Reproductive Ecology of Cleome Gynandra and Cleome Viscosa (Capparaceae)
Reproductive Ecology of Cleome Gynandra and Cleome Viscosa (Capparaceae)
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Abstract. Cleome is an important genus for the study of self- and cross-pollination through polymorphism,
and adaptations for pollination by both invertebrate and vertebrate pollinators. Cleome gynandra is
polygamodioecious, representing functionally staminate short gynoecium floral type and functionally
hermaphrodite medium and long gynoecium floral types. Cleome viscosa is functionally hermaphroditic with
short, medium and long gynoecium floral types. Both species are self-compatible and autogamous. Cleome
gynandra is ambophilous, while C. viscosa is entomophilous. In both species, mature and dry pods dehisce
septicidally and disperse seeds by wind. The seeds of C. gynandra germinate immediately and produce new
plants, if soil has moisture, while those of C. viscosa remain dormant and germinate only during rainy season.
Cleome viscosa is a C3 plant growing in cool environments, while C. gynandra is a C4 plant growing in warm
environments. Cleome gynandra is a climate resilient species and suitable for the restoration of ecologically
degraded habitats and also habitats with warm conditions.
Seeds are used as a condiment due to their pleasant In C. gynandra, ten mature buds were bagged and
flavor by the people of the Garhwal Himalaya. Poor removed three hours after anthesis. Then, micro
people who cannot afford cumin mostly use Cleome. pipette was inserted into the flower base to extract
Because of its piquant flavor, along with other spices it nectar for measurement. The average of nectar of ten
is now used extensively as a condiment in the prepa flowers was taken as the total volume of nectar/flower
ration of pickling spices, sausages, green and other and the same sample was used to measure nectar sugar
vegetables, curries and pulses. A kilogram of Cleome concentration (Dafni & al. 2005). The sugar content/
seed is exchanged for 7 kg of unhusked rice or 4 kg flower is expressed as the product of nectar volume
of wheat. Exchange is not merely for economic gain and sugar concentration per unit volume, mg/µl (Daf-
but involves reciprocity relationships among families ni & al. 2005). The caloric reward of nectar/flower/day
(Maikhuri & al. 2000). The medicinal uses of C. gy- was measured as per the formula given in Heinrich
nandra are not known. The intent of the present study (1975). Paper chromatography method described in
is to understand the functionality of sexual system Dafni & al. (2005) was followed to identify the amino
in the floral types of Cleome gynandra and C. viscosa acid types in the nectar. Ten flowers, each from five in-
with reference to natural fruit set rates and to charac dividuals of each plant species, were used to test stig-
terize pollination syndromes functional through pol- ma receptivity. It was tested with hydrogen peroxide
linating agents. Further, a careful effort is made to from mature bud stage to flower closure/drop as per
highlight their medicinal/economic values and im- Dafni & al. (2005). Further, the receptivity was also
portance in eco-restoration based on the existing rele observed visually, whether the stigma is shiny, wet or
vant literature. changing colors, or withering.
Insect foraging activity and pollination: The in-
sects were observed visually and by using binoculars;
Material and methods the insect species that could not be identified on spot
were captured and later identified with the help of
Floral biology: Cleome gynandra and Cleome vis- the identified specimens available at the Department
cosa (Capparaceae) growing seasonally in Visakhapa- of Environmental Sciences, Andhra University. The
tnam (17°42'N and 82°18'E), Andhra Pradesh, India, hourly foraging visits of each insect species on each
were selected for study during 2012–2014. Twenty- plant species were recorded on four occasions and the
five fresh flowers were used for each species to re- data was tabulated for further analysis. For each spe-
cord the floral details. Anthesis schedule and anther cies, approximately a patch of five hundred flowers
dehiscence timing were recorded by observing twen- were selected to record the foraging visits of insects.
ty -five marked mature buds in the field. For both spe- The data obtained was used to calculate the percent-
cies, 20 undehisced anthers from each flower morph age of foraging visits of each category of insects per
on ten plants were used to determine pollen output day in order to understand the relative importance of
and study pollen grain characteristics as per the pro- each category of insects. The insects were observed on
tocols given in Dafni & al. (2005). The protocols stated a number of occasions on each plant species for their
in Mondal & al. (2009) were followed to identify ami- foraging behavior such as mode of approach, landing,
no acid types present in the pollen. The protocols de- probing behavior, the type of forage collected, contact
scribed in Sadasivam & Manickam (1997) and Lowry with essential organs and inter-plant foraging activi-
& al. (1951) were followed to estimate protein content ty. The hourly forage collection activity of each spe-
in the pollen. The pollen-ovule ratio was determined cies was also recorded to understand whether any re-
as per the protocol given in Cruden (1977). In C. gy- lationship exists between standing crop of nectar or
nandra, the pollen-ovule ratio was calculated sepa- pollen and flower visiting activity.
rately for each flower morph, taking into account the Fruiting behavior: Two hundred flowers on twen-
constant number of stamens and average number of ty individual plants of each plant species were tagged
ovules per flower. In C. viscosa, the pollen-ovule ratio prior to anthesis and followed for fruit and seed set for
was calculated separately for each flower morph, tak- two weeks. The resulting fruit and seed output were
ing into account the average number of stamens and pooled up for calculating fruit and seed set rates for
the average number of ovules per flower. each species. Fruit maturation period, the fruit and
Phytol. Balcan. 22(1) • Sofia • 2016 17
seed characteristics were recorded. Fruit and seed dis- phase of flowering. But, flower morph-wise, the SGF
persal modes were carefully observed. The aspects of constituted 48–60 %, MGF 17–22 % and LGF 23–30 %
seed germination and establishment of populations of the total flower production (Table 2).
were observed briefly.
Table 1. Morphometrics of floral sex organs in the floral types
and morphs of Cleome gynandra.
Results Floral structure Staminate
floral type
Hermaphrodite floral type –
flower morphs
Medium Gynoecium
morph (mean±s.d.)
morph (mean±s.d.)
Plant phenology and flower morphology: It is an
erect branching annual weedy herb, which grows up
(mean±s.d.)
to 60 cm, in full sunlight in moist and well drained
soils. The plant grows throughout the year, if the soil
is moderately wet. The flowering and fruiting events
Gynophore (mm) 1±0.4 11±1 8±0.4 13±0.4 5±0.8
occur throughout the year at population level. How- Gynoecium (mm) 2±0.4 18±0.6 21±0.6 15±0.4 13±0.4
ever, the vegetative growth, flowering and fruiting Stamen (mm) 22±0.4 25±0.4 24±0.4 7±0.4 2±0.5
events occur simultaneously and they are very prom- Table 4. Ovule number in the floral types/morphs of Cleome
inent during August-September. During rainy sea- gynandra.
son, the plant produces pure stands in well-drained Floral type/ Sample size Range Mean±S.D.
sunlight-exposed soils. The other concurrently grow- morph
SGF 20 − −
ing plants along with this weed include: Cleome visco- MGF 20 68−175 116±34
sa (Capparaceae), Boerhaavia diffusa (Nyctaginaceae), LGF 20 66−198 120±55
MGSSF 20 21−192 130±50
Euphorbia hirta, Phyllanthus niruri, Acalypha indica, MGSeSF 20 54−168 119±25
(Euphorbiaceae), Cardiospermum halicacabum (Sap-
indaceae), and Sida cordata (Malvaceae). It flowers Table 2. Percentage of common floral types/morphs in Cleome
gynandra.
during August–December. The inflorescence is a ter- Floral type/ Initial flowering Peak flowering Final flowering
minal raceme with many flowers. The flowers are of morph (July 1st week) (August – (October 2nd
two types: staminate consisting of residual ovary de- September) week)
SGF 60 55 48
void of ovules, and bisexual consisting of function- MGF 17 20 22
al ovary and fertile stamens. The bisexual floral type LGF 23 25 30
is classified into four different flower morphs based Sample size: 210 flowers from 30 plants at each flowering phase.
especially on the length of gynoecium: Medium Gy-
noecium Flowers (MGF), Long Gynoecium Flowers In plants producing SGF, MGF and LGF, the inflo-
(LGF), Medium Gynoecium Short Stamen Flowers rescence produces 34 to 40 flowers over a period of
(MGSSF) and Medium Gynoecium Sessile Shortest two weeks; in those producing only MGSSF, the in-
Stamen Flowers (MGSeSF). The flower morphs, SGF, florescence produces 21–24 flowers over a period of
MGF and LGF are produced in the same individu- about ten days; and in those producing only MGSeSF,
al, while the other two flower morphs are produced the inflorescence produces 18 to 22 flowers over a pe-
singly on different individual plants. At population riod of about ten days. The SGF, MGF and LGF are
level, the percentage of plants producing SGF, MGF 33 ± 0.56 mm long, while MGSSF and MGSeSF are
and LGF is 60 %, of MGSSF 18 % and of MGSeSF 21 ± 0.23 mm long. The flower morphs are pedicellate
22 %. Morphologically, all flower morphs look alike and open-type, with exposed ovary and stamens. They
but closer examination only indicates certain differ- bear androphore and the gynophore. The androphore
ences in these flower morphs (Tables 1 and 4). The is the part of thalamus between the sepals, petals and
plants producing SGF, MGF and LGF are common, stamens, while the gynophore is an elongated part be-
while those producing MGSSF and MGSeSF are un- tween the stamens and gynoecium. The two parts are
common. The percentage of SGF gradually decreased collectively referred to as androgynophore. All flower
from initial to final phase of flowering while that of morphs are white and actinomorphic. The sepals are
MGF and LGF gradually increased from initial to final four, green, lanceolate, connate at the base, 3 mm long
18 Raju, A.J.S. & Rani, D.S. • Reproductive ecology of Cleome gynandra and C. viscosa
and 2 mm wide. The petals are four, white, free, ellip- as well as the number of pollen grains produced per
tical to obovate, rounded at the apex, 11 mm long and flower. SGF morphs totally lack ovules. In the oth-
5 mm wide. The stamens are six, with long purple fil- er four flower morphs, pollen-ovule ratio increased
aments and green exserted dithecous anthers; they are from initial to peak and then decreased at final phase
22 ± 0.4 mm long in SGF, 25 ± 0.4 mm long in MGF, of flowering (Table 5).
24 ± 0.4 mm long in LGF, 7 ± 0.4 mm long in MGSSF,
Table 3. Pollen output per flower in the floral types/morphs of
and 2 ± 0.5 mm long in MGSeSF (Table 1). The ovary Cleome gynandra.
is bicarpellary syncarpous, unilocular with numerous Floral type/ Initial flowering Peak flowering Final flowering
ovules on parietal placentation; the bicarpellary state morph (mean±s.d.) (mean±s.d.) (mean±s.d.)
of ovary is due to the development of a false septum SGF 60949±1572 63653±3317 61517±3820
during fruit development. The style is short and ex- MGF 63422±3292 61711±4734 59958±4047
tends into a purple capitate stigma, which is depressed LGF 63230±3636 66222±2998 65602±3968
at apex. MGSSF 23105±2057 24578±13910 22790±2303
MGSeSF 38308±4656 43220±1521 37825±4186
Floral biology: The floral characters are similar for
Sample size: Ten anthers from five plants at each flowering
all five flower morphs, unless otherwise specified. The phase.
immature buds take two weeks to mature into flow-
ers. First sepals develop and elongate fully, followed Table 5. Pollen-ovule ratio in the floral types/morphs of
Cleome gynandra.
by petals, stamens, pistil and gynophores. The flowers
open at dusk during 15:00–16:00 h, initially signaled Floral type/ Initial flowering Peak flowering Final flowering
morph (mean±s.d.) (mean±s.d.) (mean±s.d.)
by a slight relaxation of petals to create an opening at SGF − − −
the bud apex through which first the stigma, and sub- MGF 546:1 531:1 516:1
sequently the entire pistil is exserted, with the convo- LGF 526:1 551:1 546:1
luted gynophore and stamens still enclosed within the MGSSF 177:1 189:1 175:1
petals. The petals unfold and then the stamens and MGSeSF 321:1 363:1 317:1
gynophore become fully turgid and erect. The stig-
ma is receptive to pollen from the time of initial ex- In all five flower morphs, the pollen contains six
sertion, while the anthers dehisce when the filaments essential amino acids and nine non-essential amino
expand fully which takes place an hour after anthe- acids. The essential amino acids are threonine, me-
sis suggesting that the flowers are protogynous. The thionine, lysine, histidine, arginine and tryptophan.
stigma receptivity extends up to 17:00 h of the follow- The non-essential amino acids include alanine, ami-
ing day. The pollen output per flower varied with each no-butyric acid, aspartic acid, cysteine, cystine, gly-
flower morph and phase of flowering. The SGF, MGF cine, hydroxyproline, proline and serine. The to-
and LGF produce more pollen than the other flower tal protein content per 1 mg of pollen is 231.25 µg
morphs; the total output is almost the same for SGF in all five flower morphs. All five flower morphs are
during initial and final phase, while it is significantly nectariferous and the nectar is secreted by the nec-
greater during the peak phase of flowering. In case of tar glands situated at the base of each sepal; it can be
MGF, the pollen output gradually decreased from ini- seen as four minute droplets, one each at the base of
tial to final phase of flowering. In case of LGF, the pol- the sepal which glistens against sunlight. The flow-
len output was slightly less in the initial phase, when ers present nectar by the time the flower opens; it
compared to that produced during the peak and final is 0.26 ± 0.1 µl with 60 ± 0.5 % sugar concentration.
phase of flowering. In the other two flower morphs, The sugar content is 15.52 mg, which is equivalent to
the pollen output was almost the same during initial 2.59 Joules of energy. The nectar contains five essen-
and final phase but it was significantly more during tial and nine non-essential amino acids. The essen-
peak phase of flowering (Table 3). tial amino acids are threonine, lysine, histidine, argi-
In all five flower morphs, the pollen grains nine and tryptophan, while the non-essential amino
are monads, spherical, golden-yellow, powdery, acids are alanine, amino-butyric acid, aspartic ac-
19.92 ± 4.28 µm, prolate, tricolpate, reticulate, and id, cysteine, cysteine, glutamic acid, glycine, proline,
with incomplete reticulum. The pollen-ovule ratio and serine. In two-day flowers, the stamens coil and
varied depending on the number of ovules produced, contact the stigma facilitating autogamy. Further-
Phytol. Balcan. 22(1) • Sofia • 2016 19
more, the powdery pollen is driven away by wind on ed pollen and then gathered nectar in the same vis-
sunny days, it is visible to the naked eye; this is con- it; the pollen-collecting behavior effected pollination,
sidered to be affecting both self- and cross-pollina- while nectar-collecting behavior simply labeled them
tion. The petals and stamens fall off on the third day, as nectar robbers. The fly directly descended to the
while sepals fall off after ten days. petal area, landed on petals and then collected nec-
Flower visitors and pollination: All five flow- tar droplets from the base of sepals. Its flower probing
er morphs were indiscriminately visited by insects behaviour never facilitated the contact between the
as soon as they are open during dusk hours. They stamens and stigma to effect pollination and, hence,
were foraged during 15:00–18:00 h and again dur- it acted as nectar robber. Similarly, the butterfly al-
ing 07:00–09:00 h on the second day of anthesis. so came for collecting nectar, in so doing, its upper
The insects recorded were bees (Apis cerana, Trigo- parts of wings always had contact with the stamens
na iridipennis, Anthophora cingulata and Anthopho- and stigma contributing to pollination. The duration
ra), an ant (Crematogaster sp.), one unidentified fly, of stigma receptivity period was found to be in tune
and a butterfly (Pachliopta aristolochiae) (Table 7; with the foraging activity schedules of pollinator bees
Fig. 1). Of these, bees as regular and consistent vis- and the butterfly. The pollen being dry and powdery,
itors and the fly as an irregular visitor foraged dur- it easily deposited on the dorsal surface of the pol-
ing dusk hours on the day of anthesis and also on the len-probing bees and on the upper parts of wings of
following day during morning hours; the former for the nectar-feeding butterfly species. Bees moved very
pollen and/or nectar, while latter for nectar only. The swiftly from flower to flower on the same or closely
ant was a resident forager and gathered nectar con- or distantly spaced individual plants in quest of more
tinually moving between flowers mostly on the same pollen; the absence of landing place for pollen collec-
or nearby plants during daylight hours. The butter- tion appeared to be driving these bees to make vis-
fly was a regular nectar forager, but it collected nec- its to a number of flowers in quick succession across
tar only during the dusk hours on the day of anthe- population(s) to promote cross-pollination. The but-
sis. The data collected on the foraging visits of insects terfly also visited the flowers of different conspecific
showed that 69 % of the total visits were made dur- plants for want of nectar as there was competition for
ing dusk hours and the remaining percentage during the same resource from bees and the fly.
the morning hours of the following day. Bees consti-
tuted 90 %, the fly 7 % and butterflies 3 % of total vis-
its made. The insects approached the flowers in up-
right position for probing the forage. The bees either
held the staminal filaments or hovered at the anthers
to collect pollen; while doing so, they did not distin-
guish the stamens from the stigma and tried to col-
lect pollen from the stigma also. Such a behavior con-
tributed to effecting pollination. They descended to
the flower base and probed the flowers for collecting
Fig. 1. Hourly foraging activity of insets on Cleome gynandra
nectar droplets during which they never had any con- (average foraging visits recorded on four different days during
tact with the flower sex organs. The bees first collect- wet season in 2012 and 2013).
Fruiting ecology and seed dispersal: The fruit the extent of rainfall. The plant forms pure stands in
growth and development begins immediately af- certain areas and grows as scattered individuals along
ter pollination and fertilization, during which the with other plants, such as Cleome gynandra, Boer-
ovary elongates. The fruits mature, shifting col- haavia diffusa (Nyctaginaceae), Euphorbia hirta, Phyl-
our from green to brown within a week. The short lanthus niruri, Acalypha indica (Euphorbiaceae), Car-
style and capitate stigma remain so until fruit dehis- diospermum halicacabum (Cardiospermaceae), Sida
cence. The natural fruit set is 98 % in both MGF and cordata (Malvaceae), and Pedalium murex (Pedaliace-
MGSeSF morphs, 99 % in LGF morphs and 96 % in ae). The inflorescence is a lax, corymbose, 30 cm long
MGSSF morphs (Table 6). The mature and dry fruits few-flowered raceme (13.72 ± 1.34). The flowers are
vary in length with each flower morph. The fruits also borne solitary in leaf axils.
produced by MGF are 6.20 ± 0.40 cm, those by LGF The flowers are bisexual and represent three flow-
6.80 ± 0.60 cm, those by MGSSF 3.14 ± 0.56 cm, and er morphs: Short Gynoecium Flowers (SGF), Medi-
those by MGSeSF 2.30 ± 0.35 cm. The mature and dry um Gynoecium Flowers (MGF) and Long Gynoecium
fruit is a long-stalked, linear, suberect, and cylindric Flowers (LGF); all three morphs occur on the same
capsule tapering at both ends. The dry fruits dehisce plant. The SGF consist of 4 mm long gynoecium, with
septicidally releasing seeds into the air. The seeds are 100 ovules and 7 mm long stamens, MGF has 8 mm
brown, subglobose or orbicular, 1.5 mm in diame- long gynoecium, with 113 ovules and 8 mm long sta-
ter, with many concentric ribs and irregular cross- mens, and LGF has 10 mm long gynoecium, with 162
ribs. The seed output per fruit varies with the flower ovules and 11 mm long stamens (Tables 8 and 11). The
morph; it is 82.8 ± 5.51 in MGF, 148 ± 49.85 in LGF, stamen number is 19.65 ± 3.39 in SGF, 17.35 ± 6.22 in
134.6 ± 8.40 in MGSSF, and 126.2 ± 19.12 in MGSeSF. MGF and 16.1 ± 4.99 in LGF. The production rate of
Seed set rate varies with each flower morph; it is 71 % these flower morphs is almost constant throughout
in MGF, 81 % in LGF, 97 % in MGSSF, and 95 % in the flowering phase; the percentage of SGF is 18–19 %,
MGSeSF (Table 6). The seeds are non-dormant and of MGF 60–62 % and of LGF 20–21 % (Table 9). All
germinate within a week, if the soil is wet. But, seed three flower morphs are pedicellate (20 mm long) and
germination rate is high during rainy season; then the inverted-bell shaped, exposing the ovary and stamens.
plant forms pure stands or grows intermingled with The pedicel is 20 mm long during flowering phase and
other herbaceous flora in open, full sunlight. Seeds are 35–40 mm long during fruiting phase.
minute, light in weight and disperse by wind during
Table 8. Morphometrics of gynoecium and stamens in the
dry season and by rain water during rainy season. The floral morphs of Cleome viscosa.
plant reproduces exclusively by seed. Floral Short Medium Long
structures Gynoecium Gynoecium Gynoecium
Table 6. Fruit set and seed set in the floral types/morphs of flower morph flower morph flower morph
Cleome gynandra. (mean±s.d.) (mean±s.d.) (mean±s.d.)
Floral type/ No of flowers Fruit set Seed set Gynoecium (mm) 4±1 8±1 10±1
morph sampled (%) (%) Stamen (mm) 7±1 8±1 11±1
SGF 100 0 0
MGF 100 98 71 Table 11. Ovule number in the floral morphs of Cleome
LGF 100 99 81 viscosa.
MGSSF 100 96 97 Floral morph Sample size Range Mean±S.D.
MGSeSF 100 98 95 SGF 20 62−128 100±72
MGF 20 96−143 113±18
LGF 20 89−215 162±44
Cleome viscosa L.
Plant phenology and flower morphology: It is Table 9. Percentage of floral morphs of Cleome viscosa at
different phases of flowering.
an erect branching annual weedy herb, which grows
Floral Initial flowering Peak flowering Final flowering
up to 1 m in full sunlight, in wet or semi-wet soils at morph (July 1st week) (August–September) (October 4th week)
roadsides, in waste places, ruderal locations, and open (mean±s.d.) (mean±s.d.) (mean±s.d.)
places. The plant appears during early monsoon sea- SGF 19 18 18
son. The lush vegetative growth occurs by July and MGF 60 62 61
flowering occurs during August-November based on LGF 21 20 21
Phytol. Balcan. 22(1) • Sofia • 2016 21
The flower morphs are yellow and actinomor- in MGF and 23.62 ± 5.71µm in LGF. The pollen-ovule
phic. The sepals are four, green but purple outside at ratio varies depending on the number of ovules pro-
the base, lanceolate, free but connate at the base, gla- duced and the number of pollen grains produced per
brous inside, glandular hairy outside, 5–6 mm long flower. The ratio is the highest in SGF and the lowest
and 1–2 mm wide. The petals are four, yellow, free, in LGF morphs; almost the same trend exists through-
oblong-spathulate, base cuneate with a 5 mm long out the flowering season (Table 12).
claw at base, rounded at the tip, glabrous, 7–12 mm
Table 12. Pollen-ovule ratio in three floral morphs of Cleome
long and 3–5 mm wide. The stamens vary in number viscosa.
as mentioned above for all three flower morphs. They Floral Initial flowering Peak flowering Final flowering
are free, glabrous, filaments almost filiform, anthers morph (mean±s.d.) (mean±s.d.) (mean±s.d.)
linear, green, exserted and dithecous. The ovary is ses- SGF 782:1 763:1 757:1
sile, oblong-cylindric, glandular-pubescent, bicarpel- MGF 602:1 602:1 610:1
lary syncarpous, unilocular with numerous ovules on LGF 391:1 392:1 384:1
parietal placentation; the bicarpellary state of ovary is
due to the development of a false septum during fruit In all three morphs, the pollen contains six essen-
development. The style is short (2–5 mm long), slen- tial amino acids and nine non-essential amino acids.
der and extends into a capitate stigma. The essential amino acids are threonine, methionine,
Floral biology: The floral characters are similar lysine, histidine, arginine, and tryptophan. The non-
for all three flower morphs unless otherwise specified. essential amino acids include alanine, amino-butyric
The mature buds begin to open at 02:30 h by show- acid, aspartic acid, cysteine, cystine, glycine, hydroxy-
ing slits between petals and after half an hour, the sta- proline, proline, and serine. The total protein con-
mens protrude through the slits. After a short while, tent per 1 mg of pollen is 90.45 µg in all three flow-
anthesis is complete and the petals reflex, exposing er morphs. All three flower morphs are nectariferous
the stamens and stigma. The anthesis occurs during and the nectar is secreted in traces or minutely by the
03:00–04:00 h and anther dehiscence occurs by lon- nectar glands situated at the flower base around the
gitudinal slits simultaneously. The stigma is receptive ovary. The flowers present nectar by the time the flow-
to pollen two hours after anthesis and ceases its recep- er opens and is covered by the hairs around the ova-
tivity by noontime of the same day. During receptive ry. The petals fold back by noon on the day of anthe-
period, it is shiny and glistens against sunlight. The sis, enclosing the stamens and stigma. The closure of
pollen output per flower in all three flower morphs petals facilitates the contact between the stamens and
slightly varied at initial, peak and final phase of flow- stigma and effects autogamy. The flowers remain in
ering. Among these morphs, the SGF morphs produce that state, wither away the next day and drop off on
the highest number of pollen grains followed by MGF the 3rd day.
and LGF morphs, and the same trend is evidenced Flower visitors and pollination: The floral buds
throughout the flowering season (Table 10). of all three morphs provide breeding site for two spe-
cies of thrips (unidentified). These thrips occurred
Table 10. Pollen output per flower in the floral morphs of
Cleome viscosa.
during bud and flower phase, and fed on nectar and
Floral Initial flowering Peak flowering Final flowering
pollen during and after anthesis. Insect foragers were
morph (mean±s.d.) (mean±s.d.) (mean±s.d.) found to visit all three flower morphs indiscrimi-
SGF 78140±893 76281±3270 75707±2285 nately during 07:00–12:00 h, with peak activity dur-
MGF 68022±1960 68019±1744 69098±3301 ing 08:00–09:00 h (Figs. 2, 3). The insects recorded
LGF 63386±848 63476±1760 62165±2763 were bees (Apis dorsata, A. cerana, A. florea, Trigona
iridipennis (Apidae), Halictus sp., Nomia sp. and one
The pollen grains are identical and possess similar unidentified bee (Halictidae), a fly (Helophilus sp.)
characters in all three flower morphs. They are mon- and butterflies (Pachliopta hector, Catopsilia pomo-
ads, triangular, yellow, slightly sticky, prolate, tricol- na, C. pyranthe, Eurema hecabe, Pieris canidia, Cepo-
pate, lobate, with veiculate ornamentation and tectum ra nerissa and Anaphaeis aurota, Acraea violae and
reticulated. The pollen grain size varied with each flow- Danaus chrysippus, Castalius romison and Chilades
er morph, it is 19.80 ± 4.20µm in SGF, 27.45 ± 5.23µm laius (Table 13).
22 Raju, A.J.S. & Rani, D.S. • Reproductive ecology of Cleome gynandra and C. viscosa
Fig. 2. Hourly foraging visits of been and flies on Cleome viscosa Fig. 3. Hourly foraging activity of butterflies on Cleome viscosa
(average foraging visits recorded on four different days during (average foraging visits recorded on four different days during
wet season in 2012 and 2013). wet season in 2012 and 2013).
Of these, bees and butterflies were the regular for- sex organs were considered to be resulting in pollina-
agers during the entire flowering season. The bees for- tion. While collecting nectar, the bees reached the nec-
aged for both pollen and nectar, the fly for only pol- tar location and in so doing, their ventral as well as
len and butterflies only for nectar. Bees made 38 %, the dorsal surface had contact with the stamens and stig-
fly 6 % and butterflies 56 % of total visits on any giv- ma and this nectar probing behavior also contribut-
en day. Among butterflies, pierids made 62 %, nympha- ed to pollination. While collecting pollen, the fly spe-
lids 20 %, lycaenids 10 % ,and papilionids 8 % of total cies contacted the stamens and stigma with its forehead
visits. These insects approached the flowers in upright only and such a contact was considered to be effect-
position, landed on the petals and probed the flowers ing pollination. While collecting nectar, the butterflies
for pollen and/or nectar. While collecting pollen from contacted the stamens and stigma with their proboscis
the anthers, the bees gained contact with their forehead and forehead effecting pollination. The bees spent rel-
and ventral side, due to which pollen was transferred atively more time per flower while collecting pollen, as
from the anthers to their body. They did not show any compared to nectar collection. While collecting nectar,
discriminatory behavior between the stamens and the both bees and butterflies moved quickly between flow-
stigma and, hence, attempts to collect pollen from both ers and plants within and between populations.
Phytol. Balcan. 22(1) • Sofia • 2016 23
Fruiting ecology and seed dispersal: The fruit attraction to flower visitors and maximize fruit/seed
growth and development begins immediately after set in these two species.
pollination and fertilization, during which the ova- In Capparaceae, andromonoecy (Capparis herba-
ry elongates. The fruits mature within a week shift- cea, Cleome lutea and C. serrulata), trimonoecy (Cle-
ing colour from green to brown. The natural fruit ome rosea) and polygamodiecy (Cleome spinosa) sex-
set is 98 % in SGF, 100 % in MGF and 99 % in LGF ual systems have been reported (Inocencio & al. 2006;
(Table 14). Carvalho 2002; Machado & al. 2006; Cane 2008). In
the present study, Cleome gynandra is polygamodi-
Table 14. Fruit set and seed set in the floral morphs of Cleome
viscosa.
oecious, consisting of andromonoecious individuals
Floral morph Flowers sampled Fruit set (%) Seed set (%)
producing both staminate and fertile hermaphrodite
SGF 100 98 90 floral types and fertile hermaphrodite individuals. In
MGF 100 100 99 andromonoecious individuals, short gynoecium flo-
LGF 100 99 94 ral type is functionally staminate, while hermaphro-
dite flowers represent medium and long gynoecium
The mature and dry fruits vary in length with floral types. The hermaphrodite individuals produce
each flower morph. The fruits produced from SGF either medium gynoecium short stamen floral type,
are 5.30 ± 0.51 cm, those from MGF 6.30 ± 0.32 cm or medium gynoecium sessile stamen floral type.
and those from LGF 7.40 ± 0.40 cm. The dry fruits This polygamodioecious sexual system support-
are long-stalked, linear, hairy, suberect, and cylindric ed by highest fruit and seed set rates in hermaph-
capsules tapering at both ends, the upper end forms rodite floral types indicates that C. gynandra is self-
3 mm long stipe. They dehisce septicidally from compatible and autogamous. Wind causes self- and
the tip to the base by the separation of false septum cross-pollination due to liberation of light and pow-
formed in ovary and release seeds into the air. The dery pollen grains on sunny days during rainy sea-
seeds are brown, subglobose or orbicular with nar- son. Further, intra-plant foraging activity of insects
row cleft, 1–1.5 mm diameter, with strong cross-ribs results in self-pollination, while inter-plant forag-
and weak concentric ribs. The seed output per fruit ing activity across the population(s) brings about
varies with the flower morph: it is 89.80 ± 28.48 in cross-pollination. The success of these pollination
SGF, 114.23 ± 19.80 in MGF and 152.61 ± 40.37 in modes is associated with the rate of pollen produc-
LGF. Seed set rate varies with each flower morph: it tion and, in line with this, pollen is produced in huge
is 90 % in SGF, 99 % in MGF, 94 % in LGF (Table 13). amount at flower and plant level. The pollen produc-
The seeds are dormant and germinate during rainy tion rate is very high and it is almost similar in all
season. Seeds are minute and light in weight and dis- three floral types of andromonoecious individuals,
perse by wind during dry season and by rain water while it is far less in the floral types of hermaphro-
during rainy season. The plant reproduces exclusive- dite individuals, thus needing the latter to receive
ly by seed. pollen from andromonoecious individuals, especial-
ly for cross-pollination. The simultaneous produc-
tion of functionally male and hermaphrodite flow-
Discussion ers in andromonoecious individuals increases the
pollen flow, leading to elevated pollen-ovule ratio,
The flowering phenology of Cleome viscosa and which further enhances the chance of a sufficient
C. gynandra suggests that it represents a modi- pollen charge on pollinators body and, consequent-
fied steady state flowering (Gentry 1974). Both spe- ly, on stigmatic surface (Heithaus & al. 1974). The
cies produce flowers in high numbers at plant level. staminate or male-biased sex ratio throughout the
They occur together and flower concurrently; they flowering season appears to be due to the need for
show patchy distribution as pure stands in open sites pollen overproduction to ensure successful pollina-
and also scattered occurrence in other areas, which tion (Inocencio & al. 2006). Therefore, the complex
are occupied predominantly by Sida and Triumfetta sexual system observed in C. gynandra seems to be
along with other herbaceous flora. The steady state favouring its reproductive success with a high fruit
flowering and patchy distribution of plants enhance and seed set.
24 Raju, A.J.S. & Rani, D.S. • Reproductive ecology of Cleome gynandra and C. viscosa
Cleome viscosa is a hermaphroditic species pro- In genus Capparis, apomixis is reported in C. fron-
ducing short gynoecium, medium gynoecium and dosa (Mauritzon 1935), self-compatibility in C. flex-
long gynoecium floral morphs, with fertile pollen uosa, C. verrucosa (Ruiz & Arroyo 1978), C. pittieri
and functional ovaries in 1:3:1 ratio on the same indi- (Bawa & al. 1985), C. atamisquea (Aizen & Feinsing-
vidual almost throughout the flowering season. This er 1994), and C. retusa (Bianchi & Gibbs 2000). The
sexual system, coupled with highest fruit and seed members of genus Cleome have been reported to be
set rates in all three floral morphs, indicates that the polymorphic, protandrous and cross-pollinated; but
plant is self-compatible and autogamous. The closure many species are self-compatible (Iltis 1967). Cleome
of petals facilitates the coiling stamens to contact the gynandra and C. viscosa in the present study can be
capitate stigma and effect autogamy. Furthermore, considered as facultative autogamous species, ripen-
intra-plant foraging activity of insects results in self- ing fruits and viable seeds even in the absence of pol-
pollination, while inter-plant foraging activity across linators. C. gynandra is protogynous, while C. visco-
the population(s) brings about cross-pollination. The sa is protandrous, but both are self-compatible. Their
success of these pollination modes is associated with floral characteristics, such as low investment in at-
the rate of pollen production and, in line with this, tractive structures as showy petals, nectar and pollen,
pollen is produced in huge amount at flower and plant brief anthesis schedule, self-compatibility, brief period
level. The pollen production rate in the medium gy- of stigma receptivity (extended to the 2nd day in C. gy-
noecium floral morphs is almost three times greater nandra due to evening anthesis), and delayed autono-
than that produced in the other two floral morphs; it mous selfing, confirm that they are facultative autoga-
is almost the same throughout the flowering season. mous with the option kept open for allogamy (Faegri
Such a high rate of pollen production at plant lev- & van der Pijl 1979; Cruden & Miller-Ward 1981). De-
el increases the pollen flow, leading to elevated pol- layed autonomous selfing is regarded to be adaptive,
len-ovule ratio and further enhances the chance of a because it apparently assures seed production, when
sufficient pollen charge on pollinators body and, con- pollinators are scarce or absent, yet allows outcross-
sequently, on stigmatic surface (Heithaus & al. 1974). ing to predominate, when they are abundant (Wyatt
Pollen overproduction appears to be the need for 1983). Such a breeding system is a “fail-safe system”
maximizing cross-pollination (Inocencio & al. 2006). to assure the plant to achieve pollination and set fruit
Therefore, the hermaphroditic sexual system with tri- and seed in the absence of insects.
morphic floral forms observed in C. viscosa seems to Cleome gynandra and C. viscosa flowers are ac-
be favouring its reproductive success with a high fruit tinomorphic; the petals are conspicuously white in
and seed set. the former and yellow in the latter species. Despite
Some studies have shown that plants will alter the existence of four nectaries at the base of ovary in
their sexual expression when resources, such as nu- both species, nectar is secreted in minute volume in
trient or light (Solomon 1985), become limited and C. gynandra and in traces in C. viscosa. The presence
when conditions become more severe (Wells & Lloyd of this level of nectar appears to be a strategy to con-
1991), or when biotic changes to the plant take place serve the nutrient energy and attract insect visitors
(foliar herbivory or pathogenic infestion) (Lokesha for pollination. Furthermore, the pollen production
& Vasudeva 1993). In both C. gynandra and C. visco- rate is significantly high in C. gynandra, as compared
sa, floral sex is not labile and the ratios of floral types to the pollen production rate in C. viscosa. Actino-
remain almost unchanged throughout the flower- morphy with free petals allows easy access for the in-
ing season, since there is only slight change in pol- sects to pollen and nectar resources in both species.
len and ovule production rate during different phas- However, C. gynandra with a good volume of nec-
es of flowering. The consistency in the expression of tar and high amount of pollen is able to attract on-
functional floral sex could be related to the availabil- ly bees as consistent foragers, while C. viscosa with
ity of adequate nutrients, light and also their ability traces of nectar and comparably less amount of pol-
to outcompete with the co-occurring and co-flower- len is able to attract both bees and butterflies as con-
ing herbaceous flora. Therefore, the two Cleome spe- sistent foragers, suggesting that the white floral col-
cies are not exposed to environmental stress in the our of C. gynandra and the yellow floral colour of C.
study areas. viscosa are equally attractive to bees, while only the
Phytol. Balcan. 22(1) • Sofia • 2016 25
yellow floral colour of C. viscosa appears to be attrac- source of five essential amino acids and nine non-es-
tive to butterflies. sential amino acids. As the bees also collect nectar
Machado & al. (2006) reported that Cleome spi- along with butterflies and other insects, the presence
nosa is visited by bats, sphingids, bees, and hum- of minute volume of nectar in C. gynandra and traces
mingbirds, but only bats are the effective pollina- of nectar in C. viscosa compel them to visit the flow-
tors, while all others are nectar thieves. Cane (2008) ers of several plants promoting cross-pollination. In
reported that in Cleome lutea and C. serrulata, the C. gynandra, the pollen and nectar-feeding activity
flowers do not attract nocturnal visitors but attract of thrips may further drive the pollinating bees and
plentiful bees, wasps and butterflies during daylight butterflies to visit a number of conspecific plants for
hours. Chweya & Mnzava (1997) stated that C. gy- the floral rewards, due to which cross-pollination is
nandra is pollinated especially by honeybees, spi- maximized.
ders and the wind. The present study shows that in Ekpong (2009) reported that Cleome plants are
C. gynandra, the flower-opening occurs during dusk mainly propagated by seed. Keller & Kollmann
hours and it is pollinated principally by bees during (1999) observed that seed germination in Cleome is
dusk hours and again during the forenoon period of erratic and may take up to one year to reach maxi-
the next day. Anemophily occurs on clear sunny days mum germination. Chweya & Mnzava (1997) have
due to freely dispersed dry, powdery pollen grains also opined that seed germination is poor and de-
from the anthers. It is important in the afternoon pe- layed in Cleome, due to dormancy and this is one
riod, since insects do not visit the second-day flow- of the major problems in the propagation of these
ers. The ability of the plant to use both bees or insects plants. Aziz & Shaukat (2012) reported that C. vis-
and wind is indicative of ambophily. In C. viscosa, cosa completes its life from seed germination to seed
anthesis occurs during morning hours and it is pol- set in 12 weeks. In the present study, C. gynandra
linated principally by bees and butterflies; in the lat- and C. viscosa release seeds from the pods explosive-
ter category, pierids are prominent pollinators. Wind ly and they are dispersed by wind due to their light
has no role in the pollination of this species, since weight; they germinate immediately and produce
its pollen is sticky and does not disperse in powdery new plants, if soil has moisture in case of C. gynan-
form. Therefore, it is exclusively entomophilous, and dra, but remain dormant and germinate only during
if categorized specifically, it is both melittophilous rainy season in case of C. viscosa. Furthermore, the
and psychophilous. Aparadh & Karadge (2011) de- seeds of both species also disperse during early rainy
scribed pollen characteristics for these two species season by rain water. Kokwaro (1976) reported that
and the present study confirms the same regarding C. gynandra is spread by birds, and by dispersal ow-
pollen features. Ruiz & al. (1997) reported that the ing to capsule dehiscence. Therefore, the dispersal
pollen morphology and exine sculpturing of Cleome modes recorded in these species enable them to mi-
species do not indicate any relationship with pollina- grate and colonize new areas.
tion syndromes. It appears to be true in the present Baker & Stebbins (1965) stated that Cleome spe-
study also for Cleome species, especially C. gynandra, cies possess pollination traits that have long been
which has mixed characteristics adapted for versatile considered favourable for colonists. Cane (2008) re-
pollination syndrome, anemophily and entomophily. ported that self-fertility enables the first individual
Cleome gynandra and C. viscosa produce pollen that colonizes a site to produce viable seed. If polli-
in copious amount and in both species it is a source nators are absent, perhaps following some ecological
of six essential amino acids and nine non-essential perturbation such as fire or flood, they are capable
amino acids sensu DeGroot (1953). The protein con- of autogamy and facilitate self-pollination. In C. gy-
tent is relatively higher in C. gynandra than in C. vis- nandra and C. viscosa, pollination traits are expect-
cosa. Therefore, the pollen of these two species is ed to favour self-fertility, when pollinator services
nutritionally important for bees. Since pollen pro- might be unreliable. The ability of these plants to use
duction rate is huge at plant and population level in a facultative autogamous breeding system is advan-
both species, their pollen collection activity may not tageous, as the delayed autogamy would enable them
significantly reduce the pollen availability for polli- to set fruit and spread rapidly onto new sites without
nation purpose. The nectar of C. gynandra is also a precluding the ability to exchange genes within the
26 Raju, A.J.S. & Rani, D.S. • Reproductive ecology of Cleome gynandra and C. viscosa
population at large, when one develops through out- is an adaptational mechanism that enables them to
crossing (Klips & Snow 1997). survive in drier and hot environments, such as sem-
Krupnick & Weis (1998) reported that Isomer- iarid, subhumid and humid climates consisting of
is arborea (Capparaceae) produces greater num- many soil types (Osborne & Freckleton 2009; Mishra
bers of hermaphroditic flowers and fewer male flow- & al. 2011). Despite increasingly higher atmospheric
ers per inflorescence, when the flowers are damaged CO2 levels, warmer global temperatures are expect-
by the nitidulid beetle, Meligethes rufimanus. Even ed to promote the expansion of C4 species range in
though more hermaphroditic flowers are produced the near future and such a situation could represent
per inflorescence, damage to the ovaries by the flow- C4-dominated systems in warm regions (Sage 2004).
er-feeding insects is so extensive that fruit produc- Cleome viscosa is a C3 species, while Cleome gynan-
tion is lower among plants exposed to herbivory, as dra is a C4 species. The former predominates in cool
compared to plants protected from herbivory. Under environments, while the latter predominates in warm
low-herbivore conditions in natural habitats, this al- environments. Such versatility enables C. gynandra
ternation of sexes is apparent in I. arborea and al- to invade and flourish well in diverse environments
so in Cleome spinosa. Herbivory damage thus affects and extend its distribution range (Silva & al. 2011).
male and female reproductive success in ways be- Cleome gynandra is a suitable plant for considera-
yond its effect on resource allocation to sex. In this tion in the restoration of ecologically degraded and
context, Strauss & Irwin (2004) stated that herbivore warm habitats. Kumar & al. (1984) have experimen-
damage can indirectly affect plant fecundity by influ- tally proved that this plant is tolerant and resistant to
encing interactions between plants and pollinators. salt and water stress, which is important for erosion
In the present study, C. gynandra and C. viscosa are control and, hence, is an ideal weed in both warm
not exposed to herbivory, despite the presence of cer- and cool environments. Apart from these advantag-
tain beetles which commonly feed on the flowers of es, they have a unique role to play in plant commu-
herbaceous flora, such as Mylabris phalerata feeding nity restoration, bloom quickly and sustain diverse
on the occurring species Sida acuta and S. cordifolia. insect pollinator, as well as herbivore communities
Therefore, Cleome species appear to be resistant to (Cane 2008). Cleome species are used as leafy vege-
floral herbivory and, hence, are insulated from flo- tables in many regions (Theophilus & Arulanantham
ral herbivores that affect their reproductive success. 1949; Ekpong 2009). Therefore, these species are im-
The genus Cleome is a suitable subject for the portant ecologically, medicinally and economically,
study of versatile adaptations, which permit it to and are essential constituents of tropical ecosystems
invade and flourish well in diverse habitats, due to by their interactions with local insects/animals and
possession of both C3 and C4 photosynthetic mech- serve their part as constituents of biodiversity.
anisms (Benedito 2007). The C4 plants have advan-
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