Cloud Forest Dung Beetles (Coleoptera: Scarabaeinae) in the Western Ghats,a Global Biodiversity Hotspot in Southwestern India

Abstract

First-time comprehensive data on the community structure, species composition and regional endemism of dung beetle assemblage in a tropical montane cloud forest (TMCF) from South Asia is provided. High level of endemism, predominance of two montane endemic species of which one is a flightless local endemic, greater proportional abundance of roller guild, and the total absence of dweller guild, make the cloud forest dung beetle community different from the communities in the low-altitude montane forests. Distribution of major proportion of montane species in the low altitude supports the hypothesis for the origin of montane fauna through vertical colonization of the high altitudes by low-altitude species. Abundance of rollers is attributed to the availability of dung pellets of local endemic mountain goat, Nilgiri Tahr (Nilgiritragus hylocrius) and Sambar deer (Cervus unicolor) throughout the year and absence of dweller guild to the seasonal availability of fresh dung pads of Asian elephant (Elephas maximus) and gaur (Bos gaurus). Dominance by the flightless local endemic dung beetle Ochicanthon devagiriensis, belonging to the old-world tribe Canthonini with Gondwanaland distribution, indicates the stability, refugial isolation, and archaic nature of the dung beetle assemblage in the studied montane region. Since flightless species show a high level of fidelity to their preferred habitat and are efficient indicators of historical changes in their habitats, dominance and local endemism of flightless species Oc. devagiriensis makes it an ideal indicator species and effective forecaster of habitat modifications of the unique cloud forest study region in the Western Ghats.

Keywords

montane forests shola flightless dung beetles Canthonini endemism

Introduction

Patches of tropical montane cloud forests (TMCF) occur in Central and South America, tropical Africa and tropical Asia, where humid mountains are frequently covered by trade wind-derived orographic clouds and fog in combination with convectional rainfall [1 –3]. Many features of these forests, from vegetation morphology and nutrient budgets to solar insolation, are directly or indirectly related to cloud formation. A direct impact of frequent cloud cover is the deposition of cloud droplets through contact with vegetation (cloud stripping), fog drip to the forest floor (fog precipitation), and presence of moss cover on the stem of trees [4 –7]. TMCFs often occur either on mountain tops or along ridge lines between 1,000 and 3,500 m asl. Under exceptional conditions they also occur at lower altitudes such as 300–500 m asl [3, 8]. TMCFs are among the most endangered of all tropical forest types and usually harbor a high proportion of many endemic plant and animal taxa specifically adapted to cool temperatures and moist-humid conditions. Although the TMCFs are less diverse than the lowland forests, when their exceptionally high levels of regional endemism are considered their collective species diversity would probably exceed any other forest type [2, 8, 9].

A majority of the studies in Asian TMCFs refer to vertebrates [10 –13] [and plants [14 –17] [and little is known of the ground-dwelling arthropod diversity in such habitats. Search for data on the dung beetle assemblage in Asian TMCFs revealed that no data exists except that of Hanski [18] from Southeast Asia. Data from Southeast Asian TMCFs revealed low tribal, generic, and species richness, but high abundance of two species, with one being an endemic wingless species, and absence of dwellers. Moreover, no data on diel periodicity, seasonality, and functional guild composition of dung beetles is available. In such a context, we analyzed the diel periodicity (diurnal, nocturnal), seasonality (southwest and northeast monsoon, pre-summer, and summer seasons) and functional guild composition (dwellers, rollers, tunnelers) of dung beetle assemblage in a TMCF in the Western Ghats, a global diversity hotspot in southwestern India. Based on the data on dung beetles from TMCFs in Southeast Asia, we hypothesized that TMCF in the region may also have low tribal, generic, and species richness and a high abundance of endemic flightless species. In addition, we explain the rationale for the uniqueness of cloud forest dung beetle assemblage in this region with regard to their isolation, composition of major dung-producing mammals, and dung diversity.

Methods

Study area

The study site was at Eravikulam National Park [ENP (77º0′30″–77º10′E; 10º10′– 10º 20′N; 1400–2694 m asl, 97 km²; Idukki District, Kerala State) (Fig.1)] on the western slopes of the South Western Ghats Montane Rain Forests Ecoregion [19]. Patches of stunted montane evergreen forests surrounded by vast montane grasslands (also referred to as “shola forests” and “shola grasslands”) [20, 21] occur in the high altitudes at ENP (Fig.2)]. These forests occurring in the midst of montane wet grasslands, at altitudes above 1,500–1,800 m asl in the Western Ghats in southwestern India, are referred to as tropical upper montane rain forests and montane temperate forests [22, 23]. Following the recent classification of montane forests [3, 6], shola forests are categorized as tropical montane cloud forests (cloud forests). The landscape of the shola forests can be best described as “islands” of cloud forests within vast tracts of grasslands. As in other regions in the Western Ghats, as of now only small patches of these unique ecosystems remain in the ENP, because of human-induced modifications to the landscapes (e.g., plantations and settlements). Modification of the shola forests in the ENP started around the 14^th century with the entry of native tribes from the eastern slopes of the Western Ghats and the slash-and-burn cultivation techniques they practiced. This was followed by the intense transformation of high-altitude shola forests into tea plantations and game belts in the later part of the 19^th century with the arrival of the British [19, 24].

Fig. 1.

(A) Map of southwestern India showing the location of the Western Ghats; (B) Study sites in the Eravikulam National Park.

Fig. 2.

Tropical Montane Cloud Forest patch amidst grass land in Eravikulam National Park of the Western Ghats with local flightless endemic Oc. devagiriensis (inset; adopted from Latha et al 2011).

Key herbivorous mammals in ENP are the Nilgiri Tahr [Nilgiritragus hylocrius (Ropiquet and Hassanin, 2005)], Asian elephant (Elephas maximus Linnaeus, 1758), Sambar deer (Cervus unicolor Kerr, 1792), gaur (Bos gaurus Hamilton Smith, 1827), barking deer [Muntiacus muntjak (Zimmermann, 1780)] and mouse deer (Moschiola indica, Gray, 1852). Intensely undulating terrain, the climate, and the altitude of ENP make this region hostile for any mammal other than the resident endemic, the Nilgiri Tahr. ENP does not hold any resident population of Asian elephant and gaur, but serves as a corridor linking the wet western and dry eastern slopes [19, 25].

Annual climate features include temperature ranging from 17 to 20°C; relative humidity 40–90%; mean annual rainfall 1,300 mm; mean rainfall during southwest monsoon time (June–August) 260 mm, northeast monsoon time (September–November) 105 mm, pre-summer (December–February) 20 mm; and summer (March–May) 50 mm [26].

Sampling

Dung beetles were sampled using baited pitfall traps on a seasonal basis (northeast monsoon: September 2006, pre-summer: January 2007, summer: May 2007) for 24-hour periods from September 2006–May 2007. No sampling was done during the southwest monsoon time (June-August), as the heavy rain leaves the forest floor soggy and access to the site extremely difficult. Each trap consisted of a plastic tub (210 mm diameter, 150 mm deep), buried to its rim in soil, and holding a mixture of water and propylene glycol. Each trap was covered with a circular plastic tray supported on iron rods to restrict desiccation on warm days and flooding on rainy days. Two hundred grams of fresh cow dung was placed on a wire grid between the basin and the tray. Twenty such traps were placed in three shola forest patches [ten traps along a linear transect in a large forest patch at Umayamala (2,250 m asl) and four and six traps in two small patches at Anamudi (2,200 m asl)) with an intertrap distance of 50 m to minimize trap interference [27]. Beetles were collected at 0800 h and 1800 h each day. Both diurnal and nocturnal collections were made separately.

Beetles were determined to species using Arrow [28] and Balthasar [29] and confirmed by comparing with the verified specimens. Voucher specimens are temporarily deposited in the insect collections of St. Joseph's College, Devagiri, Calicut, and will be transferred to the National Insect Collections at the Zoological Survey of India (ZSI), Calicut, and the Indian Agricultural Research Institute (IARI), New Delhi. The determined species were sorted into three functional guilds: dwellers (endocoprids), rollers (telecoprids), and tunnelers (paracoprids), following Cambefort and Hanski [30], and three temporal guilds: nocturnal, diurnal, and generalist beetles based on the significance level of variation in the abundance in nocturnal and diurnal traps.

Evaluation of the sampling effort was done with the Mao-Tau sample-based rarefaction curve in the EstimateS program 8 [31]. The changes in community structure during different seasons were compared based on the number of individuals per species with dominance-diversity (rank abundance) curves [32, 33].

Significant levels of variation in the overall and species-wise abundance during seasons were tested with Kruskal-Wallis tests and species-wise abundance in nocturnal and diurnal traps with one-way analysis of variance (ANOVA). When significant differences occurred, the Mann-Whitney U-test was applied to determine which pairs of seasons differed significantly [34]. Seasonal variations in functional-guild composition based on abundance were analyzed with a Chi-square test. All statistical analyses were done using MegaStat Version 10.0 [35].

Results

Dung beetles belonging to five species, three tribes, and three genera were collected (Table 1). Onthophagus refulgens (57.96%), followed by the flightless Ochicanthon devagiriensis (24.92%) were the dominant species (Table 1). No seasonal variation in overall abundance was evident (H=1.44, df=2, p>0.05). Populations of Oc. devagiriensis peaked during the monsoon season (H=21.19, df=2, p<0.05) and those of On. refulgens in pre-summer (H=21.25, df=2, p<0.05). Ochicanthon devagiriensis was recorded throughout the study period, whereas Panelus keralai was recorded only during summer (H=10.73, df=2, p<0.05) and On. quaestus only in pre-summer (H=18.04, df=2, p<0.05). Seasonality of On. castetsi could not be determined due to low abundance. No Onthophagus species was recorded during summer and only On. refulgens and Oc. devagiriensis were recorded during the monsoon period. Onthophagus refulgens and Oc. devagiriensis did not display diel periodicity. Onthophagus quaestus (N) was nocturnal and On. castetsi (D) and P. keralai (D) were diurnal (Table 1). The assemblage of dung beetles consisted of tunnelers (three species) and rollers (two species). Tunnelers represented 60.0% of total species richness and were the most abundant functional guild (72.67 % of total abundance). Functional guild (tunnelers and rollers) composition based on abundance varied significantly among seasons (χ²=167.59, df=2, p<0.05), whereas richness-based composition of functional guilds did not (χ²=3.00, df=2, p>0.05). Tunnelers were the dominant functional guild in pre-summer and were absent in summer. Rollers dominated the assemblage in both summer and the monsoon period.

Table 1.

Seasonal abundance, species richness, diversity, diel periodicity, and functional guild composition of dung beetles in the tropical montane cloud forests of Eravikulam National Park in the Western Ghats. G-generalist, D-diurnal and N-nocturnal.

Species/Guild/Diversity/Diel periodicity	Annual data		Presummer period		Summer period		Monsoon period
	mean±SD	Total	mean±SD	Total	mean±SD	Total	mean±SD	Total
Onthophagus refulgens Arrow, 1931 (G)	1.93±4.24	116	5.55±5.91	111	0	0	0.25±0.55	5
Onthophagus quaestus Sharp, 1875 (N)	0.43±1.53	26	1.3±2.47	26	0	0	0.00	0
Onthophagus castetsi Lansberge, 1887 (D)	0.05±0.22	3	0.15±0.37	3	0	0	0.00	0
Panelus keralai Paulian, 1980 (D)	0.08±0.28	5	0.00	0	0.25±0.44	5	0.00	0
Ochicanthon devagiriensis Sabu & Latha, 2010 (G)	0.83±2.3	50	0.1±0.31	2	0.2±0.52	4	2.2±3.62	44
Abundance	200		142		9		49
Species richness	5		4		2		2
Nesting guilds
Rollers	27.63		1.41		100		89.8
Tunnelers	72.67		98.59		0		10.2

Species accumulation curves for all seasons reached a perfect level-off, denoting that sampling was adequate with less likelihood of finding more species (Fig. 3).

Fig. 3.

Expected species accumulation curves based on the Mao-Tau function for all seasons.

Dissimilar shapes and slopes of the rank-abundance curves showed differences in patterns of species diversity between the seasons. Species richness was highest during pre-summer and lowest and equal during summer and monsoon periods (Fig. 4). Dominance patterns were dissimilar among the seasons with On. refulgens dominating in pre-summer, P. keralai and Oc. devagiriensis in summer, and Oc. devagiriensis during the monsoon period.

Fig. 4.

Dominance diversity curves based on the number of individuals (mean abundance) per species of overall and seasonal data. OR- On. refulgens, OQ- On. quaestus, OC- On. castetsi, OD- Oc. devagiriensis, PK- P. keralai.

Discussion

The cloud forest dung beetle assemblage of ENP in southwestern India is similar to that from Southeast Asia and Neotropics in showing low species richness, diversity, and abundance [18, 36]. Community structure and species composition of the assemblage vary from those of the Neotropical region, but resemble those of Southeast Asia. Comparison of dung beetle faunal composition between the TMCFs in montane regions of Southeast Asia (Borneo) and the present study region in South Asia reveals notable similarities and dissimilarities. Similarity in the composition of dung beetle fauna represented by Canthonini and Onthophagini, incidence of flightless local endemics Ochicanthon hanski in southeast Asia and, Oc. devagiriensis in the Western Ghats in south Asia [18, 39, 40] and presence of low altitude montane species in the TMCFs in Borneo and the Western Ghats is obvious. These three features make it an archetypical instance of parallel evolution of related groups, but isolated spatially. However, three major differences namely, (1) higher species richness of Onthophagus, (2) presence of a non-endemic On. quaestus and, (3) presence of Panelus in the TMCFs in the Western Ghats in contrast to the low species richness of Onthophagus, total absence of non-endemics and non-record of Panelus in the peaks of south-east Asian TMCFs (18) are striking. Occurrence of Panelus in the present study site and TMCFs of Sri Lanka and North-eastern India [28, 29, 41, 42] indicate that Panelus is a widespread member of the TMCF dung beetle assemblage of South Asia and its non-record in Southeast Asia [18] may be due to the inefficiency of the fish-baited traps used.

Distribution of TMCF species in low-altitude montane forests indicates that vertical colonization by low-altitude montane species with greater dispersal abilities and adaptations to exist in cold habitats [43 –45] [lead to the movement of dung beetles to the TMCF region. However, since the Scarabaeinae are predominantly a warm-climate species [46], the relatively cooler climate of the TMCFs would have made the vertical colonization difficult for most warm-climate-adapted dung beetle species of lower altitudes [43, 47]. Among the vast list of warm-climate dung beetle species belonging to six tribes present at low-altitude montane forests [48, 28], only selected species belonging to Canthonini and Onthophagini could colonize the TMCF. These selected species might have more general dispersal abilities, ability to use both large and small dung types available (56), and special physiological adjustments for thermoregulation to withstand the low temperatures [49, 50, 51] that allow them to become established in the TMCFs. Although flightlessness is a common feature in high- altitude montane habitats with environmental stability, isolation, and limitation of habitat area [52, 53, 54], such flightlessness is unusual among dung beetles, who depend on flight capacity to reach dung resources that are often spatially and temporarily limited [55, 44]. This raises the question why only the ball-rolling and dung-pellet-preferring Oc.devagiriensis species lost flight in the region and not dung beetle species of the genera Onthophagus or Panelus. Literature on the evolutionary history and biogeographic distribution of dung beetles and dung-contributing herbivorous mammals [56 –58]; pellet dung feeding habits of Ochicanthon and Panelus belonging to the Old World Canthonini and their ancient Gondwanaland distribution; basal position of Canthonini in the cladistic analysis of dung-beetle phylogeny [57 –59]; and occurrence of dung pellet-producing Nilgiri Tahr as key resident mammalian herbivores in the TMCFs of the Western Ghats [19, 24] lead to several propositions. One is that Ochicanthon and Panelus belonging to the Old World Canthonini represent the archaic dung beetle species that reached the TMCF region before the mid-Cenozoic arrival of dung-pad producing mega herbivores (Asian elephant and gaur) and the dung-pad preferring modern tribe, Onthophagini. Among the two Canthonine taxa, Ochicanthon, whose possible dung resource is dung pellets of small mammals [59], lost flying capacity in response to the steady dung-pellet resource availability from Nilgiri Tahr, lack of competition for dung resources from other dung beetle species, and habitat persistence, environmental stability, and isolation [53, 54] in the TMCF. Presence of wings in Panelus may be due to its dependence on flight capacity to reach the generally scarce insect and rat dung pellets [59]. Subsequent arrival of the dung-pad-producing mega herbivores, Asian elephant and gaur, across Afro-Asian region in the mid- to late-Cenozoic period [56, 57, 60] might have led to the colonization and population build-up of tunnelers (Onthophagus) belonging to the dung-pad-preferring younger modern tribe, Onthophagini.

Functional guild composition of the assemblage differed from the assemblages in the low-altitude montane forests of the Western Ghats (37, 38, 48) in the total absence of dwellers and in the comparatively high proportion of rollers belonging to the rare Old World tribe Canthonini. Dwellers are well represented in regions where undisturbed large droppings are common [57, 38], and relatively high proportions of ball-rolling taxa occur in regions with low diversity in dung types, comprising mainly pellets and small droppings of omnivores and carnivores [56]. Hence, the non-record of dwellers in the TMCF study region is attributed to the seasonally limited availability of mega herbivore dung pads (personal observations) and abundance of rollers to the ready availability of mammalian dung pellets.

The abundance of tunnelers (Onthophagus) peaks during the pre-summer period that coincides with the seasonal arrival of dung-pad-producing mega herbivores (elephant and gaur) [19], and the low abundance of tunnelers during other periods leads to the suggestion that the life cycle of tunnelers in the region is synchronized with the arrival of mega herbivores and the availability of their dung pads. The chance of tunnelers (Onthophagus) moving along with the seasonal mega herbivores (elephant and gaur) is ruled out, as On. refulgens and On. castetsi are montane endemics and On. quaestus is not recorded from the surrounding low-altitude moist forests (48). Similarly, the high abundance of Ochicanthon during the wet season, which coincides with the movement of mega herbivores to dry deciduous forests in the eastern slopes of the study region, is likely to be linked to the dung pellet resource availability from the major resident mammal, Nilgiri Tahr, and of sambar deer taking shelter within TMCFs [19, 25] to escape the incessant rains and wind in the surrounding grasslands. Reasons for the rare occurrence of P. keralai during summer may be their rarity and the seasonal availability of preferred pellet dung resources of insects and rats [59].

Absence of diel periodicity by the two dominant and seasonal montane endemic species (On. refulgens and Oc. devagiriensis) may be adaptations to exploit the seasonally abundant dung resources. The nocturnal and diurnal activity in Oc. devagiriensis, along with its abundance during the wet season, indicates that a generalization saying ball rollers are diurnal and thermophilic (since warm conditions make dung-ball making easier [61]) is not applicable for Ochicanthon. Warm conditions may be a prerequisite for dung-ball making in the modern rollers (Sisyphini and Gymnopleurini), associated with the more moist, wet dung pads of larger herbivores in the low altitude montane forests of the Western Ghats [37, 38], but this is not the case for the Old World Canthonine roller, Ochicanthon. Lack of data on the life biology characteristics and low abundance of On. castetsi, On. quaestus, and P. keralai makes interpretations on diel periodicity and seasonality difficult. It highlights the need to study the habits of endemic dung beetle species in the TMCFs in the Western Ghats in order to obtain a better understanding of their habitat requirements and endemism as a study that would also help preserve the TMCFs, with their long history of geographical isolation, from further habitat modifications.

Implications for conservation

Dominance by a flightless local endemic species, belonging to the Old World tribe that occupies a basal position in dung-beetle phylogeny and with ancient Gondwanaland distribution, is indicative of the archaic nature of the dung-beetle assemblage in the TMCF region and its long history of geographical isolation. Since flightless species show high fidelity to their preferred habitat and are efficient indicators of historical changes in their habitats [62], abundance and local endemism of Oc. devagiriensis makes it an effective indicator of conservation priority and future habitat modifications of the unique TMCF ecosystem in the Western Ghats (Fig. 5).

The record of the flightless local endemic Ochicanthon species in other TMCFs in the Western Ghats, the northeast of the Indian subcontinent [40], and the Southeast Asian region [18, 39] indicates that TMCFs of the Asian region are centers of differentiation and refuge for Old World dung beetles. This highlights the need to treat TMCFs as high-priority zones from a conservation viewpoint.

Fig. 5.

Habitat of flightless local endemic dung beetle species, Oc. devagiriensis, at Eravikulam National Park of the South Western Ghats (A); “islands” of tropical montane cloud (shola) forest within a vast tract of grassland in the peak area of the Western Ghats (B); major resident mammal and local endemic mountain goat (Nilgiritragus hylocrius) (C); a herd of mountain goats along the cliff edge (D). Photos A and B by Sabu K Thomas; C and D by Joe Jesudurai.

Footnotes

Acknowledgments

Financial assistance provided by UGC (University Grants Commission, India), is gratefully acknowledged. We thank Kerala Forest and Wild Life Department for permissions; wildlife warden and field staff of Eravikulam National Park for local assistance; K.T. Thomachan (Devagiri College, Calicut) for the support in statistical analysis; A. Raman (Charles Sturt University, Australia) and two anonymous reviewers for critical comments; T.N. Ananthakrishnan (Emeritus Scientist, Chennai), Fernando Z. Vaz-de-Mello (Universidade Federal de Mato Grosso, Cuiaba, Brasil), Darren J. Mann (Oxford University Museum of Natural History, Oxford, UK) for literature; Giulio Cuccodoro (Département d'entomologie, Muséum d'histoire naturelle, Genève, Suisse) for verifications; Joe Jesudurai (Loyola College, Chennai) for images of the mountain goat; Paul Durairaj (Pallanad) for the 4WD vehicle trips along the treacherous montane tracts; Davis Erappuzhikara (Angel Home stay, Pallanad) for local hospitality; and P.J.Vineesh (Devagiri College, Calicut) for assistance during field collections. Two anonymous reviewers provided useful guidance in improving the paper.

References

Doumenge

Gilmour

D. A.

Ruiz

P. M.

and Blockhus

1995. Tropical montane cloud forests: conservation status and management issues. In: Tropical Montane Cloud Forests. Ecological Studies. Hamilton

L.S.

Juvik

J.O.

and Scatena

F. N.

(Eds.), pp. 24–37. Springer Verlag, New York.

Still

C. J.

Foster

P. N.

and Schneider

S. H.

1999. Stimulating the effects of climate change on tropical Montane Cloud Forests. Nature 4: 398.

Bruijnzeel

L. A.

2001. Hydrology of tropical montane cloud forests: A Reassessment. Land Use and Water Resources Research 1: 1–18.

Stadtmüller

1987. Cloud Forests in the Humid Tropics: A Bibliographic Review. The United Nations University, Tokyo, and Centro Agronómico Tropical de Investigación y Enseñanza, Turrialba, Costa Rica.

Frahm

J. P.

and Gradstein

S. R.

1991. An altitudinal zonation of tropical rain forests using bryophytes. Journal of Biogeography 18: 669–676.

Bruijnzeel

L.A.

and Proctor

1995. Hydrology and biogeochemistry of tropical montane cloud forests: what do we really know? In: Tropical Montane Cloud Forests- Ecological Studies. Hamilton

L. S.

Juvik

J. O.

and Scatena

F. N.

(Eds.), pp. 38–78. Springer Verlag, New York.

Holder

C. D.

2006. The hydrological significance of cloud forests in the Sierra de las Minas Biosphere Reserve, Guatemala. Geoforum 37: 82–93.

Hamilton

L. S.

Juvik

J. O.

and Scatena

F. N.

1995. Tropical Montane Cloud Forests. Ecological Studies. Springer Verlag, New York.

WWF. 2001. Wild world, WWF full report, South Western Ghats montane rain forests (IMO151), available online (http://worldwildlife.org/wildworld/profiles/terrestrial/im/im0151full.html). Accessed on 10/1/ 2009.

10.

Dowsett

R. J.

1985. Site-Fidelity and Survival Rates of Some Montane Forest Birds in Malawi South-Central Africa. Biotropica 17(2): 145–154.

11.

Rice

C. G.

1988. Habitat, population dynamics, and conservation of the Nilgiri tahr (Hemitragus hylocrius). Biological Conservation 44(3): 137–156.

12.

Brooks

T. M.

Pimm

S. L.

Kapos

and Ravilious

1999. Threat from deforestation to montane and lowland birds and mammals in insular South-east Asia. Journal of Animal Ecology 68(6): 1061–1078.

13.

Shanker

and Sukumar

1999. Synchrony in Small Mammal Populations of Montane Forest Patches in Southern India. Journal of Animal Ecology 68(1): 50–59.

14.

Foster

2001. The potential negative impacts of global climate change on tropical montane cloud forests. Earth-Science Reviews 55(1–2): 73–106.

15.

Bussmann

R. W.

2001. Epiphyte diversity in a tropical andean forest- Reserva Biologica San Francisco, Zamora, Chinchipe, Ecuador. Ecotropica 7: 43–59.

16.

Thomas

S. M.

and Palmer

M. W.

2007. The montane grasslands of the Western Ghats, India: Community ecology and conservation. Community Ecology 8(1): 67–73.

17.

Giriraj

Irfan-Ullah

Ramesh

B.R.

Karunakaran

P. V.

Jentsch

and Murthy

M. S. R.

2008. Mapping the potential distribution of Rhododendron arboreum Sm. ssp. Nilagiricum (Zenker) Tagg (Ericaceae), an endemic plant using ecological niche modeling. Current Science 94(12): 1605–1611.

18.

Hanski

1983. Distributional ecology and abundance of dung and carrion- feeding beetles (Scarabaeidae) in tropical rain forest in Sarawak, Borneo. Acta Zoologica Fennica 167: 1–45.

19.

Kerala forests and wildlife 2009. The sanctuaries and national parks in Kerala. Available online (http://www.keralaforest.org/html). Accessed on 10/1/2009.

20.

Ranganathan

C. R.

1938. Studies in the ecology of the shola grassland vegetation of the Nilgiri Plateau. Indian Forester 64:523–541.

21.

Nair

K. K. N.

and Khanduri

S. K.

2001. Knowledge on the environment, vegetation and biodiversity of the shola forests of Kerala: the present scenario. In: Shola forests of Kerala: Environment and Biodiversity. Nair

K. K. N.

Khanduri

S. K.

and Balasubramaniyam

(Eds.), pp. 3–24. Kerala forest Department and Kerala forest research Institute.

22.

Schimper

A. F. W.

1903. Plant-geography upon a physiological basis, Clarendon Press, Oxford, UK.

23.

Champion

H. G.

and Seth

S. K.

1968. Revised Survey of the Forest Types of India, Manager of Government of India Publications, New Delhi.

24.

Logan

1887. Malabar Pravisya, Malabar Manual Series- 1. The Mathrubhumi printing & publishing Co. Ltd., Kozhikode, Kerala, India.

25.

Rice

C. G.

and Madhusudan

M. D.

2009. Nilgiri Tahr (Hemitragus hylocrius Ogilby, 1838). Available online http://www.wii.gov.in/envis/ungulatesofindia/nilgiri.htm. Accessed on 05–06–2009.

26.

KDHP. 2007. Kannan Devan Hills Plantations Vaguvarai Tea Estate: Rainfall records for 2005–07 period.

27.

Larsen

T. H.

and Forsyth

2005. Trap spacing and transect design for dung beetle biodiversity studies. Biotropica 37(2): 322–325.

28.

Arrow

G. J.

1931. The Fauna of British India including Ceylon and Burma, Coleoptera: Lamellicornia (Coprinae). Taylor and Francis, London.

29.

Balthasar

1963. Monographic der Scarabaeidae und Aphodiidae der Palaearktischen und Orientalischen Region (Coleoptera: Lamellicornia). Verlag der Tschechoslowakischen Akademie der Wissenschaften. Prag.

30.

Cambefort

and Hanski

1991. Dung beetle population biology. In: Dung beetle ecology. Hanski

and Cambefort

(Eds.), pp. 36–50. Princeton University Press.

31.

Colwell

R.K.

2006. EstimateS: Statistical Estimation of Species Richness and Shared Species from Samples. Version 8. User's guide and applications available at:http://viceroy.eeb.uconn.edu/estimates.

32.

Andresen

2005. Effects of season and vegetation type on community organization of dung beetles in a tropical dry forest. Biotropica 37: 291–300.

33.

Díaz

Galante

and Favila

M.E.

2010. The effect of the landscape matrix on the distribution of dung and carrion beetles in a fragmented tropical rain forest. Journal of Insect Science 10:81 available online: insectscience.org/10.81.

34.

Weiss

N. A.

2007. Introductory Statistics, 7th edition. Dorling Kindersley, Pvt. Ltd, India.

35.

Orris

J. B.

2005. MegaStat Version 10.0. http://www.mhhe.com/support. Distributed by Mc Graw-Hill.

36.

Amat-Garcia

Lopera-Toro

and Amezquita-Melo

S. J.

1997. Patrones de distribución de escarabajos coprófagos (Coleoptera: Scarabaeidae) en relictos del bosque altoandino, cordillera Oriental de Colombia. Caldasia 19: 191–204.

37.

Sabu

T. K.

Vinod

K. V.

and Vineesh

P. J.

2006. Guild structure, diversity and succession of dung beetles associated with Indian elephant dung in South Western Ghats forests. Journal of Insect Science 6:17 available online: http://insectscience.org/6.17.

38.

Vinod

K. V.

and Sabu

T. K.

2007. Species composition and community structure of dung beetles attracted to dung of gaur and elephant in the moist forests of South Western Ghats. Journal of Insect Science 7:56, available online: insectscience.org/7.56.

39.

Krikken

and Huijbregts

2007. Taxonomic diversity of the genus Ochicanthon in Sundaland (Coleoptera: Scarabaeidae: Scarabaeinae). Tijdschrift voor Entomologie 150: 421–479.

40.

Latha

Cuccodoro

Sabu

T. K.

and Vinod

K. V.

2011. Taxonomy of the dung beetle genus Ochicanthon Vaz-de-Mello (Coleoptera: Scarabaeidae: Scarabaeinae) of the Indian subcontinent, with notes on distribution patterns and flightlessness. Zootaxa 2745: 1–29.

41.

Paulian

1980. Coléoptères Scarabaeidae Canthoninae d'Inde du Sud. Revue Suisse de Zoologie 87(1): 57–66.

42.

Paulian

1983. Sur quelques coléoptères Scarabaeoidea de la region Orientale. Revue Suisse de Zoologie 90: 615–622.

43.

Escobar

Lobo

J. M.

and Halffter

2005. Altitudinal variation of dung beetle (Scarabaeidae: Scarabaeinae) assemblages in the Colombian Andes. Global Ecology and Biogeography 14: 327–337.

44.

Escobar

Lobo

J. M.

and Halffter

2006. Assessing the origin of Neotropical mountain dung beetle assemblages (Scarabaeidae: Scarabaeinae): the comparative influence of vertical and horizontal colonization. Journal of Biogeography 33: 1793–1803.

45.

Escobar

Halffter

and Arellano

2007. From forest to pasture: an evaluation of the influence of environment and biogeography on the structure of beetle (Scarabaeinae) assemblages along three altitudinal gradients in the Neotropical region. Ecography 30: 193–208.

46.

Scholtz

C. H.

1990. Phylogenetic trends in the Scarabaeoidea (Coleoptera). Journal of Natural History 24: 1027–1066.

47.

Lobo

J. M.

and Halffter

2000. Biogeographical and ecological factors affecting the altitudinal variation of mountainous communities of coprophagous beetles (Coleoptera, Scarabaeoidea): a comparative study. Annals of the Entomological Society of America 93: 115–126.

48.

Sabu

T.K.

2010. Guild structure, taxonomic diversity and biosystematics of dung beetles (Coleoptera: Scarabaeinae) in the agriculture and forest habitats of South Western Ghats. Project report submitted to UGC, India.

49.

Verdú

J.R.

Diaz

and Galante

2004. Thermoregulatory strategies in two closely related sympatric Scarabaeus species (Coleoptera: Scarabaeinae). Physiological Entomology 29: 32–38.

50.

Jay-Robert

Lobo

J. M.

and Lumaret

J. P.

1997. Elevational turnover and species richness variation in European mountain dung beetles assemblages. Arctic, Antarctic and Alpine Research 29: 196–205.

51.

Chown

S. L.

Addo-Bediako

and Gaston

K. J.

2002. Physiological variation in insects: large-scale patterns and their implications. Comparative Biochemistry and Physiology: B-Biochemistry and Molecular Biology 531: 587–602.

52.

Lumaret

J. P.

and Stiernet

1991. Montane dung beetles. In: Dung beetle ecology. Hanski

and Cambefort

(Eds.), pp. 242–254. Princeton University Press.

53.

Darlington

P. J.

1943. Carabidae of mountains and islands: data on the evolution of isolated faunas, and atrophy of wings. Ecological Monographs 13: 37–61.

54.

Roff

D. A.

1990. The evolution of flightlessness in insects. Ecological Monographs 60: 389–422.

55.

Shultz

C. H.

2000. Evolution of flightlessness in Scarabaeoidea (Insecta, Coleoptera). Mitteilugnen der Museum Naturkunde Berlin. Deutsche Entomologen 47(1): 5–28.

56.

Davis

A. L. V.

and Scholtz

C. H.

2001. Historical vs. ecological factors influencing global patterns of scarabaeine dung beetle diversity. Diversity and Distributions 7: 161–174.

57.

Davis

A. L. V.

Scholtz

C. H.

and Philips

K. T.

2002. Historical biogeography of scarabaeine dung beetles. Journal of Biogeography 29: 1217–1256.

58.

Philips

Pretorius

and Scholtz

C. H.

2004. A phylogenetic analysis of dung beetles (Scarabaeinae: Scarabaeidae): unrolling an evolutionary history. Invertebrate Systematics 18: 53–88.

59.

Davis

A. J.

1998. Dung beetle abundance and diversity in the Maliau Basin, Sabah, Malaysian Borneo. Malayan Natural Journal 52 (3–4): 181–191.

60.

Lumaret

J. P.

Kadiri

and Bertrand

1992. Changes in Resources: Consequences for the Dynamics of Dung Beetle Communities. The Journal of Applied Ecology 29: 349–356.

61.

Krell

F. T.

Krell-Westerwalbesloh

Weiß

Eggleton

and Linsenmair

K. E.

2003. Spatial separation of Afrotropical dung beetle guilds: a trade-off between competitive superiority and energetic constraints (Coleoptera: Scarabaeidae). Ecography 26: 210–222.

62.

Yeates

D. K.

Bouchard

and Monteith

G. B.

2002. Patterns and levels of endemism in the Australian Wet Tropics rainforest: evidence from flightless insects. Invertebrate Systematics 16: 605–619.