Journal of Threatened
Taxa | www.threatenedtaxa.org | 26 April 2018 | 10(5): 11551–11565
Butterfly
diversity in human-modified ecosystems of southern Sikkim, the eastern
Himalaya, India
Prem Kumar Chettri 1, Kishor
Sharma 2, Sailendra Dewan 3 & Bhoj Kumar Acharya 4
1,2,3,4 Department of Zoology, School of Life Sciences, Sikkim
University, Tadong, Gangtok, Sikkim 737102, India
1 Present address: Forest, Environment and Wildlife
Management Department, Government of Sikkim, Deorali, Sikkim 737102, India
1 chettriprem22@gmail.com, 2 kisarma@gmail.com,
3 dewansailendra1992@gmail.com, 4 bkacharya@cus.ac.in
(corresponding author)
Abstract: Understanding wild biodiversity of agroecosystems and
other human dominated landscapes are crucial for the management and
conservation of biological resources.
Here, we studied the diversity, abundance, similarity and functionality
of butterflies in different human modified ecosystems in southern Sikkim, the
Eastern Himalaya. The study was
conducted from January 2015 to May 2015 by covering three habitat types namely,
farm-based agroforestry, large cardamom-based agroforestry and adjacent natural
forest ecosystem. We followed point
count method along the transect to collect data on
butterflies in the study area. A total
of 911 individual butterflies representing six families and 44 species were
recorded during the present study in southern Sikkim. Species richness and abundances of
butterflies were significantly different among the systems. While diversity and abundance were
higher in forest patches, each system harbored unique species assemblages with
low similarity between habitats.
The information on larval host plants were available for 41 butterfly
species which depended on 128 plant species belonging to 27 families. The butterfly community was dominated by
oligophagous II (19 species) followed by polyphagous (11 species), monophagous
(8 species) and oligophagous I (3 species). Similarly, generalist feeders had
higher species and abundance compared to specialist feeders. Specialist species
were confined to forest habitat, whereas generalist species were mostly
restricted to cultivated systems.
The findings of the study highlighted the need for conservation of
traditionally managed agroecosystems in order to conserve butterflies and other
associated biodiversity.
Keywords: Agroecosystems, butterfly, conservation, eastern
Himalaya; host plants.
doi: http://doi.org/10.11609/jott.3641.10.5.11551-11565| ZooBank:
urn:lsid:zoobank.org:pub:3C98090F-8CB7-40D4-9592-A37C23BA1E37
Editor:
Sanjay Sondhi, Titli Trust, Dehradun, India. Date of publication:
26 April 2018 (online & print)
Manuscript
details: Ms # 3641 | Received 08 July 2017 |
Final received 23 March 2018 | Finally accepted 04 April 2018
Citation: Chettri, P.K., K. Sharma, S.
Dewan & B.K. Acharya (2018). Butterfly diversity in human-modified
ecosystems of southern Sikkim, the eastern Himalaya, India. Journal of Threatened
Taxa 10(5): 11551–11565; http://doi.org/10.11609/jott.3641.10.5.11551-11565
Copyright: © Chettri et al. 2018. Creative Commons Attribution 4.0 International License. JoTT
allows unrestricted use of this article in any medium, reproduction and
distribution by providing adequate credit to the authors and the source of
publication.
Funding: This
manuscript is an outcome of the M.Sc. dissertation of the first author.
Competing interests: The authors declare no
competing interests.
Author Details: Prem Kumar
Chettri holds MSc (Zoology) from Sikkim University and currently works
at the Forest, Environment and Wildlife Management Department, Government of
Sikkim. He has a keen interest on biodiversity of Sikkim Himalaya with special
focus on butterflies and plants. Kishor
Sharma is a PhD scholar at the Department of Zoology, Sikkim University.
His research interests are to understand the diversity and distribution
patterns of birds and butterflies in the agroecosystem-forest gradient of
Sikkim Himalaya. Sailendra Dewan
is a PhD scholar at the Department of Zoology, Sikkim University. His research
focuses on distribution pattern and phylogeny of butterflies along elevation
gradients in the Sikkim Himalaya. Bhoj
Kumar Acharya is a faculty in the Department of Zoology, Sikkim
University, Gangtok. His research interests are to
understand the large-scale ecological patterns with particular emphasis on
species richness, abundance and distribution patterns along ecological
gradients in the Himalaya.
Author Contribution: Study designed by BKA, PKC, KS; data collected by PKC,
KS; analyzed the data by KS, PKC, SD, BKA and PKC, KS, SD, BKA wrote the
manuscript.
Acknowledgements:
We thank Vice
Chancellor, Sikkim University, Dean, School of Life
Sciences and Head, Department of Zoology, Sikkim University for facilities to
undertake this research, and faculty members of Zoology Department, Sikkim
University for cooperation and insightful discussion. We also thank PCCF cum Secretary, Chief
Wildlife Warden and Principal Research Officer, Forests, Environment and Wildlife
Management Department, Government of Sikkim for granting permission to carry
out the study. Support received from local communities of Ralong Village is
highly appreciated.
INTRODUCTION
Increased rates of deforestation and forest degradation over the past
century have resulted in significant biological attrition globally (Barlow et
al. 2007; Primack 2014). Due
to ever-increasing human population and subsequent conversion of primary
forests for agricultural expansion, many species have lost their potential
habitat leading to local extirpation. For example, a large percentage of
red-listed species has been threatened by agricultural intensification (Norris
2008). The increasing pressures on
the environment by humans necessitate preservation of natural areas crucial for
the persistence of biological diversity.
There is a growing concern that, loss of biodiversity will result in
declining ecosystem services (Kunte 2000; Kremen et al. 2002; Hooper et al.
2005; Tscharntke et al. 2005).
In agroecosystems, natural biodiversity provides a variety of ecosystem
services such as pollination, recycling of nutrients, regulation of
microclimate and local hydrological processes, suppression of pests and
detoxification of noxious chemicals, securing crop protection and soil
fertility, etc. (Altieri 1999; Lal 2004; Montagnini & Nair 2004). Most species, which primarily inhabit
forests, also interact with agroecosystems and a large proportion of the total
species of the region are likely to be encountered in agroecosystems (Pimentel
et al. 1992). The management of
these agricultural systems can dramatically affect overall levels of
biodiversity, as well as the sustenance of particular species. Additionally,
understanding biodiversity of agroecosystems and other human dominated
landscapes is crucial for the management and conservation of biological
resources. In the eastern Himalaya, it has been suggested to formulate planning
for land use based on butterfly-forest type associations, by considering forest
sub-types as units of conservation (Singh 2017).
Butterfly has been used as an indicator taxa to
assess the health of different land use systems (Schulze et al. 2004b). Many studies have recorded higher
diversity of butterflies in agroecosystems, e.g. in USA (Meehan et al. 2012),
Vietnam (Lien & Yuan 2003), Costa Rica (Horner-Devine et al. 2003) and
Japan (Kitahara 2004; Kitahara et al. 2008). Butterfly community is significantly
affected by habitat loss and modification, and anthropogenic disturbances
(Perfecto et al. 2003; Bobo et al. 2006; Posa & Sodhi 2006). In central Sulawesi, Schulze et al.
(2004a) found a steady decline in butterfly species diversity from natural
forest, to old secondary forest, secondary forests, agroforestry systems and
maize field sites but no significant difference between natural and old
secondary forests sites. In Cameroon, however, Bobo et al. (2006)
reported a significant decline of butterfly richness and abundance from
secondary forests and agroforestry sites towards near primary forests and
annual crop sites and high species turn over along the gradient of land
conversion but with loss of range-restricted and forest species. The studies in
tropical regions have reported decline in butterfly species richness with
increasing management intensity (Mas & Dietsch 2003; Francesconi et al.
2013). Schulze et al. (2010)
highlighted the importance of human-modified habitats for conservation of
overall biodiversity across all major tropical regions. Along a gradient from open to forest
habitats, speciesŐ habitat preferences significantly relates to population
trends; drastic decline of open-habitat species and
moderate increase of forest species (Herrando et al. 2016). Endemicity and larval host plant
specificity have been reported as significant predictors of vulnerability to
habitat disturbance for butterflies (Posa & Sodhi 2006).
Studies on butterfly communities in India have focused mostly on
protected areas or forest ecosystems (Uniyal & Mathur 1998; Uniyal 2004,
2007; Barua 2007; Barua et al. 2010; Singh 2010, 2017; Sengupta & Ghorai
2013; Sethy et al. 2014; Acharya & Vijayan 2015; Chettri 2015; Sondhi &
Kunte 2016). A few ecological
studies have reported the butterfly communities in agroecosystems in India,
mostly from the Western Ghats region (Kunte 1997; Kunte et al. 1999;
Shahabuddin & Ali 2001; Dolia et al. 2008; Mone et al. 2014). The natural vegetation types harbor
greater diversity than human-modified habitats but home gardens and
agricultural fields display distinct species composition (Kunte et al.
1999). Distance to protected area
and percentage canopy cover influenced abundance and richness of butterflies in
the Western Ghats (Dolia et al. 2008).
High butterfly diversity including legally protected species has been
reported in agri-horticultural ecosystems (Das et al. 2016) and also in tea and
coffee plantations (Bora & Meitei 2014; Mone et al. 2014).
Generally, the efforts to preserve biodiversity have focused on
establishment of protected area network (PAN) that constitute about 13% of
terrestrial lands globally and amounts to one-third of the agricultural lands
(38% land cover globally) (Venter et al. 2014; World Bank 2017). Protected areas around the world not
only conserve and safeguard biodiversity but also provide essential benefit to
local people such as protecting water supplies, food, medicines as well as
traditional values, landscape and sustenance for livelihoods. But the establishment of protected area
in human-modified landscape is not feasible which necessitates the preservation
of existing wild biodiversity in the agricultural systems and surrounding
forest patches with the involvement of local communities. The PAN in the Himalayan region is
mostly confined to the high elevation areas and there is poor coverage of PAN
at low to mid elevations although these areas are rich in biodiversity (Chettri
et al. 2008; Shrestha et al. 2010; Acharya et al. 2011; Bhardwaj
et al. 2012; Acharya & Sharma 2013).
The low to mid elevation areas are represented by mosaic landscape of
cultivated systems and forests. The management of these cultivated systems in
Sikkim are both traditional (Sharma 2009; Sharma & Acharya 2013) and
organic (Bhutia 2015).
The previous studies on butterflies of Sikkim have been conducted in PAN
or forest ecosystems (Haribal 1992; Acharya & Vijayan 2015; Chettri
2015). Rai et al. (2012), however,
reported the rediscovery of two very rare species protected under Schedule I of
Indian Wildlife (Protection) Act 1972 from human-modified ecosystems of Sikkim. PAN coverage in Sikkim is almost 31 % of
the total geographical area of the state comprising one national park and seven
wildlife sanctuaries. With the
exception of Kitam Bird Sanctuary (geographical area of 6km2), there
is no PAN coverage below 1,500m in the state. Occurrence of high species richness,
narrow elevation range of most species and absence of PAs at low to
mid-elevation has pointed a way for extension of conservation efforts to these
elevation sites (Acharya & Vijayan 2015). Since the areas below 2,000m are almost
entirely inhabited by people and the major chunk of forests fall under private
holdings, conservation can be achieved only through the involvement of the
local community as suggested for mountainous areas (Kollmair et al. 2005). Hence, the present study was undertaken
to understand the biodiversity conservation value of agroecosystems in Sikkim
by assessing the butterfly diversity in three representative human-modified
ecosystems: farm-based agroforestry systems and large cardamom-based
agroforestry system along with adjoining natural forest in southern Sikkim, the
eastern Himalaya, India.
MATERIALS AND METHODS
Study area
The study was conducted at Ralong Village (27.310N &
88.330E) in southern Sikkim located in the eastern Himalaya, India
(Fig. 1; Table 1). The village is
situated between 1,800m and 2,100m elevation with a total geographical area of
around 5km2. The region has a cool temperate type of climate with a maximum
temperature of 17–270C, minimum temperature of 02–210C
and mean annual rainfall of 162cm. Sikkim is a part of the eastern
Himalaya, which fall under one among the 35 global biodiversity hotspots
(Conservation International 2017).
Despite its small geographical area (7,096km2), Sikkim is one
of the richest Indian states in terms of biodiversity harboring around 43%
mammals, 45% birds, 50% butterflies and 11% flowering plants of the Indian
subcontinent (Acharya & Sharma 2013).
The total forest cover of Sikkim is 3,389km2, which accounts
for 47.46% of the total geographical area of the state.
We selected three representative ecosystem types for the present study
(Table 1) which are described below:
Table 1. Details of transects
established for sampling butterflies in farm-based agroforestry system (FAS),
large cardamom-based agroforestry system (LCAS) and natural forest system (NFS)
of Ralong, southern Sikkim, eastern Himalaya.
Habitat type |
Farm-based agroforestry system |
Large cardamom-based agroforesary system |
Natural forest system |
Dominant vegetation |
Schima wallichii, Alnus nepalensis, Albizia spp.,
Terminalia myriocarpa, Acer campbelli, Castanopsis hystrix |
Alnus nepalensis, Albizia spp., Terminalia
myriocarpa, Acer campbelli, Castanopsis hystrix |
Michelia spp., Pteris villosa, Quercus lamellosa, Rhus
insignis, Quercus thomsonii, Quercus spicata, Symplocos theifolia. |
Elevation (m) |
1700–1900 |
1700–2100 |
1700–2100 |
Latitude |
27.34490N |
27.33150N |
27.33480N |
Longitude |
88.34050E |
88.33660E |
88.33720E |
Sampling effort (No. of points
covered) |
90 |
90 |
90 |
Time devoted for sampling (in days) |
9 |
9 |
9 |
Farm-Based
Agroforestry System (FAS)
Farm based agroforesty system is important land use practice in hilly
terrains. It is primarily an agri-silvicultural system comprising home gardens
and livestock rearing (Sharma 2009).
A variety of crops such as maize, potato, millet, beans, pulses, peas
and cabbage are cultivated in this system.
Dominant tree species that occur in the system are Schima wallichii,
Alnus nepalensis, Albizia spp., Terminalia myriocarpa, Acer
campbelli, Castanopsis hystrix, etc.
Large Cardamom-based
Agroforestry System (LCAS)
Large cardamom-based agroforestry is a traditional farming system
basically practiced in mountain areas especially in Nepal, Bhutan, Sikkim and
Darjeeling. Large cardamom is an important cash crop grown as an understory perennial
crop predominantly under the shade of Himalayan alder Alnus nepalensis
(Sharma 2009; Sharma et al. 2016).
Other shade tree species such as Albizia spp., Terminalia
myriocarpa, Acer campbelli, Castanopsis spp., Echinocarpus
dasycarpus, Eurya acuminata, Juglans regia, Quercus lamellosa, Quercus spicata,
Rhus insignis, Symplocos theifolia, Viburnum cordifolium, Zanthoxylum sp.
etc also occur in this system.
Natural Forest
Systems (NFS)
The cultivated systems are encircled by small patches
of natural forests where the local community depends on fuel wood and cattle
fodder. The main type of vegetation in Ralong is
temperate broad-leaved forests which comprises tree species such as Michelia spp.,
Pteris villosa, Quercus lamellosa, Rhus insignis, Quercus thomsonii, Quercus
spicata, Symplocos theifolia, Zanthoxylum sp., Echinocarpus dasycarpus,
Elaeocarpus sikkimensis, Albizia procera, Beilschmiedia roxburghiana, Eurya
acuminata, Ficus hookeri, etc.
Study design and
sampling
The study was designed to cover three representative ecosystem types
available in the present study area (FAS, LCAS and NFS). Depending upon the availability of
suitable plots and accessibility, we established transect each of 1km length in
all the three study systems (Table 1; Fig. 1). Along the transects
permanent points were established which were spaced 100m apart making 10 points
per transect. We covered equal area
(approximately one hectare) in all the three ecosystem types.
We followed point count methods along the transect
for sampling butterflies in the study area following Pollard (1977) and Acharya
& Vijayan (2015). We conducted
five minutes count within 5m radius in each point
recording the identity and abundances of butterflies. The sampling of
butterflies was done by uniformly covering all the points from January to May
2015. Sampling was done on clear sunny days in the morning from 10:00 hrs to
13:00 hrs when the activity of butterflies remains at its highest. The butterflies were identified at the
wing based on photographic plates given in Haribal (1992), Kehimkar (2008) and
Sondhi et al. (2013). In cases where instant identification was not
possible, photographs were taken and identified using various resources
including ifoundbutterflies.org (Kunte et al. 2017). We completed a total of 27 transect
visit (nine in each of the study system) totaling 270 point counts. No
collection of butterfly specimens was done during this study in Sikkim.
Data Analysis
Community parameters such as species richness, abundance, Shannon-Weiner
diversity index and evenness were calculated for total samples as well as each
habitat type following Magurran & McGill (2011). Species richness was considered as the
total number of species observed and species abundance as number of individual
butterflies counted during the sampling. The diversity was analyzed using
Shannon-Wiener diversity index (H′) = – Σ pilnpi; where pi = proportion of
total sample belonging to ith species, ln= natural logarithm
(Shannon & Weaver 1949). Similarly, evenness was calculated using the
formula: Evenness (J) = H′/Hmax where Hmax= lnS, S
= number of species, H′ = Shannon–Wiener Diversity (Pielou
1969). Based on the observation, we
also estimated non-parametric species richness estimators using the software
EstimateS version 9.1.0 (Colwell 2013).
Using the various estimators and observed richness, species accumulation
curves were generated for all the three systems. Among the non-parametric estimators
Chao1, Jackknife 1 and Jackknife 2 were preferred because the data was
represented by many rare species (singletons and doubletons); these estimators
are less sensitive to the patchiness of the species distribution and
variability in the probability of encountering species (Colwell &
Coddington 1994). To understand the
species similarity among the systems, Morisita-Horn similarity index were
calculated using EstimateS version 9.1.0 (Colwell 2013).
Variation in species richness and abundances of butterflies among
systems was tested using one way ANOVA. Pair wise multiple comparisons based on
TukeyŐs HSD was also conducted to assess the significant difference in the
species and abundance of butterflies per point among the three systems. In
order to understand the species-abundance pattern of butterfly community, we tested
the four distribution model (geometric, log series,
truncated log-normal and MacArthurŐs broken stick) to describe the
species–abundance distribution pattern of ecological community (see
Magurran & McGill 2011).
We computed relative percentages of butterflies (both species richness
and abundance) in each category (butterfly family, habitat specialization and
larval host plant specificity). We also assessed the number of larval host
plants (family and species) for all the six butterfly
family, and butterfly species: host plant species ratio.
Information on habitat specialization for each of the species observed
in the study area was obtained from Wynter-Blyth (1957), Haribal (1992), Kunte
(2000) and Kehimkar (2008). Each butterfly species was then classified
into five habitat specialization classes (Forest
interior only, Forest interior + Forest edge, Forest edge only, Openland+forest
edge and Openland only) following Kitahara (2004).
Information on larval host plant for each of the
species observed in the present study was obtained from different standard
references (Haribal 1992; Kunte 2000; Kehimkar 2008; Tiple 2012; Sengupta et
al. 2014; Kunte et al. 2017) and field observations. The larval host specificity of butterfly
community was assessed by classifying them into monophagous (one species of
larval host plant), oligophagous I (>1 species of larval host plant within
only one genus in a family), oligophagous II (larval host plant in >1 genus
but within a single family) and polyphagous (multiple species of larval host
plant in several plant families) following standard methods (Steffan-Dewenter
& Tscharntke 1997; Kitahara 2004; Kitahara et al. 2008).
RESULTS
Species richness,
diversity and abundance
We observed 911 individual butterflies representing 44 species and six
families during this study in southern Sikkim. Species richness, abundance, diversity
and evenness of butterflies differed among the three systems (Table 2). Species richness was highest in NFS (32
species, 72.7%), followed by FAS (24 species, 54.5%) and least in LCAS (20
species, 45.5%). Out of the total
abundance of butterflies, about 52% were observed in FAS and the rest (48%) in
other two systems. But species per
point was significantly higher in the FAS compared to other two systems (One
way ANOVA: F 2, 267 = 65.432; P˛0.01) (Table 2; Fig.
2a). Similarly, there was a
significant variation in abundance per point of butterflies among the three
systems (One way ANOVA: F2, 267 = 85.917; P˛0.01) with
highest value in FAS (5.2±2.0) and the lowest in LCAS (Table 2; Fig. 2b). The pair-wise multiple comparisons based
on TukeyŐs HSD test showed significant difference in species per point and
abundance per point among all the system pairs (Table 3). Both evenness and Shannon-Weiner diversity
index was highest in the forest system compared to other systems (Table
2).
The species accumulation curve almost approached an asymptote in FAS and
LCAs but still rising in NFS indicating likelihood of detection of additional
species from the study area (Fig. 3).
It indicates that there was a probability of encountering few additional
species in NFS with the increasing sampling effort.
Family wise
distribution
The observed butterflies belonged to six families namely, Hesperiidae,
Papilionidae, Lycaenidae, Riodinidae, Pieridae and Nymphalidae. The butterfly families differed among
the three systems both in terms of species richness and abundance (Fig.
4). Butterflies belonging to all
the six families were observed in LCAS and NFS but species from Hesperiidae and
Papilionidae families were absent in FAS.
In terms of relative species richness, Nymphalidae was the most dominant
family in FAS (50%) with twelve species, followed by Lycaenidae (29.2%) with
seven species, Pieridae (16.7%) with four species and Riodinidae (4.2%) with
one species. Similarly, Nymphalidae
(45%) with nine species, Lycaenidae (25%) with five species, Pieridae (15%)
with three species and Papilionidae, Hesperiidae and Riodinidae (5% each) with
one species each were observed in LCAS.
In the NFS, Nymphalidae (53.1%) with 17 species, Lycaenidae (15.6%) with
five species, Pieridae (12.5%) with four species, Riodinidae (9.4%) with three
species and Papilionidae (3.1%) with one species and Hesperiidae (6.3%) with
two species were observed. In terms
of relative abundance (%), however, the most abundant family in all the three
systems (FAS, LCAS, NFS) was Pieridae (42.4%, 44.1%, 41.9%), followed by
Nymphalidae (35.9%, 26.8%, 29.1%) and Lycaenidae (21.5%, 26.8%, 19.4%). Abundance of Riodinidae was highest in
NFS (7.8%) which declined in FAS (0.2%) and LCAS
(0.6%).
Species similarity
and community structure
Among the 44 species, eight species (18.2%) were common to all the three
habitats, whereas 20 species (45.5%) were exclusively observed in a single
habitat (10 in NFS, five each in FAS and LCAS) (Table 2). FAS shared 17 species with NFS and 10
species with LCAS. LCAS shared 13
species with NFS. Based on the pair-wise Morisita-Horn similarity index value
it is observed that all three systems harbored unique assemblages of species
with low similarity between sites (Table 4).
Abundance pattern
Out of the total 911 individuals butterflies, Indian Cabbage White was
the most abundant species and constituted 32.5% of the total butterflies
followed by Metallic Cerulean (16.8 %) and Indian Tortoiseshell (10.6%).
Among the four models of species-abundance distribution pattern, data on
butterflies of the present study showed best fit to truncated log normal model
as there was no significant difference between observed and expected number of
species in each abundance class (χ2= 3.61; p =
0.60; df = 5). The abundance
distribution pattern showed that community is dominated by a few abundant and
many rare species (Fig. 5).
Table 2. Species richness, abundance,
diversity and evenness of butterfly observed in farm-based agroforestry system
(FAS), large cardamom-based agroforestry system (LCAS) and natural forest
system (NFS) of Ralong, southern Sikkim, eastern Himalaya.
Parameters |
FAS |
LCAS |
NFS |
Total |
Species richness |
24 |
20 |
32 |
44 |
Abundance |
474 |
179 |
258 |
911 |
Species per point (Mean± SD) |
3.2±1.0 |
1.4±1.1 |
2.3±0.9 |
2.3±1.2 |
Abundance per point (Mean± SD) |
5.2±2.0 |
2.0±1.7 |
2.7±1.4 |
3.3±2.2 |
Diversity (HŐ) |
2.18 |
2.07 |
2.59 |
2.4 |
Evenness (J) |
0.67 |
0.69 |
0.74 |
0.70 |
Habitat exclusive species |
5 |
5 |
10 |
20 |
Table 3. ANOVA and multiple comparison
based on TukeyŐs HSD for species per point and abundance per point of butterfly
community among farm-based agroforestry system (FAS), large cardamom-based
agroforestry system (LCAS) and natural forest system (NFS) of Ralong, southern
Sikkim, eastern Himalaya. **: significant at p˛0.01.
|
F2, 267 |
P |
Multiple comparisons |
Mean difference |
P |
Species per point |
65.432 |
0.000** |
FAS vs LCAS |
1.744 |
0.000** |
|
|
|
FAS vs NFS |
0.911 |
0.000** |
|
|
|
LCAS vs NFS |
-0.833 |
0.000** |
Abundance per point |
85.917 |
0.000** |
FAS vs LCAS |
3.256 |
0.000** |
|
|
|
FAS vs NFS |
2.522 |
0.000** |
|
|
|
LCAS vs NFS |
-0.733 |
0.000** |
Table 4. Species
similarity of butterflies between three systems at Ralong, southern Sikkim,
eastern Himalaya. The figures below diagonal represent the pair-wise
Morisita-Horn species similarity index and corresponding value above diagonal
represents the total species shared by the two systems. FAS -
farm-based agroforestry system; LCAS - large cardamom-based agroforestry
system; NFS - natural forest system.
Habitats |
FAS |
LCAS |
NFS |
FAS |
- |
10 |
17 |
LCAS |
0.49 |
- |
13 |
NFS |
0.642 |
0.362 |
- |
Habitat
specialization
Butterflies under different habitat specialization classes showed
distinct pattern in the three ecosystems (Fig. 6). As expected, forest interior
species, both in terms of species richness (4.2-25%) and abundance (0.4-12.0%),
were highest in NFS which declined slightly in LCAS
but sharply in FAS. Forest interior
+ forest edge species were absent in FAS and LCAS and recorded only in NFS with
low species richness (1.2%) and abundance (6.3%).
The species richness of forest edge only species were highest in NFS which declined by about 25% in LCAS and 50% in FAS.
Similarly, their abundance was also highest in NFS which
declined by about 50% in LCAS and four times in FAS. Species richness of
openland + forest edge species declined from FAS towards NFS through LCAS and
their relative abundance was highest in FAS and least in LCAS. Species richness
of open land only was least in NFS and increased about four and five times,
respectively in LCAS and FAS. Their abundances were also least in NFS which
increased around two times in FAS and LCAS.
Larval host plant
specificity
Out of 44 species observed in the present study, information on larval
host plant could be obtained only for 41 species representing 897 individuals. These 41 species depended on 128 plant
species (belonging to 27 families) as larval host plant (Appendix I; Table
5). The butterfly community was
dominated by oligophagous II (19 species; 46.3%) followed by polyphagous (11
species; 26.8%) and monophagous (8 species; 19.5%) and least for oligophagous I
(3 species; 7.3%) (Figure 7). In terms of abundance oligophagous II
(57.9%) showed the highest value followed by polyphagous
(25.2%), oligophagous I (12.5%) and minimum for monophagous (4.55%).
Butterflies considered as generalist feeder (Polyphagous + Oligophagous
II) showed high richness (30 species; 73.2%) compared to specialist feeder
(monophagous + oligophagous I) (11 species; 26.8%). Similar trend was observed in terms of
butterfly populations. Monophagous and oligopahgous species were restricted to
NFS, whereas oligophagous II and polyphagous were mostly confined to cultivated
systems (Fig. 7).
Table 5. Analysis of the larval host
plants of the butterflies observed in Ralong, southern Sikkim, eastern Himalaya
Butterfly family |
Butterfly species |
Host plant family |
Host plant species |
Ratio (butterfly species: host plant
species) |
Hesperiidae |
2 |
2 |
3 |
0.67 |
Lycaenidae |
6 |
6 |
19 |
0.32 |
Nymphalidae |
25 |
20 |
75 |
0.33 |
Papiliondae |
1 |
1 |
4 |
0.25 |
Pieridae |
4 |
4 |
22 |
0.18 |
Riodinidae |
3 |
1 |
3 |
1.00 |
Total |
41* |
27 |
128 |
0.32 |
*Data for larval host plant were not available for
three species (two for Lycaenidae and one for Nymphalidae family)
DISCUSSION
During this study a total of 44 species belonging to six families of
butterflies were recorded from three ecosystems in southern Sikkim, the eastern
Himalaya. These species comprise
6.38% species of the butterflies reported from Sikkim (Haribal 1992). The total
species observed during this study was low which may be because of number of
reasons, e.g., the study was conducted in a small geographical area and for a
short time span (five months; winter and pre-monsoon season) and did not cover
the monsoon and post monsoon seasons when the butterflies are most abundant in
India (Kunte et al. 1999; Acharya & Vijayan 2015; Chettri 2015). Nonetheless, this study explored the
potentiality of cultivated systems in harboring butterflies in an important
part of global biodiversity hotspot of the Himalaya.
Species richness and diversity of butterfly were high in the forest
system as compared to other systems. It is expected because forests system
comprised undisturbed patch of vegetation with tall trees and abundant
flowering plants which provide favorable habitat to
the butterflies. Butterfly
community is significantly affected by habitat loss and modification (Perfecto
et al. 2003; Bobo et al. 2006; Chettri 2010). Land use change and agricultural
intensification leads to homogenization of butterfly community (Ekroos et al.
2010) with species assemblage shifting from specialist to generalist (Bšrschig
et al. 2013). Some studies reported poor representation of butterflies in
farmland habitats (Schulze et al. 2004b; Fitzherbert et al. 2006; Vu 2009);
however, many studies have found higher diversity of butterflies in
agro-ecosystems (Horner-Devine et al. 2003; Lien & Yuan 2003; Bobo et al.
2006; Dolia et al. 2008; Kitahara et al. 2008).
Nymphalidae was the most dominant family in terms of species
richness. Similar pattern of
dominance of Nymphalidae in the butterfly communities have been reported in
other studies conducted in forests and human-modified ecosystems (Uniyal 2007;
Vu 2013; Acharya & Vijayan, 2015; Chettri 2015; Nandakumar et al. 2015;
Das et al. 2016; Singh 2017).
The butterfly communities in all the three habitats showed distinct
species assemblage with very low similarity and high turnover rate between
them. It indicates the importance of cultivated systems in conservation of
unique butterfly assemblages. The
low similarity among systems reflect the uniqueness of each habitat in terms of
quality, resource availability and their distribution pattern specific to the
preference of butterflies (Blair & Launer 1997).
Species abundance distribution pattern of butterfly fitted to truncated
lognormal distribution showing no significant difference in observed and
expected number of species in each abundance classes. This is an indication of
the rather stabilized ecological community (Magurran & McGill 2011).
Forest habitat harbored large number of specialist species (monophagous
and forest interior), whereas cultivated systems mostly harbored open habitat
and generalist species (open land and polyphagous). Similar trend was reported in the
Himalaya (Bhardwaj et al. 2012), Western Ghats (Kunte et al. 1999; Dolia
et al. 2008) and elsewhere (Francesconi et al. 2013; Herrando et al.
2016). Specialist and rare species
are mostly encountered in forests and metric decreases with increasing forest
habitat disturbance levels (Mayfield et al. 2005; Vu 2013). Conversely, common
species increase with growing forest habitat disturbance levels. Butterfly community is
mostly determined by the larval host plants (Kitahara 2004; Barua 2007;
Kitahara et al. 2008; Sengupta et al. 2014), nectar plants (Barua 2007;
Sengupta & Ghorai 2013), plant species richness, herb and shrub density
(Bhardwaj et al. 2012), tree species richness and density (Chettri 2010;
Acharya & Vijayan 2015).
Habitat specialist species confined to NFS were mostly from Papilionidae
and Hesperiidae families. Papilionids have been reported as very sensitive to
loss of primary forest habitat and land use change (Barua et al. 2010).
CONCLUSION
This short-term study on butterflies of Ralong, southern Sikkim
indicated the significance of cultivated systems and human influenced
landscapes for conservation of butterflies and other biodiversity
elements. Most of the studies on
biodiversity are focused on forests, and areas outside the protected areas are
not given due importance from the conservation point of view. This study reflects that although the
forest is richer in terms of species, there are many species
which occur only in the cultivated systems. Hence, for the conservation of these
species cultivated systems should be given due consideration in conservation
programs. Original remnant patches
of forest and native vegetation among agricultural fields can be retained in
consultation with various stakeholders and local communities and managed
without further loss of biodiversity. Further studies designed to assess
diverse taxa sampled across all the four seasons (winter, pre-monsoon, monsoon
and post monsoon) in a long term basis undertaking large geographical area,
large elevation range, diverse ecosystems covering the larval and adult stage
would provide better insights on the importance of cultivated systems in
conservation of biodiversity.
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land (% of land area). The World Bank, Washington, DC.
http://data.worldbank.org/indicator/AG.LND.AGRI.ZS accessed on 27 September
2017.
Wynter-Blyth, M.A
(1957). Butterflies of the
Indian Region. The Bombay Natural History
Society, Bombay, India, 523pp.
Appendix I. Butterflies observed in
three ecosystems of southern Sikkim, eastern Himalaya including their habitat,
larval host specificity and larval host plant. Number represents the abundances
of butterflies observed during the study.
|
Species |
Scientific name |
FAS |
LCAS |
NFS |
Total |
$Habitat |
Larval host specificity |
Larval host plants species and family |
|
Hesperiidae |
|
|
|
|
|
|
|
|
1 |
Common Small Flat |
Sarangesa dasahara Moore, 1866 |
- |
- |
2 |
2 |
FI |
Monophagous |
Asystasia macrocarpa (Acanthaceae) |
2 |
Spotted Demon |
Notocrypta feisthamelii Boisduval, 1832 |
- |
2 |
2 |
4 |
FI |
Oligophagous II |
Curcuma aromatica, Hedychium acuminatum (Zingiberaceae) |
|
Lycaenidae |
|
|
|
|
|
|
|
|
3 |
Azure Sapphire |
Heliophorus moorei Hewiston, 1856 |
5 |
1 |
3 |
9 |
FE + OL |
- |
- |
4 |
Common Cerulean |
Jamides celeno Cramer, 1775 |
- |
6 |
- |
6 |
OL |
Oligophagous II |
Butea monosperma, Crotolaria spp., Derris indica, Pongamia
pinnata, Xylia xylocarpa (Fabaceae) |
5 |
Dark Cerulean |
Jamides bochus Stoll 1782 |
1 |
- |
3 |
4 |
FE + OL |
Oligophagous II |
Butea monosperma, Crotalaria albida,
Crotalaria ferruginea,
Crotalaria mucronata, Pongamia pinnata, Xylia xylocarpa (Fabaceae) |
6 |
Golden Sapphire |
Heliophorus brahma Moore 1857 |
4 |
- |
1 |
5 |
FE |
Oligophagous II |
Polygonum nepalense, Rumex nepalensis (Polygonaceae) |
7 |
Malayan |
Megisba malaya Horsfield, 1828 |
- |
2 |
- |
2 |
FE |
Monophagous |
Allophylus cobbe (Sapindaceae). |
8 |
Metallic Cerulean |
Jamides alecto Felder, 1860 |
76 |
38 |
34 |
148 |
OL |
Oligophagous II |
Boesenbergia rotunda, Elettaria
cardamomum (Zingiberaceae) |
9 |
Pale Grass blue |
Pseudozizeeria maha Kollar, 1844 |
7 |
1 |
- |
8 |
OL |
Polyphagous |
Strobilanthes capitatus, Strobilanthes
roseus, Strobilanthes thomsoni (Acanthaceae);
Oxalis corniculata (Oxalidaceae) |
10 |
Pea Blue |
Lampides boeticus Linnaeus, 1767 |
7 |
- |
9 |
16 |
FE + OL |
Oligophagous II |
Butea minor, Crotalaria albida,
Crotalaria ferruginea, Crotolaria mucronata (Fabaceae) |
11 |
White Cerulean |
Jamides pura Moore, 1886 |
2 |
- |
- |
2 |
OL |
- |
- |
|
Nymphalidae |
|
|
|
|
|
|
|
|
12 |
Banded Treebrown |
Lethe confusa Aurivillis, 1898 |
- |
- |
1 |
1 |
FI |
Monophagous |
Poa annua (Poaceae) |
13 |
Blue Tiger |
Tirumala limniace Cramer, 1775 |
2 |
- |
1 |
3 |
OL + FE |
Oligophagous II |
Calotropis gigantea, Calotropis procera,
Asclepias curassaviva
(Apocynaceae) |
14 |
Common Bushbrown |
Mycalesis perseus Fabricius, 1775 |
2 |
- |
4 |
6 |
FI |
Oligophagous II |
Apluda mutaca, Elusine coracan, Oryza sp., Sorghum sp.(Poaceae) |
15 |
Common Crow |
Euploea core Carmer, 1780 |
1 |
- |
- |
1 |
OL + FE |
Polyphagous |
Barleria prionitis (Acanthaceae); Nerium odorum
(Apocynaceae); Ficus benghalensis, Ficus religiosa (Moraceae) |
16 |
Common Sailer |
Neptis hylas Linneaus, 1758 |
4 |
- |
5 |
9 |
OL + FE |
Polyphagous |
Bombax ceiba (Malvaceae); Elaeocarpus lanceifolius (Elaeocarpaceae);
Dalbergia sissoo, Dalbergia stipulacea (Fabaceae); Grewia sapida
(Malvaceae) |
17 |
Common Tiger |
Danaus genutia Cramer, 1779 |
- |
3 |
3 |
6 |
OL + FE |
Oligophagous II |
Asclepias curassavica, Ceropegia lawii,
Ceropegia spp. (Apocynaceae) |
18 |
Dark-brand Bushbrown |
Mycalesis mineus Linneaus, 1758 |
- |
- |
3 |
3 |
FE |
Oligophagous II |
Lopantherum spp., Pogonontherum spp., Microstegium
spp. (Poaceae) |
19 |
Glassy Tiger |
Parantica aglea Stoll, 1782 |
- |
1 |
- |
1 |
FI |
Oligophagous II |
Ceropegia bulbosa, Cryptolepis
buchananii, Tylophora carnosa, (Apocynaceae) |
20 |
Great Evening Brown |
Melanitis zitenius Herbst, 1796 |
- |
1 |
- |
1 |
FI |
Oligophagous II |
Bambusa arundinacea, Ochlandra sp. (Poaceae) |
21 |
Great Silverstripe |
Argynnis childreni Gray, 1831 |
2 |
- |
- |
2 |
OL |
Polyphagous |
Mentha longifolia (Lamiaceae); Buddleja asiatica (Buddlejaceae);
Viola diffusa, Viola serpens, Viola tricolor (Violaceae); Rubus
niveus (Rosaceae) |
22 |
Green Commodore |
Sumalia daraxa Doubleday, 1848 |
- |
4 |
2 |
6 |
FE |
Oligophagous II |
Populus gamblei, Populus glauca, Salix
tetrasperma, Salix salwinensis (Salicaceae) |
23 |
Himalayan Fivering |
Ypthima sakra Moore, 1857 |
4 |
- |
8 |
12 |
FE |
Monophagous |
Digitaria ciliaris (Poaceae) |
24 |
Himalayan Jester |
Symbrenthia brabira Moore, 1872 |
- |
- |
1 |
1 |
FI |
Oligophagous II |
Debregeasia longifolia, Elatostema
grande (Urticaceae) |
25 |
Indian Fritillary |
Argynnis hyperbius Linnaeus, 1763 |
4 |
- |
- |
4 |
OL |
Polyphagous |
Tagetes patula, Zinnia sp. (Asteraceae); Antirrhinum
majus (Plantaginaceae); Fagopyrum sp. (Polygonaceae); Viola
diffusa, Viola serpens, Viola tricolor (Violaceae) |
26 |
Indian Red Admiral |
Vanessa indica Herbst, 1794 |
14 |
2 |
- |
16 |
OL |
Polyphagous |
Digitalis purpurea (Plantaginaceae); Urtica dioica,
Boehmeria diffusa,
Boehmeria glomerulifera, Boehmeria penduliflora, Girardinia diversifolia
(Urticaceae) |
27 |
Indian Tortoiseshell |
Aglais caschmirensis Kollar, 1844 |
68 |
20 |
17 |
105 |
OL |
Oligophagous I |
Urtica dioica, Urtica parviflora (Urticaceae) |
28 |
Large Yeoman |
Cirrochroa aoris Doubleday, 1847 |
- |
- |
1 |
1 |
FI |
Monophagous |
Hydnocarpus sp. (Achariaceae) |
29 |
Orange Oakleaf |
Kallima inachus Doyere, 1840 |
- |
- |
1 |
1 |
FI+FE |
Polyphagous |
Strobilanthes cuspidatus (Acanthaceae); Prunus
persica (Rosaceae); Polygonum orientale (Polygonaceae); Girardinia
diversifolia (Urticaceae) |
30 |
Painted Lady |
Vanessa cardui Linnaeus, 1758 |
49 |
13 |
15 |
77 |
OL + FE |
Polyphagous |
Artemisia sp., Blumea sp., Echinops echinatus,
Gnaphalium affine, Gnaphalium sp. (Asteraceae); Zornia diffusa, Zornia
gibbosa (Fabaceae); Argemone mexicana (Papaveraceae); Boehmeria
diffusa, Debregeasia bicolor, Girardinia diversifolia (Urticaceae) |
31 |
Plain Tiger |
Danaus chrysippus Linnaeus, 1758 |
- |
- |
1 |
1 |
OL + FE |
Oligophagous II |
Asclepias curassavica, Calotropis
gigantea, Cryptolepis buchananii, Ceropegia sp. (Apocynaceae) |
32 |
Himalayan Queen Fritillary |
Issoria isaeea Gray, 1846 |
13 |
1 |
5 |
19 |
OL + FE |
Polyphagous |
Viola diffusa (Violaceae); Taraxacum officinale (Asteraceae) |
33 |
Red Lacewing |
Cethosia biblis Drury, 1770 |
- |
- |
2 |
2 |
FI+FE |
Oligophagous I |
Passiflora cochinchinensis, Passiflora moluccana,
Passiflora sp. (Passifloraceae) |
34 |
Scarce Woodbrown |
Lethe siderea Marshall, 1880 |
- |
3 |
- |
3 |
FI |
- |
- |
35 |
Straight-banded Treebrown |
Lethe verma Kollar, 1884 |
- |
- |
5 |
5 |
FI |
Monophagous |
Arundinaria aristata (Poaceae) |
36 |
Yellow Coster |
Acraea issoria Hubner, 1881 |
7 |
- |
- |
7 |
OL + FE |
Polyphagous |
Boehmeria sp., Pouzolzia hirta (Urticaceae); Buddleja
asiatica (Buddlejaceae) |
|
Papilionidae |
|
|
|
|
|
|
|
|
37 |
Common Peacock |
Papilio bianor Cramer, 1777 |
- |
1 |
1 |
2 |
OL + FE |
Oligophagous II |
Zanthoxylum armatum, Zanthoxylum
achanthopodium, Clausena sp.,
Citrus spp. (Rutaceae) |
|
Pieridae |
|
|
|
|
|
|
|
|
38 |
Common Grass Yellow |
Eurema hecabe Linnaeus, 1758 |
2 |
5 |
9 |
16 |
OL + FE |
Oligophagous II |
Acacia gageana, Acacia pennata, Albizia
procera, Caesalpinia sp., Cassia
fistula, Cassia mimosoides, Cassia siamea, Cassia tora, Moullava spicata,
Pithelobium dulce (Fabaceae) |
39 |
Common Jezebel |
Delias eucharis Drury, 1773 |
1 |
- |
1 |
2 |
OL + FE |
Oligophagous II |
Dendrophthoe falcata, Loranthus
longiflorus, Loranthus elasticus, Scurrula sp. and Viscum sp.
(Loranthaceae) |
40 |
Dark Clouded Yellow |
Colias fieldii Menetries ,1855 |
56 |
9 |
17 |
82 |
OL + FE |
Polyphagous |
Trifolium repens, Indigofera sp. (Fabaceae); Rubus sp.
(Rosaceae) |
41 |
Indian Cabbage white |
Pieris canidia Linneaus, 1786 |
142 |
65 |
81 |
288 |
OL + FE |
Oligophagous II |
Rorippa dubia, Rorippa indica, Brassica
juncea, Sisymbrium sp.
(Brassicaceae) |
|
Riodinidae |
|
|
|
|
|
|
|
|
42 |
Dark Judy |
Abisara fylla Westwood, 1851 |
- |
- |
15 |
15 |
FI |
Monophagous |
Maesa chisia (Myrsinaceae) |
43 |
Punchinello |
Zemeros flegyas Bosiduval, 1836 |
1 |
- |
4 |
5 |
FE |
Oligophagous I |
Maesa chisia, Maesia indica, (Myrsinaceae) |
44 |
Striped Punch |
Dodona adonira Hewitson, 1866 |
- |
1 |
1 |
2 |
FE |
Monophagous |
Maesa chisia
(Myrsinaceae) |
|
Total species richness |
|
24 |
20 |
32 |
44 |
|
|
|
|
Total abundance |
|
474 |
179 |
258 |
911 |
|
|
|
$ Habitat specialization: FI (Forest interior only),
FI+FE (Forest interior + Forest edge), FE (Forest edge only), FE + OL (Forest
edge+ Openland), OL (Openland only).
FAS- farm-based
agroforestry system; LCAS- large cardamom-based agroforestry system; NFS-
natural forest.
Data source: Haribal 1992; Kunte 2000; Barua
2007; Kunte et al. 2017; Kehimkar 2008; Tiple 2012; Sengupta et al.
2014; and field observations.
Figures indicate the number of individual
butterflies observed during the study.