Journal of Experimental Botany, Vol. 48, No. 314, pp. 1615-1622, September 1997
Journal of
Experimental
Botany
REVIEW ARTICLE
Effects of pollination on floral attraction and longevity
Wouter G. van Doom1
Agrotechnological Research Institute (ATO-DLO), PO Box 17, 6700 AA Wageningen, The Netherlands
Received 21 November 1996; Accepted 18 April 1997
Abstract
The end of a flower's attraction to pollinators may be
due to a range of visible cues such as permanent
flower closure, a colour change, and withering or
abscission of the petals. Floral attraction may be
reduced by pollination. Pollination-induced conclusion
of floral attraction is often due to a colour change or
to flower closure. This may or may not be followed by
a reduction in floral longevity, defined as the time to
petal withering, wilting or shattering. In a few species
floral longevity is increased following pollinationinduced flower closure or a pollination-induced change
in colour. Floral attraction, therefore, has to be distinguished from floral longevity.
A literature survey shows that pollination rapidly
reduces floral attraction in numerous orchids, but
among other plant families only about 60 genera have
been found to show pollination-induced shortening of
floral attraction. Although only a few species have
been investigated, it was invariably established that
the effect of pollination is blocked by inhibitors of
ethylene synthesis or ethylene perception, hence is
mediated by ethylene. The flowers that cease to be
attractive to pollinators, shortly following pollination,
tend to be from families that are known mainly to
comprise species in which flower longevity, petal
colour, or flower closure, is sensitive to exogenous
ethylene. This indicates that the effect of pollination
on floral attraction is generally mediated by endogenous ethylene.
Numerous species reportedly show a decrease in
the period of floral attraction after exposure to ethylene, whereas only for a small number of species a
decrease in the period of floral attraction induced by
pollination has been observed. This discrepancy may
1
be due to the greater attention that has been paid to
the effects of ethylene. Nonetheless, the possibility
remains that endogenous ethylene has a role in changing perianth form and colour in addition to signalling
the occurrence of pollination.
Key words: Ethylene sensitivity, flower closure, flower
longevity, pollination, petal colour, petal wilting, petal
withering, petal abscission.
Introduction
In several species the flowers are long-lived when not
pollinated, but show petal withering or petal abscission
shortly following pollination. Some authors assumed that
this pollination effect occurs in most, if not in all flowers
(Sprengel, 1793; Primack, 1985). Other studies, however,
show the absence of pollination-induced changes in pollinator attraction (Schemske et ai, 1978; Motten, 1986). It
is unclear how ubiquitous the effect of pollination on
floral attraction is, and whether the flowers that do and
do not show this effect can be categorized.
In a few species studied, the effect of pollination on
floral attraction, if it occurs, is apparently regulated by
endogenous ethylene, as the effect can be abolished by
inhibitors of ethylene synthesis and ethylene action
(Nichols et ai, 1983; Hoekstra and Weges, 1986; O'Neill
et ai, 1993). Flowers of these species are also sensitive
to exogenous ethylene, which usually produces the same
effects as pollination. The ethylene sensitivity of the
perianth of many flowers is known, and it has been
established that high sensitivity to ethylene occurs, for
example, in most orchids, which generally have a shorter
flower life following pollination. Other groups of flowers
are not sensitive to ethylene, and this may coincide with
the absence of an effect of pollination on floral attraction
to pollinators.
To whom correspondence should be addressed. Fax: +31 317 475347. E-mail: W.G.vanDoorn©ato.dlo.nl
For reasons for simplicity all perianth parts (either in flowers having separate petals or in those with a corolla) as well as the tepals (of flowers with
a perigon) will be termed petals, and both the perianth and the perigon are called perianth.
2
© Oxford University Press 1997
1616
van Doom
The aim of this paper is (a) to review how many species
show pollination-induced shortening of floral attraction,
(b) to classify the species that exhibit, and those that do
not show, this effect, and (c) to discuss the mediating role
of ethylene in pollination-induced shortening of flower
attraction. The possible role of ethylene is deduced from a
comparison between ethylene-sensitivity and pollinationinduced effects in petals, in a range of species. The physiological role of ethylene in mediating the effect of pollination
has been reviewed elsewhere (O'Neill and Nadeau, 1997).
Conclusion of floral attraction, effects of
pollination
Flowers cease to be attractive to pollinators by a range of
cues such as cessation of scent production, a colour change,
permanent flower closure, and petal2 senescence or abscission (Gartner, 1844; Wacker, 1911; Fitting, 1909). Floral
attraction may conclude shortly following pollination
(Gartner, 1844; Fitting, 1909; Stead, 1992). Several orchids,
for example, wilt within a day or two after pollination but
some species can stay turgid for as much as nine months
if unpollinated (Fitting, 1909; Faegri and van der Pijl,
1979), and in some Geraniaceae species the petals abscise
within 30-90 min of pollination, whilst in controls they
remained attached for several days (Fitting, 1911).
Depending on the species, pollination may induce early
perianth abscission, withering or wilting (Gartner, 1844;
Fitting, 1909; several species from various families), early
flower closure, as in many Orchidaceae (Fitting, 1909)
and Gentianaceae (Webb and Littleton, 1987), or a colour
change, as in some Leguminosae (Dunn, 1956),
Bignoniaceae (Stephenson and Thomas, 1977) and
Verbenaceae (Estes and Brown, 1973). In some species
the colour changes are subtle as they occur only at the
nectar guides (Gori, 1983), in others they occur in the
ultraviolet and are therefore not visible with the naked
human eye (Jones and Buchmann, 1974; Silberglied,
1979). Pollination can also stop the production of scent
and nectar, for example, in some Caryophyllaceae
(Brantjes, 1976) and Streptosolenjamesonii(Shue\,
1961),
respectively. In a few orchid species, it produces a change
in flower orientation (Gori, 1983). A colour change
following pollination is usually linked to cessation of
nectar production (Shuel, 1961; Schemske, 1980). Insects
have been found to associate flower colour with the
presence or absence of a reward, a process based on
learning (Swihart and Swihart, 1970; Erber, 1975). It is
unclear whether cessation of nectar production, following
pollination, may in some species occur without a change
in colour, nor is it clear whether pollinators are able to
smell the difference between the presence or absence of
nectar, and if so, at what distance.
Pollination-induced acceleration of floral senescence is
often similar to the senescence symptoms which eventually
occur when the flower is not pollinated (Fitting, 1909,
1910), but in a number of species the perianth response
after pollination differs from their senescence when not
pollinated. In Potentilla argentea and P. nepalensis, for
example, the petals of pollinated flowers rapidly wilt and
then abscise, whereas in the unpollinated flowers the petals
remain fully turgid even when they eventually fall (Gartner,
1844), and in Cyclamen the petals abscise soon after
pollination, but when the flower remains unpollinated the
petals eventually wilt and desiccate (Halevy et ah, 1984).
The main biological advantage of pollination-induced
shortening of floral attraction has been suggested to be
an increase in pollinator efficiency, as the floral changes
will direct the pollinators to flowers that are still virgin.
Indeed, seed set is pollinator-limited in many species
(Petersen et al., 1982). Advantages of early wilting/
withering or abscission of the petals may, furthermore,
be a diminishing petal maintenance cost and decreased
attraction to herbivores (Webb and Littleton, 1987).
Floral longevity is usually defined as the time from
(first) opening to the shedding or wilting of the petals.
Although in some species floral attraction and floral
longevity coincide, e.g. when the petals wilt or are shed
without previous flower closure or colour change, a
distinction between attractiveness and longevity is justified
in other flowers.
In many flowers attractiveness may be shortened following pollination whilst longevity is either not affected or
even increased. In a few other species the perianth of
pollinated flowers stays longer than that of unpollinated
ones, whilst pollination does not produce any additional
visible cue, hence floral attraction is apparently increased
by pollination. These groups will be discussed in some
more detail.
Decrease in duration of floral attraction combined with
unaffected or increased longevity
Flowers may close or change colour following pollination,
hence will not be visited again, but their perianth persists
unwilted and unabscised for several days, apparently
unaffected by pollination, for example, in Gentuma species
(Webb and Littleton, 1987). The persistence of the perianth well beyond pollination has been suggested to add
to the overall floral display of a plant, hence to longdistance attraction. When approaching such plants the
pollinators will avoid pollinated flowers based on neargoal orientation cues (Faegri and van der Pijl, 1979). In
tests with Lupinus argenteus and Lotus scoparius, pollinated flowers were manually removed from the plant or
were left. Although the pollinated flowers were individually unattractive to the pollinators, their removal resulted
in a lower visitation rate to the plant (Gori, 1983).
In a few orchids, pollination produces flower closure,
whilst it increases floral longevity. In pollinated
Zygopetalum mackaii and Z. crinitum, for example, the
Pollination and floral attraction
perianth shows a slight closing movement, which may be
noticeable to the pollinators. The petals wilt about a
month after flower opening when the flowers remain
unpollinated, but they remain for three months following
pollination (Fitting, 1910). In these flowers no visible
colour change was observed. Another group of orchids
has a green perianth, which becomes darker green following pollination, while showing a considerable delay in
petal wilting. Examples are Cleisostoma koordersii and C.
latifolium (Fitting, 1910). Pollinators may be able to
distinguish these shades of green, although this has
not been experimentally confirmed. In Listera ovata
(Hildebrand, 1863) and Dendrobium antennatum (Fitting,
1910), pollination also results in greener petals, but here
it is accompanied by a slight closing movement.
In Phalaenopsis violacea the petals change from white
to yellow within 2-3 d of pollination. Subsequently, the
petals close, wilt and become glassy. Two to three days
later they recover turgor, start to become green and,
unlike unpollinated flowers, subsequently stay fresh for
several months (Fitting, 1909, 1910). Similar petal yellowing and flower closure, followed by greening and
persistence of the petals, is found in Phalaenopsis cornu
cervi, Promenaea sp., and in Epidendrum macrochilum
(Fitting, 1910), but in these species the petals do not wilt
prior to becoming green.
Apparent increase in duration of floral attraction by
pollination
In the orchids Lycaste skinneri and Anguola uniflorum
pollination has no effect on petal colour nor on flower
opening, but it results in doubling of the time to wilting
(Fitting, 1910). A delay of petal wilting without other
visible effects (to the human eye) was also found in
Rhenanlhera lowii (Winkler, 1905). Possible changes in
the ultraviolet range have apparently not been investigated, but may well occur. Pollinator behaviour might
also tell whether they receive a signal after pollination.
How abundant is the pollination effect on flower
attraction?
Conclusion of flower attraction, shortly following pollination, occurs in numerous orchid flowers, and it is often
assumed that it also occurs in most other animalpollinated flowers (Sprengel, 1793; Primack, 1985).
However, only a few species are usually quoted in this
respect (Stead, 1992). Further perusal of the literature
resulted in a number of additional examples (Table 1).
Although a number of publications may have been missed,
the results indicate that, apart from the orchids, experimental proof for a pollination effect on floral attraction
is published for a relatively small number of species. It is
as yet not fully clear to what degree this paucity of
reported species where pollination stops floral attraction
is due to absence of research efforts. It is, at least partially,
1617
a biological reality as there are at least five groups of
animal-pollinated flowers that generally lack pollinationinduced shortening of floral attraction.
(1) Pollination is reported to reduce floral attraction in
species with bisexual flowers, in female flowers of
dioecious species (Gartner, 1844), and in protandrous
flowers (male phase precedes female phase), but
reportedly does not affect floral attraction in protogynous species, i.e. in flowers in which the female
phase precedes the male one. In Isopyrum biternatum
(Ranunculaceae) and Dentaria laciniata (Cruciferae),
for example, Schemske et al. (1978) found no
shortening of floral attraction following pollination,
and Motten (1986) observed no effect of pollination
in four out of eight species studied, which all were
protogynous. This adaptation makes biological sense
as protogyny would otherwise produce plants without
male fitness. Protogyny occurs in many plant families
(Lloyd and Webb, 1986).
(2) No clear effect of pollination on floral attraction has
usually been found in flowers that last less than a
day, e.g. in several Cactus species (Gartner, 1844;
Stead and van Doom, 1994). This is apparently also
true in protandrous flowers in which the female phase
lasts only a day, as in Geranium maculatum (Willson
et al., 1979). The attraction of these flowers or that
of the female phase is apparently already so short
that further limitation does not confer clear benefits.
Probably up to about one-third of all conspicuous
flowers last a day or less (Ashman and Schoen, 1996).
The plants of several families, such as Commelinaceae, Convulvulaceae, Cucurbitaceae, Pontederiaceae,
and Turneraceae, mainly have ephemeral flowers, and
in the tropics a majority of flowers are ephemeral;
the dipterocarp forest being extreme in this respect
as it seems to harbour ephemeral flowers only
(Primack, 1985; Endress, 1994).
(3) In the Asteraceae and Umbelliferae floral attraction
is often due to the large petals of ray florets, which
in several species are sterile (Darwin, 1859). As
pollination does not occur in such florets, no signal
can be transduced from the stigma to the petals, and
such a signal is apparently also generally not transmitted from adjacent, fertile, florets. Such interfloral
signals are, in contrast, reported in inflorescences of
Catalpa speciosa, where large flowers grow rather
closely together. When about four flowers are fertilized, adjacent buds develop into male rather than
bisexual flowers and the remaining buds abscise
(Stephenson, 1979).
(4) In some species the stigma closes shortly following
pollination but obvious changes in the petals are
lacking (Bertin, 1982; Stephenson, 1979; Waser and
Fugate, 1986).
1618
van Doom
Table 1. Pollination-induced hastening of the end of floral attraction"
The perianth shows permanent closure (closure), a colour change (colour), followed by (indicated by a comma) wilting or withering (w) or
abscission of turgid petals (a) as the first symptom of senescence; these symptoms may also show concurrently (wa). Other changes are indicated in
full. Plant classification is according to Cronquist (1988). nd: not determined or not published.
Family
Mouocots
Lihaceae
Orchidaceae
Pontederiaceae
DIcots
Bignoniaceae
Boraginaceae
Cactaceae
Campanulaceae
Caryophyllaceae
Cruciferae
Ericaceae
Gentianacea
Geraniaceae
Labiatae
Linaceae
Leguminoseae
Lobeliaceae
Malvaceae
Onagraceae
Polemoniaceae
Portulacaceae
Primulaceae
Species
Change(s)
Reference
Erythronium albidum
E. americanum
£. umbdicatum
Lihum martagon
Numerous species
closure, w*
closure, w
closure, w*
a
colour, and/or
closure, and/or
w, sometimes a
nd
Schemske et al, 1978
A.F. Motten, pers. comm 1996
Motten, 1986
Gartner, 1844
Chilopsis linearis
Borago officinalis
Pulmonaria officinalis
Mammillaria glochidiata
Campanula rapunculoides
Dianthus caryophyllus
D barbatus
D. superbus
Lychnis diurna
L. flos-cuculi
L. vespertina
Stellaria pubera
Cardamine (Dentara) angusta
Raphanus sativus
Streptanlhus tortuosus
Rhododendron spp.
Vaccinium macrocarpon
Gentianan saxosa
G serotina
Erodium manescavi
Geranium pyrenatcum
G. pusillum
Monurda didyma
M. clmopoda
Origanum vulgare
Linum grandiflorum
Caesalpima eriostachys
Lotus scoparius
L corniculatus
nd
a
colour, a
closure, w
Lupinus albifrons
L arizonicus
L blumeri
L pilosus
L. sparsiflorus
Medicago sativa
Parkinsonia aculeala
Trifolium spp.
Ulex europaeus
Lobelia cardinahs
Gossypium spp.
Malva sp.
Sidalcea oregana
Clarkia sp
Epilobium angustifolium
Oenolhera drummondii
Cobaea scandens
Ipomopsis aggregate!
Claytonia virginica
Porlulaca umbraticola
Anagallis philippi
Cyclamen sp.
Lysimachia quadrifolia
Primula sp.
colour
colour
colour
colour
colour
w
colour
w
closure
w
colour, closure
closure, w
rfd
a
closure, a
colour, closure
colour, wa
nd
closure*
closure, a
a
a'
a
a
Petersen et al., 1982
Fitting, 1921
Suessenguth, 1936
Kerner von Marilaun, 1891
Richardson and Stephenson, 1989
Nichols, 1977
Gartner, 1844
Gartner, 1844
Gartner, 1844
Gartner, 1844
Gartner, 1844
Motten, 1986
Motten, 1986
Ashman and Schoen, 1996
Preston, 1991
Gori, 1983
Hiemstra, 1993
Webb and Littleton, 1987
Webb and Littleton, 1987
Fitting, 1911, 1921
Fitting, 1911, 1921
Schulz, 1902; Fitting, 1911
Whitten, 1981
Whitten, 1981
Fitting, 1921
Kerner von Marilaun, 1891
Jones and Buchmann, 1974
Gori, 1983
R. Hoopingarner, pers. comm.
1996
Stead, 1992
Wainwright, 1978
Gori, 1987
Neeman and Nesher, 1995
Wainwright, 1978
McGregor, 1976
Jones and Buchmann, 1974
McGregor, 1976
Percival, 1965
Devlin and Stephenson, 1984
McGregor, 1976
Gartner, 1844
Ashman and Schoen, 1996
Addicott and Lynch, 1955
B Husband, pers. comm. 1996
Eisikowitch and Lazar, 1987
Gori, 1983
Ashman and Schoen, 1996
Motten, 1986
Aizen, 1993
Kerner von Marilaun, 1891
Halevy et al., 1984
Primack, 1985
Kerner von Marilaun, 1891
Pontederia cordata
w
closure, w
w
w
w
w
w
petal curling/w*
a*
nd
a
a
a
closure, w
closure, w
a
a
a
a
a
a
a
petal folds over stamens
colour
colour
Fitting, 1909
Ashman and Schoen, 1996
Pollination and floral attraction
1619
Table 1. (Continued).
The perianth shows permanent closure (closure), a colour change (colour), followed by (indicated by a comma) wilting or withering (w) or
abscission of turgid petals (a) as the first symptom of senescence; these symptoms may also show concurrently (wa). Other changes are indicated in
full. Plant classification is according to Cronquist (1988). nd: not determined or not published.
Family
Species
Change(s)
Reference
Ranunculaceae
Aquilegia sp.
Delphinium consohda
Hepatica americana
Nigella arvensis
Potentilla anserina
P. argentea
P. nepalensis
Rosa sp.
Ribes aureum
Digitalis sp.
Mimulus cardinalis
Atropa belladonna
Nicandra physaloides
Nicotiana rustica
N. tabacum
N syhestns
N bigelovn
N. multivalvis
N quadrivalvis
N. sanderae
Lycopersicon esculentum
Petunia hybrid
P. inflata
Turnera sp.
Lantana camara
Phyla incisa
a
a
tepals curl inwards, a'
a
a
a
a
a
a
a
a
wa
wa
w
w
wa
wa
wa
wa
wa
wa
colour, wa
colour, wa
nd
colour
colour
Gartner, 1844
Gartner, 1844
Motten, 1982
Sprengel, 1793
Gartner, 1844
Gartner, 1844
Gartner, 1844
Kerner von Marilaun, 1891
Suessenguth, 1936
Stead and Moore, 1979
Gartner, 1844
Kerner von Marilaun, 1891
Kerner von Marilaun, 1891
Gartner, 1844
Gartner, 1844
Kendall, 1918
Kendall, 1918
Kendall, 1918
Kendall, 1918
Kendall, 1918
Kendall, 1918
Gilissen, 1977
Singh et al., 1992
Primack, 1985
Mohan Ram and Mathur, 1984
Gori, 1983
Rosaceae
Saxifragaceae
Scrophulariaceae
Solanaceae
Turneraceae
Verbenaceae
"The reader is kindly requested, if he/she is aware of other examples, to share this knowledge with the author.
'The changes observed in these flowers have not been published; data from AF Motten (personal communication 1996).
'Cyclamen flowers show petal abscission after pollination, whereas the petals eventually wilt when not pollinated.
(5) Still other flowers have no conspicuous petals, but
attract pollinators by coloured stamens, for example,
many Proteaceae and Mimosaceae. No effects of
pollinators on stamen colour, or any other effect of
pollination on floral attraction, have apparently been
reported in these families.
Together, these groups of flowers may cover up to half
of all Angiosperm species that are pollinated by animals.
This, however, leaves a great number of animal-pollinated
species unaccounted for.
Pollination-induced shortening of floral attraction:
an adaptation to pollinator paucity?
Floral attraction varies from a few hours to three quarters
of a year, depending on the species (Faegri and van der
Pijl, 1979). Both the period of attraction and the lifespan
of flowers may have evolved as a compromise between
several factors, whose relative importance is, however,
presently unknown. Long flower attraction may be a
selective advantage in species that show obligate outcrossing, hence in species that are highly dependent of
pollinator activity (Primack, 1985). It may also be advantageous in environments with low pollinator activity, even
more so when a flower is specialized to be pollinated by
one species. An inverse relationship was established
between average temperature of a habitat, probably indicative of pollinator activity, and average floral lifespan
(Primack, 1985). Indeed, an inverse relationship was
found between pollinator visitation frequency and floral
lifespan (Ashman and Schoen, 1996). A long period of
floral attraction seems, therefore, at least partially, an
adaptation to a situation in which seed set can be highly
limited by pollinator activity.
The modulation of floral attraction may, in relatively
long-lived flowers, be an additional adaptation to low
effective pollinator activity, as it saves pollinator energy.
This would agree with the prominence, in orchids, which
usually feature high pollinator specificity (Faegri and
van der Pijl, 1979), of pollination-induced shortening of
pollinator attraction. Even in the tropics, where
pollinators are seemingly abundant and most other
flowers are ephemeral (Primack, 1985), seed set in most
orchid species is highly pollinator limited (Faegri and
van der Pijl, 1979). As described above, many orchid
flowers-even those in the tropics-have a long period of
floral attraction, which is usually modulated by
pollination.
1620
van Doom
Relationship between ethylene-induced and
pollination-induced effects
Numerous authors have shown that exogenous ethylene
causes, depending on the species, a colour change (Casper
and La Pine, 1984; Woltering and Somhorst, 1990), flower
closure (Nichols, 1966; Porat et al., 1994), and both petal
wilting and petal abscission (Woltering and van Doom,
1988). These changes after exposure of the flowers to
exogenous ethylene are similar to those observed after
pollination.
At least in Petunia (Hoekstra and Weges, 1986), carnation (Nichols et al., 1983) and Phalaenopsis (O'Neill et al.,
1993; Porat et al., 1994) the effect of pollination on petal
wilting is apparently mediated by endogenous ethylene as
it is delayed or prevented by inhibitors of ethylene synthesis or action. Similarly, endogenous ethylene has been
implicated in the effect of pollination on petal abscission
in Digitalis (Stead and Moore, 1979) and on colour
changes in pollinated Lupinus (Stead, 1992).
The sensitivity of flower longevity to ethylene has been
determined in some species from a small number of families
(Woltering and van Doom, 1988). Floral senescence characteristics, and the effects of ethylene on flowers, seem
often consistent among members of the same family or
subfamily, depending on the classification used (Woltering
and van Doom, 1988; McKenzie and Lovell, 1992). In
most species of the Geraniaceae, for example, the petals
abscise whilst fully turgid, petal fall being sensitive to
exogenous ethylene. In other families the perianth generally
wilts: in Caryophyllaceae, for example, wilting is ethylenesensitive and the Asteraceae it is usually ethyleneinsensitive. Although exceptions can be found, flower
closure seems also generally consistent with the families
(Fitting, 1909, 1910; Wacker, 1911). The families shown
to contain species whose floral attraction is shorter after
pollination (Table 1) are often those in which flower
longevity is highly sensitive to ethylene (Orchidaceae,
Campanulaceae, Caryophyllaceae, Geraniaceae, Labiatae,
Malvaceae, Polemoniaceae, Primulaceae, Ranunculaceae,
Rosaceae, and Scropulariaceae). Conversely, no examples
are found in families in which several species are reportedly
insensitive to exogenous ethylene, such as the Asteraceae
and Umbelliferae. A number of flowers in Table 1 are
from families whose general ethylene sensitivity, with
respect to floral longevity, has, as yet, not been reported,
but the flowers in some of these families (Boraginaceae,
Cruciferae) generally show petal abscission, which has been
always found to be ethylene-sensitive (Woltering and van
Doom, 1988). A few species mentioned in Table 1 are
from the Liliaceae, a family previously found to contain
flowers whose longevity is generally insensitive to exogenous ethylene, but also a few species such as tulips and lilies
which do show petal abscission (McKenzie and Loveb1,
1992), hence may be ethylene-sensitive. The latter species,
along with Erythronium albidum and E. americanum, which
show flower closure followed by withering (Table 1),
belong to one subfamily in the Liliaceae.
Conclusions
Flowers with a long period of floral attraction occur
mainly outside the tropics and may be an adaptation to
low pollinator activity. Within the tropical zone, such
flowers also occur, but these are highly specialized to a
small population of pollinators and are thus also subjected
to low effective pollinator activity. The cessation of floral
attraction due to pollination occurs mainly in flowers
with a relatively long period of floral attraction and may
be an additional adaptation to low pollinator activity, as
it saves pollinator energy.
Although it is often assumed that pollination rapidly
results in cessation of pollinator attraction, the literature
only shows this to be ubiquitous in the Orchidaceae,
whilst among other plant families only about 60 genera
have been found to show such an effect. It is as yet not
fully clear whether the paucity of reported species in
which pollination stops floral attraction is due to absence
of research efforts or is a biological reality. At least five
groups of flowers, probably comprising up to half of all
Angiosperm species with animal-pollinated flowers,
exhibit no reduction in floral attraction following pollination: (a) protogynous species, in which the female phase
precedes the male one, (b) flowers in which the female
phase lasts less than a day, (c) composite flowers in which
floral attraction occurs by sterile florets, (d) flowers
showing stigma closure following pollination, and (e)
flowers without conspicuous petals, which attract pollinators by colourful stamens.
Most of the flowers of Table 1, showing reduced attractiveness to pollinators shortly following pollination, are
from families in which changes in petal colour, flower
closure, and perianth longevity are sensitive to exogenous
ethylene. Experiments with inhibitors of ethylene action
or ethylene synthesis, carried out in a few species, showed
that endogenous ethylene is a mediator of the pollination
effects on the perianth. These species are also sensitive to
exogenous ethylene. The data on ethylene sensitivity,
therefore, indicate that pollination effects on floral attraction and floral longevity are generally mediated by endogenous ethylene. Evolution of the capacity to modulate
floral attraction and floral longevity by pollination, therefore, may be the reason of the presence of high ethylene
sensitivity in petals.
It is apparent from this paper that a detailed evaluation
of the effects of pollination on flower colour, closure, and
longevity is needed. It is worth recording, in the open
literature, instances where a pollinator effect on these
parameters is present, as well as the cases where no effect
is observed. A re-evaluation of the relationship between
Pollination and floral attraction
ethylene-sensitivity in flowers (with regard to changes in
flower form and colour) and the presence of pollinationinduced effects on form and colour, is also required. As
the number of flowers that show high ethylene-sensitivity
with regard to flower closure and colour, abscission, or
withering of the petals seems much larger than the number
of species recorded to show changes in pollinator attraction shortly after pollination, a role of ethylene (on petal
colour, abscission and senescence) other than in mediating
the effect of pollination cannot be excluded. Ethylene
may, for example, signal the presence of pathogens in the
petals, enabling the host to inhibit further pathogen entry
as the petals will be shed or wither as a response to
increased ethylene production. Additionally, little is thus
far known about flower signals that are meaningful to
insects, but invisible to the naked human eye or not
obvious to the human nose. It is unclear how many
flowers react to pollination by changes in ultraviolet
reflection or by changes in scent production that convey
a message to pollinators.
Acknowledgement
The discussions with Dr AD Stead, and his critical reading of
the manuscript, are gratefully acknowledged.
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