Botanical Journal of the Linnean Society (1994), 115: 165-195. With 24 figures
Pollen presenters in the flowering plants-form
and function
P. G. LADD
School of Biological and Environmental Sciences, Murdoch University, Murdoch 6150,
Western Australia
Received July 1993, accepted for publication April 1994
Pollen presenters are specific floral structures, other than anthers, from which pollen is distributed
for cross fertilization between flowers. They occur in only five families of monocotyledons and 20
families of the dicotyledons. Presenters in 15 families are described here. In the largest plant family
(Asteraceae) all taxa have pollen presenters, while in others (e.g. Myrtaceae) they occur in only
some species in a few genera. Most presenters are associated with the gynoecium and there is a wide
range of forms involving hairs or outgrowths of the stylar tissue. Despite the placement of self pollen
close to the stigma most taxa are outcrossing and avoid self fertilization by protandry, with the
stigma being covered at an thesis, or by precise placement of pollen so that is does not contact the
stigma. Likely selective advantages in the development of pollen presenters include greater accuracy
in pollen transfer than in the normal anther to stigma movement and avoidance of interference
between male and female organs in the flower. In some groups there is enhanced ability for female
choice because effective pollen delivery enables a choice from among many pollen grains, while in
others pollen presenters enhance male reproductive success. Study of the pollination biology of
plants requires a knowledge of which plants have pollen presenters and a full understanding of the
structures in the flower which are associated with the pollen presentation action.
ADDITIONAL KEY WORDS:-floral morphology - gynoecium -pollination biology.
CONTENTS
Introduction .
Methods .
Pollen presenter morphology
General form and action
Morphology in families
Discussion
Acknowledgements
References
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INTRODUCTION
The study of floral morphology has one of the longest histories in scientific
botany. The evolutionarily conservative nature of the flower which underpins
the classification system of angiosperms is in contrast to the ecological role of the
flower in reproduction. Since the pioneering work of Sprengel and Darwin the
study of the pollination biology of flowering plants has undergone a vast
expansion. In part this is a result of the fascination in the diversity of interaction
in the living ·world. Perhaps more importantly, this field is the first step in
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©
1994 The Linnean Society of London
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P. G. LADD
understanding the complexity involved in the survival and increase of plant
species. The factors affecting the efficiency of pollen transfer are likely to be some
of the more important selective factors in the evolution of floral structure.
In the majority of outbreeding plants the pollen grains are transferred from
the androecium of one flower directly to the gynoecium of another flower by
biotic or abiotic means to accomplish pollination. This is followed by fertilization
if the pollen is compatible. There is a great deal of complexity involved in the
forms of the floral sex organs and the positioning of these in the flower. There is
also great diversity in the means of transfer. Lloyd & Webb (1986) and Webb &
Lloyd ( 1986) have extensively reviewed the details associated with pollen
transfer. They have noted that some of the more important selective pressures in
the evolution of floral form have been the trade-offs necessary between the need
to transfer pollen accurately between male and female parts of different flowers
and the need to avoid interference between the androecium and gynoecium
while doing this. There has been considerable discussion of the utility of male
function in contrast to female function in relation to plant nutrition and mate
choice (e.g. Walker & Whelan, 1991). Efficiency of pollen transfer is generally
associated with male fitness so anything that increases transfer efficiency will
increase male fitness (Stephenson & Bertin, 1983). However pollen removal and
pollen receipt are different processes. Paternal fitness will be associated with
pollen dispersal and female fitness with pollen receipt (Lloyd & Yates, 1982).
One of the most efficient ways of avoiding interference between male and
female organs and seemingly increasing pollen transfer efficiency is found in a
few families offlowering plants, where it seems to have evolved independently in
different lineages. In these plants there is an intermediate step in the pollen
transfer process, called by SO!fie, secondary pollen presentation (Faegri & van
der Pijl, 1966). The pollen is initially shed from the anthers (very precisely) onto
a separate part of the same flower from where it may be picked up by the
pollinating agent for transfer to the stigma of another flower. The structure onto
which the pollen is deposited may be called a pollen presenter. This term seems
first to have been coined by Guthrie & Salter ( 1950) in relation to the
Proteaceae, but it can also be applied to structures in a number of other families,
as has been done recently in Wahlenbergia (Smith, 1992). Study and discussion of
pollen-presenting structures has occurred for some considerable time (Brown,
1818; Bentham, 1869; Carolin, 1960) with particular emphasis on the
Campanulales(Asterales groups, as they have been variously constituted over
time. Many authors do not apply a particular name to the structure involved in
secondary pollen presentation but a number of names have been suggested.
Brown used the term indusium (literally, a woman's undergarment) for the hoop
petticoat-shaped structure in the Goodeniaceae, while Carolin coined the term
pseudo-indusium to be used for the style-stigma-anther-tube apparatus of the
Lobeliaceae. However, these led to confusion with pteridophyte terminology.
Bremekamp studied the Rubiaceae and used the phrase 'ixoroid pollination
mechanism' (Verdcourt, 1958), and the terms 'receptaculum pollinis' and
'pollenbecher' (Bremekamp, 1966) for the structure involved in the intermediate
step of pollen transfer. Bremekamp also applied these last two terms to the
indusium of the Goodeniaceae and suggested that a receptaculum pollinis was
lacking in the Compositae despite the fact that secondary pollen presentation is
characteristic of this family.
POLLEN PRESENTERS
167
The term 'pollen presenter' is an unambiguous term for all structures
associated with secondary pollen presentation, and can be defined as a special
modification of part of the flower, other than the anthers, which makes pollen
available to be passed on to another flower, by either biotic or abiotic agents.
In certain cases secondary pollen presentation has been reported in families in
which pollen presenters are not present. For example Brantjes ( 1983) reported
secondary presentation in a number of families including the Stylidiaceae.
Flowers in this family do not have a pollen presenter as, although the anthers are
fused with the style, the pollen is shed directly from the anthers to a pollinator,
albeit in a rather unusual way. In Santalum acuminatum, Sedgley ( 1982) suggested
that pollen is distributed from hairs associated with the anthers and at the
junction of the ovary and perianth, while in the Commelinaceae pollen falls onto
hairs on the stamina! filaments (Faden, 1992). However these hairs do not
constitute pollen presenters as described in this paper because the anthers remain
the primary source of pollen in these taxa and placement of the pollen is not a
positive action, but occurs accidentally.
There is frequently a lack of precision in discussing parts of the gynoecium in
plants with pollen presenters. This is exemplified in a paper on the breeding
system of Cephalanthus occidentalis where the term stigma is used loosely to include
the pollen presenter and the receptive tissue of the true stigma (lmbert &
Richards, 1993). It would have been easier to understand the detail of this paper
if the terms pollen presenter and stigma had been used.
Description of secondary pollen presentation has been sporadic until recently.
Increased interest in the last few years culminated in the appearance of three
reviews shortly after this paper was submitted to the journal. These reviews
adopted somewhat different approaches, although unavoidably there were also
parallels in some aspects of the way the material was presented. This present
review is an extension of the geographically restricted study presented by Ladd
& Donaldson (1993) of taxa in the Southern African flora and advocates the
classification of pollen presenters used in that study. Howell et al. (1993)
presented mainly a literature review with detailed coverage of some groups and
recognized secondary pollen presentation in 16 families. They described nine
different types of presenter, of which 'enveloping bloom presenters' and
'androecial presenter' are not supported here as systematic pollen presenters,
although the structures, may be incidentally involved in dissemination of pollen.
Yeo ( 1993) presented an extensive study which described secondary pollen
presentation in 25 families. The study included detailed descriptions of structures
in particular species to illustrate the diversity of pollen presenters, but has less
coverage of some groups, particularly those found mainly in the southern
hemisphere. The presenters are summarized as three main forms based on those
devised by Westerkamp (1989)-Pollenhaufen (pollen heap), Nudelspritze
(noodle-squeezer) and Pseudo-Staubblatt (pseudostamen).
This present study gives details of the form and mode of action of pollen
presenters from families where, in most cases, the majority of taxa exhibit
secondary pollen presentation.
METHODS
The most reliable way to determine the presence of a functional pollen
presenter is to examine fresh material, preferably newly open flowers and mature
168
P. G. LADD
buds, as the pollen must be placed on the presenter before the flower opens. In
some genera in which pollen presenters occur, in particular species the structure
may not be functional. This is difficult to confirm from dried material. In this
survey, wherever possible fresh material has been examined. However this was
not always possible so some material has been examined from herbarium
specimens and some information has been gleaned from the literature.
POLLEN PRESENTER MORPHOLOGY
General form and action
Pollen presenters can be classified into two functional types on the basis of how
pollen is loaded onto the presenter:
(1) Active.
(2) Passive.
The active type occurs in the families Lobeliaceae, Goodeniaceae, Brunoniaceae,
Calyceraceae and Asteraceae, while the other families described here, plus one
genus (Cyphia) in the Lobeliaceae, have the passive type (see Table 1 for
summary).
In all the active types the pollen presenter is a modification of the style. A
piston action occurs where the growth of the style pushes the pollen presenter
past the anthers causing the pollen to be collected and then extruded for
presentation. In Lobeliaceae and some Asteraceae (e.g. Centaurea) probing by a
pollinator further activates the piston by differential movement between the style
and anther tube to express pollen onto the animal. In the Goodeniaceae and
Brunoniaceae the pollen is packed into the cup-shaped presenter and is
subsequently removed either by vibration by the pollinator or extension of the
stigma from the tip of the style out of the cup.
With the exception of Epacridaceae and some Fabaceae, in all families which
have passive pollen presenters, pollen is appressed to the modified part of the
style by the anthers while still in bud. In some cases adhesion is aided by the
presence of hairs on the presenter, or the hairs may constitute the presenter
(Myrtaceae) or by sticky material on the pollen or by lipidic secretion from the
anthers (M yrtaceae). In these types the presenter is either displayed by collapse
of the perianth (and anthers) from around it (Proteaceae, Rubiaceae,
Cannaceae), by elongation of the style (Campanulaceae, Rubiaceae,
Meliaceae), change in the position of the style (Proteaceae) or by active foraging
by a pollinator (Polygalaceae, Fabaceae, Marantaceae, Cyphia). In the single
species of Epacridaceae with a pollen presenter, pollen is deposited on hairs on
the petals while in a number of Fabaceae the pollen is packed onto the keel petal
and extruded from the acumen of the keel.
Self pollination is avoided either by the flowers being dichogamous, usually
strongly protandrous (except some taxa in the Lactuceae which morphologically
appear to be protogynous) with the stigmas becoming apparent some time after
the pollen is shed from the anthers, or 'microherkogamous' where pollen is
deposited slightly away from the stigma. A number of species of Polygala and
some Lobeliaceae are exceptions, as they seem to be autogamous.
The most general form of the pollen presenter is where the apical stigma has
been overgrown by stylar tissue to various degrees, so that it is immersed in
POLLEN PRESENTERS
169
nonreceptive tissue when the flower reaches anthesis. This is demonstrated
particularly well in the micrographs of Keetia zanzibarica and Vangueria infausta
(Rubiaceae) pollen presenters in Igersheim (1993a). There may also be various
embellishments of the upper part of the style in the form of hairs or cup-shaped
outgrowths (Goodeniaceae) which enhance the pollen presentation mechanism.
This is displayed well in a number of genera in the Asteraceae. In these the apex
of the style is extended beyond the stigmatic region into an apiculate tip covered
with antrorse, pointed hairs which remove the pollen from the anthers as the
style elongates. After a period during which self pollen is removed the receptive
stigmatic tissue is either exposed by recurving of the style arms (Campanulaceae,
Lobeliaceae, Goodeniaceae, Brunoniaceae, Asteraceae), grows through the style
end (e.g. Grevillea) or remains within the style so that pollen must be introduced
into, or at least near to, a pollination chamber before pollination can occur (e.g.
many Proteaceae).
Morphology in families
Epacridaceae
Pollen presentation in Acrotriche serrulata, the sole member of the E pacridaceae
to show this trait, has been studied in some detail (McConchie et al., 1986). The
flowers are small (approx. 4-5 mm across), pale green in colour, are borne
within the canopy of the plant, have a strong odour and produce copious nectar.
The pollen is deposited from the anthers onto petal hairs (called 'combs' by
McConchie et al., 1986), along with nectar and pollenkitt, as the petals recurve
during opening of the flower. Petal hairs are common in the Epacridaceae as is
copious nectar production in some species. However only A. serrulata combines
the two traits to enable secondary pollen presentation. It is considered that the
pollinators of the species are small marsupials.
Fabaceae
There are two different methods of presentation in the Fabaceae. In the more
simple case pollen is deposited onto the style below the stigma, either onto hairs
(Lavin & Delgado, 1990) or a platform formed by a broadened section of the
style (e.g. Sphaerolobium macrantherum). The anthers and style are contained within
the keel petal and visits by suitable pollinators depress this petal displaying the
style and stigma. Pollen is transferred from the presenter hairs onto the
pollinator while other pollen may be deposited from the animal onto the stigma.
Rarely the presenter may be reloaded when the style returns into the keel but in
most taxa the anthers shed all pollen simultaneously onto the presenter before
anthesis. Lavin & Delgado point out that pollen presenter hairs on the style need
to be distinguished from other sorts of hairs. Pollen presenter hairs occur on the
adaxial side of the style and around the base of the stigma and may form a tuft
on the abaxial side (e.g. Vicia) and are stiffer than hairs that may extend up the
style from the ovary.
In the second type of presenter the pollen is deposited on the inside anterior
end of the keel petal while the upper edges of the keel are strongly appressed for
much of their length, except near the apex at the acumen. Pollen is squeezed out
of the acumen (Fig. 1) when a pollinator manipulates the flower. There are two
slightly different mechanisms by which this occurs. In some taxa (e.g. Lupinus)
170
P. G. LADD
POLLE!\" PRESENTERS
171
the anther filaments swell at anthesis forming the piston which forces the pollen
out of the acumen (Weberling, 1989). In the other case the anthers are in two
whorls with the shorter whorl fitting below the longer whorl as they lie in the
keel. The upper anthers dehisce first into the apex of the keel petal (Fig. 2) while
the undehisced second whorl acts as a piston to force the pollen out of the
acumen when a pollinator manipulates the keel (also described briefly by Kalin
Arroyo, 1981). The presence of dimorphic anther whorls is a common feature in
the Fabaceae. However not all taxa with this morphology have the pollen
presentation mechanism. The mechanism occurs commonly in the Liparieae and
in some Crotalarieae and Gen1steae but species have to be examined
individually. In three species of Gompholobium (Tribe: Mirbelieae) examined
pump-type pollen presentation occurs in G. polymorphum but not in G. tomentosum
or G. knightianum.
The explosive pollination mechanism of some Fabaceae (e.g. Medicago) has
been described as secondary pollen presentation (Brantjes & van der Pijl, 1980).
However this process does not entail placement of pollen on any secondary
structure in the flower and is best categorized as pollen release rather than
secondary presentation (also supported by Yeo, 1993). The explosive tripping
mechanisms are considered most advanced by Kalin Arroyo ( 1981). The
observation seems to be based on the association between nectar reward and
explosive pollen release, but for complex traits such as are involved in the
Fabaceae much more work is needed on the degree of advancement of the
various methods of pollen transfer.
Proteaceae
The Proteaceae has the greatest diversity of pollen presenter morphology in
the flowering plants. All except the Sphalmioideae of the currently recognized
five subfamilies contain genera with pollen presenters Uohnson & Briggs, 1975).
Only 15 of the 75 genera in the family lack presenters. These include Sphalmium,
genera in the Persoonieae, Franklandia and all Conospermeae (except Petrophile
and lsopogon). The presenter is a modification of the upper part of the style. It is
either an elaboration in terms of swelling or provision of hairs, or an overgrowth
of the stigma by sterile tissue so that the stigma either remains internal within the
presenter and is accessed by a small aperture or it grows•out at some time after
anthesis. Within some of the larger genera of the family such as Protea, Banksia,
Dryandra, Grevillea and Hakea there may be a range of forms from simple to quite
elaborate. It has been suggested (Yeo, 1993) that the presenters in some
Proteaceae are sticky. This has not been found in this study although the pollen
may be variably sticky or adherent.
The presenters are displayed by collapse of the perianth (and anthers if they
are not fused to the perianth) at anthesis. In a number of taxa (e.g. Banksia,
Figures 1-6. Scale bars = I mm, except where specified. Fig. I. Crotalaria agatijlora: pollen extruded
from the acumen of the keel petal (k); Fig. 2. Gompholobium polymorphum: pollen packed into the tip of
the keel petal of a mature bud; Fig. 3. Leucospermum oleijolium: three ages of pollen presenters,
youngest with pollen to the right, oldest with gaping stigmatic slit on the left; Fig. 4. Protea cynaroides:
pollen appressed to the presenter, separated from the stigmatic slit which is at the tip; Fig. 5.
Dryandra bipinnatifida: upper part of pollen presenter with pollen covering all except the tip, apical
stigmatic slit (arrow) gaping slightly (scale bar = 0.5 mm); Fig. 6. Spatalla racemosa: pollen covering
black presenter, pilose tepa! below presenter.
172
P. G. LADD
Dryandra, Leucospermum) the style comes under tension through extension growth,
forcing initial release from the lower part of the perianth, while the presenter
remains enclosed in the still fused perianth lobes. At complete anthesis the tepal
lobes release the presenter which springs outward away from the floral axis. In
these types the combination of a dense inflorescence and projecting presenters
produces the effect of brush blossoms with presenters, rather than anthers,
producing the display and providing the pollen.
The simplest presenter forms consist of a slightly swollen end of the style with a
small apical slit giving access to the stigma. They occur in members offour of the
five subfamilies, specifically in a number of rainforest genera in north eastern
Australia (e.g. Carnarvonia), in some South African Proteeae such as Faurea and
Diastella, in the only South African grevillioid Brabejum, in the Tasmanian
endemic Bellendena and in the New Zealand Knightia among others. This form or
a slightly elongated version also occurs in the two dioecious genera from South
Africa, viz. Aulax and Leucadendron. These two taxa, despite having unisexual
flowers, have retained the pollen presenter in the male flower as a sterile relic of
its ancestral hermaphrodite origin. Of the 78 species of Leucadendron listed in
Williams ( 1972) 64 have a functional pollen presenter. In some of the species
where the presenter is non-functional the flowers snap open to scatter the pollen
(e.g. L. coniferum, L. laureolum) and these are presumably wind pollinated, or the
vestigial presenter does not reach the anthers (e.g. L. tradouwense, L. tinctum).
The simple form is elaborated by broadening of the base to form a conical
structure which occurs in Leucospermum (Fig. 3) and some Banksia, Grevillea and
Hakea species. The stigma may remain internal or grow out of the apex of the
cone as a papillate protrusion.
The third type arises by elongation of the simple form, often with the addition
of an apical swelling. In most Mimetes the presenter is a slightly grooved upper
section of the style with an apical slit giving access to the stigma; this also occurs
in many Banksia and Dryandra (Fig. 5) species. However in M. hottentoticus and
M. stokoei the apical slit is within the remarkably swollen top to the pollen
presenter. In Protea there are somewhat similar but not quite such elaborate
forms. One group of Protea has the number of functional anthers in the flower
reduced from four to three. In these species the presenter is a narrow platform for
deposition of the pollen on its adaxial side towards the end of the style (Fig. 4).
In some cases the sterile abaxial anther is appressed to the pollen presenter and
temporarily forms part of the platform. In these species the stigma is internal in
the top of the presenter and is accessible via a slit. This slit is opened by
particular action of pollinators as has been described by Ladd & Donaldson
(1993).
A fourth type of presenter is found in Xylomelum, Turrillia and Kermadecia. This
type is rather equidimensional with a barrel to club-shaped end to the style. The
most distinctive feature is the dense covering of hairs on the presenter. This
character is found in only a few of the Proteaceae. In Xylomelum the stigma is a
broad capitate top to the presenter in the bisexual flowers. The presenter also
occurs in male flowers, but is a fusiform shape and has no stigma.
The fifth type is most frequent in the Grevillioideae, particularly Stenocarpus
and Grevillea, to a somewhat lesser extent in Hakea, in a number of north-east
Australian rainforest genera, and in the South American Oreocallis and the South
African Spatalla (Fig. 6). The presenter is a broad, slightly conical disc-shaped
POLLEN PRESENTERS
173
structure at the end of the style. The style is normally recurved so that the disc
which carries the pollen faces towards the base of the flower. The stigma in this
type is generally internal and grows out at some stage after anthesis as a papillate
irruption in the centre of the presenter (Fig. 7). In Telopea the stigma is a hole
lined with papillae in the centre of the presenter, while in Stenocarpus, Strangea
and Lomatia there is a unique formation consisting of an accumulation of spirally
ornamented cells on the stigma which forms a protective covering preventing self
pollen from contacting the stigma. The spiral cells are removed with the pollen
to expose the receptive stigma.
The sixth type includes the most elaborate forms and is found in Isopogon and
Petrophile (Fig. 8), two Australian genera in the Proteoideae. The simplest form is
a fusiform swelling at the end of the style supporting sparse or dense hairs. More
elaborate types have constrictions in the swollen end or may be topped by an
unswollen portion which is densely hairy. Pollen is appressed to all or part of the
presenter (often the tip is left free) which is then displayed at the end of a thin
style rather like the lure of an angler fish. The swellings have been termed 'insect
landing knobs' (Lamont, 1985) but this is a misleading term as pollinators of
taxa with these structures tend to hover to collect pollen from the presenter and
there is no nectar produced. The stigma is either a small apical depression or is
initiaHy internal and grows out of the apex as a small mass of papillae.
The origin of presenters in the family is unclear. The ancestral
'Protoproteaceae' were assumed to have lacked presenters Oohnson & Briggs,
1975). However four of the five currently recognized subfamilies contain at least
one taxon which has a presenter. All members of the subfamily Grevillioideae
have presenters and the least elaborate types of presenters occur in a number of
the rainforest taxa. All the South African Proteoideae have presenters (some of
very simple form), but a number of Australian taxa in the subfamily lack them
and these are often the more specialized sclerophyllous forms. Unfortunately
there are few clues as to the ancestors of the Proteaceae and Johnson & Briggs
( 197 5) suggest the group is a "very early offshoot from a primitive apocarpous
line of the angiosperm complex". So there are no clues to the origin of the
presenter in ancestors to the family. From the widespread distribution of pollen
presenters in the family they seem to have evolved very early and are positively
recorded in the Eocene fossil Musgraveinanthus (Christophel, 1984) which seems
virtually identical to the extant Musgravea and Austromuellera from north eastern
Australia and is apparently the oldest recorded pollen presenter.
Myrtaceae
The Myrtaceae is a family characterized by brush blossoms where anthers act
as the attractive part of the flower. However in five genera in the Chamelaucium
suballiance bracts or petals and/or sepals have assumed the attractant function
and pollen is presented on a modified part of the style. The pollen presenter of
C. uncinatum is described in some detail by Slater & Beardsell ( 1991) and they
noted that presenters occur in Chamelaucium, Darwinia, Homoranthus and
Actinodium.
The presenter is composed of hairs or papillae which surround the upper part
of the style below the apical stigma (Figs 11, 12). Papillae occur in Actinodium
cunninghamii, while in the other genera there are hairs which may be relatively
short and simple or longer and branched, as in the most elaborate forms in a
Figures 7~12. Scale bars = I mm, except where specified. Fig. 7. Grevillea cultivar 'Honey gem':
three ages of pollen presenter, youngest to the right (pollen removed) and oldest with protruding
stigmatic papillae on left; Fig. 8. Petrophile rigida: lower presenter with pollen (except at the apex),
upper presenter older with pollen removed and stigmatic papillae at apex; Figs 9, 10. Polygala
myrtijolia. Fig. 9; Pollen covering pollen presenter in both the apical depression and in the crook
between presenter and style; Fig. 10; Presenter from young bud showing stigma; Fig. II. Darwinia
vestita: pollen presenter comprised of hyaline hairs with bulbous ends, undehisced anther indicated
by arrow (scale bar = 0.5 mm); Fig. 12. Verticordia penicillaris: pollen presenter of simple elongate
hairs, five globules of pollen in viscous fluid surround the central, still immature stigma (s).
POLLEN PRESENTERS
175
number of Verticordia species. Presenters occur in all species of Homoranthus,
Actinodium and Darwinia, they are found in most species of Chamelaucium and in
69% of Verticordia species (figure derived from George, 1991).
Pollen is deposited on the presenter in a liquid suspension before anthesis
(Fig. 12). The composition of the liquid is not clear but is identified as mainly
lipid in C. uncinatum (Slater & Beardsell, 1991) and comes either from a gland on
the apex of each anther or from within the anther loculus. The pollen suspension
may coat the stigma as well as the hairs, but the breeding system seems to be
protandrous. The study of C. uncinatum showed that the stigma was not initially
receptive until the pollen presenter hairs had reflexed to take the pollen away
from the stigma. Esterase staining of the stigma indicating receptivity correlated
with the swelling of the stigmatic papillae. In other species (e.g. C. erythrochlorum)
the hairs close over the stigma with time and trap unremoved pollen on the
stigmatic surface. In all species examined in this present survey, stigmas were
initially fairly smooth but became papillate with age. Although secondary pollen
presentation is suggested to occur from the style in some eucalypts (Howell et al.,
1993) this seems to be more a matter of incidental pollen deposition rather than
specific secondary pollen presentation. The anthers still remain the primary site
from which pollen is dispersed.
Pollen presentation in this group seems to be an advanced character in the
family. The genera are closely related (George, 1991) with the next most closely
related group being the Baeckea suballiance Uohnson & Briggs, 1981) in which
taxa do not have presenters. To some extent the pollen presenters seem to be a
reversion to the, presumably ancestral, brush blossom form with the presenters,
rather than anthers being long exserted. In many species of Darwinia, the flowers
are massed into heads producing a forest of projecting presenters at an thesis.
Polygalaceae
Pollen presenters are confirmed in species from four genera, namely Polygala,
Muraltia, Securidaca and Comesperma, but not all species in each genus have a
presenter. From illustrations in Eriksen (1993), Monnina also has a pollen
presenter similar to forms in Comesperma. The form of presenters in Polygala has
been studied quite extensively and has been compared with the various pollen
transfer mechanisms in the Fabaceae (Brantjes & van der Pijl, 1980). While
some of the comparisons are valid some seem not to be, as has been pointed out
in the section on Fabaceae above.
The pollen presenter in Polygala varies from a shield or spoon-shaped structure
anterior to the stigma to a crook-like bending of the style or a ring or basket of
hairs behind the stigma (Figs 9, 10). Pollen is placed by the anthers onto the
presenter and transferred to a pollinator when the presenter is exposed by
depression of the keel petal or when a pollinator probes across the presenter in
the species where the keel is immobile. In two sympatric species with basket-type
pollen presenters it was shown that precise differential placement of pollen from
the presenter onto a pollinator ensured reproductive isolation between the
species (Brantjes, 1982). In a number of South African species the crook-type
presenter is common. In these the pollen is deposited in a hollow near the apex of
the crook and also in the elbow of the crook, thus surrounding the stigma. It is
difficult to see how these species are not self-pollinated and a similar concern was
expressed about some Indian species (Venkatesh, 1956).
176
P. G. LADD
In most Comesperma the presenter is similar to one of the types in Polygala where
there is a platform or shield anterior to the stigma. The platform may be edged
by short hairs. In C. calymega the presenter is more similar to the hair-covered
extension of the style seen in Muraltia.
In Muraltia, functional presenters appear to occur only in some species of the
subgenus Psiloclada. In this survey only M. pauciflora and M. oxysepala could be
confirmed with functional presenters which consist of a concentration ofhairs on
a prolongation of the style anterior from the stigma.
In all species the stigma is an exposed papillate knob. In the Polygalaceae the
ancestral condition seems to be of two fused carpels with two stigmas (still found
in the Indian P. persicariaefolia, Venkatesh, 1956). The pollen presenter has
initially been derived from sterilization and modification of one of the ancestral
stigmas. In some taxa the presenter has.been lost altogether and there may be no
secondary pollen presentation, e.g. Muraltia subgenus Muraltia. However in
species such as P. vauthieri secondary pollen presentation has arisen again by
development of hairs to hold the pollen posterior from the stigma. The
classification of this type of pollen presenter as "terminal stylar presenters with
passive pollen placement and subterminal stigmas" (Howell et al, 1993) is
somewhat misleading. In P. vauthieri, the stigma is terminal and the origin of the
pollen presenter in this family means that in reality both the pollen presenter
and stigma are terminal.
Meliaceae
Trichilia, Ekebergia and Turraea have been confirmed to have pollen presenters
in this family. In the latter two genera the presenter is barrel-shaped and
smooth, while in Trichilia it is also barrel-shaped but covered in hairs. Pollen is
placed onto the sides of the presenter. In Turraea and Ekebergia there is a large
apical capitate stigma (Fig. 13) exposed at anthesis while in Trichilia the stigma
appears to be in a depression on top of the presenter.
In this family the pollen presenter seems to be an advanced character
associated with development of a stamina! tube.
Campanulaceae
There has been a considerable number of studies of pollen presenters in the
Campanulaceae from the time of the earliest botanists. Shetler ( 1979) reviewed
the earlier literature on the studies of Campanula and Lloyd & Yates ( 1982)
produced a careful study of Wahlenbergia albomarginata.
The pollen presenter is fairly uniform in most genera. It can be envisaged as
being formed by growth of stylar tissue over the stigmas so that they are covered
at an thesis. Extension of the stylar tissue has been associated with elongation of
the stigmas so that at some time after anthesis the presenter arms recurve to
expose the stigmas on their inside face. A unique feature of the Campanulaceae
presenters is the presence of unicellular, often retractile hairs which initially
support the pollen before it is removed. The hairs on the presenter in bud are
hyaline and turgid and pollen is shed on and among them before anthesis. It has
been shown (Lloyd & Yates, 1982) that rather than withering with age and
desiccation the hairs of W. albomarginata retract into the presenter to free the
pollen for removal and this has also been proposed as occurring in Campanula
species (Shetler, 1989, Nyman, 1993) and is well documented in Petromarula
POLLEN PRESENTERS
177
pinnata (Igersheim, 1993b). Nyman (l992a) however observed that in cultivated
annual species of Campanula the hairs do not retract.
The presenter may remain inside the campanulate corolla, as in most
Campanula and Wahlenbergia species or be carried beyond the corolla by
elongation of the style (e.g. Phyteuma, Petromarula pinnata, some Prismatocarpus
species). It has been reported that the hairs perform a 'sweeping action' (Shetler,
1979, Richardson & Stephenson, 1989) to remove pollen from the anthers but in
most of the species studied in this survey the pollen was deposited passively on
the presenter before elongation commenced. This is also the case in Australian
Wahlenbergia species (Smith, 1992) and in Petromarula pinnata (Igersheim, l993b).
In Phyteuma comosum there may be a partial sweeping action. In this species there
are antrorse hairs towards the apex of the presenter while lower hairs are longer
and produced at right angles to the presenter forming an overall narrow cone of
hairs which picks up pollen from the elongate anthers in this species. However
most pollen would be deposited between the presenter hairs before stylar
elongation commenced. In Phyteuma orbiculare the pollen is deposited on the
presenter before elongation of the style or presenter and becomes available to
pollinators while the presenter is still contained in the flower (Carolin, 1960).
There seem to be a number of nuances in pollen presentation in the
Campanulaceae.
In all taxa that have been examined, except Siphocodon debilis, the stigmas are
covered at anthesis. However there is variation in the time they remain
concealed. In Wahlenbergia capensis the peltate, lobed stigma is exposed almost
immediately after anthesis, forming an umbrella-shaped structure with the
pollen borne underneath the lobes (Figs 14, 15). The presenter of Phyteuma
comosum extends through the apex of the adherent corolla lobes and may have
exposed stigmatic surfaces while pollen is still adhering lower down on the
presenter. In C. afra the male phase may last up to 17 days before the stigmas are
exposed. However this time can be shortened by manipulation of the hairs on the
presenter (Nyman, 1992a). In C. persicifolia the stigmas are not exposed unless
the pollen is removed (Nyman, l992b). There is thus, in some species at least, a
feedback system which delays stigma exposure until pollen is removed. Campanula
afra flowers seem to have a very long life while other taxa such as Prismatocarpus
and Lighifootia have flowers open for only a day or two. It may be that the
control over stigma exposure only operates in the species with long lived
flowers.
Again the terminology ("subterminal stylar presenters") used by Howell et al.
(1993) for presenters in this family is unsuitable as in many species, e.g.
Petromarula pinnata, Lighifootia and Roella species, pollen is deposited over the apex
of the pollen presenter which subsequently splits and recurves to expose the
stigmas.
Siphocodon debilis is exceptional in the family in that the stigma is fully exposed
at an thesis and the pollen presenter is a zone of hairs on the style about halfway
between the stigma and ovary (thus fitting category 7 of Howell et al., 1993).
The only other species in the genus (S. spartioides) has a typical Campanulaceae
presenter.
In evolutionary terms the presenter has been derived from some ancestor to
the Campanulaceae. The reversion to an exposed stigma in S. debilis appears to
be an advancement achieved through union of the presenter arms and exertion
178
P. G. LADD
POLLEN PRESENTERS
179
of the stigma from the apex of the presenter in an analogous way to the situation
found in Lechenaultia (see below).
Lobeliaceae
Pollen presentation in this family is uniform except in Cyphia. Typically the
presenter comprises a ring ofhairs near the tip of the style above which there is a
small amount of sterile tissue covering the stigmas. Small tufts of hairs may also
be present at the tip of the presenter (Fig. 16). The hairs are unlike those found
in the Campanulaceae, being much more elongate and robust. They may be
rounded or acute at the tip and in some species are corrugated.
The presenter and style pass through the stamina! tube (Fig. 17) and the
presenter functions by elongation of the style pushing pollen dehisced from the
anthers out the end of the tube. The anterior end of the tube is usually invested
with hairs or scales which act to control pollen release. In Isotoma petraea the
process has been described in some detail (Brantjes, 1983) and most taxa with
the anther tube configuration have a somewhat similar mechanism. In Lobelia
jasionoides an almost identical configuration of hairs/scales to that in I. petraea is
found resulting in similar pollen release. In Monopsis the presenter is more
elongated and beak-like than in other members of the family.
The term pseudo-indusium has been proposed for the "connate anthers, closed
stigmatic branches and stylar hairs" (Carolin, 1960) found in 'Lobelioideae'
flowers. The term was introduced to contrast the pollen presentation mechanism
with that found in the Goodeniaceae but introduces confusing elements as there
is no structure morphologically similar to the Goodeniaceae 'indusium' in the
Lobelioideae. The term should be rejected and certainly does not seem to have
been utilized recently.
The duration of the male phase in L. cardinalis has been shown to be
influenced by the time it takes to eliminate pollen from the stamina! tube (Devlin
& Stephenson, 1984), and in this trait there is some similarity with members of
the Campanulaceae.
In general the flowers are protandrous. Elongation of the style brings the
presenter to the end of the stamina! tube where the lobes of the presenter reflex
to expose the papillate stigmas.
The presenter and configuration of the flower in Cyphia is very different from
that found in other genera in the family (Fig. 18). There is no anther tube, the
style does not elongate and the presenter is a bulbous swelling at the end of the
style covering the stigma. Short hairs may be present on the presenter. Pollen
from the anthers is passively shed onto the presenter and remains within the
throat of the corolla. The stigma may protrude through the end of the presenter
Figures 13-18. Scale bars = I mm, except where specified. Fig. 13. Turraea obtusifolia: pollen
adhering to the sides of the pollen presenter and also retained on the anthers (n), stigma exposed at
the top of the presenter (arrow); Figs 14, 15. Wahlenbergia capensis. Fig. 14; Dissected bud showing
turgid pollen presenter hairs surrounded by the undehisced anthers (n); Fig. 15; Mature presenter
with pollen (p) adhering under the spread arms, stigmatic tissue (s) is on top of the arms; Fig. 16.
Lobelia pinifolia: pollen presenter with apical corrugated hairs and a ring of smooth hairs forming the
base of the presenter (scale bar= 0.25 mm); Fig. 17. L. coronopifolia: dissected anther tube showing
the pollen presenter (arrow) at the base of the pollen (p) within the tube; Fig. 18. Gyphia triphylla:
young pollen presenter (right), intermediate with pollen (centre) and old presenter (left), the stigma
in the centre of the presenter (arrow) becomes more exposed with age.
180
P. G. LADD
or to the side below the apex of the presenter some time after an thesis, forming a
papillate mound or remain as a sticky depression in the middle of the presenter.
There has been some discussion of the position of Cyphia in the Lobelieaceae.
The presenter has been described as "an obsolete ciliate indusium" by Sander
(1894) in his treatment of the Campanulaceae. Thulin (1978) noted that "the
stylar structure has often been compared with, or considered homologous to, the
pollen-cup (indusium) of Goodeniaceae and a close affinity with the family has
often been implied", but he placed Cyphia as a marginal member of the
Lobeliaceae. Korvanda ( 1978) suggested that the genus may be a link between
the Campanulaceae and the rest of the Lobeliaceae. Lammers ( 1992) extensively
considered the position of the genus and its 'allied' taxa in the Campanulales and
recommended that they be included in a possibly unnatural family-the
Cyphiaceae because they did not fit well into either the Campanulaceae or
Lobeliaceae.
·
Lammers ( 1992) pointed out a number of critical attributes which need to be
studied and which may clarify the relationship between Cyphia and its allies.
Information on the production of iridoids in cyphoid groups is needed. Thulin
( 1978) quoting Dahlgren (in !itt.) said there were no iridoids in Cyphia while
Lammers lists no information on this point. Thulin described Cyphia as being
characterized by a style with no free stigma, but with a stigmatic cavity filled
with a slimy fluid. Lammers repeated this but also said that the Cyphiaceae taxa
have a bifid stigma. In the species examined in this survey only C. elata and
C. triphylla could be examined as fresh material. C. elata had a definite papillate
stigma (not bilobed) which protruded from the centre of the pollen presenter
some time after anthesis, while in C. triphylla the stigma was a moist circular,
slightly depressed area on the top of the presenter but there was no cavity in the
presenter. Lammers also suggested that Cyphia lacked a specialized mechanism
for protanderous pollen presentation. However the structure on top of the style
in Cyphia certainly functions as a passive pollen presenter, but it is also different
from the presenters in the Lobeliaceae and the Campanulaceae. In Carolin's
( 1960) careful considerations of the pollen presenters in the Campanulales,
Cyphia was not considered but there are certainly similarities with the
Goodeniaceae presenters, particularly those of the Dampiera type. While there
seem to be a number of superficial floral similarities between Cyphia and some
Goodeniaceae more work is needed on anatomical and chemical details, as
emphasized by Lammers ( 1992).
The pollen presenter in the Lobeliaceae is an ancestral character. However the
position of Cyphia is unclear. If Cyphia is a link with the Campanulaceae
(Korvanda, 1978) then the form of the presenter in other taxa is more advanced
than the form in Cyphia. There is the possibility that it is more advanced in Cyphia
as the display of stigmatic arms in the rest of the family is more similar to the
mechanism in Campanulaceae than to the emergence mechanism in Cyphia.
Goodeniaceae
All eleven genera in the family possess a pollen presenter. It is generally a cuplike outgrowth at the top of the style. The outgrowth begins to form in late bud
stage when the tissue around the apical stigmatic area starts to expand to form
the cup, with the stigmatic area as the floor (except in Lechenaultia where the
stigma is external to the cup).
The presenters are of the active type. Elongation of the style pushes the
POLLEN PRESENTERS
181
presenter past the anthers, collecting the pollen on the way and packing it into
the cup. As the style elongates the presenter turns through 90° so that the mouth
of the presenter faces the abaxial petals. This brings the presenter into a position
to contact pollinators probing the flower from the front. Pollen is released by
simply knocking the presenter or by growth of the stigma out of the cup. The
positioning of the presenter may be very similar to the positioning of the anther
tube in the Lobeliaceae and there seems to have been parallel development in
the general form of flowers in Lobeliajlsotoma and members of the Goodeniaceae.
There are .three main forms of presenter (after Carolin, 1960):
( l) The Lechenaultia type, which is found only in this genus. The structure is
a two-lipped sack with a fringe of hairs on the back of the upper lip. This form
differs from those in the other taxa in that the lower lip is weakly hinged and
drops open readily to release the pollen. The stigmatic area is a sticky band on
the upper lip, rather than being inside the cup, as in the. other taxa. (Fig. 20).
(2) The Dampiera type, which occurs in Dampiera and Anthotium. The
presenter is glabrous except for short stout hairs around the lip of the presenter.
The cup tends to be globular and may have a restricted top which firmly retains
the pollen or the pollen may be inefficiently loaded into the cup so it is borne on
the outside of the presenter. In A. rubijlorum, the cup remains horizontal and is
not turned downwards at maturity. The stigma in this type may expand to the
top of the cup but does not extend out of it and has less pronounced papillae
than in the Goodenia type. (Fig. 19.)
(3) The Goodenia type, which occurs in all other taxa in the family. The cup
is variably hairy on the outside as well as on the rim. At maturity it is usually
flattened but may be folded into a horshoe shape and in a small number of
Goodenia species is divided into two to four lobes. If the presenter is divided there
are partial cups. The stigma is papillate, generally two-lobed (up to four lobes in
taxa with a divided presenter) and grows out of the cup pushing the pollen out
as it expands.
The pollen presenters in the Goodeniaceae were compared with the pollen
presentation mechanisms in other families in the Campanulales (Carolin, 1960)
and it was concluded that the cup-shaped structure in the Goodeniaceae was not
related to the pollen presenters in the Campanulaceae or Lobeliaceae. The
pollen presenter in the Goodeniaceae is ancestral in the family although there is
variation between some of the genera. The Lechenaultia type would seem to be
the most derived type with a shift of the stigmatic surface from the end of the
style (inside the cup) to the upper lip of the presenter.
The presenter form in the Goodeniaceae and Brunoniaceae is classed as
"indusial stigmatic presenter" by Howell et al. ( 1993). By implication from the
table in that paper this is classed as a passive system, although in the text it is
said that "pollen is actively loaded into the open indusium before the flower
opens". The definition of the indusia) presenter is not consistent with all the
forms found in the two families. In Lechenaultia the stigma is considered to be
external to the presenter (indusium) and pollen is not loaded onto the stigma at
all as is stated for the "indusia) stigmatic presenter".
Brunoniaceae
Carolin et al. ( 1992) suggested that the monotypic Brunonia australis would be
better included in the Goodeniaceae than in its own family, as it has a close
relationship with the Lechenaultia-Anthotium-Dampiera group of the Goodeniaceae.
182
P. G. LADD
Figures 19-24. Scale bars = I mm. Fig. 19. Dampiera lavandulacea: longitidinal section of pollen
presenter from mature bud, pollen (p) and stigma (s) indicated; Fig. 20. Lechenaultia formosa:
dissected young bud showing anthers (n) arched over the mouth (arrow) of the pollen presenter (o)
about to shed pollen into the presenter; Fig. 21. Canna sp. cultivar: pollen (p) deposited on the
presenter (side of style), stigma indicated by arrow; Fig. 22. Calathea sp. cultivar: dissected young
bud with anther (n) pressed into the pollen presenter depression on the back of the stigma (s);
Fig. 23. Arctotis venusta: pollen (p) on pollen presenter, other presenters have lost their pollen;
Fig. 24. Picris sp: pollen (p) on the lower part of the pollen presenter with the stigmatic surfaces
(arrow) exposed simultaneously.
POLLEN PRESENTERS
183
However the pollen presenter is different from the types in the Goodeniaceae, as
was recognized by Carolin ( 1960).
The presenter is of the active type and has the same general cup-shaped
structure found in the Goodeniaceae. However it has hyaline, expanded
crescentic lobes, which lack hairs, forming the upper sides of the cup; the
presenter is well exserted from the flower and is not turned through 90°, all
features which do not occur in most species in the Goodeniaceae. As the
presenter is borne vertically the pollen is not tightly contained and is readily
dislodged from the cup. At maturity the bilobed, papillate stigma grows out of
the cup in the same way as occurs in the Goodenia type in the Goodeniaceae.
Rubiaceae
The Rubiaceae is a large and complex family. Three subfamilies were
recognized by Kupicha (1978) following Verdcourt (1958). However
Bremekamp (1966) disagreed with Verdcourt's arrangement and proposed nine
subfamilies, many of which contained few genera. Pollen presenters occur only in
some members of Verdcourt's subfamily Cinchonoideae while Bremekamp
( 1966) asserted that the trait is restricted to his subfamily Ixoroideae. However
Nauclea seems to have a pollen presenter and is not included in the Ixoroideae
while Alberta (A. magna definitely has a presenter) was excluded by Bremekamp
from his tribe Cremasporeae in the subfamily due to his belief that it lacked the
'ixoroid' pollination mechanism.
The presenter is either a smooth extension of the style over the back of the
stigmas or is a swelling at the top of the style enclosing the stigmas and may be
invested with hairs. Ladd & Donaldson ( 1993) recognized two basic forms but
subsequent examination of more material leads to definition of three types( I) The style tapers gradually to the tip with virtually no modification such as
hairs or swelling to show where pollen will be deposited. The presenter splits into
arms which recurve to display the stigmas (e.g. Ixora, Alberta).
(2) The presenter has an elongation fusiform shape, and may be smooth or
have short hairs. The stigmatic tissue expands out of grooves in the sides of the
presenter (e.g. Gardenia, Pavetta). ·
(3) The presenter is a barrel-shaped structure at the top of the style with an
apical stigma which appears after a period of time, or is initially visible but
becomes receptive some time after anthesis. The surface may be ribbed or
papillate (e.g. Cephalanthus, Pachystigma, Fadogia).
All taxa with the trait are woody and concentrated in the tropics, and hence
are close to the ancestral type in the family. The presenter seems more advanced
than the simple case of pollen shed directly from the anthers, requiring the
precise juxtaposition of pollen presenter and anthers. The simplest form, such as
found in Alberta and lxora really shows no obvious modification of the gynoecium
and the style/pollen presenter is very similar to the style in non presenting forms
such as Pentanisia.
The more elaborate fusiform type, as found in Pavetta, could be formed by the
stigmatic arms remaining appressed rather than recurving. The stigmatic tissue
grows out of the sutures which mark where the arms once separated. The barrelshaped forms could be derived by complete fusion of the arms and growth of the
stigma out of the apex of the presenter and could be considered the most
advanced form in the family. The micrographs in Igersheim (l993a) confirm this
184
P. G. LADD
and also emphasize the elaboration of the upper part of the style, including the
extraordinary development of the epidermal cells on the presenter itself.
Howell et al. ( 1993) proposed the term "exposed stigmatic presenters" for the
pollen presenter of Cephalanthus (Rubiaceae) deriving their information from
Imbert & Richards ( 1993). However the distinction between the pollen
presenter and the stigma in C. occidentalis is not clearly made in Imbert &
Richards ( 1993). The pollen presenter in C. occidentalis is typical of those in the
Vanguerieae of the Rubiaceae. In most taxa with this truncate, barrel-shaped
presenter self pollen is not deposited on the stigma sensu stricto. The stigma may in
fact be protected from self pollen by sterile apical extensions from the anthers as
shown in Vangueria apiculata (Igersheim, 1993a).
Calyceraceae
The family is a small one with similarities to the Campanulaceae and
Asteraceae. Cronquist ( 1981) suggested it arose from the Dipsacales while
Devore & Stuessy (1991) and Lammers (1992) put it close to the Goodeniaceae
and Asteraceae. The pollen presenter acts in the same way as in the Lobeliaceae,
the elongation of the style pushing pollen out of the anther tube. The stigma is
described as capitate (Cronquist, 1981) but no fresh material was available to be
examined in this survey so a detailed distinction between pollen presenter and
stigma could not be made.
Asteraceae
The pollen presenters in the Asteraceae are rarely mentioned as such, being
more usually called stigmas, style arms or stigmatic branches. This usage is not
strictly correct as the pollen presenter is the sterile tissue covering the stigmas at
anthesis or extending beyond the end of the stigmas. The presenters are of the
active type and the function is most similar to that in the Lobeliaceae. The
anther tube in the Asteraceae is generally less robust than in the Lobeliaceae.
The style pushes the piston of the pollen presenter past the anthers to extrude the
pollen from the tube and there are some similarities in the way anther
appendages may act 'in controlling pollen issue in both families. In the
Asteraceae the petal lobes may also act to control pollen issue from the anther
tube. The similarity between these two families goes beyond pollen dispersal and
is emphasized by the fact that Bremer ( 1987) used the Lobeliaceae as the
outgroup in a cladistic analysis of the Asteraceae.
The variation in form of the presenters and stigmatic surfaces has been used in
taxonomic studies (Bremer, 1987), with a number of forms recognized. Ladd &
Donaldson (1993) summarized Bremer's seven forms into the four listed below
taking most account of the pollen presenting structure rather than the stigma
form:
(1) Pollen presenter at style apex, thickened and cone shaped (with or
without hairs) e.g. Arctotis, Heterolepis, Chrysanthemoides (Fig. 23).
(2) Pollen presenter at style apex, cone-shaped but unthickened (with or
without hairs) e.g. Felicia.
(3) Pollen presenter on upper part of style narrowing to apex, covered with
antrorse hairs, e.g. Corymbium, Lactuceae (Fig. 24).
(4) Pollen presenter truncate, composed of the tissue covering the stigma
capped by a semicircle of blunt hairs at the apex of each arm, e.g. Senecio,
Athanasia, Stoebe, Haplotrichion.
POLLEN PRESENTERS
185
The majority of the Asteraceae are strongly protandrous. However some
members of the Lactucoideae appear to be protogynous with the tips of the
stigmas exposed before the pollen begins to be drawn out of the anther tube by
elongation of the style. The stigma/style of female flowers (florets) in radiate
heads is of a fairly uniform type across many unrelated taxa and is usually quite
different from the style/stigma/pollen presenter of the bisexual florets. In species
in which the disc florets are male the pollen presenter is retained and shows no
similarity to the style/stigma of the ray florets. There are few dioecious
Asteraceae, however in Brachylaena the stigma in female flowers is very similar to
the pollen presenter of the male flowers. The presenter is of the type 3 listed
above but the arms never reflex to expose the inside surface as occurs in the
female flowers.
The pollen presenter is an ancestral feature of the Asteraceae. Bremer ( 1987)
considered the thickened cone-shaped presenter to be the least advanced in the
family and noted the similarity with the style structure in the Lobeliaceae. The
group in which this presenter type occurs has recently been raised to subfamily
level, viz. the Barnadesioidae (Bremer & Jansen, 1992).
Cannaceae
In the single genus (Canna) in this family there is no discrete pollen presenter
structure that is distinct from the style except that the style is very broad relative
to its length. Pollen from the single anther (in fact half an anther) is passively
appressed to the side of the broad style below the stigma (Fig. 21). This is strictly
speaking microherkogamy as the pollen is spatially separated from the stigma by
a fraction of a millimetre. The pollen is not particularly coherent and is easily
brushed off the style.
Marantaceae
Pollen presenters are present in all members of the family (Dahlgren et al.,
1985) and have been studied in detail in a small group of species in Calathea
(Thompson, 1978). As in the Cannaceae the pollen is appressed to the style while
in bud, into a shallow depression in the style on the abaxial side below the stigma
(Fig. 22). The presenter is of the passive type but the style is under tension at
anthesis. Pollen is transferred to a pollinator by explosive release of the style
when the flower is probed by an insect.
Homeosis associated with the androecium assuming petaloid characteristics
has played an important role in the evolution of flowers in the Zingiberales
(Kirchoff, 1991). Pollen presentation is presumably an advanced character
associated with this process. In both families the androecium is reduced to one
half of one fertile anther. Secondary pollen presentation is related to the
increasing function of the, now petaloid, androecium in attraction of pollinators,
as responsibility for the dispersal of pollen is passed on to the gynoecium.
DISCUSSION
Pollen presenters are found in a variety of families spread throughout the
flowering plants. Presentation is predominantly associated with the gynoecium
but in two of the families described here involves the perianth. The trait has
clearly evolved a number of times as some families are not closely related to each
other. In the Campanulales/Asterales however, pollen presentation is found in
186
P. G. LADD
most families, and in this group is likely to have been derived from common
ancestors.
Pollen presenters form an unusual part of the diversity of floral morphological
traits which have evolved to enhance gene flow in the flowering plants. The
transfer of part of the male function from the anthers to another part of the
flower, usually the female part, seems counter productive. Pollen presentation is
ideal for autogamous plants (possibly present in some Polygala species) but the
majority of taxa with presenters are, at least facultatively, outcrossing. Selfing
may be avoided by chemical means, i.e. self incompatibility, by strong protandry
or by small spatial separation between pollen and receptive female tissue. In an
evolutionary sense pollen presenters are a derived condition. In seven of the
families some members of each family (and in most the majority) lack presenters
and it is in these families that the pollen presenters are an advanced character,
although some taxa subsequently lose the presenter but may gain it again (in a
different form) at an even later stage (e.g. Polygala).
Families in which taxa with pollen presenters occur are more likely to be
sympetalous (15) than have flowers with free petals (9, and one family has both)
and to have flowers with actinomorphic corollas ( 15) than zygomorphic flowers
(8, and two families have both).
Most species with pollen presenters are animal-pollinated. Only a minority of
members of the Proteaceae, i.e. some Leucadendron species and possibly Aulax
species, and a few Asteraceae such as Artemisia, are wind-pollinated, and even
these retain the pollen presenters as evidence of their animal-pollinated origins.
Despite the move from reliance on anthers for pollen dispersal to the use of the
gynoecium by plants with secondary pollen presentation many of these taxa
have returned to their roots and adopted the brush blossom form of
inflorescence. In the Myrtaceae evolution seems to have come full circle with
many species in Darwinia, Verticordia and Actinodium adopting a dense array of
pollen presenters as the pollen brush rather than anthers, as is the more normal
case in taxa such as Eucalyptus and Callistemon. The same situation pertains in
many Rubiaceae (e.g. Cephalanthus, Nauclea, Pavetta) in the Proteaceae (Banksia,
Protea), Campanulaceae (Phyteuma), Calyceraceae, Brunoniaceae and of course
the Asteraceae, where the vast majority of taxa have brush blossom
inflorescences. Apparently, despite the innovation of a new system of pollen
transfer, the need by species with pollen presenters to utilize pollinators which
were accustomed to ancestral taxa without pollen presenters was a strong
selective pressure channelling inflorescence structure back to earlier developed
forms.
There seems no particular association between stigma type (Heslop-Harrison
& Shivanna 1977) and whether or not plants have secondary pollen
presentation. This reflects the fact that pollen presenters have arisen
independently a number of times in different families. Of the taxa studied here,
pollen presenter families are fairly equally split between taxa with dry and those
with wet stigmas (Table 1). In the Rubiaceae and Myrtaceae some genera have
wet stigmas, while in others they are dry. In the Rubiaceae genera pollen
presenters occur in both wet and dry groups while in the Myrtaceae no pollen
presenter taxa were examined in the stigma study. The presentation of the pollen
in a droplet of oil in the Myrtaceae taxa which have presenters makes
determination of the stigma type difficult.
POLLEN PRESENTERS
187
While details of the flower are the main characteristics used in the
classification of flowering plants because of the conservative nature of floral
organization, the flower is also the site of intense selective pressure for optimal
reproductive efficiency (e.g. Lloyd & Webb, 1986; Stephenson & Bertin, 1983).
The advantage of secondary pollen presentation usually given is the close
correspondence between sites of pollen donation and reception in the flower (e.g.
Carolin, 1960; Shetler, 1979; Lloyd & Yates, 1982). It has been suggested (Lloyd
& Webb, 1986) that there is a clash of interests in outcrossing plants between
selection to place pollen and stigmas in similar positions for most effective
pollination and selection to avoid interference between the male and female
organs. The combination of self incompatibility and dichogamy in many species
emphasizes that avoiding interference between male and female organs (e.g.
Lloyd & Webb, 1986; Webb & Lloyd, 1986) is an important selective force in
flower evolution and could be a factor in the evolution of presenters. Pollen
presenters are a particularly precise method of avoiding interference while
maintaining accuracy of pollen delivery.
An additional advantage is the saving in resources devoted to the structural
tissue in the anthers in most groups with pollen presenters (exceptions are the
Lobeliaceae and some Fabaceae). The anthers need not be robust as they act
only to place the pollen on the presenter and do not have to survive rough
handling by pollinators. Some of the resources normally assigned to anthers can
therefore be utilized in other organs or alternatively the anthers can become
specialized for other functions, such as pollinator attraction (e.g. Cannaceae).
A generally similar situation to that in Canna is also seen in many Proteaceae
(e.g. Grevillea, Hakea) where the reflexed perianth parts become the landing
platform and pollinator attractant. The anthers in the lobes of the tepals are well
removed from the central part of the flower where, if they had been present, they
would interfere with pollinator visitation.
A number of trends can be recognized in taxa with pollen presenters.
Although secondary presentation can be recognized as a particular process the
evolutionary pressures which produced it in different groups may not be the
same in all of them and may not remain consistent within a group. In particular,
some taxa such as the Asteraceae have clearly diversified pollen dispersal and
reception processes considerably while retaining the presenter, just as there had
been diversification in pollen transfer modes in taxa where pollen passes directly
from the anthers of one flower to the gynoecium of another (e.g. Ericaceae).
Factors affecting fertilization efficiency can be categorized into male and
female functions and this is usually expressed as male competition for ovules and
female choice in ensuring ovules have the best genetic complement possible
(Stephenson & Bertin, 1983; Ayre & Whelan, 1989). As a generalization it can
be said that having a pollen presenter enhances male fitness. Avoidance of selfinterference between pollen liberation and pollen reception (increasing the
efficiency of cross-fertilization) assists paternal rather than maternal fitness
(Lloyd & Webb, 1986). The presenter also improves pollen reception on the
stigma because of the close coincidence of pollen and stigma over the case in
conventional pollen transfer.
In Wahlenbergia albomarginata, Lloyd & Yates (1982) noted that pollen is made
available slowly to pollinators by the gradual invagination of the pollen
presenter hairs. This was claimed to be a paternal fitness trait which enhanced
P. G. LADD
188
I. Summary of the features and basic forms of pollen presenters. Scale bars = I mm, solid shading
indicates the stigma if this is visible, stippling indicates the position of pollen on the presenter.
TABLE
Family
Typical Genera
[Number of genera
in Family!
No. of Genera
Confirtn<d with
Derived/
Ancestral
Stigma
Passive
Active/
Pollen Presenters
(Proportion of
T~
Most rorrumn fonn(s)
of the pollen presenter
famil)
Epacridaceae
Acrotriche serndtda
1(<.01)
p
D
IV
Lotus, Lupinus,
Crotalaria
46(.07)
p
D
III
[311]
Fabaceae
[6741]
=:)
~·
Swainsona, Vicia
Proteaceae
[75]
F11urea, Di11sttllR,
D
60(.8)
p
A
p__·.
liB
Leucadendron ,
Austomuellua,
Bellendena
Leucospermum, Grevillea,
Hakea
//
Protea,
/::." -
-·· .. ·.·
Mimetes, Banksia,
Dryandra
·:··::.···
Xylomelum, Turrillia,
Kermedacea
Spatalla, GreDillea,
Hakea, Stenocarpus,
Lomatia
Isopogon, Petrophile
5 (.04)
p
D
lll?
3 (.17)
p
D
I! A
Turr11ea, Trichilia,
Ekebergia
3(.06)
p
D
III
Rodl1, Wahlenbergia,
46 (1)
p
A
liB
Myrtaceae
[t351]
Actinodium,
Polygalaceae
Polygala
Chamelaucium,
Darwinia, Homoranthus,
Verticordia
[t81]
Muraltia, Comesperma,
some Polygala sp.
Meliaceae
[491]
Campanulaceae
[464]
Lightfootia,
Prismatocarpus
Siphocodon debilis
,._
'~
P"
D
cJ&g,
~
POLLEN PRESENTERS
TABLE
Family
[Number of genera
in Family)
Lobeliaceae
134 4, including
those in the
'Cyphiaceae']
Typical Genera
No. of Genera
Confirmed with
Pollen Presenters
(Proportion of
famil)
34 (1)
Lobelia, Laurentia
189
I.-continued
Active/
Passive
Derived/
Stigma
Moot rommon fonn(s)
Ancestral
Typel
of the pollen presenter
A
A
p
?D
11(1)
A
A
I(])
A
A
38 (.06)
p
D
6 (I)
A
A
1516 (I)
A
A
IV
Monopsis
Cyphia
Goodeniaceae
Goodenia, Scaevola
JIB
[Jt2]
Lechenaultia
Brunoniaceae
Brunoni4
[I]
Rubiaceae
]6401]
Alberta, Ixora
liB, IV
Pavetta, Gardenia,
Tarrena, Burchellia
Vangueria, Pachystigma
Calyceraceae
Calycera, Boopis
J61J
Asteraceae
[15161]
Arctotis, Arctotheca
·~­
JIB
~A\
Chrysocoma
If,
~-
Lactuca
Cannaceae
Canna
r-
rr
Stoebe, Senecio
1 (I)
p
D
Ill
21 (I)
p
D
IV
Ill
Marantaceae
[21 1]
Calathea, Maranta
'Gunn et al., 1992;
2
Carolin eta/., 1992;
3
Heslop Harrison & Shivanna, 1972;
4
Lammers, 1992
190
P. G. LADD
the placement of pollen on a number of different visitors rather than just a few,
hence providing the male with a wider selection of mates than would be the case
with rapid pollen removal. Controlled pollen release also occurs in the
Lobeliaceae with gradual dispensing of the pollen from the anther tube, and to a
variable extent in Goodeniaceae. This scenario is only successful if the individual
does not saturate its pollen vector. If the fitness gains are greater for the first
pollen produced than for subsequent releases then it is advantageous for all
pollen from one flower to be removed quickly (Charnov, 1979).
In the Proteaceae pollen is removed very quickly, so male fitness is likely to
have been important in the development of presenters in this family. This is also
the case in many Rubiaceae and in Turraea. However in the Proteaceae maternal
fitness factors have also been important in the development of the various traits
in the group.
The members of the Proteaceae which are closest to the ancestral form in the
family occur in rainforest and have multiflowered inflorescences, smooth pollen
presenters and in many of the taxa, multiple ovules in the unilocular ovary.
Rapid pollen removal and multiple ovules enhances paternal fitness as one
pollination is likely to fertilize all ovules and hence provide a large number of
offspring from the one father. This multiovular condition is in contrast to the
majority of the family which has only one or two ovules and inhabits
nonrainforest environments. The decrease in ovule number is likely to have
occurred due to resource limitation to seed set in nutrient poor soils (e.g. Stock et
al. 1989). In the Proteaceae there are a number of taxa from the rainforest (R)
with multiple ovules which have a corresponding taxon in sclerophyll (S)
vegetation with only two ovulesjlocules e.g. Stenocarpus (R) and Strangea (S),
Neorites (R) and Orites (S). Maternal fitness is limited by the mother's ability to
accrue resources (Lloyd & Yates, 1982, stating Bateman's Principle), so
maternal fitness became a driving force in the move of the Proteaceae into
nutrient-poor environments. The reliable pollen delivery assured by the pollen
presenter enables female choice on the pollen grains that are delivered to the
stigma so that the 'best possible' pollen can be selected to fertilize the ovule(s).
While the ovule itself is cheap to produce the seed is expensive, in nutrient terms,
for plants in nutrient-poor environments. In the Proteaceae there is a close
correlation between the nutrient content of the seed and the habitat from which
the species comes. Species from the rainforest have seeds with relatively low
nutrient levels compared with those from sclerophyll species (figures in Pate et
al., 1986). Charnov ( 1979) suggested that "if ovules are cheap, relative to the
final input of resources into seeds, a likely strategy would be for a plant to
produce many of them (along with more flowers that increase male function)".
In the heathland Proteaceae this is achieved through production of dense
inflorescences which produce few seeds. In the high light environment in which
most of these species grow the carbohydrate for flowers is relatively cheap
compared with the large input of nutrient to seeds.
The trait oflow ovule number is also found in taxa which lack presenters. The
loss of presenters in the Proteoideae taxa without them (e.g. Conospermum,
Synaphea, Stirlingia) seems to be a deriVed condition associated with development
of specialized pollen shedding mechanisms and has presumably arisen from
ancestors which had presenters and few ovules in the ovary. In the
Persoonioideae the reduction in ovule number also occurs but the pollen
POLLEN PRESENTERS
191
presenter situation is less clear. The rainforest tree, Placospermum, in this
subfamily appears "to preserve the greatest number of primitive character states
in the family" Oohnson & Briggs, 1975), has many ovules and lacks a presenter.
All other taxa in the subfamily have two ovules in the ovary but only Bellendena
has a pollen presenter.
In the Myrtaceae the evolution of pollen presentation may have been
influenced by pollen limitation and hence paternal fitness factors, and
pollination by animals larger than small insects. The Chamelaucium suballiance of
the Myrtaceae seems to have developed from the Baeckea suballiance Oohnson &
Briggs, 1984). Flowers in the latter group generally have a capitate stigma on a
short style and anthers of roughly the same length as the style and only shortly, if
at all, exserted from the flower. The development of a pollen presenter was one
solution to a problem of displaying pollen more obviously with little extra
expenditure of resources, i.e. only elongation of one style rather than of all the
anthers and the style. A number of taxa with pollen presenters are pollinated by
large animals such as birds (Verticordia grandis, V. penicillaris) and mammals (a
number of Darwinia species). Not all taxa in the group developed presenters,
Pileanthus retains a floral form similar to Baeckea while some Verticordia species
have exserted anthers and style without a presenter. The Myrtaceae would
provide an ideal case in which to study pollen: ovule ratios to examine the
patterns in contrasting taxa with or without pollen presenters growing in similar
environments.
While paternal fitness benefits seem to have been the main driving force in the
evolution of pollen presenters the enhancement in fertilization efficiency is likely
to have allowed subsequent development of maternal fitness traits, as has been
shown for the Proteaceae above. One of the selective pressures in favour of pollen
presentation should be a greater efficiency in production of seed through a
greater certainty of fertilization than occurs in plants without presenters.
Success in selective terms is measured by the fitness of offspring, which is the
product of the genetic makeup of the offspring and the amount of resources
available to the juvenile individual at the time of its establishment. While there
are a number of factors involved in the seed size/seed number trade-off
(Stebbins, 1971), as a generalization the larger the matenal investment in a
particular seed the more likely it is that the seedling produced will reach
maturity (references in Venable, 1992). In addition there is an inverse
relationship between number of ovules per loculus and the size of seed produced.
The increased reliability of fertilization should allow reduction in ovule number
and greater maternal investment in fewer seeds of superior genotype than occurs
generally in plants without pollen presenters. In outcrossing plants with pollen
presenters a trend which should be recognizable would be to fewer ovules per
loculus in the ovary.
In almost half of the families examined in detail here this is the case in taxa
with pollen presenters. In the Asteraceae, Calyceraceae, Brunoniaceae,
Marantaceae, Meliaceae, Polygalaceae and Acrotriche there is usually one (or at
least only a few) ovule(s) per loculus. This may be contrasted with taxa such as
orchids and asclepiads where pollen delivery is by pollinium and it might be
expected that in this case also there is a high pollination efficiency, but species in
these groups have many ovules per loculus. In these taxa, although the amount
of pollen at any one pollination event is large and it is delivered accurately, the
192
P. G. LADD
reliability of delivery is low. In Asclepias .ryriaca it was considered that clones were
regularly pollinia-limited in relation to seed production (Morse & Fritz, 1983).
Selection in this case has been driven by the need to produce as many offspring
as possible from the low number of successful pollinations.
The trend in ovule number reduction is apparent in the Zingiberales, where
the apomorphic condition is of multiovular loculi. In a recent phylogenetic
treatment of the order (Kress, I 990) it was proposed that the Cannaceae and
Marantaceae are the most advanced members in the order. There is a transition
from a multiovular condition with simple pollen presenter in the Cannaceae to a
uniovular condition with more specialized presenter in the Marantaceae. In
some Marantaceae this is extended even further with incomplete development of
some loculi (Dahlgren et al., 1985) so that only one or two, comparatively large
seeds are produced per flower. The reliability of pollen transfer in the group,
which has been afforded by the specialized pollen presenter has enabled greater
investment in individuals of the next generation than in the less specialized
Canna.
In Lammers' (I 992) examination of the Campanulales (in which he included
the Asteraceae) he noted the evolutionary reduction in the gynoecium in the
group, both in number of loculi and number of ovules per loculus, but offered no
explanation for the trend. The benefits to maternal fitness due to reliable pollen
delivery enable selection for higher quality rather than greater quantity of
offspring. This development is taken to extremes in the Asteraceae where there is
a trend from hermaphrodite through gynomonoecious to monoecious
inflorescences. Concomitantly through this progression there is a greater
likelihood of producing out bred, hence more genetically diverse, offspring due to
the fact that outer, ligulate (usually female) florets tend to open before the
central, bisexual or male florets.
In the Fabaceae, pollen presenters are another innovation in a number of
modifications involved in enhancing pollen transfer. Kalin Arroyo ( 1981)
considered that the major tendency in floral biology in the Leguminosae has
been improvements in the economy of pollen and nectar. Secondary pollen
presentation should certainly conserve pollen. Lavin & Delgado ( 1990) have
noted the possibility of using pollen: ovule ratios in the examination of
evolutionary trends associated with pollen presenters in the Fabaceae. However
care must be taken to distinguish correlations between pollen: ovule ratio and
breeding system from those between the same ratio and secondary pollen
presentation. Studies should be restr:cted to known outbreeding species.
Secondary pollen presentation is a fertile field for study in the areas of
pollination biology, floral evolution and taxonomy. In pollination biology, in
order to facilitate unambiguous discussion, it is essential that pollen presenters
are clearly distinguished from stigmas.
In evolutionary terms presenters are most likely to be associated with
increased efficiency of resource use and it is perhaps significant that many of the
groups are commonly associated with infertile soils and(or disturbed habitats
(Myrtaceae,
Proteaceae,
Polygalaceae,
Campanulaceae,
Lobeliaceae,
Goodeniaceae, Asteraceae). Examination of the fecundity of presenter and
nonpresenter species with similar vegetative morphology growing on similar soil
could provide useful information in this area. In taxonomy, study of pollen
presentation mechanisms will enhance an understanding of the reasons behind
POLLEN PRESENTERS
193
the arrangement of other parts of the flower (Lavin & Delgado, 1990) while the
presenter morphology also provides useful analytical characters.
ACKNOWLEDGEMENTS
I am grateful to theN ational Botanical Institute in South Africa for providing
facilities for part of this study, A. Alkema for early help in the project, I. Bennett,
J. Donaldson, I. Nanni, J. Manning and A. Rebelo for helpful discussion and to
J. Loedolff for producing the plates.
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