Monoecy,
anemophily, anemochory and regeneration ecology of Hildegardia populifolia(Roxb.) Schott. & Endl. (Malvaceae), an economically important endemic and
endangered dry deciduous tree species of southern Eastern Ghats, India
A.J.
Solomon Raju 1, P. Hareesh Chandra 2 & J. Radha
Krishna 3
1,2,3 Department
of Environmental Sciences, Andhra University, Visakhapatnam, Andhra Pradesh
530003, India
1 ajsraju@yahoo.com
(corresponding author), 2 hareeshchandu@gmail.com, 3 jrkrishna30@gmail.com
Abstract: Hildegardia populifolia is a
critically endangered tree species. All phenological events—leaf flushing, shedding, flowering, fruit
dispersal occur one after the other during the dry season. It is
morphologically andromonoecious but functionally monoecious. It produces a
strikingly male-biased male and bisexual flower ratio; it is self-incompatible
and obligately outcrossing. The
flowers are nectariferous and the nectar has hexose-rich sugars, some essential
and non-essential amino acids. Trigona bee and Rhynchium wasp
were the exclusive foragers, though their foraging activity does not promote
cross-pollination. The male flower
number, the pollen output, the pollen characteristics and the placement of
anthers on the top of androphore conform to anemophily. The natural fruit set does not exceed
5%. The fruit is 5-follicled with
one or two seeds. The low fruit set is compensated by the
production of more 2-seeded follicles. Fruit characteristics such as
wing-like follicles, membranous follicle sheath and being very light weight characterize anemochory. Seeds with a hard coat do not germinate
readily during the rainy season and their germination depends on the soil
chemicals and nutrient environment. The soil is deficient in nitrogen, potassium and phosphorous. Partly burned seeds due to natural or
human-caused fires germinate quickly in water saturatedsoil. The study suggests that seed
germination and seedling growth rates are regulated by intrinsic and extrinsic
factors along with natural and anthropogenic fires. We recommend that seedlings should be
raised in nurseries and then transferred to natural habitats to build up the
population.
Keywords: Anemochory, anemophily, Hildegardia populifolia, Critically
Endangered species, monoecy, obligate outcrosser, seed ecology,
self-incompatibility.
doi: http://dx.doi.org/10.11609/JoTT.o3665.5434-46
Editor: Cleofas Cervancia, University of Philippines Los
Baños College Laguna, Philippines. Date
of publication: 26 February 2014 (online & print)
Manuscript details: Ms # o3665 | Received 14 June
2013 | Final received 30 January 2014 | Finally accepted 02 February 2014
Citation:Raju, A.J.S., P.H. Chandra & J.R. Krishna (2014). Monoecy,
anemophily, anemochory and regeneration ecology of Hildegardia populifolia(Roxb.) Schott. & Endl. (Malvaceae), an economically important endemic and
endangered dry deciduous tree species of southern Eastern Ghats, India. Journal of Threatened
Taxa 6(2): 5434–5446; http://dx.doi.org/10.11609/JoTT.o3665.5434-46
Copyright: © Raju et al. 2014. Creative Commons Attribution 3.0 Unported
License. JoTT allows unrestricted use of this article in any medium,
reproduction and distribution by providing adequate credit to the authors and
the source of publication.
Funding: Ministry of Environment and Forests, Government
of India, New Delhi.
Competing Interest: The authors declare no
competing interests.
Author Contribution: AJSR conceived the concept, ideas, plan of work and did part of field work and prepared the paper. PHC and JRK did field work and tabulated
the observational and experimental work of the paper.
Author Details: Prof. A.J. Solomon Raju is
Head of the Department of Environmental Sciences, Andhra University, Visakhapatnam. He is the recipient of several national and
international awards. He has more than 250 research papers in international and
national journals. 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 MoEF and CSIR. P. Hareesh Chandra is
working as senior research fellow in the MoEF research project. He has
registered for PhD with Prof. Solomon Raju. He has published five research papers. J. Radha Krishna is working as junior
research fellow in the MoEF research project. He has registered for PhD with Prof.
Solomon Raju. He has published four
research papers.
Acknowledgements: We thank Mr. K. Venkanna, Technical
Officer, Central Research Institute for Dry land Agriculture, Hyderabad, for
doing soil NPK analysis, and Dr. K.V. Ramana for assisting in the work as and when
required.
For figures, images, tables -- click here
INTRODUCTION
Hildegardia is a genus of deciduous trees and placed
in the sub-family Sterculioideae and tribe Sterculieae of the expanded
Malvaceae. Hutchinson (1967) has
distinguished this genus from the other genera of Sterculieae by its flowers
lacking petals and epicalyx and possessing an androgynophore and by the
combination of the traits of indehiscent and thin, membranous or papery
fruits. He stated that this genus
consists of 12 species and has a pantropical distribution in West Africa, East
Africa, Madagascar, southern India, Philippines, Indonesia, northern Australia
and Cuba. Zaborsky (2009) noted
that three of them (H. barteri, H. gillettii, H. migeodii) are
found in Africa, four (H. ankaranensis, H. erythrosiphon, H. perrieri, H.
dauphinensis) in Madagascar, one (H. australiensis) in
Australia, one (H. cubensis) in Cuba, and three (H. merrittii, H.
populifolia and H. sundaica) in Asia. The African species are associated with
tropical dry deciduous wood or bushland forests while the malagasyspecies are associated with tropical dry or humid/wet forests. All Hildegardia species belong to
one of these categories—vulnerable, threatened, endangered and endemic
due to their multiple local and economic uses (Masters 1868; Merill 1914;
Arenes 1959; Wild 1961; Dorr & Barnett 1990; Cheek & Leach 1991;
Zaborsky 2009).
In the Hildegardia genus, H. populifolia is the only species which occurs in India. Its conservation
status has been reported differently by different workers such as Critically
Endangered (Sarcar & Sarcar 2002), Endangered (Ahmedullah 1990; Walter
& Gillet 1998) and Vulnerable (Reddy et al. 2001; Jadhav et al.
2001). The World Conservation
Monitoring Center (1998) assessed its conservation status as critically endangered. Sarcar & Sarcar (2002) mentioned
that its distribution is restricted to certain places of the Eastern Ghats in
Andhra Pradesh and Tamil Nadu in southern India. Rao & Pullaiah (2007) stated that it
is very rare in the dry deciduous forests in the Eastern Ghats. Sandhya Rani et al. (2007) reported that
it occurs in the middle (Anantapur and Chittoor districts of Andhra Pradesh)
and southern Eastern Ghats (North Arcot District of Tamil Nadu) above 250m. Reddy et al. (2003) mentioned that it is
endemic to the middle and southern Eastern Ghats; it occurs on the Nigidi Hills
of Anantapur and Ankalammakonda of Chittoor in Andhra Pradesh, and Kalrayan and
Pakkamalai Hills in Villupuram and also in Salem. Ahmedullah (1990) noted that it is known to be represented by a sole surviving population
comprising about 20 trees in the Kalrayan Hills of Tamil Nadu. Rao et al. (1998) recognized five
sub-populations of this species in the Rayalaseema region of Andhra Pradesh.
Rao et al. (2011) located the species mostly above 420m in Anantapur, Kadapa
and Chittoor districts in southern Andhra Pradesh, the Salem Hills in northern
Tamil Nadu and a small patch in Karnataka bordering Anantapur District of
Andhra Pradesh. They also found
that this species is restricted to top hills and rock boulders, growing in
sandy red soil. Based on their
field study, they stated that this species qualifies for vulnerable status
since there is no significant decline in population size or in the number of
individuals in different localities. In our field studies, we found that there
is only one distinct and stable surviving population near Kadiri in Anantapur
District, Andhra Pradesh.
Hildegardia genus was not studied in detail for
taxonomic characters and for any aspect of reproduction in any part of the
world despite its endemic and endangered status. The flowers in this genus are reported
to be either dioecious or monoecious or polygamous (Wild 1961; Dorr &
Barnett 1990; Cheek & Leach 1991; Sarah 2011). Steentoft (1988) stated that
Sterculiaceous flowers are nectarless and Hildegardia
barteri flowers are pollinated by bees collecting pollen in West Africa. Roma (2002) mentioned that the malagasy H. erythrosiphon is nectariferous and the
nectar volume varies over the day, peaking around midday and also varies
between individual trees. He noted
that the sunbirds Nectarinia souimanga and N. notata visit the
flowers mostly during the morning period for nectar and effect
pollination. Further, the Lesser
Vasa parrot, Coracopsis nigra serves as flower predator as well as
pollinator (Malalatiana 2002). In
India, H. populifolia has not been studied in detail for any aspect
including its taxonomy and reproductive biology so far. Therefore, the present study is
contemplated to provide details on the floral biology, pollination, fruiting
and seedling ecology keeping in view its endemic and endangered status. The information presented here forms the
basis for further studies on this genus in India and elsewhere in the
distributional areas of Hildegardia for understanding the relationships
between species within the genus.
MATERIALS AND METHODS
A small population of about 60 individuals of Hildegardia populifolialocated in the dry deciduous forest near Alampur in Kadiri area (14006’N
& 78009’E) at 360m in southern Eastern Ghats, Anantapur District
in the southern Eastern Ghats of Andhra Pradesh, was used for the study during
2011 and 2012. The
forest is characterized by steep slopes, rocky terrain, dry and poor stony
soils with deciduous vegetation. The ambient temperature range was recorded using a thermometer, the
relative humidity range using a hygrometer and wind speed range using an
anemometer. Twenty-five trees were
tagged for recording the phenological events; ten flowering inflorescences from
the same trees were used for noting the male and bisexual flower ratio in both
the study years. Fifty tagged
mature buds from ten trees were followed for recording the time of anthesis and
anther dehiscence; the mode of anther dehiscence was also noted by using a 10x
hand lens. Five flowers each from
10 trees selected at random were used to describe the flower details for male
and bisexual flowers separately. Twenty mature but undehisced anthers from male flowers of 10 different
plants were collected and placed in a petri dish. Later, every time a single anther was
taken out it was placed on a clean microscope slide (75x25 mm) and dabbed with
a needle in a drop of lactophenol-aniline-blue. The anther tissue was then observed
under the microscope for pollen, if any, and if pollen grains were not there,
the tissue was removed from the slide. The pollen mass was drawn into a band, and the total number of pollen
grains was counted under a compound microscope (40x objective, 10x eye
piece). This procedure was followed
for counting the number of pollen grains in each anther collected. Based on these counts, the mean number
of pollen produced per anther was determined. The pollen grain characteristics were
recorded by consulting the book of Bhattacharya et al. (2006). Similarly, pollen output in the anthers
of bisexual flowers was also recorded but they are sterile and not released due
to indehiscent anthers. Pollen fertility was assessed by staining them in 1% acetocarmine. Five flowers each from 10 trees were
used for testing stigma receptivity, nectar volume and sugar types. These aspects were examined following
the protocols given in Dafni et al. (2005). Nectar was also analyzed for amino acid
types by following the Paper Chromatography method of Baker & Baker
(1973). The foraging activity of
insects was observed during the daytime for 15 days in each year. In both the
years, the same insects were recorded. They were observed with reference to the type of forage they collect,
contact with essential organs to result in pollination and inter-plant foraging
activity in terms of cross-pollination. Birds were observed as visitors to the plant; the purpose of their
visits was carefully observed in order to record whether they have any role in
effecting pollination. Fifty mature
buds, five each from 10 inflorescences on five trees were bagged with a plastic
mesh with mesh size of 2x2 mm a day before anthesis without manual self
pollination to know whether fruit set occurs through autogamy. Another set of 50 mature buds was
selected in the same way, then emasculated and bagged a day prior to
anthesis. The next day, the bags
were removed and the stigmas were brushed with the freshly dehisced anthers
from the flowers of the same tree and re-bagged to know whether fruit set
occurs through geitonogamy. Another
set of 50 mature buds was selected in the same way, then emasculated and bagged
a day prior to anthesis. The next
day, the bags were removed and the stigmas were brushed with freshly dehisced
anthers from the flowers of other trees and re-bagged to know whether fruit set
occurs through xenogamy. Ten
inflorescences on each tree were tagged for fruit set in open-pollination. The bagged flowers and tagged
inflorescences were followed for eight weeks to record the results. Fruits and
seed characteristics were also recorded. Fruit is a follicle type and each one consists of 1–5
follicles. Keeping this in view,
the follicle-wise fruit set rate and seed set rate was recorded. Field observations on the fruit
maturation duration and dispersal mode were recorded. Records were maintained
on in vivo and in vitro seed germination rates. In vitro experiments were conducted in
the local forest nursery. Further,
observations were made on seedling establishment rates in the natural
habitat. The study area is exposed
to natural and human-caused fires; the state of fruits and seeds after fire was
noted. A sample of 150 partly burned seeds were collected from the study area
and used for seed germination rate in pot experiments. The soil analysis for
NPK was done by the Central Research Institute for Dry land Agriculture,
Hyderabad. Field observations on
soil status in the natural habitat were also noted. The plant habit, flowers,
fruits, seeds and seedlings were photographed with a Nikon D40X Digital SLR
(10.1 pixel). A Magellan Explorist
210 Model Digital Global Positioning System was used to record the
coordinates—latitude, longitude and altitude.
RESULTS
Hildegardia populifolia is a deciduous tree and
grows to a height of 15–20 m (Image 1a). The stem bark is smooth, pale green and
fiber-rich; the wood is silverfish white, branchlets angular and warty. The leaves are long petiolate
(6–12 cm), large, ovate-cordate, 3–5 lobed, deeply cordate at the base,
acuminate at the apex with entire margin and palmately 7-nerved. The recurring phenological events, leaf
shedding, flowering, leaf flushing and fruiting occur, one after the other. The leaf shedding activity starts at
population level any time between the 2nd and 4th week of
November and ends any time between the 2nd week of February and 3rdweek of March. At the population
level, the flowering phase starts during the fag-endof leaf shedding; the flowers begin to appear from the last week of February
and the flowering ceases by the end of the 3rd week of April. An individual tree flowers for
20–36 days (Table 1). Leaf
flushing activity starts at population level from the 1st week of
April and ceases by the end of May but individual trees complete the leaf flushing event within four weeks.
The flowers are borne on 12.5±3.2 cm long axillary or terminal
paniculate inflorescences. An individual inflorescence produces 34±8 (Range 21–52)
flowers over a period of 6–7 days. The flowers are pedicellate, 12–14 mm long and 3mm wide, scarlet
and actinomorphic. Each
inflorescence produces bisexual (Image 1d) and male flowers (Image 1e) but
their ratio varies at the tree level and also between years. The sex ratio varies at tree level and
between years. In the observed trees, the bisexual to male ratio is 1: 0.5 to
1:34 at tree level in 2011 and 1:1 to 1:72 in 2012. Four trees produced only male flowers in
2011. One tree
which produced only male flowers and another tree which showed 1:0.5 sex
ratio in 2011 did not flower in 2012. When the number of bisexual and male flowers sampled from all 25 trees
is put together, the sex ratio is 1:2 in 2011 and 1:3.6 in 2012. The flower sex ratios in both the years
indicated that the trees are strikingly male-biased at the population level
(Table 2).
The bisexual and male flowers are campanulate and morphologically alike
but the bisexual ones are slightly bulgy. In both the sexes, the calyx consisting of five petaloid sepals is
leathery, 12–14 mm long, linear-spathulate and free nearly to the
base. Its outer surface is scarlet
and inner surface dark-red; both the outside and inside is covered with simple
and stellate hairs. The corolla is completely absent. In bisexual flowers, the stamens are 10
and borne around the ovary which is raised by a 4mm
long creamy white androgynophore. In male flowers also, the stamens are 10 and borne on the top of a 8mm
long, slender creamy white androphore. In both the sexes, anthers are sessile, golden yellow and dithecous. In
bisexual flowers, the ovary is superior, hispid, 6mm long, consisting of five
free mono-locular carpels (Image 1g), each consisting of two ovules and
collectively containing 10 ovules on axile placentation. The style is single and tipped with
five-lobed pale yellow semi-wet stigma. In male flowers, the ovary is totally
absent.
The flowers of both sexes open early in the morning during
0600–0800 hr (Image 1c). In
male flowers, the anthers dehisce by longitudinal slits during mature bud stage
and the dehiscence can be confirmed by the presence of pollen on the inside of
the apical part of the calyx. In
bisexual flowers, the indehiscent anthers do not release pollen. The pollen grains in male flowers are
fertile, yellow, granular, spheroidal, smooth, tricolporate, 41.5µm in size and
powdery (Image 1f). The pollen output is 732±45.7 (Range 663–793) per
anther and 7,320 per flower in male flowers. In bisexual i, the pollen output is
949±41.14 (Range 8890–10120) per anther and 9,490 per flower; but this
pollen is sterile. The nectar secretion occurs during the mature bud stage and
it is 0.32 ± 0.04 µl (Range 0.2–0.5) per flower in both flower sexes. The sugars in the nectar include
fructose, glucose and sucrose with the first two as the most dominant. The
nectar contains both essential and non-essential amino acids. The essential
amino acids are arginine, histidine, lysine and threonine while the
non-essential amino acids are alanine, aspartic acid, cysteine, cystine,
glutamic acid, glysine, hydroxyproline, serine and tyrosine. The 5-lobed stigma in bisexual flowers
attains receptivity two hours after anthesis and remains so until the evening
of the 2nd day. The
flowers of both the sexes last for four days.
The flowers stand out visually in the absence of foliage during the
flowering period. The bisexual
flowers with indehiscent anthers are functionally female while male flowers
with dehiscent anthers presenting fertile pollen and lacking ovary structure
are functionally male. The
placement of anthers at the tip of the androphore in male flowers facilitates
easy dispersal of powdery pollen into the air. The ambient conditions at the study area
are characterized by high temperature (37–43 0C), low relative
humidity (20–40 %) and high winds (40–80 km/h) during the
daytime. Further, the area is
almost totally devoid of any vegetation. These conditions are quite conducive for the effective dispersal of
pollen by air.
The flowers were frequently foraged by the stingless bee, Trigona
iridipennis (Image 1h) and occasionally by a wasp (Rhynchium sp.)
(Image 1i) during the forenoon period. These insects had contact with the sex
organs while foraging. The bee
collected pollen and nectar from the male flowers and only nectar from the
bisexual flowers. It tended to stay
mostly on the same plant collecting the forage, especially pollen which is abundantly available due to the production of
numerous male flowers and hence its foraging visits were considered to be
effecting mostly geitonogamy. Further, the bee with its voracious pollen feeding activity was found to
be reducing the extent of fertile pollen availability for outcrossing. The wasp collected only nectar from both
the flower sexes. It tended to move
quickly from plant to plant in search of nectar and in this process was found
to be effecting outcrossing to some extent. The passerine birds such as Red-vented
Bulbul (Pycnonotus cafer - Pycnonotidae), Rufous-backed Shrike (Lanius
schach - Laniidae), Blue-tailed Bee-eater (Merops philippinus- Meropidae) and Brown-headed Stork-billed Kingfisher (Pelargopsis capensis- Muscicapidae) visited the plant for feeding on forage collecting Trigonairidipennis bees. They never probed
the flowers for nectar collection.
The hand-pollination experiments revealed that the flowers do not fruit
through geitonogamy but fruit through xenogamy only. In xenogamous pollination mode, the
fruit set rate is 70%. In open-pollination mode, the fruit set rate is 5% only
(Image 2a). In fertilized flowers,
the ovary gradually bulges and the carpels get separated forming follicles in
two weeks. The follicles take about
10 months to mature and fall to the ground. The fruits are initially greyish, turn rusty brown and then green and later
greyish-brown as they mature (Image 2b–h). The follicled fruits are thinly woody,
falcately ovate-reniform, winged, inflated and on their outside covered with
pubescent hair. A fruit produces
1–5 follicles. Likewise, a
follicle produces 1 or 2 seeds affixed at the base. Each mature and dry follicle is oblique
lanceolate, membranous initially, wrinkled when dry, 8.9±0.9 cm (Range
6.4–10.2) long and 4.1±0.3 cm (R 3.5–4.5 cm) wide; 1-seeded one is
0.764±0.120 g and 2-seeded one is 1.169 ± 0.162 g by weight. The seed weight is 0.558 ± 0.238 g (R
0.385–0.680). The
follicle-wise fruit set rate showed that 34% are 5-follicled, 29% 4-follicled,
20% 3-follicled, 13% 2-follicled and 4% 1-follicled (Table 3). The follicle-wise seed set rate is 92%
in 3-follicled fruits, 91% in 5-follicled, 87% in 4-follicled, 85% in
2-follicled and 62% in 1-follicled fruits (Table 4). The seeds are ovate-oblong, 13–14
cm long, dented, green initially and pale brown when
dry. The fruits with seeds inside
begin to fall to the ground from February and complete fruit shedding by the
end of March. The light weight fruits or follicles are dispersed effectively
by wind. The fallen follicles find
their way into rock openings/crevices and settle there. The rocky nature of the area greatly
reduces the dispersal distance of the fruits and in effect, the seeds remain
mostly within the plant area.
The follicle sheath gradually disintegrates and exposes seeds by the end
of May/early June (Image 2i,j). As
soon as the first monsoonal rains fall in June/July, the healthy and viable
seeds germinate and produce new plants (Image 3a,c-e). The ability of the seed to germinate is
dependent on the disintegration of the hard and thick seed coat. As the habitat of the plant is rocky
with little litter and moisture, the seedlings recorded in the area were very
few and even the growing ones were subjected to drought stress due to an
erratic rainfall. The soil analysis for available nitrogen (N), phosphorous (P)
and potassium (K) indicated that N is 220 kg/ha, P 13.95 kg/ha and K
17.86. These values show that these
nutrients are not present at optimal levels and hence there is deficiency in
essential nutrients in the soil.
Natural fire is an annual event in the habitat of the plant (Image 2k). The locals set fire intentionally and
unintentionally to the dry aerial plant material during March–June. Sometimes, the locals cook food in the
area and this practice also causes the dry plant material to burn. Further, the
locals intentionally light fires as a protest against the forest officials for
not allowing them to collect fuel wood. In consequence, the dry follicles together with seeds get burned (Image
2l) or charred to carbon. Human-caused fires accounted for the loss of most of the seed crop of
this plant and such a practice was found to be affecting the reproductive
success of the plant to a great extent. The partly-burned seeds due to burning
caused by fire germinated and produced seedlings (95%) (Image 3b) whereas
severely burned seeds did not germinate. Further, the plant also regenerates by sprouting from healthy stem
bases.
The seeds sown in polythene bags filled with fertile soil and watered
daily in the local forest nursery indicated that the seed germination rate is
0.42%. In such seeds, the
germination occurred after 18 weeks and the seedlings showed very slow
growth. A similar growth rate was
also noted in the natural area. The
study shows that there is no seed dormancy and germination is dependent on the
decomposition rate of the seed coat which in turn is
dependent on soil chemistry.
DISCUSSION
Hildegardia is a genus of tropical dry deciduous
woody tree species and exploited for its bark fiber, gum and wood by locals;
this over-exploitation has resulted in habitat clearance and loss. In effect,
all the species of this genus have been reported to be eithervulnerable, threatened, or endangered and endemic, based on their field status
(Masters 1868; Merill 1914; Arenes 1959; Wild 1961; Dorr & Barnett 1990;
Cheek & Leach 1991; Zaborsky 2009). Similarly, the conservation status of H. populifolia has also
been assessed differently by different workers eitheras critically endangered, endemic or vulnerable (Sarcar & Sarcar 2002;
Ahmedullah 1990; Walter & Gillet 1998; Reddy et al. 2001; Jadhav et al.
2001; Reddy et al. 2003; Rao et al. 2011). The present study found that it is a critically endangered species due
to over-exploitation for its bark and wood (Image 1b), and also due to natural
and human-caused fires, especially when follicles together with seeds fall to
the ground. The locals involved in
collecting bark from live trees are paid Rs. 80/- for one
meter length of bark. The trees which are devoid of bark subsequently wilt and
die. Rajulu et al. (2005) and Li et
al. (2004) reported that the fiber obtained from bark and stem is economically
valuable due to possession of good mechanical properties at low density. These properties make its fiber fit as
reinforcement in the preparation of natural fiber reinforced polymer composites which are referred to as “green composites”. The bark of the stem and leaves are also
used as an antidote to dog bites and to curing malaria in the traditional
medical practice of Tamil Nadu and Andhra Pradesh (Reddy et al. 2001;
Varaprasad et al. 2009). Lavanya et
al. (2012) reported that different parts of the tree are used in various ayurvedic
commercial preparations. Therefore,
the different uses of H. populifolia locally and commercially have
contributed to its current status.
In Hildegardia, the african species
occur in wood or bushland forests (Masters 1868) while the malagasy species in
dry or humid/wet forests. H. ankaranensis and H.
erythrosiphon grow on calcareous soils (Arenes 1959; Zaborsky 2009). H. cubensisgrows on rocky limestone soils and is restricted to low land semi-deciduous
forests (Dorr & Barnett 1990). In India, H. populifolia grows on the steep, rocky, dry and poor
stony red soils. Therefore, Hildegardiagenus appears to have adapted to grow in deciduous forests with calcareous or
rocky limestone or rocky red soils.
In Hildegardia, H. cubensis flowers with foliage during
the dry season (Dorr & Barnett 1990) while H. barteri and H.
australiensis flower during the dry season prior to leaf flushing (Masters
1868; Cheek & Leach 1991). In
the present study, H. populifolia is found to flower during the dry
season prior to leaf flushing. The
preliminary reports based on herbarium specimens of Hildegardia species
by different workers provide speculative information on the sexual status of
flowers. Dorr & Barnett (1990)
considered H. gillettii and H. cubensis as hermaphroditic
species. Wild (1961) noted that H.
migeodii produces male and female flowers but he has not mentioned whether
the plant is dioecious or monoecious. Cheek & Leach (1991) considered H. australiensis as a
dioecious species. H. populifolia has been reported to be polygamous by Rao
& Pullaiah (2007) and andro-, gyno- or trimonoecious by Sarcar & Sarcar
(2002). The present study revealed that in H. populifolia, all
phenological events—fruit dispersal, leaf shedding, flowering, leaf
flushing and fruiting occur, one after the other during the dry season. The individuals of this species are
morphologically andromonoecious as they possess both
male and bisexual flowers. However,
the morphologically bisexual flowers have no male function as a result of
indehiscent anthers and non-functional pollen grains. Thus, the morphologically
andromonoecious system is functionally a monoecious system, with the putative
bisexual flowers functioning only as female flowers. This kind of monoecism in H.
populifolia adds material evidence to the proposal of Bawa & Beach
(1981) that evolution of monoecism represents the continuation of the trend
seen in andromonoecious species towards the specialization of flowers into
pollen donors and pollen recipients which due in part to sexual selection and
in part to the mechanics of pollination and monoecism can arise in one step
from andromonoecism. It can so
arise by the sterilization or abortion of the stamens in hermaphrodite
flowers. Thus, the monoecious
sexual condition in H. populifolia is the result of male sterility in
hermaphrodite flowers. Sterculia
foetida also exhibits such a sexual system (Atluri et al. 2004).
Monoecy is an important step in the promotion of outcrossing (Frankel
& Galun 1977). But, the
occurrence of segregated male and female functions in separate flowers on the
same plant may still provide opportunities for self-fertilization through geitonogamy.
In some monoecious species such as Cnidoscolus texanus (Perkins et al.,
1975), C. urens (Bawa et al., 1982), Cupania guatemalensis (Bawa,
1977), Euphorbia antiquorum and E. tortilis (Reddi et al., 1995),
complete outcrossing is facilitated by synchronized dichogamy which is referred
to as temporal dioecism (Cruden 1988). Therefore, the effectiveness of monoecism as an outcrossing mechanism
may depend on the extent to which male and female reproductive functions are
separated in time rather than in space (Bawa & Beach 1981). In many monoecious species, outcrossing
is enforced by self-incompatibility (Hagman 1975; Atluri et al. 2004). H. populifoliabeing a functionally monoecious species has not adapted to sequential
maturation of male and functionally female type bisexual flowers and is an obligate
outcrosser as established by manual pollination experiments in which fruit set
occurs only in xenogamous pollinations. The additional mechanism to promote outcrossing in this species is
indehiscent anthers with sterile pollen grains in bisexual flowers. The male
sterility and blocking of such pollen grains from bisexual flowers into the air
may be thought to have evolved to reduce pollen-pistil interference which
otherwise can reduce seed production through ‘stigma clogging’ with sterile
pollen (Bertin & Newman 1993; Dinnetz 1997). However, a protrandrous condition and
powdery pollen driven by wind could contribute to stigma clogging with
self-fertile pollen to some extent. The fruit in H. populifolia is big and thus highly expensive to
mature in terms of resources. Perhaps, the resources saved by the abortion of the male function in
bisexual flowers are invested in fruit development.
In H. populifolia, the proportions of male and male-sterile
bisexual flowers produced in two successive years are not constant but they are
strikingly male-biased and also a few individual trees produce only male
flowers suggesting that the plant is struggling to increase cross-pollination
rate by producing more male flowers. Another reason for such a male-biased ratio is that the pollen output at
flower level is not commensurate with the requirement in this obligate
outcrosser (Cruden 1977). The
production of large thinly woody fruit with hard seeds is highly expensive for H.
populifolia. Fruit development takes place for over 10 months and naturally
there should be much greater allocation of resources to growing fruits. Probably, the plant reserves the
resources by reducing female flower production and invests the resources thus
saved to produce healthy fruits with viable seeds.
Dorr & Barnett (1990) considered the africanand malagasy species of Hildegardia as a natural group due to possession
of shortly divided tubular calyx at the apex and the occurrence of flowering
during the leafless state. On the
contrary, Kubitzki & Bayer (2003) noted that in H. australiensis,
the calyx is deeply divided and the sepals are reflexed. In H. populifolia also, the calyx
is deeply divided to the base and the sepals are reflexed. In Hildegardia genus, the calyx
appears to have a key role as an attractant in the pollination process since
the corolla is completely lacking. Hildegardiaspecies with tubular calyx appear to have adapted for pollination by
birds. Roma (2002) mentioned that
the malagasy H. erythrosiphon is nectariferous
and the nectar volume varies over the day, peaking around midday and also
varies between individual trees. He
noted that the sunbirds Nectarinia souimanga and N. notata visit
the flowers mostly during the morning period for nectar and effect pollination.
Malalatiana (2002) observed that the Lesser Vasa parrot, Coracopsis nigrais a flower predator as well as pollinator of H. erythrosiphon. Steentoft (1988) stated that in West
Africa, Sterculiaceous flowers do not produce nectar and in this context he mentioned
that the african species, Hildegardia barteriis pollinated by pollen collecting bees. Sarah (2011) mentioned that H. australiensis is
seemingly pollinated by insects. In H. populifolia, the deeply divided calyx holds the hexose-rich
nectar at its base but the nectar is secreted in minute quantity
which does not meet the requirement of pollinators, especially
birds. The nectar also provides
certain essential and non-essential amino acids. The pollen is produced in copious
quantities at the plant level and it is adequate enough for achieving
outcrossing through pollen vectors. Since the plant is an obligate outcrosser because of male sterility in
morphologically hermaphrodite flowers, and because of incompatibility with
geitonogamous pollen, the involvement of pollinators is essential. The nectariferous flowers of H.
populifolia are indicative of adaptation to biotic agents for
pollination. In the habitat of this
species, bees, wasps and birds occur but only Trigona bees and Rhynchiumwasps forage for the flowers; the former both nectar and pollen frequently
while the latter only nectar occasionally but their activity is confined to the
forenoon period only due to high temperatures during the day time. The voracious pollen feeding activity of
the bee is disadvantageous for the plant since it reduces the availability of
fertile pollen for cross-pollination and also its tendency to stay mostly on
the same plant for forage collection does not effect or promote
cross-pollination. On the contrary,
the wasp being a nectar forager contributes to cross-pollination due to its plant to plant flights in quest of nectar but it is not
important as pollinator due to its occasional foraging visits and confinement
of its foraging activity to the forenoon period. The birds, Pycnonotus cafer, Lanius
schach, Merops philippinus and Brown-headed Pelargopsis capensisin the area use foraging collecting Trigona bees on H. populifoliaas a protein source but do not visit the flowers for nectar. Sunbirds are also sighted in the area
but they never visited the flowers of H. populifolia. Therefore, the plant is not adapted for
pollination by biotic agents and the nectar secretion appears to be a residual
character but nonetheless, it is able to achieve cross-pollination to some
extent by the wasp in the study area.
In H. populifolia, the pollen grain size is a characteristic of
typical aerodynamic particle, which permits effective wind transport and
deposition on the stigma through impaction (Gregory 1973; Reddi 1976), and the
characters such as exine separate by lumina may reduce terminal velocity and
contribute to the increased dispersal range of pollen (Niklas 1985). Additional adaptations for anemophily
are high pollen production, synchronous anthesis and anther dehiscence at plant
level and the presence of anthers on the top of the androphore of male
flowers. High temperature and high
wind speeds in the study area are quite conducive to the easy dispersal of
powdery pollen. The area
experiences moderate to turbulent atmospheric conditions especially during the
forenoon period and this favours the efficient transport of entrained pollen
(Mason 1979). However, the wind
does not always blow at ideal speeds throughout the day and hence anemophily is
not always effective in promoting cross-pollination in this species. Therefore, H. populifoliahas its own disadvantages with anemophily as a mode of pollination and it
reflects on fruit set rate. The low
natural fruit set rate evidenced in this study could be attributable to
ineffective anemophily, fertile pollen collection by Trigona bees and
the status of the nutrient environment of the soil. However, it is
compensated by the increased number of follicles and more seed output per
flower.
In H. populifolia, the wing-like membranous follicles with one or
two seeds being very light in weight are adapted for dissemination by wind and
it is referred to as anemochory (Ashton 1982). The dry follicles disseminate by the
prevailing wind speeds. There is no
possibility for the fallen follicles to disperse further on the ground due to
the rocky terrain; they finally settle within the vicinity of parental plants.
It is effective only under ideal wind speeds and even then the rocky terrain
limits the dispersal distance of follicles (Maury-Lechon & Curtet
1998). The membranous follicle
sheath disintegrates by the end of the dry season exposing the seeds to the
soil environment. As the seed coat
is very hard, it takes time for the emergence of radical and subsequent steps
leading to seedling growth. The
disintegration of the seed coat and subsequent germination depends on the soil
chemical and nutrient environment; the rocky habitat of the plant does not
favour regeneration from seeds. The
seeds located in the litter rich areas of rock crevices/openings germinate and
produce seedlings immediately during the rainy season and hence, they are
non-dormant. Lavanya et al. (2012)
stated that the seeds of H. populifolia are viable for a few months
suggesting that they may germinate in the next rainy season. These authors also noted that the seed
mode is the main propagation method. In natural habitats, seed germination and seedling survival rate play a
critical role and indicate the future status of the plant. H. populifolia is a prolific seed producer but most of the
seeds fail to germinate while others are subjected to regular natural and
human-caused fires.
In habitats experiencing regular fires, plants and their seeds are
continually exposed to different temperature ranges due to variable fuel loads,
differences in relative moisture and wind intensity (Martinez-Sanchez et al.
1995). Plants in such habitats may
evolve hard seed coats as a means of protection against fire (Arianoutsou &
Margaris 1981). H. populifolia appears to have evolved a hard seed coat for
protection against regular seasonal fires. Fire influences seed germination in a variety of ways. It reduces inhibitory substances in soil
and litter, provides chemical stimulation from charred wood, fractures hard
seed coats, stimulates seed embryos, causes desiccation of seed coats and
enhances nutrient supply due to nutrient mobilization from burnt plant biomass
and soil microbes (Keeley et al. 1985; Gonzalez-Rabanal & Casal 1995;
Jensen et al. 2001). Seeds of H.
populifolia are not buried in the soil but stored on the soil or rocky
surface; fires here are mostly lethal for seeds especially when fuel load is
high. Partly burned seeds germinate
and produce seedlings but their continuous growth is dependent on water and
nutrient status of the soil.
Anuradha & Pullaiah (2004) reported that in this species, the
cotyledons and embryos may get damaged during maturation stage due to fungus
attack and in effect the number of viable seeds gets drastically reduced. These authors based on in vitro seed
germination studies reported that there is a dramatic increase in the
percentage of seed germination in seeds collected one month before the
harvesting time because, at this stage only 10% of the seeds exhibited damaged
cotyledons and showed 75–80 % precocious germination, but these
germinated seeds failed to grow beyond the two-leaf stage for which the reason
attributed is the physiological immaturity of the embryo. Further, they reported that the seeds
scarified with concentrated sulphuric acid showed 14% germination and 20% of
them subsequently failed to produce seedlings. This is considered to be one of the
reasons for the poor survival rate of seedlings in natural conditions leading
to its reduced population size. Saradha & Paulsamy (2012) reported that clonal propagation through
mature stem cuttings is an effective propagation method as the seed germination
rate is not at an appreciable level in H. populifolia. But, Lavanya et al. (2012) stated that
the cutting method is not efficient under varied climatic conditions to
repopulate this species in its pristine habitat. Seeds of H. populifolia were not
found with fungal attacks in the present study and hence the study does not
support the findings reported by Anuradha & Pullaiah (2004). The plants also sprout from healthy stem
bases. This study also adds that
the NPK levels in the soil collected from the areas of this species indicate
that these nutrients are not present in optimal levels. Nitrogen deficiency would affect the
growth of leaves, phosphorous the root and shoot growth while potassium the
flowering and fruiting. Erratic
rainfall and water deficit in the soil would also affect the growth rate of seedlings
and the slow growth of seedlings is a characteristic of H. populifoliain its natural habitat. In vitro
seed germination experiments also substantiate this observation. Therefore, seed germination and seedling
growth rates in H. populifolia are regulated by several intrinsic and
extrinsic factors in addition to natural and anthropogenic fires, habitat loss
and economic uses of the plant. All
other Hildegardia species also appear to be experiencing the same
regeneration problems since they are all deciduous, occur on rocky habitats,
and have small populations or a few individuals in their natural habitats. The study suggests that seedlings of H.
populifolia should be raised in nurseries and then transferred to natural
habitats in order to repopulate the species. Further, appropriate measures are
required for effective conservation and management of this endangered species
from extinction.
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