Botanical Studies (2008) 49: 261-276.

*

Corresponding author: E-mail: jmhu@ntu.edu.tw; Tel:

+886-2-33662472; Fax: +886-2-23686750.

INTRODUCTION

The ecological correlates and the potential driving

forces for the evolution of dioecy in plants have been

debated intensively over the past decades. The traditional

view suggests that dioecy has evolved mainly because

it guarantees outcrossing to avoid the drawback of

inbreeding depression (Charlesworth and Charlesworth,

1978; Lewis, 1941; Thomson and Barrett, 1981). Other

studies indicate that sexual specialization, resource

reallocation, and/or other ecological factors may also be

behind the evolution of dioecy, under which males and

females can have higher fitness than their hermaphroditic

counterparts (Bawa, 1980; Brunet and Charlesworth, 1995;

Freeman et al., 1997; Givnish, 1980; Thomson and Brunet,

1990). Despite the advantages of having separate sexes,

dioecious plants are not common, and estimates as low as

3-4% (Yampolsky and Yampolsky, 1922) or 6% (Renner

and Ricklefs, 1995) in angiosperms. However, the actual

incidents of dioecy in the local flora are variable, ranging

from 2.8% in California (Fox, 1985) to as high as 14.7%

in Hawaii (Sakai et al., 1995b).

The evolution and maintenance of dioecy has been

associated with several ecological and life history

attributes. Among these are: woodiness (Bullock, 1985;

Conn et al., 1980; Flores and Schemske, 1984; Fox,

1985; Freeman et al., 1980b; Givnish, 1980; Sakai et

al., 1995b; Webb et al., 1999), climber growth (Renner

and Ricklefs, 1995), small, inconspicuous, or greenish

flowers (Fox, 1985; Ibarra-Manriquez and Oyama, 1992),

unspecialized pollinators (Baker and Cox, 1984; Ibarra-

Manriquez and Oyama, 1992), wind pollination (Freeman

et al., 1980b; Renner and Ricklefs, 1995), fleshy fruits

(Flores and Schemske, 1984; Givnish, 1980; Ibarra-

Manriquez and Oyama, 1992; Webb et al., 1999), tropical

floras (Bawa and Opler, 1975; Givnish, 1980; Sobrevila

and Arroyo, 1982), and island habitats (Abe, 2006; Baker

and Cox, 1984; Bawa, 1980; Sakai et al., 1995a, b). Many

of these ecological traits are not necessarily the causal

factors of dioecy, and some have only been studied in a

small local flora, and the validity of these correlations

has been questioned (Fox, 1985; Renner and Ricklefs,

1995; Steiner, 1988). Recent studies using phylogenetic

analysis to examine the correlations between dioecy and

those ecological attributes have shown that although

many dioecious clades are species poor, they are strongly

associated with traits like tropical distribution, woody

growth form, abiotic pollination, small inconspicuous

flowers and inflorescences, and fleshy fruits (Vamosi et al.,

2003). In addition, dioecious lineages with more of these

traits showed a higher relative species richness upon sister-

group phylogenetic analysis, particularly those that had a

tropical distribution or fleshy fruits (Vamosi and Vamosi,

2004).

Incidences and ecological correlates of dioecious

angiosperms in Taiwan and its outlying Orchid Island

Yu-Hsin TSENG, Chang-Fu HSIEH, and Jer-Ming HU*

Institute of Ecology and Evolutionary Biology, National Taiwan University, Taipei, Taiwan 106

(Received May 29, 2007; Accepted March 31, 2008)

ABSTRACT

. Sexual systems, particularly dioecy, and the habit correlations were examined for 3052 native

angiosperms in Taiwan and 689 species from its outlying Orchid Island, and compared among different

vegetation types. The majority of angiosperms in Taiwan are hermaphrodites (74.4%, N = 2272), followed

by monoecious taxa (11.2%, N = 341), and then dioecious taxa (7.9%, N = 240) and polygamous taxa (6.5%,

N = 199). The incidence of dioecy in Taiwan (7.9%) and Orchid Island (11.9%, N = 82) exceeded world

averages, but was lower than that of most tropical oceanic islands. Dioecy in Taiwan and Orchid Island is

strongly associated with woodiness, and is over represented in trees and climbers, but not in shrubs. In woody

taxa, 175 of 1,005 (17.4%) taxa are dioecious while only 65 of 2,047 (3.2%) herbaceous taxa are dioecious

in Taiwan. The percentages of dioecy decrease with increasing altitude in Taiwan. The percentages of

dioecy varied among the six selected vegetation types in Taiwan, from 14.1% in the Linkou Laterite Terrace

secondary forest to 23.9% in the Nanjenshan plot, the highest percentage ever found in a forest plot.

Keywords: Dioecy; Flora; Orchid Island; Sexual system; Taiwan.

REPRODUCTIVE BIOLOGY

262

Botanical Studies, Vol. 49, 2008

Furthermore, dioecy has been demonstrated to be

more frequent in certain plant community types, such as

tropical forests (Bawa and Opler, 1975; Bawa et al., 1985;

Matallana et al., 2005; Momose et al., 1998), mountain

cloud forest in Venezuela (Sobrevila and Arroyo, 1982),

tropical semi-deciduous forest in Mexico (Bullock, 1985),

and some communities of the semiarid Intermountain West

in California (Freeman et al., 1980b). However, a high

incidence of dioecy has not been found associated with

certain community types in other tropical floras, such as

Puerto Rico (Flores and Schemske, 1984), palm swamps

in Venezuela (Ramirez and Brito, 1990), or dry forests

in Caatinga, Brazil (Machado et al., 2006). Most studies

of dioecy incidents were conducted for tropical floras,

particularly in the New World, and little has been studied

in Asia or subtropical regions.

Taiwan is a subtropical island on the western edge of the

Pacific Ocean about 200 km east of Fujien Province on the

Chinese mainland and 360 km north from Luzon Island in

the Philippines (Hsieh and Shen, 1994). The dry land mass

of Taiwan was formed during the Miocene as an island, but

is generally believed to have been connected to mainland

China during four glacial periods of the late Quarternary

and then disconnected permanently at the end of the last

glacial period around 0.01 million years ago (Shen, 1994).

The flora of Taiwan is then largely comprised of taxa

originating from mainland China and also from Japan

and the Philippines (Hsieh et al., 1994). According to the

comparison of nonendemic species in seed plants among

Taiwan and adjacent areas, 48.2% of total nonendemic

species in Taiwan are also spread throughout China, which

is higher than those in Japan (27.9%), Korea (9.6%), India

(15.8%), or in the Philippines (16.4%) (Ying and Hsu,

2002). Taiwan is a high mountain island of about 35,800

km

2

, and 30% of the landmass is 1,000-3,000 m above

sea level. Due to complex landscapes and the influence

of monsoons, the vegetations of Taiwan contain elements

from tropic, temperate, and even sub-arctic climates (Hsieh

et al., 1994). Therefore, predicting the incidence of dioecy

in the flora of Taiwan based on the overall habitat and

without considering the history of the flora is difficult.

It is reasonable to assume the plants that migrated

through a land-bridge between Taiwan and the Eurasia

landmass are mostly temperate components because

the weather was cold during these glacial periods when

the two lands were connected. These plants eventually

retreated to the higher altitudes of Taiwan as the weather

warmed around 10,000 years ago, the sea level rose, and

the ¡¥land-bridge¡¦ disappeared (Shen, 1994). As a result,

the majority of the lowland flora of Taiwan likely migrated

to Taiwan without any available land-bridge, i.e. they

came through long distance dispersal later than 10,000

years ago. If the incidence of dioecy is associated with

long-distance dispersal and/or tropical elements, then the

lowland flora of Taiwan should have a higher percentage

of dioecious plants.

The sexual systems in Taiwan¡¦s flora have never been

extensively studied, and most of the data are only present

in taxonomic description from the Flora of Taiwan. Here

we provide the first synopsis of sex expression data of

native angiosperms in Taiwan based on the species list

from the second edition of the Flora of Taiwan (Huang

and Editorial Committee of the Flora of Taiwan, 1993,

1996, 1998, 2000, 2003) and the recent literature. We also

conducted a separate analysis for Orchid Island (Lanyu),

a subsidiary islet about 90 km to Taiwan¡¦s southeast,

for comparison. Furthermore, seven plots of different

vegetation types in Taiwan were selected and compared

to other studies, to examine incidences of dioecy and the

correlations to plant habit.

MATERIALS AND METHODS

Data sources

The species list for this study was based on the

second edition of the Flora of Taiwan (Huang and

Editorial Committee of the Flora of Taiwan, 1993,

1996, 1998, 2000, 2003) and recent taxonomic revisions

(supplementary data 1). Only native angiosperms in

Taiwan were recorded. Gymnosperms, naturalized plants,

and cultivars were excluded in this study. To reduce double

counts at the infraspecific level, only one record will be

used for those with more than one variety, subspecies,

and forma because there is usually no variability in the

category of the sexual system within species (Sakai et al.,

1995a).

Sexual systems

Characterization of sexual expression for these

taxa was based largely on the descriptions in the

Flora of Taiwan (Huang and Editorial Committee of

the Flora of Taiwan, 1993, 1996, 1998, 2000, 2003)

and reports mentioned in the previous section. Plant

sexual systems in our study were divided into four

categories: hermaphroditic, dioecious, monoecious, and

polygamous. Species were recorded as hermaphroditic

when they had bisexual flowers (definitions sensu Bawa,

1980). Species described as monoecious or dioecious

were considered monoecious since ¡¥dioecious¡¦ records

sometimes reflect dichogamous expression of unisexual

flowers, i.e., male and female flowers open at different

times. Species listed as ¡¥dioecious or rarely monoecious,¡¦

and ¡¥functionally dioecious¡¦ were treated as dioecious.

Species described as andromonoecious, gynomonoecious,

androdioecious, polygamo-dioecious, polygamous-

monoecious, ¡¥dioecious or hermaphrodites¡¦, ¡¥dioecious or

polygamous¡¦, ¡¥monoecious or polygamous¡¦, ¡¥dioecious

or hermaphrodites or polygamous¡¦, and ¡¥dioecious

or monoecious or polygamous¡¦ were all recorded as

polygamous. The exclusion of that information is

necessary to maintain consistency in counting since

only a few taxa have been studied quantitatively for

floral types in Taiwan, and the majority of the species in

Taiwan¡¦s flora have no detailed sexual system information.

TSENG et al. ¡X Dioecy in Taiwan and Orchid Island

263

Twenty-five species with uncertain sexual systems in

Taiwan and Orchid Island were excluded due either to

the absence of a description or to one that is controversial

(see supplementary data 2). The species list and sexual

expression for the flora of Taiwan and Orchid Island were

treated separately.

Growth forms were categorized into four types: trees,

shrubs, herbs, and climbers based on the description in

the Flora of Taiwan of each species¡¦ predominant mature

morphology. Plants listed as small trees and large trees

were both recorded as trees while those listed as shrub

or shrublet were recorded as shrubs. Both herbaceous

and woody vines were scored together as climbers in

habit analysis or scored separately in the analysis for

woodiness. The herbs in our analysis included annual and

perennial herbs, regardless of whether they were parasites,

epiphytes, or aquatic plants. Trees, shrubs and woody

vines were grouped together as ¡¥woody,¡¦ and herbaceous

plants and herbaceous vine were grouped as ¡¥herbaceous¡¦

accordingly.

In comparison with the dioecy percentage in Taiwan

and other areas, we reviewed the data from different

islands and continental areas. We also compared the sexual

systems among different vegetation types from tropical

and temperate areas, including seven plots with detailed

vegetation information in Taiwan and Orchid Island.

Two of the seven study sites in Taiwan, Nanjenshan plot

I (Hsieh et al., 1992) and Nanjenshan plot II (Hsieh et

al., 1996), are at the Nanjenshan Long-Term Ecological

Research (LTER) site in southern Taiwan. The former is

a subtropical evergreen broad-leaved/seasonal forest of 3

hectares at an altitude of 300 to 340 m. Nanjenshan plot II

is a tropical seasonal forest about 2.1 hectares at an altitude

of 225-275 m. The third, a 25-hectare Fushan Forest

Dynamics Plot, is another LTER plot in northern Taiwan,

categorized as a subtropical rain forest. The forth transect

at Lopeishan is a warm temperate forest, and its altitude

ranges from 650 m in the Manyuehyuan to 1270 m on the

hillsides of a Fagus-dominated forest (Hsieh et al., 1998).

The fifth plot is the Kwangin Coastal Nature Reserve

located in the Ficus-Machilus zone of a subtropical rain

forest (Huang et al., 1991). Although this reserve plot is

near the coast, the number of seashore plants is relatively

small because it contains steep rocky slopes and does not

have a wide beach. The sixth is Linkou Laterite Terrace

Secondary Forest, which is composed of natural forests,

secondary forests, and a few plantations, categorized as a

semi-evergreen forest (Li and Huang, 1987). We included

Orchid Island, which is a 45 km

2

volcanic island off the

southeastern coast of Taiwan in the Pacific Ocean, and it

is considered to have the most tropical elements anywhere

in Taiwan or in its adjacent islands (Hsieh et al., 1994).

We recorded all angiosperm species from Orchid Island as

a whole based on their description in the Flora of Taiwan

(Huang and Editorial Committee of the Flora of Taiwan,

1993, 1996, 1998, 2000, 2003).

In order to further elucidate the correlations between

sexual systems and climatic zones, the sexual systems in

different climatic zones of Taiwan were recorded. On basis

of the definition by Su (1984), we analyzed six climatic

zones equivalent to vegetation zones in Taiwan: tropics,

subtropics, warm-temperate, temperate, cool-temperate,

and cold-temperate.

Data analysis

The distributions of sex expressions according to

life-forms were compared by chi-square tests with

Yates¡¦s correction factor. The analyses were performed for

different sexual systems on each of the categories of life

forms in corresponding columns. The null hypothesis was

that the frequency distribution of sexual systems was not

significantly different among different life-forms compared

to those of the entire flora.

RESULTS AND DISCUSSION

Sexual systems in Taiwan and Orchid Island

Our analysis is the first to examine the frequency

of sexual systems among angiosperms in Taiwan and

Orchid Island. Of the 3052 native species surveyed in

this study of Taiwan, 240 (7.9%) are dioecious, 341

(11.2%) are monoecious, 199 (6.5%) are polygamous,

and 2272 (74.4%) are hermaphrodite. At the family level,

9 of the 181 families (5.0%) in Taiwan¡¦s flora contain

only dioecious taxa; two of them (Daphniphyllaceae

and Salicaceae) are exclusively dioecious worldwide

while the other seven (Aquifoliaceae, Dioscoreaceae,

Ebenaceae, Icacinaceae, Menispermaceae, Pandanaceae,

and Smilacaceae) have mixed sex expression types within

the family although dioecy is usually the most common

type for those families. Eighteen of the 181 families (9.9%)

contain only monoecious taxa; five of them are exclusively

monoecious worldwide (Betulaceae, Ceratophyllaceae,

Sparganiaceae, Theligonaceae, and Typhaceae) while

the other 13 (Aceraceae, Begoniaceae, Buxaceae,

Callitrichaceae, Eriocaulaceae, Fagaceae, Juglandaceae,

Lardizabalaceae, Lemnaceae, Musaceae, Najadaceae,

Passifloraceae, and Zosteraceae) have mixed sex

expression types elsewhere. For the rest of the families, 99

of them are exclusively hermaphroditic, and the other 55

families have two or more mixed sex expression systems

within the family.

At the genus level, 85 of the 1120 genera (7.6%) in

Taiwan¡¦s flora contain one or more dioecious species, and

63 of them (74.1%) contain exclusively dioecious taxa

in Taiwan. In addition, since the majority of them (52

genera) contain only three or fewer species in Taiwan,

dioecy seems unassociated with diversification of the

flora. The most species-rich genera with exclusively

dioecious species are Ilex (21 spp.), Dioscorea (11 spp.,

Dioscoreaceae), Litsea (10 spp., Lauraceae), Smilax

(18 spp., Smilacaceae), and Eurya (13 spp., Theaceae).

In contrast, 87 of the 1120 genera in Taiwan contain

exclusively monoecious taxa, and the most speciose

264

Botanical Studies, Vol. 49, 2008

ones are Begonia (11 spp., Begoniaceae), Chamaesyce

(10 spp., Euphorbiaceae), Cyclobalanopsis (13 spp.,

Fagaceae), Pasania (13 spp., Fagaceae), and Pilea (13

spp., Urticaceae).

The chi-square test of the correlations between sexual

systems and life forms showed that dioecy is associated

with woodiness (P < 0.001) and hermaphroditism is

associated with an herbaceous habit (P < 0.001) (Table

2A). When analyzed with four life forms, the sexual

systems show significant correlations with all of them

(Table 2, N = 3052, df = 9, £q

2

= 422.3, P < 0.001). Dioecy

is significantly associated with trees, shrubs, and climbers,

and is strongly under-represented in the herbaceous taxa

in Taiwan (Table 2B, N

obs

= 24, compared with expected

N

exp

= 150.0). In comparison, monoecy is significantly

associated with trees (89 vs. expected 50.7), but negatively

associated with other life forms. Among 199 taxa listed as

¡¥polygamous¡¦, the association to life forms is less extreme,

but still significant (£q

2

= 11.7, P = 0.01, Table 2). Overall,

nearly half of the trees (42.3%) have unisexual flowers,

and very few herbaceous taxa are dioecious or monoecious

(11.9%). It is interesting to see that herbaceous vines have

a higher proportion of dioecious taxa than woody vines.

This is likely due to the inclusion of Smilax and Dioscorea

in the herbaceous vine category, both genera are species

rich and account for ~21% (29 species) of herbaceous

vines in Taiwan.

A strong correlation was found between dioecy and

Table 1. The incidence of dioecy in seed plants without introduced and naturalized species (unless noted) from various floras of

continental areas and islands.

Flora

Dioecy (%) No. of species Reference

CONTINENT AREAS

Portugal

2.0

2183 (Pires, 1947 in Baker and Cox, 1984)

California, USA

2.8

a

5421 (Freeman et al., 1980b)

Carolina, USA

3.5

b

3274 (Conn et al., 1980)

South Australia, Australia

3.9

2102 (Black, 1922-1952 in Parsons, 1958)

British Isles

4.3

c

, 4.4

d

1377

c

, 1380

d

(Kay and Stevens, 1986)

Alaskan arctic slope, USA

5.8

411

(Fox, 1985)

Cape flora, South Africa

6.6

c

, 6.7

d

8497

c

(Steiner, 1988)

ISLANDS

San Clemente Islands, USA

2.0

221 (Raven, 1963 in Baker and Cox, 1984)

Galapagos

3.0

439 (Wiggins and Porter, 1971 in Baker and Cox, 1984)

Reunion, Indian Ocean

4.0

838 (Cordemoy, 1985 in Baker and Cox, 1984)

Puerto Rico and the Virgin Islands

6.1

d

2037 (Flores and Schemske, 1984)

Taiwan

7.9

c

3052 This study

Seychelles, Indian Ocean

8.0

c

237 (Summerhayes, 1926 in Baker and Cox, 1984)

Barro Colorado Island, Panama

9.0

c

1212 (Croat, 1979 in Steiner, 1988)

Mauritius, Indian Ocean

11.0

682 (Baker, 1877 in Baker and Cox, 1984)

Orchid Island, Taiwan

11.9

c

689 This study

Ogasawara Islands, Japan

13.0

c

269 (Abe, 2006)

New Zealand

12-13

c

1813 (Godley, 1979)

Hawaii Islands, USA

14.7

c

971 (Sakai et al., 1995b)

Tonga, Pacific Ocean

16.0

404 (Yuncker, 1959 in Baker and Cox, 1984)

Samoa, Pacific Ocean

17.0

539 (Setchell, 1924 in Baker and Cox, 1984)

a

Including introduced species.

b

Including naturalized species.

c

Without gymnosperms.

d

With gymnosperms.

TSENG et al. ¡X Dioecy in Taiwan and Orchid Island

265

climbers (woody or herbaceous) in Taiwan, a point

rarely mentioned in the literature (Renner and Ricklefs,

1995). This association can be explained by a differential

selection for resource allocation to sexual functions

(Renner and Ricklefs, 1995). For example, females

of a dioecious climber, Dioscorea japonica Thunb.

(Dioscoreaceae) tend to pay a higher reproductive cost

than males, which implies a tradeoff between sexual

and vegetative reproduction (Mizuki et al., 2005). In

order to support heavy fruits, it is necessary to produce

a thicker, more slowly growing stem; in contrast, male

plants with pollen dispensing flowers would prefer to

grow on more exposed plant body (Renner and Ricklefs,

1995). In addition, long life spans in woody vines are

another likely explanation for the correlation with dioecy

because long-lived plants are favored for selection by

outbreeders compared with short-lived ones (Stebbins,

1950; Steiner, 1988; Matallana et al., 2005). Furthermore,

the distribution and frequency of dioecy in herbaceous

vines may also support this view, based on the fact that

40 out of 41 dioecious herbaceous vines in Taiwan are

perennial plants, including tuber or rhizomatous perennials

in Dioscoreaceae.

In comparison, Orchid Island has a higher percentage

of dioecious taxa (82 spp., 11.9%) than Taiwan (Table

3). There are 72 monoecious, 45 polygamous, and 490

hermaphroditic taxa on Orchid Island. Two families,

Cecropiaceae (1 sp.) and Myristicaceae (2 spp.), are not

found in Taiwan, and all three species are dioecious. The

incidence of dioecy in both Taiwan (7.9%) and Orchid

Island (11.9%) exceeds the estimates from most of the

continental floras (Table 1). The dioecy percentage in

Table 2. Frequencies of sexual systems in Taiwan¡¦s flora and the associations with different life forms to (A) Woodiness and (B)

Habit, and to (C) Total flora. The observed (N

obs

) and expected (N

exp

) numbers of species under different categories of life forms are

shown. The percentage corresponding to total species numbers are shown in parentheses.

(A)

Woodiness

Sexual system

Dioecy

Monoecy

Polygamy

Hermaphrodite

Life form No. species N

obs

N

exp

N

obs

N

exp

N

obs

N

exp

N

obs

N

exp

Woody

1005 175 (5.7%) 79.0 126 (4.1%) 112.3 55 (1.8%) 65.5 649 (21.3%) 748.2

Herbaceous 2047

65 (2.1%) 161.0 215 (7.0%) 228.7 144 (4.7%) 133.5 1623 (53.2%) 1523.8

£q

2

= 172.0, P < 0.001 £q

2

= 2.3, P = 0.11 £q

2

= 2.3, P = 0.11 £q

2

= 19.4, P < 0.001

(B)

Habit

Sexual system

Dioecy

Monoecy

Polygamy

Hermaphrodite

Life form No. species N

obs

N

exp

N

obs

N

exp

N

obs

N

exp

N

obs

N

exp

Trees

454 103 (3.4%) 35.7 89 (2.9%) 50.7 29 (1.0%) 29.6 233 (7.6%) 338.0

Shrubs

350

38 (1.2%) 27.5 29 (1.0%) 39.1 9 (0.3%) 22.8 274 (9.0%) 260.6

Herbs

1908

24 (0.8%) 150.0 204 (6.7%) 213.2 142 (4.7%) 124.4 1538 (50.4%) 1420.4

Climbers

340

75 (2.5%) 26.7 19 (0.6%) 38.0 19 (0.6%) 22.2 227 (7.4%) 253.1

£q

2

= 323.9, P < 0.001 £q

2

= 41.4, P < 0.001 £q

2

= 11.3, P = 0.01 £q

2

= 45.7, P < 0.001

(C)

Total

Sexual system

Dioecy

Monoecy

Polygamy

Hermaphrodite

No. species

N

obs

N

obs

N

obs

N

obs

3052

240 (7.9%)

341 (11.2%)

199 (6.5%)

2272 (74.4%)

266

Botanical Studies, Vol. 49, 2008

Taiwan¡¦s flora is within that of tropical and temperate

islands and a bit lower than that of other subtropical

islands like Norfolk island (12%) and New Zealand

(12-13%) (Baker and Cox, 1984).

The association of sexual systems with different

life forms in Orchid Island resembles what has been

observed in Taiwan (Table 3). Dioecy is associated with

woodiness (N = 71, P < 0.001), and hermaphroditism is

associated with herbs (N = 298, P = 0.014) (Table 3A). In

comparison with the plants of Taiwan, the sexual systems

only show significant correlations with dioecism and

hermaphroditism in Orchid Island (Table 3B). Dioecy is

significantly associated with trees and climbers, and is

strongly under-represented in shrubs and herbaceous taxa

(Table 3B).

A strong correlation has been demonstrated between

the level of dioecism and both proximity to the equator

and maximum island height, which is an indicator of

potential habitat diversity (Baker and Cox, 1984). Our

result shows that the percentage of dioecy in Taiwan¡¦s

flora follows this rule since Taiwan is at the Tropic of

Cancer and the highest point is near 4,000 m. However,

Taiwan is a continental island and may show a different

pattern from that of other oceanic islands listed in Baker

and Cox (1984). The plants in oceanic islands, islands that

separated from the landmass more than 45 million years

ago, are mostly comprised of colonists of long distance

dispersal regardless of whether they are at lowland or

mountain regions of the island (Sakai et al., 1995b). This

is the reason why the proportions of dioecy for the woody

plants of lowland and montane Hawaii are very similar

Table 3. Frequencies of sexual systems in Orchid Island¡¦s flora and the associations with different life forms to (A) Woodiness and

(B) Habit, and to (C) Total flora. The observed (N

obs

) and expected (N

exp

) numbers of species under different categories of life forms

are shown. The percentage corresponding to total species numbers are shown in parentheses.

(A)

Woodiness

Sexual system

Dioecy

Monoecy

Polygamy

Hermaphrodite

Life form No. species N

obs

N

exp

N

obs

N

exp

N

obs

N

exp

N

obs

N

exp

Woody

308

71 (10.3%) 36.7 30 (4.4%) 32.2 15 (2.2%) 20.1 192 (27.9%) 219.0

Herbaceous 381

11 (1.6%) 45.3 42 (6.1%) 39.8 30 (4.4%) 24.9 298 (43.3%) 271.0

£q

2

= 56.5, P < 0.001 £q

2

= 0.2, P = 0.60 £q

2

= 1.9, P = 0.13 £q

2

= 5.8, P = 0.014

(B)

Habit

Sexual system

Dioecy

Monoecy

Polygamy

Hermaphrodite

Life form No. species N

obs

N

exp

N

obs

N

exp

N

obs

N

exp

N

obs

N

exp

Trees

158 49 (7.1%) 18.8 18 (2.6%) 16.5 11 (1.6%) 10.3 80 (11.6%) 112.4

Shrubs

82

5 (0.7%) 9.8 10 (1.5%) 8.6 2 (0.3%) 5.4 65 (9.4%) 58.3

Herbs

348

2 (0.3%) 41.4 41 (6.0%) 36.4 29 (4.2%) 22.7 276 (40.1%) 247.5

Climbers

101 26 (3.8%) 12.0 3 (0.4%) 10.6 3 (0.4%) 6.6 69 (10.0%) 71.8

£q

2

= 104.6, P < 0.001 £q

2

= 6.4, P = 0.095 £q

2

= 5.8, P = 0.12 £q

2

= 13.5, P = 0.004

(C)

Total

Sexual system

Dioecy

Monoecy

Polygamy

Hermaphrodite

No. species

N

obs

N

obs

N

obs

N

obs

689

82 (11.9%)

72 (10.4%)

45 (6.5%)

490 (71.1%)

TSENG et al. ¡X Dioecy in Taiwan and Orchid Island

267

(Sakai et al., 1995a). In contrast, the flora of a continental

island is highly influenced by the plants that have migrated

from an adjacent landmass. The migration of plants will be

substantial if the island has been connected to a continent

through a ¡¥land bridge,¡¦ and no long-distance dispersal is

required for plant establishment on the island.

Sexual systems were analyzed among different climatic

zones in Taiwan, and the results showed a general trend

toward decreasing dioecy as altitude increased (Table 4).

The incidence of dioecy in the tropics, subtropics, and

temperate regions (8.2-8.8%) was similar, and it was

lowest in the cold temperate area (2.0%). A similar trend

can be observed for monoecious taxa. In comparison, the

incidence of polygamy was nearly constant among all

regions while hermaphroditism was highest in the cold-

temperate area, but remained the same in other regions

(Table 4). This data, however, should be viewed with

caution since the counting of species numbers is not

exclusive among different climatic zones. The climatic

zones are only roughly classified, and many plants are

found in more than one zone. Therefore, chi-square

statistics cannot be readily applied.

Sexual systems among different vegetation

types

The sexual systems of seven sites from Taiwan and

Orchid Island are compared with data from the literature

(Table 5). It is not easy to compare different vegetation

types since some studies only used tree data while others

used data for all plants. In general, dioecy percentages

are higher in the tropics than in the subtropics or other

regions, except for dry or semi-dry forests, a trend that

has been previously documented (Bawa and Opler, 1975;

Givnish, 1980). The Nanjenshan II plot of Taiwan had the

highest dioecy percentage (23.9%) of all the studies with

all floras analyzed. However, when only tree data were

used in the analysis, the percentage (27.2%) fell below

those from several other studies like the 40.0% from the

Okomu Forest Reserve, South Nigeria (Table 5). The flora

of Orchid Island is counted as one site and has 31.0%

dioecious plants among its trees, the highest among the

seven study sites of Taiwan/Orchid Island. Interestingly,

all seven sites we analyzed have a significantly higher

incidence of dioecy (11.9-23.9%) than the total flora

(7.9%). However, the dioecy among trees of the seven

sites is similar to the dioecy based on the total flora

(18.7-31.0% vs. 22.7% of the total trees, Table 5). The

two tropical communities in this study, Nanjenshan II and

Orchid Island, have similar proportions of sexual systems

to other tropics forests; on the other hand, the incidence

of dioecious species among the four subtropical and one

warm temperate forest is higher than that in the temperate

regions and some tropical forests.

We have to point out that estimates of sexual systems

in the flora of Taiwan have several problems, one of

which is the definition of native plants. Taiwan is one

of the world¡¦s most heavily populated countries, and

even though over 52% of Taiwan is covered with forests

(Hsieh et al., 1994), many are highly fragmented or have

suffered human disturbance in lowland areas. Many

plants adapted to this disturbed environment are then

found in the flora of Taiwan, including many herbaceous

plants. The herbaceous taxa comprise a large portion in

Taiwan¡¦s flora (62.5%), but contain only 24 dioecious

taxa. The herbaceous species are mostly found in the five

largest families¡XGramineae, Orchidaceae, Compositae,

Cyperaceae, and Leguminosae¡Xwhich comprise nearly

33.4% of Taiwan¡¦s seed plant species (Hsieh, 2003). All

five families are predominant at lower altitudes and are

dioecy-poor. Except for orchids, the other four families

are well known for their spreading ability and adaptation

to disturbed areas. The Linkou Laterite Lerrace and

Kwangin Coastal Nature Reserve are the most disturbed

plots sampled in our study. They contain 20-21% of taxa

from those four ¡¥weedy¡¦ families: 87/411 from Linkou and

62/305 taxa from Kwangin. This is probably why these

two regions have the lowest dioecy percentages (14.1%

and 14.8%, respectively).

Another problem that influences values for the

incidence and correlation of dioecy is the criterion for

assignment of sexual systems. In fact, the categorization

of sexual expression among species poses certain

Table 4. Frequencies of sexual systems of Taiwan in six climatic zones. The percentage corresponding to total species numbers in

each climatic zone are shown in parentheses.

Climatic zone

No. species

Sexual system

Dioecy

Monoecy

Polygamy

Hermaphrodite

Tropics

2029

167 (8.2%)

231 (11.4%)

137 (6.8%)

1494 (73.6%)

Subtropics

1233

102 (8.3%)

152 (12.3%)

77 (6.2%)

902 (73.2%)

Warm-temperate

799

70 (8.8%)

85 (10.6%)

59 (7.4%)

585 (73.2%)

Temperate

555

47 (8.5%)

59 (10.6%)

33 (5.9%)

416 (75.0%)

Cool-Temperate

324

21 (6.5%)

24 (7.4%)

23 (7.1%)

256 (79.0%)

Cold-Temperate

201

4 (2.0%)

10 (5.0%)

14 (7.0%)

173 (86.1%)

268

Botanical Studies, Vol. 49, 2008

Table 5. Proportions of plant sexual systems in seven study sites in Taiwan compared to other plant communities. Data including all

species (A) and trees only records (T) are separated in different column for comparison.

Forest types and locations No.

species

a

Sexual system (%)

Reference

Dioecy Monoecy Polygamy Hermaphrodite

A T A T A T A T

TROPICS

Deciduous forest

Secondary deciduous

forest, Venezuela

51/- 4.0 - 14.0 - - - 82.0 - (Jaimes and Ramirez, 1999)

Semi-deciduous forest

Tropical semi-deciduous

forest, Mexico

708/- 12.3 - 13.0 - 4.6

b

- 70.2

c

- (Bullock, 1985)

Dry Forest

Caatinga, Brazil

147/26 2.7 11.5 9.5 3.8 4.8

d

3.8

d

83.0

c

80.8 (Machado et al., 2006)

Evergreen Forest

Western Ghats, India -/656 - 20.0 - 5.0 - 16.0 - 57.0 (Krishnan and Ramesh, 2005)

Mountain forest

East Usambara mountain

forest, Tanzania

262/- 12.6 - 6.9 - 7.3 - 73.3 - (Rodgers and Homewood, 1982

in Krishnan and Ramesh, 2005)

Rain Forest

Okomu Forest Reserve,

South Nigeria

NA - 40.0 - 13.0 - - - 47.0 (Jones, 1955 in Bawa and

Opler, 1975)

Lowland rain forest, Costa

Rica

-/333 - 23.1 - 11.4 - - - 65.5 (Bawa et al., 1985)

Tropical palm swamp,

Venezuela

128/- 3.1 - 19.5 - - - 77.3 - (Ramirez and Brito, 1990)

Lowland mixed

dipterocarp forest,

Malaysia

270/- 14.1 - 8.9 - 0.7

e

- 76.3 - (Momose et al., 1998)

Lowland mixed

dipterocarp forest,

Malaysia

-/711 - 26.0 - 14.0

f

- - - 60.0 (Ashton, 1969)

Nanjenshan II, Taiwan 222/103 23.9 27.2 10.8 15.5 5.4 5.8 59.9 51.5 This study

Orchid Island, Taiwan 689/158 11.9 31.0 10.4 11.4 6.5 7.0 71.1 50.6 This study

Cloud forest

Montane cloud forest,

Venezuela

-/36 - 30.6 - - - - - 69.5

g

(Sobrevila and Arroyo, 1982)

Marine influenced vegetation

Restinga de Jurubatiba

National Park, Brazil

566/- 14.0

h

- 11.0

i

- - - 75.0 - (Matallana et al., 2005)

SUBTROPICS

Nanjenshan I, Taiwan

171/92 18.1 22.8 12.9 18.5 5.3 4.3 63.7 54.3 This study

Fushan, Taiwan

235/83 15.7 24.1 11.9 16.9 4.3 3.6 68.1 55.4 This study

TSENG et al. ¡X Dioecy in Taiwan and Orchid Island

269

difficulties especially when a species has been observed

with more than one sexual type, such as species with

¡¥monoecious or dioecious¡¦ or ¡¥dioecious or monoecious

or polygamous.¡¦ In our study, we included polygamous

species that contain sexual dimorphic (polygamodioecious,

gynodioecious, or androdioecious), monomorphic

systems (polygamomonoecious, gynomonoecious,

or andromonoecious) (definitions given by Sakai et

al., 1995b) and species having two or more sexual

expressions (except for species described as ¡¥monoecious

or dioecious¡¦). In some other studies, sexual systems were

simply classified as dioecy, monoecy, or hermaphrodite

(Bawa et al., 1985; Ramirez and Brito, 1990; Abe, 2006).

These diverse sexual systems are indeed very important for

elucidating the actual evolutionary pathway to dioecy in

specific taxa (McComb, 1966). For example, dioecy might

have orginated via the developmental transitions from

monoecy (e.g., Renner and Ricklefs, 1995; Dorken et al.,

2002; Harrison and Yamamura, 2003; Dorken and Barrett,

2004), gynodioecy (e.g., Charlesworth and Charlesworth,

1978; Ashman, 1999; Charlesworth, 1999; Weiblen et

al., 2000), androdioecy (e.g., Bawa, 1980; Charlesworth,

1999; Pannell, 2002), heterostyly (e.g., Ornduff, 1966;

Muenchow and Grebus, 1989), and dichogamy (e.g.,

Dommee et al., 1990; Pendleton et al., 2000; Pannell and

Verdu, 2006). Thus, incomplete analysis not only results in

sampling errors, it neglects the useful information behind

these sexual systems.

Another potential problem in studying the general

patterns of sexual systems is plasticity. Plasticity in gender

and sexual systems among individuals has long known in

plants (Lloyd, 1980; Lloyd and Bawa, 1984). Sex changes

can even occur in the same individual over different years

(Freeman et al., 1980a; Lloyd and Bawa, 1984; Nanami et

al., 2004). Plants can be monoecious or hermaphroditic,

but the male and female phases of the flowers can mature

dichogamously (Lloyd and Webb, 1986). Furthermore,

fitness measured by the gender functions is complicated

since they are quite variable in different plants, and thus

obscure the inference of dioecism (Delph and Wolf, 2005).

Despite of these difficulties, we hope to provide a synopsis

for the sexual systems in the flora of Taiwan for future

studies.

Forest types and locations No.

species

a

Sexual system (%)

Reference

Dioecy Monoecy Polygamy Hermaphrodite

A T A T A T A T

Kwangin coastal nature

reserve, Taiwan

305/86 14.8 30.2 11.5 18.6 8.9 7.0 64.9 44.2 This study

Linkou laterite terrace

secondary forest, Taiwan

411/101 14.1 24.8 10.9 15.8 7.8 11.9 67.2 47.5 This study

WARM TEMPERATE

Lopeishan, Taiwan

207/91 16.9 18.7 11.6 14.3 4.3 3.3 67.1 63.7 This study

TEMPERATE

Gallipolis, Ohio

-/17 - 11.0 - 83.0 - - - 6.0 (Braun, 1950 in Bawa and

Opler, 1975)

Campbellsville, Kentucky -/20 - 15.0 - 70.0 - - - 15.0 (Braun, 1950 in Bawa and

Opler, 1975)

Hueston¡¦s Woods, Ohio -/15 - 13.0 - 60.0 - - - 27.0 (Braun, 1950 in Bawa and

Opler, 1975)

Pisgah Mountain, New

Hampshire

-/13 - 6.0 - 81.0 - - - 13.0 (Braun, 1950 in Bawa and

Opler, 1975)

a

The first value is the species number of all life forms and the second value is the number of trees. NA: data non available.

b

Including 1.6% gynomonoecious, 2.0% andromonoecious, 0.3% polygamomonoecious, 0.6% gynodioecious, 0.1% androdioecious

species.

c

Including heterostylous species.

d

Andromonoecious species only.

e

Androdioecious and andromonoecious species only.

f

Including some protandrous and some protogynous, hermaphroditic species.

g

Including heterostylous and monoecious species based on the original paper.

h

Including gynodioecious and androdioecious species.

i

Including gynomonoecious and andromonoecious species.

Table 5. (Continued)

270

Botanical Studies, Vol. 49, 2008

In this study, we present the most species-rich (3052

species) survey of an island flora for its sexual systems.

This is also the first comprehensive report on the sexual

systems of continental islands. The high incidence of

dioecy in Taiwan (7.9%) is possibly due to a combination

of tropical and/or oceanic components, woodiness, and

long distance dispersal, all of which have been suggested

to be associated with dioecism (Bawa, 1980, 1984).

However, current understanding of sexual systems in

Taiwan¡¦s flora is heavily influenced by the limited data,

such as insufficient data on pollination and dispersal

modes. Therefore, further detailed investigation on

reproduction biology is required to elucidate the ecological

correlation with the richness of dioecy in Taiwan. Data

from adjacent continental regions like Southeastern China

and Indo-China are also required for comparison.

Acknowledgments. The authors thank Ya-Wen Gan and

Juinn-Yi Huang for helping on the data collection, and

Bing-Ling Shih for providing unpublished information on

Urticaceae in Taiwan.

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TSENG et al. ¡X Dioecy in Taiwan and Orchid Island

273

Supplementary data 1. References of recent taxonomic revisions referred in this paper for census, in addition to the Flora

of Taiwan, 2nd edition.

Acanthaceae (Hsieh et al., 1999), Apiaceae (Chen and Wang, 2001; Shan et al., 1985), Araceae (Li, 1979), Araliaceae (Hoo and

Tseng, 1978), Arecaceae (Pei et al., 1991), Asteraceae (Boufford and Peng, 1993; Chen, 1999; Chung and Peng, 2002; Chung et

al., 2008; Ling et al., 1979), Begoniaceae (Peng and Sue, 2000; Peng et al., 2005), Brassicaceae (Al-Shehbaz and Peng, 2000),

Boraginaceae (Wang and Shen, 2001; Wang et al., 1989), Burmanniaceae (Yang et al., 2002), Celastraceae (Liu and Yang, 2000),

Commelinaceae (Chen, 1998), Convolvulaceae (Liao et al., 2000), Cornaceae (Yang and Liu, 2002), Elaeagnaceae (Huang,

2002), Elatinaceae (Huang, 1994), Euphorbiaceae (Chen, 2000; Chen and Wu, 1997; Hs u, 2003; Kiu et al., 1996; Li, 1994),

Gentianaceae (Chen and Wang, 2000; Chen et al., 2006; Chen et al., 2008; Hsieh et al., 2007), Gesneriaceae (Wang and Wang,

2000; Wang et al., 1990), Hydrocharitaceae (Sun and Wang, 1992), Icacinaceae (Chuang, 1981), Labiatae (Huang et al., 2003),

Liliaceae (Chen et al., 1980; Peng et al., 2007), Loranthaceae (Tam, 1988), Lythraceae (Huang et al., 1989), Malpighiaceae (Chen

and Chen, 1997), Malvaceae (Cheng and Tsai, 1999), Menyanthaceae (Li et al., 2002), Melastomataceae (Yang and Liu, 2002),

Meliaceae (Chen, 1997a), Moraceae (Tzeng, 2004), Mysinacea (Chen, 1979), Nyctaginaceae (Zhou, 1996), Haloragaceae (Li

and Hsieh, 1996), Oleaceae (Chang et al., 1992), Orchidaceae (Chung, 2002; Ormerod, 2002, 2003, 2004; Su, 2002), Poaceae

(Kuoh, 2003), Polygalaceae (Hsieh et al., 1995), Polygonaceae (Kuo, 1997), Rhamnaceae (Chen and Chou, 1982; Liu et al., 1990),

Rhizophoraceae (Lu et al., 1999), Rosaceae (Hsieh and Chaw, 1996; Hsieh and Huang, 1997; Lu et al., 2005; Yang and Liu, 2002),

Rubiaceae (Lo et al., 1999a; Lo et al., 1999b), Rutaceae (Ho, 1995; Huang, 1997), Scrophulariaceae (Chen and Chou, 2008; Hsieh,

2000; Hsieh and Yang, 2002), Simaroubaceae (Chen, 1997b), Staphyleaceae (Hsu, 1981), Sterculiaceae (Hsu, 1984), Theaceae

(Wu et al., 2003), Theligonaceae (Huang et al., 1989), Ulmaceae (Chen and Tang, 1998), Urticaceae (Hsu et al., 2003; Shih, 1995;

Shih and Yang, 1998; Shih et al., 1995a; Shih et al., 1995b), Vitaceae (Hsu, 1999; Hsu and Kuoh, 1999; Hsu and Wu, 2000), and

Zygophyllaceae (Huang and Hsieh, 1994).

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276

Botanical Studies, Vol. 49, 2008

Supplementary data 2. List of species with uncertain sexual system in Taiwan and Orchid Island according to the Flora of Taiwan

(Huang and Editorial Committee of the Flora of Taiwan, 1993, 1996, 1998, 2000, 2003).

Family

Species

Note

Anacardiaceae Rhus ambigua

Des cription of the genus is polygamous but 3 out of 5 s pecies in this genus are

dioecious. Sexual system undescribed for the species.

Rhus hypoleuca

Description of the genus is polygamous but 3 out of 5 s pecies in the genus are

dioecious. Sexual system undescribed for the species.

Apiaceae

Peucedanum japonicum Description of the genus is polygamous. Sexual system undescribed for the species.

Peucedanum formosanum Description of the genus is polygamous. Sexual system undescribed for the species.

Torilis japonica

Flowers¡¦ illustration s how stam inate flower and perfect flower. Sexual system

undescribed for the species.

Torilis scabra

Sexual system undescribed for the species.

Aponogetonaceae Aponogeton taiwanensis Flowers usually bisexual or rarely unisexual by abortion in the family. Sexual sys-

tem undescribed for the species.

Araliaceae Dendropanax dentiger Description of the genus is bisexual or polygamous. Sexual system undescribed for

the species.

Dendropanax trifidus Description of the genus is bisexual or polygamous. Sexual system undescribed for

the species.

Eleutherococcus trifoliatus Description of the genus is perfect or polygamous. Sexual system undescribed for

the species.

Pentapanax

castanopsisicola

Description of the genus is bisexual or polygamous. Sexual system undescribed for

the species.

Asteraceae Anaphalis nepalensis Description of the genus is dioecious or polygamo-dioecious. Sexual system

undescribed for the species.

Anaphalis royleana

Description of the genus is dioecious or polygamo-dioecious. Sexual system

undescribed for the species.

Pterocypsela x mansuensis Sexual system undescribed for the species.

Clusiaceae Calophyllum blancoi Description of the species is flower (bisexual.).

Cyperaceae Hypolytrum nemorum Description of the genus is bearing a monandrous staminate flower. Sexual system

undescribed for the species.

Rhynchospora rugosa

subsp. brownii

Other species in this genus are monoecious or polygamous or hermaphroditic.

Sexual system undescribed for the species.

Rhynchospora malasica Other species in this genus are monoecious or polygamous or hermaphroditic.

Sexual system undescribed for the species.

Icacinaceae Gomphandra luzoniensis Description of the genus is dioecious. Sexual system undescribed for the species.

Loranthaceae Korthalsella japonica Description of the genus is unisexual. Sexual system undescribed for the species.

Malpighiaceae Ryssopterys timoriensis Description of the genus is androdioecious in flora of Taiwan and usually unisexual

in flora of China. Sexual system undescribed for the species.

Nyctaginaceae Pisonia umbellifera

Description of species is unisexual in the Flora of Taiwan, polygamous in the Flora

of China.

Oleaceae

Chionanthus coriaceus Description of the genus is polygamous or dioecious. Sexual system undescribed for

the species.

Rutaceae

Phellodendron amurense

var. wilsonii

Description of the genus is dioecious in flora of Taiwan, dioecious or polygamous in

(Ho, 1995). Sexual system undescribed for the species.

Simaroubaceae Brucea javanica

The description of the genus is dioecious, but flower¡¦s illustration shows

hermaphroditic.