Pollination
and seedling ecology of Decalepis hamiltonii Wight & Arn. (Periplocaceae), a commercially
important, endemic and endangered species
A.J. Solomon Raju 1 & K. Venkata Ramana 2
1,2 Department of Environmental
Sciences, Andhra University, Visakhapatnam, Andhra Pradesh 530003, India
Email: 1 ajsraju@yahoo.com
Date of publication (online): 26
October 2009
Date of publication (print): 26
October 2009
ISSN 0974-7907 (online) |
0974-7893 (print)
Editor: K.R. Sasidharan
Manuscript details:
Ms # o2168
Received 27 March 2009
Final received 19 June 2009
Finally accepted 03 October 2009
Citation: Raju, A.J.S. & K.V. Ramana(2009). Pollination and seedling ecology of Decalepis hamiltonii Wight
& Arn. (Periplocaceae), a commercially important, endemic and
endangered species. Journal of Threatened Taxa1(10): 497-506.
Copyright: © A.J. Solomon Raju & K. Venkata Ramana 2009. Creative Commons Attribution 3.0 Unported License. JoTT allows
unrestricted use of this article in any medium for non-profit purposes,
reproduction and distribution by providing adequate credit to the authors and
the source of publication.
Author Details: Dr. A.J. Solomon Raju is currently an
Associate Professor with more than 250 research papers. He is on the editorial
board of several international journals. He is presently working on endemic and
endangered plant species in southern Eastern Ghats forests with financial
support from DST, CSIR and UGC.
K. Venkata Ramana is working as
Junior Research Fellow from 2007 in a DST Research Project on endemic and
endangered plant species. He has registered for PhD under Dr. Raju. He has published two research papers.
Author Contributions: AJSR conceived the concept, ideas, plan of work
and did field work
and prepared the paper. KVR did extensive field work and tabulated the
observational and
experimental work for the paper.
Acknowledgements: This study is a part of the research work of a project
funded by the
Department of Science and Technology, Government of India, New Delhi.
Abstract: Decalepis hamiltoniiis a woody climber and annual bloomer. The flowers are characterized by nectariferouscoralline corona, gynostegium and polliniacontaining tetrads. The floral features
such as greenish white corolla, mild fragrance, flat-shape for easy access to
floral rewards, and ovary protection from the biting mouthparts of the
pollinator make up cantharophilous pollination
syndrome. Brachinus beetle is the principal pollinator. Thrips use floral buds to raise their offspring; they also
effect pollination while collecting nectar; but they are important largely for
self-pollination due to their short distance flying ability. The plant is a self-incompatible, obligate outcrosser and is substantiated by 2% natural fruit set,
but each fruit produces numerous seeds. Fruits dehisce during the dry season and seed dispersal is by wind. Seeds germinate as soon as they fall in a favourable place, but only a small
percentage establish seedlings. Over-exploitation, bottlenecks in sexual reproduction and seedling
establishment may contribute to the endangered status of D. hamiltonii.
Keywords: Anemochory, cantharophily, Decalepis hamiltonii,
seedling ecology, self-incompatibility.
For Images & Figures –
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Introduction
The family Periplocaceaeis an offshoot of the Asclepiadaceae based on certain
taxonomic characteristics. Most Periplocaceae taxa inhabit
tropical and subtropical forests and savannahs as woody climbers, woody shrubs,
epiphytes, or herbaceous geophytes. The
flower is complex and has evolved into many forms, always incorporating a
coralline corona, interstaminal corona-like nectaries, and stamens fused with the style-head into a gynostegium. Pollen
is borne in tetrads which are shed after anthesisinto spathulate or spoon-shaped translators that are
secreted in grooves around the periphery of the style-head (Johan et al.
2001). The members of this family are entomophilous; hawkmoths and
flies are recorded as legitimate pollinators; but this generalization is based
on a few plant species for which information is available (Ollerton& Liede 1997; Watson & Dallwitz2008).
Decalepis is a monotypic
genus of Periplocaceae; it is represented by the
species D. hamiltonii (Venter & Verhoeven 2001). In
India, it is endemic to southern India (Karnataka, Kerala, Tamil Nadu and
Andhra Pradesh) and assessed as Endangered (Ravikumar& Ved 2000; Reddy et al. 2003). It is gradually declining due to
over-exploitation and habitat destruction. The leaves and fruits are
medicinally important. The tuberous roots (Image 5g) are used as a laxative, as
an appetizer and as a health tonic. The Yanadi tribe prepares a herbal
drink from the roots, and chewing the roots is regarded to give relief from
indigestion. In the food industry, the
root extract is used as substitute for vanillin and the roots are pickled (Vedavathy 2004; Jonathan 2006). The root extract is also used as a substitute
for the roots of Hemidesmus indicus to make soft drinks and beverages. Therefore, the roots of this plant are
marketed on a large scale. Regeneration
of this species is severely affected since most of the plants are harvested in
a reproductively immature stage. D. hamiltonii is a commercially important plant due to its
importance in nutraceuticals and food products. Information on its reproduction is highly
desirable so that effective strategies for domestication can be made. Hence, we report on these aspects for the
first time and this information is useful for understanding its reproductive
ecology and the factors responsible for the threatened status of D. hamiltonii.
Materials and Methods
D. hamiltonii is a woody
climber, occurs in open rocky slopes and crevices and by stream banks, in
bushes and thickets in deciduous forests of TirumalaHills and surrounding areas of Eastern Ghats (13042’N & 79020’E;
746m). The sites for the present study
include Akasaganga and Papavinasanamof Tirumala Hills in ChittoorDistrict, Andhra Pradesh (Image 1a). This species is found to be associated with Phyllanthus polyphyllus, Syzygium alternifolium, Buchanania axillaris, Commiphora caudata, Terminalia pallida, Walsura trifolia, and Hugonia mystax. The study was conducted during 2007 and 2008. The phenology and
floral biology were examined following the methods of Dafniet al. (2005). Twenty five flowers were
used for the study of floral morphology. Observations on flower visitors (thrips and
beetles) and their foraging period with reference to pollination were recorded
by using binoculars. Beetles and thrips, ten each
were collected from the flowers for microscopic examination for observing the
presence of pollinia and/or tetrads. Twelve inflorescences with 125 flowers were
tagged and followed for quantifying flower predation rate by beetles. For autogamy, 23
inflorescences with 260 flowers were bagged and were observed for fruit
set. For open-pollination fruit set, 20
inflorescences with 193 flowers were tagged. Natural fruit set rate, maturation and fruit dehiscence, dispersal, seed
germination and seedlings establishment were thoroughly examined. Seed germination and seedlings establishment
rate was also evaluated in experimental trays/pots; 360 seeds collected from
the field were used for this purpose.
Results
In D. hamiltonii,
leaf flushing occurs in May soon after monsoon showers which occur in May. This is immediately followed by flowering
which extends up to August. An
individual climber produces a few flowers per day (Range 15-37). The flowers are borne on terminal and axillary cymose inflorescences;
each inflorescence bears 11±3 (Range 5-16) flowers which antheseover a period of 1-2 weeks. The flowers are pedicellate,
small (5mm long and 6mm across), greenish white, mildly fragrant, bisexual, actinomorphic and horizontally oriented. Sepals are five, light green, 1mm long and valvate. Petals are
five, basally united, greenish white, villous within, 4mm long and recurved. Stamens
are five, fertile, filaments short and free, free from ovary, epipetalous, near
the base of the corolla tube, fused with the style-head into a gynostegium.
The spoon-shaped structures called
“translators’ arising from the style head between the anthers conceal the stigmatic surfaces. Anthers are conniventat apex above stigma, basifixed, ovoid to rhomboid,
fused to bottom of style head and dehisce by longitudinal slits. The style-head with five grooves support the
anthers. Each anther contains four free pollinia. After anther dehiscence, the pollinia are deposited on the spoon of the translator. Each polliniumcontains free tetrads which come in different shapes - tetrahedral, rhomboidal
and linear (Image 2a-d). Single anther
contains 170-230 tetrads and the total number of tetrads per flower ranges from
850-900.
The coralline coronas are composed of
five distinct pad-like yellow-coloured segments,
positioned on the petals in one whorl, aligned with the petals and located
between the corolla and androecium. Nectariferous parts
of the corona are incorporated internally into the gynostegium(Image 1d,e). Ovary has two separate carpels each contains
70-102 ovules (Image 2e), two styles which are free up
to the stigma, and united terminally by the common stigma or style head. The stigma is apically flat, wet and covered
above by stamens and translators (Image 1f,g).
Mature buds are ovoid, begin to open
from 0700hr and are fully open by 0800hr (Image 1b,c). Anther dehiscence and stigma receptivity
occur after anthesis; the stigma receptivity extends
until the evening of the second day. The
duration of stigma receptivity is 32 hours. Hydrogen peroxide test of Dafni et al. (2005) was
followed to assess the stigma receptivity. The flowers begin to shrivel on the 3rd day and fall off on the 4th day. In
fertilized flowers, the stamens and stigma drop off within a week while calyx,
corolla and corona remain there even after fruit emergence. These floral parts fall off when the
follicles begin to diverge.
Buds and flowers were found to be
associated with thrips until senescence in all
plants. The number of thrips found per flower varied from 8 to 10. The thrips are
1-1.5 mm long, yellow (Image 2j), collected nectar aliquots from nectarine
corona and moved from flower to flower. The thrips were found with free tetrads but
not with pollinial masses. Further, Bombardier Beetle, Brachinus sp. (Carabidae)
was found visiting the flowers during daytime throughout the flowering season
(Image 2f-h). The foraging schedule is
presented in Fig. 1. The beetle is 6-9 mm long; the head and thorax are red and
the abdomen is shiny metallic black. The
number of beetles found per inflorescence is 1-2 at each hour during
daytime. The beetle collected nectar
from nectarine corona during which it was found carrying translators with
anthers/pollinia. An examination of the beetles sampled from the flowers showed pollinia. It also
fed on corona, petals and secretions of stigma (Image 2i) and such flowers have
not produced fruits. The flower
predation rate is 3%. The removal of translators and anthers by the beetle
exposed the stigma which facilitates to receive the tetrads in subsequent
visits by the beetle.
The mature buds that were bagged to
assess autogamy did not produce fruits. Natural fruit set is 2% only. Fruits begin to grow immediately after
pollination and fertilization while the petals and corona are still intact
(Image 3a). The free ovaries with
growing seeds begin to bulge and diverge in opposite directions from the
initial stage of fruit growth and seed development and produce 2-follicled
non-fleshy, dehiscent fruits (Image 3c-f). The fruits are initially green and turn dark brown when mature and ripe
(Image 3g). They take 8-9 months to
mature. The ripe follicles are
ellipsoid, cylindrical and wrinkled; each follicle is about 60mm long and 17mm
wide (Image 4a). The plant begins to
shed leaves gradually from fruit colour transitional
stage from green to brown and is leafless when fruits are ripe and dry; the
period of leafless state is from January-April. Each follicle contains 70±11, ovate, 6mm long, 4mm wide and 10mg weight
reddish-brown coloured seeds crowned with a tuft of
28mm long silky hairs, and are well seated on the denticlesof thick cylindrical placenta of the ovary (Image 4c-e). The follicles dehisce during summer season;
then the placenta with seeds intact comes out of the follicle (Image 4b). Gradually, the seeds are released from the denticles of the placenta and disseminated by wind due to
their very light weight.
D. hamiltonii seeds were
found to germinate soon after early monsoon showers in May on soil floor and
rocky areas which are rich in litter and other organic matter (Image
4f-h). The experimental results of seed
germination rate and thereof subsequent seedling growth and development are
presented in Image 5. The results showed
that seed germination rate is 13% out of which seedling establishment rate is
48% (Fig. 2). The overall seedling
establishment rate in relation to total seeds sown is only 6%. The seeds are not dormant and germination
occurs from day 4 to day 45 from the date of sowing. The number of germinated seeds gradually
increased, reached to a peak during 3rd week and then onwards gradually
decreased (Fig. 3).
Discussion
The flower in D. hamiltoniiis characterized by nectariferous coralline corona, gynostegium, and polliniacontaining tetrads; these characters are considered as evolutionary adaptations
to specialized entomophily (Rahman& Wilcock 1991; Johan et al. 2001). In Periplocaceae to
which D. hamiltonii belongs, the presence of
free staminal filaments and the production of free
pollen tetrads which are shed after anthesis, the
position of coralline corona on corolla and alignment with the corolla lobes
are important distinguishing ancestral characters (Rahman& Wilcock 1991; Fishbein2001); all these characters are found in D. hamiltonii. Coralline corollas are typical of scales or
filament-like structures in Periplocaceae, while they
are of pad type in Secamonoideae and Asclepiadoideae (Kunze 1990;
1993; Nilsson et al. 1993; Klackenberg 1998). But, D. hamiltoniibeing a Periplocaceae memberpossessess coralline coronas which are typical of
‘pad’ type, supporting the translators marginally and present nectar at the
same position.
In D. hamiltonii,
lack of fruit set in bagged untreated flowers is suggestive of pre-zygotic
self-incompatibility and hence the plant is an obligate outcrosser. This is further substantiated by the very
small percentage of natural fruit set. Anther dehiscence during the period of stigma receptivity and deposition
of tetrads from the same flower or plant on the stigma are of no use to the
plant. The long period of stigma
receptivity maximizes the options to receive tetrads from the flowers of conspecific plants. Thrips and beetles pick up and transfer translators with
tetrads/pollinia from one flower to another while
collecting nectar aliquots. The thrips are naturally short-distance flyers and hence they
largely contribute to self-pollination during their flower to flower visits on
the same plant and effect cross-pollination during their flower visits to
another conspecific plant; moderate winds of the
study areas may extend the travel distance of thripsand accordingly they may effect more cross-pollination during their plant to
plant visits. The presence of thrips in floral buds of D. hamiltoniiindicates that egg deposition by female thrips takes
place prior to bud formation and eggs hatch and produce larva or adult thrips by the time the buds open. These thripsrepresent suborder Terebrantia of the order Thysanoptera. The
females of this group of thrips have an ovipositor
with which they cut slits into plant tissue in order to insert their eggs, one
egg per slit (Heming 1993). With this
ability, these thrips raise their offspring in floral
buds.
Ollerton & Liede (1997) stated that pollination by Hymenoptera is most
common with Lepidoptera and Diptera having a
secondary, but still important role in Asclepiadaceae. Further, they mentioned that in Periplocaceae, hawkmoths and
flies are legitimate pollinators and also expressed that the range of
pollinators may be much broader. These
two categories of insects have not been found on the flowers of D. hamiltonii. Faegri & van der Pijl (1979) reported that the floral features such as
greenish-white colour, mild fragrance and flat-topped
architecture are adaptations for hawkmothpollination. In the vicinity of D. hamiltonii, the diurnal hawkmoth,Macroglossum gyransis a common visitor to Lantana camara but it
never visited D. hamiltonii and hence, this
study does not agree with the above report. The beetle, Brachinus sp. is the
principal pollinator of D. hamiltonii; the
floral features such as greenish white colour,
fragrance emission, flat-shape for easy access to floral rewards, and deep
seated ovary insulated from the biting type mouthparts of the pollinating agent
have been considered to be adaptive for beetle-pollination (Gullan& Cranston 2005). The beetle feeds on nectar aliquots
secreted by coralline corona. It also
feeds on other floral parts causing damage to the flower; the percentage of
damaged flowers is however small and hence is nearly insignificant. The flowers produced per day and per plant
are few and such a small number is not sufficient to meet the forage
requirement of the beetle. In effect,
the beetle flies to many individual plants to collect forage and transfers
tetrads to effect cross-pollination. This study adds beetles as another category of pollinators for Periplocaceae species.
The pollination mechanism in D. hamiltonii is conspicuously specialized. It involves spoon-shaped translators arising
from the style head between the anthers, which conceal the stigmatic surfaces
from pollinator and into each of which the pollen from the adjacent half-anther
is shed. The translator adheres to the
head and legs of beetle and thrips, which carry the
translator and its pollen (tetrads) to other flowers of the same and/or
different plants. Then, the stigma gets
exposed and receives pollen from other flowers in successive visits by the
pollinators (Ollerton & Liede1997; Watson & Dallwitz 2008).
The natural fruit set rate in D. hamiltonii is indicative of pollinator limitation. The extended flowering pattern with the
production of a small number of flowers per day and per plant is in a way
appears to be the principal factor to attract only a very small number of
beetles daily. However, the fruit set
rate is compensated by higher number of seeds per fruit. The fruits take a long period of time to
mature and dehisce to disseminate seeds. The dry season provides ideal conditions for fruit dehiscence and
dispersal of seeds. The timing of fruit
maturation and ripening is so perfect that it occurs during dry season when the
plant is completely leafless. The light
weight of the seed crowned with a tuft of silky hairs is an important
aerodynamic trait characterizing “anemochory”. But, anemochory is
considered inefficient because it indiscriminately places propagulesin every type of habitat (Greene & Johnson 1986). In D. hamiltonii,
the placenta with seeds well seated on its denticlescollectively comes out of the dehisced follicle, settles on the ground and then
individual seeds gradually disseminate by wind at low height. This mode of seed dispersal is more efficient
than individual seed dispersal directly from the fruit.
Seeds are not dormant and germinate
immediately if favourable conditions exist in
soil. Experimental results also
substantiate the same. A small
percentage of seed germination evidenced in the experiments suggests that all
seeds are not viable and this may be due defects in seed formation. Further, all those that germinated have not
established seedlings; this may be due to insufficient flow of nutrients into
seeds when they are being formed and to genetically inferior seeds. In the study sites also, there are a number
of seedlings emerged initially but finally a few of them have established
depending on the nutrient status of soil and their ability to compete with the
co-emerging seedlings or plants of other species. This observation is based on 980 seedlings
which have emerged naturally at the study sites; of these only 47 finally
established to grow further. Therefore,
the study suggests that extended flowering pattern, self-incompatibility,
pollinator limitation, absence of seed dormancy, abortion of a considerable percentage
of seedlings prior to establishment are contributing factors for the regulation
of population size of D. hamiltonii in its
natural areas.
The tuberous roots of D. hamiltonii are over-exploited prior to reproductive
maturity due to their economic and medicinal values. This exploitation is the main factor for
gradual decline of natural occurrence of this plant. The internal and external factors as stated
above coupled with over-harvesting of roots collectively qualify D. hamiltonii for endemic and globally endangered status.
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