Can Andromonoecy Explain Low Fruit- Flower Ratios in the Proteaceae

8/18/2019 Can Andromonoecy Explain Low Fruit- Flower Ratios in the Proteaceae

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Biological Journal

of

the Linnean Sociely

199 )

, 44:

4 1-46

an andromonoecy explain ow fruit lower

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

f o r

publication

I 1

April I99

There are several possible explanations for the low fruit: flower ratios commonly observed in the

Australian Proteaceae-some proximate and others ultimate. O ne of these, namely th at some

flowers on a plant are functionally male (andromonoe cy), has recently received con siderable

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 androm onoecy a nd and rogy ny, and

suggest tha t the y should be applie d with ca re, only after it is clear tha t t he flowers lack ovules or t ha t

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 an d B . ericifolia. T he evidence so far fails to provide su ppo rt

for widespread andromonoecy in this genus as an explanation for low fruit : lower ratios.

KEY WOR DS:-Breeding systems andromono ecy Proteaceae ruit set.

C O N T E N T S

Introduction

. . . . . . . . . . . . . . . . . . . . 41

Terminology . . . . . . . . . . . . . . . . . . . . 43

Tests for andromon oecy in Banksia spinulosa and B . ericifolia . . . . . . . . .

3

Discussion.

. . . . . . . . . . . . . . . . . . . .

44

Acknowledgements . . . . . . . . . . . . . . . . . .

5

References

. . . . . . . . . . . . . . . . . . . .

45

I N T R O D U C T I O N

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 s 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

:

lower 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

41

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1991

Th e Linnean Society of London


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B. A. WALKER AND R.

J .

WHELAN

explaining why flower numbers have not decreased over evolutionary time to

match the numb er of ovules able to be ma ture d by the plant (H aig Westoby,

1988). Ultim ate hypotheses for large flower nu m be r include pollinator

attraction, increased pollen donation (male function), optimal outcrossing

(female function), bet-hedging an d p redator satiation.

I n anothe r recent review of pollination in the Proteaceae, Collins Reb elo

1987) emphasized the possible importanc e of andro mo noec y as an explan ation

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.

How ever, ecological factors could also explain su ch p attern s of fruit set. W hela n

Goldingay (1988 ), for examp le, showed th at fruit set was mu ch less on the

lower third of the inflorescences

of

the Wara tah

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 (W hela n Go ldingay , 1988;

R. L.

Goldingay, personal

communication). Thus the lower f lowers must be hermaphrodit ic, al though

normally preve nted from setting fruits by some ecological or physiological factor.

Sutherland (1987) described a similar situation in Agave mckelveyana.

T h e 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

a n d

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 .

Cun ningh am , personal comm unication; W helan Go ldingay , 1986;

Copland Wh elan, 1989). Th us, a t least some bar ren inflorescences are capab le

of setting fruit under ap pro pri ate conditions.

It is clear from the above discussion that more direct evidence of impaired

female function of flowers must be sought if andromonoecy is to be

demon strated. Johnson Briggs (1963: 54) first proposed andro mo noecy /

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”. K eighery (1980) reported tha t: “some species

[of

Banksia]

have high numbers of male flowers in the inflorescence”. George

1981) reported th a t some flowers in a single inflorescence of

Banksia paludosa

had

shorter perianths than the others and that these were found to lack ovules..

Th is ap pa ren t suppo rt for the occurrence of adromonoecy is confounded by

later report by Johnson Briggs (1975 ): “Som e species of

Banksia

and probably

various other genera are andromonoecious, having many flowers with abortive

ovules”. Abortive ovules, however, indicate the initial potential for an active

female function and hence by definition cannot suggest andromonoecy. Grey

(1985) and Reb elo (unpu blished), cited in Collins Reb elo (1987 ), reported

natu ral ovule abortion in Dryandra and Protea bu t, 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


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ANDROMONOECY

IN

TH E 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”.

T h e contradictions app aren t in the above discussion indicate th at the evidence

for andromonoecy in the Proteaceae is still uncertain. This uncertainty could

perhaps be explained by inconsistent application of the term ‘andromonoecy’.

O n e aim of this note is therefore to clarify th e 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

T h e terms ‘androm onoe cy’ (Johnson Briggs, 1975; Wiens, 1984-cited in

Collins Rebelo, 1987) an d ‘functional andromo noecy’ (La m on t, 1982; Reb elo

Rou rke, 1986; Collins Rebelo, 1987) have bo th been applied to the

Proteac eae to describe the situation in which som e flowers on a n inflorescence d o

not produce seed. We consider that i t is important to clarify definitions of the

relevant terms an d the following definitions ar e taken from Rad ford et

al.

(1974).

Andromonoecy

Stam inate an d hermap hrodit ic f lowers (which can be

distinguished on the basis of their morphology) occur

on the same plant.

Androgyny

Staminate a nd hermaphrodit ic f lowers occur on the

sam e inflorescence.

Functional andromonoecy

All flowers on the plant are morphologically

hermaphroditic, but some flowers have reduced or

dysfunctional gynoecia (see Anderson Sym on,

1989).

All flowers on the inflorescence are morphologically

hermaphrodit ic, 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 app rop ria te term for w ha t 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

bar ren

us

non-

barren inflorescences on the same plant.

Functional androgyny

TESTS FOR ANDROMONOECY IN BANKSIA

SPINULOSA

A N D

B. ERICIFOLIA

Inflorescences from the 1988 flowering season w ere collected from ten

Banksia

spinulosa

and ten

B . ericiflia

plants at Barren Grounds Nature Reserve

(34’40’3O’’S; 150’43’ 15”E ) ne a r W ollongo ng, New So uth Wales. F or B. spinulosa

all inflorescences were collected from each plant, with numbers collected ranging

from six to 17 per plan t. Inflorescences consisted of 30-80 floral whorls, each of

which contained 7-8 pairs of flowers. An add itiona l tw o inflorescences in w hich

approximately 5 of the perianths appeared shorter tha n the others on the same


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44

B.

A.

WALKER AND R. J. WHELAN

inflorescence were also examined. For

B.

ericifolia, five inflorescences per plant

were examined. Inflorescences were chosen to represe nt the greatest ran ge 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 o u t of eac h flower. Fo r a t least on e inflorescence pe r pla nt, 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.

Ov ules app eare d dysfunctional in only three of these flowers; one ovule ap pea red

smaller than the others. I n all oth er flowers, two ovules were ap pa ren tly healthy.

Flowers from the add itional two inflorescences which ha d shorter pe rianths 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 an d 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 appe aring brown an d rotted in an oth er nine flowers from

one plant.

DISCUSSION

Although some form of andromonoecy or androgyny is possible in the

Proteaceae, as suggested by Johnso n Briggs (19 75) , Ke ighery

1980)

a n d

Collins Rebelo (1987 ), the direct evidence th at has accum ulated so far

suggests tha t it m ay not, in fact, be w idespread. Firstly, previous reports d o not

clearly indicate t h at flowers which failed to set seed necessarily showed im paire d

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 an d androgyny, therefore, can no t acco unt for either the low fruit

set per inflorescence o r the occ urrence of barren inflorescences per pla nt, a t 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 Ho rning, 1 979). O n e hypothesis for excess flowers in hermaph roditic

plants is tha t these ar e primarily aimed a t ma le function; th at 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 w ha t is

meant by the use

of

the term ‘functional andromo noecy’ to acco unt for low seed

set in hermaphroditic species in general (Stephenson, 1981) and also in the

Proteaceae (L am on t, 1982; Reb elo Rou rke, 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 exp lana tion for the evolution

of low fruit

:

flower ratios, th e p rod uctio n of stam in at e flowers (i.e. flowers


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ANDROMONO ECY IN TH E 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;

Stephe nson, 198 1). Th is is not the case in th e Banksia species studied. An

alternative hypothesis to explain a low fruit : lower ra tio is t h at ‘excess’ flowers

allow plants to abort fruits selectively, thereby increasing the average quality of

the offspring even tually produ ced (Stephe nson W insor, 1986; Lloyd , 1979 ).

This role of female function in the selection of superior matings is receiving

increased atten tion.

Current work on the pollination ecology and the mating system of Banksia

species shows consistent evidence of a h igh degree of female function occ urrin g 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 comm unication;

R . Goldingay, personal comm unication; W alker, Price Waser, unpublished

d at a) an d 50-100 of flowers in

B .

ericifolia

(Co plan d Wh elan, 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 treatme nts using either self or outcross pollen.

Nevertheless, estimates of outcrossing-rates ( t ) using genetic markers indicate

tha t seed in open-pollinated plants is highly outcrossed (C arth ew , Ayre

Whelan, 1988; Walker, Ayre

8z

Whelan, unpublished data) .

These observations ind icate th at a high deg ree of female choice is op era ting 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 op portunity for female choice, because high quality

pollen m ay be received by those flowers with no female function . T h e fitness

adva ntages conferred by increased donation of pollen a nd increased attr ac tion of

pollinators with more flowers can be achieved without androgyny.

We conclude that andromonoecy and androgyny are worth further

investigation in the P roteaceae, although c urr en t evidence does not indicate th at

they will be widespread. Mo reover, the adap tive ad va nta ge 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 acknow ledged. Fu nd ing for this study was provided b y t he Au stralian

Research Council an d the Australian Flora a nd F au na Research P rog ram of the

University of Wo llongong. T his is contrib ution no. 70 of the E cology a n d

Genetics Gr ou p a t the University of Wollongong.

REFERENCES

ANDERSON,

G .J .

SYMON, D.

E., 1989. Functional dioecy and andromonoecy in Sofanurn. Evolution, 43:

204 219.


6/6

46 B. A. WAL KER AND R. J . W HELAN

AYRE, D. J. W HELAN, R .

J.,

1989. Factors controlling fruit seti n hermaphroditic plants: Studies with the

C A R T H E W , S. M., AYRE, D. J. WHELA N, R. J . , 1988. High outcrossing rates in populations of

B a n k s i a

C H A R L E S W O R T H ,

D.,

1989. Evolution of low female fertility in plants: pollen limitation, resource

COLLINS, B. G. R EB ELO, T . , 1987. Pollination biology of the Proteaceae in Australia and Southern

COPLAND, B. J.

WHELA N, R. J . , 1989. Seasonal variation in flowering intensity and pollination

GEO RGE, A. S., 1981. Th e genus B a nk si a. N y t s i a , 3: 2 3 9 4 7 3

GREY,

J., 1985. Behaviour of honeyeaters in relation to pollinalion and resource selection.

Unpublished Master of

HAIG , D. WESTOBY, M. ,

1988.

O n limits to seed production.

A m e r i ca n N a t u r a l i s t ,

131:

757-759.

JOHN SON, L. A. S. BRIGGS, B. C., 1963. Evolution in the Proteaceae. Au st ra l i a n Journal of B o t a n y , :

JOHNSON, L. A.

S.

BRIGGS, B. C.,

1975.

T h e evolution and classification of a sou thern family.

Bo t a n i ca l

KEIGHER Y,

G., 1980.

Breeding systems in

Ba n k s i a . Au s t ra l i a n S ys t em a t i c Bo t a n y S o c i e l y ,

25:

19-20.

KOZLOW S KI ,

J.

S TEAR NS ,

S.

C., 1989. Hypotheses for the production of excess zygotes: models of bet-

LA M ON T, B. B., 1982. The reproductive biology of Grevi l lea leucopteris (Proteaceae) including reference to its

LLOYD , D. G., 1979. Parental strategies of angiosperms.

N e w z e a l a n d J o u rn al

of

B o t a g ,

17: 595-606.

LLOYD , D. G. , 1980. Sexual strategies in plants. I . A hypothesis of serial adjustment

of

maternal investment

LLOYD, D. G . H O R N I N G , D. S., 1979. Distribution of

sex

in Co p ro sm a pumila on Macquarie Island,

MUDIE, D . , 1982. Floral development in Ba n k s i a i n t eg n i o l i a with an examination of a hybridization

RAD FORD , A. E. , DICK SON, W . C., MASSEY, J. R. BELL, C. R., 1974. Va scu l a r P l a n t S ys t em a t i c s . New

REBEL O, A.

G.

R O U R K E , J. P., 1986. Seed germination and seed set in southern Australian Proteaceae:

STEPHENSON, A.

G.,

1981.

Plower and fruit abortion: proximate causes and ultimate functions.

Annual

S TEP HENS ON, A. G . B ER TIN, R . I.,

1983.

Male competition, female choice, and sexual selection in

STEPH ENSO N, A. G. WIN SOR , J. A.,

1986. Lotus corniculatus

regulates offspring quality throug h selective

S UTHER LAND, S., 1986a. Patterns of fruit set: What controls fruit-flower ratios in plants? E v o l u f i o n ,

40;

S U T H E R L A N D , S. 1986b. Floral sex ratios, fruit set and resource allocation in plants. Eco l o g y ,

67:

991-1001.

S U T H E R L A N D , S., 1987. Why hermaphroditic plants pro duce man y mo re flowers than fruits: experimental

S U T H E R L A N D , S. DELPH, L. F.,

1984.

O n the impo rtance of male fitness in plants: pattern s of fruit set.

TUR NER , V. ,

1985.

The ecology of the Eastern Pygmy Possum

Cerca t e t u s n a n u s)

and its assoriation with

V A U G H T O N , G., 1989. The breeding system of

Banksia spinulosa:

evidence of autogamy.

Austral ian Journal

o j

WIENS, D. ,

1984.

Ovule survivorship, brood size, life history, breeding systems, and reproductive sucress in

WILLSON, M. F., 1979. Sexual selection in plants. A m e r i ca n N a t u r a l i s t ,

113:

777-790.

WILL SON , M. F. BUR LEY , N., 1983. M a t e C h o ic e i n P l a n ts . Princeton: Princeton University Press.

WHEL AN, R. J GOLD INGAY, R. L., 1986. Do pollinators influence seed set of Ba n k s i a p a l u d o sa Sm. and

WHELA N, R.

J.

GOL DING AY , R. L. ,

1988.

Pollination an d fruit set in War atah .

J o u rn a l of the International

Australian Proteaceae. T r e n d s in Ecology and Evolut ion,

4:

267-272.

spinulosa R. Br and Ba n k s i a p a l u d o sa Smith. Austral ian Journal of B o t a n y , 6: 217-223.

allocation and genetic load. Tren d s i n Eco l o g y a n d Evo l u t i o n , 4: 289-292.

Africa. A u s t ra l ia n j o u r n a l of Eco l o g y , 1 2 : 387-42 I

limitation of fruit set in four co-occurring Ba n k s i a species. J o u rn a l of E c o l o g y , 7 7 : 509-523.

Applied Science Thesis, Curtin University of Technology, Western Australia.

21-61.

Journal of t h e L i n n ea n S o c i eb of Lo n d o n ,

70:

83-182.

hedging and selective abortion.

Evolut ion,

43: 1369-1377.

glandular hairs and colonising potential. Fl o ra , 1 7 2 : 1-20.

dur ing one reproductive session.

N e w P l y t ol o g is t ,

86:

69-80.

Australia.

N e w z e a l a n d J ou rn al

of

Bo t a n y , 17:

5-7.

hypothesis. Unpublished Bachelor of Science Honours Thesis. University of Melbourne, Victoria.

York: Harp er Row.

ecological determinants and horticultural problems. Act a H o r t i cu l t u ra , 185: 75-88.

Rev i ew

of

Ecology and Systemat ics, 12: 253-279.

plants. In L . Real (Ed.), Pol l inat ion Biology: 109-149. New York: Academic Press.

fruit abortion. Evo l u t i o n , 40: 453-458.

117-128.

tests with Agave mckelveyana. Evolut ion, 41: 750-759.

Eco l o g y , 65: 1093-1 104

B a n k s i a .

Unpublished Ph.D thesis, Monash University, Australia.

Bo t a n y .

plants. O e c o l o g i a B e r l i n ) , 6 : 47-63.

B . spinulosa R.Br.? Australian Journal of Eco l o g y ,

11:

181-186.

Prolea Sociely, 15: 11-12,

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Can Andromonoecy Explain Low Fruit- Flower Ratios in the Proteaceae