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).

 

References

 

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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