taprobanica (2012) vol. 4. no. 2. pages 60-119

Published date: 14th, November 2012

TAPROBANICA the Journal of Asian Biodiversity ISSN 1800-427X - Volume 04, Number 02, pp. 60-119, Pls. 3.

© 2012, Taprobanica Private Limited, 146, Kendalanda, Homagama, Sri Lanka

- Editor-In-Chief -

THASUN AMARASINGHE

[email protected]

- Deputy Editors –

NIKI AMARASINGHE

[email protected]

MOHOMED BAHIR

[email protected]

SURANJAN KARUNARATHNA

[email protected]

- Associate Editors –

JOHANNA BLEECKER

[email protected]

MADHAVA BOTEJUE

[email protected]

MICHAEL WASSERMAN

[email protected]

- Sectional Editors (Restricted fields included after the names) -

Zoological nomenclature

ALAIN DUBOIS

COLIN GROVES

SVEN KULLANDER

Gastrointestinal parasites

COLIN CHAPMAN

Snails BRENDEN HOLLAND (land)

ARAVIND MADHYASTHA (aquatic)

Branchiopod crustaceans

MIGUEL ALONSO

B. K. SHARMA

Freshwater crabs

MOHOMED BAHIR

Cerambycid beetles

EDUARD VIVES

Geotrupid beetles

OLIVER HILLERT

Odonata

DO MANH CUONG

Orthoptera

HOJUN SONG

Hymenoptera

MICHAEL ENGEL

VOLKER LOHRMANN

Lepidoptera & other insect groups

JEFFREY MILLER

Fish taxonomy

SVEN KULLANDER

Fish ecology

UPALI AMARASINGHE

REMADEVI

SUJAN HENKANATHTHEGEDARA

Amphibian taxonomy

FRANKY BOSSUYT

BIJU DAS

DJOKO ISKANDAR

ENRIQUE LA MARCA

KELUM MANAMENDRA-ARACHCHI

JODI ROWLEY

Amphibian ecology

JODI ROWLEY

Reptile taxonomy AARON BAUER

DJOKO ISKANDAR

ANDRE' KOCH

RICHARD WAHLGREN

YEHUDAH WERNER

Reptile ecology

RUCHIRA SOMAWEERA

YEHUDAH WERNER

Agamid lizards

NATALIA ANANJEVA

Crocodiles

RUCHIRA SOMAWEERA

RALF SOMMERLAD

NIKHIL WHITAKER

Geckos / skinks / lacertids

AARON BAUER

JOHN RUDGE (Geckos)

Snakes

GERNOT VOGEL

Testudines

UWE FRITZ

HANS-DIETER PHILIPPEN

Varanid lizards

ANDRE' KOCH

Bird taxonomy

BRUCE BEEHLER

Bird ecology

BRUCE BEEHLER

VARADARAJAN GOKULA


SARATH KOTAGAMA

VINCENT NIJMAN (birds of prey)

Mammal taxonomy

COLIN GROVES

Mammal ecology

COLIN CHAPMAN

LEE HARDING

Chiroptera

JUDITH EGER

Primates

COLIN CHAPMAN

VINCENT NIJMAN

JATNA SUPRIATNA

Mammal diseases

COLIN CHAPMAN

Fungi taxonomy

KEVIN HYDE

DON REYNOLDS

RAM K. VERMA

Fungi ecology

RAM K. VERMA

Plant taxonomy

H. KATHRIARACHCHI

Plant ecology

SUDHEERA RANWALA

Plant physiology & biotechnology

PRASAD SENADHEERA

Zoo biogeography

BRENDEN HOLLAND (Snails)

JEFFREY MILLER (Insects)

LAUREN CHAPMAN (Pisces)

RAFE BROWN (Herps)

ANDRE' KOCH (Herps)

ENRIQUE LA MARCA (Herps)

BRUCE BEEHLER (Birds)

COLIN GROVES (Mammals)

General ecology & conservation

LEE HARDING


SARATH KOTAGAMA

ROBERT STUEBING

Zoo-archeology & paleontology

SURATISSA DISSANAYAKE

COLIN GROVES

KELUM MANAMENDRA-ARACHCHI

Geology

ROHAN FERNANDO

Water resources

MOHOMED NAJIM

60 TAPROBANICA VOL. 04: NO. 02

EDITORIAL

Meet the Parasites: genetic approaches uncover new insights in parasitology

With the continual refinement and development of new molecular approaches, the last few years have

witnessed a dramatic increase in the number of parasitological studies using genetics to answer ecological

questions. Particularly, the advent of full genome sequencing holds promise to ``decode all life``, offering

new potential to not only understand, but cure diseases (Butler, 2010). With the over-abundance of

information and the comparable rapidity that these approaches can provide data, ecologists must be more

careful than ever to select tools that suit their objectives and provide the resolution to their data that best fits

their question, not simply the most attractive option. In this vein, Weinberg (2010) acknowledges that the

molecular revolution has allowed a new mentality of “discover now and explain later” to invade research,

and this has placed hypothesis-driven research under threat. However, regardless of potential setbacks that

molecular approaches have introduced into basic research, their contributions to the progression of science

are unquestionably more numerous and far reaching. Here, we discuss six areas where molecular approaches

are useful to ecological parasitologists.

1. Increase the Resolution of Parasite Identification

Perhaps most obviously, molecular approaches allow researchers to sub-type parasites and identify cryptic

taxa. These approaches are extremely valuable when morphological features traditionally used to identify

parasite taxa are limited, as is often the case. DNA-based approaches allow for a direct evaluation of an

organism’s genome, irrespective of environment or ontogeny, and provide absolute rather than relative data

(McManus & Bowles, 1996). This is particularly important in parasites, where morphologically

distinguishable life stages, such as adults, may be unavailable to researchers, such as when hosts are

endangered or otherwise protected from invasive sampling (Criscione et al., 2005). Molecular approaches

are also useful in uncovering cryptic parasite diversity - for example, ribosomal DNA sequencing to identify

that human and pig whipworm infections were caused by separate species (Cutillas et al., 2009), or

mitochondrial DNA sequencing to uncover multiple cryptic avian malaria parasites (Bensch et al., 2004).

2. Discover New Parasites

The recent advent of next generation high-throughput sequencing platforms has revolutionized the way

scientists discover pathogens. Previous technology, such as degenerate PCR, immunoscreening of cDNA

libraries, and microarrays (Wang et al., 2003) provide opportunity to identify new pathogens from existing

families. More recently, panmicrobial oligonucleotide arrays (Greenechips) use oligonucleotides affixed to a

glass slide that represent a diversity of vertebrate pathogens, including viruses, bacteria, fungi, and

helminths, to specifically identify pathogens genetically similar to those on the chip (Palacios et al., 2007).

While still appropriate in many instances, these technologies are still limited by availability of information –

novel, highly divergent, or low parasitaemia/titre pathogens stand little chance of discovery (Kreuze et al.,

2009). Massively parallel approaches circumvent this problem, and have been successful in uncovering and

cataloging the diversity (Liu et al., 2009; Manske et al., 2012), divergence (Lauck et al., 2011), and

evolution of pathogens (Qi et al., 2009).

3. Infer Parasite Transmission

Molecular approaches may also be used to infer how parasites are transmitted, either within or between host

species. Within host species, molecular approaches can be used to elucidate how a parasite’s biology may

affect its transmission (Mackinnon & Read, 1999) or how parasite strains are transmitted in a host population

(Anderson et al., 1995). Interestingly, genetics have also been used to identify transmission heterogeneities

or susceptible demographics in a host species. For example, using microsatellites and random amplified

polymorphic DNA (RAPD), Prugnolle et al. (2002) discovered sex-specific genetic structuring of

TAPROBANICA, ISSN 1800-427X. October, 2012. Vol. 04, No. 02: pp. 60-64.

© Taprobanica Private Limited, 146, Kendalanda, Homagama, Sri Lanka.

EDITORIAL


Schistosoma mansoni, with less genetic differentiation in male hosts than in female hosts. Between host

species, direct PCR and sequencing and RAPD, respectively, have been used to identify cross-species

transmission of avian blood parasites (Waldenström et al., 2002) and primate nodular worms (de Gruijter et

al., 2004) in complex communities where host specificity was not possible to determine through

morphological comparison. Further, with several influential publications suggesting that the number of

emerging infectious diseases have rapidly increased in recent times (Daszak et al., 2000; Jones et al., 2008),

and that many, such as HIV-1 (Gao et al., 1999) and HIV-2 (Gao et al., 1992; Wertheim & Worobey,

2009b), influenza (Subbarao et al., 1998; Webster et al., 2006), and Ebola (Leroy et al., 2009) are caused by

zoonotic pathogens (i.e., pathogens transmissible from wildlife to humans), researchers have turned to

molecular approaches to uncover transmission events from wildlife to humans. For example, Wolfe et al.

(2004) demonstrated that bushmeat hunters in direct contact with wild non-human primate body fluids were

infected with simian foamy viruses arising from three different non-human primate species, which suggests

that human contact with wildlife has allowed these retroviruses to actively cross into human populations.

Finally, a re-emerging discipline, spatial epidemiology, considers how transmission is affected by space

(Ostfeld et al., 2005). In considering landscape, this discipline can track the movement of hosts and parasites

over different spatial scales, and therefore identify where and why parasites move across heterogeneous

environments. Research in this field has effectively identified barriers to the transmission of infectious

diseases, and can be used to predict the evolution and spread of pathogens, as well as the susceptibility of

interconnected host populations (Archie et al., 2009; Smith et al., 2002). While the addition of genetics to

spatial epidemiology has been rare to date, it has allowed researchers to resolve the mechanisms behind

adaptive differentiation and parasite evolution in the context of a landscape. For example, Biek et al. (2007)

used genetic approaches to reconstruct the spatial and demographic spread of rabies virus following its

introduction into a susceptible population.

4. Identify Disease Origins

Not only can molecular approaches be used to understand the phylogenetic relationships among extant

parasites, but they can be used to infer their origins. The origins of some of the world’s most serious

infectious diseases have now been determined, such as HIV-1 (Gao et al., 1999) and Plasmodium

falciparum. In the case of the latter, Liu et al. (2010) collected feces from chimpanzees (Pan troglodytes),

western gorillas (Gorilla gorilla), eastern gorillas (Gorilla beringei), and bonobos (Pan paniscus) to isolate

Plasmodium and identify the origins of the most pathogenic form of human malaria, P. falciparum. Their

results show that P. falciparum is nearly identical to isolates from western gorillas and that these species

form a monophyletic group. This suggests that human P. falciparum likely arose via a single jump from

western gorillas to humans. This example not only provides evidence for how one may use molecular

approaches to identify the origins of parasites, but also highlights how the continual improvement of

molecular methods, such as from conventional (bulk) PCR (Escalante et al., 1995; Rich et al., 2009), to

single genome amplification (which dilutes template DNA to avoid the generation of recombinants during

PCR), may not only increase resolution, but change the interpretation of results. Finally, genetic information

can also be used to determine time since divergence and rate of evolution of a given parasite. For example,

Wertheim & Worobey (2009) used a Bayesian relaxed molecular clock to date the ages of the SIV lineages

that gave rise to HIV-1 and 2. Results suggest that the SIV lineage is surprisingly young for a retrovirus, and

that the HIV-1 group M and N share a most recent common ancestor with SIVcpz, its progenitor, in 1853

and 1921 – a useful estimate of when this virus may have jumped into human populations.

5. Understand Virulence

The majority of laboratory-based studies in parasitology attempt to understand parasite virulence. Genetic

approaches that elucidate variations in parasite strain (Mackinnon & Read, 1999) and host immunological

factors (Merrick et al., 2012) are both essential to understanding parasite virulence, and have been

instrumental in the success of this burgeoning field (Pedersen & Babayan, 2011). Recently, studies of co-

infection, which examine the result of multiple parasites invading a single host and the corresponding

immunological response, have garnered interest. One of the first to examine co-infection in populations of

wild animals was Ezenwa et al. (2010), who demonstrated that helminth infection in African buffalo

(Syncerus caffer) facilitates tuberculosis infection by supressing the microparasitic Th1 response.

EDITORIAL


6. Elucidate Host Ecology

While many researchers have used host ecology (e.g., behaviour, habitat use, foraging strategy) to explain

parasite genetic diversity, we can also use parasite genetic diversity to explain host ecology. Mackenzie

(2002) reviews how parasites can be used as biological tags in a variety of marine organisms, since

populations of a given species that experience different environmental conditions may acquire specific

parasites that can then be used for identification and tracking. Indeed, research by Criscione et al. (2006)

determined that genotyping the trematode parasites of steelhead trout (Oncorhynchus mykiss) was four times

more effective in correctly assigning the fish to its population of origin than genotyping the fish itself. In

terrestrial systems, pathogens such as the gastric bacterium Helicobacter pylori have been used to track

human migration through sequencing strain variation that replicate colonization events. The use of parasites

as tags has also recently been applied to wildlife populations. Biek et al. (2006) suggests that rapidly

evolving viruses are a useful tool in studying the population dynamics of their hosts. Using feline

immunodeficiency virus (FIV), they constructed the spatial ranges of the host (Puma concolor) in more

detail than host microsatellite analysis of the host could uncover. This suggests that such rapidly evolving

parasites are useful in characterising host population dynamics in what they termed “shallow” time.

Conclusions

While not being exhaustive, we have tried to highlight key ways in which natural historians and ecologists

can use genetic approaches to increase the resolution with which they can answer their questions. Pairing and

collaboration between field and molecular experts is becoming more and more frequent, and we believe this

to be a significant step forward in understanding parasitology in complex ecosystems.

Acknowledgements

We gratefully acknowledge the thoughts and suggestions provided by D. R. Mills and T. L. Goldberg on this

editorial.

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Ria R. Ghai1 & Colin A. Chapman

2*

*Sectional Editor: Taprobanica, the journal of Asian Biodiversity

August 12th, 2012

1 Department of Biology, McGill University

1205 Docteur Penfield, Montreal, Quebec, H3A 1B1

CANADA

2 McGill School of Environment & Department of Anthropology

McGill University, Montreal, Quebec, H3A 2T7

CANADA

64


DESCRIPTION OF A NEW GENUS OF INDIAN SHORT-TAILED

WHIP-SCORPIONS (SCHIZOMIDA: HUBBARDIIDAE) WITH NOTES

ON THE TAXONOMY OF THE INDIAN FAUNA

Sectional Editors: James Cokendolpher & Mark Harvey Submitted: 23 July 2012, Accepted: 24 Sept. 2012

Mandar L. Kulkarni

‘Aashirvad’, L. I. C. Colony-2, Near Rajiv Gandhi School, Latur- 413512, Maharashtra, India

E-mail: [email protected]

Abstract

Indian hubbardiids which were recently described but had doubtful generic placements are revised.

The new genus Gravelyzomus is described here for Schizomus chalakudicus Bastawade, 2002. A new

combination is proposed for Schizomus chaibassicus Bastawade, 2002 which is newly transferred to

the genus Burmezomus.

Key words: Gravelyzomus, Burmezomus chaibassicus, Arachnida, taxonomy, India.

Introduction

The Indian species of the arachnid order

Schizomida are very poorly characterized and

represented by only six species: Tritheryus

sijuensis Gravely, 1925; Ovozomus lunatus

(Gravely, 1911); “Schizomus” kharagpurensis

Gravely, 1912; Schizomus chaibassicus

Bastawade, 2002; Schizomus chalakudicus

Bastawade, 2002; and Neozomus tikaderi

Cokendolpher, Sissom & Bastawade, 1988. The

first effort to study Indian schizomids was by F.

H. Gravely who collected schizomids from

India and surrounding countries, while

Bastawade (1985, 1992, 2002, 2004) worked

on Gravely’s collection and described a few

new species. Recently, Harvey (2011)

transferred Schizomus lunatus to Ovozomus due

to unusual morphology of female genitalia.

Bastawade (2004) studied some species

deposited by Gravely in the Zoological Survey

of India (ZSI), and redescribed six species

using criteria developed by Reddell &

Cokendolpher (1995), of which only two

species were reported from India. Although

preparing thorough descriptions, Bastawade

(2002, 2004) maintained these species within

the genus Schizomus and placed the generic

name in inverted commas to indicate the

uncertainty of the placement of the species in

combination with the genus as given in Reddell

& Cokendolpher (1995). The descriptions

provided by Bastawade (2002) provided

illustrations of the propeltidium, pedipalp,



A NEW GENUS OF INDIAN SHORT-TAILED WHIP-SCORPIONS


female flagellum, spermatheca and gonopod,

and the descriptions are generally detailed

allowing comparison with other described

material of the order. Reddell & Cokendolpher

(1991) redescribed Schizomus crassicaudatus

O. Pickard-Cambridge, the type species of the

genus Schizomus, and hence provided strong

evidence to recognize and circumscribe this

genus (see Reddell & Cokendolpher, 1991).

This particular clarification provides many

opportunities to compare the available data and

recognize its placement of many species under

given genera. I have visited the museum of

ZSI-Kolkata where the type specimens of the

Indian schizomids were deposited.

Unfortunately the specimens could not be

located there. Therefore, I have been forced to

rely on the original descriptions and

illustrations provided by Bastawade (2002,

2004). This study was designed to attempt to

review the Indian schizomid fauna and

establish whether they could be assigned to

existing genera, based on the criteria developed

by Reddell & Cokendolpher (1995).

Family Hubbardiidae Cook, 1899

Gravelyzomus new genus

Type species: Schizomus chalakudicus

Bastawade, 2002.

Diagnosis: The new genus Gravelyzomus

differs from other Indian genera of order

Schizomida by a combination of the following

characters. Anterior process of propeltidium

with a single median seta and pair of basal

setae i.e. arranged in 1+2 manner; eye spots

absent; metapeltidium divided. Pedipalpal

trochanter without median spur, patella smooth

and without any spur on ventro-lateral surface.

Abdominal tergites and sternites smooth;

setation not known for certain, except for dorsal

median pair of setae on tergites I-IV. Flagellum

with three segments, only lateral and dorsal pair

of setae present on last annulus. Spermathecae

tubuliform, with many irregular tubes.

Etymology: This genus is named after F. H.

Gravely for his contributions to Indian

arachnology, and the generic name Zomus. The

gender is masculine.

Description: Cephalothorax: Acutely pointing propeltidum

bending forward with pair of basal setae, a

median seta and three pairs of dorsal median

setae. Sternal setae unclear.

Abdomen: Both sternite and tergite without

clear setation. Flagellum three segmented.

Spermathecae tubiliform, with many irregular

tubes on each side.

Chelicerae with basal segment wide, movable

finger without any teeth except for a single

rounded tooth at distal end, immovable finger

with three sharp teeth. Pedipalp with roughly

triangular trochanter, with 5-6 spinose setae on

exterior ventral margin, femur rounded with

inner knob.

Distribution: Chalkudi, near Cochin, Kerela,

India

Remarks: The phylogenetic relationship of

Indian schizomids is not clear yet, so far this

genus shows similarity with some Old World

genera like Ovozomus and Trithyreus by having

a divided metapeltidium, arrangement of setae

on anterior process but differs by the spination

on the abdominal tergites which are smooth in

Gravelyzomus, and the structure of the

spermathecae are also different i.e. spermatheca

in Gravelyzomus has numerous lobes and

irregular shaped gonopod.

Gravelyzomus chalakudicus (Bastawade,

2002), new combination Schizomus chalakudicus Bastawade, 2002: 90-91,

figs 1-13.

Holotype: ZSI (uncatalogued); adult female

(5.59 mm TL); Chalkudi, near Cochin, Kerela,

India; F. H. Gravely; 14-30 September 1914

(not examined).

Distribution: Chalkudi, near Cochin, Kerela,

India. This species is known only from the type

and no live population found during our field

visits to the type locality.

Remarks: The holotype is currently lost or has

been borrowed by a previous worker and not

returned to the museum. The illustration of the

spermatheca by Bastawade (2002) shows

numerous irregular lobes on each side and a

gonopod that is irregular in shape. The current

placement of this species in Schizomus cannot

be maintained, as the structure of spermathecae

KULKARNI, 2012


and the pedipalp differ from that of Schizomus

(Reddell & Cokendolpher, 1991). The

spermathecal morphology does not match any

known genus of the order; hence I here include

this species in the new genus Gravelyzomus.

Genus Burmezomus Bastawade, 2004

Diagnosis: The genus Burmezomus differs

from other Indian schizomid genera by a

combination of the following characters.

Propeltidium bent beak-like anteriorly with

either 3 (median seta and pair of basal setae) or

2 (a pair of basal setae), dorsal setation not

clear; eye spots absent; metapeltidium is

medially separated by a suture or entire.

Pedipalp patella with three spinous setae on

ventral margin. Female flagellum with 1-3

annuli. Spermathecae with an uneven number

of band-like structures, gonopod short.

Burmezomus chaibassicus (Bastawade, 2002),

new combination Schizomus chaibassicus Bastawade, 2002: 92, figs

14-26.

Holotype: ZSI (uncatalogued); adult female

(6.10 mm TL); Pass between Chaibass and

Chakradharpur, Chota Nagpur, Bihar, India; P.

E. Gravely; 1 October 1919 (not examined).

Distribution: Pass between Chaibass and

Chakradharpur, Chota Nagpur, Bihar, India.

This species is known only from the type and

no live population found during our field visits

to the type locality.

Remarks: The holotype is currently lost or has

been borrowed by a previous worker and not

returned to the museum. The original

description of this species (Bastawade, 2002)

was based upon a single female. The major

characteristics, however, do not match with the

diagnostic characters of the genus Schizomus

(see discussion above). In particular, the

structure of the female spermathecae differs

from Schizomus, i.e. in the form of elongated

lobes and in a cluster of 8-10. The female

spermathecae more closely resemble the genital

structure of Burmezomus Bastawade, 2004.

Hence, Schizomus chaibassicus is hereby

transferred from Schizomus to Burmezomus.

“Schizomus” kharagpurensis Gravely, 1912 Schizomus (Trithyreus) kharagpurensis Gravely,

1912: 108, 109-110, fig. C.

Trithyreus kharagpurensis (Gravely): Giltay, 1935:

7

Distribution: Kharagpur, West Bengal, India.

Remarks: The type specimen could not be

located in the ZSI collection and is either lost

or loaned to a previous worker and never

returned to the museum. So this particular

species is retained under the genus

“Schizomus”.

Table 1: Diagnostic characters of some Indian Hubbardiidae based on original descriptions

Gravelyzomus

chalakudicus

Ovozomus

lunatus

Neozomus

tikaderi

Trithyreus

sijuensis

Burmezomus

chaibassicus

Female flagellum,

number of segments 3 3 3 2? 1 to 3

Gonopod shape Irregular Short and

unequal size

Short and

rounded

Elongated

lobes Elongated and lobate

Number of

spermathecal lobes

Numerous

lobes Four pairs

Three to five

on each side Two pairs Eight to Nine lobes

Anterior setae on

metapeltidium* 1+2 1+2 2+1 2+1 1+2/0+2

Metapeltidium Divided Divided Entire Divided Entire

Pedipalpal

trochanter Without spur

Without

spur Without spur ?

With or Without

spur

Corneate eyes Eyespots absent Eyespots

absent Eyes present

Eyespots

absent

Inconspicuous

eyespots present

Pedipalp sexually

dimorphic

Male not

known

Sexually

dimorphic

Sexually

dimorphic

Male not

known Male not known

* First digit denotes number of setae on anterior most part of metapeltidium followed by number of setae

located behind that.


Acknowledgements

I am thankful to Lorenzo Prendini and

Adalbarto Santos for their comments on first

draft. I am grateful to K. Venkatraman

(Director - ZSI) for providing access to ZSI,

also Basudev Tripathi and Sankar Talukdar

(ZSI) for all help at ZSI-Kolkata. I would also

like to thank Nikhil Bhopale (BNHS, Mumbai)

and Kruti Chhaya (CES, Banglore) for sharing

literature.

Literature cited Bastawade D. B., 1985. The first report of the

order Schizomida (Arachnida) from Southern

India. Journal of the Bombay Natural History

Society, 82 (3): 689-691.

Bastawade D. B., 2002. Two new species of

schizomids from India with range extension for

Schizomus tikaderi (Arachnida: Schizomida).

Journal of Bombay Natural History Society, 99

(1): 90-95.

Bastawade D. B., 2004. Revision of some species

of family Schizomidae (Arachnida: Schizomida)

on the basis of types deposited by F. H. Gravely

(1911-1925) in the National Collection, ZSI,

Kolkata. Journal of the Bombay Natural History

Society, 101 (2): 211-220.

Bastawade D. B. and T. K. Pal, 1992. First record

of the arachnid order Schizomida from Arunachal

Pradesh, India. Journal of the Bombay Natural

History Society, 89 (1): 137.

Cokendolpher J. C., D. W. Sissom and D. B.

Bastawade, 1988. A new Schizomus of Indian

state of Maharashtra, with additional comments

on eyed schizomids (Arachnida: Schizomidae).

Insecta Mundi, 2 (2): 90-96.

Giltay L. 1935. Notes arachnologiques africaines.

VII. Description d’um Pѐdipalpe nouvaeu du

Congo belge (Trythyreus ghesquierei, n. sp.).

Bulletin du Musѐe Royal d’Histoire Naturelle de Belgiue, Bruxelles, 11 (32): 1-8

Harvey M. S., 2011. Notes on some Old World

schizomids of genera Ovozomus and Schizomus

(Schizomida: Hubbardiidae). Records of the Western Australian Museum, 26: 202-208.

Reddell J. and J. Cokendolpher, 1991.

Redescription of Schizomus crassicaudatus (Pickard-Cambridge) and diagnoses of Hubbardia

Cook, Stenochrus Chamberlin and

Sotanostenochrus new genus, with description of

a new species of Hubbardia from California

(Arachnida: Schizomida: Hubbardiidae). Texas Memorial Museum, Pearce-Sellards Series, 47: 1-

24.

Reddell J. and J. Cokendolpher, 1995. Catalogue,

bibliography and generic revision of the order

Schizomida (Arachnida). Texas Memorial

Museum, Speleological Monographs, 4: 1-170.

68


BOLBOCERATINE SCARABS OF GENERA Bolbohamatum KRIKKEN,

1980 AND Bolbogonium BOUCOMONT, 1911 (COLEOPTERA:

GEOTRUPIDAE) FROM CENTRAL INDIA

Sectional Editor: Oliver Hillert Submitted: 26 March 2012, Accepted: 26 July 2012

Kailash Chandra1 and Devanshu Gupta

2

1 Zoological Survey of India, New Alipore, Kolkata 700053, West Bengal, India

E-mail: [email protected] 2 Zoological Survey of India, Jabalpur 482002, Madhya Pradesh, India


Abstract

This study includes a taxonomic account of four species of genus Bolbohamatum; B. calanus

(Westwood, 1848), B. phallosum Krikken, 1980, B. marginale Krikken, 1980 and B. laterale

(Westwood, 1848) and one species of genus Bolbogonium; B. insidiosum Krikken, 1977 from Central

India (Madhya Pradesh and Chhattisgarh). The pronotal ornamentation and external male genitalia of

Bolbohamatum species has been diagnosed with the incorporation of an identification key to the

species from Central India. A checklist containing 19 Indian species of both genera (Bolbohamatum

and Bolbogonium) has also been prepared with their distribution in different states of India as well as

outside of India.

Keywords: dung beetles, pronotal ornamentation, external male genitalia, distribution, India.

Introduction

Bolboceratine scarabs in the family

Geotrupidae are commonly called Earth-boring

dung beetles because adults of most species

provision larvae in earthen burrows with dead

leaves, cow dung, horse dung, or humus. The

family Geotrupidae currently includes 620

species belonging to 68 genera in three

subfamilies; Taurocerastinae, Bolboceratinae

and Geotrupinae (Scholtz & Browne, 1996).

The first comprehensive study of Asian

Bolboceratinae was carried out by Westwood

(1848, 1852), which considered 29 species to

be in one genus Bolboceras. Later, several new

species names were added based on the

materials from tropical and eastern Asia.

Boucomont (1911) proposed Bolbogonium as a

subgenus for Bolboceras. A series of

taxonomic publications on Asian

Bolboceratinae were then made by Krikken

(1977ab, 1978ab, 1979, 1980, 1984), Carpaneto

et al. (1993), Masumoto (1984), Li et al.

(2008), Nikolajev (1979ab, 2003, 2008), Ochi



BOLBOCERATINE SCARABS OF CENTRAL INDIA


& Kawahara (2002), Ochi & Masumoto (2005)

and Ochi et al. (2010, 2011). Krikken (1977a,b)

raised the subgenus Bolbogonium to the genus

level and described seven new species, along

with producing a key to all ten Asian species.

Subsequently, Krikken (1980) proposed the

genus Bolbohamatum for four species to be

combined with Bolboceras, while also

describing nine new species and discussing the

significance of external male genitalia and

pronotal ornamentation in the accurate

identification of the various species. Recently,

Karl et al. (2006) catalogued Bolboceratine

scarabs of the Palaearctic region. The present

study includes taxonomic information for four

species of Bolbohamatum and one species of

Bolbogonium from the Madhya Pradesh and

Chhattisgarh states in India and also

incorporates new distributional records of these

beetles. A checklist of both genera from India

is included.

Materials and methods

Specimens for the study were collected using

light trap from various protected areas by

scientific teams of ZSI based in Jabalpur,

Madhya Pradesh. Pinned specimens were

identified with the help of available taxonomic

revisions of the studied genera (Krikken,

1977b, 1980). Specimens were examined under

a binocular microscope (Leica M205 A) and

photographs were taken with the help of an

attached digital camera. Male specimens were

dissected, with the abdomen separated from the

body and the aedeagus extracted from the

abdomen. The genitalia were then cleaned and

softened in a dish of hot water and further

cleaned in a hot water solution of 10% KOH.

All parts of the aedeagus were washed in 95%

ethanol and photographed. After examination,

the genitalia were stored in a glass vial

containing 70% ethanol.

The details of specimens examined, registration

number of specimens, distribution inside and

outside India, main diagnostic characters,

description, illustration of external male

genitalia, and identification key to the species

level within the genus Bolbohamatum are

provided. The classification adopted in the

article is after Smith (2006). Identified

specimens were deposited in ZSI, Jabalpur,

Madhya Pradesh (India).

Results and Discussion

Four species of the genus Bolbohamatum; B.

calanus (Westwood 1848), B. phallosum

Krikken 1980, B. marginale Krikken 1980 and

B. laterale (Westwood 1848) and one species

of genus Bolbogonium; B. insidiosum Krikken

1977 were studied from the states Madhya

Pradesh and Chhattisgarh. Bolbohamatum

calanus, B. laterale and B. phallosum are

recorded for the first time from Madhya

Pradesh, while Bolbohamatum marginale and

B. calanus constitute new reports for

Chhattisgarh. The identification of these

species is based on the structure of external

male genitalia, pronotal ornamentation and

clypeal dentations, which are shown in figures

1 to 9. Bolbogonium insidiosum shows

variations in the structure of clypeofrons (Fig.

9). The checklist for 19 Indian species of both

Bolbohamatum (11 species) and Bolbogonium

(8 species), along with their distribution within

and outside of India, are provided in Table 1.

Systematic Account

Family: Geotrupidae Latreille, 1802

Subfamily: Bolboceratinae Mulsant, 1842

Tribe: Eubolbitini Nikolajev, 1970

Genus Bolbohamatum Krikken, 1980 Bolbohamatum Krikken, 1980: 5 (Type species:

Scarabaeus cyclops Olivier, 1789: 60)

The genus includes the species, presenting one

of the largest Bolboceratine scarabs which are

distributed in both the Palaearctic and Oriental

geographic regions. It likely evolved on the

Indian subcontinent and spread at a relatively

late stage through Myanmar into Sundaland and

China (Krikken, 1980).

Generic diagnosis: Metasternum anterroiorly

always with a small spiniform protrusion and

with anterior lobe narrowly separating middle

coxae. Head of males with a pair of tubercles

on clypeus. Pronotum in case of male possess

median and lateral protrusions with the surface

between them usually concave. Fore tibia with

7-10 external denticles.

CHANDRA & GUPTA, 2012

XX TAPROBANICA VOL. 04: NO. 02

Identification key to the species of Bolbohamatum Krikken, 1980 from Central India:

1. Lateral tubercles of pronotum well developed but not marginally situated. Apex of parameres

not with reflexed paramerites …………………...………………………...………………….. 2

Lateral tubercles of pronotum well developed or completely reduced or absent if present then

marginally situated. Apex of parameres dorsally with short reflexed paramerites

…………………………………………………..……………………….……………………. 3

2. Dorsally the parameres moderately sclerotized, relatively narrow and with poorly developed

paramerite. Ventral side of parameres devoid of distinct paramerites. Basal capsule relatively

narrow ………………………………………...……..……………….. Bolbohamatum calanus

Dorsally the parameres foliate and ventrally with a pair of more or less glider-like

paramerites. Basal capsule in lateral view distally strongly emarginated ……………...………

…………………………………………….……………………….. Bolbohamatum phallosum

3. Paramedian tubercles of pronotum closely approximated and separated by less than to inter-

ocular distance while lateral tubercles well developed and marginally situated

……………………………………………………..…………….…. Bolbohamatum marginale

Paramedian tubercles of pronotum not closely approximated and separated by more than

inter-ocular distance while lateral tubercles absent ………………….. Bolbohamatum laterale

Bolbohamatum calanus (Westwood, 1848) Bolboceras calanus Westwood, 1848a: 385,

(description, distribution).

Bolboceras tumidulus Westwood, 1852: 22,

(description, distribution, illustration).

Bolbohamatum calanus Krikken, 1980: 20,

(description, keyed, distribution, illustration, comb.

nov.).

Specimens examined: Chhattisgarh:

ZSI/CZRC-A/16601; male (Length: 15.0 mm;

width: 10.0 mm); Barnavapara camp,

Barnavapara Wildlife Sanctuary, Raipur (21o

24.00’ N, 82o

25.314’ E; alt. 303.8 m); K.

Chandra & party, 01 July 2011, light trap.

Madhya Pradesh: ZSI/CZRC-A/16602; male

(Length: 16.0 mm; width: 9.0 mm); Forest Rest

House, Bandhavgarh National Park, Umaria, K.

Chandra, 10 August 2005, light trap;


width: 9.0 mm), Karmajhiri, Pench Tiger

Reserve, Seoni; K. Chandra, 13 June 2001.

Diagnosis: (Fig. 1). Brown, shiny and pilosity

yellow brown. Cephalic tubercles more or less

dentiform, isolated and placed simply on

clypeal disc. Dorsal outline of left mandible

sinuate lobate. Pronotum with a pair of feebly

developed, slightly transverse median tubercles

with lateral callosities. Pronotum abundantly

punctate, but never densely punctate

throughout. Paramedian tubercles separated by

less than inter-ocular distance. Lateral

impression of pronotum shallow.

Figure 1: B. calanus (scale: 5 mm), ZSI/CZRC-

A/16601, Barnawapara Wildlife Sanctuary, 2011.

External male genitalia: (Fig. 2) Dorsally, the

parameres moderately sclerotized, relatively

narrow and with poorly developed paramerite

while the ventral side of parameres devoid of

distinct paramerites. Basal capsule relatively

narrow.

Geographical distribution: India: Assam,

Bihar, Chhattisgarh, Karnataka, Madhya

71



Pradesh, Maharashtra, Tamil Nadu, West

Bengal and Uttarakhand. Elsewhere:

Bangladesh and Java.

New state and district record: Chhattisgarh

(Raipur) and Madhya Pradesh (Umaria and

Seoni).

Figure 2: Dorsal & ventral view of external male

genitalia of B. calanus (scale: 2 mm), ZSI/CZRC-

A/16601.

Bolbohamatum phallosum Krikken, 1980 Bolbohamatum phallosum Krikken, 1980: 21,

(description, keyed, distribution, illustration).

Specimens examined: Madhya Pradesh:


width: 9.0 mm); Turiya, Pench Tiger Reserve,

Seoni; K. Chandra, 23 June 2001; light trap;


width: 11.0 mm); Kisli Rest House, Kanha

National Park, Mandla; M. Limje & party, 13

September 2003; light trap; ZSI/CZRC-

A/16780; male (Length: 16.0 mm; width: 10.0

mm); Kisli Rest House, Kanha National Park,

Mandla; M. Limje & party; 09 September

2003.

Diagnosis: (Fig, 3). Brown, shiny and pilosity

yellow brown. Clypeus with a pair of dentiform

tubercles. Pronotum with closely approximated

paramedian tubercles and lateral protrusion not

shifted to antero-lateral corner. Juxtasutural

punctures of elytra sub obsolete and discal

striae shallowly impressed and finely punctate.

Elytral inter-striae very slightly convex and

minutely and sparsely punctured.

External male genitalia: (Fig. 4) Dorsally,

parameres foliate and ventrally with a pair of

more or less glider-like paramerites. In lateral

view, the basal capsule distally strongly

emarginated.

Geographical distribution: India: Madhya

Pradesh, Maharashtra and East India.

New state and district record: Madhya Pradesh

(Seoni and Mandla).

Remarks: B. calanus (Westwood, 1848) and B.

phallosum Krikken, 1980 show close

resemblance in their morphological characters

and cannot be separated on the basis of external

characters only, but the phalli of both the

species are very different and only the

characters of the phallus distinguish both the

species.

Figure 3: B. phallosum (scale: 5 mm), ZSI/CZRC-

A/16604, Pench Tiger Reserve, 2001.


genitalia of B. phallosum (scale: 2 mm), ZSI/CZRC-

A/16604.

Bolbohamatum marginale Krikken, 1980 Bolbohamatum marginale Krikken, 1980: 30,


Specimens examined: Chhattisgarh:


72



width: 9.0 mm); Ataria Forest House,

Amarkantak Biosphere Reserve, Bilaspur; A.

Singh & party; 18 April 2004; light trap.

Madhya Pradesh: ZSI/CZRC-A/16600; male

(Length: 15.0 mm; width: 9.0 mm); Kisli,

Kanha National Park, Mandla; M. Limje &

party, 13 September 2003; light trap.

Diagnosis: (Fig. 5). Dorsal outline of left

mandible lobate. Clypeus with a pair of

dentiform tubercles each placed against lateral

margin. Pronotum with strongly approximated

paramedian tubercles and a pair of lateral

tubercles situated almost marginally. Median

longitudinal zone and lateral declivities of

pronotum densely and coarsely punctured while

impression between paramedian and lateral

tubercles virtually devoid of punctures and

opaque. Fore tibia with seven external

denticles.

Figure 5: B. marginale (scale: 5 mm), ZSI/CZRC-

A/16599, Amarkantak Biosphere Reserve, 2004.

External male genitalia: (Fig. 6) Parameres

reduced and basal capsule enlarged. Basal

capsule of the phallus very robust in

comparison to B. laterale (Westwood, 1848)

and B. kuijteni Krikken, 1980.


genitalia of B. marginale (scale: 2 mm), ZSI/CZRC-

A/16599.

Remarks: The species can be easily

distinguished from its close relatives in having

pronotal lateral tubercles situated almost

marginally and very closely approximated

paramedian tubercle.

Geographical distribution: India: Chhattisgarh,

Madhya Pradesh, Tamil Nadu, Karnataka and

Uttarakhand. Elsewhere: West Pakistan.

New state and district record: Chhattisgarh

(Bilaspur) and Madhya Pradesh (Mandla).

Bolbohamatum laterale (Westwood, 1848) Bolboceras lateralis Westwood, 1848: 385

(description, distribution).

Bolbohamatum laterale, Krikken, 1980: 33,

(description, keyed, distribution, illustration, comb.

nov.)


ZSI/CZRC-A16730; male (Length: 19.0 mm;

width: 12.0 mm); Sitapar, Singhori Wildlife

Sanctuary, Raisen; D. K. Harshay, 16

September 2009; day collection.

Diagnosis: (Fig. 7) Cephalic tubercles

dentiform and placed on lateral margins.

Paramedian tubercles of pronotum well

separated by more than inter ocular distance.

Lateral tubercles almost absent. Median cavity

of pronotal disc absent. Punctation on pronotal

disc abundant. Front tibia with eight denticles.

Figure 7: B. laterale (scale: 5 mm), ZSI/CZRC-

A/16730, Singhori Wildlife Sanctuary, 2009.

External male genitalia: (Fig. 8) Apex of

parameres dorsally with short reflexed

paramerites. Basal capsule of phallus is robust

but not too much extant as of B. marginale

Krikken, 1980.

Geographical distribution: India: Assam,

Maharashtra, Madhya Pradesh, Jammu &

Kashmir and Karnataka.

New state and district record: Madhya Pradesh

(Raisen).

73



Remarks: The species can be easily

distinguished from its close members, B.

marginale Krikken, 1980 and B. kuijteni

Krikken, 1980 having only one pair of lateral

pronotal protrusions and abundantly punctate

pronotum.


genitalia of B. laterale (scale: 2 mm), ZSI/CZRC-

A/16730.

Tribe: Bolbelasmini Nikolajev, 1996

Genus Bolbogonium Boucomont, 1911 Bolbogonium Boucomont, 1911: 340 (as subgenus

of Bolboceras Kirby; Type species: Bolboceras

triangulum Westwood, 1852: 342).

Bolbogonium Krikken, 1977: 79 (stat. nov.).

Generic diagnosis: Middle coxae widely

separated by an anterior lobe of pyriform

metasternal disc. First antennal club segment

on proximal side shiny and glabrous distinctly

separated from surrounding pubescent surface.

Seven elytral striae between elytral suture and

humeral umbone and all virtually reaching

base.

Bolbogonium insidiosum Krikken, 1977 Bolbogonium insidiosum Krikken, 1977: 95,



ZSI/CZRC-A/16605; male (Length: 9.0mm &

width: 5.5mm); Kartoli, Singhori Wildlife

Sanctuary, Raisen (23o

11.200’ N, 78o

12.085’

E); S. S. Talmale; 13 December 2010;

ZSI/CZRC-A/16778; male (Length: 8.0mm &

width: 5.0mm); Bhamori rest house, Singhori

Wildlife Sanctuary, Raisen; S. Sambath &

Party; 17 September 2011; day collection.

Diagnosis: (Fig. 9 a, b) Yellowish brown, shiny

and pilosity yellowish. Clypeal surface regulate

punctate. Frons with three small isolated

tubercles between eye-canthi. Vertex with large

U shaped, sparsely punctate impression.

Pronotum with anterior declivity impressed and

punctation generally sparse. Scutellum finely

punctate. Elytral striae deeply impressed well

defined and with large punctures. Elytral stria

two extending further caudad. Front tibia with

8-9 denticles.

Geographical distribution: India: Madhya

Pradesh, Maharashtra, Tamil Nadu and Uttar

Pradesh.

New district record: Madhya Pradesh (Raisen).

Remarks: The species shows variation in the

shape of clypeus, ornamentation of frons and

vertex. (Fig. 9 a, b).

Figure 9: Variation of B. insidiosum (scale: 2 mm),

ZSI/CZRC-A/16605 & 16778, Singhori Wildlife

Sanctuary, 2010 & 2011.

74



Table 1: Checklist of genera Bolbohamatum and Bolbogonium from India

Name of the species Distribution

India (states) Elsewhere

Genus Bolbohamatum Krikken, 1980

B. cyclops (Olivier, 1789) Bihar, Himachal Pradesh, Madhya Pradesh, New

Delhi, Uttarakhand, Uttar Pradesh and West Bengal Nepal

B. calanus (Westwood, 1848)

Assam, Bihar, Chhattisgarh, Karnataka, Madhya

Pradesh, Maharashtra, Tamil Nadu, West Bengal

and Uttarakhand

Bangladesh

and Java

B. phallosum Krikken, 1980

Chhattisgarh, Maharashtra and Madhya Pradesh

B. pseudogrande Krikken, 1980

Assam and Himachal Pradesh

B. robustum Krikken, 1980 Himalayan Region

B. laevicolle (Westwood, 1848) Assam, Maharashtra, Orissa and Himalayan Region Bangladesh

B. pyramidifer Krikken, 1980 Orissa

B. meridionale Krikken, 1980 Puducherry

B. marginale Krikken, 1980

Chhattisgarh, Madhya Pradesh, Tamil Nadu,

Karnataka and Uttarakhand Pakistan

B. kuijteni Krikken, 1980 Maharashtra

B. laterale (Westwood, 1848) Maharashtra, Madhya Pradesh, Sikkim, Jammu &

Kashmir, Karnataka and West Bengal

Genus Bolbogonium Boucomont, 1911

B. bicornutum Krikken, 1977 West Bengal

B. howdeni Krikken, 1977 Bihar Pakistan

Afghanistan

B. impressum (Wiedemann, 1823) Himachal Pradesh and Uttarakhand Bangladesh

B. insidiosum Krikken, 1977 Karnataka, Madhya Pradesh, Maharashtra, Tamil

Nadu and Uttar Pradesh

B. davatchii (Baraud, 1973) Jammu & Kashmir, Himachal Pradesh, Uttar

Pradesh and Uttarakhand

Iran

(Nikolajev,

2008)

B. punctatissimum (Westwood, 1852) Uttar Pradesh

B. scurra Krikken, 1977 Tamil Nadu

B. triangulum (Westwood, 1852)

Andhra Pradesh, Bihar, Madhya Pradesh, Himachal

Pradesh, Uttar Pradesh, Uttarakhand and West

Bengal

Myanmar,

Bangladesh

Pakistan

Acknowledgements

The authors are thankful to K. Venkataraman

(Director, ZSI) for providing necessary

facilities and encouragement.

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Lamellicornia from Japan and Formosa. The Entomological Review of Japan, 39 (1): 73-83.

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groups belonging to the subfamily Geotrupinae.

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Bolboceratinae. Reichenbachia, Staatliciies Museum fur Tierkunde in Dresden, 17 Nr. 27,

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composition of the subfamily Bolboceratinae

from the Palaearctic faunistic region. Tethys

Entomological Research, 8: 187-206.

Nikolajev, G. V., 2008. On the systematic

position of Iranian species Bolboceras davatchii Baraud, 1973 (Coleoptera: Scarabaeoidea),

Caucasian Entomological Bulletin, 4 (2): 199-

201.

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the female of Bolbelasmus shibatai Masumoto,

1984. Kogane, 3: 31-33.

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Position of Bolbelasmus ishigakiensis Masumoto

Elytra, 33 (2): 244

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new species of Bolbochromus from the

Philippines (Coleoptera, Scarabaeidae). Kogane,

11: 97-99.

Ochi T., M. Kon and M. Kawahara, 2011.

Four new taxa of Scarabaeoidea from Southeast

Asia. Special Publication of the Japanese Society

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in the Geotrupidae (Coleoptera: Scarabaeoidea): a

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30: 597-614.

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Group Names for the Superfamily Scarabaeoidea

(Coleoptera) with Corrections to Nomenclature

and a Current Classification, Coleopterists Society. Monograph Number, 5: 144-204.

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or imperfectly known species of Bolboceras,

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384-387.

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London, 21: 19-30.

76


BREEDING ECOLOGY OF THE CRESTED SERPENT EAGLE

Spilornis cheela (LATHAM, 1790) (AVES: ACCIPITRIFORMES:

ACCIPITRIDAE) IN KOLLI HILLS, TAMIL NADU, INDIA Sectional Editor: Sujan Henkanaththegedara Submitted: 24 January 2012, Accepted: 27 June 2012

Varadarajan Gokula

Post Graduate & Research Department of Zoology, National College, Tiruchirappalli 620001, Tamil Nadu,

India; E-mail: [email protected]

Abstract

The breeding ecology of the crested serpent eagle (Spilornis cheela), focusing on nest-site selection,

food habits, and perch-site preference, was studied in the Kolli Hills of Tamil Nadu, India, from May

2005 to May 2010. Thirty-two active nests were located, with nest-site details collected from 27 nests

that were accessible. The crested serpent eagle did not construct new nests, but did renew or alter old

nests, mainly in December. Both sexes were involved in the nest renewal activities. The clutch size

was one, the mean incubation period was 41.5 days, and the mean fledging period was 64.5 days.

Nests were found largely along riverine patches. The results indicate the mature and less disturbed

riverine forests with large sized trees are critical for the breeding and conservation of this species. The

food habits of the eagle were known from prey items brought into the nest by the adult to feed the

chick and prey items fed on by the adult. In total, 173 feeding observations were made and the prey

items belonged to 17 species of vertebrates. The crested serpent eagle largely preferred reptiles,

which accounted for 74% of their diet, followed by birds, which accounted for 18% of their diet. A

total of 1237 perching records were observed. The crested serpent eagle preferred to perch on the

outer canopy of the trees found largely in the forest edges.

Key words: Clutch size, prey preference, perching preference, nesting behaviour, raptors, avian

ecology, Indian biodiversity

Introduction

Raptors are one of the most threatened groups

of birds (Brown & Amadon, 1968) and thus

knowledge of their ecological requirements is

very crucial for conservation activities. The

crested serpent eagle (CSE hereafter), Spilornis

cheela, is classified as a raptor of least concern

(Birdlife International, 2010). It is a medium

sized raptor whose range includes most of the

Indo-oriental region (Brown & Amadon, 1968).

Over 20 sub-species are recognized around the

world, all of which are associated with tropical

and subtropical forests (Brown & Amadon,



BREEDING ECOLOGY OF THE CRESTED SERPENT EAGLE - INDIA


1968). Within the Indian sub-continent, there

are five subspecies of the CSE (two endemic to

Andaman and Nicobar Islands) while the sixth

subspecies is endemic to Sri Lanka (Naoroji,

2006). Although the CSE is found in a wide-

array of suitable habitats and bio-geographical

zones of India, the ecological requirements of

the CSE, like most other raptor species, is

poorly documented in India. However, a few

behavioural descriptions are available

elsewhere (Naoroji 1994, 1999; Naoroji &

Monga, 1983; Baker 1914;

Dharmakumarsinhji, 1939; Purandare, 2002;

Waghray et al., 2003). Hence, an attempt was

made to study the breeding ecology, focusing

on nest-site selection, food habits and perch-

site preference, of CSE in Kolli Hills, Tamil

Nadu, India, from May 2005 to May 2010.

Materials and Methods

Study area: Kolli Hills (11o 11’ - 11

o 30’ N,

78o 16’ - 78

o 29’ E) covers an area of about 485

km2 (Fig. 1). Average rainfall ranges from 787

- 910 mm in the plains, while it varies from

1189 - 1333 mm in the hills. On the plateau,

temperature fluctuates from 10 – 30 oC, but in

the foothills and adjoining plains it varies from

20 – 40 oC. The total human population of Kolli

Hills is about 37, 516, with a homogeneous

community of 97% Malayalis that have largely

been managing the landscape. Most Malayalis

are directly involved in agricultural activities.

Among the crops cultivated, Cassava

dominates some parts, while millet dominates

other areas. The encroachment into forests by

local farmers, bauxite mining activity, land-use

pattern changes, disturbance of water regime,

and clogging of stream channels are the

primary threats to the biodiversity of Kolli

Hills. However, the hunting and gathering

activities of the local inhabitants may not be

overlooked in this issue.

The following forest types have been observed

in Kolli Hills; Shola forest occurs between the

altitude 900 and 1370 m a.s.l. and receives

ample rainfall during the north-east monsoon.

Memecylon edule, Persea marmacranth, and

Memecylon umbellatum are the dominant tree

species. The tropical dry evergreen forest

occurs between 900 m and 1200 m a.s.l., with

Ammora canarana, Canarium strictum,

Syzyium cumin, and Filicium decipiens the

dominant tree species. Semi-evergreen forest

occurs between 400 m and 1200 m a.s.l., with

Persea macrantha, Epiprinus mallotiformis and

Terminalia bellarica dominating this forest

type. Thorn forest occurs between 220 m

(foothills) and 1100 m a.s.l. The dominant

species is Moringa concanensis. Besides

natural forests, plantations of eucalyptus,

bamboo, tamarind, and silver oak are also

present.

Figure 1: The map of administrative units of Kolli Hills, Tamil Nadu, India.

GOKULA, 2012


Data collection: Nest searches were made by

examining trees and substrates suitable for

nesting. An active nest was identified if adults

were seen performing breeding activities (e.g.,

nest-building or renovation, incubation, feeding

the young) in or adjacent to the nest. Dates of

the presence of eggs in the nests were recorded

to estimate the breeding seasonality of CSE. I

collected data on the nests [height (m), length

(cm), and width (cm)], trees that nests were

found in [tree-height (m), and diameter at

breast height (cm)], and the surrounding

landscape of the nest trees [ground-cover (%),

shrub-cover (%), distance to water (rank),

distance to settlement (km), and canopy-

closeness (%)]. The landscape variables were

measured within a 0.07 ha circular plot centred

at the nest-tree as suggested by Titus & Mosher

(1981). Percentage of vegetation cover (shrub

and ground) was visually estimated. The

percent canopy-cover immediately over the

nest was measured using a hand mirror marked

with a grid. The shaded area was estimated as

canopy cover (Martin & Roper, 1988). All

parameters except nest measurements were

compared with similar measurements at

randomly selected sites to identify the factors

responsible for selecting a nest-site. Random

sites were selected on the basis of a place

having potential as a nest-site and being close

enough to the located nest sites. The study area

was divided into 50 m x 50 m grids and

numbered on an enlarged topographic map.

Twenty seven grids were selected using lot

method and were identified in the study area.

Once the approximate grid or site was located,

the nearest tree or shrub was made the centre of

the random plot.

Direct visual observation was used to examine

food habits of the CSE. I opportunistically

recorded the prey items delivered to the chick

by adult CSEs and the prey items eaten by

CSE. Observations were made using Vanguard

DCF10 X 42 binocular and Audubon Spotting

Scope (15 – 60 X zoom) from a distance with

minimal disturbance from the observer. Prey

items were identified up to species level if

possible. Left over/fallen prey remains, if any,

were collected from the ground to confirm the

identity if needed. In total, 173 food habit–

observations were made for the present study.

In order to understand the perching site

preference, details viz. perching height, status

of the perching tree (live or dead), and perching

canopy (inner canopy [close to trunk], outer

canopy [away from trunk], or edge of the

canopy) were recorded for all CSE sighted. A

total of 1237 perches were observed.

Data analysis: Mann-Whitney U were

performed on ranked variables (Ground-cover,

shrub-cover, distance to water, distance to

settlement, canopy-closeness) and Univariate

analyses of variances (ANOVA) were

performed on other measured variables (Nest-

tree-height, and Girth at breast height) to

compare nest-sites and random sites (Sokal &

Rohlf, 1981). Results are reported significant if

associated with a value of P < 0.05.

Results and Discussion CSE started breeding mainly in late November

and completed by early April (this includes

courtship to fledging of the young). However,

the season is extremely variable within India, as

CSE breeds much later (between February and

July) in the Northern India (Naoroji, 2006).

Circular soaring and calling, a frequent mode of

display during the breeding season, were

performed during late November. Talon

locking was observed in one pair. Mating of

CSE was observed on trees on five occasions

by different pairs. Both sexes find the available

old nest and start renovating. In total, 32 nests

were located; however, data were collected on

only 27 accessible nests. No nest was

constructed afresh, but old nests were found

renovated for use (n = 27). All the nests were

renovated mostly in December with fresh twigs

and branches. Fresh green leaves were found

inside the nests in some cases (n = 16) during

the initial period of incubation and in all cases

during the later stage of incubation.

Replacement of old leaves with new ones

during the fledgling period was also observed.

The reasons for the use of green material inside

the nest concur with Nores & Nores (1994); it

may be a strategy to diminish infestation by

ectoparasites. Both sexes were involved in nest

renovation activity. Traditional use of nest-site

every year is a strategy adopted probably to

avoid spending energy for constructing nests as

reported by Collias & Collias (1984). Clutch

size was invariably single for all cases and the

mean incubation period was 41.5 days (n = 27,

range 37 to 42 days). Only females were

involved with incubation. The male often

guarded the nest when the female left to forage.

79



The mean fledging period was 64.5 days (range

59-65 days, n = 27). However, an average

incubation period of 38.5 days (range 37 to 42

days, n = 16) and fledging period of 62 days

(range 59-65 days, n = 16) in the same locality

was reported in a previous study (Gokula,

2009). Nests were found largely along the

riverine patches of Terminalia bellirica (6),

Dalbergia latifolia (8), Tectona grandis (3),

Lagerstroemia lanceolata (7), Mangifera

Indica (6), and Bombax ceiba (2). Nests were

mostly located in the upper one-third of a tree

where two or more lateral branches extended

from the trunk to form a platform. The nests

were placed at a mean height of 18.5 m (range

15.2 to 24.5 m, n = 27) from the ground level.

The mean length and width of the nests were

103.5 cm and 57.3 cm respectively (Table 1).

Table 1: Nest-site characteristics of the CSE in comparison with random-site characters; ns, not statistically

significant

Variables Nest-plot (n = 27) Random plot (n = 27)

P value Mean SD + Mean SD +

Nest-height (m)

Nest-length (cm)

Nest-width (cm)

Nest-tree-height (m)

GBH (cm)

Ground-cover (%)

Shrub-cover (%)

Distance to water (rank)

Distance to settlement (km)

Canopy-closeness (%)

18.5

103.5

56.8

24.1

292.7

27.6

45.4

1.0

3.4

77.6

2.8

42.5

11.8

2.4

55.5

14.8

16.2

0.0

1.5

4.0

-

-

-

15.6

202.7

42.6

40.7

1.9

1.2

45.1

-

-

-

3.3

92.2

30.0

17.9

0.4

0.8

14.5

-

-

-

< 0.01

< 0.05

ns

ns

< 0.01

< 0.01

< 0.01

Table 2: List of prey items of CSE recorded in Kolli Hills

Prey species Occurrence % of occurrence

Fishes Individual | Group

Unidentified 1 0.6 0.6

Amphibians

Unidentified 12 6.9 6.9

Reptiles

Calotes rouxi 5 2.9 74.0

Draco dussumieri 1 0.6

Psammophilus dorsalis 3 1.7

Chamaeleon zeylanicus 2 1.2

Ptyas mucosus 22 12.7

Oligodon arnensis 7 4.0

Dendrelaphis tristis 22 12.7

Xenochrophis piscator 1 0.6

Ahaetulla nasuta 29 16.8

Naja naja 2 1.2

Daboia russellii 18 10.4

Unidentified snake 16 9.2

Birds

Columba livia 4 2.3 17.9

Acridotheres tristis 3 1.7

Terpsiphone paradise 4 2.3

Aegithina tiphia 5 2.9

Artamus fuscus 14 8.1

Oriolus oriolus 1 0.6

Mammals

Funambulus palmarum 1 0.6 0.6

80

GOKULA, 2012


Analysis of variance and other univariate

procedures indicated that CSE did not select

nest-sites randomly in Kolli Hills. Apparently

the sites were selected to fulfill specific nesting

requirements. CSE selected sites with

microhabitat features such as availability of

larger and broader trees, closed-canopy,

proximity to water source, and farther from

human settlement. Of the environmental

variables, except ground cover and shrub cover,

all others (nest-tree height F=18.55, P=0.0004;

nest-tree girth at breast height F=6.0375,

P=0.0244; distance to water U= 12.0,

P=0.0006; distance to settlement U= 12.0,

P=0.0048; and canopy-closeness U=0.5,

P=0.0001) differed significantly between nest-

sites and random-sites (Table 1).

Table 3: Perching site preference of CSE

No of

perches

perching

occurrence

%

Height

class of

Perching

branch

(in m)

4-5 99 8

>7-8 99 8

>8-9 470 38

>9-10 74 6

>11-12 198 16

>12-13 25 2

>13-14 123 10

>14-15 25 2

>15-16 74 6

>16-17 25 2

>17-18 25 2

Perching

tree status

Live 1150 93

Snag 87 7

Perching

canopy

preference

Inner

canopy 173 14

Outer

canopy 1064 86

The explanation for selecting the broader

(larger girth at breast height) and taller trees

concur with earlier studies reporting that the

larger Accipiters apparently use larger trees to

support their massive nests (Gokula, 1999;

Shiraki, 1994; Siders & Kennedy, 1996).

Moreover, nest placement between tree

branches and trunks facilitates adults to make

frequent trips to nests with food, and young to

early take off. Brown and Amadon (1968)

stated that a nest was in a location allowing the

parents free flight into and out of the nest. The

CSE needs wider avenues of approach to the

nest and thus the nest was positioned higher in

the forest canopy for greater accessibility.

Moreover, the CSE is a perch hunter and

selection of open habitat would facilitate its

accessibility and vigilance over the nest and

also the prey. Selas (1997) reported that for

larger species, nest-site selection may be a

response both to nest predation risk,

microclimate, foraging habitat and food supply.

In total, 173 feeding observations were made

and the prey items varied from fish to

mammals. In general, CSE seems to prefer

reptiles more than any other group as they

accounted for 74% of their diet, followed by

birds, (18%). The CSE used a total of 17

vertebrate prey species. Naoroji (1994, 2006),

Dharmakumarsinhji (1939), and Purandare

(2002) also reported snakes as part of the diet

of CSE. On one occasion, CSE even lifted a

dead Russell’s viper (Daboia russellii) and ate

it.

A total of 1237 perching records of CSE were

observed. The CSE preferred to perch on the

outer canopy of the tree found largely along

forest edges. The frequencies of usage of

different height classes of perching sites were

not equal (X2

= 1504, df = 10, P < 0.01). It

prefers perches available largely in the >8-10 m

height classes (Table 3). The CSE scan for prey

from a high lookout, usually from a tree, then

plunge down and capture the prey. Hence,

selecting moderate height classes may be to get

a wider opportunity to execute their hunting

strategy. Moderately open habitats and

perching at moderate heights may be crucial for

the CSE to improve their foraging success.

In summary, CSE constructs no new nest but

renews or alters the old available nests

preferably on the riverine patches in Kolli Hills.

Both sexes are involved in the renewal

activities. The clutch size was single. Mean

incubation period and fledging period were

41.5 and 64.5 days, respectively. The CSE

consumed 17 vertebrate prey species and

showed more preference for reptiles than any

other group. The CSE preferred to perch on the

outer canopy of the tree found largely along

forest edges.

Acknowledgements

I sincerely thank the University Grants

Commission, Hyderabad, Academy of Higher

Education, National College, Trichy and Tamil

81



Nadu Forest Department, Tamil Nadu for the

support.

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82


GROUP-SIZE AND AGE-SEX COMPOSITION OF NILGIRI LANGUR

Trachypithecus johnii (PRIMATES: CERCOPITHECIDAE) IN INDIA

Sectional Editors: Colin A. Chapman Submitted: 04 July 2012, Accepted: 18 August 2012

Debahutee Roy

Department of Zoology, Division of Wildlife Biology, A.V.C. College Mannampandal, Mayiladuthurai, Tamil

Nadu, India; Email: [email protected]

Abstract

Group size and group composition of Nilgiri langur (Trachypithecus johnii) was studied in two

habitats of Parambikulam Tiger Reserve, Kerala, India. Group size and age-sex composition data was

collected during scan sampling, 18 monitoring transect lines, road-strip count, and direct encounter of

the groups. Mean group size value significantly differ between moist deciduous forest and evergreen

forest. Group size was varied from 2 to 22. The maximum group size, 22 was recorded in evergreen

forest habitat. The mean group size of Nilgiri langur is less in moist deciduous forest and higher in

evergreen forest.

Key words: Demographic parameters, colobines, Parambikulam Tiger Reserve, Western Ghats

Introduction

Primates are typically group living, and Asian

colobines are typically organized into one-male

social group (Yeager, 2000). Group size is

influenced by environmental conditions such as

season, habitat openness, and food availability

(Leuthold & Leuthold, 1975; Southwell, 1984).

Many estimates of group size and composition

are derived from sampling transects (Jathanna

et al., 2003; Karanth & Sunquist, 1992;

Varman & Sukumar, 1995); however, such

estimates often underestimates the actual values

(Burnham et al., 1980).

Nilgiri langurs are endemic to parts of Kerala,

India and are reported to live in larger groups

of approximately 15 animals (Poirier,

1968).The group size has been varyingly

reported to range between 2 to 29. It has been

found to be smaller (6-8 animals) in deciduous

forest than in evergreen forest (18-20 animals)

(Malviya, 2011). Further, Nilgiri langur have

been studied in the Western Ghats (Horwich,

1980; Poirier, 1968; Sunderraj, 2001), but not

in the Parambikulam Tiger Reserve, Kerala,

India. Nilgiri langur, is an endangered species

and is endemic to the rainforests of the Western

Ghats of India and is listed under Appendix II

of CITES. They are also protected under the

Schedule I, Part I of Indian Wildlife Protection

Act, 1972 and are listed as Vulnerable C2A (i)





under IUCN Red data list (Malviya, 2011).

Materials and Methods Study area: Western Ghats extends from the

southern Gujarat from Surat-Dangs to the end

of Kaniyakumari in Tamil Nadu. The study

area, Parambikulam Tiger Reserve (647 km2) is

a part of Western Ghats, located in Palakad

District of Kerala (10º 20’ – 10º 26’ N, 76º 35’-

76º 50’ E). The reserve lies in between the

Anamalai hills and Nelliampathy hills. The

boundaries of the reserve are Nemmara Forest

Division in North, Vazhachal Forest Division

in South, Tamil Nadu in the East and

Chalakudy in the West. The evergreen and

moist deciduous forests are the most important

natural vegetation types. The evergreen

tropical forests are confined to small areas in

the hilltops of Karimala Gopuram and in the

foothills of Pandaravara peak which is known

by the name Karian Shola (Anon, 2012). The

sanctuary has very rich and diverse wildlife due

to the mosaic pattern of vegetation.

Data collection: The study area was surveyed

every month on foot from December 2011 to

March 2012. Data on group size and

composition were collected during monitoring

of line transect, during the scan sampling, and

from the groups which were encountered

outside of these situations. In each habitat

eighteen line transects each 1 km in length and

placed in stratified random fashion. The line

transects were monitored each day alternating

between the two habitats. Individuals in a

group were classified into different age and sex

classes based on the criteria of (Sunderraj,

2001) with some modifications.

The group was classified into following

categories: solitary males, all-male groups, and

one-male multi-female groups. Solitary adult

males and all male groups were not included in

the age-sex composition. The chances of re-

sighting of groups were possible. Hence the

data collection was restricted in selected

transects and roads once in a week.

Furthermore counts in adjoining transects were

avoided in the subsequent days to prevent

double count and pseudoreplication. Langurs

move approximately 900 m to 2 km per day

depending on season (Poirier, 1968) and the

distance between transects was only 100m. In

addition if two groups had same size then the

independence of these two data sets was

checked using group composition and marking

of the individuals of the groups.

The density and relative abundance of food

plant species, species diversity, and richness in

the two habitats were estimated by belt

transects (eight in moist deciduous forest and

ten in evergreen forest) within the Nilgiri

langur ranging area to find out which of the two

habitats appears to be more suitable for group

formation of this species. In each habitat, 1 km

transect was laid where a sub transect of 50x2m

dimension was prepared, separated by at least

100m (distance between adjacent transects) for

vegetation analysis, based on the distance

moved by the langurs. In each transects the

variables such as tree species, GBH of the tree

and vegetative phenology was recorded.

Results

A total of 18 groups were sighted and their size

varied from 2 to 22. The group size class and

frequency of sighting is shown in the Figure 1.

Other than solitary males which were recorded

most frequently, the group size of five was

most common in moist deciduous forest and the

maximum group size, 22 in evergreen forest.

The solitary individual sightings constituted

18% of overall sightings and they were all adult

males. All male groups of 17 individuals were

sighted once in the moist deciduous forest.

Figure 1: Frequency distribution of group size

classes of Nilgiri langur at PTR.

The mean group size of Nilgiri langur was

(7.72±5.54). The mean group size in evergreen

and moist deciduous forest was 11.78±5.09 and

3.67±1.50 respectively. Thus the mean group

size of Nilgiri langur was significantly higher

in evergreen forest (F=14.93; p<0.001 (Fig. 2).

An all-male group was also sighted once during

the study. A multi sex group is composed of

one adult male, few adult females with or

ROY, 2012


109N =

Habitats

MDFEvergreen

Me

an

gro

up

siz

e (

95

% C

I o

f M

ea

n)

18

16

14

12

10

8

6

4

2

0

without infants, sub-adults and juveniles (Fig.

3). Adult female constituted the highest percent

of the group size 50±2.94% and 40.6±11.59%

in both moist deciduous and evergreen forests

respectively. The percent composition of adult

male was higher in moist deciduous forest

(29%) than evergreen forests (13.04%). The

percent composition of sub-adult male, sub-

adult female and juvenile was higher in

evergreen forests (11.59%, 26% and 8.7%)

respectively. Thus the percent composition of

different age-sex classes of Nilgiri langur

varied significantly in association with the

habitat types (2=28.95; df=6; p<0.05).

Figure 2: Mean group size of Nilgiri langur in two

habitats at PTR (F=14.93; p<0.001).

Figure 3: Age sex composition of Nilgiri langur in

different habitats at PTR (2=28.95;df=6;p<0.05).

In the two habitats, tree species richness and

diversity were higher in the evergreen forest

(144 sp., H=2.8±0.4) than in moist deciduous

forest (86 sp., H=2.4±0.3). Mean tree height

and mean GBH were higher in moist deciduous

forest (43.8±7.7m, 35.8±12.4cm) than in

evergreen forest (36.1±5.9m, 30.5± 9.1cm). In

tree vegetative phenology the percent young

leaves was significantly more in the evergreen

forest (11.8%±4.39) than in moist deciduous

forest (8.3%±6.05). Percentage of mature

leaves was more in moist deciduous forest

(91.7%±6.05) than in the evergreen forest

(88.2%±4.39).

Discussion

The most basic characteristics of primate

societies have traditionally been based on social

organization alone. Asian colobines are

typically organized into one-male social group

(Yeager, 2000). Nilgiri langurs living in parts

of Kerala appear to live in larger groups of

approximately 15 animals with a higher adult

male- adult female ratio than typically reported

for most langurs (Poirier, 1968). The group size

has been varyingly reported to range between 2

to 29. It has been found to be smaller (6-8

animals) in deciduous forest as compared to

evergreen (18-20 animals) (Malviya, 2011).

Group formation and sizes can be influenced by

foraging behavior (Jarman, 1974). The number

of groups and their size are mainly determined

by food resource availability and competition

between males which leads to the splitting up

of groups (Narasimmarajan et al., 2011). The

mean group size of Nilgiri langur varied

significantly among the two different habitats.

The mean group size of Nilgiri langur was less

in moist deciduous forest than the evergreen

forest, possibly because more open habitat

could not allow the formation of larger groups

(Barrette, 1991). The standard ecological model

assumes that better predation avoidance as

group size increases favours living in larger

groups, whereas increased travel costs and

reduced net food intake due to within-group

competition for resources set the upper limit

(Steenbeek et al., 2001). There are two main

competing theories on the evolution of group

living in diurnal nonhuman primates. The first

theory claims that predation avoidance favours

group living, whereas there are only

disadvantages to feeding in a group and feeding

competition increases with group size (van

Schaik, 1983). The second theory claims that

there is a feeding advantage to group living

deriving from communal defense of high-

quality food patches and that predation is not

important (van Schaik, 1983). These theories

have not yet been rigorously tested. Though

food resources might limit the maximum group

size, predation pressure influences the



formation of groups (Jarman, 1974). Benefits of

group living for primates fall into three board

categories: predator avoidance, foraging

advantages, and avoidance of conspecific threat

(Gillespie et al., 2001). The predation

avoidance hypothesis claims that primates live

in groups to reduce the risk of predation,

despite the increased cost of within group

feeding competition (Treves et. al., 1996).

Earlier study by Sunderraj (2001), reported a

mean group size of 5-18 in Western Ghats. He

stated the variation in group size of Nilgiri

langur may be influenced by the availability of

food, temperature, and human disturbance.

Here in the current study the mean group size

of Nilgiri langur was less in moist deciduous

than evergreen forest. Barrette (1991)

emphasized that open habitat did not allow the

formation of larger groups as the distribution of

food resource may not be uniform in open

habitat. An increase in group size normally

increases the distance that must be travelled to

find adequate food supplies (Chapman et al.,

2000) where they expend more energy to

forage if they are in a large group and where

the distribution of food is not consistent.

Primates adjust their intensity of use for

foraging area and their daily movements

according to food availability (Tsuji et al.,

2009).

Tree species composition in Nilgiri langur

habitats were compared and analyzed where the

diversity and percent of young leaves is more in

the evergreen forest. Consumption of leaves

satisfied the nutrient requirement. Young leaves

are reported to contain high percentage of crude

protein and contains less fiber. Availability of

young leaves contributes to whether or not a

particular species is chosen for food (Solanki et

al., 2008). Regarding group size variation, my

observation and analysis showed that Group

size in Nilgiri langur varies with habitat type

with respect to food availability as the main

reason next to predation risk as in the current

study the result of vegetation analysis has

shown that the abundance of food plants with

respect to richness and diversity is more in

evergreen forest and also this habitat type is

supporting the larger group size. The study is

only a preliminary investigation on the

variation of group size in two different habitats.

Thus group size may increase or decrease with

food availability, food species diversity and

richness.

Acknowledgements

I thank Michael Wasserman (McGill

University, Canada) for reviewing the

manuscript, S. Sandilyan for guidance and the

Kerala Forest Department, India for permission

to conduct research within Parambikulam Tiger

Reserve. I thank M. Ashokkumar and D.

Boominathan (senior project officers, WWF)

for their help in statistical analysis and the

WWF for funding the study. I am grateful to K.

Thiyagesan, principal of A.V.C College and J.

Pandian, G. Sharmila, R. Nagarajan, S.

Shankari and M. Kartikiyan of A.V.C College,

Department of Zoology and Wildlife Biology

for their support. I would like to thank Ajay

Desai, co-chairman Asian Elephant Specialist

Group IUCN for designing the study.

Literature cited Altmann, J. 1974. Observational study of

behavior: sampling methods, Behavior, 49:227-

267.

Anon, 2012. Parambikulam Tiger Reserve,

downloaded from http:// www.parambikulam.org/

on 6 July 2012.

Barrette, C., 1991. The size of Axis deer fluid

groups in Wilpattu National Park, Sri Lanka.

Journal of. Mammalia, 55: 207-220.

Burnham, K. P., D. R. Anderson and J. L. Laake,

1980. Estimation of density from line transects

sampling of biological populations, Wildlife.

Monographs, 72: 1-202.

Chapman, C. A. and L. J. Chapman, 2000.

Constrains on group size in red tailed guenons:

Examining the generality of the ecological

constrains model. International Journal of Primatology, 21 (4): 564-585.

Gillespie, T. R. and C. A. Chapman, 2001.

Determinants of Group size in the Red Colobus

monkey (Procolobus badius): an evaluation of the

generality of the ecological constraints model.

Behavioural ecology, 50 (4): 329-338.

Horwich, R.H., 1980. Behavioural rhythms in the

Nilgiri langur, Presbytis johnii. Primates, 21 (2):

220-229.

Jarman, P. J., 1974. The social organization of antelope in relation to their ecology. Behaviour,

48: 215-220.

86

ROY, 2012


Jathanna, D., K. U. Karanth and A. J. T.

Johnsingh, 2003. Estimation of large herbivore

densities in the tropical forest of southern India

using distance sampling, Journal of Zoology., 261: 285-290.

Karanth, K. U. and M. E. Sunquist, 1992.

Population structure, density and biomass of

larger herbivores in the tropical forests of

Nagarahole, India. Journal of Tropical Ecology,

8: 21-35.

Leuthold, W. and B. M. Leuthold, 1975. Pattern

of social grouping in ungulates of Tsavo National

Park, Kenya. Journal of Zoology., 175: 405-420.

Malviya, M., A. Srivastava, P. Nigam and P. C.

Tyagi, 2011. National Study book of Nilgiri

langur (Trachypithecus johnii). Wildlife Institute

of India: 1-17

Narasimmarajan, K., R. Nagarajan and A.

Kumaraguru, 2011. Some Observations on

demography and edible plants of Lion-tailed

Macaques (Macaca silenus) in the rain forest

fragmented habitats of Anamalai Hills, Western

Ghats. Journal of Research Biology: 1 (5): 352-

362

Poirier, F. E., 1968. Analysis of Nilgiri langur

(Presbytis johnii) Home range change. Primates,

9: 29-43.

Poirier, F. E., 1970. Dominance structure of the

Nilgiri langur (Presbytis johnii) of South India.

Folia Primatologica, 12:161-186.

Schaik, C.V.P. 1983. Why are Diurnal Primates

living in Groups? Behaviour, 87 (1&2): 120-144.

Solanki G.S., Kumar, A. and Sharma B.K. 2008

b. Winter food selection and diet composition of

capped langur (Trachypithecus pileatus) in

Arunachal Pradesh, India Tropical Ecology, 49

(2):157-166.

Southwell, C. J., 1984. Variability in grouping in

the eastern grey kangaroo, Macropus giganteus.

Group density and group size. Australian

Wildlife Research, 11: 423-435.

Steenbeek, R and Schaik, C.V.P. 2001.

Competition and Group size in Thomas’s langurs

(Presbytis thomasi): the folivore Paradox

revisited. Behavioural ecology and Sociobiology,

49. 2-3

Sunderraj, S. F. W., 2001. Ecology and

conservation of Nilgiri langur (Trachypithecus

johnii). Envis Bulletin: Wildlife and Protected Areas, 1 (1): 49-59.

Treves, A. and C. A. Chapman, 1996.

Conspecific threat, predation avoidance and

resource defense: implications for grouping in

langurs. Behavioural Ecological Sociobiology,

39: 43-53

Tsuji, Y. and S. Takatsuku, 2009. Effects of

yearly change in net feeding on autumn home-

range use by Macaca fuscata on Kinkazan Island,

Northern Japan. International Journal of

Primatology, 30: 169-181.

Yeager, C. P. and K. Kool, 2000. The behavioural

ecology of Asian colobines. In: Old world monkeys, Whitehead, P. F. and C. J. Jolly (eds.).

Cambridge University Press, Newark: 496-521.

87

ESSAY


The Nasalis Affair

Sectional Editor: Colin Groves Submitted: 24 August 2011, Accepted: 08 September 2012

Lee E. Harding

SciWrite Environmental Sciences Ltd., 2339 Sumpter Drive, Coquitlam, British Columbia, Canada


Baron Friedrich van Wurmb (1781) is credited with the first description of the proboscis

monkey, endemic to Borneo, which he named Cercopithecus [now Nasalis] larvatus. This was in a

paper read to The Society of Batavia, modern day Jakarta, Indonesia, and later published in the

Society’s Memoirs. But he was not the first.

The late 18th Century must have been a wonderful time to be a naturalist—or, at least, a rich

one. As the imperial powers of Europe scoured the globe for business opportunities, they saw the

value of biodiversity. Their military and trading expeditions included naturalists who sent home many

tonnes of specimens of animals and plants. The literati back home were amazed at the endless variety

of organisms inhabiting these far-flung lands, and many nobles of wealth—who funded the

expeditions—made a hobby of collecting them. King Louis XIII of France was one of these and his

collection in the Jardin du Roi [the King’s Garden] would become the foundation of the Muséum

national d'Histoire naturelle in Paris. Carl Linnaeus (or Linné, which he adopted after he was made a

nobleman) had published his first edition of Systema Naturae in 1735, with revisions and extensions

as new specimens poured in, culminating in the tenth edition in 1758, the starting point for modern

zoology. Taxonomists pored over the collections, categorizing and naming new species. Artists

hurried to illustrate folios of strange plants and animals, lithographers made prints of them, and

publishers rushed to publish.

One of the greatest taxonomists of his day—or ever—was the French noble, Georges-Louis

Leclerc, Comte de Buffon (1707–1788). In 1742, he was given the task of describing the animals in

the cabinet du Roi (then as now, extensive biological collections were kept in cabinets with arrays of

drawers), for which he enlisted the help of his protégé, Louis Jean Marie Daubenton (1716–1799).

Under Buffon’s tutelage, Daubenton became a member of the French Academy of Sciences as an

adjunct botanist, and Buffon appointed him curator of the king's cabinet. The 36 volumes of their

jointly authored “Histoire Naturelle, Générale et Particulière, avec la Description du Cabinet du Roi”

began coming out in 1746. Volume 14 on primates appeared in 1766 with Daubenton authoring an

introductory section on “Nomenclature des Singes” [Nomenclature of the Monkeys] and detailed

anatomical descriptions of 18 species—not, however, including Nasalis larvatus (Buffon &

Daubenton, 1766).



THE NASALIS AFFAIR


But Buffon & Daubenton (1766) had a famous falling-out. For two centuries and more,

scholars have speculated on the cause of the conflict (e.g., Farber, 1975), but the two never wrote of it

themselves. Buffon dropped most of Daubenton’s detail from the descriptions in the 2nd edition

(Buffon, 1789) and dropped Daubenton as co-author, even though the latter continued working on his

anatomical descriptions of monkeys and apes. This edition included a brief description of N. larvatus,

which Buffon named the “guenon à long nez [long-nosed monkey]” crediting van Wurmb (1781) for

the Latin name and description. “Guenon” was a generic term for what we now recognize as the tribe

Colobini, of which the proboscis monkey is a member. Buffon’s 1789 Histoire Naturelle included

lithographs of a male and female proboscis monkey. The Avertissement (Introduction) written by

Bernard Germain-Étienne Lacépède (who in 1799, after Buffon’s death, would publish a revised

edition of the Histoire Naturelle), said "M. Daubenton se propose de publier un Memoire au sujet de

cet animal remarquable [Mr. Daubenton intends to publish a monograph about this remarkable

animal].”

Meanwhile, Johann Christian Daniel von Schreber, a student of Linnaeus, was translating

Linnaeus’ work and writing a German-language compendium on mammals of the world, Die

Säugethiere [The Mammals]. Von Schreber’s (1775:46, Plates 10B and 10C) hand-coloured

engravings of the proboscis monkey, “Simia nasica,” obviously by someone who had never seen one

alive (Fig. 1), were the clearly basis for Buffon’s (1789: Plates XI and XII) lithographs of the “guenon

à long nez.” So the questions are: where did von Schreber, in Germany, see a specimen or drawing of

the proboscis monkey five years before van Wurmb’s paper in Indonesia? And why did von Schreber

name it “nasica”?

Figure 1: Von Schreber’s 1775 hand-coloured engravings of the proboscis monkey (male, left; female, right)

are the first published illustrations, are the first to use the name “nasica” and are identical in posture,

background and details to Buffon’s 1789 lithographs (reproduced from Von Schreber, 1775: 46, Plates 10B &

10C).

Several early authorities (e.g., Cuvier, 1817; Cuvier, 1827; Geoffroy, 1812; Gervais, 1854; Lesson,

1834; Martin, 1837) refer to Daubenton’s 1781 or earlier description of “le nasique,” in the Mémoire

de l'Institut National des Sciences et Arts, as the basis for the synonyms nasica, nasicus, and,

ultimately, Nasalis. According to the British naturalist, William Charles Linnaeus Martin (1841: 456).

“Daubenton had previously [i.e., before van Wurmb’s description] read a memoir respecting

it, before the Academy of Sciences at Paris; but this paper was never published : there is no allusion to

it in the Supplement to Buffon's Nat. Hist, vii., where the animal is figured and described under the

title of ‘Guenon a longue nez’; and whether the memoir on the ‘Nasique’ by Daubenton, be still in

HARDING, 2012


existence, and, if so, what may be the details and statements it contains, we have no means of

ascertaining.”

In fact, it was Étienne Geoffroy Saint-Hilaire (1812) who elevated the proboscis monkey to

its own genus and renamed it Nasalis larvatus, combining Daubenton’s nasique for the genus with

van Wurmb’s larvatus for the species. Significantly, in listing the previous synonyms, Geoffroy Saint-

Hilaire cites von Schreber for the name Simia nasica after citing Daubenton for nasique, before citing

Buffon for Guenon à long nez (not in italics), and before van Wurmb’s Cercopithecus larvatus.

Daubenton’s detailed description of the proboscis monkey was not printed until after Buffon’s

death in 1788. It appeared in the “Sonnini Edition” of the Histoire Naturelle (Buffon & Sonnini,

1799). Later French naturalists continued to credit Daubenton for his description of “le nasique.”

Deterville & Sonnini (1803:536), for example state that Buffon’s guenon a long nez “...c’est le

nasique de Daubenton [is the nasique of Daubenton]”, and Gervais (1854:59) states, "On en doit la

première description à Daubenton, qui l'a fait connaitre, dans l'Histoire de l'Académie des sciences.

M. Wurmb en a parlé depuis dans les Mémoires de la societé de Batavia [We owe the first description

to Daubenton...in the memoirs of the Academy of Sciences. Mr. Wurmb later discussed it in the

Memoires of the Society of Batavia].” Daubenton’s non-Linnaean nasique, although not available for

nomenclatural purposes, is of historical interest as the probable source for von Schreber’s (1775:46,

Plates 10B and 10C) illustrations of Simia nasica.

Why wasn’t Daubenton’s monograph ever published? Could it have been related to the

famous fight between him and Buffon? In three days of searching during April 2012, with the help of

archivists, I could not find any papers by Daubenton on “le nasique” in either the French National

Library rare book collection or National Museum of Natural History archives. I did, however, find 26

letters from Buffon to Madame Daubenton. They began shortly after Daubenton’s February 1772

marriage to the former Mlle. Anne-Marie-Bernarde Boucheron, and continued through 1786. Some

were clearly love letters. Buffon sent Daubenton’s wife precious gifts and expressed his love for her

in so many words. And she wrote to him: his letter of 26 July 1773, for example, says, “J’ai reçu

toutes vos lettres, j’y ai vu le zèle de votre tendre amitié [I received all your letters, and saw the zeal

of your tender affection].” His letter in May 1772, says, “je vous aime autant que vous pouvez les

aimer [I love you as much as one can love].” The historical footnotes that archivists appended to this

letter say that Madame Daubenton, then 26 (Daubenton was 33) was “very pretty” and had an “easy

manner of the imagination, mind and heart”—a strong temptation, indeed, for one of the most

powerful men in Paris. Another footnote says that, on the Daubentons’ honeymoon in Paris, “Madame

Daubenton was greeted eagerly by all the characters in relation to Buffon, and the circle of scholars

from the Jardin du Roi.” Can this imply a somewhat public knowledge of the affair?

We may speculate that Buffon’s love for Madame Daubenton could explain the mysterious

enmity between the two colleagues. It is even possible that Buffon, who controlled the affairs of

Academy of Sciences, in some sort of reverse pique, suppressed the publication of Daubenton’s

monograph on the proboscis monkey. The Nasalis affair is, however, but a footnote in the Daubenton-

Buffon clash that is better known for the divergent approaches they took to theories of evolution (e.g.,

Butler, 1882; Farber, 1975; Wilkie, 1956).

Surrounding the Muséum National d'Histoire Naturelle are streets named after the great

naturalists who constitute foundations of modern zoology, including most of those named above: Rue

[Street] Cuvier, Rue Geoffroy-Saint-Hilaire, Rue Lacépède, Rue Linné, Rue Daubenton, and Rue

Buffon. Daubenton and Buffon streets are nearly parallel to each other and converge as they near the

Museum from opposite directions; but they never quite meet.

Literature Cited Buffon, G. L. L., 1789. Histoire naturelle, générale et particulière. Supplément. À l'histoire des animaux

quadrupèdes. Tome septiéme, Imprimerie Royal, Paris.

Buffon, G. L. L. and L. J. M. Daubenton, 1766. Histoire naturelle, générale et particulière, avec la

description du cabinet du roi. Tome quatorzième, Plassan, Paris.

Buffon, G. L. L. and C. S. Sonnini, 1799. Histoire Naturelle, Générale et Particulière. Tome trente-

cinquieme, F. Dufart., Paris.

THE NASALIS AFFAIR


Butler, S., 1882. Evolution, old and new; or, The theories of Buffon, Dr. Erasmus Darwin, and Lamarck,

as compared with that of Mr. Charles Darwin. Occasional paper 4, S. E. Cassino, Salem.

Cuvier, F., 1817. Le règne animal distribué d'après son organisation, pour servir de base à l'histoire naturelle des animaux et d'introduction à l'anatomie comparée. Tome 1, Deterville, Paris.

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91

ESSAY


Historical land-use patterns in relation to conservation strategies for the

Riverstone area, the Knuckles massif, Sri Lanka: insights gained from the

recovery of anuran communities.

Sectional Editor: Lee E. Harding Submitted: 15 December 2011, Accepted: 24 September 2012

Senarathge R. Weerawardhena 1,2

and Anthony P. Russell1

1 Department of Biological Sciences, University of Calgary 2500, University Drive NW, Calgary, T2N 1N4,

Alberta, Canada; Email: [email protected] 2 Department of Zoology, University of Kelaniya, Kelaniya 11600, Sri Lanka; Email: [email protected]

Historical land-use patterns in Sri Lanka

Agriculture on the Indian sub-continent dates back to the fourth and third millennia BC

(Lawton & Wilkes, 1979), but only in more recent times did its intensity escalate in a major way.

During the colonial era, the British established that the hilly areas of Sri Lanka were suitable for the

rearing of coffee (Coffea arabica), for which much of the arable land of the island was extensively

cultivated. Later, however, resulting from the severe impact of “Coffee Rust,” caused by the fungus

Hemileia vastatrix, the coffee industry of Sri Lanka declined dramatically (Forrest, 1967). Former

coffee plantations were abandoned, but are still distinguishable as damaged areas (Marby, 1972). The

truncation of coffee growing on the island created vacant room for another cash-crop.

After the 1960s, tea (Camellia sinensis), with a long history of commercial cultivation

(Carter, 2008; Mair & Hoh, 2009; Moxham, 2003), quickly became the major commercial agricultural

commidity in Sri Lanka. Tea was introduced to Sri Lanka directly from China by the British before

1824 as an exhibitive specimen in the Royal Botanical Gardens at Peradeniya. Prior to 1867, it was

not cultivated on a large commercial scale (Marby, 1972). In 1867, seven hectares were planted with

tea and by 1967, 24,038 ha in wet mountainous areas (700–1,300 m a.s.l.) were devoted to tea

plantations (Forrest, 1967; Jayaraman, 1975). These were established by extensively clearing the

virgin forest (Manamendra-Arachchi, 1999). By the middle of the 20th century, “Ceylon tea” (Ball,

1980) had become very popular worldwide (Mair & Hoh, 2009).

The Knuckles Mountain Forest Range

The Knuckles Mountain Forest Range (hereafter KMFR) is situated at 7° 21’ N, 81° 45’ E in

the Intermediate Zone of the Central Province of Sri Lanka. It covers approximately 2.1x104 ha. The

traditional Sinhalese name for this is “Dumbara Kanduvetiya”: “mist-laden mountain range” (Cooray,

1984) because the landscape is rugged with at least 35 peaks rising above 900 m (Ekanayake &

Bambaradeniya, 2001).



HISTORICAL LAND-USE PATTERNS IN THE KNUCKLES MASSIF, SRI LANKA


The KMFR experiences a wide range of rainfall (de Rosyro, 1958). It is oriented

perpendicular to the two principal wind currents that bring rains (the Southwest and Northeast

monsoon) to Sri Lanka and acts as a climatic barrier. The highland and western areas of the KMFR

are extremely wet throughout the year, with an annual rainfall of about 5,000 mm, whereas the lower

eastern slopes are considerably drier, experiencing less than 2,500 mm annual rainfall

(Bambaradeniya & Ekanayake, 2003). The KMFR also exhibits major temperature differentials with

the mean monthly temperature ranging from 15 °–25 °C.

The KMFR is an important watershed, housing more than 500 streams (de Silva et al., 2005)

that are the source of many rivers and streams that drain East into the lower Mahaweli River system

(Heen Ganga, Hasalaka Oya, and Maha Oya), Southwest into the upper Mahaweli River system (Hulu

Ganga), and Northeast into the Amban Ganga River system (Kalu Ganga, and Teligam Oya). The

KMFR catchments area contributes about 30 % of water to the three reservoirs (Victoria, Randenigala

and Rantambe) of the Mahaweli River system (Bambaradeniya & Ekanayake, 2003).

Traditional human settlements occur along the narrow river valleys of the KMFR. Five

ancient villages were situated in the KMFR. Currently, 80 villages are immediately outside of, and

encircle, the KMFR (Nanayakkara et al., 2009). The main food of Sri Lankans, rice (Oryza sativa),

has been cultivated in the KMFR, mainly in valleys and terraced hill slopes, for several centuries. In

addition to paddy-field cultivation, farmers use the traditional practice of slash and burn cultivation

which provides a livelihood and subsistence source of food supply (Bambaradeniya et al., 2004;

Wickramasinghe et al., 2008). This provides more than 20 % of household income of the local

villages (Gunatilake et al., 1993).

Several forested habitats of the KMFR, such as the lowland forest, the sub-montane forest,

and the montane forest, were greatly degraded as a result of commercial farming during the British

colonial era (Bambaradeniya & Ekanayake, 2003). The vast majority of forest clearing in the KMFR

was for agricultural purposes, in particular to create land for cash-crops. During this period, major

estates were located in the KMFR: Kalebokka, Nichola Oya, and Rangalle (Marby, 1972). For

example, 2,796 ha in the Kalebokka area of the KMFR were planted with tea between 1874 and 1875

(Forrest, 1967).

Cardamom (Elettaria cardamomum) was also cultivated in this region (Marby, 1972), under

the canopy of the sub-montane and the montane forest (900 m a.s.l.). Although cardamom cultivation

was initially introduced to the KMFR over a hundred years ago, it was not developed on a large

commercial scale until the 1960’s. Due to the high income generated by this cash-crop, the local

government encouraged its cultivation in the 1960s on lands of the KMFR leased to individuals and

groups for export-oriented cardamom cultivation (Wickramasinghe et al., 2008).

Some commercial plantations of tea and cardamom (legal as well as illegal) still remain in the

KMFR (Bandaratillake, 2005; Forrest, 1967). Wickramasinghe et al. (2008) documented the impact

of cardamom cultivation on the sensitive areas of the KMFR, resulting from the partial removal of the

over-storey and the complete removal of undergrowth. A recent survey conducted by the Forest

Department indicates that about 500 plots for cardamom cultivation, ranging from 2–200 ha, are

located within the KMFR. This impact is increased by the location of about 90 % of the cardamom

processing and drying barns in the KMFR. They all use wood gathered from the forest as fuel, leading

to further degradation of the forest.

As a result of these uncontrolled anthropogenic agricultural practices, in particular the

clearing of land for the cultivation of cash-crops, the sub-montane forest of the KMFR has become

highly fragmented and the virgin forest has been drastically reduced in area, with 21 % of it being

heavily degraded, and only 12 % persisting as open canopy forest (Wickramasinghe et al., 2008).

Importance of the KMFR: Floral diversity

The range of landscape and climatic features present in the KMFR supports a variety of

natural vegetation types: montane forests; sub-montane forests; lowland semi-evergreen forests;

riverine forests; rock-outcrop forests; savannah; patâna grasslands; and scrublands (de Rosyro, 1958).

In the KMFR, virgin sub-montane forest represents a transitional biological belt between lowlands

and highlands. Typical patches of the sub-montane forests are found at Cobert’s Gap; Kelabokka; and

the Riverstone area. These lie between 600 and 1,300 m a.s.l. Trees in the sub-montane forest are

stunted, much branched and aerodynamically shaped by strong winds. Three strata are present in the

WEERAWARDHENA & RUSSELL, 2012


sub-montane forest: the herb/shrub layer (2 m): the sub-canopy (5 m): and the canopy (15 m), each

consisting of its own unique plant species (Bambaradeniya & Ekanayake, 2003).

The occurrence of particular vegetation types in the KMFR is most affected by patterns of

rainfall (de Rosyro, 1958), which determines the location (Touflan & Tallow, 2009) and type of

vegetation. The different vegetation types constitute a complex mosaic structure and collectively

support a rich flora. For example, the KMFR contains approximately 1,033 vascular plant species,

including 170 endemic woody trees (3 % of which are nationally threatened) (Bambaradeniya &

Ekanayake, 2003) and several endemic flowering herbs and shrubs (Gunathillake & Gunathillake,

1995). Furthermore, the KMFR harbours 33 % of all the flowering plant species of the island, and it

has a high level of floral endemism (Ashton & Gunathillake, 1987).

Importance of the KMFR: Faunal diversity

The diverse and stratified vegetation types found in the KMFR, harbour a rich fauna, with

large numbers of endemics and some of which are threatened species. Within the KMFR, around 262

species of vertebrates have been recorded of which around 69 are endemic and around 60 are

nationally endangered.

Importance of the KMFR: Anuran diversity

Based on reliable literature (Manamendra-Arachchi & Pethiyagoda, 2005, 2006) we prepared

a list of anuran species that we expected to encounter in the Riverstone area. It is evident that few

researchers (e.g. Nizam et al., 2005) erroneously included species of doubtful occurrence and extinct

species in their listing. Our list (Table 1) was based upon confirmed occurrence and likelihood of

encounter in the habitats being investigated. The preparation of this list of anurans likely to be

encountered helped us to focus our sampling strategies.

We investigated patterns of recolonization of abandoned tea plantations by terrestrial and

arboreal anurans. Overall our five sampling periods (Weerawardhena & Russell, 2012) over a time

span of 16 months yielded a total of 237 post-metamorphic anurans, representing 21 species arrayed

among the families Bufonidae, Microhylidae, Nyctibatrachidae, Ranidae and Rhacophoridae. The

KMFR is, therefore an important locality in Sri Lanka in terms of its biological diversity and

endemism.

Why is conservation of the KMFR necessary?

The KMFR is an important natural forest in Sri Lanka in many respects – it harbours rich

floral and faunal diversity; it exhibits high endemism; it is occupied by several endangered species; it

consists of diverse habitat types; and it is an important watershed and catchment area for several

rivers and streams. However, the KMFR faces severe and imminent threats. Among these are

extensive agricultural practices, in particular illegal cardamom plantations. Much of the virgin forest

of the KMFR has been cleared to make way for the cultivation of cash-crops, and to supply timber as

well as fuelwood for villages. Illegal felling of timber and fuel wood species and illegal hunting of

animals continue to be prevalent in the KMFR. Over-collection of common and rare medicinal plants

for local use, as well as plant and animal specimens for scientific study, pose serious threats,

especially to the populations of endemic and threatened species in the KMFR. Furthermore,

unregulated research work, and the construction of resorts and other buildings including houses,

uncontrolled tourism access, and human-set forest fires constitute further threats to the KMFR.

Global Amphibian Decline

In late 1980’s herpetologists first became aware of the large scale of amphibian declines

globally, but at that time had no clear picture of the causative agents. Today we recognize that the

same basic causal agents that have led to the decline of other vertebrate taxa have also been

responsible for the declines in many amphibian species. These include deforestation, environmental

pollution, habitat destruction and degradation, introduction of invasive species, global climate change,

and infectious diseases (Stuart et al., 2004). Prominent among the diseases is chytridiomycosis,

caused by a fungus, that has been implicated in amphibian declines globally (Berger et al., 2000) and

is spread by bullfrogs, often transported live as a delicacy (Schloegel, 2012), among other vectors.

Among other causal agents, habitat destruction and degradation represents the greatest threat to



amphibians (Wells, 2007). The transformation of natural habitats into agricultural lands plays an

important role in habitat degradation. It is estimated that 9 x108 ha of the earth’s surface had been

converted into crop-lands by 2005 (Spellerberg, 2005).

Table 1: Anuran species of the Riverstone area of the KMFR ◄ The list of the possible anuran species of the

KMFR; ▼ The list of anurans species encountered in our study (Weerawardhena & Russell, 2012); E endemic to

Sri Lanka.

Abandonment of agricultural lands in the KMFR

Both slash and burn cultivation and also some cash-crop cultivation (coffee, tobacco, and tea)

have led to abandonment of land due to the loss of soil fertility. Nitrogen-phosphorus-potassium

fertilizers were used on tea plantations in large quantities and this ultimately led to lower soil fertility

over a period of several decades (Mohammed, 1996). Other factors contributing to the abandonment

of tea plantations are higher levels of soil acidity (Weerawardhena, 1993), leaf and root diseases, and

pest (in particular insects) infestations (Marby, 1972). For example, in the Duckwari Group of the

KMFR, most of its 655 ha was planted in tea prior to 1898, but by 1967 only 481 ha of the total were

planted in tea, 48 ha were under cardamom plantation, one hactare was cultivated with rice paddy, and

125 ha had been abandoned (Marby, 1972). Typically these abandoned lands have either been

replanted—for example, 20.5 ha were replanted in Guatemala grass (Tripsacum laxum) (Marby,

1972)—or allowed to secondary succession.

Secondary succession in abandoned agricultural lands

Following abandonment, secondary succession takes place and these plots become

increasingly occupied by native plant taxa. Within a few years of abandonment, dominance shifts to

fast growing tree species with intermediate and high shade tolerance. These plants tend to grow taller

than the general mass of vegetation, resulting in stratification of the forest canopy similar to that of

the primary forests.

Anuran species ◄ ▼

Adenomus kelaartii E √ -

Duttaphrynus melanostictus √ √ Fejervarya limnocharis √ -

Nannophrys marmorata E √ -

Kaloula taprobanica - √ Ramanella obscura

E √ √

Lankanectes cf. corrugatus E √ √

Hylarana temporalis E √ √

Pseudophilautus cavirostris E

√ √ Pseudophilautus fergusonianus

E √ √

Pseudophilautus fulvus E √ √

Pseudophilautus hankani E

√ -

Pseudophilautus hoffmanni E √ √

Pseudophilautus macropus E √ √

Pseudophilautus mooreorum E √ √

Pseudophilautus cf. ocularis E - √

Pseudophilautus sarasinorum E √ √

Pseudophilautus cf. silus E - √

Pseudophilautus steineri E √ √

Pseudophilautus stuarti √ √ Pseudophilautus (red head) sp. - √ Pseudophilautus (white eye) sp. - √ Pseudophilautus (yellow dorsum) sp. - √ Polypedatus cruciger

E - √

Taruga cf. eques E √ √

Total 18 21

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Factors that delay secondary succession

Secondary succession may be delayed by several factors or processes. One of the most

important of these is the availability of seeds of wild plant species. Many studies have shown that

seeds of these plant species are generally absent from the soil seed bank (Leck et al., 1989; Uhl et al.,

1981). The seeds and vegetative propagules, such as roots and stags of wild plant species, are

destroyed by agricultural practices (Skinner, 2004), and thus seeds of such species must disperse into

the abandoned agricultural plots for successful secondary succession. Wickramaratne et al. (2009a)

showed that the availability of seeds acts as a limiting factor for secondary succession in degraded

grasslands in the KMFR. Some regeneration studies have demonstrated that the seed-rain declines

rapidly within few meters of the edge of forest (Holl, 1998). According to Hooper and co-workers

(2005) seed dispersal limitation is a major barrier to natural regeneration or secondary succession.

Another contributing factor to the slow rate of recovery of abandoned agricultural plots

relates to the high percentage of such seeds that are dispersed by the wild birds and small mammals.

These animals mainly inhabit the forest or exploit habitat near the edge of the forest rather than

occupying the disturbed habitats. The seeds that do arrive in the abandoned agricultural plots are often

distributed patchily, again that delaying the process of secondary succession.

Additionally, the combination of a hard seed-coat and a hilum whose opening is controlled by

environmental conditions are also responsible for an induced dormancy of seeds of wild plant species

(Degreef et al., 2002). This dormancy also delays the process of secondary succession. Furthermore,

seed that do arrive in the abandoned agricultural plots are subjected to high rates of seed predation and

herbivory (Holl, 1998; Skinner, 2004) because common seed predators, such as ants, birds and small

mammals, constitute the main faunal components of abandoned agricultural plots. The rates of seed

predation differ between species of seed predators, which also affects the pattern of secondary

succession.

Wickramaratne et al. (2009b) pointed out that competition for above- and below-ground

resources exerted by grasses on newly established plant-seedlings can also impact the potential for

successful establishment of plant species in abandoned agricultural plots in the KMFR. The limited

colonization success of forest plant species in abandoned agricultural plots is also contributed to by

aggressive grasses that often form a monoculture in tropical environments throughout Southeast Asia

(Holl, 1998; Iwata et al., 2003; Ohtsuka, 1999; Padoch et al., 1998; Vasey, 1979). Such grasses may

limit recolonization in many ways (Nepstad et al., 1990), such as by competing for soil moisture

(Holl, 1998), increasing the possibility of fire that kills plant seedlings (Skinner, 2004), being

unattractive to seed dispersers, and providing shelter for seed and seedling predators (Hooper et al.,

2005).

The microclimatic conditions of the KMFR may also have an effect on recovery of disturbed

habitats (Skinner, 2004). Holl (1998) and Skinner (2004) noted that air and soil temperatures, as well

as light levels, are elevated and soil moisture and humidity levels are reduced in abandoned

agricultural lands compared to those of virgin forest habitats. We found that air and soil temperature

levels in abandoned agricultural lands were higher than those in the sub-montane forest, and

conversely we found that relative humidity and soil moisture were low in abandoned lands relative to

those in the virgin sub-montane forest. Such different and stressful microclimatic conditions may

facilitate and promote the growth and survival of grasses (Aide and Cavalier, 1994) while inhibiting

seed germination, plant-seedling growth and the survival of colonizing woody plants (Holl, 1998).

Ultimately these factors also limit the process of secondary succession. Additionally, the availability

of propagules (Skinner, 2004), lack of nutrients (Hooper et al., 2005; Vitousek and Sanford, 1986),

lack of mycorrhizae, (Janos, 1980) and highly compacted soil (Buschbacher et al., 1988) in

abandoned agricultural lands may also retard the process of secondary succession. The relative

importance of these factors depends on the original ecosystem, the history of disturbances, and the

landscape pattern.

Lessons learned from the recovery of anuran communities following abandonment and secondary

succession

Our main research investigated the patterns of recolonization by tropical anurans associated

with forest habitat alteration after the abandonment of tea plantations in the KMFR of the Central

Region of Sri Lanka.

96



Our results revealed that conditions in abandoned agricultural lands in former forest became

increasingly favourable for anurans in successive stages of secondary succession. For example,

relative humidity and soil moisture content increased, whereas air and soil temperature decreased. In

terms of vegetational characteristics, litter cover and depth, crown cover, density of woody trees, girth

at breast height and height of vegetation increased, whereas the density of tea plants decreased.

With increasingly favourable environmental conditions in the abandoned farm plots, anuran

species richness, complexity of species composition, and diversity increased. Furthermore, our results

indicate that the similarity between successional stages decreases as the time since abandonment

increases, indicating that species turnover rate is high. Our findings show that the various species of

anuran species encountered occupy sites with particular physico-chemical, vegetational and structural

characteristics.

Based on our field observations and from information gathered from the local community

such as forest officers, farmers and neighbouring villagers, it became evident that the natural virgin

forest in several areas had already become degraded, through various human actions, before the

establishment of tea plantations. In the Riverstone area, for example, hundreds of hectares of virgin

forest had been entirely cut down to make way for coffee plantations. Furthermore, human-induced

fires had also contributed to vegetational change.

Our field observations revealed that vegetational recovery through natural regeneration and

secondary succession proceeds at a much slower pace in open areas than in closed ones. Open habitat

had been degraded or drastically altered, making it less responsive to secondary colonization. Changes

to the substrate were both physical (erection of stone walls; digging of trenches to combat soil erosion

in the tea plantations) and chemical (higher acidity level of the soil; formation of brick layers). The

poor capacity of the open areas for recovery was also contributed to by the loss of parent trees,

without which there was no possibility of regeneration. Compared to the open areas, the regeneration

of closed areas has been much more rapid. Wind and animals (in particular birds and bats) acted as

seed dispersal agents. The seeds were derived from a wide variety of species growing in the

neighbouring virgin forest.

Our study allows us to make comments pertinent to matters relevant to enhancing the

regenerative potential of the secondary forest. We trust that our suggestions and recommendations can

be implemented in efforts to enhance regeneration efforts in the KMFR as a whole.

The impact of enforcement of conservation legislation

Illegal felling of timber and fuelwood species, the illegal hunting of wild animals, the over

collection of plants and animals have been reduced considerably, mainly as a result of enforcement of

conservation legislation by the State. Because of its unsustainable agricultural practices such as slash

and burn cultivation are now recognized as activities that damage the environment and are prohibited

in many parts of the KMFR (e.g., Laggala and Pallegama).

The virgin forests of Sri Lanka have been owned and managed by the Forest Department of

Sri Lanka since the end of the colonial period. At present, nearly all natural forest habitats are State-

owned and fall under the purview of three institutions: the Divisional Secretaries; the Department of

Wildlife Conservation; and the Forest Department. The main policy-making body for protected areas

in Sri Lanka is the Department of Wildlife Conservation. All legislation has been prepared according

to the FFPO. Current legislation relating to protected areas (buffer zones; jungle corridors; national

parks; nature reserves; refuges; sanctuaries; and marine reserves) is mainly covered by the Fauna and

Flora Protection Ordinance (FFPO)-1937 (Sri Barathi, 1979). This, is an amended form, was approved

by the Cabinet of Ministers on March 12th, 2008. Some of the policies relating to protected areas are

covered by the Management and Wildlife Conservation National Policy. Fines and penalties are

imposed for illegal activities conducted in protected areas mentioned in the ordinance.

Suggestions for improved conservation measures in the KMFR

The results of our studies provide insights that could prove useful for conservation measures

relating to wildlife, including anuran species, in the KMFR. We suggest that agricultural practices

such as tea, tobacco, and cardamom plantations should not be permitted in the remaining virgin forest

habitats, or in formerly forested areas of the KMFR, especially in areas located at 1,000 m a.s.l. or

above. In 2000, the Forest Department declared a Conservation Zone for the KMFR, in regions above

97



1,000 m a.s.l. to protect the forest in order to eliminate cardamom plantation, and to stop slash and

burn cultivation, over-grazing, illegal timber felling, and firewood cutting (Nanayakkara et al., 2009).

This zone should be rigorously enforced.

Priority monitoring

With the ever-increasing loss of habitat and their associated species, ecological monitoring

and research are required to identify the implications of these practices. However, it is neither possible

nor practical to monitor all species, communities or ecosystems, or to conduct field research that

covers all of these areas. Therefore, some kind of prioritization is needed, and such could be given to

regions or areas that have been subjected to the greatest anthropogenic impacts. In this way the effects

of land-use can be managed in a sustainable manner (Spellerberg, 2005). The Convention on

Biological Diversity (CBD) in 1993 (Heywood, 1995) identified priorities for inventorying and

monitoring habitats and ecosystems with high biological diversity and large numbers of endemic or

threatened species (Spellerberg, 2005). Preserving ecosystems involves establishing individual

protected areas and creating networks of protected areas. According to the IUCN definition, a

protected area is “a clearly defined geographical space, recognized, dedicated and managed, through

legal or other effective means, to achieve the long-term conservation of nature with associated

ecosystem services and cultural values (www.iucn.org)”. Protecting areas that contain healthy, intact

ecosystems is the most effective way of preserving overall biodiversity (Primark, 2010).

Another approach to monitoring and much less expense is by analysis of satellite images.

Methods of monitoring deforestation are well developed, can be adapted from global to site scales,

and the images readily available at modest cost (e.g., Eva et al., 2010). A central agency could

undertake such an analysis of KMFR, at, for example, annual intervals and this would not only

provide for trend analysis, but could identify where enforcement is needed.

Since 1975, Dotalugala, a prominent peak in the KMFR, has been recognized as a “Man and

the Biosphere Reserve”. Under this remit the Forest Department is authorized to protect its biological

diversity (Sri Barathi, 1979). In May 2000, this biosphere reserve was included in the 17,500 ha of the

KMFR by Gazette Notification, and according to this, area above 1,067 m a.s.l. became protected.

This declaration stipulates the cessation of anthropogenic activities, including cardamom cultivation,

within the protected area. To protect the biological diversity of the KMFR, several government

departments, non-government organizations and the environmental associations have recognized the

KMFR as a “World Heritage Site”.

Conservation strategies for anuran amphibians in the Riverstone Region – Bellweathers of habitat

recovery

Secondary forest will likely play a major role in the conservation of biological diversity in

tropical areas (Ficetola et al., 2008). There are however, few studies on their potential for supporting

forest species and for the recovery of faunal communities. During our studies of secondary succession

in the KMFR we discovered there is a high potential of recolonization by anurans of abandoned

agricultural plots that undergo extended periods of secondary succession. Furthermore, the positive

relationship between anuran species richness and the vegetational successional stages investigated

reveals that this mountain range should be managed carefully to permit the continuance and

enhancement of these recovery processes. Our studies revealed that a relatively long time period is

required before anuran fauna begin to substantially resemble those of the virgin forest – perhaps 100

years or more. Distance from a potential source area is also important in affecting the rate at which

recolonization takes place.

The conservation of the KMFR should protect the wild fauna and flora. On the other hand, it

should also generate economic benefits for the peripheral human communities. So that conservation

efforts do not negatively affect the lives of humans through restriction of their livelihoods

(Wickramasinghe et al., 2008).

Future of amphibians in the KMFR

Rapid habitat deterioration of many virgin forests has limited the number of studies that have

been able to employ sufficiently robust sample sizes and replicates. Therefore, the effects of habitat

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alteration on species and, in particular, anurans have been poorly documented and should receive

considerably more attention in the future.

We do not know whether current trends will continue as they are, will improve, or will get

worse. But we do know that, in general, amphibians are declining as their habitats are being degraded.

This implies, generally, that if their habitats survive, this may enhance the survival or recovery of

amphibians. Our studies indicate that the anurans of the KMFR are resilient and exhibit strong

tendencies to recolonize areas that revert back to a forested state through the process of secondary

succession. Thus, if land-use patterns in the KMFR are regulated and monitored effectively there is a

reasonable chance that the forest amphibian communities can recover and remain sustainable. As

indicators of the health of environments in general, anurans can then be used, through monitoring

programs, to assist in monitoring the health of the forests in general.

The practical alternative to deforestation is the introduction of economic alternatives that

permit an increase in the protection of virgin forest habitats and promote the restoration of secondary

forests in areas of high amphibian diversity while sustaining the livelihood of the local human

population.

In the light of evidence about the recolonization patterns by anurans of abandoned tea

plantations, the recovery patterns of vegetation, the discovery of several species that have not

previously been recorded from the KMFR, and the discovery of unidentified species (many more

likely await discovery) in the KMFR, we hope that our current study will prompt further research

based on the wildlife of this area. In the meantime, if proper conservation practices are continued,

these will assist in protecting the known and unknown species of wildlife in the KMFR.

We propose that anurans can be used as agents to convey a message to the general public

about the need to conserve these diminishing and invaluable habitats. If we make correct decisions,

act quickly and work accordingly such ends are achievable.

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102


Box turtles in and adjacent to Loktak

Lake, Manipur – India

Manipur is a biodiversity rich state located in the

northeastern part of India that borders Myanmar.

Situated within the western portion of the Indo-

Burma biodiversity hotspot, the state has a large

number of endemic and endangered species. The

state is also prone to habitat destruction due to

rapid clearing of forest for shifting cultivation,

which is a common practice in the hill districts

for agriculture and collection of firewood and

timber. In the valley districts, the entire forest

areas were converted to agricultural fields

leaving only a few remaining green spaces, such

as the sacred groves locally known as Umang

Lais, small hillocks, and Keibul Lamjao

National Park. Loktak Lake (Fig. 1), the largest

lake of Manipur, is situated at the southern part

of the valley and harbours a rich diversity of

both plants and animals. Two important species

of Asian box turtles (Cuora mouhotii and C.

amboinensis), locally known as “thengu” are

found in and adjacent to lake. Cuora

amboinensis is the most abundant among all

chelonians in the state, and Loktak Lake and its

adjoining wetlands have been identified as

potential habitats of the box turtles (Linthoi &

Sharma, 2009).

Loktak Lake is famous for the presence of so-

called “phumdis”, a floating landmass (Singh &

Singh, 1994). There are several thousand

phumdis floating on the lake, and the largest

corresponds to the Keibul Lamjao National Park,

the world’s only floating national park (Walker,

1994). Cuora mouhotii lives there in the floating

landmass as well as on the few islands inside the

lake.

The taxonomy of Asian box turtles (genus

Cuora, family Geoemydidae) is still in flux.

The number of recognized species varies from

ten (Fritz & Havaš, 2007) to 12 (Turtle

Taxonomy Working Group, 2011). All species

are aquatic and semiaquatic and distributed

across Southeast Asia, central to southern China,

and northeast India (i.e., Assam and Manipur

states; Fritz & Havaš, 2007; Spinks & Shaffer,

2007; Linthoi & Sharma, 2009). Throughout

Asia, turtles have been harvested at an

unsustainable rate to satisfy demands for food,

traditional medicine, and the pet trade. All

species of Cuora are listed in the IUCN Red

Data Book and nine are currently listed as

critically endangered. All species are also listed

in Appendix II of the Convention on

International Trade in Endangered Species of

Wild Fauna and Flora (CITES) (UNEP-WCMC

2005; Spinks & Shaffer, 2007).

Figure 1: Loktak Lake, Manipur, India

The turtle populations in the state of Manipur

are one of the least studied among all the turtles

of the country. Major threats to these

populations include illegal exploitation for meat

and eggs, water pollution, and habitat

destruction. Turtles are caught and sold in fish

markets (Fig. 2) across the valley towns of

Manipur. Though the trade is at low scale, the

consumption of meat by the local people is now

becoming an immediate threat to the

diminishing population of turtles in the lake and

adjoining water bodies. Turtles are also used

locally in traditional medicinal practices.

Submerging of peripheral areas of the lake and a

stagnant water body throughout the year due to

construction of Ithai Barrage has led to the



BOX TURTLES IN AND ADJACENT TO LOKTAK LAKE, MANIPUR – INDIA


destruction of the natural habitat of these turtles.

Pisciculture and agriculture in the low lying

submerged areas coupled with extensive use of

pesticides has had a great impact on the turtle

habitat and their survival.

Selling of turtles in the local markets at low

scale is an old tradition followed by local

people. However, consumption of turtle meat is

not too common. In Manipur, the different clans

have a tradition of inhibiting themselves from

consuming specific food items of a particular

species. The Ningthouja clan of the Meiteis of

Manipur considered it a taboo to consume turtle

or tortoise meat (Gupta & Guha, 2002).

Before trade and consumption of turtles

increases further, necessary conservation

strategies should be framed and implemented for

the long term conservation of these two species.

Research and conservation practices should be

initiated in collaboration with universities,

institutes and local NGOs to understand the life

cycles, threats, and present population status.

Involvement of local communities would play

an important role in the protection of the turtles

and their natural habitats at a large scale.

Increase of awareness about conservation and

promotion of research through government and

nongovernment agencies would enable the study

of the biology, distribution, threats, habitat, and

conservation of turtles in Manipur.

Figure 2: A Cuora amboinensis captured by the local

people.

Literature cited Fritz, U. and P. Havaš, 2007. Checklist of

Chelonians of the World. Vertebrate Zoology, 57

(2): 149-368.

Gupta, A. and K. Guha, 2002. Tradition and

conservation in Northeastern India: an ethical

analysis. Eubios Journal of Asian and

International Bioethics, 12: 15-18.

Linthoi, N. and D. K. Sharma, 2009. Turtles and

Tortoises in Manipur. ENVIS Bulletin: Wildlife

and Protected Areas, 12 (1). Wildlife Institute of

India: 49-52.

Singh, H. T. and R. S. Singh. Ramsar sites of

India: Loktak Lake. WWF-India, New Delhi.

Spinks, P. Q. and H. B. Shaffer, 2007.

Conservation phylogenetics of the Asian box

turtles (Geoemydidae, Cuora): mitochondrial

introgression, numts, and inferences from multiple

nuclear loci. Conservation Genetics, 8: 641–657.

Turtle Taxonomy Working Group [van Dijk, P. P.,

J. B. Iverson, H. B. Shaffer, R. Bour and A. G. J.

Rhodin], 2011. Turtles of the world, 2011 update:

annotated checklist of taxonomy, synonymy,

distribution, and conservation status. In: Rhodin,

A. G. J., P. C. H. Pritchard, P. P. van Dijk, R. A.

Saumure, K. A. Buhlmann, J. B. Iverson and R. A.

Mittermeier (eds.). Conservation Biology of

Freshwater Turtles and Tortoises: A Compilation

Project of the IUCN/SSC Tortoise and Freshwater

Turtle Specialist Group. Chelonian Research

Monographs No. 5: 000.165–000.242,

doi:10.3854/crm.5.000.checklist.v4.2011,

http://www.iucn–tftsg.org/cbftt/.

UNEP-WCMC, 2005. UNEP-WCMC Species

Database: CITES Listed Species on the World

Wide Web (http://www.sea.unep-wcmc.org)

Walker, S. (ed.), 1994. Manipur brow-antlered

deer (Cervus eldi eldi) locally known as Sangai: population & habitat viability assessment, Mysore.

Report: August 1994, Coimbatore, India.

Submitted: 11 April 2012, Accepted: 11 June 2012

Sectional Editor: Uwe Fritz

Rajkumar Robindro Singh1,2

and

Khuraijam Jibankumar Singh1,3

1 North East Centre for Environmental

Education & Research (NECEER),

Imphal West 795001, Manipur, India 2 Email: [email protected]

3 Email: [email protected]


Carapacial scute anomalies of star tortoise

(Geochelone elegans) in Western India

The basic taxonomy and classification of reptile

species and genera often use pholidotic

characters. Despite that each species has a

standard pattern, there are always deviant

individuals in terms of scale number, shape,

size, or color. Turtles are excellent models for

the study of developmental instability because

anomalies are easily detected in the form of

malformations, additions, or reductions in the

number of scutes or scales (Velo-Antón et al.,

2011). The normal number of carapacial scutes

in turtles is five vertebrals, four pairs of costals,

and 12 pairs of marginals, a pattern known as

“typical chelonian carapacial scutation”

(Deraniyagala, 1939). Any deviation of

vertebral, costal, or marginal scute numbers or

their pattern represents an anomaly. Zangerl &

Johnson (1957) documented scutation

anomalies in 118 species of turtles belonging to

seven families, with higher levels of carapace

anomalies in aquatic species compared to semi-

aquatic and terrestrial species.

Here, I present some new information on scale

anomaly observed in the Indian Star Tortoise

(Geochelone elegans), especially in western

populations. This species was first described by

Schoepff (1795). It is widely distributed in dry,

deciduous and scrub jungles of India, Sri Lanka

and Pakistan. There are three disjunct

distribution patches (Das, 1995, de Silva, 2003;

Fife, 2007; Frazier, 1992). Geochelone elegans

has a characteristic number of scales/scutes on

the carapace, consisting of five symmetric

vertebrals, four pairs of costals (pleurals),

eleven pairs of marginals, and a single supra-

caudal. A nuchal scute is lacking. On the

plastron there is a pair of gular, humeral,

pectoral, abdominal, femoral, and anal scutes,

along with paired axillary and inguinal scutes

(Das, 1995; Frazier, 1987). De Silva (2003)

provided drawings of carapace and plastron of

the species showing the typical scale

arrangement and the carapace drawings are

from the sources of Deraniyagala (1939). But

the ‘Figure 5’ (on page 13) shows something

else, an illustration which is not a typical scale

drawing of the species. This figure of a tortoise

shows abnormal scales and scutes, especially

vertebral, costal and marginal scutes, which are

in higher numbers than the provided description

of the species by Schoepff (1795).

Observations (see plate 1 for figures)

During the last eleven years (1990-2011), I

have come across many star tortoises in the

wild (n=65) and in captivity (n=135), belonging

to different ages and sizes (from hatchlings to a

55 year old, which was the largest one) (Vyas,

2011). All specimens were bred under natural

conditions (although 5 of the 6 specimens with

anomalies were later kept in captivity). The

details of anomaly of scales/scutes of each

specimen are as follows.

Specimen 1 (S1): An approximately fourteen-

year-old healthy female tortoise found in the wild

(near Timba, Panchmahal District, India) with

abnormal scutes. This female has typical scales

and scutes on the plastron and carapace except for

an extra costal scute on its left side and a

triangular vertebral scute between the 3rd

and 4th

vertebrals (Fig. 1A). This extra costal scute

developed on left side of the animal due to an

extra vertebral scute.

Specimen 2 (S2): A female tortoise, having over

nine growth rings on body scales. This animal had

an extra pair of costal scutes and a vertebral scute

on the carapace (Fig. 1B). The plastron scutes

were normal and in typical shape. This animal

was confiscated by the forest department from a

local pet owner at Vadodara. Such abnormality

of the costal and vertebral scutes might have

possibly resulted from the splitting of one of the

vertebral and costal scutes during the embryonic

development.

Specimen 3 (S3): A six-year-old healthy tortoise

found in captivity (Sayaji Baug Zoo, Vadodara)

with abnormal scutes. This tortoise had typical

TAPROBANICA, ISSN 1800-427X. October, 2012. Vol. 04, No. 02: pp. 105-107, 1 pl.


CARAPACIAL SCUTE ANOMALIES OF STAR TORTOISE


scales and scutes on the plastron, but on the

carapace it had an extra costal scute on its right

side and a triangular vertebral scute of the 4th

vertebral (Fig. 1C). All right side costal scutes

were larger than the left ones, due to this extra

costal scute development on the carapace.

Specimen 4 (S4): A five-year-old specimen from

captivity (private pet owner) having abnormal

scutes on the carapace. This tortoise had typical

scales and scutes on the plastron, but on the

carapace, it had an extra pair of costal scutes and

a large 1st vertebral scute (Fig. 1D). The extra pair

of costal scutes might be a development of

improper split on the 1st vertebral during its

embryonic development.

Specimen 5 (S5): A juvenile captive tortoise

having abnormal scutes on the carapace. This

tortoise had normal plastron, but had an extra

costal scute on its left side and an extra triangular

vertebral scute between the 4th and 5

th vertebrals

(Fig. 1E). All left side costal scutes were

narrower in comparison to the right costals.

Specimen 6 (S6): An over six-year-old healthy

captive tortoise (retrieved from a pet animal

trader) having normal and typical scutes, except

on the carapace. The specimen had an extra

pentagonal scute between the 4th and 5

th

vertebrals and an extra costal scute on its right

side (Fig. 1F).

The scale/scute anomaly was observed in 3% of

specimens. Anomalies were found only in the

carapace, in the shape and size of vertebral and

costals. These instances were recorded in a

wide age span (fourteen- to four-year-old

animals), suggesting that such anomalies have

no negative effect to the health of animals.

The occurrence of anomalies, malformations or

asymmetries in wild animals may serve as an

indicator of developmental instability, a

variable negatively correlated with fitness

(Moller, 1997). Such type of anomaly

phenomenon was earlier reported for star

tortoises by de Silva (1995, 2003), Frazier

(1987) and Fife (2007).

de Silva (1995, 2003) and Frazier (1987) stated

that the numbers of scales and scutes are

constant with hardly any distinct variation in

the species. Fife (2007) mentioned that tortoise

is occasionally seen with irregular scutes, either

an extra scute or a split scute. This condition

occurs in nature but is most commonly seen in

captive hatched specimens.

Frazier (1987) stated after examining 98

specimens (most probably from the western

population only) that “there was a tendency for

an animal with an abnormal number of left

costals to also have an abnormal of right

costals. The same applies for marginals.

Otherwise, there was no tendency for an animal

with an abnormality in one kind of scale to also

have an abnormality in another kind, abnormal

vertebrals do not usually occur with together

abnormal marginals”. Here, what I have found

does not follow the above statement. All six

specimens have abnormal costals (either on the

right side, the left side, or both) and vertebrals

but these do not reflect abnormality with the

marginal scales, except the seam contacts of the

animals.

In general, such irregular scute abnormalities

are caused by multiple genetic, biotic and

abiotic factors. Three non-exclusive sources

have been proposed as the main causes of scute

or scale anomalies in reptiles: (i) temperature

and moisture constraints during incubation

(Lynn & Ullrich, 1950), (ii) damaging effects

of pollution (Bishop et al., 1994, 1998) and (iii)

loss of genetic diversity in bottlenecked or

inbred populations (Schwaner, 1990; Soule,

1979).

Fife (2007) stated that the abnormalities in the

species are a result of higher temperatures

during the incubation. Extreme incubation

temperatures cause irregular scutes or other

deformities. The study of Velo-Antón et al.,

(2011) suggested that genetic factors play an

important role in the origin of anomalies in

wild turtle populations and might serve as an

indirect estimate of fitness in natural

populations, but many factors clearly influence

embryonic development and thus, disentangling

what factors influence the occurrence of

carapace scute anomalies in wild populations

requires further studies using integrative

approaches.

Acknowledgements

I am thankful to Superintendent of Surat Zoo

and Curator of Sayaji Baug Zoo, Vadodara

along with a number of private pet owners and

pet traders from Gujarat State for allowing me

to study and examine the tortoises from their

VYAS, 2012


collections. Thanks to Deputy Conservator

Forest (wildlife) and Range Forest Officers,

Forest Department, Vadodara, Gujarat State for

allowing me to examine few confiscated

specimens and support. Finally Richard Gemel

(NMW – Austria) and Johanna Bleecker

(McGill University – Canada) are

acknowledged for reviewing the manuscript

and valuable comments.

Literature Cited Bishop C. A., G. P. Brown, R. J. Brooks, D. R.

Lean and J. H. Carey, 1994. Organochlorine

contaminant concentrations in eggs and their

relationship to body size, and clutch

characteristics of the female common snapping

turtle (Chelydra serpentina serpentina) in lake

Ontario, Canada. Archives of environmental

contamination and toxicology, 27: 82–87.

Bishop, C. A., P. Ng, K. E. Pettit, S. W. Kennedy

and J. J. Stegeman, 1998. Environmental

contamination and developmental abnormalities

in eggs and hatchlings of the common snapping

turtle (Chelydra serpentina serpentina) from the

Great Lakes-St. Lawrence River basin (1989–91).

Environ Pollution, 101: 143–156.

Das, I., 1995. Turtles and Tortoises of India.

World Wide Fund for Nature- India & Oxford

University Press, Bombay: 176.

Deraniyagala, P. E. P., 1939. The Tetrapoda

reptiles of Ceylon Vol. 1. Testudinates and

Crocodilians. Colombo Museum: 412.

de Silva, A., 1995. The status of Geochelone

elegans in north western province of Sri Lanka:

preliminary findings. Proceedings International

Congress of Chelonian Conservation. Soptom, Gonfeeron: 47-49.

de Silva, A., 2003. The Biology and Status of the Star Tortoise (Geochelone elegans, Schoepff,

1795) in Sri Lanka. Protected Area Management

and Wildlife Conservation Project, Ministry of

Environment and Natural Resources, Sri Lanka:

100.

Fife, J. D., 2007. Star Tortoises: The Natural

History, Captive Care, and Breeding of Geochelone elegans and Geochelone platynota.

Living Art Publishing, USA: 116.

Frazier, J., 1978. Biology and conservation of

Indian turtles and tortoises. Interim report to the

American Institute for Indian studies, New Delhi:

64.

Frazier, J., 1992, Management of tropical

chelonians: Dream or Nightmare? In: Tropical Ecosystems: Ecology and Management, Singh K.

P. and J. S. Singh (eds.). Wiley Eastern Limited,

New Delhi: 125-135.

Lynn, W. G. and M. C. Ullrich, 1950.

Experimental production of shell abnormalities in

turtles. Copeia, 1950: 253–263.

Moller, A. P., 1997. Developmental stability and

fitness: A review. American Nature, 149: 916–

932.

Schoepff, J. D., 1795. Naturgeschichte der

Schildkroten mit Abbildungen erlauter (1792-

1801). Funfter Heft. Erlangen, Johann Jakob

Palm: 89-136+17-25pls.

Schwaner, T. D., 1990. Geographic variation in

scale and skeletal anomalies of tiger snakes

(Elapidae, Notechis scutatus ater complex) in

Southern Australia. Copeia, 1990: 1168–1173.

Soule, M. E., 1979. Heterozygosity and

developmental stability: another look. Evolution,

33: 396–401.

Velo-Antón, G., C. G. Becker and A. Cordero-

Rivera, 2011. Turtle Carapace Anomalies: The

Roles of Genetic Diversity and Environment.

PlosOne, 6 (4): 1-11.

Vyas, R., 2011. Record size of Indian Star

Tortoise: Geochelone elegans (Schoepff, 1795).

Russian Journal of Herpetology, 18 (1): 47-50.

Zangerl, R. and R. G. Johnson, 1957. The nature

of shield abnormalities in the turtle shell.

Fieldiana Geology, 10: 341–362.

Submitted: 26 March 2012, Accepted: 28 October 2012

Sectional Editor: Uwe Fritz

Raju Vyas

No. 505, Krishnadeep Tower, Mission Road,

Fatehgunj, Vadodara, Gujarat, India.


TAPROBANICA VOL. 04: NO. 02

PLATE 01

Figure 1: Geochelone elegans, A: extra triangular vertebral and costal (S1); B: extra vertebral and a pair of costal (S2); C:

extra vertebral and an extra left costal (S3); D: extra pair of costal and large 1st vertebral scute (S4); E: extra costal on the left

and an extra triangular vertebral scute between 4th

and 5th

vertebrals (S5); F: extra pentagon shaped vertebral and an extra

costal on its right (S6).

A B

C E

D F


Red Giant Flying Squirrel (Petaurista

petaurista) in Assam, India

Red Giant Flying Squirrel (Petaurista

petaurista) is widely distributed throughout

Asia in habitat types including moist evergreen

broadleaf forest, temperate forest, and scrub

forest in both lowlands and montane areas. It is

categorized as Least Concern on the IUCN Red

List (Walston et al., 2008). Hitherto, no

systematic studies have been done on P.

petaurista in India. We assessed the density of

individuals and habitat selection of this species

in different habitat types experiencing various

degrees of disturbance. We conducted our study

in the Jeypore Reserve Forest (JRF; 108 km2) of

Assam, India (27° 06’-27°16’ N, 95° 21’-95°

29’ E; 120-1600 m a.s.l), a rainforest patch of

the Eastern Himalayan biodiversity hotspot

region (Fig. 1).

Figure 1: Location of study trails in JRF

We classified regions of our study site as highly

disturbed (HD) if frequency of human activities

was high (e.g., lopping, traffic on forest roads,

livestock grazing) and the canopy was open

[mean tree canopy cover <40%]), moderately

disturbed (MD) if low frequencies of human

activities were observed with moderate canopy

closure (mean tree canopy cover 40–75%), or

less disturbed (LD) if human activities were not

a regular occurrence but people used the forest

only during a particular time of the year and the

canopy was closed (mean tree canopy cover

>75%). Tree canopy cover was measured by

placing ten transects of 20 m x 20 m randomly

in each habitat type. We walked a total of 11

trails in three habitat types (LD = 4; MD = 5;

HD = 2) covering a total distance of 90 km from

October 2009 to December 2009 (Table 1).

Sightings of P. petaurista were recorded on the

trails by adopting the “spotlight counts” method

(Lee et al., 1993) using PetzelTM

headlamps. We

surveyed eleven trails each month between

1800-2400 hrs, when the squirrels are most

active (Lin et al., 1988). A total of 33 night

walks with 198 hours of effort were conducted.

Each survey night a group of observers walked a

single trail at a speed of 1 km/hr or more.

Mostly the LD and MD trails were unsafe to

survey at night because of the armed insurgents

and high elephant density, reducing survey time.

On confirmation of P. petaurista, we attempted

to identify the number of individuals, perching

height on the tree, and GPS location. The index

used for estimating relative abundance for

nocturnal mammals (Das et al., 2009;

Sutherland, 2002) was used for calculating P.

petaurista encounter rate or ‘sightings’ per km.

We used the SPSS 16.0 software for statistical

analysis. We also calculated and plotted

differences in encounter rate, group size, and

percentage of sightings in relation to the

percentage canopy cover among the three forest

habitat types.

A total of 78 individuals of P. petaurista were

recorded over 90 km of trail (Table 1). The

overall average encounter rate was 0.85

individuals/km with a mean perching height of

20.21 ± 1.15 m. Average encounter rate of P.

petaurista varied among the three habitat types,

being highest in LD (1.25 individuals / km; n =

24) followed by MD (1.02 individuals / km; n =

48) and HD (0.27 individuals / km; n = 6; Table

TAPROBANICA, ISSN 1800-427X. October, 2012. Vol. 04, No. 02: 108-111.


RED GIANT FLYING SQUIRREL IN A RAINFOREST OF ASSAM - INDIA


1). The sighting height (m) on a tree also varied

among the three habitats, with a maximum in

MD (24.61 ± 1.11 m), followed by LD (16.10 ±

1.79 m), and HD (14.60 ± 1.72 m). Mean tree

canopy cover in HD habitat was 37.5%, while it

was 53% for MD and 77.5% for LD habitat.

Recorded percentage of individuals sighted in

relation to the percentage of canopy cover in

three habitat types is shown in Figure 2. Field

methods for studying squirrels are limited

(Weigl & Osgood, 1974) because of their

arboreal nature (Lee et al., 1986; Muul & Lim,

1978). The recorded encounter rate of P.

petaurista from our study varied among the

different habitat types, being highest in LD,

followed by MD and HD. This is in

confirmation with other studies [Barrett (1984),

Lee et al. (1993), Pliosungnoen et al. (2010),

Radhakrishna et al. (2006)]. There was,

however, no resemblance with the work of

Barrett (1984) in Malaysia, where he had

reported population densities of Petaurista

species to be higher in logged forests than in

unlogged forests. We recorded an average

encounter rate of 0.85 individuals/km which is

slightly higher than that of 0.37 individuals/km

reported (Radhakrishna et al., 2006) in JRF,

Assam, India, and 0.36 individuals/km reported

(Pliosungnoen et al., 2010) in Thailand. A

survey from Taiwan (Lee et al., 1993) reported

the highest average encounter rate of 1.21

individuals/km as compared to our present study

(Table 2).

Table 1: Detailed characterization of 11 forest trails walked in JRF (MD = moderately disturbed; LD = less

disturbed; HD = highly disturbed; BP = bridle path; FR = forest road; MR = motorable road).

Table 2: Comparative accounts of P. petaurista encounter rate reported from its distributional range (*Average

encounter rate reported from JRF).

Study site

Encounter rate estimate

(individual/km) (Habitat

type)

Average encounter

rate from the

study

Surveyor

Chitou Experimental

Forest

0.47 (Conifer forest)

1.96 (Hardwood forest) 1.21 Lee et al., 1993

Assam and Meghalaya,

India

0.10-0.77 (various forest

types) 0.37*

Radhakrishna et al.,

2006

Khao Ang Rue Nai

Wildlife Sanctuary,

Eastern Thailand

0.36 (Primary forest) 0.36 Pliosungnoen et al.,

2010

Trail ID

(as in

Fig.1)

Habitat

type

Trail

length

(km)

Total effort

walk (L)

Total

individuals

sighted (n)

Encounter

rate (n/L)

Average

encounter

rate (SD)

Remarks

T 1 MD 4 12 15 1.25

1.02 (0.27)

FR

T 2 MD 3 9 6 0.67 FR

T 8 MD 3 9 12 1.33 BP

T 9 MD 3.5 10.5 9 0.86 MR

T 10 MD 2 6 6 1.00 BP

T 6 LD 2 6 6 1.00

1.25 (0.64)

BP

T 7 LD 2 6 9 1.50 BP

T 4 LD 1 3 6 2.00 BP

T 3 LD 2 6 3 0.50 BP

T 5 HD 3.5 10.5 3 0.29

0.27 (0.02)

MR

T 11 HD 4 12 3 0.25 BP

Overall 90 78 0.85 (0.51)

RAY ET AL., 2012


Figure 2: Percentage of individuals of P. petaurista

sighted in different habitat types having varied

percentage of canopy cover.

In general squirrels are very much susceptible

to habitat destruction and heavily rely on tall

trees for both nesting and feeding (Lee et al.,

1986). Thus, forest structure plays an important

role in the habitat selection of arboreal

mammals (Datta & Goyal, 1996; Lemos &

Strier, 1992). The high encounter rate in the LD

habitat, which is similar to that of Lee et al.

(1993) and Pliosungnoen et al. (2010), could be

due to the presence of dense forest and

homogeneous canopies that allow P. petaurista

to move and feed with limited exposure to

predators. Increased disturbance in HD habitat

due to anthropogenic threats, such as logging,

NTFP collection, livestock grazing, and

encroachment for establishment of tea estates

(Kakati, 2004), may have affected P. petaurista

negatively.

Acknowledgements

We sincerely thank the Chief Conservator of

Forest and Chief Wildlife Warden of Assam for

giving us necessary permission to carry out the

survey, Divisional Forest Officers of

Dibrugarh, Digboi Divisions and Range

Officers of Jeypore for logistic supports. R.

Munda, S. Barman, S. Kar and R. Sonowal for

helping us in the field. Also, V. Krishna (State

University of New York, USA) is

acknowledged for his technical support. Special

thank to Primate Research Centre, Margot

Marsh Biodiversity Foundation and U.S. Fish

& Wildlife Service for sponsoring and the

financial support. Finally we thank Colin

Chapman and Michael Wasserman (McGill

University – Canada) for reviewing the

manuscript.

Literature Cited Barrett, E., 1984. The ecology of some nocturnal,

arboreal mammals in the rainforests of

peninsular Malaysia. Ph.D. Thesis, University of

Cambridge. Cambridge, UK: 187-226.

Das, N., J. Biswas, J. Das, P. C. Ray, A. Sangma

and P. C. Bhattacharjee, 2009. Status of Bengal

slow loris Nycticebus bengalensis (Primates:

Lorisidae) in Gibbon Wildlife Sanctuary, Assam,

India. Journal of Threatened Taxa, 1 (11): 558–

561.

Datta, A. and S. P. Goyal, 1996. Comparison of

forest structure and use by the Indian giant

squirrel (Ratufa indica) in two riverine forests of

Central India. Biotropica, 28: 394-399.

Kakati, K., 2004. Impact of forest fragmentation

on the hoolock gibbon in Assam, India. Ph.D.

thesis, University of Cambridge, Cambridge,

United Kingdom: 12-66.

Lee, P. F., D. R. Progulske and Y. S. Lin, 1986.

Ecological studies on the two sympatric giant

flying squirrels (Petaurista petaurista and P.

alborufus) in Taiwan. Bulletin of the Institute of

Zoology, Academia sinica, 25 (1): 113-124.

Lee, P. F., D. R. Progulske and Y. S. Lin, 1993.

Spotlight counts of gaint flying squirrels

(Petaurista petaurista and P.alborufus) in

Taiwan. Bulletin of the Institute of Zoology, Academia Sinica, 32 (1): 54-61.

Lemos De Sa, R. M. and K. B. Strier, 1992. A

preliminary comparison of forest structure and

use by two isolated groups of woolly spider

monkeys, Brachyteles archanoides. Biotropica,

24: 455-459.

Lin, Y. S., L. Y. Wang and L. L. Lee, 1988.The

behaviour and activity pattern of giant flying

squirrels (Petaurista p. grandis). Quarterly Journal Chinese Forestry, 21 (3):81-94 (in

Chinese, English abstract).

Meijaard, E., D. Sheil, R. Nasi, D. Augeri, B.

Rosenbaum, D. Iskandar, T. Setyawati, M.

Lammertink, I. Rachmatika, A. Wong, T.

Soehartono, S. Stanley and T. O’Brien, 2005. Life

after logging: reconciling wildlife conservation and production forestry in Indonesian Borneo.

Centre for International Forestry Research,

Bogor, Indonesia: 30-34.

Muul, I. and L. B. Lim, 1978. Comparative morphology, food habits, and ecology of some

Malaysian arboreal rodents. In: The ecology of

RED GIANT FLYING SQUIRREL IN A RAINFOREST OF ASSAM - INDIA


arboreal folivores, G. G. Montgomery, (ed.).

Smithsonian Institute, Washington D.C. 361-368.

Nandini, R. and N. Parthasarathy, 2008. Food

habits of the Indian giant flying squirrel

(Petaurista philippensis) in a rain forest fragment,

Western Ghats. Journal of Mammalogy, 89

(6): 1550-1556.

Pliosungnoen, M., G. Gale and T. Savini, 2010.

Density and microhabitat use of Bengal slow loris

in primary forest and non-native plantation forest.

American Journal of Primatology, 72: 1108–

1117.

Radhakrishna, S., A. B. Goswami and A. Sinha,

2006. Distribution and conservation of Nycticebus

bengalensis in Northeastern India. International Journal of Primatology, 27:971–982.

Robert, D. and P. DeVries, 1999. Tropical Rain

Forest Structure and the Geographical

Distribution of Gliding Vertebrates. Biotropica, 22 (4): 432- 434.

Sutherland, W. J., 2002. Mammals. In: Ecological censusing technique, Sutherland, W. J. (ed.).

Cambridge University Press: 260–278

Walston, J., J. W. Duckworth, S. U. Sarker and S.

Molur, 2008. Petaurista petaurista. In: IUCN

2011. IUCN Red List of Threatened Species.

Version 2011.2. <www.iucnredlist.org>.

Downloaded on 10 April 2012.

Weigl, P. D. and D. W. Osgood, 1974. Study of

the northern flying squirrel, Glaucomys sabrinus,

by temperature telemetry. The American Midland

Naturalist Journal, 92: 482-486.

Submitted: 14 May 2012, Accepted: 26 July 2012

Sectional Editor: Vincent Nijman

P. C. Ray1,5

, A. Kumar1, J. Biswas

2, N. Das

2,3,4,

A. Sangma3, K. Sarma

1 and M. Krishna

1

1 North Eastern Regional Institute of Science &

Technology, Arunachal Pradesh, India. 5Email: [email protected]

2 Primate Research Centre Northeast, Assam,

India.

3

Department of Zoology, Gauhati University,

Assam, India.

4 Department of Anthropology, Oxford

Brookes University, United Kingdom.

111


Rhesus macaque and associated problems

in Himachal Pradesh - India

Conflict between humans and primates is

common and increasing (Estrada et al., 2012;

Nijman, 2010; Sharma et al., 2011). Of the

nearly 225 living species of nonhuman primates,

three Indian species (i.e., rhesus macaque

(Macaca mulatta), bonnet macaque (Macaca

radiata) and the hanuman langur

(Semnopithecus entellus) have become

urbanized. Out of these, rhesus macaques and

hanuman langur share food and space with

humans in rural and urban areas and are often

reported in conflict with humans (Pirta, 2002;

Singh, 2000). Conflicts often occur when these

primates raid crops of farmers (Forthman, 1986;

Hill, 2000; Siex & Struhsaker, 1999).

Primate conservation in Himachal Pradesh is

facing a particular dilemma. Rhesus macaques

and hanuman langur often live in temples and

towns, where they are worshiped, provisioned

and protected by local people (Rajpurohit et al.,

2006) as they are considered the image of God

Hanuman (Jolly, 1985). However, due to their

crop raiding they are disliked in the areas of

intensive agriculture, horticulture, and

plantations (Roonwal & Mohnot, 1977). The

success of any conservation policy for primates

depends upon resolving this conflict (Pirta et al.,

1995).

Here we present baseline data on distribution of

rhesus macaques and hanuman langur and in

forested and non-forested areas of Himachal

Pradesh and discuss the intensity of the human-

nonhuman primate problem both in terms of

geographical area and economic loss. Ecological

causes which lead to the human-monkey conflict

were observed and possible measures are

proposed to deal with this conflict.

Himachal Pradesh is mainly a hilly state with

elevations ranging from 350 to 6500m lying

between 30o

22’ and 33o12’ N and from 75

o 47’

to 79o

04’ E in the lap of the northwest

Himalayas. It is divided by a general increase in

elevation from west to east and from south to

north into four biogeographical regions viz.,

Shiwalik or Outer Himalayas, Lower or Lesser

Himalayas, Higher or Greater Himalayas and

Trans Himalayas. The Shiwalik ranges, the

southernmost zone, are 40 to 60 km wide and

comprise several highly eroded low ridges. A

zone of medium to high ranges, 80 km wide, the

Lesser Himalaya, runs north of the Shiwalik and

parallel to the main range. The Great Himalayan

ranges lie just towards the North of the

Chandrabhaga River in Lahaul-Spiti and Pangi

region of Himachal Pradesh. This range is nearly

24 km wide and rises up to an elevation of over

6000 m. The Spiti area of the state constitutes a

separate and distinct unit, the Trans Himalayas.

Varied physiographic and climatic factors have

given rise to the diverse natural ecosystems

found in this region (Mahabal, 2005; Mehta,

2005; Mehta & Julka, 2002).

Surveys were conducted from October 2004 to

September 2006 with the help of local

volunteers of Himachal Gyan Vighan Samiti

(HGVS), a state social organisation encourages

scientific attitudes. Localities were selected on

the basis of parameters like access by motor

road or tracks, importance due to particular

habitat, altitude, status of locality in district and

calls from local people complaining about

monkey menace. Two workshops (2 and 9

October 2005) were also held to analyse and

evaluate observations at Shimla with different

groups of volunteers. Direct interviews were

conducted with local people in all localities in

the local dialect to learn about interaction of

rhesus macaque. This helped find groups of

monkeys after reaching each locality. In

addition, extensive group discussions were

conducted. Some assessments of rhesus

macaque crop damage were done by

categorizing the damage as heavy destruction

(above 80%), medium (between 40 to 80%) or

low (below 40 %).



RHESUS MACAQUE IN HIMACHAL PRADESH - INDIA


We documented that out of 3243 panchayats of

the state, 2301 was affected by monkey crop

damage. Panchayats are non-partisan councils

that settle disputes between individuals and

villages across a prescribed area. Of those

affected, in 1017 the intensity of damage was

less than 40%, in 670 it was between 40-80%,

and in 470 80% of crops were destroyed by

monkeys. In total, 93.89% of all panchayats

were affected by the monkeys. It was followed

by Kangra (90.79%), Solan (87.2%) and

Sirmour (80.26%) Panchayat. The monkey crop

raiding was not recorded in any of the

panchayats of Lahaul, Spiti, and Kinnaur (Table

1). Conservative estimates put the loss in USD

150,000 to horticulture, USD 200,000 to

agriculture and USD 150,000-200,000 to other

sectors. In Bilaspur district all the 38 panchayats

had high level of crop damage. It was followed

by Sirmour where 58.47% of the affected

panchayats, Chamba (49.23%) and Shimla

(42.23%) had high levels (> 80%) of the crop

damage. Despite the highest percentage of

affected panchayats in Hamirpur, the percentage

of highly affected panchayats (crop damage

>80% of area) was only 6.05% (Table 1). The

threat posed by macaques can be placed in

perspective when one realizes that 84% families

in the state possess just 1 acre of agricultural

land and 70% people depend on agriculture and

horticulture. This forces people to keep their

land vacant which is a dangerous in a land-use

based economy, like that of Himachal Pradesh.

Table 1: Monkey affected Panchayats in Himachal Pradesh

District Total no. of

Panchayats

No. of affected

Panchayats

(%)

Level of the damage to crop

(Number of Panchayats)

Low

(<40 %)

Medium

(40-80%)

High

(>80 %)

(%)

Bilaspur 151 38

(25.17) - -

38

(100)

Chamba 283 135

(47.7) 28 40

67

(49.23)

Hamirpur 229 215

(93.89) 148 54

13

(6.05)

Kangra 760 690

(90.79) 300 225

165

(23.91)

Kinnaur 65 - - - -

Kullu 204 139

(68.14) 119 20 -

Lahul & Spiti 41 - - - -

Mandi 473 347

(73.36) 114 187

46

(13.26)

Shimla 363 206

(56.75) 19 100

87

(42.23)

Sirmaur 228 183

(80.26) 26 50

107

(58.47)

Solan 211 184

(87.2) 142 42 -

Una 235 164

(69.79) 40 52

72

(43.9)

Total 3243 2301

(70.95) 936 770 595

We found that diminishing food in their natural

habitat is one of important cause of their crop

raiding. During last few decades, availability of

a food base in forest areas has decreased due to

fragmentation and continuous degradation of

broad leaved and evergreen forests, as well as

monoculture practices of conifers (Wada, 1983

& 1984).

Conflicts between humans and monkeys and

other wild animals are a manifestation of a

larger ecological crisis. Wild animals have

moved out of wild habitats to human habitation

due to rising human population, increased and

constant human interference in the wildlife

habitats and continuously declining forest cover.

An estimate of Forest Survey of India indicates

that during 2000-2003 there was decline of 1453

SINGH & THAKUR, 2012


km2 in dense forest category and increase in

open forest category by 1446 km2 (Table 2).

There is heavy demand for horticultural land

(Singh, 1991), and the emphasis is on economic

crops and other developmental activities (Vaidya

& Sharma, 1994). This may be detrimental to

both rhesus macaque and hanuman langur

populations. Unlike many other primates, rhesus

macaques are well adapted to life near humans

and can thrive in highly disturbed environments.

48.5% of rhesus macaques in northern India live

in villages, towns, cities, temples and railway

stations. About 37.1% of the population lives

with some human contact on roadsides and canal

banks and only 14.4% of the rhesus macaques in

the northern part of the country live in isolation

from humans and do not rely on them at all for

food (Southwick & Siddiqi, 1994). Rhesus

macaques derive, both directly and indirectly, a

substantial part of their diet from human

activities (Richard et al., 1989). In fact, up to

93% of their diet can be from human sources,

either from direct handouts or from agricultural

sources (Southwick & Siddiqi, 1994).

Table 2: Change in nature of forest over the period

2000 to 2003 in Himachal Pradesh (SFR, 2003).

Nature of

forest

Area under forest

(sq. km) in years Change

2000 2003

Dense 10429 8976 -

Open 3931 5377 +

Total 14360 14353 -7

One of the most important reasons for rise in

conflict between humans and nonhuman

primates is the rapid growth in population of

monkeys due to easily available food resources

near human settlements. In 1980, Himachal

Pradesh had 60,000 monkey population, but this

rose to 317, 112 in 2004) and there was a growth

of 530% between 1908 and 2004 (Table 3). This

is far greater than the carrying capacity of the

state (Mohnot et al., 2005) and if their growth

rate is not checked, it will reach alarming

proportions in the near future.

One of the important factors for this increase is

the sharp decline in the predator population.

Potential predators include raptors, dogs,

weasels, leopards, tigers, sharks, crocodiles, and

snakes (Fooden, 2000). Leopards are numerous

in Himachal Pradesh, but they are unable to

check the population growth of monkeys due to

monkeys association with human settlements.

Table 3: Growth of Rhesus Monkey population in

Himachal Pradesh (FD, 2006)

Year of

assessment Population

1964-65 60,000 - 70,000

(forest rhesus population)

1988-89 155,000

1995 223,014

2004 317,112

Entry of monkeys into human habitations for

food has lead to their dependence on

cooked/processed food. Devotees and animal

lovers feel gratified in feeding monkeys in

temples, highways or roof tops and consider it a

noble deed. As a result, monkeys have become

habitual of snatching food from people,

attacking them, in extreme cases taking lives. In

places, particularly between Solan and Shimla

on National Highway 22, they sit along the road

and often cause accidents.

Increase in population of monkeys is attributable

to other factors also. One of the factors is ban on

the export of monkeys for biomedical research.

Before 1978, India was the largest exporter of

monkeys, exporting 60-70 thousands monkeys

per year (Southwick & Siddiqi, 2001). Due to

ban on their export in 1978 and their adaptability

to human-disturbed environments, the Indian

population of rhesus macaque is increasing

(Rao, 2003). Various body parts of monkeys are

still used as an effective experimental medium

for characterization of various human pathogens

(Ahamed et al., 2004; Mehedi et al., 2002;

Shafee & AbuBakar, 2011) and lifting the ban

on export of monkeys from India would help

control their population.

A thorough understanding of potential risks and

perceptions by local people are important factors

in any management strategy (Madden, 2004).

Restoration of their natural habitat in densely

populated areas may decrease conflict. In the

long-term, management will be necessary to

conserve healthy populations of rhesus

macaques and prevent persecution by humans

from being a threat to their survival (Muroyama

& Eudey, 2004). Assessment of public opinion

is needed for effective management of man-

monkey conflict (Marchal & Hill, 2009; Isabirye

et al., 2008; Eudey, 2008).

In a human population of 6,800,000 in Himachal

Pradesh, monkey population is 317,000 (2004

Forest department survey estimates) and must

http://pin.primate.wisc.edu/factsheets/glossary#195

RHESUS MACAQUE IN HIMACHAL PRADESH - INDIA


have proportionately increased by now. This is

one of the largest concentrations of monkeys; in

fact there is 1 monkey for every 18 humans. The

state forests cannot support such a large

concentration of monkeys, therefore they are

posing a grave threat to agriculture. Recently,

human-wildlife conflict has increased

alarmingly and in the absence of an appropriate

management plan this problem is only going get

worse in future. Today, crop raiding monkeys

are the biggest and most urgent issue troubling

farmers in Himachal Pradesh.

Acknowledgements

The authors are grateful to the Chairman,

Department of Biosciences, Himachal Pradesh

University, Shimla for encouragements. Thanks

are also due to Himachal Gyan Vighyan Samiti

for field assistance provided in the form of

volunteers. Finally Michael Wasserman (McGill

University) for reviewing the manuscript.

Literature cited Ahamed, T., K. M. Hossain, M. M. Billah, K. M.

D. Islam, M. M. Ahasan and M. E. Islam, 2004.

Adaptation of Newcastle Disease Virus (NDV) on

vero cell line. International Journal of Poultry

Science, 3 (2): 153-156.

Estrada, A., B. E. Raboy and L. C. Oliveira, 2012.

Agroecosystems and primate conservation in the

tropics: a review. American Journal of

Primatology, published online: 17 may 2012.

Eudey, A. A., 2008. The crab eating macaque

(Macaca fasciclais): widespread and rapidly

declining. Primate Conservation, 23: 129-132.

FD (Forest Department), 2006. Himachal Pradesh,

Shimla: 50-51.

Fooden, J., 2000. Systematic review of the rhesus

macaque, Macaca mulatta (Zimmermann, 1780).

Field Zoology, 96: 1-180.

Forthman, Q. D. I., 1986. Activity budgets and

consumption of human food in two troops of

baboons, Papio anubis, at Gilgil, Kenya. In: Else,

J. G. and P. C. Lee (eds.). Primate Ecology and

Conservation. Cambridge University: 221-228.

Giriraj, A., S. Babar and C. S. Reddy, 2008.

Monitoring of Forest Cover Change in Pranahita

Wildlife Sanctuary, Andhra Pradesh, India Using

Remote Sensing and GIS. Journal of Environmental Science and Technology, 1: 73-79.

Hill, C. M., 2000. Conflict of interest between

people and baboons: Crop raiding in Uganda.

International Journal of Primatology, 2: 299-315.

Isabirye-Basuta, G. M. and J. S. Lwanga, 2008.

Primate population and their interactions with

changing habitats. International Journal of Primatology, 29:35-48.

Jolly, A., 1985. The evolution of primate behavior,

(2nd edition), Macmillan, New York: 416.

Lin, Z-S. and H-Y. Liu, 2006. Biodiversity

Response to Human-Caused Habitat Destruction in

Different Eras. Trends in Applied Sciences Research, 1: 162-171.

Lindburg D. G., 1971. The rhesus monkey in north

India: an ecological and behavioral study. In:

Rosenblum L.A. (ed.). Primate behavior:

developments in field and laboratory research.

Academic Press, New York: 106.

Maan, M. A. and A. A. Chaudhry, 2001. Wildlife

Diversity in the Punjab (Pakistan). Journal of

Biological Sciences, 1: 417-420.

Madden, F., 2004. Creating coexistence between

humans and wildlife. Global perspective on local

efforts to address human wildlife conflict. Hum

Dim Wildlife. 9: 247-257.

Mahabal, A., 2005. Aves. In: Fauna of Western

Himalaya. Zoological Survey of India: 275-339.

Makwana S. C., 1978. Field ecology and behavior

of the rhesus macaque (Macaca mulatta): Group

composition, home range, roosting sites, and

foraging routes in the Asarori Forest. Primates, 19

(3): 483-92.

Mani, A., 1981. The Himalayan aspects of change.

India International Centre, New Delhi: 481.

Marchal, V. and C. Hill, 2009. Primate crop-

raiding; A study of local perceptions in four

villages in north Sumatra. Indonesia. Primate

conservation, 24: 431-435.

Mehedi, M., K. M. Hossain, M. J. F. A. Taimur, B.

K. Sil and M. R. Islam, 2002. Haemagglutination

antigen preparation of Newcastle Disease Virus on

vero cell line. Online Journal of Biological Sciences, 2 (10): 648-649.

Mehta, H. S., 2005. Fauna of Western Himalaya

(Part-2): Himachal Pradesh. Zoological survey of

India: 1-4.

115

SINGH & THAKUR, 2012


Mehta, H. S. and J. M. Julka, 2002. Mountains:

Northwest Himalaya. In: Alfred, J. R. B., A. K.

Das and A. K. Sanyal (eds.). Ecosystems of India.

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Mohnot, S. M. and A. K. Chhangani, 2005.

Monkey Menace in Himachal Pradesh, Report

prepared by the Committee appointed by the

AWBI-Ministry of Environment & Forests,

Primate Research Centre: 1-4.

Muroyama, Y. and A. A. Eudey, 2004. Do

macaque species have a future? In: Thierry B., M.

Singh and W. Kaumanns (eds.). Macaque

societies: a model for the study of social

organization. Cambridge University: 328-332.

Narwade, S. S., G. A. Jathar and A. R. Rahmani,

2006. Himachal Pradesh. In: Bibliography of the

birds of North India. Buceros, 11 (1): 34-54.

Nijman, V. and K. A. -I. Nekaris, 2010. Testing a

model for predicting primate crop-raiding using

crop- and farm-specific risk values. Applied

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1995. Management of the rhesus monkey Macaca mulatta and Langur Presbytis entellus in Himachal

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106.

Rajpurohit, L. S, A. K. Chhangani, R. S.

Rajpurohit, N. R. Bhaker, D. S. Rajpurohit and G.

Sharma, 2006. Man monkey conflict and

urbanization in non human primates. International Journal of Primatology, 27 (1): 1-17.

Rao, A. J., 2003. Use of nonhuman primates in

biomedical research in India: current status and

future prospects. In: Vaupel S. (ed.). International perspectives: the future of nonhuman primate

resources. Washington DC: 21-28.

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1989. Weed macaques: the evolutionary

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2011. Study of man-monkey conflict and its

management in Jodhpur, Rajasthan, India. Journal

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1009-1020.

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Distributors, Dehradun: 1251.

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commensalisms: the rhesus monkey in India.

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conservation and management of primates in India.

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areas (a case study of District Shimla, HP).

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monkey at Kumaon Himalaya. Journal of Bombay

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355-362.

Submitted: 29 May 2012, Accepted: 10 August 2012

Sectional Editors: Colin Chapman & Lee Harding

Vikram Singh1,2

and M.L. Thakur1

1 Department of Biosciences,

Himachal Pradesh University, Shimla 171 005, India 2 Email: [email protected]

116


Cannibalism of Indian Palm Squirrel

(Funambulus palmarum)

The palm squirrel is one of the common small

mammals in Sri Lanka and the Indian Palm

Squirrel (Funambulus palmarum) is the

commonest of all being distributed throughout

the island. All palm squirrels are essentially

herbivores, however diet varies depending on

the species. F. palmarum has a broad,

opportunistic diet, consuming a range of foods

that vary depending on season (Phillip, 1980).

Its diet includes nuts, a range of seeds, fruits,

flowers, young shoots, barks, lichens and it

occasionally eats insects such as termites and

beetles (Philiip, 1980). Some semi-tame

individuals in the urban areas are fond of bread

and rice (Phillip, 1980). We were able to

observe cannibalistic behavior of this species

from an anthropogenic habitat and this is the

first record on cannibalism of Indian Palm

Squirrel reported from Sri Lanka. The

observation was made on 25 August 2010 at

15:55 hr at an anthropogenic habitat at

Kesbawa of Colombo District of Sri Lanka. A

palm squirrel nest had been built 2.3 m above

ground on a lamp on the wall of a verandah.

Two litters inhabited the nest and were 5 days

old on the day of observation. At 15:59 hr an

adult male Indian palm squirrel arrived and

entered into one chamber of the nest. The adult

male was holding the neck of one of the litter in

its mouth. The pup started to give out a

repeated alarm call. Responding to the alarm

call, the mother, who was approximately 10 m

from the nest, came towards the male and bit

the tail of the adult male. However the male

dragged the pup out from the nest. The female

chased the male for a while and started to give

alarm calls. The male after moving out walked

along the wall and jumped onto the gate post

about 3m from the nest. The pup started to give

out an alarm call but this time there was no

response from the female. The male walked

along the gate post to the opposite side and then

jumped onto a creeper on a Cassia fistula

(Family: Fabaceae) tree and rested on it. At

around 16:03 hr the male started to feed on the

pup. Feeding was initiated from the the head.

During the feeding process the male changed

its sitting position several times and moved its

tail horizontally. It rested for around 2 minutes,

curled its tail, looked around and continued

devouring the head of the pup. After continuing

feeding on the head, the male tried to jump onto

another creeper while holding the pup by the

fore arms. When trying to move to the other

creeper, the pup fell onto the ground approx.

1.8 m. The male climbed down and searched

the ground for around 30 minutes but could not

find the dead pup. It then left the ground and

climbed back onto the same tree. After that

dead pup was photographed (Fig. 1).

Figure 1: The fallen dead Funambulus palmarum

pup, with its head consumed.

Literature cited Phillips, W. W. A., 1980. Manual of the Mammals of Sri Lanka - part II (2

ndrevised

edition). Wildlife and Nature Protection Society

of Sri Lanka: 267.

Submitted: 16 June 2012, Accepted: 03 July 2012

Sectional Editor: Colin A. Chapman

G. M. Edirisinghe1 and

B. S. A. T. H. Sudasinghe1,2

1 Young Zoologists’ Association of Sri Lanka,

National Zoological Gardens, Sri Lanka. 2 [email protected]

TAPROBANICA, ISSN 1800-427X. October, 2012. Vol. 04, No. 02: pp. 117.


1 cm


A taxonomic note on Impatiens disotis

Hooker, 1906 (Family: Balsaminaceae)

The genus Impatiens consists of over 1000

species distributed in the Old World tropics and

subtropics (Janssens et al., 2009, Yuan et al.,

2004). In India, the genus is represented by

more than 200 species that occur mainly in

three major centers of diversity, Western

Himalayas, North East India, and the Western

Ghats (Vivekananthan et al., 1997), of which

the state of Kerala harbours 72 species (Nayar

et al., 2006), most of which are rare,

endangered or threatened.

As part of the survey of rare and threatened

plants of Western Ghats, the authors collected

Impatiens disotis in Kallar Valley, Idukki

District, Kerala, India. Impatiens disotis was

described by Joseph Dalton Hooker in 1906,

and while he failed to cite specimens, the

species was indicated to be restricted to the

Travancore and Tinnevely hills. This suggests

that he had access to at least two specimens.

However, our enquiry of herbaria at Edinburgh,

Kew and Manchester proved futile. At this

point in time we refrain from designating a

neotype pending further investigation. Alfred

Meebold, a New Zealand botanical collector,

writer and anthroposophist, visited India three

times and on his third visit in 1910 he collected

I. disotis from Deviculam (Devicolam, Idukki

District in what is now the state of Kerala; see

http://apps.kew.org; Barcode: K000683314, K).

Gamble (1915) accepted Hookers species but it

is evident from his description that Gamble

never saw the Meebold collection. Bhaskar &

Razi (1978) provided a vague description of

flower colour, but as they failed to cite any

herbarium specimens to support their findings it

is difficult to know how they arrived at their

conclusion. In fact, Vivekananthan et al. (1997)

went so far as to state that the species had not

been collected after 1906, and so seemingly

they were unaware of the Meebold collection.

In his monograph on Impatiens of Western

Ghats, Bhaskar (2012) treated I. disotis as

vulnerable. He pointed out that neither Hooker

nor Gamble, or any later worker, provided a

detailed description of the species. He

presented a more detailed description based

mainly on a B.V. Shetty collection (Shetty

33049, MH!) from the Myhendragiri Hills in

the Kanyakumari District region of Tamil

Nadu. Here a description, illustration (plate 2)

and an array of photographs (plate 3) are

provided to facilitate identification of the

species.

Impatiens disotis Hooker, 1906

Hooker, J. D. 1906. An epitome of the British

Indian species of Impatiens. Records of the Botical

Survey of India, 4: 43, 48, figs. 1 & 2.

Specimen examined: TBGT 70438; Kallar

Valley, Idukki District, Kerala, India; E. S.

Santhosh Kumar & P. E. Roy; 22 Mar 2012.

Herbs 50-100 cm high; stem herbaceous,

simple or rarely branched, subterete to

shallowly sulcate. Leaves alternate, 7-13 x 4-6

cm; petiole to 3-5 cm with 1-2 cilia; leaf blade

elliptic, elliptic-lanceolate or broadly elliptic

with 4-6 pairs of lateral veins, dark green

above, pale green beneath, glabrous on both

surfaces, attenuate at base, acuminate-caudate

acuminate at apex, broadly crenate along

margins with minute ciliate. Flowers in axillary

racemes, 6-8-flowered, creamy-white with

saffron-red patches; peduncle solitary, to 5 cm

long; pedicels 2-3 cm long; bracts subulate,

0.6-0.7 cm long, glabrous; lateral sepals 2,

ovate-lanceolate, acuminate at apex, 3-5

nerved, slightly concave, 10-12 x 5-6 mm, pale

green; lip cymbiform, slightly compressed

laterally, to 14 mm long, anterior part of mouth

with a slightly curved beak to 3 mm long and a

tubular spur to 5 mm long; standard broadly

ovate to suborbicular, keeled along the dorsal

side, beaked at apex, 9-10 x 8-9 mm; wing

TAPROBANICA, ISSN 1800-427X. October, 2012. Vol. 04, No. 02: pp. 118-119, 2 pls.



petals 3-lobed, 12-16 mm long with basal lobe

acuminate at apex and upper lobe ovate-oblong,

slightly undulating marginally. Androecium

4.5-5 mm long; filaments to 3.5 mm long,

glabrous; anthers to 1 mm long. Ovary

ellipsoid-ovoid, 1.2-1.6 x 0.5-0.6 cm; style

short; stigma obtuse apically. Capsule 2 cm

long, tapering at both ends. Seeds 5-9 per

capsule, brownish.

Flowering: December – March

Ecology: Terrestrial, growing in evergreen

forests in association with Impatiens goughii

(Balsaminaceae), Sarcandra chloranthoides

(Chloranthaceae) and Strobilanthes rubicundus

(Acanthaceae) at an altitude of 1400 m.

Distribution: India (Kerala and Tamil Nadu),

endemic.

Remarks: Impatiens disotis is allied to I.

campanulata Wight by its herbaceous habit,

alternate leaves, and a spur that is distinctly

shorter than the lip. From that species, I. disotis

may be distinguished by its oblong sepals with

acute apices (not ovate with narrowly

acuminate apices) and by its longer spur (5 cm

vs 2-2.5 mm long).

Acknowledgements

The authors are grateful to the Director

(JNTBGRI), P. G. Latha, for use of the

facilities and for her encouragement. They are

also thankful to J. F. Veldkamp (National

Herbarium, Netherlands), The Keeper and The

Indian Liaison Officer of the Royal Botanic

Gardens, Kew for their consultation, and to the

Kerala Forest Department for permission to

conduct our research. Finally Steven Janssens

(KU Leuven - Belgium) is acknowledged for

valuable comments and reviewing.

Literature Cited Bhaskar, V. and B. A. Razi, 1978. Studies on

south Indian Impatiens L. II. General. Indian Journal of Forestry, 1: 191-198.

Bhaskar, V., 2012. Taxonomic monograph on

Impatiens L. (Balsaminaceae) of Western Ghats,

South India. The key genus of endemism. Centre

for Plant Taxonomic Studies, Bangalore: 239.

Gamble, J. S., 1915. Flora of the Presidency of

Madras. Volume 1, part 1. Adlard & Son,

London: 144.

Hooker, J. D. 1906. An epitome of the British

Indian species of Impatiens. Records of the

Botical Survey of India, 4: 37-58.

Janssens, S., E. Knox, S. Huysmans, E. Smets and

V. Merckx, 2009. Rapid radiation of Impatiens (Balsaminaceae) during Pliocene and Pleistocene:

Result of global climate change. Molecular Phylogenetics and Evolution, 52: 806-824.

Nayar, T. S., B. Rasiya, N. Mohanan, and G. Raj

Kumar, 2006. Flowering plants of Kerala – A

handbook. Tropical Botanic Garden and Research

Institute, Thiruvananthapuram: 133.

Vivekananthan, K., N. C. Nair, M. S.

Swaminathan and L. K. Ghara, 1997.

Balsaminaceae. Flora of India, 4: 93-102.

Yuan, Y. -M., Y. Song, K. Geuten, E.

Rahelivololona, S. Wohlhauser, E. Fischer, E.

Smets and P. Küpfer, 2004. Phylogeny and

biogeography of Balsaminaceae inferred from

ITS sequences. Taxon, 53: 391-403.

Submitted: 5 October 2012, Accepted: 16 October 2012

Sectional Editor: James L. Reveal

E. S. Santhosh Kumar 1,2

,

A. G. Pandurangan 1 and P. E. Roy

1

1 Jawaharlal Nehru Tropical Botanic Garden &

Research Institute, Palode, Kerala 695562,

India

E mail: [email protected]


PLATE 02

Figure 1: Impatiens disotis, A, Twig; B, Flower; C, Bract; D1, Standard petal (dorsal view); D2, Standard petals (ventral

view); E1 & E2, Lateral sepals; F1 & F2, Wing petals; G, Lip; H1 & H2, Stamens; I. Capsule (immature).


PLATE 03

Figure 2: Impatiens disotis, A, Twig; B, Flower (front view); C, Flower (lateral view); D, Dorsal petal; E & F, Lateral

sepals; G & H, Wing petals; I, Lip; J, Capsule (immature).

taprobanica (2012) vol. 4. no. 2. pages 60-119

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