Pseuduvaria species (Su
Inflorescence Structure. Inflorescence structure in
Petalolophus is essentially the same as that in Pseudu-
varia. Each inflorescence consists of a terminal flower
with a varying number of lateral rhipidia (Fig. 1A): in
Ps. sessilifolia, for example, the continued growth of
rhipidia produces up to 13 flowers, and Pe. megalopus
similarly produces up to five flowers (Fig. 1A).
Despite these similarities, Pe. megalopus differs from
Pseuduvaria in terms of the lengths of the rachides, pe-
duncles and pedicels, depending on specific species.
The internodal length in Ps. sessilifolia, for example, is
very short, resulting in very short rachides (ca. 5 mm
long), whereas the internodes are very long in Ps. filipes
(Lauterb. & K. Schum.) J. Sinclair, resulting in rachides
up to ca. 35 mm long. Petalolophus megalopus has short
rachis internodes (Fig. 1A), similar to those of most
Pseuduvaria species.
Flowering peduncles have proved to be very impor-
tant in species circumscription within Pseuduvaria,
since they are very variable in length (Su 2002). Petal-
olophus megalopus has remarkably long flowering pe-
duncles, generally 100–165(–270) mm long (Figs. 1A,
2A); similarly long peduncles are encountered in four
Pseuduvaria species from New Guinea, viz., a new, un-
described species (120–210 mm long), Ps. dolichonema
(ca. 200 mm long), Ps. nova-guineensis (50–100 mm
long), and Ps. sessilifolia (44–92 mm long). Petalolophus
megalopus has long flowering pedicels, (50–)65–95 mm
long (Figs. 1A, 2A), as well. Most Pseuduvaria species
have shorter pedicels (4–20 mm long), although com-
paratively long pedicels (up to 60 mm long) are ob-
served in some species, including Ps. multiovulata (C.
E. C. Fisch.) J. Sinclair.
Floral Sex. Although most species of Pseuduvaria
are monoecious or dioecious, with separate staminate
and pistillate flowers, it has recently been demonstrat-
ed (Su 2002) that several species from New Guinea
have bisexual flowers: Ps. grandifolia (Warb.) J. Sinclair
and Ps. pulchella (Diels) J. Sinclair are androdioecious,
and Ps. beccarii (Scheff.) J. Sinclair and Ps. nova-guineen-
sis appear to be wholly bisexual, with only hermaph-
roditic flowers. Although earlier reports suggested that
the flowers of Pe. megalopus are bisexual (Heusden
1992; Keßler 1993), the species is actually androdioe-
Perianth Structure. Contrary to the reports by
Hutchinson (1923, 1964), Pe. megalopus flowers consist
of six petals, not three. The perianth of Pe. megalopus
and all Pseuduvaria species are essentially the same: the
calyx consists of three small sepals, and the corolla
consists of two whorls of three petals each, with the
inner petals generally markedly longer than the outer
(Fig. 1B). The inner petals of both Petalolophus and
Pseuduvaria are apically connivent over the reproduc-
. 4. Leaf crystals of Pseuduvaria (5Petalolophus)megalopus. A. Adaxial leaf surface, showing druse crystals. B. Abaxial
leaf surface, showing rhombic crystals. (A, B, A. N. Millar NGF 13801). Scale bars: 50 mm.
tive organs; the base of the inner petals is clawed, re-
sulting in a dome-shaped structure with three lateral
apertures that enable entry of pollinators (Fig. 1B). The
claws are narrow, but their lengths vary significantly
between species.
The most notable diagnostic feature of Pe. megalopus
is the presence of the extraordinary undulating wings
that extend abaxially from the midrib of the inner pet-
als (Figs. 1A, 2B). These wings are large (ca. 30–70 mm
long, 20–45 mm wide) and deep red-purple. Pseudu-
varia species lack these wings entirely.
Within Pseuduvaria, the inner petals possess glands
that are diagnostically very important, since they ex-
hibit substantial taxonomic variation in both number
and shape. One or two glands are commonly located
on the inner surface of the inner petals, although some
species lack inner petal glands. Inner petal glands are
absent in Petalolophus.
Androecial Structure. Pseuduvaria species typically
have uvarioid stamens (sensu Prantl 1891), in which
the anthers are covered by broadened and flattened
connectives. This feature also occurs in Pe. megalopus
(Figs. 1E, 5A). Stamen number is diagnostically im-
portant within Pseuduvaria, with variation between 16
and 153 per flower, according to species. Petalolophus
megalopus flowers possess ca. 60 and 90 stamens in bi-
sexual and staminate flowers respectively.
Gynoecial Structure. The number of carpels per
flower is similarly useful taxonomically in Pseuduvaria,
in which species have (1–)2–30 carpels. Petalolophus me-
galopus has ca. 15 carpels per flower, and is therefore
within the range for Pseuduvaria species. The structure
of the carpels in Pe. megalopus is similar to those of
Pseuduvaria: they are free, lack styles, and are ellipsoid
and very densely hispid. There are approximately six
ovules per carpel, arranged in two rows with lateral
Pollen Structure. The structure of the pollen of 42
species of Pseuduvaria has recently been described by
Su and Saunders (2003). The pollen is consistently re-
leased as acalymmate tetrads, and is inaperturate, is-
opolar, and radially symmetrical, with four basic pat-
terns of exine sculpturing, viz. rugulate, verrucate, sca-
brate and psilate. The pollen of Pe. megalopus shares
these tetrad arrangement, aperture and shape features
(Walker 1971), and has a scabrate exine (Fig. 5B). Su
and Saunders (2003) also highlighted different mech-
anisms of cohesion between pollen grains of Pseudu-
varia, both within and between tetrads, including short
exinal connections and non-sporopollenin pollen-con-
necting threads; similar cohesion mechanisms occur in
Pe. megalopus (Fig. 5C, D).
Fruit and Seed Morphology. Petalolophus and Pseu-
duvaria have essentially similar fruits. Petalolophus mon-
ocarps are globose, smooth, and sessile (Figs. 1F, 2B).
Monocarp shape is not very variable in Pseuduvaria,
being predominantly globose, or sometimes ellipsoid,
ovoid, or obovoid; Pseuduvaria monocarps are further-
more variably smooth, rugulose or rugose, and are also
variably sessile or stipitate. The seeds of Pe. megalopus
and most Pseuduvaria species are rugose.
Generic Status of Petalolophus. Recent molecular
phylogenetic analyses of the tribe Miliuseae and relat-
ed genera (Mols et al. 2004) have shown that Pe. me-
galopus is nested within a clade of four Pseuduvaria spe-
cies, providing strong evidence that the two genera are
congeneric. The morphology of Pe. megalopus has never
previously been critically examined, and many struc-
tural features are reported or described here for the
first time, including leaf crystal structure and distri-
bution, stomatal structure, inflorescence structure, car-
. 5. Stamen and pollen of Pseuduvaria (5Petalolophus)megalopus (scanning electron micrographs). A. Isolated stamen. B.
Pollen in tetrads. C. Short exinal connections (arrowed) linking pollen grains of adjacent tetrads. D. Pollen-connecting thread
(arrowed) linking grains within a tetrad. (A, T. G. Hartley 11333; B–D, W. Takeuchi & D. Ama 16235). Scale bars: A 5500 mm;
B520 mm; C, D 55mm.
pel and stamen number and shape, and pollen ultra-
structure. It is clear that Pe. megalopus shares many
characteristics with Pseuduvaria, and that the only sig-
nificant morphological difference is the possession of
elaborate perianth wings, extending abaxially from the
midribs of the three inner petals. Previous descriptions
of the large size of the inner petals in Pe. megalopus
refer to the size of these wings: the main lamina of the
inner petal is actually small, as in all Pseuduvaria spe-
cies. There are therefore no convincing morphological
criteria to support the continued acceptance of Petalo-
lophus as a distinct genus, since the presence of large
lateral wings on the inner petals is autapomorphic. The
formal transfer of Pe. megalopus to Pseuduvaria is ac-
cordingly validated below.
Taxonomic Affinities. Pseuduvaria megalopus has
greatest similarities with several other Pseuduvaria spe-
cies (Table 2), which are significantly also from New
Guinea (Su 2002). Remarkably long flowering pedun-
cles are observed in four species in addition to Ps. me-
galopus, viz. Ps. dolichonema,Ps. nova-guineensis,Ps. ses-
silifolia, and a new, undescribed species. These species
are also broadly united by the absence of petioles, ex-
cept Ps. dolichonema and Ps. nova-guineensis, which have
short petioles, 2–6 mm long. Within this group of pu-
tative relatives, Ps. megalopus is arguably most similar
to Ps. nova-guineensis, since they both have long pedi-
cels (although this is a feature observed in several oth-
er species, including Ps. mulgraveana Jessup, Ps. multio-
vulata,Ps. reticulata (Blume) Miq., and Ps. villosa Jes-
Although the majority of Pseuduvaria species are di-
oecious or monoecious, with unisexual flowers, a lim-
ited degree of variability is evident in the species from
New Guinea: the androdioecy reported here for Ps. me-
galopus is also found in Ps. grandifolia and Ps. pulchella;
and solely hermaphroditic flowers are observed in Ps.
beccarii (Scheff.) J. Sinclair and Ps. nova-guineensis.Itcan
be assumed that there has been an evolutionary tran-
sition within Pseuduvaria from hermaphroditic flowers
(which is the widespread condition in the Annonaceae,
and therefore presumably plesiomorphic) to unisexual
flowers (often with sterile staminodes in the pistillate
flowers), possibly via androdioecious intermediates.
On the basis of these characteristics, it is tentatively
suggested that Ps. megalopus is most closely related to
Ps. nova-guineensis.
Evolution of Sapromyophily. Pijl (1961) was the
first to provide a functional interpretation of floral
structure in Pseuduvaria with respect to pollination sys-
tem. In the absence of field observations, he suggested
that the genus is fly-pollinated based on the floral
structure, particularly the mitriform inner petals and
petal pigmentation. This has subsequently been con-
firmed for three Australian species, viz. an unidenti-
fied species which is assumed here to be Ps. mulgra-
veana var. glabrescens Jessup on the basis of published
photographs (Morawetz 1988), and Ps. froggattii (F.
Muell.) Jessup and Ps. hylandii Jessup (Silberbauer-
Gottsberger et al. 2003). The latter study was more de-
tailed, but all three species appear to show the same
basic features. Initial anthesis is diurnal, with the outer
petals spreading open to reveal apertures between the
claws of the inner petals. As the flowers mature, spe-
cific areas of the inner petals become progressively
darker red-purple, and glands located marginally on
the adaxial surface of the inner petals enlarge and be-
gin secreting nectar. The flowers of Ps. froggattii are
reported to emit a strong odor of ‘‘old dishwater and
vomit’’ (Silberbauer-Gottsberger et al. 2003). These fea-
tures suggest that these species of Pseuduvaria are sap-
romyophilous, in which flies are attracted by the scent
and appearance of rotting meat. The pollinators were
identified as small flies in both studies (Morawetz
1988; Silberbauer-Gottsberger et al. 2003), and specifi-
cally Drosophilidae in the case of P. froggattii (Silber-
bauer-Gottsberger et al. 2003).
Although the pollination ecology of other Pseuduvar-
ia species has not been studied, it is suggested here
that sapromyophily is not ubiquitous in the genus:
many species (such as Ps. rugosa) have basically light
yellow petals and lack the prominent glands and lo-
calized pigmentation described above. These species
are presumably myophilous, but attract flies with
sweet nectar rather than by mimicking carrion.
The elaborate inner petal wings observed in Ps. me-
galopus are presumably adaptations for pollinator at-
traction. The wings are dark purple and have an irreg-
ular, undulating appearance, reminiscent of carrion
(Fig. 2B). Field observations have revealed that the
flowers are visited by comparatively large flies, and
the species is therefore also likely to be sapromyophil-
ous. Casual observations did not reveal any specific
odor, nor the occurrence of inner petal glands; it is
possible, however, that the absence of these features is
correlated with immaturity of the flowers observed. It
is suggested that the large inner petal wings are visual
stimuli for flies, and that the species is sapromyophil-
ous. If this is true, the species represents a distinct sap-
romyophilous lineage within Pseuduvaria, in which the
attractant for the flies are massively enlarged perianth
wings rather than the small pigmented glands ob-
served in other species.
Pseuduvaria megalopus (K. Schum.) Y. C. F. Su & J.
B. Mols, comb. nov.—Petalolophus megalopus K.
Schum. in K. Schum. & Lauterb., Nachtr. Fl.
Deutsch. Schutzg. Su¨ dsee 265. 1905.—T
: precise locality not known, without date,
G. Bamler 42 (lectotype: WRSL [photo!], designat-
ed by Diels 1913: 162).
Specimens Examined. PAPUA NEW GUINEA. M
: north of Walium station, Ramu subprovince, 58
309S, 1458249E, S. H. Sohmer & P. Katik LAE 75132
: Atzera range, 2 miles N of Lae, T. G.
Hartley 11333 (K, LAE); Oomsis, near Lae, 68359S, 1468
259E, E. E. Henty NGF 10676 (LAE); Oomsis logging
area, Lae, 68409S, 1468459E, E. E. Henty NGF 14900
(L, LAE); Oomsis logging road, near Oomsis river, Lae,
68459S, 1478209E, P. Katik LAE 77973 (L, LAE); 3 mile
agriculture station, near Lae, 68459S, 1478E, P. Katik
& J. S. Womersley NGF 24872 (LAE); Lae, 68459S, 1478
E, A. N. Millar NGF 13801 (LAE); Atzera range, ridge
adjacent to 7–8 mile settlement, 68419S, 1468579E, W.
Takeuchi 9260 (L), 9260B (LAE); near Bubia, 68409S,
1468569E, W. Takeuchi & D. Ama 15599 (L), 15682 (L),
16235 (L, LAE); hills near Taraka, Lae, W. Takeuchi &
D. Ama 16666 (L); Kamiali wildlife management area,
N of Tabare (Tabali) river, 78169S, 1478069E, W. Tak-
euchi, D. Ama & A. Towat i 15167 (L, LAE); near Surin-
umu, Sogeri region, Central district, 98259S, 1478259
E, J. S. Womersley NGF 19131 (LAE).
. Financial support for this project was
provided by grants from the Hong Kong Research Grants Council
(HKU 7358/03M, awarded to RMKS), and The University of Hong
Kong CRCG (awarded to YCFS and RMKS). We are also grateful
to the directors of K, L, and LAE for the loan of material; Dr
Krzysztof Swierkosz (WRSL) for providing a photograph of the
lectotype; J. H. van Os for the excellent line drawing; staff of the
Electron Microscope Unit at the University of Hong Kong for tech-
nical assistance; and David Johnson, Tom Ranker and an anony-
mous reviewer for their comments.
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... Gottsberger, 1999;. Despite the prevalence of beetle pollination in the family, a diverse array of other insect guilds also act as pollinators, including thrips (Gottsberger, 1970;Webber & Gottsberger, 1995;Küchmeister et al., 1998;Momose, Nagamitsu & Inoue, 1998a;Momose et al., 1998b;Silberbauer-Gottsberger et al., 2003), flies (Gottsberger, 1985;Morawetz, 1988;Norman, Rice & Cochran, 1992;Su et al., 2005), bees (Olesen, 1992;Carvalho & Webber, 2000;Silberbauer-Gottsberger et al., 2003;Teichert, 2007;Teichert et al., 2009) and cockroaches (Nagamitsu & Inoue, 1997). There is therefore convincing evidence that many pollination systems in Annonaceae are specialized at the pollinator guild level. ...
... Flowers of most of the genera studied are visited exclusively or predominantly by small beetles, although other pollinator guilds are also important, including large beetles (Malmea R.E.Fr.: Gottsberger, 1999;Mosannona Chatrou: Schatz, 1987, 1990Murray, 1993;Chatrou & Listabarth, 1998), thrips (Bocageopsis R.E.Fr. : Webber & Gottsberger, 1995;Silberbauer-Gottsberger et al., 2003;Oxandra A.Rich.: Webber & Gottsberger, 1995;Popowia A.Rich.: Momose et al., 1998a, b;Roubik et al., 2005), bees (Sapranthus Seem.: Olesen, 1992;Unonopsis R.E.Fr.: Carvalho & Webber, 2000;Silberbauer-Gottsberger et al., 2003;Teichert, 2007;Teichert et al., 2009) and flies (Pseuduvaria Miq.: Morawetz, 1988;Silberbauer-Gottsberger et al., 2003;Su et al., 2005;Su & Saunders, 2006). ...
... Despite the vast diversity of dipterans and their evident importance in pollination, there are few reports of fly pollination in Annonaceae: flower visits by flies have only been reported for Annona (Webber, 1981b; as secondary floral visitors only), Asimina (Norman et al., 1992), Monodora (Gottsberger, 1985;Gottsberger et al., 2011), Pseuduvaria (Morawetz, 1988;Silberbauer-Gottsberger et al., 2003;Su et al., 2005) and Uvariopsis (Gottsberger et al., 2011). It should be noted, however, that Norman et al. (1992) did not observe any pollen attached to the common drosophilid flies that visited Asimina flowers (pollination resulted from visits by nitidulid beetles and rarer calliphorid flies), and that pollen transfer between flowers was not demonstrated in any of the other studies. ...
The pollination biology of Annonaceae has received considerable attention, with data now available for > 45% of the genera (or genus‐equivalent clades) included in recent molecular phylogenetic analyses. This provides a basis for understanding evolutionary shifts in the pollination system within the family. The present study focuses on subfamilies Anaxagoreoideae, Ambavioideae and Annonoideae, for which robust, well‐resolved phylogenetic trees are available. Information is summarized on the pollination biology of individual clades and the evolutionary adaptations favouring different pollinator guilds evaluated. Although the majority of species of Annonaceae are pollinated by small beetles, five other pollinator groups are known: large beetles, thrips, flies, bees and cockroaches. Small‐beetle pollination is inferred as the ancestral pollination system, with all other systems being derived. Evolutionary shifts to pollination by large beetles, thrips and flies are unlikely to have been significantly constrained by previous adaptations favouring pollination by small beetles, as many of the adaptations to these different pollinator guilds are similar (including protogyny, partially enclosed floral chambers and olfactory cues). In contrast, however, the evolutionary shift to bee pollination has presumably been constrained by both protogyny (as pollen‐collecting bees are unlikely to visit pistillate‐phase flowers) and the presence of floral chambers. © 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2012, 169, 222–244.
... Y.C.F. Su & Mols [19]. Silberbauer-Gottsberger et al. furthermore suggested that P. hylandii Jessup and P. villosa Jessup were also probably pollinated by flies [18], but no empirical data was provided. ...
... Previous studies of the pollination biology of Pseuduvaria species have indicated fly pollination [17], [18], [19]. The possibility that the unidentified fly species observed visiting flowers of P. mulgraveana may act as a pollinator cannot be precluded; this would certainly be consistent with morphological characteristics of the flowers that are indicative of fly pollination, including the localized areas of dark red-purple pigmentation on the petals, and the presence of nectary glands. ...
... Silberbauer-Gottsberger et al. furthermore suggested that P. hylandii Jessup and P. villosa Jessup were also probably pollinated by flies [18], but no empirical data was provided. Although several of these species may be sapromyophilous (e.g., P. froggattii [18], P. megalopus [19]), it has been suggested that sapromyophily is unlikely to be ubiquitous in the genus as many species (e.g., P. rugosa (Blume) Merr. and P. trimera (Craib) Y.C.F. ...
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Unlike most genera in the early-divergent angiosperm family Annonaceae, Pseuduvaria exhibits a diversity of floral sex expression. Most species are structurally andromonoecious (or possibly androdioecious), although the hermaphroditic flowers have been inferred to be functionally pistillate, with sterile staminodes. Pseuduvaria presents an ideal model for investigating the evolution of floral sex in early-divergent angiosperms, although detailed empirical studies are currently lacking. The phenology and pollination ecology of the Australian endemic species Pseuduvaria mulgraveana are studied in detail, including evaluations of floral scent chemistry, pollen viability, and floral visitors. Results showed that the flowers are pollinated by small diurnal nitidulid beetles and are protogynous. Pollen from both hermaphroditic and staminate flowers are shown to be equally viable. The structurally hermaphroditic flowers are nevertheless functionally pistillate as anther dehiscence is delayed until after petal abscission and hence after the departure of pollinators. This mechanism to achieve functional unisexuality of flowers has not previously been reported in angiosperms. It is known that protogyny is widespread amongst early-divergent angiosperms, including the Annonaceae, and is effective in preventing autogamy. Delayed anther dehiscence represents a further elaboration of this, and is effective in preventing geitonogamy since very few sexually mature flowers occur simultaneously in an individual. We highlight the necessity for field-based empirical interpretations of functional floral sex expression prior to evaluations of evolutionary processes.
... Although sapromyiophilous flowers rely heavily on olfactory attractants (discussed in Section 2.3), there are also distinctive visual syndromes, with dull red petals that are often enlarged and have a corrugated surface (Chen et al., 2015). Examples within Annonaceae include Asimina parviflora (Norman et al., 1992), Meiogyne species formerly classified as Fitzalania ( Fig. 1C; Thomas et al., 2012), Monodora tenuifolia , Pseuduvaria megalopus (Su et al., 2005), and Stenanona flagelliflora (Xicohténcatl-Lara et al., 2016). A similar saprocantharophilous syndrome has been reported for Duguetia cadaverica , involving the attraction of nitidulid beetles rather than flies. ...
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Potential key functional floral traits are assessed in the species‐rich early divergent angiosperm family Annonaceae. Pollinators (generally beetles) are attracted by various cues (particularly visual, olfactory and thermogenic), with pollinators rewarded by nectar (generally as stigmatic exudate), heat and protection within the partially enclosed floral chamber. Petals sometimes function as pollinator brood sites, although this may be deceptive. Annonaceae species are self‐compatible, with outcrossing promoted by a combination of protogyny, herkogamy, floral synchrony and dicliny. Pollination efficiency is enhanced by pollen aggregation, changes in anthesis duration, and pollinator trapping involving a close alignment between petal movements and the circadian rhythms of pollinators. Most Annonaceae flowers are apocarpous, with syncarpy restricted to very few lineages; fertilization is therefore optimized by intercarpellary growth of pollen tubes, either via stigmatic exudate (suprastylar extragynoecial compitum, EGC) or possibly the floral receptacle (infrastylar EGC). Although Annonaceae lack a distinct style, the stigmas in several lineages are elongated to form ‘pseudostyles’ that are hypothesized to function as sites for pollen competition. Flowers can be regarded as immature fruits in which the ovules are yet to be fertilized, with floral traits that may have little selective advantage during anthesis theoretically promoting fruit and seed dispersal. The plesiomorphic apocarpous trait may have been perpetuated in Annonaceae flowers since it promotes the independent dispersal of fruit monocarps (derived from separate carpels), thereby maximizing the spatial/temporal distance between seedlings. This might compensate for the lack of genetic diversity among seeds within fruits arising from the limited diversity of pollen donors. This article is protected by copyright. All rights reserved.
... Extensive morphological convergence of floral characters is widespread in Annonaceae (Saunders, 2010) and is manifest in the historical absence of a consensus higher-level classification for the family (Koek-Noorman & al., 1990). Recent molecular phylogenetic research into the family has enabled a broad consensus on major clades and has resulted in many changes in generic delimitation, involving either the merging of previously recognized genera (Su & al., 2005Nakkuntod & al., 2009;Zhou & al., 2009Zhou & al., , 2010 or the splitting of existing genera (Mols & al., 2008). ...
Generic delimitation of Cyathocalyx and Drepananthus has been controversial, with some authors recognizing them as distinct genera, and others recognizing a more broadly defined Cyathocalyx, inclusive of Drepananthus. Some doubt also exists regarding the relationships between these taxa and Cananga. Molecular phylogenetic analyses are presented based on combined psbA‐trnH spacer, trnL‐F, matK and rbcL sequences. Results indicate that Cananga, Cyathocalyx s.str. and Drepananthus form three generally well‐supported clades, although with inadequate resolution of relationships among the three clades. Morphological variation is re‐evaluated, and the narrower delimitation of Cyathocalyx proposed, necessitating 21 new nomenclatural combinations following the recognition of Drepananthus as a distinct genus. Divergence times are estimated using an uncorrelated lognormal distributed (UCLD) relaxed molecular clock. Historical biogeographical analysis suggests that the ambavioid lineage originated in Africa, with subsequent dispersal into Asia. Alternative hypotheses for this dispersal, involving rafting on the Indian tectonic plate versus migration via the extensive boreotropical forests associated with the Eocene thermal maximum, are evaluated, and the latter route identified as the most consistent with the divergence age estimates and the geological and palaeoclimatic data.
... Moreover, most of these groups of insects are not known as pollinators (Proctor & Yeo, 1973;Proctor et al., 1996;Ollerton, 1999;Silva & Domingues, 2010). Furthermore, although the flowers of S. flagelliflora were visited by several groups of insects, such as it has been recorded in other Annonaceae species (Nagamitsu & Inoue, 1997;Küchmeister et al., 1998;Carvalho & Webber, 2000;Silberbauer-Gottsberger et al., 2003;Ratnayake et al., 2006aRatnayake et al., , 2007; they have several traits that are associated with fly pollination (Norman et al., 1992;Gottsberger, 1999;Silberbauer-Gottsberger et al., 2003;Su et al., 2005;Gottsberger et al., 2011). For instance, the flowers of S. flagelliflora are dark purple -red in colour, grow on the surface of the ground (Schatz & Wendt, 2004); produce stigmatic exudates (Corona, 2012) and pollen grains (Endress & Doyle, 2009) as rewards for their pollinators; and form a floral chamber (Gottsberger, 1989(Gottsberger, , 1999Silberbauer-Gottsberger et al., 2003;Teichert et al., 2011). ...
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Stenanona flagelliflora was described in 2004. There are no studies on its biology. The goal of this study was to document some aspects of its reproductive biology. The particular objectives were to: i) describe the variation on vegetative and floral traits; ii) establish the composition of the community of floral visitors; iii) estimate the mating system and reproductive success; and, iv) establish the relationship between vegetative traits and reproductive success. The study was conducted within the Los Tuxtlas Biosphere Reserve, Veracruz, Mexico. We quantified several vegetative and floral traits; conducted observations and collected floral visitors; and determined the mating system and reproductive success. Stenanona flagelliflora has relatively few stamens and carpels, but a relatively high viability of pollen grains. The most abundant floral visitors were dipterans from the Phoridae Family. Mating system is between xenogamous and facultative xenogamous; thus, pollination depends upon pollen vectors. Fruit-set was relatively high; but seed-set was very low, because most monocarps did not contain seeds. Our results suggest that reproduction of S. flagelliflora is not limited by resource availability, but by pollinator frequency and effectiveness. To our knowledge, this is the first study on the reproductive biology of a species within the Stenanona genus.
... As per the current understanding, Annonaceae have four subfamilies: Anaxagoreoideae, Ambavioideae, Annonoideae and Malmeoideae . Phylogenetic studies on Annonaceae (Mols et al. 2004;Erkens et al. 2007;Su et al. 2008;Nakkuntod et al. 2009;Chatrou et al. 2012) have brought significant changes in circumscription and nomenclature of several genera due to the strict adherence to the principle of monophyly (Su et al. 2005(Su et al. , 2010Rainer, 2007;Mols et al. 2008;Saunders, 2009;Chaowasku et al. 2011Chaowasku et al. , 2012Xue et al. 2012Xue et al. , 2014. The problematic case of the polyphyletic genus Polyalthia Blume s.l. ...
... The ubiquitous occurrence of protogyny in hermaphroditic flowers in Annonaceae is likely to have imposed significant constraints on the evolution of alternative pollination systems. Unlike many plant families with equivalent levels of species diversity, Annonaceae are remarkably uniform in pollination biology (Saunders, 2012): the great majority of species are pollinated by beetles (with distinct small-and large-beetle pollination syndromes evident: Gottsberger, 1999Gottsberger, , 2012Silberbauer-Gottsberger et al., 2003;Goodrich, 2012;Saunders, 2012), although thrips (Gottsberger, 1970;Webber & Gottsberger, 1995;Küchmeister et al., 1998;Momose et al., 1998a, b;Silberbauer-Gottsberger et al., 2003) and flies (Gottsberger, 1985;Morawetz, 1988;Norman et al., 1992;Su et al., 2005) are also important pollinators to a lesser extent. ...
Annonaceae flowers are generally hermaphroditic and show high levels of outcrossing, but unlike many other early-divergent angiosperms lack a self-incompatibility mechanism. We reassess the diversity of mechanisms that have evolved to avoid self-pollination in the family. Protogyny occurs in all hermaphroditic flowers in the family, preventing autogamy but not geitonogamy. Herkogamy is rare in Annonaceae and is likely to be less effective as beetles move randomly around the flowers in search of food and/or mates. Geitonogamy is largely avoided in Annonaceae by combining protogyny with floral synchrony, manifested as either pistillate/staminate-phase synchrony (in which pistillate-phase and staminate-phase flowers do not co-occur on an individual) or heterodichogamy (in which two phenologically distinct and reproductively isolated morphs coexist in populations). Unisexual flowers have evolved independently in several lineages, mostly as andromonoecy (possibly androdioecy). Functionally monoecious populations have evolved from andromonoecious ancestors through the loss of staminate function in structurally hermaphroditic flowers. This has been achieved in different ways, including incomplete pollen/stamen development and delayed anther dehiscence. Angiosperms display an enormous diversity of mechanisms to promote xenogamy, many of which are easily overlooked without fieldwork. Floral phenology is particularly important, especially cryptic differences in timing of organ maturation or abscission. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 93–109.
... Most species studied in Annonaceae are pollinated by beetles and exhibit characteristics typical of small or large beetle pollination syndromes, including fleshy petals or food bodies, fruity, spicy or decaying scents and the formation of protective chambers (Momose et al., 1998b;Gottsberger, 1999;Silberbauer-Gottsberger et al., 2003;. Although fly pollination is less common in the family (Willson & Schemske, 1980;Norman, Rice & Cochran, 1992;Su et al., 2005), Silberbauer-Gottsberger et al. (2003) noted the occasional occurrence of characters consistent with this syndrome in Old and New World Annonaceae: spots of translucent tissue, unpleasant, sour or fermenting scents and nectar production. Thrips have been identified as either primary or secondary pollinators in a few species of Annonaceae (Momose et al., 1998a;Jürgens et al., 2000;Norman, 2003;Silberbauer-Gottsberger et al., 2003). ...
Many species of Annonaceae are known for their distinctive, penetrating floral aromas. Numerous pollination studies have documented floral scents which probably play a key role in specialized pollination strategies. In particular, floral scents appear to play crucial roles in deceptive pollination strategies, contributing to floral mimicry of ripe or decaying fruits, fungi and, potentially, carrion or faeces. Occasionally, floral scent may advertise genuine floral rewards, as is the case for two species of Unonopsis pollinated by male euglossine bees. To date, ten studies have chemically characterized floral scent for 24 species representing 11 genera of Annonaceae. In this review, I discuss the chemical composition and diversity of the analysed floral scents in Annonaceae. I also summarize and discuss a wide range of (human) perceptual descriptions of floral scent found throughout the literature on Annonaceae. I have framed discussions of floral scent in Annonaceae in ecological and evolutionary contexts whenever possible. © 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2012, 169, 262–279.
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Biologists are fascinated by species-rich groups and would like to discover the causes for abundant diversification. Understanding the evolution of the family of Annonaceae (c. 2500 species in 130 genera) can contribute greatly to our understanding of the processes that have led to the assembly of current day biodiversity. The available phylogenetic data on Annonaceae and dates for all the clades in the family can be used to study diversification patterns in order to identify factors that drive speciation and the evolution of morphological (key-) characters. In this study it was found that, except for Goniothalamus, the largest genera in the family are not the result of radiations. Furthermore, the difference in species numbers between the Long Branch Clade and Short Branch Clade cannot be attributed to significant differences in diversificati on rate. Most of the speciation within Annonaceae is not discernible from a stochastic ERM branching model (i.e. chance) and no special explanations are therefore necessary for the distribution of species-richn ess across the major part of the Annonaceae phylogeny. Because of geographic structure, a number of clades might be species- rich as the result of a radiation after a founder event. Also, large clade sizes within Annonaceae need not have resulted from intrinsic key-innovations that have influenced the rate of diversificati on. Only for a small number of clades, key- innovations might be invoked to explain the elevated rate of diversification.
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The Annonaceae show a broader flower biological radiation than originally thought, with flowers being pollinated not only by beetles, but also by thrips, flies and even bees. The majority of species have hermaphroditic protogynous flowers. Species with white or yellowish-white, small, delicate, day-active flowers, may be pollinated either solely by thrips, or by thrips and small beetles (e.g., species of Bocageopsis, Oxandra, Xylopia). Several of these thrips-pollinated species have stamens with an elongated, tongue-like connective. Pollination by flies is not well documented for American species, notwithstanding it appears to be more common in Old World species, e.g., in the genus Pseuduvaria. The mitriform flowers exhale an unpleasant smell, produce nectar in purple-colored petal glands and have a sapromyiophilous syndrome. Flies enter the flower center through large openings between the inner petals. Beetle-pollinated Annonaceae have flowers with comparatively thick and, often, fleshy petals, which, during anthesis frequently form a pollination chamber with the petals inclining over the flower center. The stamens usually have peltate connective shields, probably a device for protection against voracious beetles. Some cantharophilous species have flowers which are day-active while others are night-active. When they are in their pistillate phase, the beetles are attracted by characteristic odor components. They enter the pollination chamber and usually remain in the interior of the flower until the flower has changed to its staminate phase, when pollen is shed and afterwards petals and stamens detach. Two lines of cantharophilous Annonaceae are recognizable on the basis of present knowledge. Species with smaller and more delicate flowers are pollinated by small beetles (Nitidulidae, Curculionidae, Chrysomelidae and Staphylinidae), whereas species with large, more robust flowers in the Neotropics are pollinated by large beetles of the family Scarabaeidae, subfamily Dynastinae. Some species of the cantharophilous Annonaceae, especially the large-flowered ones, but also some species with smaller flowers, produce beat during anthesis (thermogenesis). Food bodies, developed on the adaxial surfaces or sides of the petals, provide unique nourishment possibilities for beetles when they stay inside the flowers during the pistillate phase. In the staminate stage of the flower, after pollen is shed, beetles also feed on pollen. Apparently, no dynastid-flower relationship has evolved in Asia and Australia. Pollination by bees was discovered recently in Unonopsis guatterioides in Amazonia and Uvaria concava in North Queensland: the first by scent-collecting euglossine males and the second by pollen-collecting Meliponinae. The general trends in morphological/functional floral characteristics in the family are discussed in a presumptive phylogenetic context.
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The tribe Miliuseae (Annonaceae) comprises six genera distributed in Asia: Alphonsea, Mezzettia, Miliusa, Orophea, Platymitra, and Phoenicanthus. A phylogenetic study to investigate the putative monophyly of the tribe and the intergeneric relationships is presented here. Nucleotide sequences of the plastid gene rbcL, trnL intron, and trnL-trnF intergenic spacer were analyzed from 114 Annonaceae taxa, including 24 Miliuseae species and two outgroups using maximum parsimony and Bayesian inference. The two data sets (rbcL and the trnL-trnF regions) were analyzed separately and in combination. Miliuseae were found to be polyphyletic due to the position of Mezzettia and are part of a large, predominantly Asian and Central-American clade (miliusoid clade). Although intergeneric relationships were poorly resolved, all genera, except Polyalthia, were monophyletic, supporting previous generic delimitation based on morphology. A group of three Polyalthia species seems the most likely sister group of Miliusa. Several infrageneric groups of Miliusa, Orophea, and Polyalthia are supported by both molecular and morphological data. No morphological synapomorphies have yet been found for the miliusoid clade. Molecular clades within the miliusoid clade, however, can be characterized by size and the shape of the outer petals, number of ovules per carpel, and the size of the fruits.
1. The study of flower-classes does not lead to delimitations of groups, but can supply the ecological background for evolutionary trends in such groups. The preference of visitors is not, as thought by Goebel, always just utilization of a loose incidental character. 2. In the class of sapromyophiles a complex of characters fitted for flies is demonstrated to be a convergence. This explains much in the Annonaceae. In some orchids regression to fly pollination leads to a return to radial symmetry. Knowledge of the character complex serves to revise the separation of genera for conspicuous structures, still inside the ecological complex (Cryptophoranthus and Cirropetalum). 3. In one of the melittophilous subclasses, viz. the Xylocopa-flowers, there evolved a new protection against "unwanted" activities of rude pollinators, an ant-guard. The failing of such contraptions in flowers for birds and bumblebees, used by anti-selectionists, seems an as yet unbalanced condition. 4. The study of the floral spectrum of some families has divulged that some "ecologisms" have already become suprageneric "morphologisms." The parallelism of forms in distant groups is not undirected, kaleidoscopic morphological repetition as believed by Good, but is convergence. 5. In ornithophiles we also find a typical complex of characteristics though superimposed on different, older, "morphological" substrata. There are many transitional flowers, fitted for unspecialized birds. Independent development in the Old and New Worlds has led to differences in style. 6. In chiropterophily we find transitional cases, visited by transitional nectar-bats, still mainly destructive. Some families, as Bignoniaceae and Cactaceae, show a preadaptive basis, sometimes leading separately to bat-pollination in Old- and New-World forms. Some points of the syndrome (flagelliflory and cauliflory) explain typically "tropical" characteristics. Seed-dispersal by bats may also provide a pre-adaptive basis.
Walker, J. W. (Dept. Bot., Univ. Mass., Amherst, Mass., USA.) Contributions to the pollen morphology and phytogeny. of the Annonaceae. I. Grana 11:45-54. Illus. 1971.-In an earlier paper, which includes pollen descriptions for 93 genera and approximately 430 species of the large, tropical family Annonaceae, the author laid the foundation for a generic reclassification and natural phylogeny of the family based largely on comparative palynology. The present paper includes generic pollen descriptions for an additional 18 genera and 21 species of Annonaceae.
Chromosome counts are presented for 12 genera and 20 species of AustralianAnnonaceae (all diploid with 2n = 16 or 18; Table 1) and two species ofEupomatiaceae (2n = 20, partly from Papua New Guinea). Detailed studies on interphase nuclear structure, condensing behaviour of chromosomes, and fluorochrome and Giemsa C-banding patterns also includeHimantandraceae (Galbulimima) andAustrobaileyaceae. — Eupomatiaceae completely correspond withAnnonaceae karyologically, their base number 2n = 20 is interpreted to have evolved from 2n = 18 by ascending dysploidy from common ancestors.Eupomatia laurina andE. benettii differ in DNA and constitutive heterochromatin (hc) quantity; their evolution from high to low DNA content probably corresponds to general progressions inMagnoliidae. Austrobaileya has nuclei of the presumably primitive “Tetrameranthus type” which is closely related to that ofGalbulimima and several other primitive taxa inMagnoliidae. Karyomorphology and other characters support the maintainance of two main branches within theMagnoliidae, Laurales andMagnoliales, withAustrobaileya probably intermediate; theWinteraceae appear more remote.—InAnnonaceae the reestablishment ofAncana is underlined by its chromosome number (2n = 18) the unexpected and specialized disulcate pollen, and various morphological characters which point to a close alliance with the Australian endemic generaFitzalania andHaplostichanthus (also disulcate) and the American genus pairSapranthus/Desmopsis; they are united in the provisionalSapranthus tribe, with a more distant position toFissistigma s. str. (2n = 16). AustralianAnnonaceae exhibit a high generic and a low species diversity; they can be considered as an ± old and partly impoverished outpost of the family with phytogeographical relationships to Asia, Africa and America.—On the base of field observations three main types of floral development inAnnonaceae are proposed, the most elaborated one found in the fly pollinated genusPseuduvaria. The growth form change from shrubs to lianas during the ontogeny ofDesmos andMelodorum, the vegetative propagation of anAncana species and the ecological and evolutionary patterns of the taxa investigated are discussed.
The structure of the pollen of 42 species of Pseuduvaria (Annonaceae) is described. The pollen is consistently inaperturate, isopolar and radially symmetrical. Four basic patterns of exine sculpturing are identified: rugulate, verrucate, scabrate and psilate. The exine stratification of one representative species, P. macrocarpa, is shown to be entirely ectexinal. The ectexine consists of a discontinuous outer tectal layer, a columellar infratectal layer, and an inner lamellar foliated foot layer; the intine is very thin and fibrillar. The pollen is invariably released as acalymmate tetrads, in which the tectum is absent from the proximal walls. The individual pollen grains within the tetrads are connected by crosswall cohesion, involving both exine and intine; this form of cohesion has not hitherto been reported in the Annonaceae. In addition, pollen grains of neighbouring tetrads are connected in two different ways, viz. short exine connections and non-sporopollenin pollen-connecting threads. Neither of these cohesion mechanisms has previously been reported for the genus. The function of the various forms of cohesion between pollen grains and tetrads in Pseuduvaria is discussed as a mechanism to enhance the efficiency of pollination by enabling the fertilization of multiple ovules following a single pollinator visit. © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 143, 69−78.
Intracellular inclusions in the pedicel and calyx-tube tissues of Chamelaucium uncinatum Schauer (Myrtaceae) flowers are irregular in shape. They were shown, by polarised light and scanning electron microscopy, to be birefringent 8.9–29.5 μm druse (i.e. aggregate) crystals. Energy-dispersive X-ray spectroscopy showed that these crystals were predominantly composed of calcium. Histochemical and acid-solubility tests indicated that the crystals were calcium oxalate. Raman microprobe spectroscopy was used to confirm this chemical identity. The calcium oxalate crystals were located in xylem-vessel lumens and also in parenchyma cells adjacent to vascular tissues. Thus, the crystals may function to regulate soluble calcium concentrations in C. uncinatum tissues near sites where calcium is unloaded from the xylem.
Recherches sur les Annonacées d'IndoChine. Anatomie foliare—Répartition géographique. Mémoires du Muséum d
JOVET-AST, S. 1942. Recherches sur les Annonacées d'IndoChine. Anatomie foliare—Répartition géographique. Mémoires du Muséum d'Histoire Naturelle 16: 125–308.
Anonaceae. Pp. 23–29 in Die natürlichen Pflanzenfamilien
PRANTL, K. 1891. Anonaceae. Pp. 23–29 in Die natürlichen Pflanzenfamilien. Div. III, vol. 2, ed. A. Engler, & K. Prantl. Leipzig: Wilhelm Engelmann.