Download Can andromonoecy explain low fruit : flower ratios in the Proteaceae

Biological Journal of the Linnean Sociely ( 199 I ) , 44: 4 1-46
Can andromonoecy explain low fruit :flower
ratios in the Proteaceae?
BEVERLEY A. WALKER AND ROBERT J. WHELAN
Biology Department, University of Wollongong, Wollongong, NS W, 2500, Australia
Received 12 February 1990, accepted for publication I 1 April I990
There are several possible explanations for the low fruit: flower ratios commonly observed in the
Australian Proteaceae-some proximate and others ultimate. One of these, namely that some
flowers on a plant are functionally male (andromonoecy), has recently received considerable
attention. However, the term andromonoecy appears to have been misused in the pollination
ecology literature. I n this note, we clarify the use of the terms andromonoecy and androgyny, and
suggest that they should be applied with care, only after it is clear that the flowers lack ovules or that
they possess dysfunctional gynoecia. These terms should not be applied to post-fertilization events
which result in ovule abortion. Further, we review the current evidence for andromonoecy or
androgyny in the Proteaceae, especially the genus Banksia, and present the results of studies on two
additional Banksia species, B . spinulosa and B . ericifolia. The evidence so far fails to provide support
for widespread andromonoecy in this genus as an explanation for low fruit : flower ratios.
KEY WORDS:-Breeding
systems - andromonoecy - Proteaceae - fruit set.
CONTENTS
Introduction . . . . . . . . . . . .
Terminology . . . . . . . . . . . .
Tests for andromonoecy in Banksia spinulosa and B . ericifolia
Discussion. . . . . . . . . . . . .
Acknowledgements
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References
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INTRODUCTION
The low levels of fruit set commonly found in many hermaphroditic species
are currently an active area of investigation (e.g. Lloyd, 1980; Stephenson, 1981;
Willson & Burley, 1983; Sutherland & Delph, 1984; Sutherland, 1986a, b, 1987;
Ayre & Whelan, 1989; Charlesworth, 1989; Kozlowski & Stearns, 1989). The
family Proteaceae contains many species which display consistently low levels of
fruit production, measured as numbers of fruits produced either per inflorescence
or per plant (Collins & Rebelo, 1987).
Focusing on the Proteaceae, Ayre & Whelan (1989) discussed a range of
hypotheses which might explain low fruit :flower ratios, and distinguished
between proximate and ultimate hypotheses. The former relate to ecological
factors which operate in the short term and include pollen limitation, pollen
source, resource limitation and predation. Ultimate hypotheses propose that an
excess of flowers over fruits is adaptive, for one of several reasons, thereby
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1991 The Linnean Society of London
42
B. A. WALKER AND R. J. WHELAN
explaining why flower numbers have not decreased over evolutionary time to
match the number of ovules able to be matured by the plant (Haig & Westoby,
1988). Ultimate hypotheses for large flower number include pollinator
attraction, increased pollen donation (male function), optimal outcrossing
(female function), bet-hedging and predator satiation.
In another recent review of pollination in the Proteaceae, Collins & Rebelo
( 1987) emphasized the possible importance of andromonoecy as an explanation
for low levels of fruit set. Spatial patterns of fruit set among flowers on an
inflorescence or among inflorescences on a plant may provide hints of the
occurrence of female-sterile flowers. Consistent lack of fruit production in the
apex of some Banksia inflorescences (Turner, 1985; Vaughton, 1989) has been
taken as an indication that female parts of these flowers are dysfunctional.
However, ecological factors could also explain such patterns of fruit set. Whelan
& Goldingay (1988), for example, showed that fruit set was much less on the
lower third of the inflorescences of the Waratah (Telopea speciosissima) . However,
fruit set could be enforced on the basal flowers by removing the flowers on the
apical two-thirds and/or by providing the basal flowers with supplementary
outcross pollen (Whelan & Goldingay, 1988; R. L. Goldingay, personal
communication). Thus the lower flowers must be hermaphroditic, although
normally prevented from setting fruits by some ecological or physiological factor.
Sutherland (1987) described a similar situation in Agave mckelveyana.
The high proportion (40-65%) of barren infructescences in Banksia (Turner,
1985) may also be seen as evidence for male-only inflorescences. However,
experiments on B. integrgolia, B. spinulosa, B. paludosa and B . ericifolia, in which
natural pollination of inflorescences was supplemented by hand pollination using
outcross pollen, have produced increases in the total number of infructescences
(S. Cunningham, personal communication; Whelan & Goldingay, 1986;
Copland & Whelan, 1989). Thus, at least some barren inflorescences are capable
of setting fruit under appropriate conditions.
I t is clear from the above discussion that more direct evidence of impaired
female function of flowers must be sought if andromonoecy is to be
demonstrated. Johnson & Briggs (1963: 54) first proposed andromonoecy/
androgyny ( s e w stricto, see below) in Banksiu as follows: “In many species of
Banksia, many of the flowers examined, although outwardly perfect, contained
no ovules. This may be an adaptation of value in a densely crowded
inflorescence of the Banksia type”. Keighery (1980) reported that: “some species
[of Banksia] have high numbers of male flowers in the inflorescence”. George
( 1981) reported that some flowers in a single inflorescence of Banksia paludosa had
shorter perianths than the others and that these were found to lack ovules..
This apparent support for the occurrence of adromonoecy is confounded by a
later report by Johnson & Briggs (1975): “Some species of Banksia and probably
various other genera are andromonoecious, having many flowers with abortive
ovules”. Abortive ovules, however, indicate the initial potential for a n active
female function and hence by definition cannot suggest andromonoecy. Grey
(1985) and Rebelo (unpublished), cited in Collins & Rebelo (1987), reported
natural ovule abortion in Dryandra and Protea but, like Johnson & Briggs (1975),
provided no evidence that this occurred pre-fertilization. This is necessary if
andromonoecy or androgyny is to be invoked. A. S. George (personal
communication) pointed out that his observation of male-only flowers (see
ANDROMONOECY IN THE PROTEACEAE
43
above) was an isolated instance. He therefore considered andromonoecy to be
rare in the genus Banksia. Mudie (1982) dissected flowers of Banksia integrtfolia
over a flowering season and found no “aborted ovules”.
The contradictions apparent in the above discussion indicate that the evidence
for andromonoecy in the Proteaceae is still uncertain. This uncertainty could
perhaps be explained by inconsistent application of the term ‘andromonoecy’.
One aim of this note is therefore to clarify the terminology relating to the flowers
which exhibit male-only function, in relation to previous studies on the
Proteaceae. O u r second aim is to present the results of a search for
andromonoecy in two species of Banksia common in eastern Australia.
TERMINOLOGY
The terms ‘andromonoecy’ (Johnson & Briggs, 1975; Wiens, 1984-cited in
Collins & Rebelo, 1987) and ‘functional andromonoecy’ (Lamont, 1982; Rebelo
& Rourke, 1986; Collins & Rebelo, 1987) have both been applied to the
Proteaceae to describe the situation in which some flowers on an inflorescence do
not produce seed. We consider that it is important to clarify definitions of the
relevant terms and the following definitions are taken from Radford et al. (1974).
Andromonoecy
Androgyny
Functional andromonoecy
Functional androgyny
Staminate and hermaphroditic flowers (which can be
distinguished on the basis of their morphology) occur
on the same plant.
Staminate and hermaphroditic flowers occur on the
same inflorescence.
All flowers on the plant are morphologically
hermaphroditic, but some flowers have reduced or
dysfunctional gynoecia (see Anderson & Symon,
1989).
All flowers on the inflorescence are morphologically
hermaphroditic, but some flowers have reduced or
dysfunctional gynoecia.
It is clear that the application of all of these terms should be reserved for
situations in which the absence or impaired function of ovules can be
demonstrated. Lack of fruit set is insufficient evidence. These definitions also
indicate that androgyny is the appropriate term for what has been discussed in the
genus Banksia. Andromonoecy is relevant when discussing the occurrence of male
flowers at the whole plant level and is suitable when referring to barren us. nonbarren inflorescences on the same plant.
TESTS FOR ANDROMONOECY IN BANKSIA SPINULOSA AND B. ERICIFOLIA
Inflorescences from the 1988 flowering season were collected from ten Banksia
spinulosa and ten B. ericiflia plants at Barren Grounds Nature Reserve
(34’40’3O’’S; 150’43’ 15”E) near Wollongong, New South Wales. For B. spinulosa,
all inflorescences were collected from each plant, with numbers collected ranging
from six to 17 per plant. Inflorescences consisted of 30-80 floral whorls, each of
which contained 7-8 pairs of flowers. An additional two inflorescences in which
approximately 5% of the perianths appeared shorter than the others on the same
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B. A. WALKER AND R. J. WHELAN
inflorescence were also examined. For B. ericifolia, five inflorescences per plant
were examined. Inflorescences were chosen to represent the greatest range of age
classes possible. Banksia ericifolia inflorescences consisted of 30-80 floral whorls
with 13-14 pairs of flowers in each whorl.
Inflorescences were hand-sectioned transversely through the floral whorls and
ovules dissected out of each flower. For at least one inflorescence per plant, every
flower was examined. For the remaining inflorescences, subsamples were taken
by sectioning the first, second, fourth, eighth, 16th and 32nd whorl (where
appropriate) from each end of the inflorescence.
For B. spinulosa, c. 35000 flowers from 100 inflorescences were examined.
Ovules appeared dysfunctional in only three of these flowers; one ovule appeared
smaller than the others. In all other flowers, two ovules were apparently healthy.
Flowers from the additional two inflorescences which had shorter perianths were
found to have what appeared to be a fungal rot at the base of the style (which
most likely accounts for the reduction in length) and ovules which appeared
brown and diseased.
For B. ericifolia, c. 20000 flowers from 50 inflorescences were examined. Five
flowers contained shrivelled ovules. Fungal attack was thought to be responsible
for normal size ovules appearing brown and rotted in another nine flowers from
one plant.
DISCUSSION
Although some form of andromonoecy or androgyny is possible in the
Proteaceae, as suggested by Johnson & Briggs (1975), Keighery (1980) and
Collins & Rebelo (1987), the direct evidence that has accumulated so far
suggests that it may not, in fact, be widespread. Firstly, previous reports do not
clearly indicate that flowers which failed to set seed necessarily showed impaired
female function (i.e. dysfunctional ovules). Secondly, the three Banksia species
which have now been examined in detail all have apparently normal ovules in
almost every flower, i.e. flowers are at least structurally hermaphroditic.
Andromonoecy and androgyny, therefore, cannot account for either the low fruit
set per inflorescence or the occurrence of barren inflorescences per plant, at least
in the populations of the three species examined.
The existence of an hermaphroditic flower does not necessarily imply that it
will contribute genes to the next generation equally through pollen and ovules;
that is, the sex of a flower may differ from its functional gender (Lloyd, 1979;
Lloyd & Horning, 1979). One hypothesis for excess flowers in hermaphroditic
plants is that these are primarily aimed at male function; that is, the evolution of
excess flowers has been produced through male competition. Plants with more
flowers are able to father more seeds than plants with fewer (e.g. Sutherland &
Delph, 1984). This notion of ‘functional maleness’ appears to have been what is
meant by the use of the term ‘functional andromonoecy’ to account for low seed
set in hermaphroditic species in general (Stephenson, 1981) and also in the
Proteaceae (Lamont, 1982; Rebelo & Rourke, 1986; Collins & Rebelo, 1987).
This has contributed to the confusion in the application of the term
‘andromonoecy’ (cf. definitions above).
If the male-function hypothesis is indeed the sole explanation for the evolution
of low fruit : flower ratios, the production of staminate flowers (i.e. flowers
ANDROMONOECY IN THE PROTEACEAE
45
lacking female structures) should be favoured, because resources would not then
be wasted in the production of pistillate tissue (Willson, 1979; Lloyd, 1980;
Stephenson, 1981). This is not the case in the Banksia species studied. An
alternative hypothesis to explain a low fruit : flower ratio is that ‘excess’ flowers
allow plants to abort fruits selectively, thereby increasing the average quality of
the offspring eventually produced (Stephenson & Winsor, 1986; Lloyd, 1979).
This role of female function in the selection of superior matings is receiving
increased attention.
Current work on the pollination ecology and the mating system of Banksia
species shows consistent evidence of a high degree of female function occurring in
all flowers, with the resulting seed being the survivors of some discrimination
mechanisms. Stigma receptivity has been used as an indicator of perfect flowers
with female function (Stephenson, 1981). In Banksia, pollen-tubes have been
found in 57-95% of flowers in B. spinulosa ( S . Carthew, personal communication;
R. Goldingay, personal communication; Walker, Price & Waser, unpublished
data) and 50-100% of flowers in B. ericifolia (Copland & Whelan, 1989; R. L.
Goldingay personal communication; S . Schibeci personal communication).
More importantly, the high proportion of flowers with pollen-tubes has been
observed in hand-pollinated treatments using either self or outcross pollen.
Nevertheless, estimates of outcrossing-rates (t) using genetic markers indicate
that seed in open-pollinated plants is highly outcrossed (Carthew, Ayre &
Whelan, 1988; Walker, Ayre 8z Whelan, unpublished data).
These observations indicate that a high degree of female choice is operating in
Banksia species. It seems unlikely that androgyny would have positive adaptive
value in these circumstances. Androgyny would be likely to reduce the average
seed quality by limiting the opportunity for female choice, because high quality
pollen may be received by those flowers with no female function. The fitness
advantages conferred by increased donation of pollen and increased attraction of
pollinators with more flowers can be achieved without androgyny.
We conclude that andromonoecy and androgyny are worth further
investigation in the Proteaceae, although current evidence does not indicate that
they will be widespread. Moreover, the adaptive advantage of female-sterile
flowers, if they are shown to occur, is not obvious. We suggest that the terms
andromonoecy and androgyny should be applied only in situations where
flowers are morphologically male, i.e. where flowers obviously lack ovules or
female dysfunction can be demonstrated.
ACKNOWLEDGEMENTS
Comments from David Ayre, Bryan Barlow, Barbara Briggs, Sue Carthew,
Ross Goldingay, Caroline Gross, Mike Ramsey and Glenda Vaughton are
gratefully acknowledged. Funding for this study was provided by the Australian
Research Council and the Australian Flora and Fauna Research Program of the
University of Wollongong. This is contribution no. 70 of the Ecology and
Genetics Group at the University of Wollongong.
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