You are on page 1of 41

THE BOTANI CAL REVI EW

VOL. 59 APRIL-JUNE, 1993 No. 2


Dichogamy in Angiosperms
ROBERT I. BERTIN AND CHRI STI AN M. NEWMAN
Department of Biology,
College of the Holy Cross,
Worcester, Massachusetts 01610, USA
Abst ract ............................................................................................................................................................................................... 113
R6sum6 ................................................................................................................................................................................................ 114
I. Int roduct i on ......................................................................................................................................................................... 115
II. Met hods .................................................................................................................................................................................. 116
A. Dat a Gat heri ng .......................................................................................................................................................... 116
B. Dat a Analysis ............................................................................................................................................................. l 19
III. Results and Di scussi on ................................................................................................................................................ 119
A. Relative Abundance of Prot andry and Protogyny ......................................................................... I 19
B. Di chogamy and Phylogeny .............................................................................................................................. 121
1. Monocot s and Di cot s .................................................................................................................................... 121
2. Differences Among Dicot Subclasses ................................................................................................ 123
C. Di chogamy and Di st ri but i on .......................................................................................................................... 124
1. Latitude ................................................................................................................................................................... 124
2. Habi t at ..................................................................................................................................................................... 124
D. Di chogamy and Breeding Syst em ............................................................................................................... 126
1. Sexual Syst em ..................................................................................................................................................... 126
2. Selfing Ability ..................................................................................................................................................... 128
E. Di chogamy and Floral Biology ..................................................................................................................... 130
1. Fl ower Size ........................................................................................................................................................... 130
2. Phenology .............................................................................................................................................................. 131
3. One- Day Flowers ............................................................................................................................................. 131
4. St amen Signals and Rewards .................................................................................................................. 132
5. Removal of Sexual Structures ................................................................................................................ 132
6. Stigma and Ant her Exsertion .................................................................................................................. 133
7. Facilitation ............................................................................................................................................................ 133
8. Rel at i onshi p Between Intrafloral and Interfloral Di chogamy ........................................ 134
F. Di chogamy and Pollination ............................................................................................................................. 134
1. Wi nd Pollination .............................................................................................................................................. 135
2. Biotic Pollination ............................................................................................................................................. 136
3. Bee and Fly Pollination ............................................................................................................................... 136
4. Beetle Pollination ............................................................................................................................................. 137
Copies of this issue [59(2)] may be purchased from the Sci-
entific Publications Depart ment , The New York Botanical Gar-
den, Bronx, NY 10458-5126 USA. Please inquire as to prices.
The Botanical Review 59:112-152, Apr.-June, 1993 112
9 1993 The Ne w York Botanical Garden
D1CHOGAMY IN ANGIOSPERMS 113
5. Trap and Brood Species .............................................................................................................................. 137
6. Frequency of Visitation ............................................................................................................................... 138
7. Upwardly-Moving Vectors on Vertical Inflorescences ........................................................ 138
G. Limitations of Our Study .................................................................................................................................. 138
H. Avoidance of Selfing Vs. Avoidance of Pollen-Pistil Interference ..................................... 139
IV. Conclusions .......................................................................................................................................................................... 140
V. Acknowledgments ............................................................................................................................................................ 141
VI. Literature Cited ................................................................................................................................................................. 141
Appendix I: Conventions for Recording Data ........................................................................................... 144
Appendix II: Dichogamy Attributes by Family ........................................................................................ 146
Ab s t r a c t
We obt ai ned i nformat i on on di chogamy and other aspects of the biology of over
4200 species of angiosperms from several hundred published and unpublished sources.
We used this i nformat i on to describe patterns of occurrence of di chogamy and to
test specific hypotheses relating di chogamy to other characteristics of plants or their
envi ronment s.
Prot andry was more common t han prot ogyny at the intrafloral level, but the reverse
was true at the interfloral level. Patterns of di chogamy vari ed significantly among
maj or taxa, with prot ogyny mor e common among monocot yl edons and pri mi t i ve
dicotyledons, and prot andry expecially common in the Asteridae. Arctic species
tended to be less di chogamous and mor e protogynous t han t emperat e and tropical
species. Aquatic and alpine species were especially protogynous. Patterns ofdi choga-
my vari ed among sexual systems, with gynomonoeci ous and gynodioecious species
especially protandrous, and monoeci ous species highly protogynous. Aut ogamous
and self-compatible species were disproportionately protogynous. Flowers ofi nt rafl o-
rally di chogamous species were slightly larger t han those of adi chogamous species,
owing to the presence of many aut ogamous species in the latter group. Species with
interfloral prot ogyny bore much smaller flowers t han di d species with interfloral
protandry. Early-blooming species in nort h-t emperat e and polar regions were dis-
proport i onat el y protogynous. Sexual structures t hat abscised, shriveled or moved
after compl et i on of their function tended to be presented first, and those t hat facil-
itated the other sexual function were presented second. A negative association existed
between type of intrafloral and interfloral di chogamy in diclinous species. Most
animal-pollinated flowers were protandrous, except beetle-pollinated and refuge and
t rap blossoms. Wi nd pollination was markedl y associated with protogyny. Vertical
inflorescences visited by upwardl y-movi ng vectors were protandrous.
Our results suggest t hat three pri mary factors may be i nvol ved in promot i ng di-
chogamy: selection for avoi dance of pollen-pistil interference, selection for avoi dance
of self-fertilization, and selection for synchrony of pollen discharge and stigma re-
ceptivity in the different flower types of diclinous species. In contrast to many earlier
workers we reject the thesis t hat avoi dance of self-fertilization is the universal or
even the most i mpor t ant force in the evolution of most forms of dichogamy.
We attribute the prevalence of intrafloral prot andry to selection for avoiding in-
terference between pollen export and pollen receipt. Intrafloral prot ogyny was as-
sociated with imprecise pollen transfer, where ot her means of avoiding pollen-pistil
interference (e.g., herkogamy) are likely to be of limited value. The prevalence of
interfloral prot ogyny seems to reflect the smaller size of unisexual flowers t han bisexu-
114 THE BOTANICAL REVIEW
al flowers, the absence of intrafloral pollen-pistil interference in diclinous species,
and selection for synchrony of pollen discharge from one flower type with stigma
receptivity in the other.
R~sum~
Les informations obtenues sur la dichogamie et les autres aspects de la biologie de
plus 4200 esp~ces d' angiosperme proviennent de plusieurs centaines de sources pu-
bilges ou non. Nous nous sommes servis de ces informations pour d~crire les modes
d' apparition de la dichogamie et pour mettre a l'essai des hypotheses sp6cifiques
mettant en relation la dichogamie avec d' autres caract6ristiques des plantes et leur
environnement.
Au niveau intrafloral la protandrie s'est r6v616e fitre plus fr6quente que la proto-
gynie, mais le contraire s'est v6rifi6 au niveau interfloral. Les formes de la dichogamie
different de faqon significative parmi les principaux taxons avec la protogynie plus
frequente chez les monocotyl6dones et les dicotyl6dones primitives, de m~me que la
protandrie plus particuli~rement fr6quente chez les Asteridae. Nous avons remarqu6
chez les esp~ces arctiques une tendance/i gtre plus protogyniques et moins dichogames
que les esp~ees tropicales. Les esp~ces alpines et aquatiques 6talent particuli~rement
protogyniques. Les formes de la dichogamie changeaient selon le systeme sexu6: les
esp~ces gynomon6ciques et gynodi6ciques 6taient particuli~rement protandres tandis
que les esp~ces mon6ciques 6taient grandement protogyniques. Les esp~ces autoga-
miques et auto-compatibles 6taient protogyniques de fa$on disproportionn6e. Les
fleurs des e s pi e s dichogames 6taient sensiblement plus grandes que celles des esp~ces
adichogamiques en raison de la pr6sence de nombreuses es pi es autogamiques pr6-
cedemment cit6es. Les esI~ces avec une protogynie interflorale portaient des fleurs
nettement plus petites par rapport aux esp~ces ~ protandrie interflorale. Les esp~ces
~t floraison pr6coce des r6gions nord-temp6r6 et polaire 6taient protogyniques de
fa~on disproportionn6e. Les structures sexu6es qui se d6tachaient, se fl6trissaient ou
changeaient de place apr~s accomplissement de leur fonction, se pr6sentaient habi-
tueUement en premier tandis que celles qui facilitaient l' autre fonction sexuelle se
pr6sentaient en seconde position. Dans les esp~ces diclines il existait une association
n6gative entre la dichogamie de type intrafloral et celle de type interfloral. La plupart
des fleurs pollinis6es par les animaux 6taient protandres except6 celles f6cond6es par
des col6opt~res ou celles servant de refuge ou de pi~ge pour insectes. La pollinisation
par le vent 6tait associ6e de faqon marqu6e ~ la protogynie. Les inflorescences ver-
ticales visit6es par des vecteurs ascendants 6taient protandres.
Les r6sultats obtenus sugg~rent que trois facteurs de base puissent ~tre impliqu6s
pour mettre en 6vidence la dichogamie: s61ection afin d' 6viter l'interf6rence entre le
pollen et le pistil, s61ection afin d' 6viter l' autof6condation et enfin s61ection en faveur
d' une synchronie entre le d6p6t du pollen et la r6ception des stigmates dans les
diff6rents types de fleurs d' esp~es diclines. Contrairement/i de nombreux chercheurs
qui ont travaill6 auparavant sur ce m~me sujet, nous rejetons la th~se que le fait
d' 6viter l' autof6condation soit l' importance de poids darts l' 6volution de la plupart
des formes de la dichogamie.
Nous attribuons la pr6dominance de la protandrie intraflorale g la s61ection d' une
non-interference entre l' exportation et la r6ception du pollen. La protogynie intra-
florale 6tait associ6e gun transport de pollen impr6cis alors que d' autres moyens de
non-interf6rence entre le pollen et le pistil (par example l'erkogamie) avaient de fortes
DICHOGAMY IN ANGIOSPERMS 115
chances d'6tre de valeur limit6e. La pr6dominance de la protogynie interflorale semble
refl6ter la plus petite taiUe des fleurs unisexu6es par rapport ~ ceUe des fleurs bisexu6es,
l'absence d'une interf6rence intraflorale pollen-pistil dans les esp6ces diclines, et la
s61ection d'une synchronie du d6p6t de pollen/i partir d' un type de fleurs avec
r6ception de stigmates dans rautre type de fleurs existant.
I . I n t r o d u c t i o n
Dichogamy, the temporal separation of male and female functions, has been ob-
served in plants for over 200 years (K61reuter, 1761; cited in Stout, 1928). Two
forms are recognized: protandry, in which the male function precedes the female,
and protogyny, in which the female function precedes the male. Dichogamy may be
expressed within a flower (intrafloral dichogamy), or among flowers in diclinous
species (interfloral dichogamy) (Lloyd & Webb, 1986). The sexual functions usually
overlap in part (incomplete dichogamy), but sometimes are completely separated
(complete dichogamy) (Lloyd & Webb, 1986; Stout, 1928).
Dichogamy has usually been interpreted as a mechanism to reduce self-fertilization
(A1-Shehbaz, 1977; Bennett, 1870; Cruden, 1988; Darwin, 1876; Gray, 1879; Jones,
1939; Kerner von Marilaun, 1895; Lindsey, 1982; Miiller, 1883; Ponomarev, 1960;
Proctor & Yeo, 1972; Thomson, 1881). However, various workers have challenged
this explanation (Godley, 1955; Kerner von Marilaun, 1895; Lloyd & Webb, 1986;
Lloyd & Yates, 1982; Palmer et al., 1989; van der Pijl, 1978; Wyatt, 1983). A recent
analysis (Bertin, 1993) suggested that protogyny may be at least in part a mechanism
for reducing self-fertilization, but found no evidence that the same was true ofprotan-
dry.
Several alternative benefits ofdichogamy have been proposed. One is that dichoga-
my is advantageous in avoiding mutual interference between male and female sexual
functions (Bernhardt & Thien 1987; Brantjes, 1982; Lloyd & Webb, 1986; Lloyd &
Yates, 1982; van der Pijl, 1978; Wyatt, 1983). Second, dichogamy (specifically pro-
tandry) may have resulted from selection in favor of early or prolonged pollen pre-
sentation (Bawa & Beach, 1981; Lloyd & Webb, 1986; Webb, 198 l). Third, dichoga-
my may reflect the existence of different optimal positions for receiving and dispatching
pollen in species wherein increases in plant height or degree of anther exsertion occur
between the two sexual phases (Kerner von Marilaun, 1895; Lloyd & Webb, 1986).
A fourth explanation applies to species that have both bisexual and unisexual flowers,
and in which intrafloral or interfloral dichogamy already exists. In gynomonoecious
species, for example, if the female flowers open before the bisexual flowers, intrasexual
selection should favor protandry in the latter flowers, reflecting the opportunities for
fertilization presented by the early-opening female flowers. Similarly, in andromon-
oecious species wherein hermaphroditic flowers are protogynous, intrasexual selec-
tion on the male function should lead to interfloral protandry to take advantage of
mating opportunities presented by the first-opening stigmas (Bell, 1971; Knuth, 1906-
1909; Miiller, 1883; Pellmyr, 1987; Schlessman, 1978, 1982; Webb, 1981). Fifth, a
combination of intrafloral protandry and interfloral protogyny may minimize com-
petition for resources between male and female functions (Lovett Doust, 1980; Sil-
vertown, 1987). Sixth, dichogamy has been said to be advantageous in allowing
interspecific hybridization (Kerner von Marilaun, 1895). Seventh, interfloral pro-
togyny in the Asteraceae has been explained as a non-adaptive "developmental side
effect" of selection for increased ray length (Ingram & Taylor, 1982), based on a
116 THE BOTANICAL REVIEW
demonstrated inverse relationship between male expression and ray length in Senecio
squalidus. Finally, dichogamy may be a "phylogenetic relict" in species in which
other outcrossing mechanisms have subsequently evol ved (Faegri & van der Pijl,
1979).
Whatever its significance, dichogamy is widespread among angiosperms. Papers
by Henslow (1888), Kerner von Marilaun (1895 ), Stout (l 928), Faegri and van der
Pijl (1979), Bawa and Beach (1981), and Wyatt (1983) have put forth several generali-
ties or hypotheses involving the occurrence or significance of dichogamy (Table I).
In the subject' s major work to date, Lloyd and Webb (1986) reviewed previous
literature and gave numerous predictions as to the circumstances under which either
prot andry or protogyny should be advantageous.
While the presence or absence of dichogamy has been not ed in numerous des-
criptive studies of floral biology, this information has never been systematically
gathered and analyzed. Lloyd and Webb (1986) could not, for example, even state
with certainty whether prot andry was more or less common than protogyny.
Our paper is an effort to assemble the scattered data on dichogamy and to use this
information to document the occurrence of dichogamy and to evaluate various hy-
potheses concerning its distribution and adaptive significance (Table I). To avoi d
duplication, we defer an explanation of specific hypotheses to the discussion section.
II. Met hods
A. DATA GATHERI NG
We began our literature search by examining the senior author' s reprint collection,
expanding our sample to include cited references from all articles examined. We
obtained additional references from a search of Bioabstracts and the BIOSIS data
base, and unpublished information from several scientists. Almost all references are
in English, with a few each in Spanish and French. Unfortunately we could not use
sources in other languages, although translations of the compendia of Miiller (1883)
and Knut h (1906-1909) were invaluable in summarizing early European studies. A
total of 1240 references was examined, of which 840 provided useful information.
We recorded information from each species on a single data sheet, and subsequently
coded the data and entered them into a comput er file. We recorded some general
i nformat i on as well as data needed to test specific hypotheses (Table II). In recording
data we used the conventions summarized in Appendix I, and those relating specif-
ically to pattern of dichogamy, which are discussed here.
Dichogamy was scored at two different levels: intrafloral and interfloral. For in-
trafloral dichogamy we used five categories (l = protandry, 2 = protandry to adi-
chogamy, 3 = adichogamy, 4 = adichogamy to protogyny, 5 = protogyny). A separate
category was used for species showing the range from protandry to protogyny. I f a
species was represented by multiple conditions, any rare conditions, representing
only a few percent of the flowers, were ignored.
Interfloral dichogamy was scored in the same categories as above, but two addi-
tional conditions were recognized, duodichogamy and heterodichogamy. Duodichog-
amy involves a sequence of male flowers, female flowers, male flowers (Lloyd &
Webb, 1986; Stout, 1928). Heterodichogamous species consist of two morphs, one
of which is protandrous and the other protogynous (Lloyd & Webb, 1986; Stout,
1928). The timing of flowering is such that male flowers of one morph are functional
DICHOGAMY IN ANGIOSPERMS
Ta b l e I
Hy p o t h e s e s a n d o b s e r v a t i o n s e v a l u a t e d i n t hi s s t udy
117
Overall frequency of protandry and protogyny
1. Protandry is more common than protogyny (Bennett, 1870).
Dichogamy and phylogeny
2. Plant families are often wholly protandrous or wholly protogynous (Bennett, 1870).
3. Protogyny is more common among monocots than among dicots (Knuth, 1906--1909).
4. Protogyny is more common among primitive angiosperms than among advanced angiosperms
(Henslow, 1888).
Dichogamy and distribution
5. Protogyny is more common than protandry among alpine species (Henstow, 1888).
6. Protogyny is more common than protandry among species of shady habitats (Henslow, 1888).
Dichogamy and breeding system
7. Monoecious species are disproportionately protogynous (Kerner yon Marilaun, 1895; Knuth,
1906-1909).
8. All gynodioecious species exhibit dichogamy (Darwin, 1888).
9. Adichogamy is more common among SI species than among SC species (Lloyd & Webb, 1986).
10. Protogyny is more common in SC species than in SI species (Bawa & Beach, 1981).
11. Protogyny is more common among species that can self-fertilize without the aid of vectors than
among others (Henslow, 1888).
Dichogamy and floral biology
12. Dichogamy is more common in species with larger flowers than among those with smaller flowers
(Henslow, 1888).
13. Smaller flowers are more likely to be protogynous than protandrous (Henslow, 1888).
14. Protogyny is more common in species flowering early in the season than among later-flowering
species (Henslow, 1888).
15. One-day flowers are especially likely to be protandrous (Bawa & Beach, 1981).
16. Protogyny is more common in species whose stamens are associated with signals or rewards than
in other species (Lloyd & Webb, 1986).
17. Pollen flowers are rarely dichogamous (van der Pijl, 1978).
18. Pollen flowers are rarely protogynous (Richards, 1986).
19. Among species in which the sexual organs of one gender facilitate the other sexual function, the
organs of the facilitating function are presented second (Lloyd & Webb, 1986).
20. The sporophyll (anthers or stigma) projecting furthest should be presented second (Lloyd &
Webb, 1986).
21. I f one sporophyll abscises, moves or shrivels after presentation, then it is presented first (Lloyd
& Webb, 1986).
Dichogamy and pollination
22. Protandry is more common than protogyny among insect-pollinated (Behrens, 1885) and animal-
pollinated species (Lloyd & Webb, 1986).
23. Protogyny is more common among wind-pollinated species than among other species (Mtiller,
1883; Henslow, 1888).
24. Wind-pollinated hermaphrodite flowers exhibit complete dichogamy (Kemer yon Marilaun, 1895).
25. Moth- and butterfly-pollinated species are especially likely to be dichogamous (Willemstein,
1987).
26. Plants pollinated by bees and flies are predominantly protandrous (Wyatt, 1983).
27. Plants pollinated by vectors other than flies and bees are predominantly protogynous (Wyatt,
1983).
28. Protogyny is associated with beetle pollination (Faegri & van der Pijl, 1979).
29. Plants producing flowers or inflorescences serving as traps or broodplaces are protogynous (Bawa
& Beach, 1981).
30. Dichogamy is more common in species with frequent insect visits than in those with few insect
visits (Miiller, 1883).
31. Species with vertical acropetally-maturing inflorescences pollinated by upwardly-moving vectors
are protandrous (Darwin, 1862, 1876).
32. Protogyny is especially common in species with unreliable pollination (Bawa & Beach, 1981).
118 THE BOTANICAL REVIEW
during the female phase of the other morph. Andromonoeci ous species were scored
as prot androus i f mal e flowers preceded perfect flowers, and protogynous i f mal e
flowers followed perfect flowers. Among gynomonoeci ous species, the designation
was prot ogynous i f female flowers preceded perfect flowers, and prot androus i f perfect
flowers preceded female.
In all, our sampl e included dat a on 4277 species. The distribution of the sampl e
among families is given in Appendi x II.
B. DATA ANALYSIS
We analyzed dat a separately for intrafloral and interfloral dichogamy. Where spe-
cies were to be grouped into prot androus and protogynous categories for analysis,
Tabl e I I
Informat i on on species sampl ed
scientific name
family
continental location
latitude
habitat
growth form
pcrennation
sexual system
flowering time
self-sterility
pollen/ovule ratio
flower size
flower lifespan
inflorescence verticality
flower maturation pattern within inflorescence
pollinator movement pattern within inflorescence
pattern of intrafloral dichogamy
intrafloral pollen-stigma overlap
spontaneous autogamy
sporophyll projecting furthest
facilitating sex
post-presentation stigma changes
post-presentation stamen changes
pollinators
use of blossoms for traps or broodplaces
pollen reward
other stamen rewards or attractants
pattern of interfloral dichogamy
interfloral pollen-stigma overlap
nectar production
outcrossing rate
literature reference
DICHOGAMY IN ANGIOSPERMS 119
we included categories 1 and 2 as prot androus and categories 4 and 5 as protogynous.
Prel i mi nary analyses treated category 1 (only) as prot androus and category 5 (only)
as protogynous, but the results from this classification were i nvari abl y the same as
with the l umped categories, so only analyses with the latter groupings are presented
in this paper. For tests involving categorical compari sons we empl oyed log-likelihood
tests using the G-statistic. Unless otherwise stated, we tested the null hypothesis t hat
plant characteristic (e.g., wind- vs. animal-pollinated) was i ndependent of di chogamy
category (e.g., prot andry vs. protogyny). Where we state t hat one type of di chogamy
is more or less common t han the other, this means t hat the two kinds of categories
were not independent.
For ot her tests it was most conveni ent to calculate di chogamy scores. These were
calculated separately for intrafloral and interfloral di chogamy by obtaining an average
over the species included in the analysis for those species in di chogamy categories
number ed 1-5. Thus a score of 1.0 indicates universal protandry, a score of 3.0
indicates neither prot andry nor protogyny, and a score of 5.0 indicates universal
protogyny.
For other tests it was necessary to have a score representing divergence from the
adi chogamous condition, irrespective of direction. Such adi chogamy scores were
calculated as the absolute value of the di chogamy score mi nus three. An adi chogamy
score of 0.0 indicates universal adichogamy, and a score of 2.0 indicates universal
dichogamy. Not e t hat a sampl e with an average di chogamy score of 3.0 mi ght have
an average adi chogamy score ranging from 0.0 to 2.0, depending on whether the
di chogamy average represented a group of species each having a di chogamy score of
3.0 or a group containing equal numbers of species with scores of 1.0 and 5.0.
We empl oyed nonparamet ri c tests for analyses of di chogamy scores and adichoga-
my scores owing to non-normal pat t erns in these data. Nevertheless, because of the
few (five) steps in our system for ranking dichogamy, we often encountered significant
differences among samples which had the same median. For this reason we also
report means and standard errors when we report di chogamy scores.
Three variables were log-transformed pri or to analysis by paramet ri c methods:
pollen/ovule ratio, flower size and inflorescence size. Significance levels are denoted
with asterisks: * < 0.05, ** < 0.01, *** < 0.001.
III. Res ul t s and Di s c us s i on
A. RELATIVE ABUNDANCE OF PROTANDRY AND PROTOGYNY
Prot andry was significantly mor e common t han prot ogyny at the intrafloral level.
Of 3151 species having intrafloral dichogamy, 66.2% were protandrous, and 33.8%
were protogynous (G = 338.22***). However, at the interfloral level, the reverse was
true, with 77.90/0 of 565 species being prot ogynous (G = 186.08"**).
These numbers could be biased by the uneven distribution of our sampl ed species
among taxa. In an at t empt to evaluate this bias we calculated weighted average
di ehogamy scores separately for intrafloral and interfloral dichogamy. To do this we
multiplied the mean di chogamy score for each family in our sampl e t i mes the number
of species in t hat fami l y as report ed by Mabbefl y (1987). Where we had dat a for
120 THE BOTANICAL REVIEW
both intrafloral and intcrfloral dichogamy within a family we apportioned species in
the family among intra- and interfloral categories based on the number of species in
our sample for that family exhibiting each kind of dichogamy. Our weighted average
intrafloral score, representing 157 families and 191,490 species, was 2.38. The overall
interfloral score, representing 43 families and 3 l, 127 species, was 4.20. These results
are consistent with the uncorrected results reported above.
Several authors have stated that protandry is more common than protogyny (Bawa
& Beach, 1981; Bennett, 1870; Bunt, 1977; Darwin, 1876; Henslow, 1888; Jones,
1939; Lloyd & Yates, 1982; Miiller, 1883; Thomson, 1881; Wyatt, 1983). Two sets
of data have previously been examined in this regard. Of 235 hermaphroditic species
from New Zealand, 37% were protandrous and 8% were protogynous (Thomson,
1881; Wyatt, 1983). Among 180 dichogamous species from the Biological Flora of
the British Isles series in the Journal of Ecology as summarized by Lloyd and Webb
(1986), 43% were protandrous and 57% were protogynous. This sample included
both hermaphroditic and monoecious species, and included an unrepresentatively
high proportion of wind-pollinated species (Lloyd & Webb, 1986).
Several explanations have been proposed for the commonness ofprotandry. Hens-
low (1888), Faegri and van der Pijl (1979), Wyatt 0983) and Willemstein (1987)
suggested a mechanistic explanation, that intrafloral protandry simply reflects the
usual centripetal pattern of maturation of floral pans. By this reasoning, stamens
should mature first because they lie outside the pistils. This explanation does not
make any prediction about interfloral dichogamy, and the fact that protandry is not
more common than protogyny at the interfloral level is consistent with this hypoth-
esis. Difficult to reconcile with this explanation, however, is the almost universal
protogyny in the most primitive dicot subclass (see below). Thus we must either
assume that protandry in more advanced dicots is a derived condition (Bernhardt
& Thien, 1987), which would be inconsistent with this hypothesis, or that the more
advanced dicots are derived from some unknown protandrous ancestor of the modern
Magnoliidae. While Willemstein (1987) suggests that protandry may in fact have
arisen very early in angiosperm evolution, we know of no evidence to support the
existence of a protandrous ancestor.
One adaptive explanation for the prevalence of protandry is that intrasexual se-
lection among males favors early pollen release because early-arriving pollen on a
stigma is at a competitive advantage (Bawa & Beach, 1981; Webb, 198 I). Conversely,
selection should favor receptivity of stigmas after pollinators have removed pollen
from a diverse array of genotypes (Bawa & Beach, 198 l) because the availability of
a sufficient quality and quantity of pollen may enhance the number and/ or quality
of seeds produced. This explanation seems plausible at the intrafloral level, but it
should also lead to a high frequency of protandry at the intcrfloral level, which is
not the case.
Silvertown (I 987) suggested that protandry is advantageous because it generates
a convex fitness set for male and female functions. He reached this conclusion from
an experimental study of the monoecious species Cucumis sativus, wherein he showed
that male function has no cost in terms of female function, but that female function
strongly affects male flower production. Thus he reasoned that with protandry, male
function does not overlap in time the female function. Protogyny would be less
beneficial because female expenditures continue during fruit production, meaning
that pollen release would be delayed for a long time alter female flowering. Silver-
town' s predictions seem most applicable to monoecious species because these prob-
DICHOGAMY IN ANGIOSPERMS 121
ably have the greatest flexibility in the timing of male and female sex expression
since stamens and pistils are separated among flowers, yet these species are predom-
inantly protogynous (see below) in contrast to his prediction. Hermaphroditic species
(defined in this paper as species having only bisexual flowers) having no synchrony
in timing of sexual stages among flowers are mostly protandrous, yet Silvertown' s
prediction would be least applicable to this group because demands of resources for
male and female functions in different flowers are likely to overlap in such species,
lessening the benefits of temporal separation within a flower.
Anot her possible explanation is that the expansion of carpels into fruits dictates
that these structures should be presented after the stamens so as not to get in the
latter' s way (Lloyd & Webb, 1986). This explanation would apply primarily intraflo-
rally, since the presence of androecia and gynoecia in different flowers would usually
allow more room for fruit maturation. It is not clear, however, whether carpel ex-
pansion after fertilization is rapid enough to obstruct male function in most flowers.
Yet another explanation for the greater abundance of prot andry than protogyny
intraflorally is that removal of one set of sexual organs will commonl y be useful to
avoid pollen-stigma interference and perhaps self-fertilization. This is so because the
effectiveness of many pollination mechanisms requires pollen and stigma to be pre-
sented at very nearly the same location. Removal of androecia is generally easier
than removal of gynoecia because gynoecial but not androecial function persists after
flowering (Lloyd & Webb, 1986; Lloyd & Yates, 1982). This explanation is funda-
mental enough to apply to most plants, and yet it is irrelevant at the interfloral level,
which would explain why protandry is not more common there. Thus this explanation
and perhaps the previous one seem to be most consistent with the data. Both invoke
avoidance of pollen-stigma interference as a maj or force in the evolution of dichoga-
my, and especially protandry.
B. DI CHOGAMY AND PHYLOGENY
When average family dichogamy scores were calculated, a plot of frequency versus
dichogamy score gives a trimodal distribution, with peaks at 1, 3 and 5. The pattern
remains when families represented in our sample by only one species were eliminated
(Fig. 1). Such families would be represented only by whole numbers i f included in
Figure 1, and their inclusion would enhance the trends described. Most families
tended to be either wholly protandrous, wholly protogynous, or adichogamous. Rela-
tively few families had intermediate scores. The patterns were similar for interfloral
and intrafloral dichogamy, although the latter plot shows a much greater proportion
of families at the protogynous peak (Fig. 1). This clustering of family dichogamy
scores at the extremes of the range was ment i oned by Bennett (1870), and suggests
a degree of evolutionary conservatism to dichogamy.
1. Monocots and Dicots
Intrafloral protogyny was much more common among monocots than among
dicots, a trend also not ed by Knut h (1906-1909) and Lloyd and Webb (1986). Only
28.8% of di cot s were protogynous, compared to 69.4O/o of monocots (G = 192.76"**,
n = 307, 2947, respectively). Less difference occurred with regard to interfloral
protogyny, with 73.0% protogyny among monocots and 81.1~ among dicots (G =
5.12", n = 226, 339, respectively). The greater frequency of intrafloral protogyny
122 THE BOTANICAL REVIEW
Fig. 1. Di st ri but i on of angiosperm families among dichogamy score categories: 1 = protan-
dry, 3 = adichogamy, 5 = protogyny. Families represented in the data set by a single species
were excluded.
DICHOGAMY IN ANGIOSPERMS 123
among monocot s t han among dicots can be explained partly by ecological factors.
Specifically, wind- and beetle-pollination are associated with prot ogyny (see below)
and are mor e common among monocot s t han among dicots, as are t rap and brood
plants. Even with all these categories eliminated, however, monocot s were still more
prot ogynous t han dicots (42.3% protogyny, n = 222), again suggesting evol ut i onary
conservatism.
2. Differences Among Dicot Subclasses
The relative frequencies ofintrafloral prot ogyny and prot andry differed significantly
among the six dicot subclasses (Kruskal-WaUis, Tabl e III). Members of the Mag-
noliidae, the most pri mi t i ve subclass, and the Hamamel i dae were al most exclusively
protogynous. In contrast, the most advanced subclass (Asteridae) had the lowest
(most protandrous) score. Prot andry in the latter case undoubtedly reflects the stereo-
typed mechani sm of pollen presentation in the Asteraceae and Campanulaceae, wherein
pollen is released into a t ube and presented or pushed forward by the pistil (Thomson,
1881). Such a compl ex mechani sm undoubt edl y constrains evol ut i on towards pro-
togyny by individual species. The commonness of prot andry in advanced families
such as these was not ed by Jones (1939), Percival (1965), Cadqui st (1976) and Faegri
and van der Pijl (1979).
While an association between protogyny and pri mi t i ve angi osperms has often been
not ed (Bernhardt & Thien, 1987; Henslow, 1888; Lloyd & Webb, 1986; Willemstein,
1987), its basis is unclear. Beetle pollination and t rap and brood bl ossoms (which
tend to be associated with protogyny, see below) are common in the Magnoliidae,
yet even when these two groups of species are deleted, the Magnoliidae remai n
decidedly protogynous, with a medi an di chogamy score of 5.0 and a mean of 3.6 (n
= 223). Bernhardt and Thi en (1987) also note the prevalence of prot ogyny in even
the non-beetle-pollinated member s of this group. Furt hermore, wind pollination,
which is commonl y associated with protogyny, is rare in this subclass. Lloyd and
Webb (1986) not ed t hat the st amens of some pri mi t i ve species produce floral scents
or nectar or bear structures with a presumed attractive function. They suggested t hat
such traits will favor prot ogyny because "t he integrity of the floral syndrome then
depends on the st amens being present and intact throughout anthesis. " As not ed
below, however, we found no association between prot ogyny and the use of st amens
for signals and rewards, and therefore we have no reason to t hi nk t hat it is an
i mpor t ant selective force here. Unless unidentified ecological factors underlie the
Tabl e I I I
Mean intrafloral di chogamy scores in the five dicot subclasses"
Subclass Mean Median SE N
Magnoliidae 3.90 5.0 0.099 271
Hamamelidae 3.88 5.0 0.507 16
CaryophyUidae 2.49 2.0 0.112 208
Dilleniidae 2.98 3.0 0.076 376
Rosidae 2.07 1.0 0.041 1676
Asteridae 1.95 1.0 0.050 906
" Kruskal-Wallis H = 402.10"**, 5 df.
124 THE BOTANICAL REVIEW
protogyny of primitive dicots, an explanation involving some sort of evolutionary
constraints must be invoked.
Even while pattern of dichogamy appears to be a relatively constant trait in certain
higher taxa, other families such as the Gentianaceae, Ericaceae, Polemoniaceae and
Rosaceae exhibit wide variation from protogyny to protandry (Bennett, 1870; Kerner
von Marilaun, 1895). Furthermore, several studies have identified variation at the
intraspecific level (A1-Shehbaz, 1977; Knuth, 1906-1909; Mtiller, 1883; Percival,
1965; Phillip, 1985; Schoen, 1977; Wyatt, 1984), and others reveal environmental
influences on dichogamy (Pistolesi et al., 1986) indicating either that selective pres-
sures or resistance to selection are much more variable in some families than in
others.
C. DICHOGAMY AND DISTRIBUTION
1. Lat i t ude
Intrafloral dichogamy exhibited two patterns with respect to latitude. Average
dichogamy scores differed significantly among plants in arctic, temperate and tropical
categories (Table IV), with arctic species being more protogynous than temperate or
tropical species. Adichogamy scores also varied among the three categories, with
tropical species being most dichogamous and arctic species being least so (Table IV).
Scores for interfloral dichogamy showed the same pattern, with arctic species being
most protogynous and tropical species least so (Table IV). However, all scores were
on the protogynous side of the distribution (greater than 3.0). There were no significant
differences in interfloral adichogamy scores.
The high incidence of adichogamy in the Arctic may reflect the higher frequency
of species adapted for self-pollination at such latitudes, owing to the uncertainty of
pollinator availability. Similarly, the relative commonness of protogyny could reflect
allowance for self-pollination in the absence of insect visitation. Mosquin and Martin
(1967), though not specifically mentioning dichogamy, argued that there is little
selection for traits promoting outcrossing in the Arctic.
The more pronounced dichogamy in tropical species might reflect the unimportance
of self-pollination, or perhaps the greater premium placed on avoidance of selfing or
pollen-pistil interference. However, tropical species are less well known than tem-
perate species, and it is possible that cases of pronounced dichogamy are more likely
to be recognized than cases of adiehogamy in poorly known floras, increasing the
apparent incidence of dichogamy in the tropics.
2. Habi t at
Average intrafloral dichogamy scores differed significantly among species from
different habitats (Table V). The most protogynous scores were for aquatic species,
and the most protandrous scores for shrubby habitats, reflecting the large sample of
protandrous Proteaceae from Australian scrub. Intrafloral adichogamy scores also
varied significantly with habitat (Table VI) with desert species showing the least
dichogamy and aquatic and alpine species the most. Interfloral dichogamy scores
differed significantly among habitats, though with no well-sampled habitats diverging
far from protogyny (Table V).
The prevalence of protogyny among aquatic plants appears unrelated to known
DICHOGAMY IN ANGIOSPERMS
Table IV
Dichogamy scores of plants at different latitudes
125
Latitude Median Mean SE N
Intrafloral dichogamy scores H = 29.22***
Arctic 3.00 3.08 0.16 99
Temperate 1.00 2.25 0.04 2040
Tropical 1.00 2.45 0.07 600
Intrafloral adichogamy scores H = 59.03***
Arctic 2.00 1.43 0.07 99
Temperate 2.00 1.61 0.02 2040
Tropical 2.00 1.78 0.02 600
Interfloral dichogamy scores H = 9.18**
Arctic 5.00 5.00 0.00 4
Temperate 5.00 4.43 0.09 227
Tropical 5.00 3.98 0.13 184
Interfloral adichogamy scores H = 0.08ns
Arctic 2.00 2.00 0.00 4
Temperate 2.00 1.97 0.14 227
Tropical 2.00 1.98 0.13 184
ecological factors. El i mi nat i on of beetle-pollinated, wind-pollinated, and trap and
brood species decreased the average intrafloral dichogamy score only from 4.39 to
4.28, still well above that of non-aquat i c species. The monocots, and the dicot
subclasses Magnoliidae and Dilleniidae are disproportionately represented among
Table V
Dichogamy scores for species in different habitats
Habitat Median Mean SE N
Intrafloral dichogamy a
Forest 1.0 2.47 0.086 401
Shrub/scrub 1.0 1.26 0.057 228
Grassland 1.0 2.08 0.117 178
Swamp/marsh 3.0 3.07 0.117 218
Aquatic 5.0 4.39 0.179 51
Alpine 3.0 3.13 0.330 31
Rock/ledge 1.0 2.15 0.262 33
Disturbed 3.0 2.65 0.107 196
Desert 2.0 2.00 0.180 31
Interfloral dichogamy b
Forest 5.0 3.56 0.193 96
Shrub/scrub 5.0 3.40 0.980 5
Grassland 5.0 4.94 0.056 18
Swamp/marsh 5.0 4.70 0.152 46
Aquatic 5.0 4.73 0.185 30
Alpine 5.0 5.00 0.000 2
Disturbed 5.0 4.58 0.202 38
Desert 3.0 3.67 1.330 3
Intrafloral Kruskal-Wallis H = 239.41"**, 8 df.
b Interfloral Kruskal-Wallis H = 31.03***, 7 df.
126 THE BOTANICAL REVIEW
Tabl e VI
Di chogamy scores of plants with different sexual systems
Sexual system Median Mean SE N
Intrafloral dichogamy a
Hermaphroditism 1.0 2.17 0.040 1634
Gynodioecy 1.0 1.56 0.150 62
Gynomonoecy 1.0 1.23 0.101 74
Androdioecy 5.0 5.00 0.000 3
Andromonoecy 1.0 2.31 0.153 131
Trioecy 1.0 1.00 0.000 4
Heterostyly 3.0 2.71 0.522 7
Interfloral dichogamy b
Monoecy 5.0 3.83 0.098 339
Gynomonoecy 5.0 5.00 0.000 84
Andromonoecy 5.0 4.15 0.162 103
Trioecy 5.0 5.00 -- 1
a Intrafloral Kruskai-Wallis H = 49.60***, 7 df.
b Interfloral Kruskal-Wallis H = 34.11"**, 3 df.
aquatics also, and elimination of these taxa gives an average intrafloral di chogamy
score of 2.33, much closer to t hat of non-aquatics similarly truncated (2.07, n = 6,
2802). Thus it appears t hat the prevalence of protogyny among aquatic plants reflects
partly the nature of the taxa occupying aquatic habitats.
Alpine species were typically mor e protogynous t han ot her species, although few
alpine species were present in our sample. Of 27 alpine species, 55.5% were prot o-
gynous, compared to 30.8% of 1194 species of other habitats (G = 6.88**). Thi s
pattern was not ed by Henslow (1888), who suggested t hat the low alpine t emperat ures
limit the devel opment of androecia more t han the devel opment of gynoecia. We
know of no evidence to support this contention. Thi s pattern may instead be related
to the greater incidence of self-compatibility (SC) and spontaneous aut ogamy in such
habitats. Of 16 alpine species for which we have data, 69% exhibited spontaneous
aut ogamy, compar ed to 45% of 969 ot her species. Similarly, only 5% of 19 alpine
species were self-incompatible (SI), compared to 25.3% of 1034 other species. As
not ed elsewhere, prot ogyny seems to be associated bot h with SC and the capacity
for spont aneous self-fertilization, presumabl y because it permi t s backup self-polli-
nation should outcrossing fail.
Henslow (1888) described an association between prot andry and shady habitat,
suggesting t hat the cooler t emperat ures of such habitats differentially limit mal e
devel opment . However, we found no differences between forests and ot her habitats
in the incidence of intrafloral prot andry among the herbaceous plants (intrafloral G
= 1.50ns; n = 125, 1079; interfloral G = 0.38ns; n = 27, 236, respectively).
D. DICHOGAMY AND BREEDING SYSTEM
1. Sexual System
Average intrafloral di chogamy scores differed substantially for species with different
sexual systems (Table VI). Species categorized as gynodioecious, gynomonoeci ous
and trioecious all exhibited a marked propensity towards protandry, although the
sampl e size for trioecious species was small. The androdioecious category was the
DICHOGAMY IN ANGIOSPERMS 127
only one to have a protogynous average, although the sample included only three
species. All ot her sexual systems had average scores slightly to the protandrous side
of adichogamy. The prevalence of prot andry among gynomonoecious and gyno-
dioecious species is noteworthy because in bot h such groups prot andry could be
viewed as resulting from intrasexual (male) competition to take advantage of available
female flowers.
Intrafloral adichogamy scores were also significantly variable among sexual systems
(Table VII). Heterostylous species were least dichogamous, hermaphroditic and mon-
oecious species were moderately dichogamous, and species with ot her systems were
highly dichogamous. The relative lack of dichogamy among heterostylous species
was also noted by Willemstein (1987), and is consistent with the view of heterostyly
as a mechanism that reduces inappropriate crosses (Darwin, 1888). Dichogamy is
then superfluous as a mechanism for reducing either self-fertilization or pollen-stigma
interference. Furthermore, the existence of dichogamy would reduce pollination ef-
ficiency by limiting the simultaneous deposition and removal of pollen on different
parts of a vector' s body.
While the average interfloral dichogamy scores differed among sexual systems
(Table VI), all showed substantial protogyny. There were no significant differences
among sexual systems in interfloral adichogamy scores.
The incidence ofinterfloral protogyny among monoecious species was greater than
the incidence of intrafloral protogyny among hermaphrodites. Of 334 monoecious
species, 71.0% exhibited interfloral protogyny, while only 27.0% of 1706 hermaphro-
dites showed intrafloral protogyny (G = 227.92"**). Wyatt (1983) and Cruden (1988)
likewise observed an association between monoecy and protogyny in smaller samples,
although Richards (1986) suggested an association between monoecy and protandry.
Monoecious species were disproportionately wind-pollinated (45.9%, compared to
only 8.9% among 1072 hermaphrodites). While wind-pollination is associated with
protogyny (see below), the elimination of wind-pollinated species from our sample
of monoecious plants left a mean dichogamy score of 3.87 (n = 256), virtually
unchanged from the mean for all monoecious species (Table VI).
An alternative explanation was suggested by Wyatt (1983). He argued that pro-
togyny reflects the normal pattern of floral devel opment in species such as Arum
nigrum. Female flowers in such taxa are basal to male flowers, and an acropetal
pattern of devel opment yields protogyny. This explanation takes for granted the basal
position of female flowers, which itself requires explanation.
We believe that the commonness of protogyny in monoecious species lies instead
Table VII
Intrafloral adichogamy scores in various sexual systems a
Sexual system Median Mean SE N
Hermaphroditism 2.0 1.66 0.018 1634
Monoecy 1.5 1.25 0.479 4
Gynodioecy 2.0 1.76 0.075 62
Gynomonoecy 2.0 1.96 0.023 74
Androdioecy 2.0 2.00 0.000 3
Andromonoecy 2.0 1.77 0.053 131
Trioecy 2.0 2.00 0.000 4
Heterostyly 0.0 0.86 0.404 7
"Kruskal-Wallis H = 27.22***, 8 df.
128 T HE BOT ANI CAL REVI EW
in two ot her factors: the smaller average size of flowers in monoecious species com-
pared to those of hermaphrodites, and the reduced need for stamen removal during
the pistillate phase. The former factor is i mport ant because flowers of monoecious
protogynous species were markedly smaller than flowers of monoecious protandrous
species (2.3 mm vs. 6.5 mm; SE -- 1.26, 1.29; n = 10, 13; t = 2.92**). Furthermore,
the average size of the flowers of monoecious species was considerably less than the
average size of flowers of hermaphrodites (4.1 mm vs. 11.7 mm; SE -- 1.17, 1.04; n
= 32, 537; t = 6.45***). With smaller flowers the risk of self-pollen deposition would
seem to be greater, and therefore the period of ensured freedom from self-pollen in
protogynous dichogamy may be particularly important. A second factor is that the
need for removing one set of sex organs to prevent interference with the other set in
the same flower is absent in the unisexual flowers of monoecious species. The need
for removal of such structures has, we believe, been a maj or force in the evolution
ofintrafloral protandry, and hence the absence of this selection pressure is consistent
with the more frequent protogyny in monoecious species.
Like monoecious species, andromonoecious and gynomonoecious species were
primarily protogynous interflorally (Table VI). We believe that the explanation lies
in the intrafloral prot andry of the bisexual flowers, which therefore also requires
explanation. Among andromonoecious species, the percentage ofintraflorally protan-
drous species (65.0%, n = 177) di d not differ from the percentage of species of all
breeding systems having protandrous flowers (66.2%, n = 3151), and therefore there
is no need to invoke selection pressures beyond those at work in hermaphrodites,
discussed earlier. Bisexual flowers ofgynomonoeci ous species are more often protan-
drous than in other species (94.4% protandry, n = 126). This is due to the fact that
121 of these species are in the Asteraceae, with a stereotyped mode of pollen pre-
sentation wherein pollen is released into a tube through which the pistil grows, pushing
the pollen out ahead of it. Gi ven the prevalence of intrafloral prot andry in bot h
gynomonoecious and andromonoecious species, we believe that interfloral protogyny
is favored as a means of timing stigma receptivity to ensure pollen availability, and
timing pollen release when many stigmas are available (Bell, 1971; Knuth, 1906--
1909; Miiller, 1883; Pellmyr, 1987; Schlessman, 1978, 1982; Webb, 1981). Interfloral
protogyny in an intraflorally protandrous andromonoecious species involves anther
dehiscence followed by stigma receptivity of bisexual flowers, followed by dehiscence
of anthers of male flowers. This increases the likelihood (relative to interfloral protan-
dry) that pollen release from male flowers overlaps stigma receptivity of bisexual
flowers on the same or other plants in the population. In gynomonoecious species,
similar benefits are provided by interfloral protogyny, with the sequence: stigma
receptivity of female flowers, anther dehiscence of bisexual flowers, stigma receptivity
of bisexual flowers.
Gynodioecious species were not exclusively dichogamous, as suggested by Darwin
(1888), and in fact were no more likely to be dichogamous than were other species.
Of 72 gynodioecious species, 90.3% were dichogamous, compared to 86.5% among
2333 ot her species (G = 0.94ns).
2. S e l f i n g A b i l i t y
I f dichogamy were generally or universally i mport ant as a mechanism for reducing
self-fertilization, we would predict that dichogamy should be less common in SI than
SC species, since SI species possess a physiological mechanism for limiting self-
fertilization. In fact, dichogamy was not more common in SC than in SI species
DICHOGAMY IN ANGIOSPERMS 129
(Berlin, 1993) suggesting that it is not generally a mechanism for reducing inbreeding.
When separate analyses were undertaken for intrafloral prot andry and intrafloral
protogyny, the former was associated with SI and the latter with SC (Bertin, 1993).
The greater frequency of prot andry among SI than SC species is the reverse of what
we would expect i f prot andry had evolved primarily to reduce selling. The protogyny
results are, however, consistent with a role for this form of dichogamy in reducing
selfing. This trend was also not ed by Willemstein (1987). Our results are consistent
with the suggestion by Lloyd and Webb (1986) that avoidance of self-ferlilization is
likely to have been more i mport ant in the evolution of protogyny than protandry.
However, additional factors may also contribute to this association, as not ed below.
A separate examination of pr ot ogny and protandry at the inteflioral level revealed
no difference in the incidence of either form of dichogamy in SI and SC species
(Berlin, 1993). Thus there is no basis for assuming that these forms of dichogamy
are related to avoidance of self-ferlilization.
The form of intrafloral dichogamy was related to a species' ability to self-pollinate
without a vector. Specifically, among dichogamous SC species, those capable of
autogamy were more often protogynous than were species incapable of autogamy
(59.2% vs. 40.4%; n = 228, 109; G = 10.54"*). The greater prevalence ofi nt rafl oral
protogyny in the former group presumably lies in the possibility of backup self-
pollination in such species should outcrossing fail. Such a possibility is unlikely in
protandrous species. An association between protogyny and regular self-fertilization
was suggested by Henslow (1888) without explanation. Cruden and Hermann-Parker
(1977) and Bawa and Beach (1981) not ed that the capability for backup self-polli-
nation may be an advantage of protogyny. The greater incidence of protogyny among
SC species than SI species not ed earlier results partly from the autogamous species
in the SC group. I f autogamous and unknown species are removed from the SC
category, the incidence ofprot ogyny among SC species declines from 35.4% to 32.3%,
but this is still significantly greater than the 20.9% incidence of protogyny among SI
species (n = 136, 239; G = 5.90*).
We also considered dichogamy in relation to ot her aspects of breeding system:
pollen/ovule ratios, capability for autogamy, and outcrossing rate. Not surprisingly,
species capable of selfing without a pollen vector exhibited less intrafloral dichogamy
than non-autogamous species, as suggested by Ornduff (1969) and Richards (1986).
Mean adichogamy scores for these two groups were 1.27 (SE = 0.045, n = 426) and
1.61 (SE = 0.035, n = 486), and the difference was significant (Mann-Whitney W =
172,893***).
Adichogamous species might be expected to have lower P/ O ratios than dichoga-
mous species, because of the association between autogamy and adichogamy. The
trend was in this direction (723 vs. 1396; SE = 1.5, 4.2; n = 29, 151), however the
difference was not significant (t -- 1.60ns). Protogynous species did, however, have
higher average P/ O ratios than protandrous species (2065 vs. 1130; SE = 1.2, 1.2; n
= 53, 98; t -- 2.06*). This observation is consistent with the idea not ed above that
protogyny is the form of dichogamy likely to be particularly effective at avoiding
selfing or pollen-stigma interference. Species in which outcrossing makes a particu-
larly large contribution to fitness would be expected to have effective means of
avoiding selfing and pollen-pistil interference, as well as high P/ O ratios (Cruden,
1977).
Intraflorally, adichogamous species have lower outcrossing rates than dichogamous
species (Table VIII; t = 2.32", 55 df). This is not surprising in view of the earlier-
not ed association between adichogamy and autogamy. Protandrous and protogynous
130
THE BOTANICAL REVIEW
Tabl e VI I I
Di chogamy and out crossi ng rat e
Outcrossing Rate"
Type of dichogamy Mean Median SE N
All species
Protandry 5.2 7.0 0.70 28
Protogyny 3.2 1.0 1.27 9
All dichogamy 4.7 6.0 0.62 37
Adichogamy 2.6 1.0 0.70 20
SC species
Protandry 4.8 5.0 1.02 16
Protogyny 2.3 1.0 1.41 6
Adichogamy 2.7 1.0 0.83 14
9 Outcrossing rates were scored on a scale of 0 to 9, with 0 = 0--10% outcrossing and 9 = 90-
100% outcrossing.
species do not , however, differ i n t hei r average out crossi ng rates (t = 1.37ns, 35 df).
These out crossi ng rates may not pr ovi de a part i cul arl y good measur e o f t he effect o f
t ype o f di chogamy on out crossi ng because so ma ny ot her aspects o f floral bi ol ogy
are likely t o influence out crossi ng rate, such as her kogamy, SI, and t he at t ract i veness
and rewards o f t he flowers. I f we consi der onl y SC species, pr ot andr y appears mor e
effective at pr omot i ng out crossi ng t han does pr ot ogyny (Table VIII), but because o f
t he small sampl es and ot her uncont r ol l ed variables, we at t ach little i mpor t ance t o
t hi s result.
E. DICHOGAMY AND FLORALBIOLOGY
1. Fl ower Si ze
Int rafl oral l y di chogamous species bore flowers o f a slightly larger average size t han
adi chogamous species (11.5 mm vs. 9.7 mm; SE = 1.04, 1.07; n = 607, 199; t --
2.09*). Thi s difference ma y be rel at ed t o t he preval ence o f species t hat are largely
selfed i n t he f or mer group. Whe n species habi t ual l y sel f-pol l i nat ed and t hose capabl e
ofsel fi ng wi t hout a vect or were el i mi nat ed f r om t he sampl e, t he sizes of di c hoga mous
and adi chogamous flowers di d not differ significantly (10.9 mm vs. 10.6 mm; SE =
1.09, 1.05; n = 510, 138; t -- 0.74ns).
Amo n g species wi t h intrafloral di chogamy, flowers o f pr ot ogynous species were
slightly larger t han flowers o f pr ot andr ous species (Table IX). Mos t o f this difference
Tabl e IX
Fl ower size (di amet er i n mm) and di chogamy
Intrafloral a Interfloral ~
Mean SE N Mean SE N
Protandry 10.3 1.05 382 15.7 1.28 21
Protogyny 13.9 1.08 225 2.6 1.22 28
" For intrafloral dichogamy t = 3.24**.
b For interfloral dichogamy t = 5.56***.
DI C HOGAMY I N ANGI OS P E RMS 131
reflects the greater frequency of large, beetle-pollinated flowers in the former group.
I f species known to be beetle-pollinated are eliminated from bot h groups, the dif-
ference becomes only marginally significant (t = 1.99, P = 0.047). Even so, this result
does not support Wilson' s (1878) suggestion that more conspicuous flowers are espe-
cially likely to be protandrous. Among species exhibiting interfloral dichogamy, how-
ever, flowers of protogynous species were markedly smaller than flowers of protan-
drous species (Table IX). Miiller (1883) and Henslow (1888) suggested an association
between protogyny and small, inconspicuous flowers. They seem to have viewed the
association in terms of the greater likelihood of self-fertilization in smaller flowers,
which they feel will be promot ed by protogyny (perhaps as a fail-safe mechanism).
This would apply intraflorally for the most part, and we found no size differences at
this level. Our interfloral difference is unrelated to wind pollination, as only 2 of 37
species in the sample were wind-pollinated. A possible explanation of the interfloral
pattern is that in inflorescences of smaller flowers the greater separation of functions
afforded by protogyny becomes more i mport ant because of possible contamination
with self-pollen from adjacent flowers. This explanation requires some synchrony of
the stages among flowers within inflorescences.
2. Phenology
Species flowering earlier in the year were disproportionately protogynous. For this
analysis, only species in north-temperate regions were used. Of species starting flow-
ering in January through April, 62% exhibited intrafloral protogyny, compared to
only 37% of those flowering later in the year (G = 32.80***; n = 167,628, respectively).
The same result obtains i f early flowering is considered to extend through May. These
results contrast with those of Lloyd and Webb (1986) based on a smaller sample of
62 species from the Biological Flora of the British Isles. We found little difference
between early- and late-flowering species with regard to interfloral dichogamy.
An association between early flowering and protogyny was not ed by Henslow
(1888), citing such genera as Helleborus, Prunus, Crataegus, Aesculus and Mandra-
gora. He suggested that cold temperatures often check the growth of corolla and
stamens without affecting the pistil, of which we have no evidence. Bawa and Beach
(1981) suggested instead that early spring blooming implies pollinator unpredictabili-
ty (e.g., Schemske et al., 1978), and that protogyny permits subsequent selfing should
outcrossing fail under such conditions (see also Cruden & Hermann-Parker, 1977).
This seems reasonable, but cannot be evaluated with our data. We do note that wind-
pollinated species (which are disproportionately protogynous) did not differ from
other species in their average flowering times. From the taxonomic viewpoint, mem-
bers of the Magnoliidae and Hamamelidae were disproportionately represented among
early bloomers and members of the Asteridae were disproportionately represented
among late bloomers. The former groups are relatively protogynous, while the As-
teridae is relatively protandrous. Thus there may be some phylogenetic basis to the
observed patterns.
3. One-Day Flowers
The percentage of species with intrafloral prot andry (48.8%) among 43 species with
one-day flowers did not differ from the percentage (54.2%) of 216 species with flowers
lasting two or more days (G = 0.40ns). Patterns of interfloral dichogamy and flower
duration were likewise independent.
132 THE BOTANICAL REVIEW
Bawa and Beach (1981) suggested that prot andry should be common in one-day
flowers, reasoning that the female phase of a protogynous flower would be useless in
one-day flowers unless pollinators carry appreciable amounts of pollen from the
previous day. Our rejection of this hypothesis could have several causes. One is that
pollinators may indeed carry viable pollen overnight. A second is that the duration
of the female phase may be bri ef enough, and flower times sufficiently staggered, that
pollen is available for all but the earliest-opening flowers. Finally, our small sample
of species with one-day flowers may simply be inadequate to provide a sufficiently
powerful test of this hypothesis.
4. Stamen Signals and Rewards
Intrafloral protogyny was not more common in species whose stamens are asso-
ciated with signals or rewards than in other species (G = 1.04ns; n = 29, 3227).
However, among species whose pollinators consume pollen, protogyny was more
common than among other species (47.4% protogyny, n = 443; 30.4% protogyny, n
= 2813, respectively; G = 48.16***).
Lloyd and Webb (1986) argued that where stamens provide either attractants or
rewards to pollinators, the necessity for keeping the stamens intact throughout an-
thesis favors protogyny. Implicit in their argument is the expectation that such re-
wards and attractants will be available before the male phase begins, but would not
be available after it ends. The lack of support for their prediction in species that
provi de staminate rewards other than pollen may reflect our small sample size, or
may suggest a reevaluation of the argument' s premises. In fact we can think of no
clear reason to expect stamen rewards to function primarily before pollen release
rather than after.
The greater prevalence of protogyny among pollen-reward species is surprising
from the viewpoint of pollinator attraction, because only with prot andry will a reward
potentially be present during the female phase. The observed pattern contrasts with
Richards' s (1986) statement that "pollen flowers are almost never protogynous. "
Among 58 pollen-reward species that provide no nectar, 34.5% were protogynous,
a slightly higher proportion than in the overall sample. Perhaps the activities of
pollen-gatherers (e.g., buzz pollinators) are more likely to result in considerable self-
pollination than the activities of nectar-feeders. Thus the advantages of avoiding
selfing or pollen-pistil interference may be sufficient to offset potentially lower pol-
linator visitation caused by lack of rewards during the female phase of a protogynous
flower.
Our data support van der Pi j rs (1978) suggested association between pollen flowers
and adichogamy. Among the 58 pollen-reward species in our sample, 40% were
adichogamous, compared to 14% in the entire sample (n -- 3785, G = 22.69***).
Presumably the greater incidence of adichogamy in pollen-reward flowers reflects the
importance of pollen in attracting pollinators during stigma receptivity.
5. Removal of Sexual Structures
Sexual parts that abscise, move or shrivel (remove) after presentation were usually
presented first. Among 73 species wherein pistil removal was observed 47.9% were
protogynous, compared to 32.3% of 3183 other species (G = 7.50**). Similarly, 89.1%
of 110 species with anther removal were protandrous, compared to 66.6% among
DICHOGAMY IN ANGIOSPERMS 133
the remaining 3146 species (G = 29.42***). It is quite possible, however, that ob-
servers are more likely to record removal of the first-produced sporophylls than the
second-produced sporophylls simply because the former event often takes place
during flowering, while the latter may not occur until later, perhaps after observations
have been concluded.
Lloyd and Webb (1986) suggested that flowers wherein the removal of androecia
is easier than removal ofgynoeci a should present their stamens before their stigmas.
The reverse should be true i f gynoecia are easier to remove than androecia. Thus
the easily-removed structures can present themselves, and then avoi d interference
with structures representing the other gender. In our sample, species wherein pistil
removal was not ed were disproportionately protogynous, and those wherein stamen
removal was not ed were disproportionately protandrous. As Lloyd and Webb (1986)
observed, stamens will generally be easier to remove than pistils, because the male
function is ephemeral. Therefore this selective pressure may be an i mport ant reason
why prot andry is more common overall than protogyny. This selective pressure would
be of little or no importance interflorally, which may partly explain the low incidence
of interfloral protandry.
6. Stigma and Anther Exsertion
We found no consistent relationship between relative exsertion of stigma and
anthers and the type of dichogamy. Of 130 species wherein the stigma projected
furthest, 40.8% were protogynous, compared to 32.3% of ot her species (G = 5.90*).
But among species wherein anthers projected furthest, 42.9% were protandrous,
compared to 67.5% of ot her species (G = 7.12**; n = 29). When all data on species
wherein the furthest-projecting structure was recorded (n = 158) were combined into
a single contingency table, the projecting structure was independent of kind ofdi chog-
amy (G = 2.50ns).
Selection to avoi d pollen-pistil interference should lead to the furthest-projecting
sporophyll being presented second, according to Lloyd and Webb (1986). Our results
on this point are equivocal, with the expected tendency among species with anthers
projecting furthest, but not among species with stigmas projecting furthest. Perhaps
this reflects an asymmet ry in the ability of male and female functions to interfere
with one another. Stamens projecting beyond the stigma and presented first would
seem very likely to cause some pollen to be deposited intraflorally, with attendant
problems either from self-fertilization or from pollen-pistil interference. In contrast,
a stigma projecting beyond the anthers is not likely to result in intrafloral deposition
of self pollen. Further, unless it is very large or feathery (as in wind-pollinated species)
it may not interfere much with pollen export. No association between relative exser-
tion and synchronous complete dichogamy was observed by Cruden (1988).
7. Facilitation
Among species in which the sexual organs of one gender facilitate the other sexual
function, the organs of the facilitating function were almost invariably presented
second. Eight hundred and sixteen species exhibited female facilitation, mostly in-
volving presentation of pollen on the stigma, as in the Asteraceae, Campanulaceae
and Proteaceae. Of these, 99.8% were protandrous, while only 56.5% of ot her species
were protandrous (G -- 745.24***). We found no cases of male facilitation.
134 THE BOTANICAL REVIEW
Lloyd and Webb (1986) argued that species with secondary pollen presentation
should be protandrous because protogyny or adichogamy would result in automatic
self-pollination and interference between pollen receipt and pollen removal. Our data
are in striking agreement with this prediction.
8. Relationship Between Intrafloral and
Interfloral Dichogamy
There is a marked pattern of association between the types of intrafloral and
interfloral dichogamy in diclinous species. A G-test for andromonoecious species
indicates a significant association between these two variables (G = 6.32"), with 83%
of 66 intraflorally protandrous, compared to 56% of 16 intraflorally protogynous
species. All of 73 gynomonoecious species examined combined intrafloral protandry
with interfloral protogyny.
These patterns are consistent with Webb's (1981) view that sexual selection may
be important in causing anther dehiscence at times when stigmas are available. In
an andromonoecious species with protandrous perfect flowers, for example, one
would expect male flowers to be borne largely after the perfect ones, to take advantage
of fertilization opportunities afforded by the female phases of the perfect flowers
(Bell, 1971; Knuth, 1906-1909; Mtiller, 1883; Pellmyr, 1987; Schlessman 1978,
1982). This selection pressure may also contribute to the higher incidence ofdichoga-
my among monoecious, gynomonoecious and andromonoecious species than among
hermaphrodites, as suggested by Pellmyr (1987). Of 2008 hermaphrodites in our
sample, 85.6% were dichogamous. In contrast, of 515 species in other categories,
99.0% exhibited interfloral dichogamy and 93.0% of 199 species had intrafloral
dichogamy.
Lovett Doust (1980) has argued that the combination of intrafloral protandry and
interfloral protogyny could be a means of minimizing resource competition between
male and female functions. However, it is by no means clear that such patterns avoid
competition because the time of female flowering may not coincide with the time of
maximal female demand on resources. Such demand may be greatest at a later time,
during ovary enlargement. The timing of resource use by male and female functions
would have to be determined to evaluate this hypothesis adequately.
F. DICHOGAMY AND POLLINATION
Species with different pollen vectors differed in their intrafloral dichogamy scores
(Table X), but not in their interfloral dichogamy scores (Kruskal-WaUis H = 5.54ns).
Wind-pollinated species were most protogynous, and bird-pollinated species were
most protandrous. There was a significant difference among pollen vectors in in-
trafloral adichogamy score (Table X), with autogamous species showing the greatest
adichogamy.
The different groups of insect-pollinated plants showed significant differences both
in intrafloral and interfloral dichogamy (Table XI, XII). All species had average
intrafloral scores between 2.0 and 3.0 except species pollinated by beetles, which
were markedly protogynous, and species pollinated by butterflies and moths, which
were largely protandrous. Intrafloral adichogamy scores also exhibited significant
variation among groups, with moth-pollinated species least dichogamous and beetle-
pollinated species most dichogamous (Table XI). In contrast, Willemstein (1987)
found moth- and butterfly-pollinated species to have the lowest frequency of adi-
DICHOGAMY IN ANGIOSPERMS
Table X
Pat t er ns o f i nt r af l or al di c hoga my i n r el at i on t o mode o f pol l i na t i on
135
Dichogamy S c o r e s " Adichogamy S c o r e s b
Median Mean SE N Median Mean SE
Autogamy 3.0 3.21 0.130 90 1.0 0.86 0.096
Insects 2.0 2.47 0.049 1071 2.0 1.48 0.025
Birds 1.5 3.87 0.159 120 2.0 1.85 0.047
Mammal s 1.0 2.18 0.519 11 2.0 1.73 0.195
Water 1.0 1.00 - - 1 2.0 2.00 - -
Wi nd 5.0 4.23 0.102 150 2.0 1.61 0.060
a Dichogamy Kruskal-Wallis H = 200.05***.
b Adichogamy Kruskal-Wallis H = 85.85***.
chogamy. Speci es di d not di ffer wi t h r egar d t o i nt er f l or al a di c hoga my ( Kr us kal - Wal l i s ;
H = 12.83ns).
I. Wind Pollination
Pr ot ogyny was mor e c o mmo n a mong wi nd- pol l i na t e d speci es t han a mong a ni ma l -
pol l i nat ed speci es at t he i nt r af l or al but not t he i nt er f l or al l evel . At t he f or mer l evel ,
88. 5% o f wi nd- pol l i na t e d speci es wer e pr ot ogynous , c o mp a r e d t o 34. 8% o f speci es
known t o have ot her mode s o f pol l i nat i on (G = 203.72***; n = 187, 1353). I nt er -
f l or al l y t her e was no di fference (G = 2. 16ns; n = 111, 204) .
Wi nd- pol l i na t e d speci es wi t h bi sexual fl owers wer e not necessar i l y mor e di choga-
mous t han a ni ma l - pol l i na t e d speci es, as suggest ed by Ke r ne r von Ma r i l a un (1895)
a nd Wi l l e ms t e i n (1987). Of wi nd- pol l i na t e d he r ma phr odi t e s 82. 8% wer e di choga-
mous, c o mp a r e d t o 79. 6% o f ot her speci es (G --- 1.26ns). Fur t he r mor e , t he per cent ages
o f wi nd- pol l i na t e d a nd ot her speci es exhi bi t i ng no ove r l a p o f sexual functions wer e
not si gni f i cant l y di f f er ent (13. 0% vs. 9.0%; n = 69, 702; G = 1.14ns). I t ha d been
suggest ed t hat a gr eat er s epar at i on o f sexual f unct i ons i n wi nd- pol l i na t e d speci es
woul d r esul t f r om t he gr eat er l i kel i hood o f de pos i t i on o f sel f - pol l en owi ng t o t he
i mpr e c i s i on o f wi n d - me d i a t e d pol l en t r ansf er .
An associ at i on bet ween pr ot ogyny and wi nd- pol l i nat i on was not ed by MOiler (1883),
Table XI
Pat t er ns o f i nt r af l or al di c hoga my i n i ns ect - pol l i nat ed speci es
Dichogamy ~ Adichogamy ~
Median Mean SE N Median Mean SE
Bees 1.0 2.39 0.082 388 2.0 1.53 0.041
Hies 2.0 2.37 0.156 95 2.0 1. 45 0.079
Wasps 1.0 2.29 0.714 7 2.0 1. 86 0.143
Beetles 5.0 4.72 0.192 29 2.0 2.00 0.000
Butterflies 1.0 1. 73 0.256 22 2.0 1.54 0.171
Moths 3.0 2.43 0.248 30 1.5 1.10 0.175
Bees and flies 3.0 2.66 0.134 145 2.0 1. 42 0.069
Butterflies and moths 1.0 1. 67 0.373 9 2.0 1. 55 0.242
Dichogamy Kruskai-Wallis H = 57.55"**.
b Adichogamy Kruskal-Wallis H = 24.28***.
136 THE BOTANICAL REVIEW
Table Xl I
Patterns of interfloral dichogamy in insect-pollinated
species"
Pollinator Median Mean SE N
Bees 5.0 4.26 0.213 54
Hies 5.0 4.37 0.308 19
Wasps 5.0 4.82 0.182 22
Beetles 5.0 4.84 0.160 25
Butterflies 1.0 1.00 0.000 1
Moths 5.0 5.00 -- 1
Bees and flies 5.0 3.75 0.479 16
Butterflies and moths 5.0 5.00 -- l
a Kruskal-Wallis H = 18.83".
Behrens (1885), Henslow (1888), Lloyd and Webb (1986), Willemstein (1987) and
Cruden (1988). Lloyd and Webb (1986) attributed this pattern in part to the lack of
a need in such species for sturdy stigmas and styles to withstand the movement s of
animal vectors. Consequently the stigmas and styles of wind-pollinated species are
more easily disposed of after pollination, making protogyny a more likely option for
avoiding pollen-stigma interference. An additional possibility reflects the imprecise
nature of pollen transfer by wind. Under such circumstances, protogyny may well
be more effective at avoiding the deposition of self pollen (Faegri & van der Pijl,
1979; Ll oyd & Webb, 1986; Willemstein, 1987).
2. Biotic Pollination
Among animal-pollinated species, intrafloral protandry was more common than
intrafloral protogyny (865 vs. 437 species, G - 143.34"**). The reverse was true at
the interfloral level (29 vs. 171 species; G = 111.68"**).
Lloyd and Webb (1986) found a two-fold excess of protandry among animal-
pollinated species from the Biological Flora of the British Isles, although they did
not distinguish intrafloral and interttoral categories. Willemstein (1987) and Cruden
(1988) also not ed an association between protandry and animal pollination, and
Behrens (1885) not ed the same for insect pollination. The intrafloral pattern in our
data could be explained by any of the arguments used to explain the greater abundance
of pr ot andr y than protogyny among all species. Also, as suggested by Lloyd and Webb
(1986), the relative ease of removal of male and female structures may differ between
wind- and animal-pollinated species, favoring early presentation of pollen in the
latter. We concur with Lloyd and Yates (1982) that removal of male structures is
often easier than removal of female structures in animal-pollinated species. Addi-
tionally, in those species with vertical, acropetally-maturing inflorescences that are
visited by upwardly-foraging vectors, prot andry confers additional benefits as not ed
below (Best & Bierzychudek, 1982; Darwin, 1862; Lloyd & Webb, 1986; Pyke, 1978;
Wyatt, 1983).
3. Bee and Fly Pollination
In comparison to plants pollinated by other vectors, bee- and fly-flowers were more
often protandrous at the intrafloral level (56.9% vs. 39.6%; n = 824, 1129; G =
55.00***). This supports Wyatt' s (1983) contention that prot andry is the domi nant
DICHOGAMY IN ANGIOSPERMS 137
form of dichogamy among plants pollinated by bees and flies, which he attributed
to the tendency of such species to move upwards when they forage (see vertical
inflorescences, below). As predicted, the percentage of prot andry among bee/fly spe-
cies with vertical, acropetally-maturing inflorescences (78.0%) was significantly great-
er than the percentage of prot andry among bee/fly species with non-vertical inflo-
rescences (61.9%; G -- 4.38*; n = 41, 307).
4. Beetle Pollination
There was a significant association between beetle pollination and intrafloral pro-
togyny. Of 37 beetle-pollinated species, 89.2% were protogynous, compared to only
32.7% of 3255 other species (G = 51.02"**). The trend was similar at the interfloral
level (96.0% vs. 77.7%; n = 25, 561; G = 6.52*). The results were unchanged at bot h
levels i f trap and brood blossoms were excluded.
An association between protogyny and beetle pollination was not ed by Gottsberger
(1977), Faegri and van der Pijl (1979), Bawa and Beach (1981), and Wyatt (1983).
The association partly reflects the tendency of many beetles to visit trap blossoms.
Typically the beetles enter blossoms during their female phase on one day, remain
there overnight, then emerge dusted with pollen from the male phase flowers on the
next day (Bawa & Beach, 1981; Proctor & Yeo, 1972). However, since a significant
association between beetle pollination and protogyny remained even when trap and
brood species were excluded, we must seek additional explanations. I f the habitual
view of unspecialized beetles as inefficient pollinators is correct, the results may
reflect Bawa and Beach' s (1981) suggestion that unreliable pollination favors pro-
togyny over prot andry to provide backup self-pollination for failed cross pollination.
Alternatively, it may not be the failsafe aspects of protogyny that are important, but
rather that in cases of incomplete dichogamy, protogyny is simply more effective
than protandry at separating the sexual functions (Bernhardt & Thien, 1987; Lloyd
& Webb, 1986). This becomes especially critical i f pollen transfer is imprecise and
therefore herkogamy is less effective at preventing intrafloral pollen transfer (Bawa
& Beach, 1981; Willemstein, 1987). Consistent with this view is the greater frequency
of dichogamy among beetle-pollinated species than among those visited by other
vectors (Table XI).
5. Trap and Brood Species
Trap and brood species were invariably protogynous. All 33 trap and brood species
exhibiting interfloral dichogamy were protogynous, compared to 81.4% of 311 ot her
species (G = 140.38"**). Similarly, all 16 trap and brood species with intrafloral
dichogamy were protogynous, compared to only 30.2% of 2012 species known not
to be trap or brood species (G = 37.97***).
Trap and brood blossoms are occupied for a more or less extended period by a
pollinator. Many authors have observed that protogynous devel opment will either
facilitate cross-fertilization or reduce pollen-pistil interference (Dafni, 1984; Faegri
& van der Pijl, 1979; Lloyd & Webb, 1986 and references therein). Our data are
wholly in line with the expectation ofprot ogyny, and the species involved cut broadly
across taxonomic lines, including members of the Araceae, Nymphaeaceae and Mora-
ceae. This is one of the few cases of marked congruence between patterns at the
interfloral and intrafloral levels, no doubt reflecting the functional equivalence of
trap flowers and trap inflorescences.
138 THE BOTANICAL REVIEW
6. Frequency of Visitation
The presence of dichogamy was associated with frequency of visitation among
insect-pollinated species. Those species that are habitually self-fertilized were more
often adichogamous than those primarily pollinated by insects (49.5% vs. 19.8%; n
= 99, 1453; G = 40.02***).
The greater frequency of adichogamy among species that receive few visits (desig-
nated autogamous in our sample) is to be expected (Ornduff, 1969). Arguments for
temporal separation of sexual functions to reduce inbreeding or pollen-pistil inter-
ference become superfluous in these species.
7. Upwardly-Moving Vectors on Vertical Inflorescences
Species with vertical acropetally-maturing inflorescences that are pollinated by
vectors thought to forage upwards (bees, flies; Proctor & Yeo, 1972; Wyatt, 1983)
typically exhibited intrafloral protandry. Of 34 bee- or fly-pollinated species with
vertical, acropetaUy-maturing inflorescences, 88.2% were protandrous, compared to
only 28.2% of 39 species with other pollen vectors (G - 29.06***). Considered another
way, of bee- and fly-pollinated species, protandry was more common among those
with vertical, acropetaUy-maturing inflorescences than among those with other types
of inflorescences (78.0% vs. 61.9%; n = 41, 307; G = 4.38*).
Protandry in acropetally-maturing vertical inflorescences has been interpreted both
as a means of promoting outcrossing and as a means of preventing pollen-pistil
interference (Best & Bierzychudek, 1982; Catling, 1983; Darwin, 1862; Faegri & van
der Pijl, 1979; Lloyd & Webb, 1986; Pyke, 1978; Wilson, 1878; Wyatt, 1983). Our
data provide strong support for the association ofprotandry and acropetal maturation
in vertical inflorescences visited by pollinators thought to forage upwards. Our result
does not, however, rule out explanations other than avoidance of selfing or pollen-
stigma interference in explaining this pattern (Corbet et al., 1981; Lloyd & Webb,
1986). Unfortunately our sample contains insufficient data on basipetaUy-maturing
inflorescences and those visited by downwardly-moving vectors to test for an asso-
ciation between these characteristics.
G. LIMITATIONS OF OUR STUDY
There are several difficulties to be considered in evaluating the conclusions of this
study. First there are limitations in the accuracy of the data, arising from several
sources. Our data are likely to vary in quality. For example, most workers deduce
stigma receptivity based on the appearance of the stigma rather than any chemical
tests or experimental pollinations. Stigma appearance is often a useful indicator of
receptivity, but it may not always be. Our unit of data collection was the species,
but different populations of a given species sometimes exhibit different temporal
relationships of stigma receptivity and anther dehiscence (AI-Shehbaz, 1977; Knuth,
1906-1909; Percival, 1965; Philipp, 1985; Schoen, 1977), and environmental factors
may also influence these patterns (Pistolesi et al., 1986). There may also be errors
in transcribing data, given the large size of the data set. We checked all data in the
computer file against the original data sheets, but we have only spot checked original
references against the computer file. The low incidence of detected errors suggests
that undetected errors will not influence our major findings.
DICHOGAMY IN ANGIOSPERMS 139
Many of the analyses performed in this study were tests of independence. Such
tests assume independence of the included species. Yet pairs of species share varying
lengths ofphylogenetic history, and therefore violate this assumption of independence
(Clutton-Brock & Harvey, 1984; Felsenstein, 1985). Unfortunately, the detailed and
accurate phylogenies that would be needed to eliminate redundancy in the data are
not yet available, and therefore the sort of analysis advocated by Donoghue (1989)
is not yet practical. We hope that as more accurate phylogenies become available,
our analyses can be modified to incorporate this information.
A further difficulty in our analyses is dealing with correlated variables. Ideally a
multifactorial approach should be used, so that in analyzing the relationship between
a particular variable and dichogamy, the effects of all potentially confounding var-
iables are controlled. We have not opted for this approach because the data on each
species is to some degree incomplete, meaning the number of species for which, for
example, we have complete data on five or six maj or variables is limited. A multiway
contingency table would have many cells that were empt y or contained samples too
small for analysis. We have tried to compensate for our inability to take a multifac-
torial approach by considering the effects of possible correlations of variables in
interpreting our results.
H. AVOIDANCE OF SELFING VS. AVOIDANCE OF
POLLEN-PISTIL INTERFERENCE
Two maj or competing explanations for the evolution and maintenance ofdichoga-
my are that dichogamy aids in avoiding self-fertilization and the attendant costs of
inbreeding depression, and that dichogamy avoids the detrimental effects of pollen-
pistil interference. A maj or problem in distinguishing these two explanations is that
most of the predictions that they yield are identical.
For example, acropetally-maturing vertical inflorescences visited by upwardly-
moving vectors were predicted to have protandrous flowers (Lloyd & Webb, 1986)
so that outcross pollen "i s deposited without interference or competition from self-
pollen, and pollen is subsequently picked up without being obstructed by flowers."
Nevertheless, this pattern could also be favored as a means of reducing self-fertiliza-
tion (Richards, 1986). Thus our demonstration of the predicted pattern does not help
us to distinguish between these two alternatives. The early presentation of easily-
moved structures and the presence of protogyny in trap and brood blossoms could
also be predicted in terms of advantages related to avoidance of either inbreeding or
pollen-stigma interference.
The only prediction we can think of that effectively distinguishes these two ex-
planations relates to pattern of self-fertility. Specifically, i f avoidance of selfing has
been the maj or selective force in the evolution ofdichogamy, we predict that dichoga-
my should be more common in SC than in SI species, because in the latter group,
selling is prevented by a physiological barrier and dichogamy would be irrelevant in
this regard. On the other hand, dichogamy could be advantageous in avoiding pollen-
pistil interference in either SC or SI species, and therefore we would not expect the
incidence ofdi chogamy to differ between SI and SC species. In fact, $I and SC species
do not differ in incidence of either prot andry or protogyny at the interfloral level
(Bertin, 1993). At the intrafloral level only protogyny is more common among SC
than SI species (Bertin, 1993). Thus intrafloral protogyny is the only form ofdichoga-
my for which avoidance ofselfing seems to have been an i mport ant selective pressure.
140 THE BOTANICAL REVIEW
While avoidance of selfing has long been considered important in the evolution of
floral biology, considerations of pollen-pistil interference have been more recent.
This phenomenon is the interference between male and female functions as a result
of deposition of self-pollen or other factors. Detrimental effects on female function
may occur because self-pollen restricts access of cross-pollen to the stigma, interferes
with the growth of cross-pollen tubes, or reduces access of cross-pollen tubes to the
ovules. Negative effects on the male function can result because pollen deposited
within a flower is unavailable for export. Pollen-pistil interference is sometimes
referred to as stigma clogging (Shore & Barrett, 1984) or pollen-stigma interference
(Bertin & Sullivan, 1988). We prefer the designation pollen-pistil interference because
the interference may involve parts of the pistil other t han the stigma.
An important reason for the difficulty of distinguishing self-fertilization from pol-
len-pistil interference as important selective pressures is that both typically involve
self-pollination. Deposition of self-pollen is a necessary prerequisite of self-fertiliza-
tion, and most forms of pollen-pistil interference also involve deposition of self-
pollen. (Some do not, such as carpel expansion interfering with anther positioning.)
Thus adaptations for avoidance of self-pollination may have been favored because
of advantages related to avoidance of either inbreeding or pollen-pistil interference.
While we agree with Lloyd and Webb (1986) and Webb and Lloyd (1986) that
pollen-pistil interference is a neglected and potentially very important selective force
acting on floral biology, we resist embracing it at this time as a general explanation
for dichogamy because of the lack of empirical study. Only a handful of studies has
considered the potential effects of pollen-pistil interference on female success, and
fewer still have found detrimental effects (Barrett & Glover, 1985; Bertin & Sullivan,
1988; Broyles & Wyatt, 1993; Ockendon & Currah, 1977; Palmer et al., 1989; Shore
& Barrett, 1984). Only one study has apparently examined effects of pollen-pistil
interference on male success (Kohn & Barrett, 1992). They found no effect of style
removal on siring ability of the long-styled morph oftristylous Eichhornia paniculata.
Additional studies are needed to establish the frequency of occurrence and magnitude
of effects of pollen-pistil interference in natural populations.
IV. Conclusions
We adhere to the view expressed by Lloyd and Webb (1986) that multiple selection
pressures are likely to be responsible for the evolution and maintenance ofdichogamy.
In this paper we have shown an association between dichogamy and numerous
ecological or life history attributes. We believe that most or all of these associations
can be attributed to three factors.
Avoidance of self-fertilization does not have the universal importance in the evolu-
tion of dichogamy that is often attributed to it. Our results are, however, consistent
with a role for selfing avoidance in the evolution ofintrafloral protogyny. We believe
that this pattern partly underlies the greater prevalence of protogyny in SC species
than in SI species.
We tentatively conclude that avoidance of poUen-pistil interference has been the
most important factor in the evolution of dichogamy, a conclusion consistent with
the predictions of Lloyd and Webb (1986). Our conclusion is tentative because of
the difficulties noted earlier in distinguishing effects of selection for avoiding self-
fertilization from selection for avoiding pollen-pistil interference. We emphasize the
latter factor because of the similar incidence of most forms of dichogamy among SI
DICHOGAMY IN ANGIOSPERMS 141
and SC species. I f our conclusion is correct, selection for avoidance of pollen-pistil
interference is likely to have been i mport ant in the (l ) greater prevalence of pr ot andr y
than protogyny, (2) more frequent prot andry in acropetally-maturing vertical inflo-
rescences visited by upwardly-moving vectors, (3) (perhaps in conjunction with
avoidance of selfing) higher prevalence of protogyny in wind-pollinated, beetle-pol-
linated and trap and brood species, and (4) prevalence of prot andry in species with
secondary presentation of pollen on stigmas or styles.
Selection for relative timing of male and female functions to secure effective fer-
tilization may have been i mport ant in two contexts. First, it appears to have selected
for contrasting patterns of intrafloral and interfloral dichogamy in diclinous species.
It may also have contributed to selection for protogyny rather than prot andry in
dichogamous species capable of autogamy and those flowering early in the year when
pollinators may be unreliable. In bot h such circumstances protogyny combines an
initial period when the sexual functions are separated, with a subsequent period of
potential overlap that allows backup self-pollination.
While the distinction between interfloral and intrafloral dichogamy has often been
recognized, these levels have often been lumped in analyzing data. Our results show
that such a treatment of data is inappropriate. The incidence of prot andry and
protogyny differs at the two levels, as do correlations between form of dichogamy
and various ecological and life history attributes. Therefore it appears that the relative
importance of different selection pressures differs at the two levels, and they should
be treated separately in the future.
While several selection pressures potentially i mport ant in the evolution ofdichoga-
my have been identified, other patterns of distribution of dichogamy appear to have
a taxonomic basis. While it is certainly possible that unconsidered ecological factors
underlie these patterns, several of t hem remain even when effects of known ecological
factors are controlled. Some of the patterns that appear to reflect phylogeny are (1)
the tendency for members of many families to be clustered around protandry, pro-
togyny or adichogamy, (2) the greater incidence of protogyny among monocot s than
dicots, and (3) the marked incidence of protogyny in the Magnoliidae and Hama-
melidae and of prot andry in the Asteridae.
V. Acknowl edgments
We thank S. C. H. Barrett, A. Dafni, E. A. James, C. E. Galen, J. D. Karron, C.
M. McCall, M. J. McKone, R. J. Mitchell, C. Murcia, S. S. Renner, M. A. Schlessman,
S. R. Seavey and A. G. Stephenson for supplying us with unpublished information
or references. We are also grateful to A. Dafni, D. G. Lloyd, E. E. Lyons, O. Pellmyr
and M. A. Schlessman for helpful discussion or comment s on earlier versions of this
manuscript. A.-L. Bellenger and G. R. Hoffmann kindly assisted in preparing the
French abstract, and K. Prestwich in preparing the figure. A sabbatical leave from
Hol y Cross College provi ded time for much of this work.
VI. Literature Cited
AI-Shehbaz, I.A. 1977. Protogyny in the Cruciferae. Syst. Bot. 2: 327-333.
Barrett, S. C. H. & D. E. Glover. 1985. On the Darwinian hypothesis of the adaptive signif-
icance of tristyly. Evolution 39: 766-774.
142 THE BOTANICAL REVIEW
Bawa, K. S. & J. H. Beach. 1981. Evolution of sexual systems in flowering plants. Ann.
Missouri Bot. Gard. 68: 254-274.
Behrens, W. J. 1885. Text-book of general botany. Young J. Pentland, Edinburgh.
Bell, C.R. 1971. Breeding systems and floral biology of the Umbelliferae. Pages 93-107 in
V. H. Heywood (ed.), The biology and chemistry of the Umbelliferae. Academic Press,
New York.
Bennett, A. W. 1870. Observations on protandry and protogyny in British plants. J. Bot. 8 :
315-321.
B e r n h a r d t , P. & L. B. Thien. 1987. Self-isolation and insect pollination in the primitive
angiosperms: New evaluations of older hypotheses. PI. Syst. Evol. 156:159-176.
Bertin, R. I. 1993. Incidence of monoecy and dichogamy in relation to self-fertilization in
angiosperms. Amer. J. Bot. 80 (in press).
- - & M. Sullivan. 1988. Pollen interference and cryptic self-fertility in Campsis radicans.
Amer. J. Bot. 75:1140-1147.
Best, L. S. & P. Bierzychudek. 1982. Pollinator foraging on foxglove (Digitalis purpurea): A
test of a new model. Evolution 36: 70-79.
Brantjes, N. B. M. 1982. Pollen placement and reproductive isolation between two Brazilian
Polygala species (Polygalaceae). P1. Syst. Evol. 141: 21-52.
Broyles, S. B. & R. Wyatt. 1993. The consequences of self-pollination in Asclepias exaltata,
a self-incompatible milkweed. Amer. J. Bot. 80: 41--44.
Burtt, B. L 1977. Aspects of diversification in the capitulum. Pages 41-59 in V. H. Heywood,
J. B. Harborne & B. L. Turner (eds.), The biology and chemistry of the Compositae. Vol.
1. Academic Press, London.
Carlquist, S. 1976. Tribal interrelationships and phylogeny of the Asteraceae. Aliso 8: 465-
492.
Catling, P. M. 1983. Pollination of northeastern North American Spiranthes (Orchidaceae).
Canad. J. Bot. 61: 1080-1093.
Clutton-Brock, T. H. & P. H. Harvey. 1984. Comparative approaches to investigating adap-
tation. Pages 7-29 in J. R. Krebs & N. B. Davies (eds.), Behavioural ecology, an evolutionary
approach. Sinauer Associates, Sunderland.
Corbet, S. A., I. Cuthill, M. Fallows, T. Harrison & G. Hartley. 1981. Why do nectar-foraging
bees and wasps work upwards on inflorescences? Oecologia 51: 79-83.
Cronquist, A. 1981. An integrated system of classification of flowering plants. Columbia
University Press, New York.
Cruden, R. W. 1977. Pollen-ovule ratios: A conservative indicator of breeding systems in
flowering plants. Evolution 31: 32-46.
- - . 1988. Temporal dioecism: Systematic breadth, associated traits, and temporal pat-
terns. Bot. Gaz. 149: 1-15.
- - & S. M. Hermann-Parker. 1977. Temporal dioecism: An alternative to dioecism?
Evolution 31: 863-866.
Dafni, A. 1984. Mimicry and deception in pollination. Ann. Rev. Syst. Ecol. 15: 259-278.
Darwin, C. 1862. On various contrivances by which British and foreign orchids are fertilised
by insects. Murray, London.
1876. The effects of cross and self fertilisation in the vegetable kingdom. Murray,
London.
1888. The different forms of flower on plants of the same species. John Murray,
London.
Donoghue, M. J. 1989. Phylogenies and the analysis ofevolutionary sequences, with examples
from seed plants. Evolution 43:1137-1156.
Faegri, K. & L. v a n d e r Pijl. 1979. The principles of poUination ecology. Pergamon, Oxford.
F e l s e n s t e i n , J. 1985. Phylogenies and the comparative method. Amer. Naturalist 125:1-15.
Godley, E. J. 1955. Monoecy and incompatibility. Nature 176:1176-1177.
DICHOGAMY IN ANGIOSPERMS 143
Gottsberger, G. 1977. Some aspects of beetle pollination in the evolution of flowering plants.
P1. Syst. Evol. Suppl. 1:211-226.
Gray, A. 1879. Gray's botanical textbook. Vol. 1. Structural botany. Amer. Book Co., New
York.
Henslow, G. 1888. The origin of floral structures through insect and other agencies. Keg,an,
Paul and Trench, London.
Ingrain, R. & L Taylor. 1982. The genetic control of a non-radiate condition in Senecio
squalidus L. and some observations on the role of ray florets in the Compositae. New
Phytol. 91: 749-756.
Jones, S. G. 1939. Introduction to the floral mechanism. Chemical Publ. Co., New York.
Kerner von Marilann, A. 1895. The natural history of plants. Vol. 2. Blackie, London.
Knuth, P. 1906-1909. Handbook of flower pollination (English translation). 3 volumes. Clar-
endon Press, Oxford.
Kohn, J. R. & S. C. H. Barrett. 1992. Floral manipulations reveal the cause of male fitness
variation in experimental populations of Eichhornia paniculata (Pontederiaceae). Funct.
Ecol. 6: 590-595.
Kiilrenter, J. G. 1761. Vorl~iufige Nachricht von einigen das Geschlecht der Pflanzen betref-
fenden Versuchen und Beobachtungen. Leipzig.
Lindsey, A. H. 1982. Floral phenology patterns and breeding systems in Thaspium and Zizia
(Apiaceae). Syst. Bot. 7: 1-12.
Lloyd, D. G. & C. J. Webb. 1986. The avoidance of interference between the presentation of
pollen and stigmas in angiosperms. 1. Dichogamy. New Zealand J. Bot. 24: 135-162.
- - & J. M. A. Yates. 1982. Intrasexual selection and the segregation of pollen and stigmas
in hermaphrodite plants, exemplified by Wahlenbergia albomarginata (Campanulaceae).
Evolution 36:903-913.
Lovett Donst, J. 1980. Floral sex ratios in andromonoecious Umbelliferae. New Phytol. 85:
265-273.
Mahberley, D. J. 1987. The plant-book. Cambridge Univ. Press, Cambridge.
Mosquin, T. & E. H. Martin. 1967. Observations on the pollination biology of plants of
MeUville Island, N.W.T., Canada. Canad. Field-Naturalist 81: 201-205.
Miiller, H. 1883. The fertilisation of flowers. MacMillan, London.
Ockendon, D. J. & L. Currah. 1977. Self-pollen reduces the number of cross-pollen tubes in
the styles of Brassica oleracaea L. New Phytol. 78: 675-680.
Ornduff, R. 1969. Reproductive biology in relation to systematics. Taxon 18:-121-133.
Palmer, M., J. Travis & J. Antonovics. 1989. Temporal mechanisms influencing gender
expression and pollen flow within a self-incompatible perennial, Amianthium muscaetox-
icum (Liliaceae). Oecologia 78:231-236.
Pellmyr, O. 1987. Multiple sex expressions in Cimicifuga simplex: Dichogamy destabilizes
hermaphroditism. Biol. J. Linn. Soc. 31: 161-174.
Percival, M. 1965. Floral biology. Pergamon Press, Oxford.
Philipp, M. 1985. Reproductive biology of Geranium sessiliflorum 1. Flower and flowering
biology. New Zealand J. Bot. 23: 567-580.
Pijl, L. van der. 1978. Reproductive integration and sexual disharmony in floral functions.
Pages 79-88 in A. J. Richards (ed.), The pollination of flowers by insects. Linn. Soc. Symp.
Ser. No. 6.
Pistolesi, G., F. Cecconi, S. Baroneelli & M. Rocca. 1986. Stressing sunflower (Helianthus
annuus L.) plants as a method for speeding breeding techniques. Z. Pflanzenziicht. 96:
90-93.
Ponomarev, A.N. 1960. Concerning proterandry in Umbelliferae. Dold. Akad. Nauk. S.S.S.R.
135: 750-752. (translation)
Proctor, M. & P. Yeo. 1972. The pollination of flowers. Taplinger, New York.
Pyke, G. H. 1978. Optimal foraging in bumblebees and coevolution with their plants. Oecolo-
gla 36: 281-293.
144 THE BOTANICAL REVIEW
Richards, A. J 9 1986. Plant breeding systems. Allen and Unwin, London.
Schemske, D. W, M. F. Willson, M. N. Melampy, L. J. Miller, L Verner, K. M. Schemske
& L. B. Best 9 1978. Flowering ecology of some spring woodland herbs. Ecology 59: 351-
366.
Schlessman, M. A. 1978. Systematics and reproductive biology of Lomat i um f ari nosum
(Geyer ex Hooker) Coulter & Rose (Umbelliferae). Madrofio 25: 1-9.
9 1982. Expression ofandromonoecy and pollination of tuberous lomatiums (Umbel-
liferae). Syst. Bot. 7: 134-149.
, P. P. Lowry, II & D. G. Lloyd. 1990. Functional dioecism in the New Caledonian
endemic Polyscias pancheri (Araliaceae). Biotropica 22:133-139.
Schoen, D. J. 1977. Morphological, phenological, andpollen-distributionevidenceofautoga-
my and xenogamy in Gilia achilleifolia (Polemoniaceae). Syst. Bot. 2: 280-286.
Shore, J. S. & S. C. H. Barrett. 1984. The effect of pollination intensity and incompatible
pollen on seed set in Turnera ulmifolia (Turneraceae). Canad. J. Bot. 62: 1298-1303.
Silvertown, J. 1987. The evolution of hermaphroditism: An experimental test of the resource
model. Oecologia 72: 157-159.
Stout, A.B. 1928. Dichogamy in flowering plants. Bull. Torrey Bot. Club 55: 141-153.
Thomson, G. M. 1881. On the fertilization, etc., of New Zealand flowering plants. Trans.
Proc. New Zealand Inst. 13: 241-291.
Webb, C. J. 1981. Andromonoecism, protandry, and sexual selection in Umbelliferae. New
Zealand J. Bot. 19: 335-338.
- - & D. G. Lloyd. 1986. The avoidance of interference between the presentation of pollen
and stigmas in angiosperms. II. Herkogamy. New Zealand J. Bot. 24: 163-178.
Willemstein, S. C. 1987. An evolutionary basis for pollination ecology. Leiden Botanical
Series Vol. 10, E. J. Brill, Leiden.
Wilson, A. S. 1878. On the association of an inconspicuous corolla with proterogynous
dichogamy in insect-fertilised flowers. Nature 18: 508-509.
Wyatt, R. 1983. Plant-pollinator interactions and the evolution of breeding systems. Pages
51-95 in L. Real (ed.), Pollination biology. Academic Press, Orlando.
9 1984. The evolution of self-pollination in granite outcrop species of Arenaria (Car-
yophyllaceae). Morphological correlates. Evolution 38:804-816.
A p p e n d i x I
C o n v e n t i o n s f or Re c o r d i n g D a t a
Following each recorded variable, we list the categories into which species were placed. Where
a species could not readily be placed into any of the categories, it was not scored for that
variable. Where the species varied among categories, but one category was predominant, the
species was assigned to that category. The numbers of species falling into each category are
stated parenthetically.
Scientific Name. The name provided in the original source unless inspection of more recent
works indicated revised nomenclature. Generic names were made consistent with Mabberley
(1987) where possible, otherwise left as found.
Family. Familial designations were made consistent with Cronquist (1981).
Continental Location. North America (669), South America (450), Europe (384), Africa
(199), Asia (135), Australia (925), Eurasia (438), circumhoreal (218), other combinations (66).
North America (including Greenland) and South America were divided in northern Mexico.
Europe was considered to extend from the Urals west, including the southern and eastern shores
of the Mediterranean. Africa referred to the continent south of the Mediterranean region, and
Asia was the area extending east from the Urals and the Near East. The Australian region
included Australia, New Zealand and other west Pacific Islands west to Wallace's Line.
Latitude. arctic (113), temperate (2252), tropical (752). Divisions between temperate and
arctic were at the timberline, and between temperate and tropical were at the Tropics of Cancer
and Capricorn.
DICHOGAMY IN ANGIOSPERMS 145
Habi t at . forest (506), scrub/shrub (232), grassland (194), vegetated wetland (271), aquatic
(83), alpine (31), rocky (35), disturbed (228), desert (33), other (68).
Growth Form. herb (1742), vine (102), shrub (835), tree (222).
Perennation. annual (399), biennial (47), variable monocarpic (16), perennial iteroparous
(2459), varies (60).
Sexual System. hermaphrodite, here referring to species having only bisexual flowers (2040),
monoecy (380), gynodioecy (75), gynomonoecy (139), androdioecy (4), andromonoecy (187),
trioecy (7), heterostyly (12), other (6), varies (52). Dioecious species were excluded.
Flowering Time. year-round (18), January (34), February (36), March (80), April (194), May
(313), June (437), July (277), August (88), September (24), October (21), November (19),
December (18). Typical month of first flowering.
Self-Sterility. yes (263), no (749), varies (41). Species were considered self-incompatible i f
so designated or i f quantitative information showed less than 50% fruit or seed production
following selfing as compared to outcrossing.
Pollen-Ovule Ratio. (194) Expressed per flower for hermaphrodites and per #a nt for others.
Flower Size. (870) Diameter of average female flowers in monoecious species, and hermaph-
rodites in others.
Flower Lifespan. (355) Number of days that average flowers are open and functional; female
flowers of monoecious species, perfect flowers in others.
Inflorescence Verticality. yes (151), no (1468). Yes i f inflorescences are markedly elongate.
Flower Maturation Pattern. acropetal (89), basipetal (3), other (9), varies (2). For species
with vertical inflorescences only.
Pollinator Movement Pattern. up (34), down (1), varies (1). For species with vertical inflo-
rescences only.
Pattern of Intrafloral Dichogamy. protandry (2087), protandry to adichogamy (105), adichog-
amy (529), adichogamy to protogyny (159), protogyny (905), protandry to protogyny (63). The
first five categories received the numerical designations 1-5. See text.
Intraltoral Pollen-Stigma Overlap. yes (931), no (131), varies (3). Yes i f viable pollen and
receptive stigma are present simultaneously within a flower.
Slmntaneous Autogamy. yes (444), no (511), varies (30). Yes i f undisturbed #ant s set ap-
preciable seed.
Slmrophyll Projecting Furthest. stigma (163), anther (56), varies (41), neither (116).
Facilitating Sex. male (0), female (821), neither (987). Female when the stigma or style is
involved in pollen presentation.
Post-Presentation Stigma Changes. yes (83). Yes i f movement, shriveling, dehiscence or
elongation was noted.
Pest-Presentation Stamen Changes. yes (134). Yes i f movement, shriveling, dehiscence or
elongation was noted.
Pollinators. autogamy (100), insects (1647), birds (135), mammals (15), water (5), wind
(361), varies (20). Insect pollinators were further characterized as bees (548), flies (168), wasps
(30), beetles (63), butterflies (39), moths (38), bees and flies (194), butterflies and moths (17),
other (251).
Use of Flowers for Traps or Broodplaces. yes (57), no (2593). Yes i f the flower or inflorescence
typically served one of these functions.
Pollen Reward. yes (436), no (183). Yes i f typical pollinators feed on pollen.
Other Stamen Rewards or Attractants. yes (33), no (295). Yes i f involved in production,
edible staminodes, etc.
Pattern of Interfloral Dichogamy. protandry (122), protandry to adichogamy (3), adichogamy
(6), adichogamy to protogyny (1), protogyny (439), protandry to protogyny (18), heterodichoga-
my (9), duodichogamy (7), varies (5).
Iuterfloral Pollen-Stigma Overlap. yes (97), no (72), varies (3). Yes i f viable pollen is released
while receptive stigmas are present on the same plant.
Nectar Production. yes (1183), no (163), varies (2).
Outcrnssing Rate. 0-10% (21), 11-20% (7), 21-30% (3), 31--40% (2), 41-50% (2), 51--60%
(1), 61-70% (6), 71-80% (5), 81-90% (4), 91-100% (13).
Reference. Coded reference to original source.
146 THE BOTANICAL REVIEW
E
,.m ,~a
o
,.~
? 5
q q i I l q l 0 l l ~ . . . . . . . . I ~ m ~ l l ~ 0 I 0 l 0 1
~ 0 0 0 0 0 0 ~ 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
~ 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 ~ 0
0 0 0 0 0 0 0 ~ 0 0 0 0 0 0 0 0 0 ~ 0 0 0 0 ~
~ 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0 0 0 ~ 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 ~ 0 0 0 0 ~ 0 0 0 0 0 0 0 0 0
~ 0 0 0 ~ 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 ~ 0
N
0 0 0 ~ 0 0 0 0 ~ 0 0 ~ 0 0 0 ~ 0
I q q q ~ q q ~ q ~ q q q q q q q i 0 i ~ I .
0 0 0 0 0 0 0 0 0 0 ~ 0 ~ 0 0 0 0 0 0 0 0 0 0 0
0 0 0 ~ 0 ~ 0 ~ 0 ~ 0 ~ 0 ~ 0 0 0 ~ 0 ~
~ 0 ~ 0 0 0 0 0 ~ 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
~ 0 0 0 0 ~ 0 0 0 0 ~ 0 0 0 0 0 0 0 0 0 ~ 0 ~
0 0 0 0 0 0 0 0 0 0 ~ 0 0 ~ 0 0 0 0 0 0 0 0 0 0
< < < < < < < < < < = = = = = =
D I C H O G A M Y I N A N G I O S P E R M S 1 4 7
0 0 O0 0 0 O0
I I I I I 0 I I I 0 . I I I I I I I 0 . ~ . I I 0 . I I I O I I 0 . 0 .
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 ~ 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 ~ 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 ~ 0 0 0 ~ 0 0 0 0 0 0 0 ~ 0 0 0 0 0 0 0 0 0 0 ~
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 ~ 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 ~ 0 0 0 ~ 0 0 ~ 0
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
1 0 0 0 0 ~ 0 I ~ Q ~ q O ~ O ~ I I
0 0 ~ 0 0 0 0 0 0 0 0 0 0 0 ~ 0 0 0 0 0 0 0 0 ~ 0 0 0 0 0
0 ~ 0 0 0 0 0 0 0 0 0 0 0 ~ 0 0 ~ 0 ~ 0 0 0 0 0 0 0 0 0
~ 0 0 0 0 ~ 0 0 0 0 0 ~ 0 0 0 ~ 0 ~ 0 ~ 0 ~ 0 0 0
148 THE BOTANICAL REVIEW
~ 0 0 0 0 0 0 0 0 0 0 ~ 0 0 0 ~ 0 0 0 0 0 0 0 0 ~ 0 ~ 0 0
r- on ~,% O 0 0
~. I I I I I I I I I I I ~ I I O I I I I I I I I O O I O I I
"~ 6 e4 . 4 . 4 -:
0 0 0 0 0 0 0 0 0 0 0 0 ~ 0 0 ~ 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
~ 0 0 0 0 0 0 0 0 0 0 ~ 0 0 ~ 0 0 0 0 0 0 0 0 0 0 0 0 0 0
~ 0 0 0 0 0 0 0 0 0 0 0 ~ 0 0 ~ 0 0 0 0 0 0 0 0 ~ 0 0 0 0
~ 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0 0 0 ~ 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
~ 0 0 0 0 0 0 0 0 0 0 0 0 0 0 ~ 0 0 0 0 0 0 0 0 0 0 0 ~ 0 0
O 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 M O 0
o o o o o - o o o o o i i o - i ~ o ~ o ~ o o o o o o
0 0 0 0 0 0 0 0 0 0 ~ 0 0 0 0 0 0 0 ~ 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0 ~ 0 0 0 0 0 0 0 ~ 0 0 0 ~ 0 0 0 0 0 0
0 0 0 0 0 0 ~ 0 0 ~ 0 0 0 ~ 0 0 ~ 0 0 0 ~ 0 0 ~ 0 0 0
0 0 0 0 0 ~ 0 0 0 0 ~ 0 0 0 0 0 ~ 0 ~ 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 ~ 0 0 ~ 0 0 0 ~ 0 ~ ~ 0 ~ 0 0 0 0
9 o ~ ~ " ~ = ~ - , ~ ' ~ a = ~ ~
~ . ~ ~ ~" ~ , ' o = = ~ ' ~ = . ~ ~,
D I C H O G A M Y I N A N G I O S P E R M S 1 4 9
e . o
0 0 0 0 ~ 0 0 0 0 ~ 0 0 0 0 0 0 0 0 0 0 0 0 ~ 0 0 0 0 0 ~
0 0 0 O n O
I I I I 0 . I I I I O . I I I I I I I I I I I I O . I I I I I ~ . O .
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 ~ 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 ~ 0 0 0 0 0 0 0 0 0 0 0 0 ~ 0 0 0 0 0 0 ~
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 ~ 0
0 0 0 0 ~ 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 ~ 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 ~ 0
0 0 0 0 ~ 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 ~ 0 0 0 ~ 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 ~ 0 0 0 0 0 ~ 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
~ 0 ~ 0 0 0 0 ~ 0 0 ~ 0 ~ 0 ~ 0 0 ~ 0 0 0 0 0 ~ 0 ~ 0 0
0 0 ~ 0 0 0 0 ~ 0 0 0 0 ~ 0 0 0 0 0 0 ~ 0 0 0 0 0 0 0 0 0 0
~ 0 ~ 0 0 0 0 ~ 0 0 0 ~ 0 ~ 0 0 ~ 0 ~ 0 ~ 0 0 0
150 THE BOTANICAL REVIEW
0 ~ 0 0 0 ~ 0 0 0 0 0 0 0 0 0 ~ 0 ~ 0 0 0
0 0 0 0
I O . I I I O . I I I I I I I I I O . I O . I I I
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
O 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
O 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 ~ O 0 0
O ~ O 0 0 ~ O 0 0 0 0 0 0 0 0 ~ O ~ O 0 0
O 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
O 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
O 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
O 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
O O 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 ~ 0 0 0 0 0 0 0 0 0 0 0 0 0 ~
O 0 0 0 ~ O ~ O 0 0 0 ~ O 0 0 ~ O ~ O 0 ~
, - _ ~ ~ u ' ~ _ ~ ~ o . - ~ ~ o
~ z z z o o o o c ~ , ~ , ~ ~
DI CHOGAMY I N ANGI OSPERMS 151
0 0 0 0 0 ~ 0 ~ 0 0 0 0 0 0 ~ 0 0 0 0 0 ~
0 I' -
I I I ~ I ~ I I I I I I I I I I I I I I ' e .
0 0 0 0 0 0 0 0 0 0 0 0 0 0 ~ 0 0 0 0 0 0
0 0 0 0 0 0 0 ~ 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 ~ 0 0 0 0 0 0 0 0 0 0 0 0 0 0 ~
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 ~
0 0 ~ 0 0 ~ 0 0 0 0 0 0 0 0 0 0 0 ~ 0 ~
0 0 ~ 0 ~ 0 0 ~ 0 0 0 0 0 0 ~ 0 0 0
1 5 2 T H E B O T A N I C A L R E V I E W
m , o
~ O
0 0 0 0 0 0
~ I ~ I I I I I I I ~ I I I I I I q I
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 ~ 0 0 0 0 0 0 0 0 0 0 0 0 0
~ 0 0 0 0 0 0 0 0 0 ~ 0 ~ 0 0 0 0 0 0 ~ 0
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 ~ 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0 0 ~ 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 ~ 0 0 ~ 0 ~ 0 ~ 0 0 0 0
J q @ q q q q ~ q I ~ q q q ~ q Q q I q
0 0 0 0 0 0 0 0 0 0 0 ~ 0 0 0 0 0 0 0 0 0
0 ~ 0 0 0 ~ 0 0 0 0 0 ~ 0 ~ 0 0 ~ 0 ~
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 ~ 0 0 0 0 0
0 0 0 0 0 0 0 ~ 0 0 0 0 0 ~ 0 0 0 0 0 0 0
"~ ~ ~ ~ ~.) r.% ~ ~2 ~ O~ ~