ArticlePDF Available

Climate structuring of Batrachochytrium dendrobatidis infection in the threatened amphibians of the northern Western Ghats, India

Authors:

Abstract and Figures

Batrachochytrium dendrobatidis (Bd) is a pathogen killing amphibians worldwide. Its impact across much of Asia is poorly characterized. This study systematically surveyed amphibians for Bd across rocky plateaus in the northern section of the Western Ghats biodiversity hotspot, India, including the first surveys of the plateaus in the coastal region. These ecosystems offer an epidemiological model system since they are characterized by differing levels of connectivity, edaphic and climatic conditions, and anthropogenic stressors. One hundred and eighteen individuals of 21 species of Anura and Apoda on 13 plateaus ranging from 67 to 1179 m above sea level and 15.89 to 17.92° North latitude were sampled. Using qPCR protocols, 79% of species and 27% of individuals tested were positive for Bd. This is the first record of Bd in caecilians in India, the Critically Endangered Xanthophryne tigerina and Endangered Fejervarya cf. sahyadris. Mean site prevalence was 28.15%. Prevalence below the escarpment was
This content is subject to copyright.
rsos.royalsocietypublishing.org
Research
Cite this article: Thorpe CJ, Lewis TR, Fisher
MC,WierzbickiCJ,KulkarniS,PryceD,DaviesL,
Watve A, Knight ME. 2018 Climate struc turing
of Batrachochytrium dendrobatidis infection in
the threatened amphibians of the northern
Western Ghats, India. R.S oc.open sc i. 5: 180211.
http://dx.doi.org/10.1098/rsos.180211
Received: 7 February 2018
Accepted: 4 May 2018
Subject Category:
Biology (whole organism)
Subject Areas:
ecology/biogeography/environmental science
Keywords:
Western Ghats, chytrid, amphibians,
caecilians, plateaus
Authors for correspondence:
Christopher J. Thorpe
e-mail: christopher.thorpe@plymouth.ac.uk
Tod d R. Lewis
e-mail: ecolewis@gmail.com
Electronic supplementary material is available
online at https://dx.doi.org/10.6084/m9.
gshare.c.4114046.
Climate structuring of
Batrachochytrium
dendrobatidis infection in
the threatened amphibians
of the northern Western
Ghats, India
Christopher J. Thorpe1,ToddR.Lewis
2, Matthew C.
Fisher3, Claudia J. Wierzbicki3, Siddharth Kulkarni4,
David Pryce1, Lewis Davies1,AparnaWatve
5and
Mairi E. Knight1
1Ecology, Behaviour and Evolution Research Group, School of Biological and Marine
Sciences, University of Plymouth, Drake Circus, Plymouth, Devon PL4 8AA, UK
2Westeld, 4 Worgret Road, Wareham, Dorset BH20 4PJ, UK
3Department of Infectious Disease Epidemiology, Imperial College London,
London W2 1 PG, UK
4Department of Biological Sciences, George Washington University, 2121 I St NW,
Washington, DC 20052, USA
5Tata Institute of Social Sciences, Apsinga Road, PO B oxNo. 09, Tuljapur 413 601,
District-Osmanabad, Maharashtra, India
CJT, 0000-0002-1045-8408; TRL, 0000-0001-5433-8777;MCF,
0000-0002-1862-6402
Batrachochytrium dendrobatidis (Bd) is a pathogen killing
amphibians worldwide. Its impact across much of Asia
is poorly characterized. This study systematically surveyed
amphibians for Bd across rocky plateaus in the northern section
of the Western Ghats biodiversity hotspot, India, including
the first surveys of the plateaus in the coastal region. These
ecosystems offer an epidemiological model system since they
are characterized by differing levels of connectivity, edaphic
and climatic conditions, and anthropogenic stressors. One
hundred and eighteen individuals of 21 species of Anura
and Apoda on 13 plateaus ranging from 67 to 1179 m above
sea level and 15.89 to 17.92° North latitude were sampled.
Using qPCR protocols, 79% of species and 27% of individuals
tested were positive for Bd. This is the first record of Bd
in caecilians in India, the Critically Endangered Xanthophryne
tigerina and Endangered Fejervarya cf. sahyadris.Meansite
prevalence was 28.15%. Prevalence below the escarpment was
2018 The Authors. Published by the Royal Society under the terms of the Creative Commons
Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted
use, provided the original author and source are credited.
2
rsos.royalsocietypublishing.org R. Soc. open sci. 5: 180211
................................................
31.2% and 25.4% above. The intensity of infection (GE) showed the reverse pattern. Infection
may be related to elevational temperature changes, thermal exclusion, inter-site connectivity and
anthropogenic disturbance. Coastal plateaus may be thermal refuges from Bd. Infected amphibians
represented a wide range of ecological traits posing interesting questions about transmission routes.
1. Introduction
Batrachochytrium dendrobatidis (Bd)[1] is an aggressive species of chytrid fungus that can cause the lethal
amphibian infection chytridiomycosis [2]. Following the emergence of a hypervirulent lineage of Bd, the
global panzootic lineage (BdGPL) [3], in the early twentieth century, the pathogen has been responsible
for the loss of entire species [4] and is considered a significant threat wherever it is found [5]. The presence
of Bd in the Western Ghats (WG) biodiversity hotspot [6] has been known since 2011 [7], with its known
range in the WG extended in 2015 [8], and chytridiomycosis was reported from the northern WG in 2013
[9]. It was identified as an endemic Asian strain in 2013 [9]. It remains unclear what factors regulate
the distribution of Bd in the WG and its transmission, and what the reasons are for its current generally
sub-lethal state in the region. In a peculiar twist of fate, regions that are home to the world’s greatest
amphibian diversity are also most suitable for Bd [10]. In a global model, Olson et al.[2] found the entire
WG to be suitable habitat for the pathogen [2].
The WG in southwest India occupy just 5% of the country’s land mass and yet are home to some 42%
of its amphibian species (approx. 161 species) [11,12]. Not only are the WG highly specious but many
of its amphibian species are rare, with 87% being WG endemics [12]. The amphibians that are endemic
to the rocky plateaus (plateaus) face both proximate and ultimate threats including climate change [13],
and regional stressors (population growth [14]), along with rapid habitat loss through mining, tourism
and wind turbine installations [1518]. They also face challenges from pathogens such as the fungus
Batrachochytrium dendrobatidis (Bd)[79]. Systematic studies on Bd in Asia are under-represented in the
literature [19], and this study aims to help to address that shortfall.
The three studies that have been published so far examining Bd infection in the Western Ghats
biodiversity hotspot cover almost the entire length of the WG and report widely differing levels of
infection ranging from 0.6% [7] to 25% [9]. The most geographically extensive study, covering the
northern, central and southern WG, reported an infection rate of 1.6% [8]. All three studies excluded
the low-lying sites between the coast and the hills. Molur et al. [8] published a predictive model showing
higher risk of infection south of approximately 14.5°N in the central section of the WG.
This present study adds considerably to the previous WG publications by surveying low elevation
sites for the first time. In addition, this is the first study in the WG to offer data on habitat specific
infection rates, and infection patterns across a wide range of elevations. Such data are highly important
as the high-level plateaus are becoming recognized as centres of endemism for a number of taxonomic
groups and data on all threats are urgently needed for their effective management [1720].
2. Methods
2.1. Study area
The WG are a chain of hills some 1500 km in length running parallel and slightly inland from the south
west coast of India from the Maharashtra/Gujarat state border to the country’s southern tip (figure 1).
They are part of the Western Ghats–Sri Lanka biodiversity hotspot [6] and the eighth ‘hottest’ hotspot
on the planet [21]. Unlike the granitic central and southern sections, the northern section in western
Maharashtra, known as the Deccan Traps (DT), is formed from basalt. The plateaus are ferricretes of
laterite forming hilltop carapaces above the escarpment on the western edge of the WG rising to 1200 m
above sea level (m), with extensive low-lying plateaus below in an area known as the Konkan [22].
Temperatures range from 15°–40°C in the Konkan and 4°–42°C above the escarpment [23]. The higher
elevation amphibian populations are exposed to lower temperatures that may be more conducive to Bd
infection [24].
2.2. Amphibian sampling
Amphibians were sampled from 13 representative plateaus situated in the northern WG both above and
below the North–South escarpment in western Maharashtra during the early monsoon in 2013 and 2014
3
rsos.royalsocietypublishing.org R. Soc. open sci. 5: 180211
................................................
towns
mines
state boundary
Western Ghats BDH
01020 40km
Figure 1. Map of study area, with study area location within India (inset). Nearest large towns areshown for reference points. Blue circles
denote plateaus in the High Region and green triangles those in the Low Region. Mine sites are indicated to reect one of the risks to
these sites. The biodiversity hotspot (BDH) [6] outline wascreated in ArcGIS based on data downloaded from ESRI (Environmental Systems
Research Institute, Redlands, California, USA).
(late July–early August; figure 1, electronic supplementary material, table S3). Plateaus were selected to
represent the latitudinal and elevation extent of laterite in western Maharashtra together with the range
of land uses in each region (electronic supplementary material, table S3). Visual encounter surveys with
supplementary refugia searching were performed along four 6m by 100 m transects on each plateau
in each year [25,26]. Anthropogenic disturbance factors assessed at each site were: removal of loose
rocks, surfaced road, unsurfaced road, built structures on the plateau, domesticated animal grazing,
surfaced road within 200 m of plateau, tourism, part conversion to plantation, adjacent built structures
4
rsos.royalsocietypublishing.org R. Soc. open sci. 5: 180211
................................................
and importation of topsoil. Sites with 0–3 factors were considered to have low levels of disturbance,
those with 4–7 medium disturbance and with 8+high disturbance (electronic supplementary material,
table S3).
Sampled amphibians were identified by morphological comparison with the best literature available
(including [2745]). Many WG amphibians are taxonomically cryptic or unstable [4345]; in cases where
species-level identification may be in doubt we use ‘cf.’.
2.3. Field sampling and laboratory techniques
Amphibians were all hand-captured, individually bagged and transported to shelter where skin swabs
were taken from ventral surfaces. Swabbing was performed by a pair of surveyors using sterile cotton
tip swabs (T/S16-B; Technical Service Consultants Ltd) [46,47]. The ventrum, drink patch, thighs and
toe-webbing of each adult anuran and metamorph were swabbed multiple times following published
standardized protocols [48]. For caecilians a simpler approach of multiple swab strokes along the whole
of the body was used. Swabs were broken off into sterile vials of 99% ethanol. Disposable equipment
(latex gloves and polythene bags) were replenished between specimens and sites. Other equipment was
sterilized using VirkonS™ solution or dried to minimize cross-contamination.
DNA extraction from the swabs followed the protocol described by Boyle et al.[46,49]. A quantitative
real-time polymerase chain reaction (qPCR) diagnostic assay was used with Bd specific probes for the
ribosomal gene region ITS-1/5.8S [49]. The qPCR was run on an Applied Biosystems QuantStudio 7 Flex
Real-Time PCR System with an additional 10 cycles being added to the Boyle protocol (60 cycles total).
Standards of known concentration of Bd DNA (100, 10, 1, 0.1 Bd GE (zoospore genomic equivalents))
were used as positive controls and standards together with no template control (NTC) of molecular
grade water as a negative control. The samples were run in duplicate with single positives repeated. A
positive result was a sample with a GE greater than 0.1 in both samples in a qPCR pair, a single was a
sample for which only one of each qPCR pair had a GE greater than 0.1 and a weak signal was where
only one out of four qPCR scores was greater than 0.1.
2.4. Environmental correlates
Bd is sensitive to a range of changes in the abiotic environment. Plateau soils are acidic, ranging as
low as pH 4.9 which is below the Bd optimum of pH 6–8 [16,23,50]. In addition, Bd is temperature-
sensitive, growing best between 17 and 25°C with an optimum of 23°C [50,51]. Temperature may
also regulate the pathogenicity of Bd, with frogs exposed between 17 and 23°C more likely to die
than those exposed at 27°C [52]. The fungus is reported to die when the temperature exceeds
30°C, a level exceeded at times on all plateaus [10,16]. Lower seasonal temperatures, such as those
during the monsoon at higher elevations in the WG, are known to favour the pathogen [50]. The
plateaus are mosaics of microhabitats set in a heterogeneous landscape with unknown degrees of
connectivity for Bd [15,16,23,53]. Microhabitats include expanses of exposed rock often with associated
loose rocks. Exposed rock absorbs solar radiation giving it a surface temperature higher than the
air, perhaps creating microclimates that may reduce the intensity and presence of the pathogen [54].
Other microhabitats include loose rocks and fissures offering refugia from dry areas and excessive
temperatures [5557]. Optimum rainfall for Bd is reported to be between 1500 and 2500 mm a year.
Only the low lying plateaus fall within this range, the plateaus along the top of the escarpment
receiving between 4000 and 9000 mm, with the exception of Masai which is east of the ridge and may be
drier [10,55].
Macro-environment and physiochemical data were recorded for each site: air, soil and water
temperature (°C) and pool pH using a calibrated electrical probe (Hanna Instruments™ HI 9064);
elevation (m), latitude and longitude for the start and end of each transect using a hand held GPS
(Garmin™ 60csx GPS).
3. Permission for eldwork
Permission for accessing biodiversity in India including the fieldwork was granted by the National
Biodiversity Authority, India, to C. J. Thorpe, permit number MC200621. The permit authorizes some
other authors to assist with sampling.
5
rsos.royalsocietypublishing.org R. Soc. open sci. 5: 180211
................................................
4. Data analysis
To help make analytical comparisons at a range of spatial scales, the study area was divided into two
regions: above the Western Ghats escarpment (High Region), and below it (Low Region). The dividing
line was set at 700 m above sea level. Each region was arbitrarily sub-divided into three latitudinal
groups North, Central and South (electronic supplementary material, table S3). Correlations between
site elevation, temperature and pH were explored through Pearson product moment correlation for
parametric data and Spearman rank correlation for non-parametric data. To assess the impact of the
spatial arrangement and disturbance on Bd GE values, general linear model (GLM) and one-way ANOVA
analyses were performed to investigate elevation, latitude, region, disturbance type and disturbance
intensity. Results are reported with a confidence level (CL) of 95% together with upper and lower bi-
nomial confidence bounds (CB), which are the outer values of the confidence interval that are expressed
as percentages [58,59].
5. Results
5.1. Overview of Bd infection in the study area
A total of 118 sample swabs were taken from individuals belonging to 2 orders, 6 families, 14 genera
and 19 taxa (table 1; electronic supplementary material, tables S4 and S5). Seventy-nine per cent of the
taxa tested had individuals positive for Bd (table 1; electronic supplementary material, tables S4 and S5).
The study does not provide an inventory of infection for the area as it only covered one ecosystem and
complete detection of both species and infection is problematic [60]. Total prevalence in the sample was
11% (95% CL; CB 7–19), 22% (95% CL; CB 15–31) if single positives were included and 27% (95% CL; CB
19–36) including weak positives. As in other WG studies, all GE values recovered were low and all those
with a single GE value greater than 0.1 were included in the analysis (table 1; electronic supplementary
material, tables S4 and S5 [79,61]).
All four species of caecilian found in the study were infected (table 1; electronic supplementary
material, tables S4 and S5). The critically endangered Amboli toad, Xanthophryne tigerina, was infected
with low prevalence (6.7%; 95% CL; CB 1–32) as were 33% of the endangered frog Fejervarya cf.
sahyadris in the sample (95% CL; CB 13–65) [51]. One site, Amboli High, returned no positives out
of six Xanthophryne tigerina samples. Amboli High was the only site without any positive results. No
amphibians were detected with external signs of chytridiomycosis.
5.2. Spatial distribution of Bd infection
Site prevalence varied between 0 and 50% and species infection rate was 0–60% (table 1;electronic
supplementary material, table S4). Macroscale variations in GE values were found with the regions
exhibiting a significant 10-fold difference in mean GE (ANOVA, F1,2 =3.99, p=0.06) (electronic
supplementary material, table S2; figure 2a,b). The Low Region had more infected individuals (56%;
95% CL; CB 26–62) than the High Region (44%; 95% CL; CB 37–56). Individual GE value increased with
elevation (ANOVA, F11,20 =4.85, p<0.01).
5.3. Environmental relationships with Bd infection
As both water temperature and pH covaried with elevation, and pH with water temperature,
elevation alone was used to explore spatial relationships (electronic supplementary material, table S1).
Temperature in the Low Region had a notable maximum of 36.4°C (mean 30.9°C), much higher than
above the escarpment at 28.3°C (mean 22.5°C; minimum 19.3°C) (table 2). Both regions had minimum
pH values below the Bd optimum although mean values were within the pathogen’s tolerance range
(table 2).
GLM ANOVA analysis was used to assess the factors regulating the distribution of infection intensity
(figure 3a–e). Plateau elevation had the greatest impact showing an upward trend with elevation
(figure 3b). Land-use was the second most crucial factor: agriculture had a negative impact on sites below
the escarpment, and above the escarpment the type of land-use did not have a clear impact (figure 3c).
The intensity of disturbance was related to an increasing trend in infection intensity (figure 3d). Latitude,
which includes Low and High Region sites in each class, suggests a limited decreasing trend with
increasing latitude (figure 3e).
6
rsos.royalsocietypublishing.org R. Soc. open sci. 5: 180211
................................................
proportional infection
log GE X15
Western Ghats
01020 40km
proportional infection
Low: mean site GE
High: mean site GE
Western Ghats
01020 40km
(a)(b)
Figure 2. (a) The proportional dierence in regional values of mean site GE values. (b) The individual site mean GE.
Table 1. Taxonomy, risk and infection as prevalence. Where nomenclature is uncertain the rules of the International Code of Zoological
Nomenclature (ICZN) have been followed. Where identication is hampered by cryptic species a most likely identity is shown with the
prex ‘cf’. IUCN threat status and known habitat associations accessed 10/02/2017 [51]. NA, not assessed; DD, Data Decient; LC, Least
Concern; EN, Endangered; CR, Critically Endangered. Prevalence is the percentage of the sample tested positive for Bd.
order family taxa IUCN Nprevalence (%) CB (%)
Anura Bufonidae Duttaphrynus melanostictus LC 7 43 10–82
.........................................................................................................................................................................................................................
Anura Bufonidae Xanthophryne tigerina CR 15 6.7 1–32
.........................................................................................................................................................................................................................
Anura Dicroglossidae Euphlyctis cf. cyanophlyctis LC 2 0 0
.........................................................................................................................................................................................................................
Anura Dicroglossidae Fejervar ya cf. brevipalmata DD 9 11 0.003–0.48
.........................................................................................................................................................................................................................
Anura Dicroglossidae Fejervar ya cf. caperata DD 4 75 19–99
.........................................................................................................................................................................................................................
Anura Dicroglossidae Fejervar ya cf. cep NA 7 14 0.01–58
.........................................................................................................................................................................................................................
Anura Dicroglossidae Fejervar ya cf. sahyadris EN 14 36 13–65
.........................................................................................................................................................................................................................
Anura Dicroglossidae Fejervar ya sp. 10 33 7–65
.........................................................................................................................................................................................................................
Anura Dicroglossidae Hoplobatrachus tigerinus LC 9 56 21–86
.........................................................................................................................................................................................................................
Anura Dicroglossidae Sphaerotheca dobsonii LC 5 20 1–72
.........................................................................................................................................................................................................................
Anura Micorhylidae Microhyla ornata LC 1 0 0
.........................................................................................................................................................................................................................
Anura Micorhylidae Uperodon globulosus LC 1 0 0
.........................................................................................................................................................................................................................
Anura Ranixalidae Indirana cf. chiravesi LC 3 33 1–91
.........................................................................................................................................................................................................................
Anura Rhacophoridae Pseudophilautus sp. 1 0 0
.........................................................................................................................................................................................................................
Anura Rhacophoridae Raorchestes ghatei NA 5 60 15–95
.........................................................................................................................................................................................................................
Gymnophiona Indotyphlidae Gegeneophis cf.ramaswamii LC 5 20 1–72
.........................................................................................................................................................................................................................
Gymnophiona Indotyphlidae Gegeneophis seshachari DD 9 44 14–79
.........................................................................................................................................................................................................................
Gymnophiona Indotyphlidae Indotyphlus cf. battersbyi DD 2 50 1–99
.........................................................................................................................................................................................................................
Gymnophiona Indotyphlidae Indotyphlus maharashtraensis DD 3 33 1–91
.........................................................................................................................................................................................................................
7
rsos.royalsocietypublishing.org R. Soc. open sci. 5: 180211
................................................
log10 individuals GE
highmedlow
1.5
1.0
0.5
0
–0.5
–1.0
1.5
1.0
0.5
0
–0.5
–1.0
disturbance intensity
NorthCentralSouth
latitudinal groups
(e)
(d)
HighLow
25
20
15
10
5
0
log10 individuals GE
region
(a)
*
*
log10 individuals GE
1000–1200900–1000800–900100–2000–100
1.5
1.0
0.5
0
–0.5
–1.0
elevation groups, m.a.s.l.
1.5
1.0
0.5
0
–0.5
–1.0
light windfarm tourist tour/agr agriculture light/ag
r
land-use
(b)(c)
*
*
*
**
Figure 3. Log10 transformed GE data for individuals. Quartile 2 and 3 are shaded with the dividing line as the median. The whiskers
indicate quartiles 1 and 4. Outliers are indicated by asterisks. (a) Regions (above, High, and below, Low, the Western Ghats escarpment).
GLM ANOVA results for the other classes: (b) elevation groups, F=12.77, d.f.factor =1, d.f.error =24, p<0.01; (c)land-use,F=10.88,
d.f.factor =1, d.f.error =24, p<0.01; (d) disturbance intensity, F=2.99, d.f.factor =4, d.f.error =24, p<0.05; (e) latitudinal groups,
F=3.33, d.f.factor =1, d.f.error =24, p=0.08.
Table 2. Physio- chemical parameters described for the sur vey area as a whole and the two regions. Temperature =water temperature
in °C.
variable Region mean minimum maximum
temperature Low 30.9 26.2 36.4
.........................................................................................................................................................................................................................
temperature High 22.5 19.3 28.3
.........................................................................................................................................................................................................................
temperature all 24.8 19.3 36.4
.........................................................................................................................................................................................................................
pH Low 6.7 5.0 9.6
.........................................................................................................................................................................................................................
pH High 7.6 5.3 12.2
.........................................................................................................................................................................................................................
pH all 7.3 5.0 12.2
.........................................................................................................................................................................................................................
6. Discussion
There was widespread but low intensity infection of Bd on almost all the plateaus sampled except for one,
Amboli High, and in 79% of the amphibian species examined on the rocky plateaus in the northern WG
8
rsos.royalsocietypublishing.org R. Soc. open sci. 5: 180211
................................................
(table 1; electronic supplementary material, tables S3 and S4). These are the first records of infection in
the critically endangered Amboli toad, Xanthophryne tigerina; the endangered frog Fejervarya cf. sahyadris;
and four species of caecilian, Gegeneophis cf. ramaswamii, Gegeneophis seshachari, Indotyphlus cf. battersbyi
and Indotyphlus maharashtraensis [62]. Three of the caecilian species are described by the IUCN as Data
Deficient (table 1). Infection was detected in two species yet to be assessed by the IUCN, Fejervarya
cf. cepfi and Raorchestes cf. ghatei; and two other Data Deficient species, Fejervarya cf. brevipalmata and
Fejervarya cf. caperata (table 1). This is the first study to investigate Bd infection in low lying coastal sites,
where there was higher prevalence but lower intensity infection than on sites above the WG escarpment
(electronic supplementary material, tables S2 and S3; figure 3a). Site elevation, with its covariables, and
disturbance intensity were the most significant explanatory factors in the pattern of Bd distribution
(electronic supplementary material, tables S2 and S3; figure 3b,c). However, another explanation, not
explored here, for the observed pattern in Bd distribution is that the amphibian populations are relics of
ancient dispersals isolated from the pathogen’s transmission vectors [63].
6.1. Low elevation plateaus are less conducive to Bd but with greater connectivity
Puschendorf et al.[54] suggest that disease-free amphibian refuges are created in drier areas with
temperatures above those tolerated by Bd [54]. We suggest our findings, with lower infection intensities
on the Konkan plateaus, support them as a possible refugia for some amphibian species from Bd.
However, the higher prevalence on plateaus below the escarpment is more difficult to explain. The
plateaus’ specific environment derived from their open habitat may have created thermal refugia from
Bd in rock pools and surrounding habitats where temperatures exceed the pathogen’s upper thermal
tolerance, but it should also restrict transmission. The pools are scattered across plateaus with surface
temperatures, especially on the exposed rock, greatly more than the pathogen’s thermal maximum,
which should restrict the pathogen’s persistence and transmission [23,64].
Low Region water temperatures were higher than those above the escarpment, on average 30.9°C,
with a maximum of 36.4°C, a figure well above published critical zoospore thermal thresholds of 23–
28°C (tables 1and 2;figure 3a; electronic supplementary material, table S2 and S3) [2,10,50,65]. Even more
lethal are the rock surface temperatures which can exceed 50°C [23]. The region is also drier, with less rain
and fewer wet days than above the escarpment. The annual rainfall falls within the pathogen’s preferred
rainfall range of 1500–2500 mm but it only rains for five months a year, with the remaining seven months
being almost completely dry with very low relative humidity [10,23,65,66]. Infection intensity decreased
slightly with increasing latitude possibly reflecting the latitudinal decline in the number of wet days
(figure 3e)[56,57,66].
Regional differences in habitat and micro-habitat availability may also help explain the pattern in
Bd distribution, through behavioural mitigation where amphibians move to, or persist on, plateaus
with micro-habitats that are refugia from Bd [55,57,67]. Conversely, stream micro-habitats offer one
possible transmission route in the Low Region, where streams are more frequent [55]. Sub-tropical
stream-breeders are more susceptible to Bd and may be disease vectors with the pathogen spreading
from streams into the terrestrial realm [67,68]. Increased landscape connectivity in the Low Region,
resulting from lower inter-site variation in elevation (Low Region 103m, High Region 370 m), may enable
greater inter-site transmission through amphibians dispersing between plateaus, explaining the higher
prevalence and supporting the findings of Heard et al. [69] (electronic supplementary material, table S2
and S3) [53,70]. The picture is complex though as some refugia such as woody plants and large loose rocks
may enable behavioural avoidance of excessive temperatures for both amphibians and Bd [51,69,71]. This
idea possibly supported by the results for the four species of caecilian in the study which have similar
prevalence to non-fossorial taxa (table 1; electronic supplementary material, tables S4 and S5). They are
frequently found under loose rocks where temperatures are tolerable for Bd and are close to streams
which may be used by stream-breeding anuran vectors [55,67].
6.2. Bd in the High Region
Despite the High Region offering a more equitable temperature range for Bd with a mean of 22.5°C,
within the pathogen’s in vitro optimum of 17–25°C, prevalence was less than below the escarpment where
the pathogen’s upper limit was often exceeded. This suggests the High Region’s greater topographical
heterogeneity produces barriers to transmission which may explain the lower number of infected
individuals (tables 1and 2; electronic supplementary material, tables S2–S4; [10,50,51]).
9
rsos.royalsocietypublishing.org R. Soc. open sci. 5: 180211
................................................
Individual GE loadings were greater above the escarpment reflecting the High Region’s optimal
temperature (table 2 and electronic supplementary material, table S2; [10,51]). While excessive
temperatures below the escarpment may regulate the pathogen through mortality the High Region’s
lower temperature regime may encourage Bd, even when the temperature falls below the organism’s
lower optimum value (17°C). A temperature of 4°C was used by Voyles et al.[57] as their minimum in
a study assessing the impact of temperature regimes on Bd life history; the same minimum temperature
was also recorded by Watve [23] on High Region plateaus. Their lower temperature regime resulted
in extended zoospore longevity meaning zoospore numbers in water bodies could be expected to be
greater than in warmer pools. The trait may lead to greater encounter rates and thus infection prevalence
contrary to our findings [57]. However, they also found their low temperature regime increased zoospore
production, which offers a plausible explanation for the elevated site GE values in the High Region.
6.3. The impact of anthropogenic disturbance on Bd distribution
Elevated prevalence close to human settlement is to be expected but with unknown causes [72]. The study
found that Low Region plateaus, which are less isolated from human settlement, had higher prevalence
than their more isolated High Region counterparts [72].
In addition to proximity of human habitation, changes in land-use influences amphibian distribution,
and possibly their susceptibility and exposure to disease [55,73,74]. Sites near human habitation are likely
to have anthropogenic land-uses. We found land-uses differed either side of the escarpment. Land-use
had an impact on mean individual infection intensity with Low Region agricultural sites having higher
infection intensity than the nearest sites with limited disturbance (figure 3c). Land-use in the High Region
had a negligible impact on mean individual infection levels (figure 3c). Sites with little disturbance,
on our arbitrary scale, had lower mean individual GE compared to plateaus with higher disturbance
(figure 3d). The actual mechanisms remain unclear, but we can support anthropogenic disturbance as a
negative factor in Bd infection. The sites disturbed by tourism had amphibian assemblages dominated
by generalist species, but this had no impact on mean individual infection intensity suggesting mobile
species may not be pathogen vectors [55].
The impact of disturbance on Bd infection intensity was less than that of elevation (figure 3b–d).
Site prevalence did not reflect land-use (electronic supplementary material, table S3; figure 3b–e). As
all the sites with tourism were above the escarpment and elevation had the greater explanatory power,
we believe spatially driven climate has more effect than land-use. There is a clearer indication that
agriculture negatively impacts infection intensity as seen in our Low Region sites, where there is little
inter-site variation in elevation but a significant difference in infection intensity (figure 3c).
7. Conclusion
It is clear that the Bd pathogen is very widely distributed in this area and anthropogenic land-use
increases the infection risk. The infected plateau amphibians include several threatened and poorly
understood species whose infection we record for the first time. None of the individuals that tested
positive for Bd showed any external signs of chytridiomycosis. The disease has been reported in
Nyctibatrachus humayuni from sites close to the northern edge of this survey [9]. The infection level
reported here is well below the mortality threshold of 1–10000 zoospores [75] and is more indicative
of an historical infection, or species that are carriers that do not go on to develop chytridiomycosis [76
78]. The triggers for this low intensity infection to develop into a lethal outbreak of chytridiomycosis are
unknown.
Transmission vectors are poorly understood globally as well as in the WG, but we would support the
possible explanation of water birds as vectors with lapwing species (Vanellus indicus) being frequently
observed on all the plateaus [79]. Proximity to human habitation is a risk factor but the mechanisms of
transmission are unknown.
Until there is a better understanding of the mechanisms triggering benign Bd infection to become
lethal chytridiomycosis, its presence should be considered in all future conservation policy decisions.
Preservation of dispersed populations on sites with refugial properties, good connectivity and
preservation of refugia on individual plateaus is essential in offering the best prospect of long-term
species persistence [69,80]. The need for further work on modelling infection on a wider scale, especially
in the low lying coastal areas, characterized here for the first time for Bd, is a priority. A study into
the evolutionary history of Bd in the entire WG area would also help with its management. There is
an urgency to determine the routes of transmission and triggers for the pathogen to become lethal.
10
rsos.royalsocietypublishing.org R. Soc. open sci. 5: 180211
................................................
That urgency is illustrated by the 2015 publication of the addition of Duttaphrynus melanostictus to
Hoplobatrachus tigerinus as invasive species in another biodiversity hotspot, Madagascar, [81]. Both of
these species had high Bd prevalence in this study, 43% and 56% respectively. Resolution of these
questions may be helped by a better understanding of the historical lineage of the Bd strain in the WG.
Ethics. Advice was sought from the University of Plymouth Animal Welfare and Ethics Committee representative who
advised that no formal consent was required since the swabs were non-invasive, collected from external swabbing
only. Further they advised following strict international handling protocols and these are described under Methods.
Sampling was undertaken by kind permission of the National Biodiversity Authority, Chennai, India under permit
number: Maharashtra 2014 MC200621.
Data accessibility. The raw data of infection intensity with species and site localities are available in the electronic
supplementary material.
Authors’ contributions. C.J.T. designed and coordinated the study, obtained permits, collected field data, processed
samples in the laboratory, executed the statistical analysis and drafted and submitted the manuscript. T.R.L. assisted
by L.D. and D.P. collected field data, T.R.L. helped edit the manuscript. M.C.F. and C.J.W. carried out the molecular
analysis and refined the manuscript. S.K. participated in the data collection and fieldwork logistics. A.W. helped with
the permit and logistics and assisted with fieldwork. M.E.K. supervised the project, assisted in some of the fieldwork,
and helped to refine the manuscript. All authors gave final approval for publication.
Competing interests. We have no competing interests.
Funding. C.J.T.: The Royal Geographical Society with IBG through Geographical Fieldwork Grants in 2013 and 2014
and the Monica Cole Award 2012. C.J.T.: The Erasmus Darwin Barlow Expedition Fund, Zoological Society of
London grant in 2014. T.R.L.: Percy Sladen Memorial Trust award in 2014. M.C.F.: The Leverhulme Trust grant no.
RPG-2014-273.
Acknowledgements. We thank Dr Neelesh Dahanukar and an anonymous reviewer for their help in refining the
manuscript. Many people have helped to bring the project to fruition: Dr Aparna Watve, Sanjay Thakur and Dr Varad
Giri for their tireless support; Dr Hemant Ghate and Dr Anand Padhye helped with laboratory space and resolving
identification; David Gower aided caecilian identification; Dr N. Dahanukar for freezer space to preserve the swabs;
Nikhil Gaitonde for his field assistance; Dr Ramana Athreya kindly provided bench space to A.W. and C.J.T.; Jennifer
Shelton and Pria Ghosh for DNA extraction; and Felicity Wynne for help in interpretation. Dr Robert Puschendorf
gave invaluable help in many stages of the study.
References
1. Longcore JE, Pessier AP, Nichols DK. 1999
Batrachochytrium dendrobatidis gen. et sp.nov.,
a chytrid pathogenic to amphibians. Mycologia91,
219–227. (doi:10.2307/3761366)
2. Olson DH, Aanensen DM, Ronnenberg KL, PowellCI,
WalkerSF,BielbyJ,GarnerTWJ,WeaverG,Fisher
MC, The Bd Mapping Group. 2013 Mapping the
global emergence of Batrachochytrium
dendrobatidis, the amphibian chytrid fungus.
PLoS ONE 8, e56802. (doi:10.1371/journal.pone.
0056802)
3. FarrerRA et al. 2011 Multiple emergences of
genetically diverse amphibian-infecting chytrids
include a globalized hypervirulent recombinant
lineage. Proc. Natl Acad.Sci. USA 108, 18 732–18 736.
(doi:10.1073/pnas.1111915108)
4. FisherMC, Garner TW, Walker SF. 2009 Global
emergence of Batrachochytriumdendrobatidis and
amphibian chytridiomycosis in space, time,and
host. Annu.Rev.Microbiol.63,291310.(doi:10.1146/
annurev.micro.091208.073435)
5. Rödder D etal. 2009 Global amphibian extinction
risk assessment for the panzootic chytrid fungus.
Diversity 1, 52–66. (doi:10.3390/d1010052)
6. MyersN, Mittermeier RA, Mittermeier CG, da
Fonseca GAB, Kent J. 2000 Biodiversity hotspots
for conservation priorities. Nature 403, 853–858.
(doi:10.1038/35002501)
7. NairAS,DanielO,GopalanSV,GeorgeS,KumarKS,
Merila J, TeacherAGF. 2011 Infectious disease
screening of Indirana frogs from the WesternGhats
biodiversity hotspot. Herpetol. Rev.42, 554–557.
8. MolurS, Krutha K, Paingankar MS, Dahanukar N.
2015AsianstrainofBatrachochytriumdendrobatidis
is widespread in the WesternGhats, India. Dis.
Aquat. Organ. 112, 251–255. (doi:10.3354/dao02804)
9. DahanukarN, Krutha K, Paingankar MS, Padhye AD,
Modak N, Molur S. 2013 Endemic Asian chytrid strain
infection in threatened and endemic anurans of the
northern Western Ghats, India. PLoSONE 8,e77528.
(doi:10.1371/journal.pone.0077528)
10. Ron SR. 2005 Predicting the distribution of the
amphibian pathogen Batrachochytrium
dendrobatidis in the New World.Biotropica 37,
209–221. (doi:10.1111/j.1744-7429.2005.
00028.x)
11. Aravind NA, Gururaja KV. 2011 Theme paper on the
amphibians of the Western Ghats.Repor t
submitted to WesternGhats Ecology Expert Panel.
Available at: MoEF Electronic database,see http://
www.westernghatsindiaorg/sites/default/les/
Amphibians.
12. Giri V. 2016 Diversity and conservation status of the
Western Ghats amphibians.In Threatened
amphibians of the world (eds SN Stuart, M Homan,
JS Chanson, NA Cox, R Berridge, P Ramani,
BE Young),pp. 80–82. Barcelona, Spain: Lynx
Ediciones.
13. IPCC. 2014 International Panel on Climate Change,
Chapter 24: Asia 2014. See http://www.ipcc.ch/pdf/
assessment-report/ar5/wg2/WGIIAR5- Chap24.
14. Cincotta RP, Wisnewski J, Engelman R. 2000 Human
population in the biodiversity hotspots. Nature 404,
990–992. (doi:10.1038/35010105)
15. Thorpe C, Watve A. 2016 Lateritic plateaus in the
Northern Western Ghats, India; a review of bauxite
mining restoration practices. J. Ecol. Soc. 28,
25–44.
16. Watve A. 2013 Status reviewof rocky plateaus in the
northernWesternGhatsandKonkanregionof
Maharashtra, India with recommendations for
conservation and management. J. Threat.Taxa 5,
3935–3962. (doi:10.11609/JoTT.o3372.3935-62)
17. Kasturirangan K et al. 2013 Report of the higher level
working group on WesternGhats. Ministr y of
Environment and Forests,Government of India.
18. Bharucha EK. 2010 Current ecologicalstatus and
identication of potential ecologicallysensitive areas
in the Northern Western Ghats. Pune, Maharashtra:
Bharti Vidyapeeth Deemed University, Research
IoEEa.
19. Whittaker K, VredenburgV. 2011 An overview of
chytridiomycosis. Availablefrom: http://www.
amphibiaweb.org/chytrid/chytridiomycosis.html.
20. Porembski S, Silveira FAO, FieldlerPL, Watve A,
Rabarimanarivo M, Kouame F, Hopper SD. 2016
Worldwide destruction of inselbergs and related
rock outcrops threatensa unique ecosystem.
Biodiversity Conserv. 25,2827–2830.
(doi:10.1007/s10531-016-1171-1)
21. Sloan S, Jenkins CN, Joppa LN, Gaveau DLA,
Laurance WF. 2014 Remaining natural vegetation in
the global biodiversity hotspots. Biol. Conserv.177,
12–24. (doi:10.1016/j.biocon.2014.05.027)
22. Widdowson M, CoxK. 1996 Uplift and erosional
history of the Deccan Traps, India: evidence from
11
rsos.royalsocietypublishing.org R. Soc. open sci. 5: 180211
................................................
laterites and drainage patterns of the Western
Ghats and Konkan Coast. Earth Planet. Sci. Lett.137,
57–69. (doi:10.1016/0012-821X(95)00211-T)
23. WatveA. 2010 Rocky plateaus (special focus on the
Western Ghats and Konkan). Report to ‘ Western
Ghats Ecology Expert Panel. Pune,India: BIOME
Conservation Foundation.
24. Laurance WF, McDonald KR, Speare R. 1996
Epidemic disease and the catastrophic decline of
Australian rain forest frogs. Conserv. Bio l. 10,
406–413. (doi:10.1046/j.1523-1739.1996.1002
0406.x)
25. Crump ML, Scott NJ. 1994 Visual encountersur veys.
In Measuring and monitoring biological diversity:
standard methods for amphibians (eds WR Heyer,
MADonnelly,RWMcDiarmid,LCHayek,MSFoster),
pp. 84–92. Washington,DC: Smithsonian
Institution Press.
26. Vonesh JR, Mitchell JC, Howell K, Crawford AJ. 2010
Rapid assessments of amphibian diversity. In
Amphibian ecology and conservation: a handbook of
techniques (ed CK Jnr Dodd), pp. 263–280. Oxford,
UK: Oxford University Press.
27. Bhatta G. 1998 A eld guide to the caecilians of the
Western Ghats,India. J. Biosci. 23,73–85.
(doi:10.1007/BF02728526)
28. Dubois A, Ohler A-M, Biju SD. 2001 A new genus and
species of Ranidae (Amphibia, Anura) from
south-western India. Alytes 19,5379.
29. Bossuyt F. 2002 A new species of Philautus (Anura:
Ranidae) from the Western Ghatsof India. J.
Herpetol. 36,656–661.(doi:10.1670/0022-1511
(2002)036[0656:ANSOPA]2.0.CO;2)
30. Biju SD, Bossuyt F. 2009 Pseudophilautus amboli
(Biju & Bossuyt, 2009) IUCN Red List 2009. See
http://www.iucnredlist.org/details/58910/0.
31. Biju SD, Bossuyt F. 2009 Systematics and phylogeny
of Philautus gistel, 1848 (Anura, Rhacophoridae) in
the Western Ghats of India, with descriptions of 12
new species. Zool.J.Linn.Soc.155,374–444.
(doi:10.1111/j.1096-3642.2008.00466.x)
32. Biju SD, Van Bocxlaer I, Giri V, Loader S, Bossuyt F.
2009 Twonew endemic genera and a new species
of toad (Anura: Bufonidae) from the WesternGhats
of India. BMC Res. Notes 2,241.(doi:10.1186/1756-
0500-2-241)
33. Daniel J. 2002 The book of Indian reptiles and
amphibians. Oxford, UK: Bombay Natural History
Society and Oxford University Press.
34. Giri V, Wilkinson M, Gower D. 2003 A new species of
Gegeneophis Peters (Amphibia: Gymnophiona:
Caeciliidae) from the WesternGhats of southern
Maharashtra, India, with a key to the species of the
genus. Zootaxa 351,1–10.(doi:10.11646/zootaxa.
351.1.1)
35. Giri V, Gower DJ, WilkinsonM. 2004 A new species
of Indotyphlus Taylor (Amphibia:Gymnophiona:
Caeciliidae) from the WesternGhats, India. Zootaxa
739,119.
36. Kuramoto M, Joshy SH. 2003 Two new species of the
genus Philautus (Anura: Rhacophoridae) from the
Western Ghats,southwestern India. Cur r. H erpetol.
22, 51–60. (doi:10.5358/hsj.22.51)
37. Kuramoto M, Joshy SH, KurabayashiA, Sumida M.
2007 The genus Fejervarya (Anura: Ranidae) in
central WesternGhats, India, with descriptions of
four new cryptic species. Curr. Herp etol. 26, 81–105.
(doi:10.3105/1881-1019(2007)26[81:TGFARI]2.
0.CO;2)
38. Dinesh K, Radhakrishnan C, Gururaja K, Bhatta G.
2009 An annotated checklist of amphibian of India
with some insights into the patterns of species
discoveries, distribution and endemism. Recordsof
the Zoological Survey of India, Miscellaneous
publication ; occasional paper no 302.
39. Dinesh K, Radhakrishnan C, Channakeshavamurthy
B, Kulkarni NU. 2015 Checklist of amphibians of
India. See http://mhadeiresearchcenter.org/
wpcontent/uploads/2014/01/2017_April_Checklist-
of-Amphibians- of-India.pdf.
40. Frost DR. 2017 Amphibian species of the world: an
online reference. Version6 Electronic database.
See http://research.amnh.org/vz/herpetology/
amphibia/content/search?taxon&subtree&sub.
41. Padhye A, Sayyed A, Jadhav A, Dahanukar N. 2013
Raorchestes gha tei, a new species of shrub frog
(Anura: Rhacophoridae) from the WesternGhats of
Maharashtra, India. J. Threat.Taxa 5, 4913–4931.
(doi:10.11609/JoTT.o3702.4913-31)
42. Dinesh KP, Vijaykumar SP, Channakeshavamurthy
BH, TorsekarVR, Kulkarni NU, Shanker K. 2015
Systematic status of Fejervarya (Amphibia, Anura,
Dicroglossidae) from South and SE Asia with the
description of a new species from the Western
GhatsofPeninsularIndia.Zootaxa 3999,16.
(doi:10.11646/zootaxa.3999.1.5)
43. Garg S, Biju S. 2017 Description of four new species
of burrowing frogs in the Fejervarya ruf escens
complex (Dicroglossidae) with a notes on
morphological anities of Fejervarya species
in Western Ghats. Zootaxa 4277, 451–490.
(doi:10.11646/zootaxa.4277.4.1)
44. Garg S, Biju SD. 2016 Molecular and morphological
study of leaping frogs (Anura, Ranixalidae) with
description of two new species. PLoS ONE 11,
e0166326. (doi:10.1371/journal.pone.0166326)
45. Dahanukar N, Modak N, Krutha K, Nameer P,
Padhye AD, Molur S. 2016 Leapingfrogs (Anura:
Ranixalidae) of the Western Ghats of India: an
integrated taxonomic review. J. Threat. Taxa 8,
9221–9288. (doi:10.11609/jott.2532.8.10.
9221-9288)
46. Hyatt AD et al. 2007 Diagnostic assays and sampling
protocols for the detection of Batrachochytrium
dendrobatidis.Dis. Aquat.Organ. 73, 175–192.
(doi:10.3354/dao073175)
47. Brem F, Mendelson III JR, Lips KR. 2007
Field-sampling protocol for Batrachochytrium
dendrobatidis from living amphibians, using alcohol
preserved swabs. Arlington, VA:Conser vation
International. See http://www.amphibians.org.
48. Vredenburg V, Briggs C. 2009. Chytrid swabbing
protocol. Amphibia Web. See https://amphibiaweb.
org/chytrid/swab_protocol.html.
49. Boyle AHD, Boyle D, Olsen V, Morgan J, Hyatt A.
2004 Rapid quantitative detection of
chytridiomycosis (Batrachochytriumdendrobatidis)
in amphibian samples using real-time TaqmanPCR
assay. Dis.Aquat. Organ. 60, 141–148. (doi:10.3354/
dao060141)
50. Piotrowski JS, Annis SL, Longcore JE. 2004
Physiology of Batrachochytrium dendrobatidis,a
chytrid pathogen of amphibians. Mycologia96,
9–15. (doi:10.1080/15572536.2005.11832990)
51. Pounds AJ et al. 2006 Widespread amphibian
extinctions from epidemic disease driven by global
warming. Nature 439, 161–167. (doi:10.1038/nature
04246)
52. Berger L et al.2004 Eect of season and
temperature on mortality in amphibians due to
chytridiomycosis. Aust.Vet.J.82,434–439.
(doi:10.1111/j.1751-0813.2004.tb11137.x)
53. Ghalambor CK, Huey RB, Martin PR, Tewksbury JJ,
Wang G. 2006 Are mountain passes higher in the
tropics? Janzen’s hypothesis revisited. Integr. Comp.
Biol. 46, 5–17. (doi:10.1093/icb/icj003)
54. Puschendorf R, Hoskin CJ, Cashins SD, McDonald K,
Skerratt LF, Vanderwal J, AlfordR A. 2011
Environmental refuge from disease-driven
amphibian extinction. Conse rv. Biol. 25, 956–964.
(doi:10.1111/j.1523-1739.
2011.01728.x)
55. Thorpe CJ, Lewis TR, Kulkarni S, Watve A, Gaitonde
N, Pryce D, Davies L, Bilton DT, Knight ME. 2018
Micro-habitat distribution drives patch quality for
sub-tropical rocky plateau amphibians in the
northern Western Ghats, India. PLoSONE 13,
e0194810. (10.1371/journal.pone.0194810)
56. Puschendorf R, Carnaval AC, VanDerWal J,
Zumbado-UlateH,ChavesG,BolañosF,AlfordRA.
2009 Distribution models for the amphibian chytrid
Batrachochytrium dendrobatidis in CostaR ica:
proposing climatic refuges as a conservation tool.
Divers. Distrib.15, 401–408. (doi:10.1111/j.1472-4642.
2008.00548.x)
57. Voyles J, Johnson LR, Briggs CJ, Cashins SD, Alford
RA, Berger L, Skerratt LF, Speare R, Rosenblum EB.
2012 Temperaturealters reproductive life history
patterns in Batrachochytrium dendrobatidis,alethal
pathogen associated with the global loss of
amphibians. Ecol. Evol. 2,2241–2249.(doi:10.1002/
ece3.334)
58. Vogt WP, Johnson RB. 2011 Dictionary of statistics &
methodology: a nontechnical guide for the social
sciences. Thousand Oaks, CA: Sage Publications.
59. Maestri R, Monteiro LR, Fornel R, de Freitas TRO,
Patterson BD. 2018 Geometric morphometrics meets
metacommunity ecology: environment and lineage
distribution aects spatial variation in shape.
Ecography 41, 90–100. (doi:10.1111/ecog.03001)
60. Guimarães M, Doherty Jr PF, Munguía-Steyer R.
2014 Strengthening population inference in
herpetofaunal studies by addressing detection
probability. S.Am.J.Herpetol.9,1–8.
(doi:10.2994/SAJH-D-13-00020.1)
61. Clare F, Daniel O, Garner T, Fisher M. 2016 Assessing
the ability of swab data to determine the true
burden of infection for the amphibian pathogen
Batrachochytrium dendrobatidis.Ecohealth13,
360–367. (doi:10.1007/s10393-016-1114-z)
62. IUCN. 2016 The IUCN Red List of Threatened Species
2016-2. See http://www.iucnredlist.org/search.
63. Weinstein SB. 2009 An aquatic disease on a
terrestrial salamander: individual and population
level eects of the amphibian chytrid fungus,
Batrachochytrium dendrobatidis,onBatrachoseps
attenuatus (Plethodontidae). Copeia2009,
653–660. (doi:10.1643/CH-08-180)
64. Retallick RW, McCallum H, Speare R. 2004 Endemic
infection of the amphibian chytrid fungus in a frog
community post-decline. PLoS Biol. 2,e351.
(doi:10.1371/journal.pbio.0020351)
65. India Go. Indiastat, Meteorogical data, rainfall 2017
See http://www.indiastat.com/
meteorologicaldata/22/rainfall/238/stats.aspx.
66. IMD, India Meteorological Department. 2016 Onset
and withdrawal of southwest monsoon 2016:
12
rsos.royalsocietypublishing.org R. Soc. open sci. 5: 180211
................................................
Ministry of Earth Sciences, Government of India;
See http://www.imd.gov.in/pages/monsoon_
main.php.
67. Lips KR et al. 2006 Emerging infectious disease and
the loss of biodiversity in a Neotropical amphibian
community. Proc.Natl Acad. Sci. USA 103,
3165–3170. (doi:10.1073/pnas.0506889103)
68. Scherer RD, Muths E, Noon BR, Corn PS. 2005 An
evaluation of weather and disease as causes of
decline in two populations of boreal toads.
Ecol.Appl. 15, 2150–2160. (doi:10.1890/
05-0431)
69. Heard GW, Thomas CD, Hodgson JA, Scroggie MP,
Ramsey DS, Clemann N. 2015 Refugia and
connectivity sustain amphibian metapopulations
aictedbydisease.Ecol. Lett. 18, 853–863.
(doi:10.1111/ele.12463)
70. JanzenDH.1967Whymountainpassesarehigherin
the tropics. Am. Nat.101, 233–249. (doi:10.1086/
282487)
71. ScheersBR,EdwardsDP,DiesmosA,WilliamsSE,
Evans TA.2014 Microhabitats reduce animal’s
exposure to cl imate extremes. Glob. Change Biol. 20,
495–503. (doi:10.1111/gcb.12439)
72. Bosch J, Donaire D, El Mouden EH,
Fernández-Beaskoetxea S, FisherMC, Slimani T.
2011 First record of the chytrid fungus
Batrachochytrium dendrobatidis in North Africa.
Herpetol. Rev.42,71–75.
73. Cortés-Gómez AM, Castro-Herrera F,
Urbina-Cardona JN. 2013 Small changes in
vegetation structure create greatchanges in
amphibian ensembles in the Colombian Pacic
rainforest. Trop.Conserv. Sci. 6,749–769.
(doi:10.1177/194008291300600604)
74. N ewbol d T etal. 2014 A global model of the
response of tropical and sub-tropical forest
biodiversity to anthropogenic pressures.Proc. R.
Soc. B 281,20141371.(doi:10.1098/rspb.2014.
1371)
75. VredenburgV T, Knapp RA, TunstallTS, Briggs CJ.
2010 Dynamics of an emerging disease drive
large-scale amphibian population extinctions. Proc.
NatlAcad.Sci.USA107, 9689–9694. (doi:10.1073/
pnas.0914111107)
76. Daszak P, Cunningham AA, Hyatt AD. 2003
Infectious disease and amphibian population
declines. Divers. Distrib.9, 141–150. (doi:10.1046/
j.1472-4642.2003.00016.x)
77. Padgett-Flohr GE, Hopkins II RL. 2009
Batrachochytrium dendrobatidis, a novelpathogen
approaching endemism in central California. Dis.
Aquat. Organ. 83,19.(doi:10.3354/dao
02003)
78. O uellet M, Mikaelian I, PauliBD, Rodrigue J, Green
DM. 2005 Historical evidence of widespread chytrid
infection in North American amphibian
populations. Conser v.Bi ol. 19, 1431–1440.
(doi:10.1111/j.1523-1739.2005.00108.x)
79. GarmynA,VanRooijP,PasmansF,HellebuyckT,
Van Den Broeck W, HaesebrouckF, Mar tel AN. 2012
Waterfowl: potential environmentalreservoirs of
the chytrid fungus Batrachochytrium dendrobatidis.
PLoS ONE 7, e35038. (doi:10.1371/journal.pone.
0035038)
80. Heard GW, Scroggie MP, Ramsey DSL, Clemann N,
Hodgson JA, Thomas CD. 2017 Can habitat
management mitigate disease impacts on
threatened amphibians? Conserv.Lett. 11,e12375.
(doi:10.1111/conl.12375)
81. Moore M, Fidy JFSN, Edmonds D. 2015 The new toad
in town: distribution of the Asian toad,
Duttaphrynus melanostictus, in the Toamasina area
of eastern Madagascar.Trop. Conserv.Sci. 8,
440–455. (doi:10.1177/194008291500800210)
... Our sampling locations fell into four different land cover categories: forests, croplands, (natural) vegetation and waterbodies. We divided our sampling sites into high and low disturbance areas by following disturbance factors (modified to fit our context) described by Thorpe et al. (2018a). Disturbance factors recorded were: surfaced road, unsurfaced road, surfaced road within 200 m, domesticated animal grazing, tourism, adjacent built structures and agricultural activities. ...
... Only P. leucomystax was previously found in infected frogs from Cambodia (Mendoza et al. 2011) and Singapore (Gilbert et al. 2012), while the other eight species discovered are newly infected hosts. However, E. cyanophlyctis tested for Bd found negative in India (Dahanukar et al. 2013;Thorpe et al. 2018a). Samples for these studies collected from forests (Dahanukar et al. 2013) and streams (Thorpe et al. 2018a) where the infection intensity was low (Thorpe et al. 2018a). ...
... However, E. cyanophlyctis tested for Bd found negative in India (Dahanukar et al. 2013;Thorpe et al. 2018a). Samples for these studies collected from forests (Dahanukar et al. 2013) and streams (Thorpe et al. 2018a) where the infection intensity was low (Thorpe et al. 2018a). Two of our Bdpositive samples of E. cyanophlyctis were collected from forest and waterbodies where the prevalence rate is high. ...
Article
Full-text available
Global amphibian populations are facing a novel threat, chytridiomycosis, caused by the fungus Batrachochytrium dendrobatidis (Bd), which is responsible for the severe decline of a number of species across several continents. Chytridiomycosis in Asia is a relatively recent discovery yet there have been no reports on Bd-presence in Bangladeshi amphibians. We conducted a preliminary study on 133 wild frogs from seven sites in Bangladesh between April and July 2018. Nested PCR analysis showed 20 samples (15.04%) and 50% of the tested taxa (9 species from 6 genera and 4 families) as Bd-positive. Eight of the nine species are discovered as newly infected hosts. Analysis of Bd-positive samples shows prevalence does not significantly vary among different land cover categories, although the occurrence is higher in forested areas. The prevalence rate is similar in high and low disturbed areas, but the range of occurrence is statistically higher in low disturbance areas. Maximum entropy distribution modeling indicates high probabilities of Bd occurrence in hilly and forested areas in southeast and central-north Bangladesh. The Bd-specific ITS1-5.8S-ITS2 ribosomal gene sequence from the Bd-positive samples tested is completely identical. A neighbor-joining phylogenetic tree reveals that the identified strain shares a common ancestry with strains previously discovered in different Asian regions. Our results provide the first evidence of Bd-presence in Bangladeshi amphibians, inferring that diversity is at risk. The effects of environmental and climatic factors along with quantitative PCR analysis are required to determine the infection intensity and susceptibility of amphibians in the country.
... In our study area, four out of six amphibian species have been tested as Bd positive, although in comparison with other regions in Marocco, they have lower infection rate. Lower GE values are probably the result of unfavorable conditions, such as changes in the abiotic environment (Ron, 2005;Thorpe et al., 2018). It has been reported that Bd is temperature sensitive, with optimal growth ranging between 17 and 25 °C (Piotrowski et al., 2004;Pounds et al., 2006), with higher temperature (more than 30 °C) reported as unfavorable for its development (Watve, 2013). ...
... It has been reported that Bd is temperature sensitive, with optimal growth ranging between 17 and 25 °C (Piotrowski et al., 2004;Pounds et al., 2006), with higher temperature (more than 30 °C) reported as unfavorable for its development (Watve, 2013). Previous studies have shown that lower temperature regime resulted in extended zoospore longevity and in such conditions zoospores numbers in water bodies could be expected to be greater than in warmer water (Voyles et al., 2012;Thorpe et al., 2018). The higher temperatures (more than 30 °C) recorded in the study area expected to have a negative impact on the development of this fungal pathogen. ...
... The higher temperatures (more than 30 °C) recorded in the study area expected to have a negative impact on the development of this fungal pathogen. Additionally, optimum rainfall for Bd development has been reported to range between 1500 and 2500 mm/year (Thorpe et al., 2018), which are much higher values of the one observed in the Tensift region. Only, Oukaimden approach these rainfall values, but in general remains below to optimum parameters for the development of Bd. ...
Article
Full-text available
The chytrid fungus Batrachochytrium dendrobatidis (Bd) is a generalist pathogen that affects many amphibian species and responsible of chytridiomycosis, considered as the main causes of species deaths and populations declines worldwide. The chytrid fungal pathogen has been first described in North Africa in 2011 by our research group. The present work reported the first survey on Bd prevalence and intensity in the Tensift region of Morocco. The survey has been conducted on 11 different localities by collecting skin swabs and tissue samples of 97 amphibian individuals. Using quantitative Polymerase Chain Reaction (qPCR) protocols, low-intensity of Bd infection has been detected in the area of study. In fact, the chytrid fungal pathogen have been identified in only 10 individuals distributed in six of 11 sites investigated, placing the 95% confidence interval for overall prevalence at 5.5-19.6%. The survey confirmed the occurrence of Bd at both high and low altitude localities, on four species out of seven known to inhabit the region and added two additional species (Pelophylax saharicus and Sclerophrys mauritanica) to the list of Bd infected amphibians in Morocco. The present records extended Bd distribution more than 400 km in the South of Morocco, indicating that the chytrid fungal pathogen is more widespread in the country than previously thought.
... The arrival of Bd in high altitude areas has been facilitated by human movement that has spread the fungus among isolated water bodies, but also climate change can facilitate such spread modifying the environment that anurans inhabit 63 and further force the severity of infection 35 . In addition to altitude, temperature and precipitation appear to be relevant climatic variables shaping the occurrence of Bd in Chile, as previously reported for other world regions 21,27,36,43,[69][70][71][72][73] . However, other studies have found sometimes different patterns (e.g., 39,41,74 ), suggesting that the mechanisms between these climatic factors and Bd occurrence are complex. ...
... As with prevalence, the same association has been shown with intensity of infection, namely a positive association of Bd loads with anthropogenic disturbance 71 . The highest observed Bd prevalence was in the Chilean Matorral ecoregion, an area considered as a priority for global biodiversity conservation 83 . ...
Article
Full-text available
Amphibian chytridiomycosis, caused by the fungus Batrachochytrium dendrobatidis (Bd), has caused the greatest known loss of biodiversity due to an infectious disease. We used Bd infection data from quantitative real-time PCR (qPCR) assays of amphibian skin swabs collected across Chile during 2008–2018 to model Bd occurrence with the aim to determine bioclimatic and anthropogenic variables associated with Bd infection. Also, we used Bd presence/absence records to identify geographical Bd high-risk areas and compare Bd prevalence and infection loads between amphibian families, ecoregions, and host ecology. Data comprised 4155 Bd-specific qPCR assays from 162 locations across a latitudinal gradient of 3700 km (18º to 51ºS). Results showed a significant clustering of Bd associated with urban centres and anthropogenically highly disturbed ecosystems in central-south Chile. Both Bd prevalence and Bd infection loads were higher in aquatic than terrestrial amphibian species. Our model indicated positive associations of Bd prevalence with altitude, temperature, precipitation and human-modified landscapes. Also, we found that macroscale drivers, such as land use change and climate, shape the occurrence of Bd at the landscape level. Our study provides with new evidence that can improve the effectiveness of strategies to mitigate biodiversity loss due to amphibian chytridiomycosis.
... Moreover, D. melanostictus has been showed to have a high Bd prevalence (43%) in its native areas in India (Thorpe et al., 2018), which may be linked to a low prevalence of Bd-inhibitory bacteria, although it has not been tested there. A screen of the microbiome diversity of D. melanostictus from its native areas, and where Bd has been detected, could give new insights about microbiome patterns. ...
Article
Full-text available
Biological invasions are on the rise, with each invader carrying a plethora of associated microbes. These microbes play important, yet poorly understood, ecological roles that can include assisting the hosts in colonization and adaptation processes or as possible pathogens. Understanding how these communities differ in an invasion scenario may help to understand the host's resilience and adaptability. The Asian common toad, Duttaphrynus melanostictus is an invasive amphibian, which has recently established in Madagascar and is expected to pose numerous threats to the native ecosystems. We characterized the skin and gut bacterial communities of D. melanostictus in Toamasina (Eastern Madagascar), and compared them to those of a co-occurring native frog species, Ptychadena mascareniensis, at three sites where the toad arrived in different years. Microbial composition did not vary among sites, showing that D. melanostictus keeps a stable community across its expansion but significant differences were observed between these two amphibians. Moreover, D. melanostictus had richer and more diverse communities and also harboured a high percentage of total unique taxa (skin: 80%; gut: 52%). These differences may reflect the combination of multiple host-associated factors including microhabitat selection, skin features and dietary preferences.
... Infection dynamics can also depend on the infecting Bd fungus lineage or on the receptivity of the infected amphibian species (Kärvemo et al. 2018, Greener et al. 2020. Moreover, changing environmental conditions such as rising temperatures and anthropogenic disturbance can alter the prevalence and influence host−pathogen dynamics in de termining the outcome of infection (Bosch et al. 2007, O'Hanlon et al. 2018, Thorpe et al. 2018. ...
Article
The pathogenic chytrid fungi Batrachochytrium dendrobatidis (Bd) and B. salamandrivorans (Bsal) cause infections that have become primary drivers of amphibian biodiversity loss. While globally widespread, the distribution margins of Bd and Bsal have not been determined, and the presence of these pathogens has probably gone unnoticed in many areas, especially in northern Eurasia. To better understand the presence and distribution of both pathogens in the northern temperate and boreal forest biomes, 243 individuals were sampled from 8 native amphibian species across Estonia. Additionally, 68 amphibians were sampled from captive collections in Estonia and Latvia. Pathogen infection was assessed using metabarcoding of the ITS2 marker. No positive matches for Bsal infection were found. Bd was detected in 13 specimens, 3 of which were sampled at the Riga Zoo (with a prevalence of 5.2%) and 10 in natural environments in Estonia (3.3%). The infected wild individuals belonged to 6 amphibian species and were detected throughout the mainland of Estonia, but not on islands. Prevalence of infection with Bd ranged between 3.1 and 12.5% among native species. In addition, we found molecular evidence for a potentially new sister species to Bd in nature. Although outbreaks of chytridiomycosis have never been observed in Estonia, it cannot be excluded that the dynamics of local amphibian populations are affected by Bd infections. Therefore, further work, including capture-mark-recapture studies and long-term monitoring, are required to clarify the impact of Bd on amphibians in Northern Europe.
... Our discoveries of the five new Raorchestes species described in this study were made from forested areas in the State of Kerala, encompassing the hill ranges of Agasthyamalai, Cardamom (south of Palghat gap), and Nilgiris, Siruvani, Wayand (North of Palghat gap). Amphibians in these regions are known to be facing increasing anthropogenic threats (Biju et al., 2008;Nair et al., 2011;Thorpe et al., 2018) and all the new species are found either outside protected areas or in fragmented primary forest patches and highly disturbed secondary forest areas. The new species will therefore require immediate assessment of threats to the known populations and habitats, and their conservation status. ...
Article
Full-text available
The genus Raorchestes is a large radiation of Old World tree frogs for which the Western Ghats in Peninsular India is the major center for origin and diversification. Extensive studies on this group during the past two decades have resolved long-standing taxonomic confusions and uncovered several new species, resulting in a four-fold increase in the number of known Raorchestes frogs from this region. Our ongoing research has revealed another five new species in the genus, formally described as Raorchestes drutaahu sp. nov., Raorchestes kakkayamensis sp. nov., Raorchestes keirasabinae sp. nov., Raorchestes sanjappai sp. nov., and Raorchestes vellikkannan sp. nov., all from the State of Kerala in southern Western Ghats. Based on new collections, we also provide insights on the taxonomic identity of three previously known taxa. Furthermore, since attempts for an up-to-date comprehensive study of this taxonomically challenging genus using multiple integrative taxonomic approaches have been lacking, here we review the systematic affinities of all known Raorchestes species and define 16 species groups based on evidence from multi-gene (2,327 bp) phylogenetic analyses, several morphological characters (including eye colouration and pattern), and acoustic parameters (temporal and spectral properties, as well as calling height). The results of our study present novel insights to facilitate a better working taxonomy for this rather speciose and morphologically conserved radiation of shrub frogs. This will further enable proper field identification, provide momentum for multi-disciplinary studies, as well as assist conservation of one of the most colourful and acoustically diverse frog groups of the Western Ghats biodiversity hotspot.
... Unfortunately, however, improper sampling techniques initially including handling without gloves could have led to false positives and inflated the present findings. Another recent study also performed in Africa confirmed the prevalence of Bd in four species not reviewed in the Gower study, providing confirmation of the pathogen's presence in African species of caecilians (Thorpe et al., 2018). However, this study had small sample sizes making it difficult to extrapolate the range of this disease across the broader population. ...
Article
Full-text available
This review presents an overview of research from 1998-2018 regarding interactions of Batrachochytrium dendrobatidis with both potential hosts and predators. To this end, 23 different studies collected from the Web of Science database along with two external journals were utilized, encompassing numerous taxonomic groups. Numerous groups of animals were identified as potential vectors for the fungus, with crayfish and reptiles standing as the most prominent and consistent non-amphibian hosts warranting their inclusion in any future broadscale distribution surveys. an important area for future research. Additionally, Daphnia were noted to serve as predators of the zoospores when exposed in mesocosm scenarios, reducing infection levels in corresponding tadpoles. Caecilians have also been observed to be carriers of Bd, though the level as to which the chytrid impacts these organisms needs to be further researched. In total, this review indicates that future research needs to begin including freshwater crustaceans, caecil-ians and reptiles in field studies for presence/absence, while a broader range of taxa need to be tested to see whether they serve as vectors or hosts in natural scenarios.
Article
Chytridiomycosis is an emerging infectious disease affecting amphibians globally and it is caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd). Chytridiomycosis has caused dramatic declines and even extinctions in wild amphibian populations in Europe, Australia, Central and North America. Spanning over two and a half decades, extensive research has led to discovery of epizootic and enzootic lineages of this pathogen. However, the Bd–amphibian system had garnered less attention in Asia until recently when an ancestral Bd lineage was identified in the Korean peninsula. Amphibians co-exist with the pathogen in Asia, only sub-lethal effects have been documented on hosts. Such regions are ‘coldspots’ of infection and are an important resource to understand the dynamics between the enzootic pathogen—Bd and its obligate host—amphibians. Insights into the biology of infection have provided new knowledge on the multi-faceted interaction of Bd in a hyperdiverse Asian amphibian community. We present the findings and highlight the knowledge gap that exists, and propose the ways to bridge them. We emphasize that chytridiomycosis in Asia is an important wildlife disease and it needs focussed research, as it is a dynamic front of pathogen diversity and virulence.
Article
Full-text available
Infection records of Batrachochytrium dendrobatidis (Bd), a pathogen that has devastated amphibian populations worldwide, have rapidly increased since the pathogen’s discovery. Dealing with so many records makes it difficult to (a) know where, when and in which species infections have been detected, (b) understand how widespread and pervasive Bd is and (c) prioritize study and management areas. We conducted a systematic review of papers and compiled a database with Bd infection records. Our dataset covers 71 amphibian families and 119 countries. The data revealed how widespread and adaptable Bd is, being able to infect over 50% of all tested amphibian species, with over 1000 confirmed host species and being present in 86 countries. The distribution of infected species is uneven among and within countries. Areas where the distributions of many infected species overlap are readily visible; these are regions where Bd likely develops well. Conversely, areas where the distributions of species that tested negative overlap, such as the Atlantic Coast in the USA, suggest the presence of Bd refuges. Finally, we report how the number of tested and infected species has changed through time, and provide a list of oldest detection records per country.
Article
Full-text available
Volume 30 (April 2020), 99-111 Published by the British Herpetological Society We conducted a systematic review to evaluate the knowledge base for amphibian chytrid Batrachochytrium dendrobatidis (Bd) infection in the continent of Asia. Despite an indication of geographic bias in terms of studying chytrid fungus distribution in Asia, 167 amphibian species (145 spp. native to Asia) from 16 countries have been reported as infected with Bd. Our meta-analysis shows that overall prevalence is 8.19 % (out of 28,433 samples), and Bd-positive rate in amphibia significantly varies among sampling sources (χ 2 = 380.57, DF= 6, P< 0.001) and age categories (χ 2 = 22.09, DF= 2, P< 0.001). We used Kernel Density analysis to produce a hotspot map for chytrid infection, and Digital Elevation Model to understand the distribution of chytrid positive locations across different elevations. In our meta-analysis, most of the Bd-positive sites range between 4.45-27.49 °C, 167-4,353 mm rainfall, 10-40°N, and at lower elevations (<500 m). Using land cover analysis, we did not find a statistically significant difference among six different land cover categories in relation to the prevalence of Bd across Asia. Although no mass die-off events have been reported so far, Maximum Entropy modelling shows that Bd distribution and infection may potentially occur across a vast region of southeast Asia. In conclusion, we call for more systematic research and monitoring strategies in place for countries with little to no information, but have a moderately higher risk of chytrid distribution and infection.
Article
Full-text available
The importance of patch quality for amphibians is frequently overlooked in distribution models. 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 characterise 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 species 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 microhabitats using a stepwise analysis of the AICc subroutine (distLM, Primer-e, v7). Generalist taxa were associated with increased numbers of microhabitat types. Non-significant associations are reported for the remaining 9 taxa. Microhabitat distribution was spatially structured 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.
Article
Full-text available
The Rufescent Burrowing Frog, Fejervarya rufescens, is thought to have a wide distribution across the Western Ghats in Peninsular India. This locally abundant but secretive species has a short breeding period, making it a challenging subject for field studies. We sampled 16 populations of frogs morphologically similar to F. rufescens in order to understand the variation among populations found across the Western Ghats. Our study shows significant morphological and genetic differences among the sampled populations, suggesting that F. ‘rufescens’ is a complex of several undescribed species. Using evidence from morphology and genetics, we confirm the presence of five distinct species in this group and formally describe four as new. The new species were delineated using a phylogeny based on three mitochondrial genes (16S, COI and Cytb) and a haplotype network of a nuclear gene (Rag1). Hereafter, the distribution of F. rufescens is restricted to the state of Karnataka and adjoining regions of northern Kerala. Three new species (Fejervarya kadar sp. nov., Fejervarya manoharani sp. nov. and Fejervarya neilcoxi sp. nov.) are from regions south of Palghat gap in the state of Kerala, and one (Fejervarya cepfi sp. nov.) from the northern Western Ghats state of Maharashtra. These findings indicate that Fejervarya frogs of the Western Ghats are more diverse than currently known. Our results will also have implications on the conservation status of F. rufescens, which was previously categorized as Least Concern based on its presumed wide geographical distribution. Furthermore, in order to facilitate a better taxonomic understanding of this region’s fejervaryan frogs, we divide all the known Fejarvarya species of the Western Ghats into four major groups—Fejervarya nilagirica group, Fejervarya rufescens group, Fejervarya sahyadris group and Fejervarya syhadrensis group, based on their morphological affinities.
Article
Full-text available
Patterns of univariate trait variation across metacommunities are widely explored, as are searches for their underlying causes. Surprisingly, patterns of multivariate shape remain unknown, and the search for drivers of functional traits of communities often neglect the biogeographical distribution of phylogenetic clades. Our aim was to investigate multivariate shape distribution across metacommunities and to determine the main environmental drivers of shape beyond/taking into account the phylogenetic distribution of lineages. We obtained mean skull and mandible shape for 228 species of Neotropical sigmodontine rodents through geometric morphometrics (GM), and then calculated mean shapes for 1°x1° cells across the Neotropics based on the incidence of sigmodontines. We investigated the effects of lineage distribution on mean trait variation by using phylogenetic fuzzy weighting to calculate Principal Coordinates of Phylogenetic Structure (PCPS). Effects of environmental variables on shape variation incorporating phylogenetic composition were realized through redundancy analysis. We found that the different distributions of major lineages throughout the Neotropics were responsible for much of the mean shape variation. The association of landscape features with tribal groupings (Oryzomyini with Amazonia and Phyllotini and Abrotrichini with the Andes) were standouts. Environmental variables and lineage distribution explain the same (i.e. shared) portion of shape variation, suggesting phylogenetic niche conservatism at the metacommunity level. Seasonality in temperature and land cover were the best environmental predictors of mean shape: larger tympanic bullae, incisive foramina, and check teeth are all associated with highly seasonal and less vegetated areas. Our new approach of using GM shape across metacommunities was demonstrably useful in understanding large-scale biogeographical patterns of shape variation and identifying its underlying causes. The overlap between environmental variables and phylogenetic lineage distribution suggests that a process of niche conservatism is likely: the phenotype-environment correlation is mediated by the differential biogeographical distribution of the main clades.
Article
Full-text available
Chytridiomycosis has decimated amphibian biodiversity. Management options for the disease are currently limited, but habitat manipulation holds promise due to the thermal and physicochemical sensitivities of chytrid fungi. Here, we quantify the extent to which habitat management could reduce metapopulation extinction risk for an Australian frog susceptible to chytridiomycosis. Our modelling revealed that: (i) habitat management is most effective in climates where hosts are already less susceptible to the disease; (ii) creating habitat, particularly habitat with refugial properties adverse to the pathogen, may be substantially more effective than manipulating existing habitat, and; (iii) increasing metapopulation size and connectivity through strategic habitat creation can greatly reduce extinction risk. Controlling chytridiomycosis is a top priority for conserving amphibians. Our study provides impetus for experiments across a range of species and environments to test the capacity of habitat management to mitigate the impacts of this pervasive disease. This article is protected by copyright. All rights reserved
Article
Full-text available
The anuran family Ranixalidae is endemic to India, with a predominant distribution in the Western Ghats, a region that is home to several unique amphibian lineages. It is also one of the three ancient anuran families that diversified on the Indian landmass long before several larger radiations of extant frogs in this region. In recent years, ranixalids have been subjected to DNA barcoding and systematic studies. Nearly half of the presently recognized species in this family have been described over the last three years, along with recognition of a new genus to accommodate three previously known members. Our surveys in the Western Ghats further suggest the presence of undescribed diversity in this group, thereby increasing former diversity estimates. Based on rapid genetic identification using a mitochondrial gene, followed by phylogenetic analyses with an additional nuclear gene and detailed morphological studies including examination of museum specimens, new collections , and available literature, here we describe two new species belonging to the genus Indirana from the Western Ghats states of Karnataka and Kerala. We also provide new genetic and morphological data along with confirmed distribution records for all the species known prior to this study. This updated systematic revision of family Ranixalidae will facilitate future studies and provide vital information for conservation assessment of these relic frogs.
Article
Full-text available
Leaping frogs of the family Ranixalidae are endemic to the Western Ghats of India and are currently placed in a single genus, Indirana. Based on specimens collected from their entire range and a comprehensive study of type material defining all known species, we propose a revised taxonomy for the leaping frogs using an integrative approach including an analysis of the mitochondrial 16S rRNA and nuclear rhodopsin genes, as well as multivariate morphometrics. Both genetic and morphological analyses suggest that the genus Indirana is paraphyletic and a distinct monophyletic group, Walkerana gen. nov is described herein. The new genus is separated from Indirana sensu stricto by an apomorphic character state of reduced webbing, with one phalange free on the first and second toe (vs. no free phalanges), two phalanges free on the third and fifth toe (vs. one free phalange), and three phalanges free on the fourth toe (vs. 2–2½ phalanges free). This review includes (i) identification of lectotypes and redescription of three species of the genus Walkerana; (ii) identification of lectotypes for Indirana beddomii and I. semipalmata and their redescription; (iii) redescription of I. brachytarsus and I. gundia; and (iv) descriptions of four new species, namely, I. duboisi and I. tysoni from north of the Palghat gap, and I. yadera and I. sarojamma from south of the Palghat gap; and (iv) a key to the genera and species in the family Ranixalidae.
Article
Full-text available
In many parts of the world rock outcrops form important landscape elements that play a role in generatingandmaintainingbiodiversityinadditiontoprovidingkeyecosystemservices.Theserock outcrops rise abruptly from the surrounding landscape, have a patchy distribution, and represent centersofdiversityandendemismforbothanimalandplantlife(HopperandWithers 1997).Known as ‘inselbergs’ and often composed of Precambrian granitoids, these outcrops occur across all continents. Inselbergs are particularly noteworthy inancient biodiversityhotspots, e.g., the Brazilian Atlantic Forest, Guinean Forests of West Africa, Madagascar, the Greater Cape and Southwest Australian Floristic regions (Hopper et al. 2016). The ecological and evolutionary processes that operate in these ancient environments differ significantly from comparatively more recent environments (Hopper 2009). Their conservation is of global importance, in great part because they support unique, endemic biota of recent and deep phylogenetic history. Many inselbergs are threatened by alarming rates of mining, weed invasion (de Paula et al. 2015), water harvesting, tourism, and urbanisation, resulting in biodiversity loss and degradation of their ecosystem services (Fig. 1). Illustrative of this destruction, the World Resources Institute (WRI 2003) reports that nearly one-third of all active mining sites are located within undisturbed areas with conservation value and nearly 75 % are within areas of ecological significance. Reasons for inselberg conservation include their extraordinarily high numbers of geographically restricted and threatened species; functioning as terrestrial habitat islands; (Bussell and James 1997); and serving as centers of diversity for highly specialized life forms such as carnivorous (Seine et al. 1995) and desiccation-tolerant plants (Porembski and Barthlott 2000). These naturally stress-tolerant species may be important sources of genetic information to generate new crops (Costa et al. 2016). Remarkably, a few inselberg endemics have evolved the smallest known angiosperm genomes (Greilhuber et al. 2008), suggesting that inselberg conservation translates to conservation of novel evolutionary strategies. Inselbergs influence the water and nutrient supplies of surrounding landscapes (Schut et al. 2014). Due to low rates of soil development and the general absence of soil across the inselberg surface, most precipitation is lost through runoff, benefiting the surrounding vegetation. In several countries, the supply of bottled drinking water largely depends on runoff from inselbergs. Inselberg rock pools provide essential habitat for endemic animals (Jocque´ et al. 2010) and plants (Vogiatzakis et al. 2009); serve as refugia (Pinder et al. 2000); and control hydrological cycles by modulating water storage and recharging the adjacent landscape (Cross et al. 2015). They have been used by humans for more than 3000 years to support human and livestock populations (Bauer and Morrison 2006). Finally, inselbergs play an important role in the evolution of vital human habits including lifestyle preferences (Larson et al. 2004). Iconic examples of outcrops important from the religious and economic points of view include Mt. Arafat (Mecca), the Mahabalipuram Temple and Shravanabelagola (India), Wave Rock (Australia), and Sugar Loaf Mountain in Rio de Janeiro (Brazil). Unfortunately, human activities threaten the biodiversity and ecosystem services of inselbergs, including quarrying, plant overharvesting, weed invasion, uncontrolled fires (Yates et al. 2003), climate change, and unsustainable uses, including adjacent farming, hunting, logging roads, temple construction, and tourism/sports/cultural activities (Porembski and Barthlott 2000). In India, entire inselbergs have vanished due to quarrying of high value granite. Surprisingly, inselbergs have rarely been considered in the context of the degradation of Earth’s natural ecosystems. Unfortunately, there are no reliable estimates on global rates of inselberg destruction that would be urgently needed to promulgate effective conservation strategies. It is time to develop international legislation for inselberg conservation, which includes the creation of protected areas in centers of endemism; weed prevention and eradication; local educational programs in water and nutrient cycling; ex situ conservation programs for threatened species when quarrying is inevitable; and implementation of effective restoration strategies. All will be important to conserve at least part of these iconic, globally important, and highly threatened ecosystems.
Article
Full-text available
The northern Western Ghats are characterised by plateaus and hilltop carapaces formed from ferricretes rich in aluminium ore. Ferricretes in Western Ghats are home to a high number of endemic species, many with extremely limited distribution. The heterogeneity of microhabitats on ferricretes supports a great diversity of plant and animal communities. With little overburden and a high percentage of recoverable metals they are targeted for mining which leads to removal of all soil, vegetation and microhabitats. Vegetation and faunal diversity of unmined sites from Kolhapur district were studied providing reference data used to discuss restoration efforts on two mined sites in the region. Restoration efforts have faced ecological and legal hurdles. The international literature for the restoration of bauxite mines fails to demonstrate any successful model to return the species assemblage to a pre-mining profile. Restoration practices fail to adequately replicate microhabitat heterogeneity; often restoring sites to a different ecosystem from the original. The present mining policies do not take cognizance of the special nature of plateau habitats, ecology or the ecosystem functions they provide. We suggest a moratorium on mining of the high level lateritic plateaus in Western Maharashtra is justified until the biodiversity value and ecosystem
Article
Batrachochytrium dendrobatidis is a pathogen of amphibians that has been implicated in severe population declines on several continents. We investigated the zoospore activity, physiology and protease production of B. dendrobatidis to help understand the epidemiology of this pathogen. More than 95% of zoospores stopped moving within 24 h and swam less than 2 cm before encysting. Isolates of B. dendrobatidis grew and reproduced at temperatures of 4–25 C and at pH 4–8. Growth was maximal at 17–25 C and at pH 6–7. Exposure of cultures to 30 C for 8 d killed 50% of the replicates. B. dendrobatidis cultures grew on autoclaved snakeskin and 1% keratin agar, but they grew best in tryptone or peptonized milk and did not require additional sugars when grown in tryptone. B. dendrobatidis produced extracellular proteases that degraded casein and gelatin but had no measurable activity against keratin azure. The proteases were active against azocasein at temperatures of 6–37 C and in a pH range of 6–8, with the highest activity at temperatures of 23–30 C and at pH 8. The implications of these observations on disease transmission and development are discussed.