Distribution Patterns of Slender Loris Subspecies ( Loris lydekkerianus ) in Kerala, Southern India

Distribution Patterns of Slender Loris Subspecies(Loris lydekkerianus) in Kerala, Southern India

Sindhu Radhakrishna & Honnavalli N. Kumara &

R. Sasi

Received: 21 October 2010 /Accepted: 11 February 2011 /Published online: 19 April 2011# Springer Science+Business Media, LLC 2011

Abstract Gray slender lorises (Loris lydekkerianus) are 1 of 2 nocturnal primategenera occurring in India. Although the distribution and abundance of the species isknown for some parts of southern India, the relative distribution of the 2 subspecies,Loris lydekkerianus lydekkerianus and L. l. malabaricus, and their comparativedensities and extent of overlap between their distributions remains largely unknown.We investigated the distribution pattern and relative density of slender lorises in theWestern Ghats mountain range in the state of Kerala in southern India. We surveyed36 forest ranges in 17 forest divisions of northern and central Kerala from Februaryto November 2009 for the presence of lorises. We sighted slender lorises in 22 forestranges in a variety of vegetation types, and the relative abundance of the speciesranged from 0.02 to 1.44 lorises/km. Our results confirm that both loris subspeciesare present in Kerala: Mysore slender lorises have a narrow patchy distribution onthe eastern edges of the Western Ghats mountain range, and Malabar slender loriseshave a fairly contiguous distribution on the western slopes of the Western Ghats. Werecommend more detailed surveys in southern Kerala to identify the distributionpatterns of the subspecies in these areas.

Keywords Abundance . Distribution . Forest type . Kerala . Slender loris . Subspecies

Introduction

Slender lorises are small nocturnal primates that are endemic to southern India andSri Lanka (Roonwal and Mohnot 1977). According to current taxonomic

Int J Primatol (2011) 32:1007–1019DOI 10.1007/s10764-011-9518-7

S. Radhakrishna (*) : H. N. Kumara : R. SasiNational Institute of Advanced Studies, Indian Institute of Science Campus, Bengaluru 560 012, Indiae-mail: [email protected]

H. N. KumaraSálim Ali Centre for Ornithology and Natural History, Anaikatti P.O., Coimbatore 641108, India

R. SasiDepartment of Anthropology, University of Madras, Chennai 600005, India

classification, Loris lydekkerianus, the gray slender loris, inhabits southern India andcentral and northcentral Sri Lanka, and Loris tardigradus, the red slender loris,southwestern Sri Lanka (Brandon-Jones et al. 2004; Groves 2001). Two subspeciesof the slender loris are recognized in southern India: a dry-forest form, the Mysoreslender loris (Loris lydekkerianus lydekkerianus) and a wet-forest form, the Malabarslender loris (Loris lydekkerianus malabaricus). Habitat loss, hunting, and trappingfor folk medicine have been identified as major survival threats to the slender loris inIndia, and population levels are predicted to decline in the future (IUCN 2010;Molur et al. 2003).

In common with many lorisiform primates, little is known about the distributionand ecology of the slender loris (Nekaris and Bearder 2007). Three issues inparticular are relevant in the context of this article. First, existing records on lorisdistributional limits in India are dated, based on secondary information or thelocations of museum specimens, and largely inaccurate in the present scenario offorest fragmentation and severe habitat loss (Hill 1933; Kumara et al. 2006).Although more recent population surveys have identified slender loris presence andabundance in the state of Karnataka and in some parts of Tamil Nadu and AndhraPradesh (Kumar et al. 2002, 2006; Singh et al. 1999, 2000), the distribution of thespecies is still unknown for a large part of southern India.

Second, little is known about the distribution pattern of the 2 subspecies. Groves(2001), Roonwal and Mohnot (1977), and Schulze and Meier (1995) have describedthe 2 forms as inhabiting the Eastern Ghats mountain range or “south and east India”(Loris lydekkerianus lydekkerianus) and the Western Ghats mountain range (L. l.malabaricus) (Fig. 1). The Western Ghats mountains run along the western coast ofIndia, south of the Tapti River, through the states of Maharashtra, Goa, Karnataka,Kerala, and Tamil Nadu, almost to the southern tip of the Indian peninsula. Identifiedas a biodiversity hotspot (Myers et al. 2000), the region is home to >55 endemicplant genera and nearly 30 endemic mammalian and bird taxa. The Eastern Ghatsranges are more discontinuous; interrupted by plateaus and escarpments, they runalong the eastern coast of India covering parts of the states of Orissa, AndhraPradesh, Tamil Nadu, and Karnataka. Researchers have claimed that the 2 slenderloris forms overlap in distribution in southern India (Groves 2001; Molur et al. 2003)but there is no field evidence to substantiate this assumption. The only study of therelative distributions of the 2 subspecies showed that they have completely separatedistributions in the state of Karnataka (Kumara et al. 2006). Kumara et al. (2006)also concluded that the distribution of the Malabar slender loris north of the PalaghatGap (a major pass in the Western Ghats that is recognized as an importantbiogeographic barrier) is confined to the rain forests on the western slopes of theWestern Ghats and that it is absent in the dry forests on the eastern slopes In a mapof the potential geographic distribution of slender loris subspecies in southern India,Kumara and his colleagues present the distribution of the Malabar slender loris asrestricted to the western slopes of Western Ghats, whereas the Mysore slender lorisdistribution extends over a wide range of forest types in the Eastern Ghats (Kumaraet al. 2009). The study also posited the presence of an unidentified subspecies that isdistributed in patchy habitats along the eastern slopes of the Western Ghats in TamilNadu and Karnataka, and contended that the 3 subspecies (?) had separate,nonoverlapping distributions (Kumara et al. 2009).

1008 S. Radhakrishna et al.

Third, the few studies on slender lorises in India have largely focused on Mysoreslender lorises; little attention has been paid to Malabar slender lorises. The onlyinformation on abundance levels and distribution pattern of Malabar slender lorises

Fig. 1 Presumed historical distribution of slender lorises in India. Map redrawn based on slender lorisdistribution map (Fig. 2) in Schulze and Meier (1995).

Slender Loris Subspecies in Kerala, India 1009

comes from Karnataka (Kumara et al. 2006). The state of Kerala is a large andcritical part of the distributional range of Malabar slender lorises, yet very little dataare available for this area. Although some researchers mentioned the presence ofslender lorises in some of the forests in Kerala (Rai and Kumar 1993; Rajamani2001), the subspecific identity is not clear in these cases. Nor is there anyinformation on the presence of lorises in different habitat types across Kerala.

Our specific objectives were therefore to examine distribution patterns andabundance of slender lorises in the Western Ghats mountain ranges in the state ofKerala and to map the distribution patterns of the 2 subspecies. We also investigatedif 3 main environmental parameters of surveyed locations, i.e., the vegetation types,altitudinal range, and degree of protection within the forest patch, significantly affectthe abundance of the species therein.

Methods

Study Area

The state of Kerala (8°18′–12°48′N and 74°52′–72°22′E) on the western coast ofIndia is a critical part of the Western Ghats biodiversity hotspot, as the Ghats runthrough the entire length of the state, covering an area of ca. 20,000 km2 (Nair1991). The state is home to remarkably diverse flora and fauna and harbors highlevels of endemic amphibians, reptiles, birds, mammals, and flowering plants. Basedon 2 important biogeographic features of the Western Ghats, i.e., the Palghat Gapand the Shencottah Gap, we divided the forest areas of Kerala into 3 main regions: 1)northern Kerala, from Kannur forest division to Wayalar range north of the PalghatGap; 2) central Kerala, comprising the Nelliampathy Hills, the High Ranges,Anamalais, and the Sholayar forests; and 3) southern Kerala, from Periyar TigerReserve and extending south of the Shencottah Gap to Kanyakumari (Fig. 2).

Methodology

We conducted our survey in 36 forest ranges across northern and central Kerala(Fig. 2) from February 2009 to November 2009. We covered 17 forest divisions.(Government-protected forest lands in India are subdivided into several hierarchicalunits for ease of administration. A Forest Range refers to a tertiary-level unit ofadministration that is headed by Forest Range Officer. Two or more forest ranges areusually grouped to form a Forest Division that is headed by a Divisional or DistrictForest Officer). Two observers conducted surveys during the night from 20:00 h to04:00 h on natural and existing trails, using headlamps and flashlights (Sterling andRamaroson 1996; Walsh and White 1999). Slender lorises display a distinctiveorange-red eyeshine in response to flashed light that can be seen from a distance of>100 m, and we used this feature to detect their presence (Singh et al. 1999). Weconducted nocturnal surveys on foot and in vehicles (Nekaris and Jayewardene2004; Singh et al. 1999, 2000), in accordance with the terrain of the area. Theaverage speed of vehicle transects was 5 km/h (Singh et al. 1999), and that of foottransects was 1 km/h (Sterling and Ramaroson 1996).


Owing to the large area of the survey and the time constraints involved, weestimated relative abundances and distribution patterns of the 2 subspecies instead ofabsolute densities of surveyed populations (Kumara et al. 2006). We calculated therelative abundance index as the number of lorises observed per kilometer. We used aGPS unit to record the geographical location of sighted individuals and a laserrangefinder to determine subject-to-observer distances. When we sighted a loris, wealso recorded details such as subspecies identity, age–sex class, height from ground,

Fig. 2 Slender loris survey sites in Kerala.


substratum and tree species used, and habitat type whenever possible. Forestdepartment regulations did not permit handling of lorises, and we scrutinized sightedindividuals to identify subspecies using morphological characteristics. Malabarslender lorises are reddish brown with large circumocular patches, whereas Mysoreslender lorises are relatively larger (ca. 260 g vs. 180 g of Malabar sender lorises)and grayish-brown with narrow circumocular patches (Kumara et al. 2006).Opportunistic photographs also allowed for analyses of morphological differences.We used loris subspecies identity in different study sites to map the distribution ofthe taxa. We expended more survey effort in Chinnar Wildlife Sanctuary, located onthe eastern slopes of southern Western Ghats, to test the hypothesis of Kumar et al.(2009) regarding a new loris subspecies in this area.

We tested for differences in loris sightings with respect to vegetation type andprotected status of forests (Wildlife Sanctuaries and National Parks, labeled asProtected Areas, experience greater levels of state protection than do ReservedForests) using G test of goodness of fit (McDonald 2009), and for differences withrespect to altitude using a χ2 test.

Results

Overall Abundance

We covered a total distance of 1041 km during the course of our survey: 423 innorthern Kerala and 618 in central Kerala. We sighted a total of 117 slender lorises,73 in northern Kerala and 44 in central Kerala. Loris encounter rates ranged from0.02/km to 1.44/km; we sighted the highest abundance of lorises in Aralam WildlifeSanctuary in northern Kerala, and the lowest in Begur and Sulthan Bathery innorthern Kerala (Table I).

Loris Abundance and Vegetation Types, Altitudinal Range, and Protected Statusof Forests

There was a significant difference in the relative abundance of lorises in differentvegetation types (G=54.31, df=4, p<0.001; Fig. 3). The greatest number of lorissightings occurred in evergreen forests (44.4%), closely followed by dry deciduousforests (35.0%). We also sighted lorises in moist deciduous forests (14.5%) and inforest plantations that were sometimes intermixed with scrub forests or riverine forests(5.9%), but did not sight lorises in private coffee or cashew plantations. Lorisdetection distances varied with vegetation type; they were greatest in forest plantations(mean±SD=18.88±11.42 m) and least in evergreen forests (6.86±5.38 m). Detectiondistances were 16.07±13.67 m in dry deciduous forests and 12.45±7.15 m in moistdeciduous forests.

Loris sightings varied significantly with respect to altitude (χ2=144.877; df=6;p<0.001).We most commonly sighted lorises at altitudes of <300 m asl (50.0%),next often at 601–900 m asl (22.8%), and least >1500 m asl (1.8%; Fig. 4).

We sighted slender lorises in only 22 of the 36 forest ranges surveyed. The majorityof loris sightings (69.2%) occurred in Protected Areas, and only 30.8% of sightings


Table I Slender loris sightings in Kerala

Forestdivision

Forest range Officialstatus

km walked/motored

No. oflorises

Subspecies identity Individuals/km (±SD)

Northern Kerala

Kannur Aralam PA 44 43 Loris lydekkerianusmalabaricus

1.44 (±1.07)

WayanadNorth

Begur RF 24 1 L. l. m. 0.02 (±0.03)

Periya RF 19 2 L. l. m. 0.23 (±0.43)

WayanadSouth

Pulpally RF 18 4 L. l. m. 0.27 (±0.35)

WayanadWildlife

Tholpetty PA 12 4 L. l. m. 0.25 (±0.29)

Kurichat PA 21 1 L. l. m. 0.05 (±0.09)

Sulthan Bathery PA 38 1 L. l. m. 0.02 (±0.05)

Muthanga PA 21 0 — —

Calicut Peruvannamuzhy RF 22 4 L. l. m. 0.16 (±0.14)

Nilambur Nilambur RF 12 2 L. l. m. 0.12 (±0.17)

Edavanna RF 30 3 L. l. m. 0.21 (±0.25)

Vazhikadavu RF 28 1 L. l. m. 0.08 (±0.14)

Karulai RF 22 0 —. —

Kalikavu RF 12 2 L. l. m. 0.12 (±0.25)

Mannarkad Silent Valley PA 26 0 — —

Agali RF 22 0 — —

Attapadi RF 18 3 Not known 0.16 (±0.19)

Palakkad Olavakode RF 17 0 — —

Walayar RF 17 2 Loris lydekkerianuslydekkerianus

0.07 (±0.15)

Central Kerala

Trissur Machad RF 7 0 — —

Pattikad RF 12 0 — —

Peechi PA 17 0 — —

Nemmara Kollengode RF 15 6 L. l. l. 0.40 (±0.04)

Nelliampathy RF 36 3 L. l. l. 0.05 (±0.09)

Chimmoney Chimony PA 9 5 L. l. m. 0.60 (±0.57)

Parambikulam Perambikulam PA 36 0 — —

Thunakadavu PA 117 0 — —

Orukomban PA 52 0 — —

Karimala PA 34 0 — —

Chalakudy Pariyaram RF 14 0 — —

Vellikulankara RF 9 0 — —

Vazhachal Sholayar RF 17 1 L. l. m. 0.06

Chinnar Chinnar PA 207 23 L. l. l. 0.10 (±0.08)

Malayatur Kuttampuzha RF 14 2 L. l. m. 0.13 (±0.18)

Idukki Thattekad PA 15 3 L. l. m. 0.29 (±0.29)

Idukki PA 7 1 Not known 0.13 (±0.18)

Total 1041 117 0.14 (±0.37)

RF = Reserve Forest; PA = Protected Area


occurred in Reserved Forests. However, the relative abundance of lorises did not differsignificantly between Protected Areas and Reserved Forests (G=1.73; df=1; p>0.05).

Slender Loris Subspecies Distribution

In northern and central Kerala, slender lorises occurred in dry deciduous habitatsalong the eastern edge of the state, whereas sightings in the western parts werelargely restricted to evergreen and moist deciduous forests (Fig. 5). On the basisof their morphological characteristics, we identified individuals sighted in AralamWildlife Sanctuary, Wayanad Forest Division, Calicut Forest Division, NilamburForest Division, Chimony Wildlife Sanctuary, Malayatoor Forest Divison,Thattekad Bird Sanctuary, and Vazhachal Forest Division as Malabar slenderlorises (Fig. 6) and individuals sighted in Palakkad Forest Division, NemmaraForest Division, and Chinnar Wildlife Sanctuary as Mysore slender lorises (Fig. 7).

Fig. 3 Slender loris sightings indifferent vegetation types. Barvalues on the x-axis representmean ± SD.

Fig. 4 Slender loris sightings indifferent altitudinal ranges.


Fig. 5 Slender loris sightings in northern and central Kerala.


We were unable to identify clearly the slender loris form in Mannarkad ForestDivision and Idukki Wildlife Sanctuary.

Discussion

Gray slender lorises appear to be present in all the forest patches of northern andcentral Kerala. Although we did not sight lorises in some sites in northern andcentral Kerala, notably Peechi Wildlife Sanctuary, Parambikulam Wildlife Sanctuary,and Silent Valley Wildife Sanctuary, their presence has been reported previously inPeechi, Parambikulam, and Agali range, Mannarkad (Easa and Balakrishnan 1990;Nameer 2000; Nameer et al. 2007). Hence we argue that slender lorises have a fairlycontiguous distribution in northern and central Kerala. However, except for AralamWildlife Sanctuary in Kannur district, where the relative density of the species was1.44/km, slender loris abundances in other parts of northern and central Kerala wereuniformly low, with a range of 0.02–0.60/km.

Fig. 6 Malabar slender loris inAralam Wildlife Sanctuary.

Fig. 7 Mysore slender loris inKollengode forest range.


In northern and central Kerala, Mysore slender lorises occur at a lower density(0.16/km) than the Malabar form (0.25/km). This is an uncommon pattern becauseprevious studies on slender loris populations in India and Sri Lanka indicated thatdensities are higher for dry forest forms than wet forest forms (Kumara et al. 2006;Nekaris and Jayewardene 2004; Singh et al. 1999, 2000). Abundance estimates forslender lorises in Sri Lanka are 0.86–13 individuals/km in the wet zone, and 0.33–50individuals/km in dry zones (Nekaris and Jayewardene 2003), whereas surveys ofMysore slender lorises in southern India yielded estimates of 0.4–3.6 individuals/kmin Dindigul, Tamil Nadu, 0.01–0.48 individuals/km in southern Andhra Pradesh(Singh et al. 1999, 2000), and 0.41 individuals/km in Karnataka (Kumara et al.2006). Malabar slender loris abundance in Kerala is similar to an estimate obtainedfrom Karnataka (0.22 individuals/km, Kumara et al. 2006) but is lower thanelsewhere in the country.

In the absence of detectability assessments, abundance comparisons across sitesare problematic (Norvell et al. 2003; Pliosungnoen et al. 2010). However, theassumptions underlying distance sampling methods make them incompatible withthe time constraints involved in conducting large-scale nocturnal animal surveys(Duckworth 1998). Our methods combine detection efficiency with large areacoverage (Kumara et al. 2006; Nekaris and Jayewardene 2003, 2004; Singh et al.1999, 2000); but suffer from a visibility bias that may over- or underestimate trueabundance. Using natural trails as transects may cause greater sightings of “edge”species such as lorises, thereby overestimating its abundance. Visibility is alsogreater in dry habitats than in wet ones, and may result in overestimating abundancein dry habitats. Though it was not possible to correct the first bias, the fact thatdetection distances were least in evergreen forests, although this vegetation typecontained the highest abundance of lorises, suggests that abundance estimatesobtained from this study, though not completely free of bias, are useful and ofsignificant conservation value.

Many parts of the Aralam Wildlife Sanctuary are almost devoid of tree cover as aresult of tree cutting and branch lopping, particularly in the foothills beside the StateFarm. Slender loris sightings in these areas were very high, contributing to theoverall high density of Malabar slender lorises in the Sanctuary. Population surveysfor Mysore slender lorises in Tamil Nadu and Andhra Pradesh in southern India notethat the highest densities for the taxa are seen in scrub forests and near croplands,and suggest that this may be related to the high insect density in such habitats (Singhet al. 1999, 2000). We hypothesize that the unusually high density of Malabarslender lorises in Aralam may similarly be allied to the degraded state of the habitat;a more detailed study of the behavioral ecology of this population is required toclarify the issue.

Our results do not support the proposition that Mysore slender lorises aredistributed along the Eastern Ghats or south and east India, while Malabar slenderlorises inhabit the wet forests of the Western Ghats (Groves 2001; Roonwal andMohnot 1977; Schulze and Meier 1995). Instead, we found Malabar slender lorisesalong the western slopes of the Western Ghats in Kerala, but also found smallpopulations of Mysore slender lorises in Western Ghats, along the eastern slopes.

Contrary to the hypothesis of Kumara et al. (2009), the results of our study do notsupport the presence of a new loris subspecies on the eastern slopes of the Western


Ghats. Instead, our study shows that north of the Palghat Gap, Malabar slenderlorises are distributed in the wet and dry forests of the Western Ghats. Also, northand south of the Palghat Gap, Mysore slender loris populations occur in the forestson the eastern edge of the Western Ghats, while Malabar slender lorises occur inforests on the western slopes. We therefore suggest that it is Mysore slender lorisesthat extend their distribution from the foothills of the Eastern Ghats, albeit patchily,westward into the eastern slopes of the Western Ghats. The 2 forms do have separatedistributions in northern and central Kerala, with Mysore slender lorises present insmall patchy populations on the eastern edges of the Western Ghats, and Malabarslender lorises in fairly contiguous populations on the western slopes, but it is notclear if the same pattern extends southward. More detailed surveys in southernKerala and the adjoining regions of Tamil Nadu will shed light on the distributionpatterns of the subspecies in this area. We also recommend genetic studies on the 2forms; their distinct morphological characteristics certainly warrant a reexaminationof their taxonomic status, and perhaps a reassessment of their IUCN status.

Acknowledgments This study was supported by the Ministry of Environment and Forests, GOI, NewDelhi. We thank the Chief Wildlife Warden of Kerala for research permits to conduct the study andcountless officials of the Kerala Forest Department for their help with field logistics. We gratefullyacknowledge the support and aid of S. Ramkumar and his family; J. Sriram and his family; AnindyaSinha, R. Suganthasakthivel, K.K. Ramachandran, and P. Vijayakumaran Nair of KFRI; P. Hemalatha; N.Radhakrishna; Anil Govind; and Shanthala Kumar in our work. We also thank Joanna Setchell and 2anonymous reviewers for their discerning comments that helped strengthen this paper.

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Distribution Patterns of Slender Loris Subspecies ( Loris lydekkerianus ) in Kerala, Southern India

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