Journal of Threatened
Taxa | www.threatenedtaxa.org | 26 February 2026 | 18(2): 28287–28295
ISSN 0974-7907 (Online) | ISSN 0974-7893 (Print)
https://doi.org/10.11609/jott.9964.18.2.28287-28295
#9964 | Received 28 May 2025 | Final received 07 January 2026 | Finally
accepted 29 January 2026
Flower bud growth, mortality
rate, and population structure of Sapria himalayana Griffith f. albovinosa
Banziger & Hansen (Rafflesiaceae)
in a subtropical forest, northeastern India
K. Shamran Maring
1 & Athokpam Pinokiyo
2
1,2 Department of Botany, Dhanamanjuri University, Imphal,
Manipur 795001, India.
1 puikans1996@gmail.com
(corresponding author), 2 pinkiathokpam@gmail.com
Editor: Inocencio
Buot Jr., University of the Philippines Los Banos, Laguna, Philippines. Date of publication: 26 February 2026 (online & print)
Citation: Maring, K.S. & A. Pinokiyo (2026). Flower bud
growth, mortality rate, and population structure of Sapria
himalayana Griffith f. albovinosa
Banziger & Hansen (Rafflesiaceae)
in a subtropical forest, northeastern India. Journal of Threatened Taxa 18(2): 28287–28295. https://doi.org/10.11609/jott.9964.18.2.28287-28295
Copyright: © Maring & Pinokiyo
2026. Creative Commons Attribution 4.0 International
License. JoTT allows unrestricted use, reproduction,
and distribution of this article in any medium by providing adequate credit to
the author(s) and the source of publication.
Funding: None.
Competing interests: The authors declare no competing interests.
Author details: K.
Shamran Maring is currently pursuing PhD degree at Dhanamanjuri
University, Manipur, working on the
angiosperm flora of Tengnoupal
District, Manipur. Her research focuses on plant taxonomy, primarily concentrating on floristic, ecological studies, and biodiversity conservation. Prof. Athokpam Pinokiyo is currently working as the Head, Department of Botany, Dhanamanjuri University, Imphal,
Manipur, and she has got a teaching experience for about 15 years.
Her keen work is on taxonomy,
diversity, ecology, and conservation of lichens (including Angiosperms). She has got a research experience of more
than 24 years in the field of taxonomy (angiosperms and lichens).
Author contributions:
KSM: conceptualised
the study design, carried out the field surveys, data collection, data
handling, data curation, photography,
visualisation, statistical
analysis, writing, review and
editing of the manuscript. AP: supervised
the research work and revision of the manuscript. Both authors read and agreed
to the final
manuscript.
Ethics and field
compliance statement: The field research was conducted with prior permission from the relevant forest and community authorities. Prior informed
consent was obtained from the Machi Village
Authority, a Maring
community, inhabiting the study area, with approval letter no. MCI-VA/85/2-2025 dated
03 October 2025. All field activities were conducted in accordance with the local customs,
cultural values, community protocols, traditional knowledge and the ethical
standards for research in the Machi Village
community forest. No endangered
or protected species were harmed or removed from their natural
habitats during the course of this research. All observations and data collection were conducted in a non-destructive and minimally invasive manner consistent with best ecological research practices.
Acknowledgements: The authors
are grateful to the Department of Botany, Dhanamanjuri University, Imphal, Manipur, for helpful advice and permission given for this
study. K SHAMRAN MARING express
gratitude to the National Fellowship for Higher Education for Schedule Tribe Students (NFST), bearing Award
No. 202223-NFST-MAN-02118, Ministry of Tribal Affairs, Government of India, for the financial assistance provided.
Also, thanks are due to the
local people of Machi Village who
gave a helpful hand in the
field survey of the present study.
Abstract: Sapria himalayana
Griff. f. albovinosa Banziger
& Hansen (Rafflesiaceae) is rare and endemic to
northeastern Thailand, Vietnam, and Manipur, with a short flowering season
ranging from late October to late November, due to which its detailed phenology
is poorly understood. To protect this valuable taxon from extinction threats,
monitoring the growth of flower buds is crucial. The objectives of this study
were to analyse the growth of flower buds at various
developmental stages, the mortality rate, and the population structure of Sapria himalayana
f. albovinosa. The buds were monitored,
vertically photographed, and measurements of the plant buds and flowers were
recorded for every observation. The present study resulted in the flower bud
growth having six different developmental stages, namely the copule, copule-bract transition,
bract, bract-perigone transition (BPT), perigone, and anthesis stage, with a
diameter range of 0.3–2.3 cm, 2.4–4.0 cm, 4.1–5.5 cm, 5.6–6.1 cm, 6.2–8.1 cm,
and 16–20 cm, respectively. The population was dominated by the copule stage in the initial observation, while it was
dominated by the perigone and anthesis stages in the final observation, which
indicated that the optimal flowering season was from late October to late
November. A total of 58 flower buds were recorded, out of which 24.13% of
flower buds were dead without reaching maturity due to fungal infections and
were injured due to anthropogenic interventions. Hence, the information on the
growth of buds, flower development stages and their mortality rate is vital for taxonomic studies, field monitoring, and
conservation purposes.
Keywords: Anthesis, anthropogenic, bract, conservation, copule, crucial, endemic, extinction, perigone, rare.
INTRODUCTION
Sapria himalayana Griffith f. albovinosa Banziger
& Hansen (Banziger et al. 2000), a new form of
the Hermit’s Spittoon, is rare and endemic to the northeastern
Thailand and Vietnam Lang Biang plateau, but a new
distribution is recorded from India at the evergreen sub-tropical forest of Machi Village, Tengnoupal
District, Manipur (Maring & Pinokiyo
2024). It is differentiated from the typical form in having white dotted warts
more or less evenly distributed on the entire wine-red perigone lobe instead of
having sulphur-yellow dotted warts on blood-red perigone lobes (Banziger et al. 2000). All members of the genus Sapria are distinctive and narrowly
host-specific plants belonging to the family Rafflesiaceae.
The typical form of Sapria himalayana is rare throughout its range from northeastern India, southwestern China, Thailand, Myanmar,
to Vietnam. Being a member of the holoparasitic plant
family, Rafflesiaceae, and growing on various species
of Tetrastigma (Vitaceae),
it is a little-understood species (Wu & Raven 2003; Nikolov
& Davis 2017; Tran et al. 2018; Tanaka et al. 2019; Syiemiong
et al. 2022). In India, the typical species of Sapria
was first reported from the tropical wet evergreen forests of the Mishmi Hills
of Lohit District by William Griffith in 1847 and
later from the Aka Hills in Kameng District by Norman
Loftus Bor in 1938 (Andreas & Jis
2014; Borah & Ghosh 2018). This species is the largest root parasitic
angiosperm, having a host-specific relationship with the plant genus Tetrastigma of the Vitaceae
family.
Tetrastigma bracteolatum (Wallich) Planchon and T. serrulatum (Roxb.) Planchon have been reported as the host plant of Sapria in Namdapha Park
(Arunachalam et al. 2004; Borah & Ghosh 2018). The members of the Rafflesiaceae have a reduced vegetative body among all
angiosperms (Nikolov et al. 2014). Sapria is well distinguished from the other two
genera of Rafflesiaceae, Rafflesia
R.Br. ex Thomson and Rhizanthes Dumort by the presence of 10 perianth lobes in two whorls
(Meijer 1997; Nikolov & Davis 2017; Tanaka et al.
2019).
At present, the genus Sapria
consists of four species, viz., S. himalayana
Griffith. which has the widest distribution range among them (Wu & Raven
2003; Bendiksby et al. 2010; Ahmad et al. 2020; Syiemiong et al. 2022), with one form, S. himalayana Griffith f. albovinosa
Banziger & Hansen (Banziger
et al. 2000), endemic to northeastern Thailand, S.
poilanei Gagnep,
endemic to Cambodia (Gagnepian 1941), S. ram H
Bänziger & B Hansen, endemic to Thailand (Banziger & Hansen 1997), and S. myanmerensis
Nob. Tanaka, Nagam, Tagane
& M.M. Aung, endemic to Myanmar (Tanaka et al. 2019). Sapria
himalayana has lost about 44% of conserved genes
in Eurosids that are enriched for functions like
photosynthesis, plastid organisation, defence, stress response, and nutrient
assimilation. It has also gained some genes from its hosts through horizontal
gene transfer, showing extreme genome remodelling under parasitism (Cai et al.
2021).
In Rafflesiaceae, previous
studies on the bud development, growth rate, mortality, flower phenology, life
history and autecology have been conducted for several species of Rafflesia, where only a few were found for Sapria and none for Rhizanthes.
Hidayati et al. (2006) and Nais
(2001) studied Rafflesia patma, R. keithii, and
R. pricei for their similar rapid later-stage
bud growth and low bloom success. Sofiyanti et al.
(2007) reconstructed the life cycle of Rafflesia
hasseltii, which was redrawn from Nais (2001). Galindon et al.
(2016) and Tolod et al. (2020) reported a new species
of Rafflesia, namely R. consueloae
and studied its first flower and fruit development and life history. Susatya (2020) reported the growth of the flower bud, life
history and population structure of R. arnoldii.
Recent work by Rambey et al. (2023) reported on the
population and ecology of the endangered R. meijeri
in Indonesia. Also, Wee et al. (2024) reported the bud development, flower
phenology and life history of R. cantleyi. The
earlier works on ecology, status, and conservation of Sapria
himalayana Griffith. was done by Elliot (1992).
Also, Arunachalam et al. (2004) reported on the population and conservation of S.
himalayana Griffith. in Namdapha
National Park, Arunachal Pradesh, India.
Currently, there is little information regarding the
studies on the flower bud growth of S. himalayana
Griffith f. albovinosa Banziger & Hansen (2000), even though it is essential
for conservation purposes. The main objectives of this study were to observe
the flower bud growth at different developmental stages of S. himalayana f. albovinosa
and the change of its population structure with respect to the growth of
the flower bud.
MATERIALS AND
METHODS
Study area
The study was conducted in the subtropical evergreen
rainforest of Machi Village, situated under the
jurisdiction of Tengnoupal District, Manipur, northeastern India. The site is located at a latitude of
24.504O N and a longitude of 94.143O E with an elevation of about 1,477 m. Machi Village is about 62 km away from the capital city, Imphal, of the state of Manipur. The motorable road to the
village is in poor condition, with several potholes and uneven surfaces and is
also prone to landslides during the monsoon season, which could completely
block the way. The present research site is located in a remote area of the
village, also there is no motorable road to the site as shown in Image 1. The
village is situated in the Indo-Myanmar biodiversity hotspot, which is a region
rich in floral and faunal diversity, and harbours numerous interesting and
endangered species. The vicinity of the village is inhabited by the Maring Tribe, one of the indigenous tribes of Manipur,
which has rich ethnic cultures and traditions. The people of the village
practice jhumming cultivation as their main source of
income. The entire region of the village crossing the International
Indo-Myanmar Road harbours the tropical rainforest to sub-tropical evergreen,
and deciduous forests. It is also an ideal habitat for various rare and
endangered carnivores and birds.
Field data
collection
The present study was carried out from July to November
2024 at the study site. Sapria himalayana f. albovinosa were
found at the community evergreen forest of Machi
Village, Manipur, and were monitored, and the measurements of the plant buds
and flowers were recorded for every observation at the study site. The
observation was made at two-week interval for five months. The flower buds of Sapria himalayana
f. albovinosa are found only on the roots of
the host plant, Tetrastigma, unlike many
species of Rafflesia found on both roots and
climbing stems of the hosts. They are covered by the litter of the forest
floors, making it difficult to observe at first sight. All the buds were
discovered through thorough searching, scrutinising, and by removing forest
litter in search of other buds whenever a bud was first detected at the study
site. As such, this may prove to be an inevitable study limitation and may underestimate
the actual population. While there were cases in which some undetected
below-ground buds escaped the initial observation, when they grew bigger and
surfaced above ground later, they were eventually added to the monitoring
system (Wee et al. 2024). The diameters of Sapria
buds and flowers were measured by the widest diameter length (Elliot 1992).
The observation of this study was limited to the visible structure of bud and
flower developmental stages of Sapria himalayana f. albovinosa
(Susatya 2020). Each bud and flower was
vertically photographed, and its diameter was measured at every observation (Nais 2001; Kamal et al. 2022). The bud development was then
categorized into different size classes for further analysis, following the
methods by Nais (2001), Susatya
(2020), and Tolod et al. (2020). The dead buds of all
bud diameter sizes were recorded for every observation. Then the mortality rate
of the Sapria buds was calculated by
the formula given below (Nowak et al. 2004).
Total number of dead buds
Mortality rate =
–––––––––––––––––––––––––x 100
Total number of buds recorded
The abiotic parameters, such as air temperature, wind
speed, humidity, soil temperature, soil moisture, soil pH, and light intensity,
at the present study site were recorded using a thermometer and a 4-in-1 soil
tester.
Statistical
analysis
A non-linear regression analysis was conducted to obtain
the exponential growth model equation and coefficient of determination (R2)
for the observed bud diameters to demonstrate a J-shaped bud growth curve.
Also, correlation analysis was performed to examine the relationships between
environmental factors such as ambient temperature, humidity, wind speed, soil
pH, soil temperature, light intensity, and mortality of the buds for a
five-month observation. A chi-square test was conducted to assess the bud stage
distribution shifts across time of the observation. All statistical analyses
were performed using SPSS version 26.
RESULTS AND
DISCUSSIONS
Flower bud
growth of Sapria himalayana
f. albovinosa
The present study showed that the life cycle of Sapria himalayana
f. albovinosa is complex, as most
members of Rafflesiaceae have two parts – the
invisible and visible parts (Hidayati et al. 2006; Nais 2001; Kamal et al. 2022). The invisible part includes
the inoculation and germination of Sapria’s
seed occurring inside its host plant roots, whereas the visible part is the
emergence of the flower bud, mature bud, and anthesis. The visible part
consists of several flower buds developing and is also the only plant structure
that is exposed to external environmental factors. Therefore, flower buds at
different sizes exhibited different growth rates and developmental stages. The
observation limited to only the visible parts of the life cycle resulted in six
different development stages of the flower, which were then categorized into
the copule, copule-bract
transition (CBT), bract, bract-perigone transition (BPT), perigone and anthesis
stages (Image 2). Copule, bract and perigone stages
were defined by 80–100% of the images of vertically photographed bud
respectively covered by copule, bract, and perigone
structures. A bud was categorized into CBT, if it grew between copule and bract stages, and the coverage of the images of
the photographed bud by the bract reached 40% to 80%. Meanwhile, a bud was
grouped into BPT, if it grew between the bract and the perigone stages, with
coverage of the images of the photographed bud by the perigone reaching 40% to
80%. Any bud with less than 40% of the coverage by either bract or perigone was
also categorised into either copule or bract stages (Susatya 2020). The anthesis stage occurred once during the
observation at the bud’s diameter range of 16–20 cm. The observation resulted
that the diameter range of copule, CBT, bract, BPT,
and perigone stages respectively were 0.3–2.3 cm, 2.4–4.0 cm, 4.1–5.5 cm,
5.6–6.1 cm, and 6.2–8.1 cm (Table 1). The growth development of Sapria’s bud was not in a discrete pattern, where
one stage was replaced completely by the next stage. The same growth
development was also observed in the typical species of Sapria
(Elliot 1992). It consisted of a series of overlapping development stages,
where before one stage was complete, the following stage had already developed.
It was a basic reason why transition stages were introduced in this research.
The first visible structure was copule, which was
basically the bark of the host plant root covering the actual Sapria structure. The first visible structure of S.
himalayana f. albovinosa
at Machi had the diameter range of 0.3–2.3 cm (Table.
1). The start of the development of the inner structures of Sapria
was still unknown though it is needed to be studied whether all the inner
structures had been developed in the copule stage or
not. The inner structures in the species of Rafflesia
had already developed in the copule stage while
observing its dead bud of 6 cm diameter (Susatya
2020). As the bud grew, the upper copule started to
crack to allow the first true structure of the Sapria
or bract to be visible. Bract was originally pastel pink and white colour, but
eventually turned black as it grew older. The bract was gradually replaced by a
pale pink perigone stage consisting of buds with a diameter range of 6.2–8.1 cm
(Image 2).The bract consisted of two series of five imbricate and whorled
scales (Elliot 1992). The pinkish perigone lobes of the bud indicated anthesis
to occur within 3–4 days. The field observation showed that when the upper
layer of the perigone lobe was slightly raised, then the anthesis would take
place within 2–3 days, and lasted between 4–5 days. All flower structures
decomposed within a month after flowering. The column was the only female
structure that did not decompose and further developed into mature fruit
(Elliot 1992). As the flowers opened, they emitted an odour similar to that of
rotting meat, which lasted for 2–3 days. Within 3–4 days after opening, flowers
started to darken and eventually turned black. As the flowers turned black, all
the plant structures shrank. The base of male flowers and their attachment to
the host shriveled rapidly and eventually detached
from their host roots. In female flowers, the perigone tube and lobes,
diaphragm and disk shriveled as in males, but the
column, ovary and surrounding tissues at the base of the column remained alive
(Elliot 1992). The base of the perigone tube swelled and remained white
externally for about two months after flower opening. This structure
constituted the fruit of S. himalayana
f. albovinosa, though a detailed study on the
fruits and seeds dispersal is required. The growth rate of flower buds at
earlier stages was found to be very slow, while the buds at older stages showed
higher growth rates. Therefore, the growth curve of the flower bud showed a
typical J-shaped growth curve or an exponential growth curve (Figure 1).
The non-linear regression equation y = 1.2123 e0.0149x
and R2 = 0.9722 was obtained by plotting the bud mean diameter
across the number of observed days. The bud diameter grows by about 1.49% of
its current size in every additional day. This means the bud diameter doubles
roughly every 46–47 days under the observed growth pattern. Therefore, on the
initial day of observation, the bud starts at about 1.5 cm in diameter, then,
by about 150 days, they grow to above 13 cm in diameter, matching the measured
data points (Figure 1).
The present study showed that S. himalayana
Griffith f. albovinosa found at Machi comparatively has crateriform
and bilobed or multilobed ramenta apices in male and
female flowers, respectively, while the Vietnamese taxon is also bilobed or
multilobed (female) or crateriform (male) (Maring & Pinokiyo 2024). The
diameter of the crest disk and aperture of the diaphragm for the Machi individuals are 3.4–3.5 cm and 1.9–2.0 cm,
respectively. The S. himalayana Griffith f. albovinosa from Machi
Village has a comparatively larger floral span (13–20 cm diameter) than the S.
himalayana Griffith f. albovinosa
(11–16 cm diameter) (Banziger et al. 2000), S. myanmerensis (10 cm) (Tanaka et al. 2019), S. poilanei (6.5–12 cm), and S. ram (5.5–11 cm) (Banziger & Hansen 1997).
Population
structure of Sapria himalayana
f. albovinosa
The population status of S. himalayana
f. albovinosa is very small when
compared to the other higher plants. Also, the population of this endemic
infraspecific taxon is much smaller than that of the typical species of Sapria (Elliot 1992). The initial observation
in the month of July showed that the total population is 100% dominated by the
copula stage. At the second observation in August, the population structure was
75% copule and 25% copule
bract transition (CBT) Stage (Figure 2). Meanwhile, buds at CBT were fewer due
to the changes in the flower bud development stage. Larger stages, such as
bract and BPT, were observed respectively with 18.96% and 10.34% in September
(Figure 3). Within three months, the population structure was significantly
changed due to the mortality, new recruitment, and growth of buds from one
stage to the next growth development stages. The population structure of this
period was shifted toward bract and BPT. During the next observation, in the
month of October, the population structure interestingly exhibited all six bud
stages, where the bract stage dominated it with 36.20% (Figure 4). The pattern
of population structure appeared to be opposite to the initial one, where the
perigone and anthesis stages were exhibited with 18.96% and 13.79%,
respectively. In the last month’s observations, the population structure was
dominated by full bloom/anthesis and after-blooming flowers. The flower buds
were found at their full bloom stage in October to December, but the optimal
flowering season is from late October to late November. During the initial
period of research, the number of flower buds increased gradually due to the
new recruitment of the buds, while the population size decreased in the later
months of observation. This condition could be due to insufficient nutrients
for the population of the flower bud to maintain its viability and complete its
life cycle (Figure 5). A chi-square test revealed a significant shift in bud
stage distribution across time (X2 = 202.997, df
= 20, p = 2.87 x 10-32), this indicates that the proportion of buds
at different developmental stages varied markedly with time and did not remain
constant over time.
In the five-month observation, a total of 58 flower buds
were recorded, out of which 28 buds were recruits and 14 buds died without reaching
maturity. The causes of the bud mortality were fungal infections and injuries
from anthropogenic interventions, where the injured parts of flower buds were
immediately followed by a rotting process that led to the bud mortality. All
losses occurred at buds belonging to the copule, CBT,
bract, and BPT with copule-bract transition (CBT)
stage showing the highest mortality rate of 42.85% (Figure 6). The population
structure of S. himalayana f. albovinosa showed a mortality rate of 24.13%,
which is much lower when compared to the mortality rate 40% of the typical
species (Elliot 1992). Although the mortality rate is much lower than that of
the typical species of Sapria, the total
population status of this endemic taxon is very small, indicating an alarming
signal concerning the future population of S. himalayana
f. albovinosa.
Abiotic factors
of Sapria himalayana
f. albovinosa habitat
The ambient temperature of the study site was found to
decrease from 23°C (July) to 19°C (November),which is due to the onset of the
winter season. The air humidity ranges 67–86 %, and the light intensity was
found to be very low, ranging 90–100 lux, probably be caused by the dense
canopy cover (Table 2). The high air humidity and low light intensity play a
vital role in the existence of S. himalayana
f. albovinosa because the plant preferably
grows on the understory of forest floors. Also, in the present study, the
flower buds showed higher mortality rates as the light intensity increased. There
is a moderately strong positive correlation between light intensity and bud
mortality, with a correlation value (r) = 0.6123, indicating that higher
mortality rates are generally associated with higher light intensity. Whereas,
the soil pH showed a moderate negative correlation (r = -0.326) with the bud
mortality. In Table 2, the soil pH ranges 5.5–6.5, and it is classified as
acidic, while the soil temperature ranges 18–24 °C. The soil moisture showed
very wet conditions in July, which could be due to the monsoon season, while
the soil was dry in November, which could be due to the winter season.
Therefore, the abiotic parameters of the environment play an important role in
the growth of flower buds as well as in the population dynamics of this rare endemic
taxon.
CONCLUSION
The flower bud growth of Sapria
himalayana f. albovinosa
has six developmental stages consisting of the copule,
CBT, bract, BPT, perigone, and anthesis stages. More detailed studies on the
growth rate, mortality rate and population structure of this rare parasitic
plant are required to determine the fate of the young flower buds and to
estimate its complete life cycle. The findings from this study are useful in
intensifying the knowledge of this rare parasitic plant that is becoming
vulnerable and is on the brink of extinction. Due to its rarity, ongoing habitat
loss, vandalism of existing colonies, and high degree of host specificity,
various conservation actions are required to protect this taxon. Hence, the
information on the growth of buds, different flower bud developmental stages,
and population status is vital for taxonomic studies, field monitoring, and
conservation purposes.
Table 1. The range of
diameters of buds and flowers
according to its stages.
|
Name of bud stages |
Range of bud diameter (cm) |
|
Copule |
0.3–2.3 cm |
|
Copule-bract transition
(CBT) |
2.4–4.0 cm |
|
Bract |
4.1–5.5 cm |
|
Bract perigone transition (BPT) |
5.6–6.1 cm |
|
Perigone |
6.2–8.1 cm |
|
Anthesis |
16–20 cm |
Table 2. The abiotic
factors of Sapria himalayana
f. albovinosa in Machi
evergreen rainforest, Manipur.
|
Abiotic factors |
July |
August |
September |
October |
November |
|
Mean air temperature (°C) |
23 |
23 |
22 |
20 |
19 |
|
Mean humidity (%) |
80 |
84 |
86 |
72 |
67 |
|
Mean wind speed (m/s) |
1.60 |
1.66 |
1.66 |
1.66 |
1.66 |
|
Mean soil temperature (°C) |
19 |
24 |
21 |
20 |
18 |
|
Mean soil pH |
6.5 |
6.5 |
6.0 |
5.5 |
5.5 |
|
Mean soil moisture |
Wet+ |
Wet |
Wet |
Normal |
Dry |
|
Mean light intensity (lux) |
90 |
90 |
100 |
100 |
100 |
For figures & images - - click here for full PDF
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