Journal of
Threatened Taxa | www.threatenedtaxa.org | 26 July 2018 | 10(8): 12123–12129
Root holoparasite Balanophora
polyandra Griff. (Balanophoraceae)
in eastern Himalaya (Sikkim, India): distribution, range, status and threats
Prem K. Chhetri
1, Alexander R. O’Neill 2 & Bijoy Chhetri 3
1,2,3 G.B. Pant National Institute of Himalayan
Environment and Sustainable Development, Sikkim Unit, Pangthang,
Gangtok, Sikkim 737103, India
1 Forest Environment and Wildlife Management
Department, Govt. of Sikkim, Pakyong, Sikkim, 737106,
India
2 United States-India Education Foundation (USIEF) and the United States Fulbright
Commission, Washington, D.C., 20037, United States of America
1 chhetriprem22@gmail.com, 2 alexander.o.neill@duke.edu,
3 chhetribijoy@yahoo.co.in (corresponding author)
doi: http://doi.org/10.11609/jott.3644.10.8.12123-12129
Editor: V. Sampath
Kumar, Botanical Survey of India, Howrah, India. Date of
publication: 26 July 2018 (online & print)
Manuscript details: Ms
# 3644 | Received 08 July 2017 | Final received 04 May 2018 | Finally accepted
01 July 2018
Citation: Chhetri, P.K., A.R. O’Neill
& B. Chhetri (2018).
Root holoparasite
Balanophora polyandra
Griff. (Balanophoraceae)
in eastern Himalaya (Sikkim, India): distribution, range, status and threats. Journal
of Threatened Taxa 10(8): 12123–12129; http://doi.org/10.11609/jott.3644.10.8.12123-12129
Copyright: © Chhetri et al. 2018.
Creative Commons Attribution 4.0 International 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: G.B. Pant National Institute of Himalayan Environment & Sustainable
Development, Kosi-Almora, India.
Competing interests: The authors declare no competing interests.
Acknowledgements: We appreciate the guidance of P.P. Dhyani,
Director of GBPNIHESD; H.K. Badola, Scientist ‘F’ and
Scientist-in-charge, GBPNIHESD-Sikkim Unit; D.K. Agrawala,
Scientist-D, Botanical Survey of India-Gangtok; and
the Department of Forests, Environment and Wildlife, Government of Sikkim.
Abstract: Balanophora J.R. Forster & G. Forster (Balanophoraceae) is a poorly studied genus of root holoparasite native to temperate and tropical regions of
Asia and the Pacific. The
occurrences of Balanophora polyandra Griff. were first reported within two protected areas in eastern
Himalaya (Sikkim, India), namely, Khangchendzonga
National Park and Pangolakha Wildlife Sanctuary. The study assessed the distribution range of B.
polyandra in Sikkim using data collected from
both field surveys and herbarium records, and discussed the threats faced by Balanophora populations in the region.
Keywords: Balanophora,
India, root holoparasite, Sikkim Himalaya.
Botanical
surveys have exponentially increased throughout the eastern Himalaya over the
past decade (Kandel et al. 2016). The diversity and status of parasitic plants,
however, remain poorly understood (O’Neill & Rana 2016). Balanophora J.R. Forster & G. Forster (Balanophoraceae) is a genus of root holoparasite,
native to the temperate and tropical regions of Africa, Asia, and the
Pacific. There is a paucity of
ecological records (Shumei & Murata 2003; Pelser et al. 2014; Rao et al.
2015). Around the world, 19 species in
this genus have been recognized so far, of which four are reported in the
Himalaya: Balanophora dioica
R.Br. ex Royle, B. harlandii
Hook.f., B. involucrata Hook.f. & Thomson, and B. polyandra
Griff. (Eberwein
et al. 2009; Su et al. 2012; Rai et al. 2014). These species exhibit drastically reduced
morphologies, including minute flowers and scaly leaves (Nickrent
& Garcia 2009; Su et al. 2012). They
forego photosynthesis, and obtain nutrients from diverse hosts using tuberous
organs similar to haustoria (Eberwein
et al. 2009). In this article, the
occurrence of B. polyandra populations within
two protected areas in Sikkim Himalaya (India), namely, Khangchendzonga
National Park and Pangolakha Wildlife Sanctuary (Fig.
1), are discussed.
Further, the distribution range of B. polyandra,
B. dioica, B. harlandii,
and B. involucrata in Sikkim is assessed using
data collected from both field surveys and herbarium records of the Botanical
Survey of India, Gangtok, Sikkim. Our report addresses the necessary aspects of
conservation planning in eastern Himalaya, which may guide future IUCN Red List
of Threatened Species assessments.
Methods
Study area
Sikkim
is located in northeastern India between 27.533000N
and 88.519440E surrounded by Bhutan in the east, Nepal in the west,
West Bengal in the south, and the Tibetan Autonomous Region of the People’s
Republic of China in the north, and is contiguous with the Himalayan
Biodiversity Hotspot (Telwala et al. 2013).
Data collection
Quarterly
surveys were conducted in two protected areas, namely, Khangchendzonga
National Park (IUCN Category II) and Pangolakha
Wildlife Sanctuary (IUCN Category IV), between October 2015 and March 2017,
following a systematic pollard walk transect methodology
(see Pollard & Yates 1993; Kerr et al. 2000). While the transect in Khangchendzonga
National Park extended from Kisong-Tholung to Panchpokhari, and in Pangolakha
Wildlife Sanctuary extended from Lingtam to Zuluk (c. 1,600–4,500 m).
During surveys, we recorded botanical characters and ecological notes,
and confirmed our identifications at Regional Centre of Botanical Survey of
India in Gangtok, Sikkim (see O’Neill & Rana 2016). Digital
media of these specimens are available upon request. The taxonomic designations of Shumei & Murata (2003) were crucial during the
identification process, and served as the foundation of the systematic
account. Eventually, a digital elevation
model for Balanophora spp. populations using
ArcGIS Version 9.3 was generated (Fig. 1).
Results and
Discussion
Systematic Account
Balanophora polyandra Griff., Proc. Linn. Soc. London 1: 220. 1844.
Holoparasitic herb, dioecious, tubers clustered in coarse
agglomeration, cylindrical, surface covered in stellate protuberances and gray to white haustoria, 2–5 cm
in diam., chiffon to blush. Scapes emerge from apex of root segment, 2.0–10.0 × 0.5–1.5
cm, cream to crimson. Leaves decussate,
4–10, whorled, obovate to broadly oblong, concave,
apex rounded, margin entire, base attenuate, 1.5–2 × 1.0–1.2 cm, cream to
crimson. Inflorescences emerge
endogenously from apex of root segments.
Staminate inflorescence terminal, narrowly ellipsoid and spadix-like,
racemose, 3–10 cm; pedicelled,
bracts truncate, c. 1.0mm, cream to tan.
Staminate flowers bisymmetrical to
zygomorphic, numerous, spirally arranged in conspicuous vertical rows, c. 1cm
in diam., pedicels 2–4 mm, apex truncate; lateral tepals
deltoid to ovate; syndaria subdiscoid,
4–5 mm in diam., anthers 25–50 locelli, dehiscent,
white. Pistillate inflorescence terminal,
ellipsoid to oblong-ovoid, 2.0–3.0 x 1.0–2.5 cm, orange to crimson; spadicles clavate, 1.5–2.5 mm;
“apical 1/2 to 2/3 ellipsoid to obovoid, cuticular ridges of apical cells short but distinct and
congested” (Shumei & Murata 2003). Pistillate flowers zygomorphic, numerous and minute, c. 1.5mm, arranged on
main axis of inflorescence and basal stipe of spadicles,
white to cream. Flowering period
from August to November.
Distribution and Habitat
B. polyandra exhibits a broad distribution throughout
the Himalaya, with populations reported in Bhutan, India (Sikkim), Myanmar,
Nepal (Kaski, Mustang, Sankhuwasava,
Taplejung), and the People’s Republic of China
(Guangxi, Hubei, Hunan, Xizang, and Yunan) between
1,000m and 3,000m (Shumei & Murata 2003; O’Neill
& Rana 2016).
This species was first reported in the eastern Himalaya by J.D. Hooker
in the mid-19th century, and has 11 herbaria records at the
Botanical Survey of India in Gangtok (Hooker 1855;
Appendix 1). The current study is a
first time report of seven new occurrences of the species within two protected
areas in the Sikkim Himalaya: namely, the Khangchendzonga
National Park (KNP) and Pangolakha Wildlife Sanctuary
(PWS). In KNP, five populations comprised of 24 individuals (5 staminate and 19 pistillate
inflorescences) were found; in the PWS, two populations comprising of four
total individuals (1 staminate and 3 pistillate inflorescences; Image 1) were found. These populations found growing in
warm-temperate forests (2,000m and 2,300m) dominated by the following woody
taxa: Acer campbellii (Sapindaceae),
Alnus nepalensis (Betulaceae), Betula utilis (Betulaceae), Castanopsis tribuloides
(Fagaceae), Engelhardia
spicata (Juglandaceae),
Eurya japonica (Pentaphylacaceae),
Exbucklandia populnea
(Hamamelidaceae), Juglans
regia (Juglandaceae), Quercus lamellosa (Fagaceae), Q. pachyphylla
(Fagaceae), and Viburnum grandiflorum
(Adoxaceae).
The preferred habitat of B. polyandra is
shaded, northeastern slopes (35–550), in
soils with 5–8 cm of humus. This species
parasitized seven species belonging to four families: Castanopsis
tribuloides (Fagaceae),
Quercus lamellosa,
Q. pachyphylla (Fagaceae),
Eurya japonica (Pentaphylacaceae),
Evodia fraxinifolia
(Rutaceae), Symplocos
theifolia, and S. spicata
(Symplocaceae).
During autumn (October and November 2015), it was observed that Apis cerana (Apidae) was pollinating pistillate
flowers of B. polyandra in KNP.
Threats
Deforestation
threatens B. polyandra populations in Sikkim (Chettri et al. 2002; Pandit et
al. 2007; Sharma et al. 2007, 2015). A
rough estimate projects up to 40% decrease in forest cover by 2100, with
transformations driven by road expansion for defense
and ecotourism purposes (Sundriyal & Sharma 1996;
Maharana et al. 2000; Chettri
et al. 2002; Pandit et al. 2007). Herbaria records from the late 1990s suggest
that populations of B. polyandra and the
congeneric B. dioica were inundated during the
construction of the Rangit Dam between Nauprik and Bey. The Government of Sikkim, however, has taken
progressive strides to mitigate potential forest loss and habitat degradation
through polices such as Sikkim Forests and Water Courses (Preservation and
Protection) Act 2007. Moreover, the 2016
inscription of KNP as a UNESCO World Heritage Site extends additional
protection to the B. polyandra populations.
Agricultural expansion of large Cardamom (Amomum
subulatum, Zingiberaceae)
may also threaten Balanophora spp.
habitat in Sikkim (Gaira et al. 2016; Sharma et al. 2016). The acute ramifications of forest conversion
for agricultural purposes, however, may be overshadowed by chronic
environmental changes, including range shifts of host-plant (Quercus spp.) populations (Kumar 2012; Telwala et al. 2013).
These host plant populations, too, face high extraction pressures in
rural Sikkim (Chettri et al. 2002; Tambe et al. 2011).
Although Balanophora spp. are reported for their medicinal value, including the
treatment of skin diseases, internal parasites, and sexually transmitted
infections, they face minimal extraction pressure for these purposes in the
eastern Himalaya (Venkatareddi 1969; Podimuang et al. 1971; Ignacimuthu
et al. 2006; Tao et al. 2009; Wang et al. 2013; Sharma 2015).
Based
on IUCN Red List of Threatened Species criteria, Balanophora
polyandra is a Least Concern (LC) species both in
Sikkim and throughout the eastern Himalaya due to its wider distribution
(extent of occurrence EOO >20,000km2) and population stability
within several protected areas (O’Neill & Rana
2016). Botanical records suggest that B.
dioica, B. harlandii,
and B. involucrata, too, are Least
Concern (LC) species due to their wider distributions reportedly correlated
with host-species ranges (Sharma 2002; Shumei &
Murata 2003; Thriveni et al. 2016), and location
within the protected areas (Jamir & Pandey 2003; Rai et al.
2014). Agricultural expansion threatens Balanophora habitats throughout the eastern
Himalaya, as well as Assam and Manipur, where mining has increased in recent
decades (Sharma 2002; Bora et al. 2010).
Census data for Balanophora spp.
remains limited. One additional species
in the Balanophoraceae, Rhopalocnemis
phalloides, also has a literature record in
Sikkim; however, no herbaria accessions are available as of December 2016. MaxEnt habitat
suitability modeling may further clarify the range
and status of Balanophoraceae in Eastern Himalaya (Kumar 2012; Chhetri & Badola 2017).
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Appendix 1. Records of Balanophora spp. (Balanophoraceae)
in Sikkim Himalaya based on herbarium data, (Sikkim Himalayan Regional Centre,
BSI, Gangtok) and present field study (marked with *)
Species |
District |
Locality |
Altitude |
Coordinates (0N | 0E) |
Date of Collection /date of study |
Collector(s)/observer(s) |
Collection no./Acc. no. |
Notes from Herbarium labels |
|
Balanophora dioica Royle |
West Sikkim |
Sachen (Old Goath
Below) |
N/A |
27.41353 |
88.19674 |
2009 |
S.K. Rai; K.
Das |
44711 |
Petals 4, anthers many, flowers white,
clustered in dome head, young one pinkish, leafy stem |
Balanophora dioica Royle |
West Sikkim |
Sachen (Old Goath
Below) |
N/A |
27.41353 |
88.19674 |
2009 |
S.K. Rai; K.
Das |
44712 |
Petals 4, anthers many, flowers white,
clustered in dome head, young one pinkish, leafy |
Balanophora dioica Royle |
East Sikkim |
Dikchu (NHPC Dam Site) |
750m |
27.38785 |
88.50788 |
1997 |
S.K. Jana |
33657 |
Grows on marshy land |
Balanophora dioica Royle |
East Sikkim |
Dikchu (NHPC Dam Site); Note: Probably from Nauprik to Bey |
720m |
27.38785 |
88.50788 |
1997 |
S.K. Jana |
33661 |
Grows on marshy land |
Balanophora dioica Royle |
East Sikkim |
Dikchu (NHPC Dam Site) |
720m |
27.38785 |
88.50788 |
1997 |
S.K. Jana |
33660 |
Grows on marshy land |
Balanophora dioica Royle |
East Sikkim |
Dikchu (NHPC Dam Site) |
721m |
27.40359 |
88.52144 |
1997 |
S.K. Jana |
33659 |
Grows on marshy land |
Balanophora dioica Royle |
East Sikkim |
Dikchu, Right Flank |
N/A |
27.40359 |
88.52144 |
19-97 |
B.K. Shukla |
33658 |
Root parasite, petal coffee colour,
herbs up to 20cm tall |
Balanophora dioica Royle |
East Sikkim |
Dikchu, Right Flank |
N/A |
27.40359 |
88.52144 |
1997 |
B.K. Shukle |
22604 |
Root parasite, petal coffee colour,
herbs up to 20cm tall |
Balanophora dioica Royle |
East Sikkim |
Dikchu, Right Flank |
N/A |
27.40359 |
88.52144 |
1997 |
B.K. Shukla |
22602 |
Root parasite, petal coffee colour,
herbs up to 20cm tall |
Balanophora dioica Royle |
West Sikkim |
Tshoka to Gumsa |
N/A |
27.38785 |
88.50788 |
2009 |
S.K. Rai; K.
Das |
44625 |
Flowering head pinking, stem yellow,
sheathed; root parasite |
Balanophora dioica Royle |
West Sikkim |
Tshoka to Gumsa |
N/A |
27.38785 |
88.50788 |
2009 |
S.K. Rai; K.
Das |
44626 |
Flowering head pinking, stem yellow,
sheathed; root parasite |
Balanophora involucrata Hook.f. |
North Sikkim |
Singba 'A' |
N/A |
27.80109 |
88.76956 |
2011 |
Dr. K Das; S.K. Rai |
43891 |
Root parasite, found in the Rhododendron
forest, head pinkish, red, root dotted below |
Balanophora involucrata Hook.f. |
North Sikkim |
Singba 'A' |
N/A |
27.80109 |
88.76956 |
2011 |
Dr. K Das; S.K. Rai |
43892 |
Root parasite, found in the Rhododendron
forest, head pinkish, red, root dotted below |
Balanophora involucrata Hook.f. |
North Sikkim |
Lachung to Dombeyang |
N/A |
27.73649 |
88.21318 |
1987 |
D.C.S. Raju;
S. Singh |
15918 |
Roots or stem parasites, whole plant
yellow, leaves and flowers yellow |
Balanophora involucrata Hook.f. |
North Sikkim |
Lachung to Dombeyang |
N/A |
27.73649 |
88.21318 |
1987 |
D.C.S. Raju;
S. Singh |
15917 |
Roots or stem parasites, whole plant
yellow, leaves and flowers yellow |
Balanophora involucrata Hook.f. |
East Sikkim |
Karponang |
N/A |
27.39104 |
88.77742 |
1984 |
B. Krishna; S. Singh |
5636 |
Root parasite, petals 5, reddish |
Balanophora involucrata Hook.f. |
East Sikkim |
Karponang |
N/A |
27.39104 |
88.77742 |
1984 |
B. Krishna; S. Singh |
5637 |
Root parasite, petals 5, reddish |
Balanophora involucrata Hook.f. |
East Sikkim |
Forest behind Elephant Mansion, Gangtok |
N/A |
27.30574 |
88.36578 |
1980 |
P. Chakraborty |
4345 |
N/A |
Balanophora involucrata Hook.f. |
East Sikkim |
Forest behind Elephant Mansion, Gangtok |
N/A |
27.30574 |
88.36578 |
1980 |
P. Chakraborty |
4578 |
Fleshy leaves with tuberous roots |
Balanophora polyandra Griff. |
South Sikkim |
Rabongla (East Side) |
N/A |
27.30654 |
88.3648 |
2008 |
S.K. Rai |
42932 |
Herbs, flowers white, powdery, male cone
reddish, bracteate, lanceolate |
|
|
|
|
|
|
|
|
|
|
Balanophora polyandra Griff. |
South Sikkim |
Rabongla (East Side) |
N/A |
27.30654 |
88.3648 |
2008 |
S.K. Rai |
42933 |
Herbs, flowers white, powdery, male cone
reddish, bracteate, lanceolate |
Balanophora polyandra Griff. |
South Sikkim |
Rabongla (East Side) |
N/A |
27.30654 |
88.3648 |
2008 |
S.K. Rai |
42931 |
Herbs, flowers white, powdery, male cone
reddish, bracteate, lanceolate |
Balanophora polyandra Griff. |
West Sikkim |
Karchi R.F. |
2,000m |
27.37405 |
88.3648 |
1999 |
B.K. Shukla |
22603 |
Root parasite grows in temperate forest
up to 15 cm tall |
Balanophora polyandra Griff. |
West Sikkim |
Karchi R.F. |
2,000m |
27.37405 |
88.3648 |
1999 |
B.K. Shukla |
35022 |
Root parasite grows in temperate forest
up to 15 cm tall |
Balanophora polyandra Griff. |
West Sikkim |
Karchi R.F. |
2,000m |
27.37405 |
88.3648 |
1999 |
B.K. Shukla |
35023 |
Root parasite grows in temperate forest
up to 15 cm tall |
Balanophora polyandra Griff. |
West Sikkim |
Karchi R.F. |
2,000m |
27.37405 |
88.3648 |
1999 |
B.K. Shukla |
35024 |
Root parasite grows in temperate forest
up to 15 cm tall |
Balanophora polyandra Griff. |
West Sikkim |
Yuksom; After Karthok
Pokhari |
N/A |
27.37233 |
88.22231 |
1992 |
R.C. Srivastava |
35025 |
Parasitic herbs on hil
base in bridge; basal thint yellowish seed stem
brown flowers whorled |
Balanophora polyandra Griff. |
West Sikkim |
Yuksom; After Karthok
Pokhari |
N/A |
27.37233 |
88.22231 |
1992 |
R.C. Srivastava |
35026 |
Parasitic herbs on hil
base in bridge; basal thint yellowish seed stem
brown flowers whorled |
Balanophora polyandra Griff. |
West Sikkim |
Yuksom; After Karthok
Pokhari |
N/A |
27.37233 |
88.22231 |
1992 |
R.C. Srivastava |
35027 |
Parasitic herbs on hil
base in bridge; basal thint yellowish seed stem
brown flowers whorled |
Balanophora polyandra Griff. |
West Sikkim |
Yuksom-Bakhim Trek (Sachen) |
N/A |
27.39917 |
88.21318 |
2004 |
S.K. Rai; Arun Kr. Chhetri |
43293 |
Saprophytic, flowers globose
white |
Balanophora polyandra Griff. |
North Sikkim |
Khangchend-zonga National Park |
2,227m |
27.57263 |
88.49970 |
2016 |
P.K.Chhetri, B. Chhetri* |
N/A |
Herbs, flowers, male cone reddish, female cone cream colour,
grows on shady area of sloppy temperate region |
Balanophora polyandra Griff. |
North Sikkim |
Khangchend-zonga National Park |
1,991m |
27.55239 |
88.49929 |
2016 |
P.K.Chhetri, B. Chhetri* |
N/A |
Herbs, flowers, male cone reddish, female cone like racemose with cream colour, grows on shady area of sloppy
temperate region |
Balanophora polyandra Griff. |
North Sikkim |
Khangchend-zonga National Park |
2,183m |
27.57242 |
88.49916 |
2016 |
P.K.Chhetri, B. Chhetri* |
N/A |
Herbs, flowers, male cone reddish, female cone like racemose with cream colour, grows on shady area of sloppy
temperate region |
Balanophora polyandra Griff. |
North Sikkim |
Khangchend-zonga National Park |
2,376m |
27.5765 |
88.51075 |
2017 |
P.K.Chhetri, B. Chhetri* |
N/A |
Herbs, flowers, male cone reddish, grows on shady area of
sloppy temperate region |
Balanophora polyandra Griff. |
North Sikkim |
Khangchend-zonga National Park |
1,826m |
27.5765 |
88.51075 |
2017 |
P.K.Chhetri, B. Chhetri* |
N/A |
Herbs, flowers, male cone reddish, grows on shady area of sloppy temperate
region |
Balanophora polyandra Griff. |
East Sikkim |
Pangolakha Wildlife Sanctuary |
2,044m |
27.2378 |
88.76441 |
2017 |
P.K. Chhetri* |
N/A |
Herbs, flowers, male cone reddish and
female cone turned into blackish,grown
on shady area of temperate forest |
Balanophora polyandra Griff. |
East Sikkim |
Pangolakha Wildlife Sanctuary |
2,152m |
27.23868 |
88.76996 |
2017 |
P.K. Chhetri* |
N/A |
Herbs, flower male cone reddish grown on
shady area of temperate forest |