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Pollen Morphology of Nepenthes khasiana hook. f. (Nepenthaceae), An EndemicInsectivorous Plant from IndiaAuthor(s): Sadhan K. Basumatary, Swati Tripathi, Samir K. Bera and Subodh KumarSource: Palynology, 38(2):324-333. 2014.Published By: AASP: The Palynological SocietyURL: http://www.bioone.org/doi/full/10.1080/01916122.2014.912993

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Pollen morphology of Nepenthes khasianaHook. f. (Nepenthaceae), an endemic insectivorousplant from India

Sadhan K. Basumatary*, Swati Tripathi, Samir K. Bera and Subodh Kumar

Quaternary Palynology Division, Birbal Sahni Institute of Palaeobotany, 53 University Road, Lucknow-226007, India

The pollen morphology of Nepenthes khasiana (the pitcher plant) from India, was investigated using both lightmicroscopy and scanning electron microscopy. This was to investigate fine details that may contribute to thetaxonomic characterisation of species, as well as to utilise the knowledge of its morphology in order to correlate itwith Bornean Nepenthes species. The size of the tetrad is the defining feature. The pollen grain is non-aperturate, thesexine is spinuliferous and thicker than the nexine. The study indicates that the species is similar in shape, apertureand ornamentation, and can be discriminated by the size of the tetrad, the length of the spines and the exinethickness. The size of the tetrad (30.7 mm) is closer to two Bornean species such as N. rafflesiana and N. mirabilis(30.5 and 31.0 mm respectively). These observations will be helpful in morphotaxonomy for accurate identification.This will help in finding these taxa from modern and sub-surface soils in order to study the present status of pollenpreservation and decipher the palaeovegetation and past climate of the region.

Keywords: Nepenthes khasiana; pollen morphology; Meghalaya; northeast India

1. Introduction

The state of Meghalaya (lat. 25�470 to 26�100 N, long.

89�450 to 92�450 E) is located in the northeastern part

of India, and situated in the transition between the

eastern Himalayan foothills and the Indo-Burma hot-

spot region (Figure 1). The rich biodiversity is due to

several reasons including topography, physiography

and rainfall. Nepenthes khasiana is one of the endemic

plant species of India and belongs to the family Nepen-thaceae. It is a scandent insectivorous plant of the trop-

ical and subtropical climatic regions covering the

eastern Himalayan tract up to an altitude of 1400 m

above sea level (asl) in northeast India (Kanjilal et al.

1934�1940; Hajra 1974; Rao & Haridasan 1982;

Ahmedullah & Nayar 1987; Nayar & Sastry

1987�1990; Ghopalan & Henry 2000). It grows in

association with Licuala peltata, Calamus erectus, Lith-ocarpus dealbata and fern species like Alsophila gigan-

tea, Dicranopteris lanigera, D. splendens, Thelypteris

lakhimpurensis, Lycopodium cernuum and Gleichenia

dichotoma. In the Nokrek Biosphere Reserve of

Meghalaya, N. khasiana is intensively exploited by the

Garo tribal inhabitants for their medicinal use and as a

source of income for their daily basic needs. They pro-

cure the plants from the nearby area and sell them tonearby markets for cheap prices, approximately

20�30 rupees per seedling plant (Singh et al. 2011).

The powder of the roots and pitcher is applied for skin

diseases, juice from unopened pitchers is used as eye-

drops against eye diseases and the pitcher with the juice

is frequently used by cholera patients (Singh & Mudgal

1999). A few years ago, N. khasiana was naturally

growing abundantly in the valley of Nokrek Biosphere

Reserve (Haridasan & Rao 1984), as well as in the

Nangalbibra and Siju forests (Plate 1). It is thought to

attract prey by means of blue fluorescence (Kurupet al. 2013). The species has a localised distribution,

and is rarely found in the wild. Isolated populations

are known to occur in the Jarain area of the Jaintia

Hills and the Baghmara area of the Garo Hills, adja-

cent to the Khasi Hills region of Meghalaya. Neverthe-

less, N. khasiana exhibits considerable genetic diversity

(Bhau et al. 2009). The Khasi people call the plant

‘tiew-rakot’, which means ‘demon-flower’ or‘devouring-plant’. The Jaintias call it ‘kset phare’,

which is roughly translated as ‘lidded fly net’. The

Garo call the plant ‘memang-koksi’, which literally

means the ‘basket of the devil’ (Haridasan & Rao

1985�1987). However, due to overexploitation and

deforestation, the plant is already threatened and clas-

sified as an endangered species. The effect of fire on N.

khasiana was also recorded and it was noticed thatsometimes the controlled forest fires damage the pri-

mary habitat of this species, along with grazing and

browsing of animals which plays an important role in

reducing its further growth.

The genus Nepenthes comprises more than 100 cur-

rently described species (Phillipps et al. 2008; McPherson

2009) that are the result of a recent (and ongoing)

*Corresponding author. Email: sbasumatary2005@yahoo.co.in

� 2014 AASP � The Palynological Society

Palynology, 2014

Vol. 38, No. 2, 324�333, http://dx.doi.org/10.1080/01916122.2014.912993

diversification in the Malaysian region (Krutzsch 1985,

1989; Meimberg et al. 2001). The centre of diversity is

located on the islands of Borneo (36 species), Sumatra

(>30 species) and the Philippines (21 species). The rateof endemism is extremely high (approximately 75% for

Sumatra, 80% for Borneo and 95% for the Philippines),

and especially, many of the montane species have a very

narrow distribution range (Clarke 1997, 2001; McPher-

son 2009). The species richness of the genus is mirrored

by a remarkable diversity of trap designs. The leaves of

Nepenthes are highly modified to form passive pitfall

traps that vary between species in size and shape. Prey(mainly arthropods) are attracted to the pitchers by a

combination of nectar secretion and visual and olfactory

cues, and captured by means of specialised slippery sur-

faces on the upper pitcher rim (peristome) and the upper

part of the inner pitcher wall (Juniper et al. 1989; Gaume

et al. 2002; Bohn & Federle 2004; Bauer & Federle

2009). The lower part of the pitcher is filled with a diges-

tive fluid that not only contains specialised microfaunaand the enzymes needed to release the nutrients from the

prey (Amagase 1972) but, in some species, also ensures

effective prey retention due to its viscoelastic properties

(Gaume & Forterre 2007; Bauer et al. 2011; Bonhomme

et al. 2011).

Some scattered reports have been published based

on the morphology of Nepenthes pollen from Borneo

(Adam &Wilcock 1999). Hitherto, no work on the pal-ynological aspects of N. khasiana has been undertaken.

Within the last four decades, the study of pollen has

been expanded to such an extent that it now has an

extensive separate literature and is a discipline of its

own. Pollen grains can easily be observed and studied

under the light microscope but, for the study of its fin-

est details such as wall architecture and exine sculptur-

ing, the transmission electron microscope (TEM) and

scanning electron microscope (SEM) are necessary.

Pollen grains are comparatively little altered by the

process of preparing herbarium specimens; thus, her-

baria have been extensively used as a source of refer-ence material for comparative studies in palynology

(Brenan 1968). The fact that fossil pollen retains most

of its structural detail is of great significance in estab-

lishing evolutionary trends in angiosperms (Muller

1970). For angiosperm phylogeny, palynology is

unique, in that through no other study can obtain as

great an amount of information from so little material

in such a short time (Walker & Doyle 1975). An excel-lent review of the systematic applications of palynology

in the plant kingdom was given by Erdtman (1943).

Examples of the usefulness of pollen characters in

delimiting plant taxa were given by Cerceau-Larrival

(1971) for the Umbelliferae and Skvarla & Turner

(1966) in the Compositae. Erdtman & Metcalfe (1963)

gave an example in which palynology and anatomy

can be used to solve taxonomic problems, and Jeffrey(1964) used pollen morphology to establish a new sys-

tem of classification for the Curcubitaceae. Features of

pollen and spores are being increasingly used in sys-

tematic studies including size and shape (the principal

characters of pollen grains), pollen type, number and

position of the apertures and pollen wall architecture

(Heywood 1976). Therefore, for the first time, an

attempt has been undertaken with the aid of the lightmicroscope (LM) and SEM to examine some new char-

acters in Nepenthes that might help in identification

and redefining the species classification. This will help

in the precise recognition of its modern and fossil coun-

terparts in surface soil and sediment respectively for

deciphering past vegetation and climate change. Pub-

lished data from Balpakram Valley, Meghalaya, and

Yunnan, China, documents preservation of Nepenthes

Figure 1. Map of Meghalaya showing the sampling sites.

Palynology 325

Plate 1 1. View of Nepenthes khasiana showing the flowering stage in the Nangalbibra area, Meghalaya. 2. Luxuriant growth ofNepenthes khasiana with Gleichenia dichotoma and Lycopodium cernuum in the Siju wildlife sanctuary, Meghalaya.

326 S.K. Basumatary et al.

in surface soil and moss samples respectively (Song

et al. 2012; Basumatary et al. 2014).

2. Floral diversity with special emphasis on endemic

and threatened plants

The floral diversity of Meghalaya is rich. It has about

3128 species of flowering plants and contributes about

18% of the total flora of the country, including 1237

endemic species (about 40% of the total flora) (Khan

et al. 1997). According to Takhtajan (1988), the flora

of the Khasi and Jaintia Hills is most richly saturated

by eastern Asiatic elements, and the area is one of themost important centres of survival of the Tertiary flora

of eastern Asia. The species that were common some

20 to 30 years ago are becoming rare due to overexploi-

tation, deforestation and habitat destruction. Some

fern species, namely Dipteris wallichii and Cyathea

gigantea, have become rare in Meghalaya. Ilex embe-

loides, Styrax hookerii and Fissistigma verrucosum,

which are considered extremely rare, were procuredfrom a sacred grove recently after several decades

(Upadhaya 2002; Jamir & Pandey 2003). Several

orchid genera such as Dendrobium, Pleione, Paphiope-

dilum and Vanda, having ornamental value, are becom-

ing rare in nature. Podocarpus neriifolia, Cyathea

gigantea, Ilex khasiana and Balanophora dioica and

saprophytic orchids like Galeola falconeri, Epipogium

roseum and Eulophia sanguinea are becoming rare dueto habitat destruction (Kataki 1986). Nepenthes khasi-

ana, which is one of the rare insectivorous plants, is

reported only from a small pocket in Meghalaya. Rao

& Haridasan (1982) have reported 54 rare and threat-

ened plants, and Haridasan & Rao (1985�1987) have

listed 44 rare dicotyledonous plants from Meghalaya.

The forests have been over-exploited due to road and

other infrastructural development. As a result, naturalforest stands are decreasing in aerial extent day by day

which in turn increases the percentage of threatened

plants in Meghalaya (Bera et al. 2006).

3. Materials and methods

3.1. Light microscopy

The fresh polliniferous material (flowers/stamens) was

added to a small amount of water and crushed gradu-

ally in a plastic centrifuge tube. The materials were

then passed through a 150 mm mesh sieve and centri-

fuged, and then water was decanted off. We centri-

fuged the leftover material with glacial acetic acid

(GAA) and further decanted off. In the centrifugetube, about 5 cm3 of acetolysing mixture (9:1 acetic

anhydrate and concentrated sulphuric acid, H2SO4)

was added and it was placed in a hot water bath for

about 2 minutes (Erdtman 1954). After this, the mate-

rial was treated with GAA again. Thereafter, the mate-

rial was washed with water at least two to three times

to remove all acid content. Finally the material wastreated with 50% glycerine and centrifuged, and the

glycerine was decanted off. The material was then

mounted on a glass slide with glycerine jelly. The slides,

being labelled with full details, were deposited in the

sporothek of Birbal Sahni Institute of Palaeobotany,

Lucknow, India. Microphotographs were taken with

an Olympus microscope BX 61 with Olympus DP 25

camera (Plate 2, figures 1�3). However, some pollenphotos with finer measurement were taken with an

Olympus BX 51 with Olympus DP 26 camera (Plate 2,

figures 4�6).

3.2. Scanning electron microscopy

The pollen grains were prepared for the SEM by the

methods described by Erdtman (1952). The pollen

grains suspended in a drop of water were placed on a

piece of glass plate (due to its smooth surface), then

transferred to a double-sided tape-affixed stub with a

fine pipette and coated with gold-palladium in a sput-

tering chamber (Polaron sputter coater, SC 7640).

Coating was restricted to 100 A�. The specimens were

examined with an LEO-430 microscope at 15 kV and

photographed (Plate 3).

4. Results and discussion

4.1. Pollen unit and shape

The single species of Nepenthes in India, N. khasiana,

produces pollen in tetrahedral tetrads, which represent

retention of the four products of meiosis from a single

pollen mother cell. Since all the pollen units are in tet-

rads, it is not possible to identify the shape of each pol-

len grain (the size of a monad is 20.14 � 15.03 mm).This character is common with all other species of

Nepenthes. However, the size of monad is reported for

the first time in our study and can be one of the chief

characters used to discriminate different species of

Nepenthes.

4.2. Tetrad size

The pollen tetrad diameter of Nepenthes khasiana is

about 30�31 mm, and falls into the medium-sized class

of Nepenthes spp. from Borneo where species were

divided into three groups. Group I comprises a single

species, N. gracilis (section Vulgatae), which has thesmallest mean pollen tetrad diameter (27 mm). Group

II is represented by species from five sections of Danser

(1928), and shows continuous variation between all the

Palynology 327

Plate 2. Pollen of Nepenthes khasiana (light microscope). 1. Polar view with high focus. 2. Polar view with low focus. 3. Polarview with clear sporoderm. 4. Showing pollen length measurement. 5. Showing monad measurement. 6. Showing measurement ofexine (sexine þ nexine).

328 S.K. Basumatary et al.

Plate 3. Pollen of Nepenthes khasiana (scanning electron microscope). 1. Group of tetrads adherent due to spines. 2. Close-upview showing two tetrads. 3, Polar view showing the tetrad lining and the spinulate pattern. 4. Close-up view showing sexine orna-mentation and spine length. 5 and 7. Polar view showing the tetrad lining and the spinulate pattern. 6. Closer view showing thesporoderm pattern and surface. 8. Close-up view of the outer wall of a monad showing the distance between two spines.

Palynology 329

species with tetrad diameter ranges from 28.5 to

34.7 mm (Table 1). Group III is represented by three

species of section Regiae and one species of section

Insignes. Numerous reports in the literature suggestthat pollen grain size can be a rather unstable character

(Stanley & Linskens 1974; Walker & Doyle 1975; Kiew

1984; Som 1988). Pollen size might be somewhat

affected or influenced by the method of preparation.

Even though chemical treatment and mounting media

can influence pollen size, these two factors can be elimi-

nated since Nepenthes spp. from Borneo were identi-

cally treated chemically and mounted in the samemedia. Variation in pollen size helps in deciphering the

onset of pastoral activity, where size of pollen is the

major character (especially in the family Poaceae) to

distinguish wild species from cultigens (Dixit & Bera

2011). Adam (1998) reported Nepenthes species from

Borneo bearing spinose pollen tetrads with diameters

ranging from 20 to 40 mm. His study shows that mean

pollen tetrad size range from 27 to 38.9 mm, thus

falling into the small- and medium-sized grain classes

of Walker and Doyle (1975). Thus, the genus

Nepenthes therefore belongs to a derived angiosperm

group with N. khasiana closer to N. rafflesiana (widestdistribution range and oldest species in the section

Insignes) and N. mirabilis on the basis of size proxim-

ity. The tetrad of Droseraceae (40�95 mm) is very simi-

lar to Nepenthaceae except for the size difference

(Erdtman, 1952). Thus, size could be a chief character

to identify different Nepenthes species.

4.3. Aperture type

Apertures are specifically delimited, more or less

obscure, generally thin-walled areas in the outer pollen

wall or exine through which the pollen tube usually

(but not always) emerges at the time of germination.

Pollen is lacking a germination furrow or aperture.

The same morphological character is observed in all

other species of Nepenthes. Therefore, this charactercould not play a valuable role in distinguishing species.

4.4. Exine sculpturing

The ornamentation of the pollen grain is spinulose.

This pattern of sporoderm is similar to that of

Nepenthes species from Borneo. The size of the spines

varies from 0.3 to 0.5 mm, whereas the distancebetween two spines is 0.7 to 2 mm. The exine is thick

(approximately 1.26 mm). The sexine (approximately

0.97 mm) is thicker than the nexine (approximately

0.39 mm). Details of measurements of the exine and

the spines are reported for the first time for

N. khasiana. Such information is not published any-

where in regard to any species of Nepenthes. Thus, it is

required to study these finer details in other species aswell to search for accurate characters that might con-

tribute to redefining taxonomic characterisation of

species.

Our observations regarding a single Nepenthes spe-

cies from India and its comparison with species from

Borneo found some morphological differences regard-

ing size of the tetrad which falls within Group II of the

Bornean Nepenthes species. Owing to the close sizeproximity of the tetrad, it is well established that the

N. khasiana tetrad size character is the only morpho-

logical difference by which it can be distinguished from

species from Borneo. The pollen morphology is similar

in relation to pollen type and shape, but differs in tet-

rad size to some extent. However, spine length, sporo-

derm thickness and interspinal space could be other

finer morphological features which should be takeninto consideration for comparison at the species level.

The spines of the pollen help during pollination time

and the plant is entomophilous (Adam 1998).

Table 1. List of the 28 Nepenthes species with their pollentetrad size and group from Borneo and India (after Adamand Wilcock 1999).

Name of species Pollen tetrad size (mm) Group

N. gracilis 27 I

N.ampullaria 28.9 II

N. bicalcarata 28.9 II

N. mapuluensis 28.9 II

N. hirsuta 28.9 II

N. curtisii 29.7 II

N. northiana 29.8 II

N. tentaculata 29.8 II

N. rafflesiana 30.5 II

N. khasiana (India) 30.7 II

N. mirabilis 31 II

N. albomarginata 31.8 II

N. muluensis 32 II

N. hookeriana 32.2 II

N. faizaliana 32.3 II

N. veitchii 32.3 II

N. lowii 33 II

N. reinwardtiana 31.6 II

N. alisaputraiana 33.7 II

N. macrovulgaris 34.2 II

N. clipeata 34.4 II

N. edwardsiana 34.4 II

N. fusca 34.8 II

N. rajah 34.7 II

N. mollis 37.2 III

N. villosa 37.2 III

N. ephippiata 38.5 III

N. kinabaluensis 38.9 III

330 S.K. Basumatary et al.

Flowering of N. khasiana extends from November to

February; thus, this is the best time to explore this sin-

gle endangered species in order to examine more details

regarding not only pollen morphology but genetic,chemical and other details to save the taxon which is in

danger of becoming extinct in the near future. The

great difference between N. khasiana and Nepenthes

species from Borneo could be due to climatic variation

(high rainfall in Meghalaya) and genetic differences.

There is no chance of cross pollination in N. khasiana

(monospecific) for the generation of different species.

Pollen size is often influenced by internal and externalfactors (genetic and environmental) (Via do Pico &

Dematteis 2013). It is also observed that N. khasiana

procured from various altitudes in Meghalaya (Bagh-

mara, 20 m asl; Balpakram national park, 700 m asl;

Shillong, 1500 m asl) show absolutely no morphomet-

ric differences.

5. Conclusions

Here, for the first time, an attempt has been initiated to

study the finer morphological details of N. khasiana, an

endemic plant of Meghalaya which is on the verge of

extinction. It attracts taxonomists, palynologists, environ-

mentalists and ethnobotanists to investigate the obscure

aspects of its plant parts due to the existence of only asingle species in India. Comparison of the morphology of

its pollen with that of Nepenthes species growing in Bor-

neo is another aim of the present study. During our

examination of pollen morphology, a minute size differ-

ence between the pollen tetrad of N. khasiana and the

species from Borneo came into focus. Pollen tetrads

(30.7 mm) of N. khasiana are closer to N. rafflesiana and

N. mirabilis of Group II. However aperture type, exinesculpture and tetrad type are similar. For the first time,

we also measured sporoderm thickness, spine length and

monad size, and found there is no considerable difference

among the species procured from different altitudes.

Thus, our study will be helpful for the accurate identifica-

tion of pollen of Nepenthes up to a specific level, and will

in turn help in the recognition of its fossil counterparts in

sediments for interpretation of past vegetation and cli-mate. The inevitable pressure due to the commercializa-

tion of N. khasiana is leading to the severe destruction of

the species, and may create the scarcity of the species in

the near future. Therefore, joint efforts need to be imple-

mented by the local Garo villagers with governmental

and non-governmental agencies for conservation and sus-

tainable use of N. khasiana. The government may also

take the initiative by allotting demarcated forest areas tothe villagers as village forest, thus motivating the villagers

to take special care for its protection and rehabilitation,

and for a sustainable output.

Acknowledgements

We thank Professor Sunil Bajpai, Director of the BirbalSahni Institute of Palaeobotany, for providing laboratoryfacilities and permission to publish the manuscript. We arealso thankful to the forest officials of Meghalaya for theirhelp during sample collection.

Author biographies

SADHAN K. BASUMATARY wasawarded a BSc from the University ofGauhati in 1995, an MSc in botanyfrom the University of Gauhati in 1998and a PhD on Quaternary palynologyfrom the University of Lucknow in2011. He is currently a Scientist ‘C’ atthe Birbal Sahni Institute of Palaeobo-tany in Lucknow, working on palaeocli-

matology using multiproxy data. He has 12 years researchexperience, and has published 58 papers in national and inter-national journals.

SWATI TRIPATHI is currently work-ing as a Scientist ‘B’ at the Birbal SahniInstitute of Palaeobotany. She focuseson palaeoclimatology using Quaternarypollen as proxy. She was awarded a BScin botany from Lucknow University in2005. Later, she received three GoldMedals for obtaining the highest per-centage of marks in the MSc (botany),

at Lucknow University in 2007. She undertook PhD studiesand received her doctorate in 2011 from the Department ofBotany, Lucknow University. Swati worked as a ResearchFellow and Birbal Sahni Research Associate before joiningas a Scientist. She is also the recipient of the Dr. B.S. Venka-tachala Memorial Medal, 2012, for outstanding research inpalaeobotany. She has 20 research papers published in peer-reviewed journals.

SAMIR K. BERAwas awarded a BSc inbotany from the University of Calcuttain 1976, an MSc in botany from theUniversity of Burdwan in 1978 and aPhD from the University of Lucknow in1989. He is currently a Scientist ‘F’ at theBirbal Sahni Institute of Palaeobotany inLucknow, working on palaeoclimatologyusing Quaternary pollen as a proxy.

Samir has 33 years research experience, and has published 75papers in peer-reviewed journals. He has visited Antarcticatwice, and has supervised several research students.

SUBODH KUMAR was awarded anMSc in physics from Gurukul KangriVishwavidyalaya Haridwar in 1997 andan MPhil in instrumentation from theUniversity of Roorkee (now IITR) in1998. He also received a PhD fromLucknow University in 2013. He is cur-rently working as a Technical Officer‘B’ and is in charge of the scanning elec-

tron microscopy unit in the Birbal Sahni Institute of Palaeo-botany, Lucknow. Subodh Kumar has published threepapers in peer-reviewed journals.

Palynology 331

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