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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 NIKI AMARASINGHE JOHANNA BLEECKER - Deputy Editors – MOHOMED BAHIR - Associate Editors – MADHAVA BOTEJUE SURANJAN KARUNARATHNA MICHAEL WASSERMAN

- 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 Published date: 14 , November 2012



TAPROBANICA, ISSN 1800-427X. October, 2012. Vol. 04, No. 02: pp. 60-64. © Taprobanica Private Limited, 146, Kendalanda, Homagama, Sri Lanka.

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




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 coinfection, 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.




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. Literature cited Anderson, T. J. C., M. E. Romero-Abal and J. Jaenike, 1995. Mitochondrial DNA and Ascaris microepidemiology: the composition of parasite populations from individual hosts, families and villages. Parasitology, 110: 221-229.
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Ostfeld, R.S., G. E. Glass and F. Keesing, 2005. Spatial epidemiology: an emerging (or re-emerging) discipline. Trends in Ecology and Evolution, 20: 328-336. Palacios, G., Q. Phenix-Lan, O. J. Jabado, S. Conlan, D. L. Hirschberg, L. Yang, Z. Junhui, N. Renwick, J. Hui, H. Hegyi, A. Grolla, J. E. Strong, J. S. Towner, T. W. Geisbert, P. B. Jahrling, C. Büchen-Osmond, H. Ellerbrok, M. P. Sanchez-Seco, Y. Lussier and P. Formenty, 2007. Panmicrobial Oligonucleotide Array for Diagnosis of Infectious Diseases. Emerging Infectious Diseases, 13: 73-81. Pedersen, A. B. and S. A. Babayan, 2011. Wild immunology. Molecular Ecology, 20: 872-80. Prugnolle, F., T. De Meeûs, P. Durand, C. Sire and A. Théron, 2002. Sex-specific genetic structure in Schistosoma mansoni: evolutionary and epidemiological implications. Molecular Ecology, 11: 1231-1238. Qi, W., M. Käser, K. Röltgen, D. Yeboah-Manu and G. Pluschke, 2009. Genomic Diversity and Evolution of Mycobacterium ulcerans Revealed by Next-Generation Sequencing. Plos Pathog, 5: e1000580. Rich, S. M., F. H. Leendertz, G. Xu, M. LeBreton, C. F. Djoko, M. N. Aminake, E. E. Takang, J. L. Diffo, B. L. Pike, B. M. Rosenthal, P. Formenty, C. Boesch, F. J. Ayala and N. D. Wolfe, 2009. The origin of malignant malaria. Proceedings of the National Academy of Science USA, 106: 14902-14907. Smith, D. L., B. Lucey, L. A. Waller, J. E. Childs and L. A. Real, 2002. Predicting the Spatial Dynamics of Rabies Epidemics on Heterogeneous Landscapes. Proceedings of the National Academy of Sciences USA, 99: 3668-3672. Subbarao, K., A. Klimov, J. Katz, H. Regnery, W. Lim, H. Hall, M. Perdue, D. Swayne, C. Bender, J. Huang, M. Hemphill, T. Rowe, M. Shaw, X. Xu, K. Fukuda and N. Cox, 1998. Characterization of an Avian Influenza A (H5N1) Virus Isolated from a Child with a Fatal Respiratory Illness. Science, 279: 393-396. Waldenström, J., S. Bensch, S. Kiboi, D. Hasselquist and U. Ottosson, 2002. Cross-species infection of blood parasites between resident and migratory songbirds in Africa. Molecular Ecology, 11: 1545-1554. Wang, D., A. Urisman, Y. -T. Liu, M. Springer, T. G. Ksiazek, D. D. Erdman, E. R. Mardis, M. Hickenbotham, V. Magrini, J. Eldred, J. P. Latreille, R. K. Wilson, D. Ganem and J. L. DeRisi, 2003. Viral Discovery and Sequence Recovery Using DNA Microarrays. Plos Biology, 1: e2. Webster, R. G., M. Peiris, H. L. Chen and Y. Guan, 2006. H5N1 outbreaks and enzootic influenza. Emerging Infectious Diseases, 12: 3-8. Weinberg, R., 2010. Point: Hypotheses first. Nature, 464: 678-678. Wertheim, J. O. and M. Worobey, 2009. Dating the Age of the SIV Lineages That Gave Rise to HIV-1 and HIV2. PLos Computational Biology, 5: e1000377. Wolfe, N. D., W. M. Switzer, J. K. Carr, V. B. Bhullar, V. Shanmugam, U. Tamoufe, A. T. Prosser, J. N. Torimiro, A. Wright, E. Mpoudi-Ngole, F. E. McCutchan, D. L. Birx, T. M. Folks, D. S. Burke and W. Heneine, 2004. Naturally acquired simian retrovirus infections in central African hunters. The Lancet, 636: 932-937.

Ria R. Ghai1 & Colin A. Chapman2*

Sectional Editor: Taprobanica, the journal of Asian Biodiversity August 12th, 2012

Department of Biology, McGill University 1205 Docteur Penfield, Montreal, Quebec, H3A 1B1 CANADA

McGill School of Environment & Department of Anthropology McGill University, Montreal, Quebec, H3A 2T7 CANADA

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TAPROBANICA, ISSN 1800-427X. October, 2012. Vol. 04, No. 02: pp. 65-68. © Taprobanica Private Limited, 146, Kendalanda, Homagama, Sri Lanka.

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:

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,




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).

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.

Family Hubbardiidae Cook, 1899 Gravelyzomus new genus Type species: Bastawade, 2002. Schizomus chalakudicus

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.

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




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.

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”.

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

Table 1: Diagnostic characters of some Indian Hubbardiidae based on original descriptions Gravelyzomus Ovozomus Neozomus Trithyreus Burmezomus chalakudicus lunatus tikaderi sijuensis chaibassicus Female flagellum, 3 3 3 2? 1 to 3 number of segments Short and Short and Elongated Gonopod shape Irregular Elongated and lobate unequal size rounded lobes Number of Numerous Three to five Four pairs Two pairs Eight to Nine lobes spermathecal lobes lobes on each side Anterior setae on 1+2 1+2 2+1 2+1 1+2/0+2 metapeltidium* Metapeltidium Divided Divided Entire Divided Entire Pedipalpal Without With or Without Without spur Without spur ? trochanter spur spur Eyespots Eyespots Inconspicuous Corneate eyes Eyespots absent Eyes present absent absent eyespots present Pedipalp sexually Male not Sexually Sexually Male not Male not known dimorphic known dimorphic dimorphic 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 schizomids Schizomus Journal of (1): 90-95. D. B., 2002. Two new species of from India with range extension for tikaderi (Arachnida: Schizomida). Bombay Natural History Society, 99

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: 124. Reddell J. and J. Cokendolpher, 1995. Catalogue, bibliography and generic revision of the order Schizomida (Arachnida). Texas Memorial Museum, Speleological Monographs, 4: 1-170.

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.

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TAPROBANICA, ISSN 1800-427X. October, 2012. Vol. 04, No. 02: pp. 69-76. © Taprobanica Private Limited, 146, Kendalanda, Homagama, Sri Lanka.

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

Kailash Chandra1 and Devanshu Gupta2

Zoological Survey of India, New Alipore, Kolkata 700053, West Bengal, India E-mail: 2 Zoological Survey of India, Jabalpur 482002, Madhya Pradesh, India E-mail:

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




& 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.




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 interocular 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.).

throughout. Paramedian tubercles separated by less than inter-ocular distance. Lateral impression of pronotum shallow.

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; ZSI/CZRC-A/16603; male (Length: 17.0 mm; 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

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

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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).

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 2: Dorsal & ventral view of external male genitalia of B. calanus (scale: 2 mm), ZSI/CZRCA/16601.

Bolbohamatum phallosum Krikken, 1980
Bolbohamatum phallosum Krikken, 1980: 21, (description, keyed, distribution, illustration). Figure 3: B. phallosum (scale: 5 mm), ZSI/CZRCA/16604, Pench Tiger Reserve, 2001.

Specimens examined: Madhya Pradesh: ZSI/CZRC-A/16604; male (Length: 15.0 mm; width: 9.0 mm); Turiya, Pench Tiger Reserve, Seoni; K. Chandra, 23 June 2001; light trap; ZSI/CZRC-A/16779; male (Length: 17.0 mm; width: 11.0 mm); Kisli Rest House, Kanha National Park, Mandla; M. Limje & party, 13 September 2003; light trap; ZSI/CZRCA/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

Figure 4: Dorsal & ventral view of external male genitalia of B. phallosum (scale: 2 mm), ZSI/CZRCA/16604.

Bolbohamatum marginale Krikken, 1980
Bolbohamatum marginale Krikken, 1980: 30, (description, keyed, distribution, illustration).

Specimens examined: Chhattisgarh: ZSI/CZRC-A/16599; male (Length: 16.0 mm;

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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.

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.)

Specimens examined: Madhya Pradesh: 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 5: B. marginale (scale: 5 mm), ZSI/CZRCA/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.

Figure 7: B. laterale (scale: 5 mm), ZSI/CZRCA/16730, Singhori Wildlife Sanctuary, 2009.

Figure 6: Dorsal & ventral view of external male genitalia of B. marginale (scale: 2 mm), ZSI/CZRCA/16599.

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).

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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.

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 8: Dorsal & ventral view of external male genitalia of B. laterale (scale: 2 mm), ZSI/CZRCA/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: (description, keyed, distribution, illustration). 95,

Specimens examined: Madhya Pradesh: 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

Figure 9: Variation of B. insidiosum (scale: 2 mm), ZSI/CZRC-A/16605 & 16778, Singhori Wildlife Sanctuary, 2010 & 2011.

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Table 1: Checklist of genera Bolbohamatum and Bolbogonium from India Distribution Name of the species India (states) Genus Bolbohamatum Krikken, 1980 Bihar, Himachal Pradesh, Madhya Pradesh, New Delhi, Uttarakhand, Uttar Pradesh and West Bengal Assam, Bihar, Chhattisgarh, Karnataka, Madhya Pradesh, Maharashtra, Tamil Nadu, West Bengal and Uttarakhand Chhattisgarh, Maharashtra and Madhya Pradesh Assam and Himachal Pradesh Himalayan Region Assam, Maharashtra, Orissa and Himalayan Region Orissa Puducherry Chhattisgarh, Madhya Pradesh, Tamil Nadu, Karnataka and Uttarakhand Maharashtra Maharashtra, Madhya Pradesh, Sikkim, Jammu & Kashmir, Karnataka and West Bengal Genus Bolbogonium Boucomont, 1911 West Bengal Bihar Himachal Pradesh and Uttarakhand Karnataka, Madhya Pradesh, Maharashtra, Tamil Nadu and Uttar Pradesh Jammu & Kashmir, Himachal Pradesh, Uttar Pradesh and Uttarakhand Uttar Pradesh Tamil Nadu Andhra Pradesh, Bihar, Madhya Pradesh, Himachal Pradesh, Uttar Pradesh, Uttarakhand and West Bengal


B. cyclops (Olivier, 1789) B. calanus (Westwood, 1848) B. phallosum Krikken, 1980 B. pseudogrande Krikken, 1980 B. robustum Krikken, 1980 B. laevicolle (Westwood, 1848) B. pyramidifer Krikken, 1980 B. meridionale Krikken, 1980 B. marginale Krikken, 1980 B. kuijteni Krikken, 1980 B. laterale (Westwood, 1848)

Nepal Bangladesh and Java



B. bicornutum Krikken, 1977 B. howdeni Krikken, 1977 B. impressum (Wiedemann, 1823) B. insidiosum Krikken, 1977 B. davatchii (Baraud, 1973)

Pakistan Afghanistan Bangladesh

Iran (Nikolajev, 2008)

B. punctatissimum (Westwood, 1852) B. scurra Krikken, 1977 B. triangulum (Westwood, 1852)

Myanmar, Bangladesh Pakistan

Acknowledgements The authors are thankful to K. Venkataraman (Director, ZSI) for providing necessary facilities and encouragement. Literature cited Boucomont, A., 1911. Contribution à la classification des Geotrupidae (Coleoptera), Annales de la Société entomologique de France, 79: 335-350.
Carpaneto, G. M., R. Mignani and E. Piatella, 1993. A revision of the Afro-Indian genus Bolboceratops (Coleoptera, Scarabaeoidea, Geotrupidae), Journal of African Zoology, 107: 329-353.

Kral, D., I. Löbl and G. V. Nikolajev, 2006. Bolboceratidae. In: Catalogue of the Palaearctic Coleoptera - 3. Löbl, I. and A. Smetana (eds.). Apollo Books, Stentrup, Denmark: 82-84. Krikken, J., 1977a. The genus Bolbelasmus Boucomont in Asia, with notes on species occurring in other regions (Coleoptera: Geotrupidae). Zoologische Mededelingen, 51 (17): 278-292. Krikken, J., 1977b. Asian bolboceratine scarabs of the genus Bolbogonium Boucomont (Coleoptera-Geotrupidae), Tijdschrift voor Entomologie, 120 (3): 77-108.

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Krikken, J., 1978a. The Afro-Asian Bolboceroides validus group (Coleoptera; Geotrupidae), Zoologische Mededelingen, 52 (26): 301-311. Krikken, J., 1978b: Taxonomic notes on Bolboceras indicum Westwood and its relatives (Coleoptera: Geotrupidae). Entomologische Berichten Amsterdam, 38: 72-77. Krikken, J., 1979. The Genus Bolbocerosoma Schaeffer in Asia (Coleoptera: Geotrupidae), Zoologische Mededelingen, 54 (3): 35-51. Krikken, J., 1980. Bolboceratine scarabs of the Oriental genus Bolbohamatum nov. (Coleoptera, Geotrupidae), Tijdscrift voor Entomologie, 123: 1-38. Krikken, J., 1984. A generic reclassification of the Afrotropical Bolboceratini (Coleoptera: Geotrupidae). Zoologische Mededelingen, 58: 2345. Li, C. L., C. C. Wang, K. Masumoto, T. Ochi and P. S. Yang, 2008. Review of the Tribe Bolboceratini s.l. from Taiwan (Coleoptera: Scarabaeoidea: Geotrupidae) with a Key to the Eurasian Genera. Annales of the Entomological Society of America, 100 (3): 474-490. Masumoto, K., 1984. New coprophagous Lamellicornia from Japan and Formosa. The Entomological Review of Japan, 39 (1): 73-83. Nikolajev, G. V., 1970. Taxonomic status of the groups belonging to the subfamily Geotrupinae. Results of the Second Scientific Conference of Young Specialists and Postgraduates, celebrated 100 years from the date of birth of V. I. Lenin and 50 years from the date of origin of Kazakhstan: 31-34. Nikolajev, G. V., 1979a. Eine neue BolbelasmusArt aus Asien (Coleoptera, Scarabaeidae, Bolboceratinae. Reichenbachia, Staatliciies Museum fur Tierkunde in Dresden, 17 Nr. 27, 225-227. Nikolajev, G. V., 1979b. Neue Gattungen und Untergattungen der Blatthornkäfer (Coleoptera, Scarabaeidae). Reichenbachia, Staatliciies Museum fur Tierkunde in Dresden, 17 Nr. 23, 189-191.

Nikolajev, G. V., 2003. The taxonomic 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): 199201. Ochi T. and M. Kawahara, 2002. Description of the female of Bolbelasmus shibatai Masumoto, 1984. Kogane, 3: 31-33. Ochi T. and K. Masumoto, 2005. Systematic Position of Bolbelasmus ishigakiensis Masumoto Elytra, 33 (2): 244 Ochi T., K. Masahiro and K. Masakazu, 2010. A 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 of Scarabaeoidology, Tokyo 1: 153-162. Scholtz, C. H. and D. J Browne, 1996. Polyphyly in the Geotrupidae (Coleoptera: Scarabaeoidea): a case for a new family. Journal of Natural History, 30: 597-614. Smith, A. B. T., 2006. A Review of the FamilyGroup Names for the Superfamily Scarabaeoidea (Coleoptera) with Corrections to Nomenclature and a Current Classification, Coleopterists Society. Monograph Number, 5: 144-204. Westwood, J. O., 1848. Description of some new or imperfectly known species of Bolboceras, Proceedings of the Linnaean Society London, 1: 384-387. Westwood, J. O., 1852. Descriptions of some new or imperfectly known species of Bolboceras Kirby, Transactions of the Linnean Society London, 21: 19-30.

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TAPROBANICA, ISSN 1800-427X. October, 2012. Vol. 04, No. 02: pp. 77-82. © Taprobanica Private Limited, 146, Kendalanda, Homagama, Sri Lanka.

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:

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,




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 widearray 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 perchsite preference, of CSE in Kolli Hills, Tamil Nadu, India, from May 2005 to May 2010. Materials and Methods Study area: Kolli Hills (11o 11’ - 11o 30’ N, 78o 16’ - 78o 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 canopycloseness (%)]. 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 (Nesttree-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.

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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-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 (%)

Nest-plot (n = 27) Mean SD + 18.5 2.8 103.5 42.5 56.8 11.8 24.1 2.4 292.7 55.5 27.6 14.8 45.4 16.2 1.0 0.0 3.4 1.5 77.6 4.0

Random plot (n = 27) Mean SD + 15.6 3.3 202.7 92.2 42.6 30.0 40.7 17.9 1.9 0.4 1.2 0.8 45.1 14.5

P value < 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 Fishes Unidentified Amphibians Unidentified Reptiles Calotes rouxi Draco dussumieri Psammophilus dorsalis Chamaeleon zeylanicus Ptyas mucosus Oligodon arnensis Dendrelaphis tristis Xenochrophis piscator Ahaetulla nasuta Naja naja Daboia russellii Unidentified snake Birds Columba livia Acridotheres tristis Terpsiphone paradise Aegithina tiphia Artamus fuscus Oriolus oriolus Mammals Funambulus palmarum

Occurrence 1 12 5 1 3 2 22 7 22 1 29 2 18 16 4 3 4 5 14 1 1

% of occurrence
Individual | Group

0.6 6.9 2.9 0.6 1.7 1.2 12.7 4.0 12.7 0.6 16.8 1.2 10.4 9.2 2.3 1.7 2.3 2.9 8.1 0.6 0.6

0.6 6.9 74.0



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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 nestsites and random-sites (Table 1).
Table 3: Perching site preference of CSE perching No of occurrence perches % 4-5 99 8 >7-8 99 8 >8-9 470 38 >9-10 74 6 Height >11-12 198 16 class of Perching >12-13 25 2 branch >13-14 123 10 (in m) >14-15 25 2 >15-16 74 6 >16-17 25 2 >17-18 25 2 Live 1150 93 Perching tree status Snag 87 7 Inner Perching 173 14 canopy canopy Outer preference 1064 86 canopy

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

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.

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Nadu Forest Department, Tamil Nadu for the support. Literature cited Baker, E. C. S., 1914. Some notes on tame Serpent Eagle Spilornis cheela, Avicultural Magazine, 5 (5): 154-159.
BirdLife International 2010. Species factsheet: Spilornis cheela. Downloaded from <> on 3/6/2010 Brown, L. H. and D. Amadon, 1968. Eagles, Hawks and Falcons of the world. McGraw-Hill, New York: 945 Collias, N. E. and E. C. Collias, 1984. Nest Building and bird behaviour. Princeton University Press, Princeton, New Jercey: 336. Dharmakumarsinhji, K. S., 1939. The Indian Crested Serpent Eagle Spilornis cheela. Journal of Bombay Natural History Society, 41 (1): 177. Gokula, V., 1999. Bird communities of the thorn and dry deciduous forests in Mudumalai Wildlife sanctuary, Tamil Nadu, India. Ph.D thesis, Bharathiyar University, Coimbatore, Tamil Nadu, India: 186. Martin, T. E. and J. J. Roper, 1988. Nest Predation and nest-site selection of a western population of the Hermit Thrush. Condor, 90: 5157. Naoroji, R. K., 1994. Observations on the courtship, nesting and hunting behaviour of the Crested Serpent Eagle Spilornis cheela. Journal of Bombay Natural History Society, 94 (2): 398400. Naoroji, R. K., 1999. Status of diurnal raptors of Corbett National Park with notes on their Ecology and Conservation. Journal of Bombay Natural History Society, 96 (3):387-398. Naoroji, R. K., 2006. Birds of prey of the Indian Subcontinent. Om Books International, India: 692. Naoroji, R. K and S. G. Monga, 1983. Observations on the Crested Serpent Eagle Spilornis cheela in Rajpipla forests - South Gujarat. Journal of Bombay Natural History Society, 80 (2): 273–285.

Nores, A. I. and M. Nores, 1994. Nest building and nesting behaviour of the Brown Cacholote. Wilson Bulletin, 106 (1): 106-120. Purandare, K., 2002. Attempt by the Crested Serpent Eagle Spilornis cheela to seize the Indian Cobra Naja naja. Journal of Bombay Natural History Society, 99 (2): 299. Selas, V., 1997. Nest-site selection by four sympatric forest raptors in southern Norway. Journal of raptor Research, 31 (1): 116-125. Shiraki, S., 1994. Characteristics of white-tailed sea eagle nest sites in Hokkaido, Japan. Condor, 96: 1003-1008. Siders, M. S. and P. L. Kennedy, 1994. Nesting habitat of accipiter hawks: is body size a consistent predictor of nest habitat characteristics? Studies in Avian Biology, 16: 9296. Sokal R. R. and F. J. Rohlf, 1981. Biometry, 2nd edition. W. H. Freeman & Company, New York: 937. Titus, K. and J. A. Mosher, 1981. Nest site habitat selected by woodland hawks in the central Appalachians. Auk, 98: 270-281. Waghray, P., I. Siddiqui and A. Siddigui, 2003. Saving Andhra’s Tigers. Sanctuary, 23 (6): 5459.

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TAPROBANICA, ISSN 1800-427X. October, 2012. Vol. 04, No. 02: pp. 83-87. © Taprobanica Private Limited, 146, Kendalanda, Homagama, Sri Lanka.

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:

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 resighting 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 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, subadult 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).
18 16 14 12 10 8 6 4 2 0
N= 9 10

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 highquality 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




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




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, 49:227267.
Anon, 2012. Parambikulam Tiger Reserve, downloaded from http:// 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.

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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): 352362 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 homerange 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.

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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 E-mail:

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).




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




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 SaintHilaire 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 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 DaubentonBuffon 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 trentecinquieme, F. Dufart., Paris.




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. Cuvier, G., 1827. A synopsis of the species of the class Mammalia. In: The animal kingdom arranged in conformity with its organization, Cuvier, G. and E. Griffith (eds.). Geo. B. Whittaker, London: 2-391. Deterville, J. -F. -P. and C. -N. -S. Sonnini De Manoncourt (eds.), 1803. Nouveau dictionnaire d'histoire naturelle, appliquée aux arts, principalement à l’agriculture et àl economie rurale et domestique: par une société de naturalistes et d’agriculterus; avec des figures tirés des trois règnes de la nature. Tome XX Société de Naturalistes et d'Agriculteurs, Paris. Farber, P. L., 1975. Buffon and Daubenton: divergent traditions within the Histoire naturelle. Isis, 66: 6374. Geoffroy, S-H, É., 1812. Tableau des quadrumanes, ou des animaux composants le premier ordre des la classe des mammifères. Tome dix-neuvieme. In: Annales du museum d'historie naturelle, Cuvier, F. G. (ed.). Dufour et Compagne, Paris: 85-170 Gervais, P., 1854. Histoire naturelle des mammifères, avec l'indication de leurs moeurs, et de leurs rapports avec les arts, le commerce et l'agriculture Tome I Primates, Cheiroptères, Insectivores et Rongeurs. Tome I, L. Curmer, Paris. Lesson, R. P., 1834. Histoire naturelle generale et parciculiere de mammiferes et des oiseaux decouverts depuis la mort de Buffon. Tome IV Suite des Mammiferes, Pourrat Freres Editeurs, Paris. Martin, W. C. L., 1837. Notes on the anatomy of the proboscis monkey (Simia nasalis). Proceedings of the Zoological Society of London, 5: 70-73. Martin, W. C. L., 1841. A general introduction to the natural history of mammiferous animals: with a particular view of the physical history of Man and the more closely allied genera of quadrumanes, or monkeys. Vol. 1, Wright and Co., London. Van Wurmb, F., 1781. Verhandelingen van het Bataviaasch genootschap van Kunsten en Wetenschappen. III, Batavia [Jakarta]. Von Schreber, J. C. D., 1775. Die säugethiere in abbildungen nach der natur mit beschreibungen. Vol. I, Wolfgang Walther, Erlangen. Wilkie, J. S., 1956. The idea of evolution in the writings of Buffon. Annals of science, 12: 48-62.

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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

Department of Biological Sciences, University of Calgary 2500, University Drive NW, Calgary, T2N 1N4, Alberta, Canada; Email: 2 Department of Zoology, University of Kelaniya, Kelaniya 11600, Sri Lanka; Email:

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).




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




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. 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

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.

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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.

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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 Stateowned 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

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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 (”. 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. Literature Cited Aide, T. M. and J. Cavelier, 1994. Barriers to lowland tropical forest restoration in the Sierra Nevada de Santa Marta, Colombia. Restoration Ecology, 2: 219 – 229.
Ashton, P. S. and C. V. S. Gunathillake, 1987. New light on the plant geography of Ceylon 1. Historical plant geography. Journal of Biogeography, 14: 249 – 285. Ball, S., 1980. An account of the cultivation and manufacture of tea in China. Garland Publishing, New Yolk, USA: xix+382. Bambaradeniya, C. N. B. and S. P. Ekanayake, 2003. A guide to the Biodiversity of Knuckles Forest Region. IUCN, Country office, Colombo, Sri Lanka: vi+68. Bambaradeniya, C. N. B., J. P. Edirisinghe, D. N. De Silva, C. V. S. Gunatilleke, K. B. Ranawana and S. Wijekoon, 2004. Biodiversity associated with an irrigated rice agro-ecosystem in Sri Lanka. Biodiversity & Conservation, 13 (9): 1715-1753. Bandaratillake, H. M., 2005. The Knuckles Range: Protecting livelihoods, protecting forests. In: Durst, P. B., C. Brown, H. D. Tacio and M. Ishikawa, (eds.). In search of excellence: Exemplary forest management in Asia and the Pacific. FAO, RECOFTC: 22. Berger, L., R. Speare and A. Hyatt, 2000. Chytrid fungi and amphibian declines: Overview, implications and future directions. In: A. Campbell (ed.), Declines and disapparances of Australian frogs Canberra, Australia: Environmental Australia: 21-31. Buschbacher, R., C. Uhl and E. A. S. Serrao, 1988. Abandoned pastures in eastern Amazonia: 1. Patterns of plant succession. Journal of Ecology, 76: 663–681. Carter, R. E., 2008. The Japanese arts and self-cultivation. State University of New Yolk Press, Albany, USA: 185. Cooray, P. G., 1984. An introduction to the geology of Sri Lanka. Department of Geology, Government Printing Press, Colombo, Sri Lanka: xix+340.

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Degreef, J., O. J. Rocha, T. Vanderborght and J. P. Baudoin, 2002. Soil seed bank and seed dormancy in wild populations of lima bean (Fabaceae): Consideration for in-situ and ex-situ conservation. American Journal of Botany, 89 (10): 1644-1650. de Rosyro, R. A., 1958. The climate and vegetation of the Knuckles Region of Ceylon. The Ceylon Forester, 3 (3&4): 207-260. de Silva, A., A. M. Bauer, C. C. Austin, S. Gunawardene, J. Drake, P. de Silva, M. G. T. H. Abeyrathna, T. Dassanayaka, G. S. Samarawickrama, R. D. C. S. K. Dasanayaka, A. M. R. K. Amarakoon and M. M. Goonasekara, 2005. The diversity of the Knuckles ecosystem: with special reference to its herpetofauna, The diversity of the Dumbara Mountains (The Knuckles Massif, Sri Lanka): With special reference to its herpetofauna. Lyriocephalus (Special issue), 6 (1&2): 13-33. Ekanayake, S. P. and C. N. B. Bambaradeniya, 2001. Trekking in the Knuckles Forest: A trekking guide to Alugallena, Dekinda and Nite cave nature trails. IUCN, Country office, Colombo, Sri Lanka: i+27. Eva, H., S. Carboni, F. D. R. Achard, N. Stach, L. Durieux, J. -F. O. Faure and D. Mollicone, 2010. Monitoring forest areas from continental to territorial levels using a sample of medium spatial resolution satellite imagery. Journal of Photogrammetry & Remote Sensing, 65 (2): 191-197. Ficetola, G. F., D. Furlani, G. Colombo and F. de. Bernardi, 2008. Assessing the value of secondary forest for amphibian, Eleutherodactylus frogs in a gradient of forest alteration. Biodiversity & Conservation, 17 (2): 2185-2195. Forrest, D. M., 1967. A hundred years of Ceylon tea: 1867-1967. Chatto and Windus, London, United Kingdom: 320. Garwood, J., 1989. Tropical soil seed banks: a review. In: Leck, M. A., M. A. V. T. Parker and R. L. Simpson, (eds.). Ecology of soil seed banks. Academic Press, San Diego, California: 149-209. Gunatillaka, N. and C. V. S. Gunatillake, 1995. Knuckles: Sri Lanka in WWF and IUCN (1994-1995) Centers of plant diversity: A guide and strategy for their conservation, 2: 123-126. Gunatilake, H. M., D. M. A. H. Senaratne, P. Abeygunawardena, 1993. Role of non-timber products in the economy of peripheral communities of the Knuckles National Wilderness Area of Sri Lanka: Farming systems approach. Economic Botany, 47 (3): 271 – 281. Holl, K. D., 1998. Tropical moist forest restoration on agricultural land in Latin America, In: Rana, B. C. (ed.). Damaged ecosystems and Restoration. World Scientific Corporation Limited, Farrer Road, Singapore: 25-42. Heywood, V. H., 1995. The Global Biodiversity Assessment. United Nations Environmental Programme, Cambridge University Press, Cambridge, United Kingdom: xi+1140. Hooper, E., P. Legendre and R. Condit, 2005. Barriers to forest regeneration of deforested and abandoned land in Panama. Journal of Applied Ecology, 42: 1165-1174. IUCN, 2007. The red list of threatened fauna and flora of Sri Lanka. Ministry of Environment and Natural Resources of Sri Lanka: xiii+148. IUCN & Forest Department, 1994. Management plan for the conservation of the Knuckles Forest (Phase 2). Forest Department, Battaramulla, Sri Lanka: 22. Iwata, T., S. Nakano and M. Inoue, 2003. Impacts of past riparian deforestation on stream communities in a tropical rain forest in Borneo. Ecological Applications, 13 (2): 461-473. Janos, D. H., 1980. Mycorrhizae influence tropical succession. Biotropica, 12 (Supplement), 56 –64. Jayaraman, R., 1975. Caste continuities in Ceylon: A study of the social structure of three tea plantations. Popular Prakashan, Bombay, India: ix+240.

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Lawton, H. W. and P. J. Wilke, 1979. Ancient agricultural systems in dry regions. In: Hall, A. E., G. H. Cannell and. H. W. Lawton (eds.). Agriculture in semi-arid environments. Springer-Verlag Berlin Heidelberg, Germany: 1-44. Leck, M. A., M. A. V. T. Parker and R. L. Simpson, 1989. Ecology of soil seed banks. Academic Press, San Diego, California: xxii+462. Mair, V. and E. Hoh, 2009. The true history of tea. Thames and Hudson Ltd, London, United Kingdom: 280. Manamendra-Arachchi, K. and R. Pethiyagoda, 1999. Sri Lanka: the global amphibian hotspot. Sri Lanka Nature, 51-54. Manamendra-Arachchi, K. and R. Pethiyagoda, 2005. The Sri Lankan Shrub-frogs of the Genus Philautus Gistel, 1848 (Ranidae: Rhacophorinae), with description of 27 new species. The Raffles Bulletin of Zoology (Supplement), 12: 163-303. Manamendra-Arachchi, K. and R. Pethiyagoda, 2006. “Sri Lankave Ubayajiween” (Amphibians of Sri Lanka – Sinhala text). Wildlife Heritage Trust, Colombo, Sri Lanka: 440+88pls. Marby, H., 1972. Tea in Ceylon: An attempt at a regional and temporal differentiation of the tea growing areas in Ceylon. Franz Steiner Verlar GMBH - Wiesbaden, Germany: xxii+238. Meegaskumbura, M., F. Bossuyt, R. Pethiyagoda, K. Manamendra-Arachchi, M. M. Bahir, M. C. Milinkovitch and C. J. Schneider, 2002. Sri Lanka: An Amphibian hot spot. Science, 298: 379. Meegaskumbura, M., K. Manamendra-Arachchi and R. Pethiyagoda, 2009. Two new species of shrub frogs (Rhacophoridae: Philautus) from the lowlands of Sri Lanka. Zootaxa, 2122: 51 - 68. Mohammed, F. 1996. Tea and environmental pollution. Journal of Tea and Coffee Trade, 2. Moxham, R. 2003. Tea: Addiction, exploitation and empire. Carroll and Graf Publishers, New Yolk, 10038-2607, USA: 224. Nanayakkara, A., H. M. D. R. Herath and K. Wickremasinghe, 2009. Forest Governance Project, Strengthening voices for better choices: Sri Lanka Country Report. IUCN, Country Office, Colombo, Sri Lanka: 63. Nepstad, D. C., C. Uhl and E. A. Serrão, 1990. Surmounting barriers to forest regeneration in abandoned, highly degraded pastures: a case study from Paragominas, Pará, Brazil, In: Anderson, A. B. (ed.). Alternatives to deforestation: Steps towards sustainable use of the Amazon Rain Forest. Colombia University Press, New York, USA: 215-229. Nizam, B. Z., U. K. G. K. Padmalal and S. W. Kotagama, 2005. Amphibian species diversity alone the northern flank of the Knuckles Range in Sri Lanka, The diversity of the Dumbara Mountains (The Knuckles Massif, Sri Lanka): With special reference to its herpetofauna. Lyriocephalus (Special issue), 6 (1 & 2): 267 – 273. Ohtsuka, T., 1999. Early stages of secondary succession on abandoned cropland in north-east Borneo Island. Ecological Research, 14 (3): 281-290. Padoch, C., E. Harwell and A. Susanto, 1998. Swidden, sawah, and in-between: agricultural transformation in Borneo. Human Ecology, 26 (1): 3-20. Pethiyagoda, P., K. Manamendra-Arachchi, M. M. Bahir and M. Meegaskumbura, 2006. Sri Lankan amphibians: diversity, uniqueness and conservation, In: Bambaradeniya, C. N. B. (ed.). The fauna of Sri Lanka. IUCN – The World Conservation Union, Sri Lanka: 125-133. Schloegel, L. M., L. F. Toledo, J. E. Longcore, S. E. Greenspan, C. A. Vieira, M. Lee, S. Zhao, 2012. Novel, panzootic and hybrid genotypes of amphibian chytridiomycosis associated with the bullfrog trade. Molecular Ecology, published online 31 July 2012.

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Skinner, K. E., 2004. Tree seedling regeneration in Camelia sinensis estates: assessing the potential for forest restoration across the forest-grassland boundary in Knuckles Forest reserve, central Sri Lanka. MSc thesis: 87. Spellerberg, I. F., 2005, Monitoring ecological change. Second Edition, The Edinburgh Building, Cambridge, CB2 2RU, United Kingdom: 350. Sri Barathi, K. P., 1979. Man and Biosphere reserves in Sri Lanka. Sri Lanka Forester, 14 (1&2): 37-40. Stuart, S., J. S. Chanson, N. Cox, B. Young and R. W. Waller, 2004. Status and trends of amphibian declines and extinctions worldwide. Science, 306: 1783-1786. Stuart, S., M. Hoffmann, J. Chanson, N. Cox, R. Berridge, P. Ramani and B. Young, 2008. Threatened amphibians of the world. Lynx Edison, Barcelona, Spain, IUCN, Gland, Switzerland and Conservation International, Arlington, Virginia, USA: 758. Touflan, P. and B. Tallow, 2009. Spatial reliability of soil charcoal analysis: the case of subalpine forest soils. Ecoscience, 16 (1): 23-27. Uhl, C. K., H. Clark, K. Clark and P. Murphy, 1981. Early plant succession after forest cutting and burning in the Upper Rio Negro region of the Amazon Basin. Journal of Ecology, 69: 631-648. Vasey, D. E., 1979. Population and agricultural intensity in the humid tropics. Human Ecology, 7 (3): 269283. Vitousek, P. M. and J. Sanford, 1986. Nutrient cycling in moist tropical forest. Annual Review of Ecology and Systematics, 17: 137 – 167. Weerawardhena, S. R., 1993. Some aspects of the population ecology of earthworms in the Central Region of Sri Lanka. Proceedings in Sri Lankan Association for Advancement of Science, 49: 153 – 154. Weerawardhena, S. R. and A. P. Russell, 2012. Cover-dependency of anurans in the Riverstone, Knuckles mountain forest range, Sri Lanka. Taprobanica, 4 (1): 12-19. Wells, K. D., 2007. The ecology and behaviour of amphibians. The University of Chicago Press, Chicago, USA: xi+1148. Wickramaratne, S. D. D. W., S. M. Weerasinghe, C. V. S. Gunathilake, D. F. R. P. Burslem and A. M. T. A. Gunarathna, 2009a. Seed availability as a limiting factor for the succession in degraded grasslands in the Knuckles Forest Reserve, Sri Lanka. Proceedings of the National Forestry Research Symposium: 23. Wickramaratne, S. D. D. W., S. M. Weerasinghe, I. A. U. N. Gunathilake, C. V. S. Gunathilake and D. F. R. P. Burslem, 2009b. The effect of some biotic and abiotic factors for the establishment of Macaranga indica in grasslands at the Knuckles Conservation area, Proceedings of the National Forestry Research Symposium: 24 – 25. Wickramasinghe, K., P. Steele and A. Senaratne, 2008. Socio-economic impacts of forest conservation on peripheral communities: Case of Knuckles National Wilderness Heritage of Sri Lanka. 12th Biennial Conference of the International Association for the Study of Commons, Cheltenham England, available online <>: 1-15.

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TAPROBANICA, ISSN 1800-427X. October, 2012. Vol. 04, No. 02: pp. 103-104. © Taprobanica Private Limited, 146, Kendalanda, Homagama, Sri Lanka.

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 IndoBurma 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 socalled “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




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.

analysis. Eubios Journal of 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– UNEP-WCMC, 2005. UNEP-WCMC Species Database: CITES Listed Species on the World Wide Web ( 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

Figure 2: A Cuora amboinensis captured by the local people.

Rajkumar Robindro Singh1,2 and Khuraijam Jibankumar Singh1,3

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

North East Centre for Environmental Education & Research (NECEER), Imphal West 795001, Manipur, India 2 Email: 3 Email:



TAPROBANICA, ISSN 1800-427X. October, 2012. Vol. 04, No. 02: pp. 105-107, 1 pl. © Taprobanica Private Limited, 146, Kendalanda, Homagama, Sri Lanka.

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 semiaquatic 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 supracaudal. 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 fourteenyear-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




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 5th 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 5th vertebrals and an extra costal scute on its right side (Fig. 1F).

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

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



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 (17921801). 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. CorderoRivera, 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. E-mail:










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).


TAPROBANICA, ISSN 1800-427X. October, 2012. Vol. 04, No. 02: 108-111. © Taprobanica Private Limited, 146, Kendalanda, Homagama, Sri Lanka.

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).

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

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




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). Trail ID (as in Fig.1) T1 T2 T8 T9 T 10 T6 T7 T4 T3 T5 T 11 Overall Habitat type MD MD MD MD MD LD LD LD LD HD HD Trail length (km) 4 3 3 3.5 2 2 2 1 2 3.5 4 Total effort walk (L) 12 9 9 10.5 6 6 6 3 6 10.5 12 90 Total individuals sighted (n) 15 6 12 9 6 6 9 6 3 3 3 78 Encounter rate (n/L) 1.25 0.67 1.33 0.86 1.00 1.00 1.50 2.00 0.50 0.29 0.25 0.27 (0.02) 0.85 (0.51) 1.25 (0.64) 1.02 (0.27) Average encounter rate (SD)



Table 2: Comparative accounts of P. petaurista encounter rate reported from its distributional range (*Average encounter rate reported from JRF). Encounter rate estimate Average encounter Study site (individual/km) (Habitat rate from the Surveyor type) study Chitou Experimental Forest Assam and Meghalaya, India Khao Ang Rue Nai Wildlife Sanctuary, Eastern Thailand 0.47 (Conifer forest) 1.96 (Hardwood forest) 0.10-0.77 (various forest types) 0.36 (Primary forest) 1.21 0.37* 0.36 Lee et al., 1993 Radhakrishna et al., 2006 Pliosungnoen et al., 2010



RAY ET AL., 2012

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.
Figure 2: Percentage of individuals of P. petaurista sighted in different habitat types having varied percentage of canopy cover.

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

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.




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. <>. 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. Biswas2, N. Das2,3,4, A. Sangma3, K. Sarma1 and M. Krishna1

North Eastern Regional Institute of Science & Technology, Arunachal Pradesh, India. 5 Email:

Primate Research Centre Northeast, Assam, India.


Department of Zoology, Gauhati University, Assam, India.

Department of Anthropology, Oxford Brookes University, United Kingdom.

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TAPROBANICA, ISSN 1800-427X. October, 2012. Vol. 04, No. 02: pp. 112-116. © Taprobanica Private Limited, 146, Kendalanda, Homagama, Sri Lanka.

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 humannonhuman 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 75o 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 %).




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
Total no. of Panchayats No. of affected Panchayats (%) 38 (25.17) 135 (47.7) 215 (93.89) 690 (90.79) 139 (68.14) 347 (73.36) 206 (56.75) 183 (80.26) 184 (87.2) 164 (69.79) 2301 (70.95) Level of the damage to crop (Number of Panchayats) Low (<40 %) 28 148 300 119 114 19 26 142 40 936 Medium (40-80%) 40 54 225 20 187 100 50 42 52 770 High (>80 %) (%) 38 (100) 67 (49.23) 13 (6.05) 165 (23.91) 46 (13.26) 87 (42.23) 107 (58.47) 72 (43.9) 595


Bilaspur Chamba Hamirpur Kangra Kinnaur Kullu Lahul & Spiti Mandi Shimla Sirmaur Solan Una Total

151 283 229 760 65 204 41 473 363 228 211 235 3243

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




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). Area under forest Nature of (sq. km) in years Change forest 2000 2003 Dense 10429 8976 Open 3931 5377 + Total 14360 14353 -7

Table 3: Growth of Rhesus Monkey population in Himachal Pradesh (FD, 2006) Year of Population assessment 60,000 - 70,000 1964-65 (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 manmonkey 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

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.




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 cropraiding; 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.

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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. Zoological Survey of India: 410. 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 Animal Behaviour Science, 127: 125-129. Pirta, R. S., M. Gadgil and A. V. Khaashikar, 1995. Management of the rhesus monkey Macaca mulatta and Langur Presbytis entellus in Himachal Pradesh, India. Biological Conservation, 79: 97106. 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. Richard, A. F., S. J. Goldstein and R. E. Dewar, 1989. Weed macaques: the evolutionary implications of macaque feeding ecology. International Journal of Primatology, 10 (6): 569594. Roonwal, M. L. and S. M. Mohnot, 1977. Primates of South Asia. Harvard University Press, Cambridge, Mass, 18: 421. SFR (State of Forest Reports), 2003. Himachal Pradesh, Forest Survey of India, Dehradun: 63.

Shafee, N. and S. AbuBakar, 2011. Characterization of dengue type 2 NGC virus infection in C6/36, vero and MRC-5 cells. International Journal of Virology, 7 (1): 24-32. Sharma, G., C. Ram, Devilal and L. S. Rajpurohit, 2011. Study of man-monkey conflict and its management in Jodhpur, Rajasthan, India. Journal of Evolutionary Biology Research, 3 (1):1-3. Siex, K. S. and T. T. Struhsaker, 1999. Colobus monkey and coconut. A study of perceived humanwildlife conflict. Journal of Applied Ecology, 36: 1009-1020. Singh, V., 1991. Ecological impact of apple cultivation in the Himalaya. International Book Distributors, Dehradun: 1251. Southwick, C. H. and M. F. Siddiqi, 1994. Primate commensalisms: the rhesus monkey in India. Review Ecology, 49: 223-31. Southwick, C. H. and M. F. Siddiqi, 2001. Status, conservation and management of primates in India. In: Gupta A. K. (ed.). Non-human primates of India. Wildlife Institute of India, Dehradun: 81-91. Vaidya, C. S. and T. R. Sharma, 1994. Decentralised planning model for developing hill areas (a case study of District Shimla, HP). Kurukshetra, 42 (6): 5-10. Vedwan, N. and R. E. Rhodes, 2001. Climate change in the Western Himalayas of India: a study of local perception and response. Climate Research, 19: 109-117. Wada, K., 1983. Ecological adaption in rhesus monkey at Kumaon Himalaya. Journal of Bombay Natural History Society, 80: 469-498. Wada, K., 1984. Rhesus monkey distribution in lower Himalayas and secondary forest succession. Journal of Bombay Natural History Society, 81: 355-362.
Submitted: 29 May 2012, Accepted: 10 August 2012 Sectional Editors: Colin Chapman & Lee Harding

Vikram Singh1,2 and M.L. Thakur1
Department of Biosciences, Himachal Pradesh University, Shimla 171 005, India 2 Email:

114 116


TAPROBANICA, ISSN 1800-427X. October, 2012. Vol. 04, No. 02: pp. 117. © Taprobanica Private Limited, 146, Kendalanda, Homagama, Sri Lanka.

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).

1 cm 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 (2ndrevised 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

Young Zoologists’ Association of Sri Lanka, National Zoological Gardens, Sri Lanka. 2



TAPROBANICA, ISSN 1800-427X. October, 2012. Vol. 04, No. 02: pp. 118-119, 2 pls. © Taprobanica Private Limited, 146, Kendalanda, Homagama, Sri Lanka.

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; 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



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

Jawaharlal Nehru Tropical Botanic Garden & Research Institute, Palode, Kerala 695562, India E mail: santhoshkumares@gmail.com2




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).



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).