DIOECISM IK TROPICAL FOREST TREES
K. S. BAWA'
Gray Herbarium, Harvard University, Cambridge, Massachusetts
P. A.
Organization for Tropical Studies, Universidad de Costa Rica, Costa Rica
Received January 25, 1974
The existence of dioecism among angio-
sperms is universally acknowledged, yet is
poorly understood both from the ecological
and evolutionary points of view. The
reason for this hiatus might be that some
have believed the relative proportion of
dioecious taxa to be low (Yamplosky and
Yamplosky, 1922; Lewis, 1942), while
others have felt that since the number of
seed-bearing individuals is halved in a dioe-
cious population its evolution is an unlikely
and perhaps inconsequential event (Heslop-
Harrison, 1972). However, recent studies
have reported a large proportion of dioe-
cious tree species in tropical forests
(Ashton, 1969; Bawa, 1974; see also
Tomlinson, 1974); this indicates that the
incidence and importance of dioecism may
have been underestimated in the past.
These new data are significant in at least
one other respect. Dioecious (and monoe-
cious) flowers in temperate plants are
presumed to have evolved in response to
selective pressures favoring wind-pollination
(Grant, 1951; Stebbins, 1951), yet wind-
pollination is probably either absent or
uncommon in tropical forests (Whitehead,
1969; see also Daubenmire, 1972).
Here we present an overview of the adap-
tive and evolutionary significance of dioe-
cism in general and its expression in certain
tropical forests in particular. We first
present data on the frequency of dioecious
species in a lowland tropical semi-deciduous
forest in Costa Rica, then proceed to an
examination of available information on
'Present address: Department of Biology,
University of Massachusetts, Boston, MA 02125.
'Present address: Office of Endangered Species,
Fish and Wildlife Service, Washington, D.C. 20240.
EVOLUTION 29: 167-179. March 1975
OPLER'
the occurrence of dioecious taxa in other
tropical and temperate forests. After show-
ing that the large number of dioecious (and
monoecious) species in the tropics are ento-
mophilous, we review the widely held belief
that selective forces favoring anemophily
have been responsible for the evolution of
dioecism. Finally, we discuss specific
hypotheses that might explain the selective
pressures responsible for the evolution and
maintenance of dioecism.
MATERIAL AND METHODS
The experimental portion of our study
was carried out in a lowland tropical semi-
deciduous forest on Comelco Property, 5 km
northwest of Bagaces, Guanacaste Province,
Costa Rica (for a detailed vegetation
description see Holdridge et al., 1971).
An intensive survey of the flora's woody
component was undertaken to determine the
frequency of dioecious species. Insights
gained during the survey phase led to
studies of the pollination biology of selected
species, and the collection of data concern-
ing flower size and color; amount of nectar
per flower; fruit production (expressed as
fruits per infructescence ) ; and flowering
seasonality.
In order to assess the significance of dioe-
cism on more than a local basis, the fre-
quency of dioecious species was also
reviewed for other tropical and temperate
areas. For this purpose, sex expression of
trees in species lists from several previous
vegetation studies was compiled. As will be
discussed later, information concerning the
sexuality of flowers and individual plants
in published floras is frequently unreliable
especially for tropical trees. Therefore, the
167
168 K. S. BAWA AND P. A. OPLER

TABLE 1. Dioecious tree species in a semi-deciduous forest in Guanacaste Province, Costa Rica.'

Family Species Voucher no.s

Anacardiaceae Astronium graveolens Iacq, PAO 1630

Spondias nigrescens Pittier REH 119
Boraginaceae Cordia collococca Sond. PAO 571
C. panamensis Riley' PAO 645
Burseraceae Bursera simarouba (L.) Sarg." GWF 157
B. tomentosa (Jacq.) Triana & Planch' PAO 759
Ebenaceae Diospyros nicaraguensis Standley PAO 761, 872
Erythroxylaceae Erythroxylum lucidum var. cosiaricense O. E. Schulz PAO 392
Euphorbiaceae Bernardin nicaraguensis Standley & Williams PAO 102
Margaritaria nobilis (LJ.) Muell.-Arg," PAO 162, 1690
Flacourtiaceae Xylosma anisophylla Standley PAO 493, 576
Xylosma sp. PAO 567, 760
Guttiferae Rheedia edulis Triana & Planch No specimen
Meliaceae Guarea sp. GWF 96
Trichilia anisopleura C. DC. PAO 916
T. cuneate RadIk. PAO 635, 646, 1689
T. hirta L. PAO 681
T. trijolia L. PAO 656
Moraceae Cecropia peltata L. No specimen
Chlorophora tinctoria (L.) Urban PAO 839
N yctaginaceae Pisonia mocranthocarpa Donnell Smith GWF 230
Polygonaceae Coccoloba caracasana Meisn," PAO 559
C. jloribundo Lindau' PAO 315, 758
C. padijormis Meisn.' PAO 555, 763
Ruprechtia costata Meisn. PAO 566, 1679
Triplaris americana L. PAO 509
Sapindaceae Allophyllus occidentalis L: PAO 153, 680
Simaroubaceae Alvaradoa amorphoides subsp. typica Cronquist PAO 511
Picramnia quaternaria Donnell Smith PAO 658
Simarouba glauca DC: PAO 81
Rubiaceae Genipa caruto HBK. GWF 140, 145
Randia subcordata Standley GWF 111
R. spinosa (Jacq.) Karst PAO 102
Rutaceae Zanthoxylum setulosum P. Wilson PAO 697
1All found on Comelco Property, 5 km northwest of Bagaces.
z Occasionalpistillate and/or perfect flowers on staminate trees.
3 Trees with staminate, pistillate, and staminate plus pistillate and/or perfect flowers respectively.

'Trees with staminate or staminate and perfect, and pistillate flowers respectively.
5 Vouchers in the herbarium of Missouri Botanical Garden (MO). PAO =Paul A. Opler, REH =
Raymond E. Heithaus, GWF =Gordon W. Frankie.

figures for different categories in Table 2 RESULTS AND INTERPRETATION

should be treated as minimal approxima-
tions. Caution is also required in interpret-
ing the significance of differences between
areas with respect to relative frequencies of
each category due to possible sampling
errors. These errors could have resulted
from differences in sample size or sampling
techniques.
Our presentation of results consists of
two groups of data. As mentioned earlier
we will put forward information on the fre-
quency of dioecism in several well studied
tropical and relatively complex temperate
forests. After establishing the importance
of dioecism in tropical forests we then
present information on several aspects of
 TROPICAL TREES 169

TABLE 2. Relative proportions of hermaphroditic, monoecious and dioecious species and individuals in
tropical and temperate forests.

Sex expression
% Species 0/0 Individuals
Hermaph- Monee- Dioe- Hermaph- Monoe- Dioe-
Forest type and locality roditic cious do us roditic do us do us

Tropical forests
Semideciduous forest,
Guanacaste Province, Costa Rica 68' 10' 22'
Plot I (1000 m") 71 0 29 76 0 24
Plot II (1500 m") 78 1 21 91 1 8
Plot III (4000 m") 75 2 23 72 1 17
Plot IV (1600 m") 73 0 27 69 0 31
Rain forest,
South Nigeria" 47 13 40 48 14 38
Upper story 41 22 37 42 36 22
Middle story 50 13 37 47 4 49
Lower story 49 13 38 54 3 43
Lowland mixed Dipterocarp
forest, Central Sarawak" 60 14' 26
South Florida" 61 12 27
Temperate forests"
Galipolis, Ohio t 83 11 15 75 10
Campbellsville, Kentucky 15 70 15 17 76 7
Pivot Rock, Arkansas 0 83 17 0 92 8
Hueston's Woods, Ohio 27 60 13 8 87 5
Pisgah Mountain, New Hampshire 13 81 6 1 98 1
1 These figures are for the total area and not the averages of intensively studied plots.
2 Based on a species list in Jones (1955).

3 From Ashton (1969).

'Includes some protandrous and some protogynous, hermaphroditic species.

"From Tomlinson (1974); for the whole of South Florida and not a particular forest.
• Based on species lists in Braun (1950).

floral biology and pollination phenology
which we contend will characterize the gen-
eralized reproductive strategy of tropical
dioecious trees. In particular, these trees
have small generalized flowers adapted for
visitation and pollination by small insects of
several orders, especially small bees. The
nature of floral reward presentation, both
in space and time, is such that it maximizes
the probability of adequate fruit set.
Incidence of Dioecism
Frequencies of dioecious species.-It is
difficult to determine the true frequency of
dioecious species in any flora since in a
majority of cases the flowers have both
staminate and pistillate parts, but only one
set is functional. Furthermore, these plants
occasionally have either bisexual flowers or
flowers of the opposite sex present in low
numbers. Thus, unless the viability of
pollen and ovules and the relative frequency
of flowers with different sex expression are
also examined, conclusions concerning
sexuality may prove erroneous. It is, there-
fore, not surprising that several recent
studies have revealed dioecism and monoe-
cism in taxa previously considered hermaph-
roditic (Lee, 1967; Tomlinson and Fawcett,
1972; Styles, 1972). On the basis of obser-
vations of floral biology and fruit set of
marked individuals we estimate that 22%
of the tree species at our study site are dioe-
cious (Table 1). In several other tropical
forests, the relative proportion of dioecious
species is similar to that of our study site
170 K. S. BAWA AND P. A. OPLER

• Dioedou.a species
portion of dioecious species and individuals
in north temperate forests is generally lower
20 o Her1ll&phroditic sdf-incolllpatible spede. than in tropical forests (Table 2) ; however,
the proportion of monoecious species and
individuals is always much higher in tem-
.
u
perate than in tropical forests, while the
~ reverse is true for hermaphroditic taxa.
" 10
Tropical vs. temperate floras.-The fre-
i quency of dioecious species has been calcu-
lated for only a few floras and is as follows:
Great Britain, 3.1% (McComb, 1966) ,
California, 2.6% (Baker, 1967) , New
Zealand, 14.5% and Hawaii, 27.5% (Carl-
quist, 1966). The high incidence of dioe-
cism in Hawaii may have two explanations.
Flower size
(log length
II log breadt.h of corolla in
DIll) First, evolution of dioecious taxa there may
FIG. 1. Frequencies of various flower size have occurred in response to selective pres-
classes for dioecious and hermaphroditic, self- sures for outcrossing after the islands were
incompatible species. colonized (Baker, 1967; see also Raven,
1973 for a similar interpretation of dioecism
in New Zealand). Secondly, tropical floras
(Table 2). The rain forest of southern may contain proportionately more dioecious
Nigeria (Jones, 1955) appears to be extra- species than do temperate floras since
ordinarily rich in dioecious species; how- dioecism is more prevalent for trees and
ever, the species list from which the shrubs than for other life forms. For
frequency of dioecious taxa was calculated example, in our study area, in contrast to
did not include all tree species which occur 22% trees and 11% of the shrubs, only one
in that forest, and the difference could be (Lycoceris grandis-Compositae) of the ap-
due to sampling errors (see Material and proximately 300 herbs is dioecious, while no
Methods), More likely, it is due to the vines, lianas or epiphytes there are known
dominance of species representing the by us to be dioecious. Further, among
ebenaceae and meliaceae, both consisting the families studied in Costa Rica, only
almost entirely of dioecious taxa. Boraginaceae, Nyctaginaceae and Rubia-
Frequency of dioecious individuals.-A ceae contain both herbaceous and woody
consideration of the overall importance of genera; dioecism in all three families is
dioecism on the basis of relative proportions confined to the woody members, primarily
of dioecious and hermaphroditic species trees, while without exception the herba-
alone may be misleading, since there may be ceous species are hermaphroditic. Since
differences in the proportions of individuals. temperate floras have proportionately fewer
Therefore, the relative proportions of dioe- woody species than tropical floras the low
cious and hermaphroditic individuals were incidence of dioecism among the former
also compared. The main point that might be expected, although further
emerges from such a comparison (Table 2) information from other floras is needed to
is that the number of dioecious individuals test this idea.
may be as high as 38% of all trees in a given
area. It should also be noted that where Floral Morphology and
vegetation is stratified (e.g., south Nigerian Pollination Biology
rain forest), the frequency of dioecious
species and individuals may differ between Flower size and color.-Although dioe-
stories. cious taxa are found in a diverse array of
Tropical vs. temperate forests.-The pro- families representing quite different evolu-
 TROPICAL TREES 171

TABLE 3. Comparison of the amount of nectar' in staminate and pistillate flowers of selected" dioecious
species."

Amount of nectar!

Staminate flower Pistillate flower

Pistillate/
Average ~Iax- Average Max- Staminate
Species imum- imurn- flower

Coccoloba caracasana .18 .24 .05 .09 0.28

C. padijormis .09 .24 .32" .36 3.5
Cordia collococa .41 1.32 .92 1.32 2.2
Simarouba glauca .11 .31 .72 2.12 6.5
Trichilia cuneata .17 1.02 .31 1.56 1.8
Triplaris americana .16 .25 .66 .81 4.1

'The amount of nectar produced by a flower is influenced by several variables such as climatic
conditions, location of the tree, and location of flowers. Therefore the data in this table do not
represent the quantity of nectar produced by flowers of respective species, but merely indicate a trend
in differences in the relative amounts of nectar in the two kinds of flowers.
2 The species available in adequate numbers at time of experiment.

"Bagged inflorescences were checked periodically throughout the day for maximum production.
Average is the mean of all positive readings.
• In microliters per hour.
"Figures represent the greatest amount found in a single flower.
"Data from perfect flowers; female flowers were unavailable at the time of sampling.

tionary lineages, most show remarkable
constancy in flower size and color. For the
majority, flowers are small (generally :-: :; 1.0
em in length and breadth), and the color
ranges from white to yellow or pale green.
A comparison of flower size of con-
familial dioecious and hermaphroditic taxa
within the study area indicated that the
former usually have smaller flowers than
the latter. The notable exceptions were
members of the Rubiaceae, in which dioe-
cious taxa (Genipa caruto and Randia
subcordata) have strikingly large flowers.
However, because of small sample size the
generality of these differences remains
obscure and therefore actual measurements
have not been presented. But, when one
compares mean flower size for all dioecious
species with known hermaphroditic, self-
incompatible species from the study area, it
becomes apparent that the former have
significantly smaller flowers than the latter
(Fig. 1).
In addition to discrepancy in floral size
when contrasted with related hermaph-
roditic taxa, tropical dioecious trees fre-
quently display sexual dimorphism in
flower size within species. In our study
area 14 of 20 species (70%), whose flowers
were measured had staminate flowers
smaller than pistillate. Empirically, we
observe this is probably in order to accom-
modate the bulkiness of the ovary and en-
larged nectaries of pistillate flowers. These
results are in contrast with those of Baker
(1948) who asserts the reverse, i.e., that
pistillate flowers are smaller than staminate
in temperate dioecious taxa. Perhaps these
two generalizations reflect further upon
the basic differences between pollination
biology of tropical and temperate dioecious
plants (see discussion). One would suppose
that the need for greater pollen production
and absence of nectar production in ane-
mophilous taxa is responsible for the reverse
trend in flower size reported earlier by
Baker.
Staminate/ pistillate flower ratios.- Three
factors contribute to this ratio in any popu-
lation of dioecious plants, number of flowers
per inflorescence, number of inflorescences
per plant, and the relative number of plants
with staminate and pistillate flowers (sex
ratio). Research in progress indicates that
for the majori ty of the dioecious species in
our Costa Rican study site, all three factors
172 K. S. BAWA AND P. A. OPLER

TABLE 4. Flower visitors of some dioecious species.'

Flower visitors

:g'"" ;g"'" ::="" "'" -e'""

'"" ::= " .s"'" 'c
~
';;'
0
" "
'c "
"" ~ee :gu'" ::="'Co
" ;g"'" '" 0
Co
0

""..:
;: ..
..." :t~
"'"
"" ~
'a
8.
"0
::='" E
:aCo .g ~E :a"" :a"u ]"
1= ~ >'l ~ ~ ...""
E
Species
'" ..: ::E >
~
"
(f) (f)
0
(f)
"
>'l

Coccoloba caracasana ~
(j>
+
40 8 3 6
C. padiformis ~ 15*
(j> 1 11 28
Cordia collococca s I 4 2 3 1* 1
(j> 3 1 3 4* 1
Simarouba glauco <5 3 18 15 21 9 19 9 3 3 46 10 8
(j> 4 2 3 1* 3* +
Trichilia ClIneata ~ 14 3* 2
(j> I 1* 2*
Triplaris americana s 12* 5
(j> 2 3*
, A plant of each sex was sampled with an insect net for a thirty minute period during the time of
maximum visitation. The numbers refer to individuals captured, while plus sign indicates presence but
none captured.
Bold face type = most likely primary poIlinators.
* Same species on both ~ and (j> trees.

contribute to an excess of staminate flowers
over pistillate flowers (Opler and Bawa, in
prep.).
Floral rewards.-Only staminate flowers
offer pollen to potential flower visitors,
while both staminate and pistillate flowers
may provide a nectar offering. Pistillate
flowers usually have a significantly greater
amount of nectar per flower (Table 3).
Among the species studied in Costa Rica
(Table 1) only Cecropia peltaia and
Chlorophora tinctoria (Moraceae) fail to
present nectar offerings; these might be
anemophilous.
Pollinators.-The flower visitors of some
dioecious species are shown in Table 4.
Most visitors are small, relatively unspecial-
ized insects which coincide with the small
flowers of these dioecious trees. The excep-
tions, hummingbirds, hawkmoths and large
bees, visit the concomitantly large flowers
of Genipa caruto and Randia subcordata.
The species composition of the flower
visitor complement of most dioecious trees
is remarkably similar, and is much like that
of other trees in the same habitats with
small generalized flowers. Many of the
insects are opportunists to the small flowers
which present no barrier to the attainment
of the floral rewards, yet it is likely that
small bees belonging to the families
Anthophoridae, Halictidae, Megachilidae,
and Apidae (subfamily Meliponinae),
because of their foraging behavior, bring
about most fertilizations. The stingless bees
Trigona (s.l.) and Melipona, the most fre-
quent visitors to these trees, are known to
forage no more than 200 meters from their
colonial nests, and to be effective polli-
nators only where inter-tree distances be-
tween staminate and pistillate individuals
are relatively small. These social insects are
present year-round and are therefore highly
predictable pollinatory resources.
Phenology.-A survey of phenological
events displayed by trees of the study area
has been recently published (Frankie et al.,
1974). This study of seasonality of flower,
fruit and leaf production did not consider
dioecious species as a separate unit. For all
 TROPICAL TREES 173

•• _- •••••• Hermaphroditic and monoec i.ous species

30

- - - Dioecious species

25
....... .. .....

.,,
20
,
.~

c,
"-
,,
" 15
0

,
1
10 -..
~ '

N F' A J A

Hont h of the year

FIG. 2. Flowering seasonalities of dioecious, and hermaphroditic and monoecious species.

the trees as a group there are three flower- pistillate flowers. In addition, the flowering
ing peaks, two closely juxtapositioned peaks seasonalities of dioecious species also sug-
during early to middle dry season (January gest zoophily. The principal flowering peak
to March) and a third at the dry-wet season of many dioecious trees (Fig. 2) coincides
interface (April/May). When one con- with the onset of the rainy season, simul-
siders the phenological patterns shown by taneous with a major emergence of many
dioecious trees, as contrasted with those of small insects (Janzen, 1973). Furthermore,
hermaphroditic taxa, several striking con- Janzen has shown that during the later half
trasts are revealed with regard to flowering of the dry season, most small insects which
seasonality. As we can see from Figure 2, pass the dry season as adults become con-
flowering for dioecious species occurs during centrated in riparian areas where most
two periods; a small number of species dioecious trees are concentrated.
flower during the first dry season peak, The fact that as many as 53% of the trees
while the majority flower at the dry-wet in a tropical forest have unisexual flowers
interface. and animals as pollen vectors makes it
obvious that unisexual flowers in these trees
DISCUSSION have not evolved in response to selec-
The flower morphology and pollination tive pressure for wind-pollination as has
biology of dioecious tropical tree species been suggested for temperate plants by
indicate that these species are insect-polli- Grant (1951) and Stebbins (1951).
nated. Floral morphology, though unspe- Further, although many unisexual plants
cialized, is adapted for small pollen vectors of the north temperate zone are wind-
which are attracted first by the sticky pollinated, it is conceivable that a change
pollen or nectar in staminate, and later to from hermaphroditism to unisexuality pre-
the relatively large nectar reward of ceded the change from zoophily to ane-
174 K. S. BAWA AND P. A. OPLER
mophily. I t should also be noted that
anemophilous, unisexual flowers of many
temperate trees, such as a majority of the
Amentiferae, typically have no trace of the
opposite sex and an extremely reduced
perianth. On the other hand, unisexual
flowers of most entomophilous tropical
trees, such as those listed in Table 1, exhibit
either an aborted androecium or gynoecium
in pistillate and staminate flowers respec-
tively. Furthermore, the perianth, though
small in size as compared to hermaphroditic
flowers of related taxa, is not reduced to
the same extent as in temperate wind-
pollinated flowers. It is thus possible that
the two kinds of unisexual flowers are
products of differing selective pressures
associated with the different pollination
strategies. However, regardless of whether
selective pressures responsible for the evolu-
tion of unisexual flowers in zoophilous and
anemophilous species were the same or not,
there is still no plausible reason for sug-
gesting that the evolution of dioecism even
in temperate plants was in response to
anemophily.
If dioecism in tropical trees has not
arisen in response to wind-pollination, to
what factors can one attribute its origin?
In order to answer this question, we must
know (a) the nature of breeding systems
from which dioecism has evolved, and (b)
the adaptive significance of dioecism.
There are several evolutionary pathways
to the dioecious condition. It can arise from
gynodioecism (Ross, 1970) , monoecism
(Lewis, 1942), heterostyly (Baker, 1958)
and hermaphroditism (Baker, 1967; Raven,
1973). The particular pathway through
which a given taxon has evolved dioecism
can be determined only by comparative
studies of taxa that contain related species
with different breeding systems (see for
example, Lloyd, 1972a,b). Such studies,
particularly for trees, are largely lacking.
Nevertheless, with the possible exception of
Cordia collococca, C. panamensis, Genipa
caruto and Randia subcordata, where dioe-
cism has apparently arisen from a hetero-
morphic self-incompatible breeding system,
we believe that in a majority of investigated
taxa, dioecism has evolved from a breeding
system characterized by floral bisexuality
(hermaphroditism) and self-compatibility.
The original bisexual condition of these
flowers is still revealed by the presence of
an aborted gynoecium on staminate flowers
and an aborted androecium on pistillate
flowers. The evidence for self-compatibility
is indirect and rests on two arguments. One
line of reasoning, notwithstanding its
circular nature, is a corollary of the assump-
tion that the main selective force for the
evolution of dioecism has been pressure for
increased outcrossing; it follows that self-
fertilization was prevalent in the original
breeding system. The other argument rests
on the nature of dioecious flowers. A prob-
able explanation for the small, relatively
inconspicuous flowers of dioecious trees
would be that they represent the ancestral
condition; self-compatible species as com-
pared to related self-incompatible species
are known to have small, inconspicuous
flowers (Lewis, 1956; Lloyd, 1965). In
the remainder of this discussion, we will be
concerned primarily with the evolution of
dioecious from self-compatible breeding
systems.
As far as the adaptive significance of
dioecism is concerned, we feel the main
selective advantage of the dioecious habit is
due to its enforcement of outcrossing. The
number of flowers in the crown of a tree
is so large that intra-tree visits by the
pollinators are many times more than inter-
tree visits; under such circumstances, the
trees when subjected to selective pressure
for outcrossing are likely to evolve obligate
outcrossing mechanisms rather than dichog-
amy or monoecy which by themselves may
be inadequate to eliminate large scale self-
ing. However, obligate outcrossing in
addition to dioecy can also result from self-
incompatibility; one might therefore ask:
when selective pressure for outcrossing
arises, what determines whether a particular
taxon will acquire self-incompatibility or
dioecy? Here, we try to answer this ques-
tion, and, in so doing, attempt to elucidate
 TROPICAL TREES
factors responsible for the evolution and
maintenance of dioecism. Since our argu-
ments are highly speculative, they are
advanced in the form of hypotheses that
may then be tested through the collection
of appropriate experimental data. I t should
also be mentioned that the hypotheses given
below are not mutually exclusive.
Hypothesis I. The evolution of dioecism
is a simple genetic and physiological change
whereas the acquisition of self-incompati-
bility alleles is a complex process.-This
possibility was first suggested by Baker
(1967). Although experimental proof is
lacking and may be difficult to provide,
there is indirect evidence to support Baker's
contention. Whitehouse (1950) has sug-
gested that self-incompatibility has been
acquired only once in the evolution of angio-
sperms. Although Whitehouse's claim
appears to be exaggerated (Bateman,
1952), the fact that very broad taxonomic
alliances often have one or the other kind
(gametophytic or sporophytic) of self-
incompatibility system would seem to indi-
cate that the acquisition of self-incompati-
bility systems is a relatively rare event. On
the other hand, the relative ease with which
floral sexuality can be altered (for a review,
see Heslop-Harrison, 1972) indicates that a
change from hermaphroditism to dioecism
is easy to accomplish, and the widespread
distribution of dioecious species in families
that are exclusively or predominantly
hermaphroditic suggests that dioecism has
originated many times during the evolution
of flowering plants. Raven (1973) has
pointed out that in the New Zealand flora
many taxa have evolved dioecism in
response to selective pressure for outcross-
ing, whereas only a single species there is
presumed to have become self-incompatible
over the same period.
Hypothesis II. Dioecism is selected for
since under certain conditions it permits
greater pollination success than is allowed
for by a self-incompatible breeding system.
-In obligately outcrossed species, pollina-
tion efficiency, here defined as the amount
of floral resource expended in the fertiliza-
175
tion of an ovule, is largely determined by
the relative ease with which pollen is trans-
ferred from one plant to another. One
might expect that a low rate of inter-plant
movement by pollen vectors would reduce
pollination efficiency. Most tropical dioe-
cious trees have small flowers and relatively
small pollinators, mostly social bees which
might be expected to show less inter-plant
movement than do large pollinators such as
solitary bees, hawkmoths, and bats. Yet,
dioecism may be viewed as a mechanism
which more efficiently uses the small scale
inter-plant movement of these pollinators
for pollination success than does a self-
incompatible breeding system. For exam-
ple, a pistillate inflorescence receiving a
visit of a pollen-contaminated flower visitor
is likely to have most visited flowers suc-
cessfully pollinated. By contrast, a similar
visit by a visitor to an hermaphroditic
inflorescence may be less successful as the
flower's own pollen may either displace
compatible pollen carried from another tree
by the pollen vector or limit the space for
it on the stigma.
Another way by which pollination effi-
ciency may be increased in dioecious species
is by increased inter-plant movement of
pollinators brought about by the spatial
and temporal variation in the nature
and amount of floral reward presented.
Although staminate plants offer both pollen
and nectar, pistillate plants offer only
nectar and in greater amounts concentrated
in fewer flowers than staminate plants.
Temporal variation is introduced as stami-
nate plants offer their rewards earlier in the
day than do pistillate plants. This also
suggests that inter-plant movement of polli-
nators, during the same or sequential
foraging trips, is most likely from a stami-
nate to a pistillate plant.
Finally, the average inter-plant distance
for reproductive individuals may be reduced
for dioecious species, while maintaining the
same optimal inter-plant distance between
seed-bearing individuals as for less closely
aggregated hermaphroditic taxa (d. Janzen,
1970). Thus higher population densities of
176 K. S. BAWA AND P. A. OPLER
TABLE 5. Fruit flower ratio in some dioecious and
self-incompatible species.
Species Fruit/Flower ratio
Dioecious species
Coccoloba caracasana .423
C. padijormis .166
Cordia collococca .213
Simarouba glauca .180
Trichilia columina' .335
Self-incompatible,
hermaphroditic species
Andira inermis .008
Dalbergia retusa .085
Lonchocarpus eriocarinalis .035
Piscidia carthagenensis .203
Pterocarpus rohrii .089
Value of t = 1.47 (N.S.)
'Three seeds per fruit.
dioecious taxa would suffer levels of seed
destruction no greater than for hermaph-
roditic species, and yet at the same time
inter-plant distances are decreased for dioe-
cious populations enhancing the inter-plant
movement of their small pollinators.
The above assumptions would lead us to
expect (a) a higher incidence of dioecism
among species with relatively small flowers
and small pollinators than among species
~th large flowers and large pollinators, (b)
higher pollination efficiency in dioecious
species than for self-incompatible species
under comparable conditions of population
density? floral reward, and pollinators, and
(c) a higher degree of clumping in dioecious
species than for hermaphroditic self-
incompatible species. ' flowers pollinated, but also of the amount of
The first expectation appears to be
realized by data presented in Figure 1.
However, it should be noted that not all
species with small flowers and pollinators
are likely to acquire a dioecious breeding
system when subjected to increased selective
pressure for outcrossing. Certainly some
taxa might evolve self-incompatibility by
an accompanying change in some other
parameter of their reproductive biology.
For example, an increase in flower size
would attract large pollinators that forage
over long distances. Close aggregation of
flowers to form a large unit of floral reward
might also give similar results. In addition,
Mean
or alternatively, ovule number might be
increased so that the effects of a successful
pollination effort are fully exploited by the
production of a large number of seeds per
fruit.
.263 There are two sets of data which indicate
that the second expectation is realized. If,
in species with one seed per fruit the
fruit/flower ratio is taken as a measure of
pollination efficiency, then we observe that
this ratio is much higher for dioecious
species than for self-incompatible species
.084 (Table 5). However, differences are not
statistically significant and one probable
reason for this is that all self-incompatible
species in Table 5 have flower size much
larger than any of the dioecious species
included in the sample, and are pollinated
by large solitary bees. Thus, they may have
pollination efficiency greater than what
might be expected if the flower size and
pollinator foraging ranges were comparable
to dioecious species. The second set of data
derives from gynodioecious species in which
pistillate plants often produce a larger
proportion of fruits than do hermaphroditic
plants (Darwin, 1877; Ludwig, 1879;
Burrows, 1960; but for the opposite view
see Vaarama and ]aaskelainen, 1967) .
However, several objections can be raised to
the use of these data as evidence for the
putatively greater pollination efficiency of
dioecious taxa. First, the fruit/flower ratio
is not only a function of the number of
metabolites available for maturation of
fruits and the degree of flower and fruit
mortality due to feeding by animals. The
relative contribution of these factors to the
fruit/flower ratios presented in Table 5 is
unknown. Secondly, differences in the
fruit/flower ratio can also be accounted for
by variation due to apomictic tendencies
and the average distance between con-
specific individuals. A third objection is
that the fruit/flower ratio in dioecious
species must be adjusted to include the
 TROPICAL TREES 177

negative contribution of staminate plants. pressure from seed predators, any mutation
Theoretically, this adjustment would not causing a change from hermaphroditism to
be difficult to make, but sex ratios of trop- dioecism is likely to carry a high selective
ical dioecious taxa are often skewed from value.
unity (Opler and Bawa, in prep.), a Any postulated increase in net reproduc-
phenomenon which injects further uncer- tive output resulting from enhanced escape
tainty into the calculation of absolute from seed predation (and increased polli-
fruit/flower ratios. It should also be men- nation efficiency) could offset negative
tioned that pollination efficiency as defined effects on reproductive output resulting
here takes into account quantitative, but from having only about half the members of
ignores qualitative, aspects of pollen flow. a population bear seeds.
From a selective point of view, if both Hypothesis IV. Dioecism may be
aspects are taken into consideration, a plant selectively advantageous since sexually
with high fruit/flower ratio can have lower dimorphic species-populations exploit a
pollination efficiency than a plant with low wider variety of microhabitats than
fruit/flower ratio, provided the latter has sexually monomorphic species-populations.
been pollinated by a larger number of -In dioecious species, males spend a
genotypes (Janzen, pers. comm.). smaller proportion of their energy towards
As far as the third expectation is con- sexual reproduction and a greater propor-
cerned, relevant data on comparative tion towards vegetative growth and repro-
dispersion patterns of dioecious and self- duction than do females (Putwain and
incompatible species are not available. Harper, 1972). This is a consequence of the
Hypothesis III. Dioecism is favored increased energetic cost of seed production
since increased seed set, a consequence of by females. Thus, males might be expected
dioecism, can provide an escape from seed to exploit a wider variety of microhabitats
predators (we use this term in the strict than females. However, in trees which
sense as intended by Janzen (1970) for devote a relatively small proportion of
seed feeding insects whose ecological effects energy to reproduction in contrast with
are analogous to insect parasi toids) .-This herbs, the presumed greater versatility of
hypothesis rests on the assumption that males than females in habitat exploitation
dioecism leads, whatever the mechanism, to may be questioned.
an increase in the size of seed crop, and
from this stem further assumed advantages SUMMARY
(Janzen, 1971). Thus, it complements the
In tropical lowland forests, one fourth to
preceding hypothesis. Janzen has discussed
one half of all species have unisexual
in detail the effect of large seed crop and
the increased distance between seed bearing flowers, and a majority of such species are
dioecious. Almost all dioecious species have
individuals, the two consequences of dioe-
relatively small (::S; 1.0 ern in length and
cism, on the probability of escaping seed
breadth) pale yellow to pale green flowers.
predation in tropical forests, and those
Field observations of selected species
arguments need not be repeated here. How-
indicate that a large number of dioecious
ever, we wish to emphasize that to the species are pollinated by small bees
extent that the individuals with the largest such as various species of Anthophoridae,
seed crops have an increasing likelihood of Halictidae, Megachilidae and Meliponinae,
contributing the genotypes to the next while a small number is pollinated by
generation, seed predators may directly moths. In the light of the high incidence
select for dioecism since, regardless of of dioecism and the prevalence of ento-
pollination efficiency, on energetic grounds mophily in tropical trees, it is suggested
it is one of the most effective ways to that as far as tropical trees are concerned,
increase seed crop size. Thus, under intense anemophily cannot be invoked to explain
178 K. S. BAWA AND P. A. OPLER
the origin of dioecism (and monoecism)
as has been done for temperate plants. In
order to explain the evolution of dioecism in
tropical trees, it is postulated that, with the
exception of a few taxa where dioecism has
evolved from heterostyly, in a majority of
investigated species dioecism has probably
evolved from a self-compatible breeding
system in response to selective pressure for
outcrossing. The main question on which
attention is focused is: When selective
pressure for outcrossing arises, what favors
the evolution of dioecy over self-incompati-
bility? Four specific hypotheses are
proposed which provide possible answers to
the question. These are based on the
assumptions of relative ease with which
dioecism can arise, increased pollination
success allowed by dioecism under certain
conditions, enhanced escape from seed
predators under a dioecious breeding system
and the ability of dioecious species to exploit
a wider variety of microhabitats than
hermaphroditic species.
ACKNOWLEDGMENTS
The study was supported by NSF grant
GB-25592 and was conducted under the
auspices of the Organization for Tropical
Studies. One of us (KSB) also acknowl-
edges the support from the Bullard and
Cabot Foundations as well as the Atkins
Fund of Harvard University. The findings
reported in this paper are part of a larger
study on poIlination mechanisms and
breeding systems of tropical forest trees
being conducted jointly with H. G. Baker
and G. W. Frankie. We thank our col-
leagues for their generous help in all aspects
of this work. The manscript has benefited
much from the comments of H. G. Baker,
G. W. Frankie, S. P. Hubbell, S. K. Jain,
D. H. Janzen, D. M. Porter, P. H. Raven,
O. T. Solbrig, P. R. Stevens and P. B.
Tomlinson. We are grateful to the W.
Hagnauer family and D. Stewart Wilson
for allowing us to work on their property,
and to Jorge Campabadal and his staff for
welcome logistic support.
LITERATURE CITED
ASHTON, P. S. 1969. Speciation among tropical
forest trees: some deductions in the light of
recent evidence. BioI. J. Linn. Soc. 1:155-196.
BAWA, K. S. 1974. Breeding systems of tree
species of a lowland tropical community.
Evolution 28:85-92.
BAKER, H. G. 1948. Corolla-size in gynodioecious
and gynomonoecious species of flowering
plants. Proc. Leeds Phil. Soc. (Sci. Sect.) 1948:
136-139.
- - . 1958. Studies on the reproductive biology
of West African Rubiaceae. ]. West African
Sci. Ass. 4:9-22.
- - . 1967. Support for Baker's law-as a rule.
Evolution 21:853-856.
BATEMAN, A. J. 1952. Self-incompatibility sys-
tems in angiosperms. Heredity 6:285-310.
BRAUN, E. L. 1950. Deciduous forests of Eastern
North America. Blakiston, Philadelphia, 596 p.
BURROWS, D. J. 1960. Studies in Pimelia. I.
The breeding system. Trans. Roy. Soc. Xew
Zealand (Botany) 1:217-223.
CARLQUIST, S. 1966. The biota of long distance
dispersal. IV. Genetic systems in the flora of
oceanic islands. Evolution 20:433-455.
DARWIN, C. 1877. The different forms of flow-
ers on plants of the same species. Murray,
London, 352 p.
DAUBENMIRE, R. 1972. Phenology and other
characteristics of a tropical semi-deciduous
forest in Northwestern Costa Rica. J. Ecol.
60: 147-170.
FRANKIE, G. W., H. G. BAKER, AXD P. A. OPLER.
1974. Comparative phenological studies of
trees in tropical wet and dry forests in the
lowlands of Costa Rica. J. Ecol. 62:881-919.
GRANT, V. 1951. The fertilization of flowers.
Sci. Amer. 184:52-56.
HESLOP-HARRISON, J. 1972. Sexuality of angio-
sperms, p. 133-289. In F. C. Steward (ed.)
Plant physiology-a treatise 6c. Academic
Press, New York.
HOLDRIDGE, L. R, W. C. GRENKE, W. H.
HATHEWAY, T. LIANG, AND J. A. TOSI, JR.
1971. Forest environments in tropical life
zones: a pilot study. Pergamon Press, New
York, 747 p.
JANZEN, D. H. 1970. Herbivores and the num-
ber of tree species in tropical forests. Amer.
Natur. 104:501-528.
- - . 1971. Seed predation by animals. Ann.
Rev. Ecol. Sys, 2 :465-492.
- - . 1973. Sweep samples of tropical foliage
insects: effect of seasons, vegetation types,
elevation, time of day and insularity. Ecology
54: 687-701.
JONES, E. W. 1955. Ecological studies on the
rain forest of Southern Nigeria IV. The
 TROPICAL TREES
plateau forest of the Okomu Forest Reserve.
J. Ecol. 43: 564-594.
LEE, H. Y. 1967. Study of Swietenia (Meliaceae)
-an observation on the sexuality of flowers. J.
Arnold Arbor. 48: 101-104.
LEWIS, D. 1942. The evolution of sex in flower-
ing plants. BioI. Rev. 17:46-67.
1956. Genetics and plant breeding. Brook-
haven Symp. BioI. 9:89-100.
LLOYD, D. G. 1965. Evolution of self-compati-
bility and racial differentiation in Leaven-
worthia (Cruciferae). Contr. Gray Herb. 195:
3-134.
- - . 1972a. Breeding systems in Cotula L. I.
The array of monoclinous and diclinous sys-
tems. New Phytol. 71:1181-1194.
1972b. Breeding systems in Cotula L. II.
Monoecious populations. New Phytol. 71:
1195-1202.
LUDWIG, F. 1879. Uber die Bllitenformen von
Plantago lanceolata und die Erscheinung der
Gynodibcie-c-Z. des Naturw. LII. Folge, 4:
441--449.
MCCOMB, J. A. 1966. The sex form of species in
the flora of the southwest of Western Australia.
Australian J. Bot. 14:303-316.
PUTWAIX, P. D., AND J. L. HARPER. 1972. Studies
in the dynamics of plant populations. V. Mech-
anisms governing the sex ratios in Rumex
acetosa and R. acetosella. J. Ecol. 60: 113-129.
RA\"E!\" , P. H. 1973. Evolution of subalpine and
179
alpine plant groups in New Zealand. New
Zealand J. Bot. II: 177-200.
Ross, M. D. 1970. Evolution of dioecy from
gynodioecy. Evolution 24:827-828.
STEBBINS, G. L. 1951. Natural selection and
differentiation of angiosperm families. Evolu-
tion 5: 299-324.
STYLES, B. T. 1972. The flower biology of the
Meliaceae and its bearing on tree breeding.
Silv. Genet. 21: 175-182.
TOMLINSON, P. B. 1974. Breeding mechanisms in
trees native to tropical Florida; a morpho-
logical assessment. J. Arnold Arbor. 55: 269-
290.
TOMLINSON, P. B., AND P. FAWCETT. 1972. Dio-
ecism in Citharexylum (Verbenaceae). J.
Arnold Arbor. 53 :386-389.
VAARAMA, A., AND O. JAiiSKELAINEN. 1967. Studies
on gynodioecism in the Finnish populations of
Geranium silvaticum L. Ann. Acad. Sci. Fenn.
Ser. A. Biologica 108:3-39.
WHITEHEAD, D. R. 1969. Wind pollination in
the angiosperms: evolutionary and environ-
mental considerations. Evolution 23:28-35.
WHITEHOUSE, H. L. K. 1950. Multiple allelo-
morph incompatibility of pollen and style in
the evolution of angiosperms. Ann. Bot. N. S.
14: 199-216.
YAMPLOSKY, c., AND H. YAMPLOSKY. 1922. Dis-
tribution of sex forms in the phanerogamic
flora. Bibl. Genet. 3: 1-62.