Micro-habitat distribution drives patch quality
for sub-tropical rocky plateau amphibians in
the northern Western Ghats, India
Christopher J. Thorpe
*, Todd R. Lewis
*, Siddharth Kulkarni
, Aparna Watve
, David Pryce
, Lewis Davies
, David T. Bilton
, Mairi E. Knight
1Ecology and Evolution Research Group, School of Biological and Marine Sciences, University of Plymouth,
Drake Circus, Plymouth, Devon, United Kingdom, 2Westfield, Wareham, Dorset, United Kingdom, 3George
Washington University, Washington D.C., United States of America, 4Tata Institute of Social Sciences,
Taljapur, Osmanabad, Maharashtra, India, 5National Centre for Biological Sciences, Rajiv Gandhi Nagar,
Kodigehalli, Bengaluru, Karnataka, India
☯These authors contributed equally to this work.
*Christopher.email@example.com (CJT); firstname.lastname@example.org(TRL)
The importance of patch quality for amphibians is frequently overlooked in distribution mod-
els. Here we demonstrate that it is highly important for the persistence of endemic and
endangered amphibians found in the threatened and fragile ecosystems that are the rocky
plateaus in Western Maharashtra, India. These plateaus are ferricretes of laterite and char-
acterise the northern section of the Western Ghats/Sri Lanka Biodiversity Hotspot, the
eighth most important global hotspot and one of the three most threatened by population
growth. We present statistically supported habitat associations for endangered and data-
deficient Indian amphibians, demonstrating significant relationships between individual spe-
cies and their microhabitats. Data were collected during early monsoon across two seasons.
Twenty-one amphibian taxa were identified from 14 lateritic plateaus between 67 and
1179m above sea level. Twelve of the study taxa had significant associations with microhab-
itats using a stepwise analysis of the AICc subroutine (distLM, Primer-e, v7). Generalist
taxa were associated with increased numbers of microhabitat types. Non-significant associ-
ations are reported for the remaining 9 taxa. Microhabitat distribution was spatially struc-
tured and driven by climate and human activity. Woody plants were associated with 44% of
high-elevation taxa. Of the 8 low-elevation taxa 63% related to water bodies and 60% of
those were associated with pools. Rock size and abundance were important for 33% of high
elevation specialists. Three of the 4 caecilians were associated with rocks in addition to soil
and stream presence. We conclude the plateaus are individualistic patches whose habitat
quality is defined by their microhabitats within climatic zones.
The Western Ghats-Sri Lanka Biodiversity hotspot is the eighth hottest global biodiversity hot-
spot and one of the three most threatened by human population growth [1–3]. The northern
PLOS ONE | https://doi.org/10.1371/journal.pone.0194810 March 26, 2018 1 / 20
Citation: Thorpe CJ, Lewis TR, Kulkarni S, Watve
A, Gaitonde N, Pryce D, et al. (2018) Micro-habitat
distribution drives patch quality for sub-tropical
rocky plateau amphibians in the northern Western
Ghats, India. PLoS ONE 13(3): e0194810. https://
Editor: Judi Hewitt, University of Waikato, NEW
Received: July 18, 2017
Accepted: March 9, 2018
Published: March 26, 2018
Copyright: ©2018 Thorpe et al. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Data Availability Statement: All data are contained
in the paper and Supporting Information file.
Funding: This work was supported by the
following: CJT: The Royal Geographical Society
with IBG (www.rgs.org) through Geographical
Fieldwork Grants in 2013 and 2014 and the Monica
Cole Award 2012. CJT: The Erasmus Darwin
Barlow Expedition Fund, Zoological Society of
London (https://www.zsl.org) grant in 2014. TRL:
Percy Sladen Memorial Trust (https://www.linnean.
org ›The Society ›Medals, Awards, Prizes and
section of the Western Ghats (NWG) is unique, being geologically distinct and biologically iso-
lated from the central and southern sections of the Western Ghats (WG) on the Indian penin-
sular (Fig 1; [4–7]. Its’ rich amphibian fauna contains many critically endangered, endangered
species and data deficient species [8,9]. The area is characterised by rocky flat mesa-like hilltop
‘plateaus’ formed from ferricretes of laterite, a rock like material with a high metal content (Fig
2; [10–12]). The individual ‘plateau’ habitat is a complex matrix of microhabitats. The avail-
ability of each microhabitat varies between plateaus, but some macroscale patterns are evident.
The plateaus are set within a landscape of varying complexity [13,14]. Rocky plateaus are of
international importance for their substantial contribution to regional biodiversity and ende-
mism [15–17] and are globally threatened ecosystems [15,18]. Those in the NWG are recog-
nised as threatened and vulnerable ecosystems .
Plateau biodiversity is under pressure from demands placed by on its habitats by the rapidly
growing human population. Proximate threats, that impact habitat availability, falling into two
broad categories: localised threats such as illegal hunting, extraction of non-timber forest prod-
ucts (NTFPs), livestock grazing, and forest fires, and landscape-level threats such as mining,
road construction, hydro power projects, wind farms, large-scale agricultural intensification
including the creation of monoculture plantations and tourism [3,20,21]. Open-cast bauxite
mining is a significant current threat in the NWG [22,23]. Current mine restoration policy
does not identify the importance of preserving the pre-existing habitat or its mix of microhabi-
The WG is home to 161 of India’s 419 amphibians in only 5% of its land area, making the
WG the most amphibian rich land area in India [24–26]. In the WG they are a highly diverse
group displaying exceptional levels of endemism (87%; [3,24,27]. Many are endemic with a
very localised distribution resulting from their Gondwanan vicariant origin, having speciated
in situ because of topographical isolation and diverse ecological pressures [24,28–31]. The res-
olution of their taxonomy is improving but in common with much of the paleo tropics little
has been published on their ecology including their habitat requirements and the environmen-
tal factors regulating their distribution (but see: [25,32–34].
Amphibian distribution is known to be highly dependent upon habitat features (see e.g.
[21,35]) resulting in their populations being spatially determined by microhabitat availability.
In tropical regions the diversity of specialist micro-environments facilitates elevated levels of
species richness and endemism through heterogeneity in: seasonality or microclimate ,
gradients in precipitation [37,38], soil moisture [39,40] and elevation [41,42]. Evidence for
this in the WG comes from the high number of reproductive strategies with at least 40 different
reproductive strategies currently recognised in the region [43–48], each using different habitat
resources for mate advertising, mating, egg deposition, spawning, tadpole and neonate feeding.
In addition to their dependence on specific microhabitats the amphibians of the WG are
threatened by the fungal pathogen Batrachochytrium dendrobatidis . To mitigate these
risks, networks of suitable sites with adequate connectivity are necessary .
There is a globally recognised shortfall in amphibian population and ecological data .
To address this the Amphibian Conservation Action Plan (ACAP) was devised by the Interna-
tional Union for the Conservation of Nature (IUCN) in 2005 to prioritise research directions
. Two of the four key strategies of ACAP are to understand the causes of population declines
and changes in diversity . To achieve this, baseline data are required on their ecological
requirements [52,53]. Specifically, it is highlighted as essential to identify the key environmental
and habitat resources required by each taxon [54–56]. The IUCN recognise the importance of
preserving habitat to conserve species . However, the IUCN do not adequately account for
habitat specificity in heterogeneous topography, resulting in the ranges of many species being
overstated . At present it is almost impossible to assess the conservation status of the
Neo-tropical amphibian distribution is driven by micro-habitats in the Western Ghats Biodiversity Hotspot
PLOS ONE | https://doi.org/10.1371/journal.pone.0194810 March 26, 2018 2 / 20
Grants) award in 2014. The funders had no role in
study design, data collection and analysis, decision
to publish, or preparation of the manuscript.
Competing interests: The authors have declared
that no competing interests exist.
amphibians of the WG due to a serious deficiency in ecological data. It is likely WG amphibians
reflect the global pattern where the group is declining because of one or more stressors which
frequently work synergistically: climate change; habitat destruction; pollution; over-harvesting;
Fig 1. Map of study sites within the study area inset with location within India. Green triangles denote surveyed site
locations below the Western Ghats escarpment and blue circles sites above it. Some mine site locations are included to
illustrate the proximity of threat of mining. The biodiversity hotspot outline is derived data downloaded from ArcGIS,
Environmental Systems Research Institute, Redlands, California, USA.
Neo-tropical amphibian distribution is driven by micro-habitats in the Western Ghats Biodiversity Hotspot
PLOS ONE | https://doi.org/10.1371/journal.pone.0194810 March 26, 2018 3 / 20
Fig 2. Illustrations of the varied microhabitats present on the lateritic plateaus of western Maharashtra, NWG.
Neo-tropical amphibian distribution is driven by micro-habitats in the Western Ghats Biodiversity Hotspot
PLOS ONE | https://doi.org/10.1371/journal.pone.0194810 March 26, 2018 4 / 20
alien species introduction and/or disease [59–61]. Further work is urgently needed in the WG
in the face of climate change scenarios and alterations in land use .
Amphibian patch occupancy is dependent upon patch quality and regional factors includ-
ing patch distribution, the nature of the intervening landscape, and climate . The impor-
tance of patch quality in regulating species distribution is becoming widely recognised as a key
factor . Many species distribution studies only consider landscape scale processes as cli-
mate suitability when even with a suitable climate species may be excluded by smaller scale
processes including microhabitat availability [64,65]. We propose the availability of a suitable
suite of microhabitats on a plateau define its quality and are a result of variations in macrocli-
mate, edaphic processes and anthropogenic activities .
Given that the NWG are part of a key priority for conservation, and that their amphibians
are part of a data deficient globally vulnerable group, it is imperative that this shortfall in eco-
logical data is urgently addressed. That urgency is acute for the NWG rocky plateaus, as these
fragile ecosystems are being rapidly lost and damaged by human activity and are home to criti-
cally endangered endemic species [24,25,66]. As the first quantitative study of rocky plateau
amphibian habitat associations, the data herein will serve as a baseline to help in forming evi-
dence-based conservation decisions [25,34].
Materials and methods
The study investigated microhabitat associations of individual amphibian taxa on the isolated
lateritic plateaus in the NWG (Fig 1). These island-like plateaus are dominated by areas of
exposed rock but contain a varied mixture of other habitats forming a heterogenous mosaic
(Fig 2). The study focussed on 14 representative lateritic plateaus in the areas both above and
below the North-South trending escarpment in the northern section of the Western Ghats/Sri
Lanka Biodiversity Hotspot in western Maharashtra. The study area extends over 2˚ latitude
(15.89˚-17.92˚N) and a 1112 m change in plateau elevation (67–1179 m above sea level [m]).
Above the escarpment the plateaus are raised hilltop carapaces elevated from the ecologically
As temperature, rainfall seasonality and rainfall amount varies across the survey area, for
comparative purposes the area was sub-divided into 2 Regions (High and Low), separated by
the escarpment. Each region was further subdivided into three arbitrary latitudinal sections:
North, Central and South. These are referred to as ‘eco-zones’ (similar to life-zones but in the
absence of specific environmental data for the plateaus the term eco-zone is preferred .
Rainfall across this area ranges from <2000 mm per annum on low sites to >6000 mm on
high sites peaking at >9000 mm on one high site [12,68,69].
These sites encompass a range of land-uses (Fig 1;Table 1). As anthropogenic disturbance
within a patch is likely to change the availability of some microhabitats its type was recorded,
and an arbitrary metric calculated by summing the number of disturbance factors observed on
each site (Table 1). Although the figure is arbitrary, no relevant literature exists, and it allows
for initial between patch comparisons. Disturbance factors recorded were; removal of loose
rocks, surfaced road, unsurfaced road, built structures on the plateau, domesticated animal
grazing, surfaced road within 200m of plateau, tourism, part conversion to plantation, adjacent
built structures, importation of topsoil. Sites with 0–3 factors were considered to have low lev-
els of disturbance, 4–7 Medium Disturbance, 8+ High Disturbance. Anthropogenic distur-
bance changed the availability of some classes of microhabitat, most notably the removal of
loose rocks, reduction in woody plants in conversion for grazing and agriculture, creation of
pools on some low-level sites and importation of soil at Panchgani (Fig 2).
PLOS ONE | https://doi.org/10.1371/journal.pone.0194810 March 26, 2018 5 / 20
Field data collection methodology
Sampling of both microhabitat and amphibian presence was performed along the same belt
transects concurrently. The rocky plateaus are relatively simple ecosystems dominated by
areas of exposed rocks with varying amounts of other microhabitats. Their size varies by an
order of magnitude but based upon the smaller sites within the survey it was determined that
four belt transects each 100 m long and 6 m wide would adequately encompass all the micro-
habitat types available on an individual plateau. The direction and path of each transect was
determined at each site to maximise sampling of all available microhabitats. The same method-
ology was applied on each survey on the same plateaus in each year but with different transect
locations making a total surveyed area 4800m
To maximise detection, both diurnal and nocturnal surveys were deployed during two tem-
porally comparable survey seasons . Surveying took place each year in the same weeks at
the onset of the monsoons in late July to early August in 2013 and 2014 . Survey timing
was selected for the known range of amphibian autecology, encompassing taxa with both
explosive and prolonged breeding strategies [36,72].
To make samples comparable, standardised Visual Encounter Surveys (VES) with refugia
searching  along the belt transects were performed [73,74]. The identity of each amphibian
taxa their abundance and their microhabitat associations were recorded for each section of the
transect . Where species identity was not immediately obvious in the field photographs
were taken to permit later clarification.
Microhabitat variables recorded along the same transects as the VES surveys comprised;
maximum refugia rock size (mm), number of loose rocks >50mm, woody plant cover (as %
cover on transect), presence of soil depressions with vegetation, presence of flowing streams,
presence of static pools, presence of surface flooding (vernal pools). Although some microhab-
itats co-occurred, e.g. surface flooding and stream presence, all were included in the analysis
so that finer scale associations could be detected (Fig 2). As some NWG amphibians are semi-
terrestrial humidity levels may be considered as a micro-habitat therefore Relative humidity
included in the analysis, it was measured with a calibrated hygrometer (Hanna Instruments™
HI 9064; .
All amphibians were identified using the best available literature, and their nomenclature
considered using the latest taxonomical authorities [6,26,69,77–85]. The classification of
Table 1. Disturbance values and dominant land use for each site surveyed. To facilitate spatial comment, the study area has been sub divided into three latitudinal
zones each side of the escarpment.
Site Latitude Longitude Land use Disturbance intensity Eco-zone
Chalkewadi 17.5736 73.8261 Wind turbine Medium High North
Jagmin 17.5927 73.8181 Natural grazing Low High North
Mhavashi 17.4310 73.9313 Wind turbine Medium High North
Panchgani 17.9217 73.8045 Tourism High High North
Masai 16.8181 74.0779 Tourism/grazing High High Central
Zenda 16.9226 73.8072 Natural grazing Low High Central
Amboli Low 15.9374 74.0027 Tourism High High South
Amboli High 15.8903 74.0403 Natural grazing Low High South
Shipole 17.9735 73.0527 Agriculture Low Low North
Ratnagiri 16.9627 73.2962 Agriculture Medium Low Central
Lanja 16.7419 73.4204 Natural grazing Low Low Central
Kudopi 16.2327 73.5105 Natural grazing Low Low South
Dhamapur 16.0315 73.584 Agriculture Medium Low South
PLOS ONE | https://doi.org/10.1371/journal.pone.0194810 March 26, 2018 6 / 20
several of the taxa found in this study is still evolving. While many herpetologists have adopted
the new suggested taxonomies entirely, this study adhered to recommendations within  and
 by presenting former nomenclature alongside more recent identifications to maintain the
continuity of identification in years following taxonomic amendments. This system introduces
new and unstable taxa with the formerly acknowledged genera first and the newly identified
genera in parentheses. For example, although the changes proposed by Frost  for the genus
Rana were made at the generic level, biologists wishing to recognize the subdivisions of this
genus, but maintain the stability of familiar species names and still follow rules of the Interna-
tional Code of Zoological Nomenclature (ICZN), can recognise newly created subdivisions of
these genera as subgenera [86,87,89]. Under ICZN rules, the subgenus category may follow the
genus name in parentheses, e.g., Fejervarya (Minervarya)sahyadris or Rana (Lithobates)pipiens.
Statistical analytical methods
Primer-e and Permanova+, Primer-e v7 [90,91] were used to investigate the relationships
between taxa in the study area and their microhabitats. Biotic data were represented by a Bray-
Curtis similarity matrix of square root transformed abundance. Environmental data were rep-
resented by a Euclidian Distance matrix which was normalised before analysis. Analyses were
performed for all taxa combined and each individual taxon. Ordination and visualisation of
the model was performed in distance-based redundancy analysis (dbRDA). To identify the
microhabitats with significant taxa associations’ step-wise analysis was performed in distLM.
The step-wise routine commences with a null model then adds each criterion before checking
by tentative removal thus optimising the selection. As the sample and number of predictor var-
iables were small the Akaike Information Criterion with second order correction (AICc), was
used as it to accounts for the ratio of samples to predictor variables being lower than 40 and
performed in distLM [91,92]. The explanatory power of microhabitats for the distribution of
the biota was assessed using LINKTREE, a form of constrained binary divisive clustering. The
routine maximises the value of Rat each division in the biotic matrix in concordance with the
underlying distribution of microhabitats within each patch (site) with the B% being the differ-
ence in each linkage [90,93].
Sampling was undertaken by kind permission of the Indian National Biodiversity Authority,
Chenai, India under permit number: Maharashtra 2014 MC200621.
The advice from the representative of the University of Plymouth’s Animal Welfare and
Ethics Committee was that no formal consent was required since the animals were only
observed or received minimal handling on their site of origin. We followed strict handling and
preventative measures for cross-contamination, following standard practice for working with
amphibians as described on http://www.amphibiaweb.org. No endangered animals were spe-
cifically targeted in the study.
A total of 325 individual amphibians from 2 orders, 6 families, and 21 taxa were detected over
the two years of study (S1 Table). Abundance, taxa and microhabitats varied between all sites.
Only 47% of recorded microhabitat associations were in accordance with the IUCN habitat
descriptions (Tables 2&3; ). The 21 taxa in the study represent a small proportion of the
known amphibian taxa from India (419 from India  and 161 from Western Ghats )
but almost 40% of those that are known to occur in Maharashtra [53;94]. Distribution data
can be accessed in the Supporting Information.
PLOS ONE | https://doi.org/10.1371/journal.pone.0194810 March 26, 2018 7 / 20
Spatial distribution of microhabitats
Sites could be spatially separated at the macroscale by the relative microhabitat composition
with notable differences above and below the escarpment illustrated in Figs 3and 4(Fig 4;
R = 0.53, B% = 85%; Fig 3). The two most distinctive sites, Amboli High (Fig 4; R = 0.89,
B% = 91) and Zenda (Fig 4; R = 0.37, B% = 68), are low disturbance sites that have retained
much of their loose rock cover and have taxa associated with rock refugia (Fig 3). Lanja, a low
Table 2. Habitat association results from significant habitat associations identified in step wise analysis using AICc in distLM, Permanova+, Primer-e v7, where =
P<0.05, = P<0.01.Status is the IUCN threat status: Accessed 10/02/2017 . NA- Not Assessed; DD-Data Deficient; LC-Least Concern; EN-Endangered; CR-Criti-
cally Endangered. Population stability:/S-Stable; /D-Decreasing; /I-Increasing. RH-Relative Humidity; Rock -large loose rocks >50 mm; Rock N-abundance of small
rocks<50 mm; Plant-%of area with woody plant cover; Soil-% of area with soil; Stream-stream in surveyed area; Pool-lentic pools within surveyed area; Flood-plateau sur-
face flooded to a depth >25 mm; Agree-our habitat association agree with published findings; Elev-altitude above sea leavel taxa were found; Habitat Associations are
those listed by the IUCN.
Taxa Status RH Rock Rock N Plant Soil Stream Pool Flood Agree Elev Habitat Associations
All taxa combined 0–1179
Duttaphrynus melanostictus LC/I 0.09 x 809–1131 Generalist
Euphlyctis cyanophlyctis LC/S x 85–1131 Lentic, ephemeral water, forest, shrubland
Fejervarya (Zakerana) cf.
caperata DD 0.07 x 1156–
Semi-aquatic, grassland, plateaus,
Fejervarya (Zakerana)cepfi NA 0.08 85–156 Degraded forest
Gegeneophis cf. ramaswamii LC/S 0.08 x 809 Generalist, fossorial.
Gegeneophis seshachari DD 90–156 Forest, plantations, gardens, degraded forest
Hoplobatrachus tigerinus LC/S x 67–1131 Generalist very adaptable
Indirana chiravesi LC/D x 1015 Aquatic, lotic
Indotyphlus maharashtraensis DD x 1179 Dry grassland
Microhyla ornata LC 0.06 x 85–170 Savanna, shrubland, grassland, lentic, lotic
sahyadris EN/D 85–170 Grassland, pasture, seasonal flooding, lentic
Xanthophr yne tigerina CR/D 0.08 x 809–854 Lateritic plateaus
Table 3. The most important microhabitats for taxa that tested without significant habitat associations in the AICc analysis in distLM Permanova+, Primer-e v7.
Status is the IUCN threat status. Accessed 10/02/2017 . NA- Not Assessed; DD-Data Deficient; LC-Least Concern; EN-Endangered; CR-Critically Endangered. Popula-
tion stability:/S-Stable; /D-Decreasing; /I-Increasing. RH-Relative Humidity; Rock -large loose rocks >50 mm; Rock N-abundance of small rocks<50 mm; Plant-%of area
with woody plant cover; Soil-% of area with soil; Stream-stream in surveyed area; Pool-lentic pools within surveyed area; Flood-plateau surface flooded to a depth >25
mm; Agree-our habitat association agree with published findings; Elev-altitude above sea leavel taxa were found; Habitat Associations are those listed by the IUCN.
Taxa Status RH Rock Rock
Plant Soil Stream Pool Flood Agree Elev Habitat Associations
Fejervarya (Zakerana) cf.
brevipalmata DD x x x 1131–
Forest, grassland, wetland, degraded forest
Fejervarya sp. x 1090
Indotyphlus cf. battersbyi DD x 974 Forest, shrubland, plantations, gardens,
Philautus sp. x 170
Polypedates maculatus LC/S x 156 Forest, shrubland, lentic, disturbance tolerant
Pseudophilautus sp. x 170 Forest, degraded forest.
Raorchestes ghatei NA x 1131–
Sphaerotheca dobsonii LC/D x 85–974 Lowland forest, shrubland, seasonal lentic
Uperodon globulosus LC/S 0.07 67 Generalist, anthropogenic environments,
disturbance tolerant, generalist
PLOS ONE | https://doi.org/10.1371/journal.pone.0194810 March 26, 2018 8 / 20
disturbance site, is the most charismatic of the low region sites (Fig 4; R = 0.55, B% = 43; Fig
2). The most diverse eco-zone was the High North as illustrated by the distribution of the data
points in the dbRDA plot, reflecting the impact of three types of land use on microhabitat
availability (Fig 3,Table 1).
Pools were more abundant below the escarpment where many are manmade; their hydro-
period is shorter on the northern sites and more consistent above the escarpment. The number
of annual wet days declines south to north by 11% and there 12.7 times as many wet days
above the escarpment (Fig 1; [69–96]). Rainfall amount peaks at Amboli where it exceeds 9000
mm per annum resulting in the microhabitat ‘surface water’ separating the two Amboli sites
from the rest (Fig 3). Soil is scant on the plateaus but deepens where it has accumulated in shal-
low depressions in the ferricrete but it has also has been imported onto Panchgani plateau to
assist in tourism related activity . Loose rock abundance, important as refugia, breeding
sites and mate advertising posts, was reduced by collection from accessible sites for construc-
tion resulting in a disturbed distribution pattern (Fig 1; Tables 2&3; [12,13,48,97]). Larger
loose rocks were most absent from plateaus below the escarpment and most abundant where
human access was difficult for example in the remoter High Region plateaus for example
Zenda and Amboli High and to a lesser extent Jagmin. (Fig 2;Fig 4B, 4H & 4L; [98–100]).
Fig 3. dbRDA analysis for microhabitats with sites illustrated within eco-zonesto allow spatial comparison. dbRDA1 explained 39.3% of fitted
data and 25% of total variation with dbRDA2 explaining 19.3% of fitted data and 12.3% of total variation.
PLOS ONE | https://doi.org/10.1371/journal.pone.0194810 March 26, 2018 9 / 20
That, combined with greater woody plant cover, and for some sites surface water, separated
them from the low sites and explained much of the latitudinal divisions (Figs 3&4A, 4B, 4H,
4I, 4J and 4K).
Most sites were characterised by combinations of microhabitats and their associated taxa
(Fig 3; Tables 2&3). Such combinations are key for some taxa for example soil and rocks used
by caecilians as refugia and egg deposition sites associated with soil close to water. We found
56% of microhabitats to be impacted by anthropogenic activity Tables 2&3).
Spatial distribution of taxa and explanatory microhabitats
Pond presence on low elevation sites was the most significant abiotic variable separating their
amphibian assemblages from those above the escarpment where woody plants, surface water
and relative humidity were the principal characters (Figs 3&4). Woody plant abundance,
maximum loose rock size, surface water and pond presence were significant factors defining
the differences in the biota above and below the escarpment in both the dbRDA and LINK-
TREE analyses (Fig 3;Fig 4, 4A, 4B & 4D).
High-level sites had 9 taxa not found on low sites (Figs 2&3; Tables 2&3). Woody plants
were significantly associated with 44% of exclusive high-level taxa with no such associations
for low-level specialists (Tables 2&3). Of the 8-taxa found exclusively on low sites 63% had
significant relationships with water bodies and 60% of those were associated with pools com-
pared to only 22% on high-level sites. However, all 8 had a relationship with the co-occurring
surface flooding, highlighting the need to carefully define the types of water body.
Fig 4. Linktree analysis of plateau similarities based upon microhabitat explanations for the biotic distribution, Primer-e v7. Annotated for Eco-zones; HS-High
South; HC-High Central; HN-High North; LS-Low South; LC-Low Central; LN-Low North. A: R = 0.53; B% = 85; Woody plants<-0.117(>-0.0826). B: R = 0.89; B% =
91; Max loose rock size<0.832(>2.26) or Surface water<0.848(>1.67) or Woody plants>-0.999(<-1.23). C: R = 0.55; B% = 43; Surface water>-1.19(<-1.6) or Woody
plants<-0.345(>-0.117). D: R = 0.37; B% = 29; Woody plants<-0.738(>-0.607). E: R = 0.54; B% = 20; Stream>0.743(<-1.1) or Max loose rock size<-0.871(>0.00354)
or Surface water>-0.377(<-0.785) or Woody plants>-0.738(<-0.999). F: R = 0.00; B% = 11; Max loose rock size<0.00354(>0.832) or Soil Cover<-0.791(>0) or N.
Rocks>-0.0943(<-0.7) or Surface water>-0.785(<-1.19). G: R = 1.00; B% = 26; N. Rocks<-1.09(>2.13) or Pools<-0.832(>1.23) or Surface water>0.848(<-1.19) or Soil
Cover<0(>1.58) or Max loose rock size<-1.42(>-0.0425) or Stream>0.743(<-0.177) or Woody plants<-0.607(>-0.345). H: R = 0.37; B% = 68; N. Rocks<-0.067
(>1.63) or Woody plants>0.376(<-0.0826). I: R = 0.54; B% = 67; Woody plants>2.31(<1.39) or N. Rocks<-1.03(>-0.997). J: R = 0.63; B% = 55; Soil Cover<0(>2.37)
or N. Rocks<-0.206(>-0.067). K: R = 0.50; B% = 42; Surface water<-0.377(>0.44). L: R = 0.50; B% = 23; Stream<-1.1(>1.66) or Max loose rock size<-1.24(>0.786) or
Woody plants<0.376(>1.39) or Surface water>1.26(<0.44) or Soil Cover<-0.791(>0) or N. Rocks<-0.997(>-0.206) or Pools<-0.832(>-0.317).
PLOS ONE | https://doi.org/10.1371/journal.pone.0194810 March 26, 2018 10 / 20
Twelve of the 21-study taxa had significant habitat associations with the remaining 9 having
associations that, whilst not significant, were identifiable (Tables 2&3). Taxa in the study are
described as generalists after the IUCN description where they lack habitat specificity. Gener-
alists that are very widely distributed indicating broad climatic and habitat tolerances are
described as ubiquitous . The remaining taxa, Uperodon globulosus, characterised as a gener-
alist, was only detected when it was raining and had a relationship with relative humidity per-
haps explaining its limited detection (Table 3 ). The generalist taxa did not have a
noticeably higher number of habitat associations than other taxa except Hoplobatrachus tigeri-
nus, which whilst currently described as a generalist, should more appropriately be assessed as
Some 52% taxa were found in habitats other than those recorded by the IUCN, with 91% of
the taxa sampled not previously recorded from lateritic plateaus . Just over 67% of taxa in
the study were associated with water bodies. Surface Flooding was the most important form of
water on the plateaus being significant for 48% of taxa, Pools for 33% and Streams for 24%. Of
the pool specialists 50% were only found on low level sites where pools were more common.
Loose rocks measured by both size and abundance were the next most important microhabitat
being significant for 33% of taxa, 19% with small rock abundance and 14% associated with
large rocks. Rock sizes and abundance were meaningful in defining the different regions
where large rocks were important for 33% of high-level specialists (Tables 2&3). The abun-
dance of small rocks (<50 mm) was essential for 33% of exclusively low-level taxa but only one
high-level specialist (Tables 2&3).
There were 29% of taxa associated with soil-filled depressions. Only 19% of taxa were asso-
ciated with woody plants despite their being one of the defining microhabitats (Fig 2, Tables 2
&3). The IUCN lists just 2 of the 21 taxa found as being associated with lateritic plateaus .
Generalist taxa were associated with a higher number of microhabitats (mean 3.7) than the
other taxa (1.7). Fejervarya (Zakerana) cf. cepfi,Raorchestes cf. ghatei have not been assessed
yet and their association should be noted with their first assessment. Fejervarya (Zakerana) cf.
caperata,Gegeneophis seshachari,Indotyphlus maharashtraensis and Indotyphlus cf. battersbyi
are all data deficient, thus the data presented here will form part of their initial assessment.
Many amphibians were detected under lateritic rock refugia in diurnal surveys. Only 5 taxa,
Hoplobatrachus tigerinus,Fejevarya cf. caperata,Fejevarya (Minevarya) cf. sahyadris,Indoty-
plus cf. beddomii and Xanthophryne tigerina were found across open areas during the day, and
these were only encountered during rainy periods. The above open area taxa were often well
camouflaged against the texture of the lateritic rock or among short grass growing on soil
depressions. Nocturnal transects confirmed the presence of most of the diurnal anurans with-
out adding new taxa to the sample.
Caecilian microhabitats on lateritic plateaus
Soil is important for many amphibians providing sites to aestivate but is critical the semi-fos-
sorial caecilians [101–103]. Three of the 4 caecilian taxa were associated with rocks in addition
to areas of soil or stream presence (Tables 2&3). The exception was Gegeneophis cf. ramaswa-
mii, considered a generalist fossorial taxon, a view this study supports from results associating
it with soil-filled depressions (Table 2; ). We observed that Indotyphlidae sp, were detected
diurnally under lateritic rocks that were positioned on soil depressions indicating the impor-
tance of co-occurrence of some microhabitats. These soil depressions were often no deeper
than 10 cm. Gegeneophis cf. ramaswamii,G.seshachari,Indotyphlus cf. battersbyi and I.mahar-
ashtraensis were all located between the rock and the soil substrate although not significantly
for G. cf. ramaswamii. One single I.maharashtraensis at Jagmin was found emerging from a
PLOS ONE | https://doi.org/10.1371/journal.pone.0194810 March 26, 2018 11 / 20
soil depression next to rain fed flowing run-off stream after nearby terrain was disturbed by
searching activity. The rocks caecilians were detected under were all within a short distance (no
more than 20 m) from surface run-off, stream, or wet seep areas supporting the view soil mois-
ture was likely to be highly important to the group . The Gegenophis sp are oviparous and
use rocks to shelter their young, for example, Gegeneophis seshachari at Kudopi comprised a mix-
ture of adult and juveniles all found under rocks within a single 50m stretch of wet run-off .
Much literature only describes the broad habitat and not the microhabitats required by the indi-
vidual taxa for example forest or savannah . The distribution of microhabitats on the plateaus
in the NWG was non-random irrespective of the scale of observation as their pattern reflects
the edaphic processes, macroclimate and disturbance factors at play in the region (Figs 2,3&
4). The presence and abundance of some of those microhabitats were changed by human activ-
ity. All taxa in the study had identifiable habitat associations, with the majority being significant
(Tables 2&3). The study found that each lateritic plateau, whilst having core microhabitat simi-
larities, had a unique habitat and thus identity. Therefore, a macroscale distribution amphibian
pattern derived from macroclimate and surrounding countryside alone was imperfect and
patch quality in terms of microhabitat availability and thus regulating patch habitat must be
included as explanatory factor. We find patch quality, within a climatic region, was best defined
by its microhabitat mix. Some microhabitat availability was directly related to anthropogenic
activity. The rarest taxa in the study were the most sensitive to anthropogenic habitat alteration.
The plateaus have localised microclimates and offer habitats, comprised of mosaics of
microhabitats, and are at high ecological contrast to the surrounding landscape . There is
evidence to suggest that has resulted in genetic isolation between plateaus in other taxa [105,
106]. The resulting amphibian distribution reflects both the isolation and divergent pressure
within the WG through the exceptional levels of endemism on the plateaus of the NWG; 61%
of the sample were endemic to Asia, 52% to India and 38% to the WG with Raorchestes ghatei
and Xanthophryne tigerina only known from lateritic plateaus (Tables 2&3). More common
taxa, which we characterise as generalists, are able to move through the countryside between
plateaus and can persist on plateaus through metapopulation dynamics [13,65,107]. Both the
common taxa and the rare ones that cannot cross the space between plateaus are reliant upon
suitable habitat availability within each plateau [12,13,64]. Therefore, habitat quality was
highly important in determining the presence and persistence of many taxa but most impor-
tantly the rare ones. That quality depends on both landscape level variables including climate,
seasonality and topography and within-plateau elements .
Many amphibians use water as their primary habitat to avoid desiccation or predation and
as a breeding resource and that was reflected with the majority (67%) of the sample being asso-
ciated with water bodies, a figure very close to that published for other areas in the WG (62%),
(Tables 2&3; [25,43,102]). However, non-aquatic microhabitat associations were also found
for 78% of the sample taxa (Tables 2&3). Those microhabitats, climatic and habitat combina-
tions fulfil a variety of ecological purposes beyond their basic physiological requirements; refu-
gia from climatic extremes  and predators [109,110], mate advertisement perches ,
sites for egg deposition [111,112], breeding resources [36,43,113]; reproductive behaviour is
selected for by suitable rainfall and relative humidity conditions [48,106,114].
Seasonal changes in microhabitat use
Many of the plateau taxa breed close to the start of the monsoon and they may have been
detected in association with their breeding microhabitats [48,115]. The plateaus are all highly
PLOS ONE | https://doi.org/10.1371/journal.pone.0194810 March 26, 2018 12 / 20
seasonal only receiving rainfall for around four months a year resulting in the need for sea-
sonal movement to avoid desiccation and to access breeding sites [36,106,115]. Rainfall,
hydroperiod and the associated relative humidity are important factors for taxa with terrestrial
or semi-terrestrial larvae for example Xanthophryne tigerina which was found only in the very
wet southern high sites [6,36,48].
Generalist taxa microhabitat associations
Generalist taxa in this study were associated with more than twice as many types of microhabi-
tat than the mean for other taxa (Table 2). However, the IUCN definition may be spatially
too coarse to adequately describe patch quality as it makes little reference to microhabitat asso-
ciations. There were two non-generalist taxa, Gegeneophis seshachari and Microhyla ornata,
with very similar number of associated microhabitats (4) to the generalist total (3.7) suggesting
that they too were generalists. However, such a result can be explained by co-occurrence
microhabitats necessary for some taxa. For example, the microhabitats for Gegeneophis sesha-
chari encompass a range predictable for a caecilian; rock, soil and water (Table 2). Another,
Gegeneophis cf. ramaswamii, was perhaps wrongly identified as a generalist as it appears to
require specific combinations of microhabitats to persist but can also be found among a range
of landscapes. Similarly, Microhyla ornata should be reclassified as a habitat generalist in the
context of lateritic plateaus. The generalist taxa, Duttaphrynus melanostictus and Hoplobatra-
chus tigerinus each have associations with all three aquatic microhabitats. This was an unsur-
prising result as both are pond breeding taxa that are also associated with abundant woody
plant cover (Table 2; [32,33]).
Impact of elevation on microhabitat associations
Tropical site habitats are known to change with elevation a view supported by this study (Figs
2&3; [41,42,116]. The drivers of elevational differences in the amphibian assemblages on the
plateaus of the NWG were microhabitats dependent upon rainfall increasing which increased
in frequency and volume with increasing elevation and hydroperiod which decreases with lati-
tude. Although not directly related to elevation the ease of access onto low elevation sites, and
their agricultural land use, has increased man-made pool frequency and reduced the abun-
dance of large rocks (Figs 2,3&4). The combination of long periods of rainfall, the related
high relative humidity and abundance of loose rocks on Amboli High and to a lesser extent
Amboli Low creates a special habitat the critically endangered and declining Amboli Toad,
Xanthophryne tigerina, The large rocks provide three major resources, refugia, breeding sites
and mate advertisement sites . All of these are highly important resources for not only X.
tigerina,but as breeding sites for Caecilians . Woody plant abundance was one of the
main microhabitats to define the regional difference between the high and low-level sites (Figs
3&4). Together with its associated soil filled depressions woody plants were highly important
in amphibian distribution on the NWG plateaus across all elevations but impacting different
taxa (Tables 2&3).
The effect of anthropogenic disturbance on amphibian microhabitats
Microhabitat availability was changed by three forms of anthropogenic disturbance on the
plateaus; removal e.g. loose rocks, damage e.g. trampling or cutting down of plants and alter-
ation by addition of foreign material e.g. soil at Panchami. Anthropogenic disturbance was
also evidenced by construction and pollution. We did not examine the impact of addition by
construction, pollution or trampling and therefore cannot comment specifically on these,
although the sites with wind turbines had some construction on them. All rural communities
PLOS ONE | https://doi.org/10.1371/journal.pone.0194810 March 26, 2018 13 / 20
close to the plateaus carried out the common practice of harvesting loose rock and utilising it
for construction of dwellings, walls and memorials . Therefore, sites at which there were
quantities of rocks >50 mm
were often farther from human residences. Given that many of
the amphibian taxa in this study were associated with, detected under, or proximate to cover
provided by rocks >50 mm
we suggest that the natural occurrence of rocks >50 mm
teau sites is an essential microhabitat resource for all amphibians, and one that is a rapidly
emerging conservation concern for all plateaus.
Disturbance by the addition of soil, together with tourist related activity; on the high-level
site Panchgani has shifted the taxa assemblage towards one dominated by generalist or widely
distributed taxa (Tables 2&3). The addition of soil has closed almost all the fissure refugia and
all large loose rocks and most small ones have been removed, limiting the available types of
refugia, breeding and mate advertisement sites. This site is popular with equine tourism and
this local industry has resulted in infrastructure development (cafes, stables and roads), soil
compaction and increasing levels of domestic refuse. The pools also have a high silt load from
the imported soil and grazing. A total of 24 individual amphibians were recorded from this
plateau. Although amphibian counts were relatively high in comparison to lower disturbance
sites, several of the taxa recorded (D.melanostictus,E.cyanophlyctis and H.tigerinus) are con-
sidered widespread or generalist taxa, listed as ’’least concern’’ in the IUCN status reports
(Tables 2&3). D.melanostictus,E.cyanophlyctis and H.tigerinus were anticipated as taxa
known to associate with anthropocentrically disturbed or modified habitats (Daniel, 2002).
However, the presence of Raorchestes cf. ghatei and Fejevarya cf. brevipalmata may be sur-
prising as they had limited distribution and are data deficient taxa in need of more robust
ecological and population studies (Tables 2&3). Panchgani has a number of large pools con-
structed for watering livestock and anthropogenic uses. The largest is likely to hold some water
throughout an average year possibly shaping the community by offering aquatic refugia in the
dry season not seen on many sites. That may be a significant factor structuring the assemblage
as it would favour pond specialist taxa .
Surface topography on the low-level plateaus creates some pools but many additional ones
have been created by farmers in association with their agricultural land use. At a landscape
level pool frequency is important in maintaining population connectivity and persistence
Impact of climate change on the amphibians of the northern Western
Two changes in climate are predicted to impact the amphibian microhabitat requirements in
the NWG: increasing temperature and fragmentation of the monsoon rains . Both will
require microhabitat resources to mitigate their effects; as refugia from increased temperatures
and desiccation [107,122]. The woody plants and rocks in this study provide thermal refugia
allowing behavioural temperature regulation and are therefore key microhabitats worthy of
preservation . Breaks in rainfall that occur when larvae are in pools or in hygropetric hab-
itats are likely to cause significant losses. To offset these, maximum availabilities of both popu-
lations and microhabitats should be preserved.
We conclude that microhabitat availability is a good way of defining patch quality for amphibi-
ans within a climatic zone and preserving patch quality is important for conserving amphibi-
ans. The study, as the first statistically supported in the NWG, has added substantially to
known amphibian microhabitat associations. Spatial variation in microhabitat distribution in
PLOS ONE | https://doi.org/10.1371/journal.pone.0194810 March 26, 2018 14 / 20
part explains amphibian diversity on the threatened lateritic plateaus in the NWG. The preser-
vation of a wide a range of microhabitats is clearly important for amphibian conservation. It is
clear that the NWG lateritic plateaus, with their unique microhabitat assemblages, are highly
important habitats for a significant number of threatened amphibians and conservation policy
should aim to preserve representative plateaus from each eco-zone. Preservation of microhabi-
tats that provide thermal and desiccation refugia will become increasingly important for the
persistence of plateau amphibians in the face of increasing temperatures and a more frag-
mented monsoon; these include pools, large rocks and woody plants .
S1 Table. Breakdown of abundance data by taxa, site, eco-zone, year and day-night time
Many people have helped to bring the project to fruition: Dr. Aparna Watve and Sanjay Tha-
kur for their tireless support; Anand Padhye, Nikhil Gaitonde, Hemant Ghate, David Gower
and Varad Giri helped resolve identification. We also thank the numerous local residents
across the Western Ghats for tea and helping navigate us to awkward plateau summits.
Conceptualization: Christopher J. Thorpe, Aparna Watve.
Formal analysis: Christopher J. Thorpe.
Funding acquisition: Christopher J. Thorpe, Todd R. Lewis.
Investigation: Christopher J. Thorpe, Todd R. Lewis, Siddharth Kulkarni, Aparna Watve,
Nikhil Gaitonde, David Pryce, Lewis Davies, Mairi E. Knight.
Methodology: Christopher J. Thorpe.
Project administration: Christopher J. Thorpe, Aparna Watve.
Resources: Christopher J. Thorpe, Siddharth Kulkarni.
Supervision: David T. Bilton, Mairi E. Knight.
Writing – original draft: Christopher J. Thorpe.
Writing – review & editing: Christopher J. Thorpe, Todd R. Lewis, David T. Bilton, Mairi E.
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