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New species, diversity, systematics, and conservation assessment of the Puppet Toads of Sumatra (Anura: Bufonidae: Sigalegalephrynus)

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Using a combination of morphological and molecular data we recognize three new species of Puppet Toad, Sigalegalephrynus Smart, Sarker, Arifin, Harvey, Sidik, Hamidy, Kurniawan & Smith, a recently described genus endemic to the highland forests of Sumatra, Indonesia. Phylogenetic analysis of mitochondrial DNA sequences recovered a monophyletic relationship among all Puppet Toads, with two distinct evolutionary clades, a northern and a southern. The northern clade includes Sigalegalephrynus gayoluesensis sp. nov., and S. burnitelongensis sp. nov., and the southern clade includes S. harveyi sp. nov., S. mandailinguensis, and S. minangkabauensis. With the discovery of these three new species, Sigalegalephrynus contains more endemic species than any other genus of toad in Indonesia. We used maximum entropy, implemented in MaxEnt, to identify suitable habitats and occurrence probability of additional undescribed new species from the island. The most important predictors of Sigalegalephrynus distribution were elevation (64.5%) and land cover (7.11%). Based on the probability of presence, it is likely that there are many more species of the genus awaiting discovery in Sumatra. Our analysis, based on IUCN Red List of Threatened Species category and criteria, shows that all of the five species of Sigalegalephrynus are in great risk of extinction and should be placed into the Endangered (EN) category of IUCN Red List.
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ZOOTAXA
ISSN 1175-5326 (print edition)
ISSN 1175-5334 (online edition)
Accepted by C. Onn: 28 Aug. 2019; published: 2 Oct. 2019 365
Zootaxa 4679 (2): 365–391
https://www.mapress.com/j/zt/
Copyright © 2019 Magnolia Press Article
https://doi.org/10.11646/zootaxa.4679.2.9
http://zoobank.org/urn:lsid:zoobank.org:pub:4C01C8CC-DB67-461C-886C-B3AE154B27EF
New species, diversity, systematics, and conservation assessment of the
Puppet Toads of Sumatra (Anura: Bufonidae: Sigalegalephrynus)
GOUTAM C. SARKER1,4, ELIJAH WOSTL1, PANUPONG THAMMACHOTI1, IRVAN SIDIK2,
AMIR HAMIDY2, NIA KURNIAWAN3 & ERIC N. SMITH1
1Amphibian and Reptile Diversity Research Center (ARDRC) and Department of Biology, The University of Texas at Arlington, Arling-
ton, TX 76019, USA.
2Laboratory of Herpetology, Museum Zoologicum Bogoriense, Research Center for Biology, Indonesian Institute of Sciences-LIPI,
Widyasatwaloka Jl. Raya Jakarta Bogor km 46, Cibinong, West Java, Indonesia
3Department of Biology, Universitas Brawijaya, Jl. Veteran, Malang, East Java, Indonesia
4Corresponding author. E-mail: gsarker@uta.edu or goutam.sarker@mavs.uta.edu
Abstract
Using a combination of morphological and molecular data we recognize three new species of Puppet Toad,
Sigalegalephrynus Smart, Sarker, Arifin, Harvey, Sidik, Hamidy, Kurniawan & Smith, a recently described genus
endemic to the highland forests of Sumatra, Indonesia. Phylogenetic analysis of mitochondrial DNA sequences recovered
a monophyletic relationship among all Puppet Toads, with two distinct evolutionary clades, a northern and a southern.
The northern clade includes Sigalegalephrynus gayoluesensis sp. nov., and S. burnitelongensis sp. nov., and the southern
clade includes S. harveyi sp. nov., S. mandailinguensis, and S. minangkabauensis. With the discovery of these three new
species, Sigalegalephrynus contains more endemic species than any other genus of toad in Indonesia. We used maximum
entropy, implemented in MaxEnt, to identify suitable habitats and occurrence probability of additional undescribed new
species from the island. The most important predictors of Sigalegalephrynus distribution were elevation (64.5%) and land
cover (7.11%). Based on the probability of presence, it is likely that there are many more species of the genus awaiting
discovery in Sumatra. Our analysis, based on IUCN Red List of Threatened Species category and criteria, shows that all
of the five species of Sigalegalephrynus are in great risk of extinction and should be placed into the Endangered (EN)
category of IUCN Red List.
Key words: GeoCAT, Indonesia, IUCN Red List, MaxEnt, Niche modeling, Sigalegalephrynus burnitelongensis sp. nov.,
Sigalegalephrynus gayoluesensis sp. nov., Sigalegalephrynus harveyi sp. nov., Sigalegalephrynus mandailinguensis,
Sigalegalephrynus minangkabauensis, Southeast Asia, Sunda Shelf
Introduction
Amphibians are a highly threatened and poorly-known animal group worldwide (Tapley et al. 2018), as is indicated
by the many new species that have been described in recent years from numerous biodiversity hotspots. Unfortu-
nately, these animals are facing extinction due to global spread of zoonotic disease (Rödder et al. 2009, Brito et al.
2011, O’Hanlon et al. 2018), habitat destruction and fragmentation (Margono et al. 2014, Harris et al. 2017), and
anthropogenic climate change (Rödder et al. 2010, Bickford et al. 2010). Southeast Asia is a hotspot of amphibian
diversity (Inger 1999), but still poorly understood (Brown & Stuart 2012, Chan & Grismer 2019, Coleman et al.
2019) and with many new species awaiting discovery (Bickford et al. 2010). Here, Sumatra is one of the least ex-
plored lands in terms of herpetological research (Harvey et al. 2017a). Extensive surveys are needed to understand
its biodiversity (Brown & Stuart 2012) and to develop conservation strategies of this island (Bickford et al. 2010,
Coleman et al. 2019).
The International Union for the Conservation of Nature (IUCN) Red List of Threatened Species is a widely-ac-
cepted index for assessing species extinction risks and an effective source for conservation planners (Lamoreux et
al. 2003; Rondinini et al. 2013; Trull et al. 2017). Although there is a constant rate of discovery of amphibian spe-
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366 · Zootaxa 4679 (2) © 2019 Magnolia Press
cies, an IUCN Red List status assessment accompanying those publications has declined from 2004 to 2015 (Tapley
et al. 2018). Even though 24% of the amphibian species have been categorized as Data Deficient (DD) (Nori et al.
2018), about 80% do not have their up-to-date IUCN Red List status (Tapley et al. 2018) (many in Malaysia, Indo-
nesia, Papua New Guinea, China). To help prioritize conservation for the newly discovered arboreal Puppet Toads,
genus Sigalegalephrynus Smart, Sarker, Arifin, Harvey, Sidik, Hamidy, Kurniawan & Smith (2017), we describe
three newly discovered populations as new species and provide IUCN Red List status assessment for all members
of this Sumatran endemic genus.
The genus Sigalgalephrynus contains two species: S. mandailinguensis, from Gunung Sorikmerapi, Batang
Gadis National Park, Sumatera Utara province, and S. minangkabauensis, from Gunung Kunyit, a peak in the Bari-
san Range of the province of Jambi (Smart et al. 2017). In 2015, we collected additional specimens of this genus,
from the Burni Telon volcano and Highlands of Gayo Lues in the province of Aceh, and from Dempo volcano of
the Sumatera Selatan province. Based on morphological characteristics, genetic divergence and advertisement calls,
we recognize these populations as distinct species under the lineage-based Unified Species Concept of de Queiroz
(2007). Herein we formally describe these three montane populations of Puppet Toads as new species, estimate their
phylogenetic relationships, and discuss the distribution and conservation of the genus.
Materials and methods
Specimens of the new species described in this study were collected in July and August 2015. We strictly followed
protocols approved by the UTA Institutional Animal Care and Use Committee (IACUC; number UTA IACUC
A12.004) for collecting, handling and euthanizing specimens. We took photographs of live animals, and then pic-
tures of dorsal, ventral and lateral aspects immediately after euthanasia. Specimens were fixed in 10% formalin,
and then transferred to 70% alcohol for permanent storage. Prior to fixation, we took liver or muscle tissue samples
and preserved them in 1.5 mL of cell lysis buffer solution (0.5 M Tris/0.25% EDTA/2.5% SDS, pH = 8.2). Finally,
we deposited all specimens at Laboratory of Herpetology in the Museum Zoologicum Bogoriense (MZB), and the
Amphibian and Reptile Diversity Research Center (ARDRC) of the University of Texas, Arlington (UTA). All other
museum acronyms follow Sabaj Perez (2016).
Morphological data. Our morphological terminology is based on Matsui (1984), Duellman (2001), and Kok
& Kalamandeen (2008). We used digital calipers or an ocular micrometer to measure each character to the nearest
0.1mm. We measured: 1) snout–vent length (SVL)—tip of snout to anterior margin of vent; 2) head length (HL)—
posterior angle of jaw to tip of snout; 3) head width (HW)—ventrally at angles of jaw, excluding warts; 4) snout
length (SNL)—anterior corner of eye to snout tip; 5) intercanthal distance (ICD)—distance between anterior edges
of canthi; 6) internarial distance (IND)—distance between anterior ends of nares; 7) eye to naris distance (END)—
distance from the anterior corner of eye to posterior border of naris; 8) naris to snout distance (NSD)—distance from
anterior border of naris to the tip of snout; 9) interorbital distance (IOD)—minimal distance between upper eyelids;
10) eye length (EL)—horizontal distance from anterior to posterior junctions of upper and lower eyelids; 11) tym-
panum length (TML)—horizontal width of tympanum; 12) forearm length (FAL)—tip of elbow to proximal margin
of outer metacarpal tubercle; 13) hand length (HAL)—proximal margin of metacarpal tubercle to Finger III tip; 14)
thigh length (THL)—center of cloaca to distal surface of knee, appressed; 15) tibia length (TBL)—greatest length
of tibia when positioning hind limb in a Z pattern; 16) tarsus length (TRL)—tibio-tarsal articulation to proximal
margin of outer metatarsal tubercle; 17) foot length (FTL)—proximal margin of outer metatarsal tubercle to Toe IV
tip; 18) outer metacarpal tubercle length (OMCL)—from the anterior to the posterior end of the outer metacarpal
tubercle; 19) outer metacarpal tubercle width (OMCW)—greatest width of outer metacarpal tubercle measured
perpendicularly to OMCL; 20) inner metacarpal tubercle length (IMCL)—from the anterior to the posterior end of
the inner metacarpal tubercle; 21) inner metacarpal tubercle width (IMCW)—greatest width of outer metacarpal
tubercle measured perpendicularly to IMCL; 22) inner metatarsal tubercle length (IMTL)—from the anterior to the
posterior end of the inner metatarsal tubercle; 23) inner metatarsal tubercle width (IMTW)—greatest width of inner
metatarsal tubercle measured perpendicularly to IMTL; and 24) length of fingers (F1L–F4L)—from tip of fingers
to first phalangeal-metacarpal joint; 25) length of toes (TlL–T5L)—from tip of fingers to first phalangeal-metatarsal
joint; 26) width of third finger disc (F3PD)—at right angle to digital axis; 27) width of the proximal end of the pen-
ultimate phalanx of third finger (F3PB)—at right angle to digital axis. Along with mensural data, we took qualitative
SIGALEGALEPHRYNUS, THE PUPPET TOADS OF SUMATRA Zootaxa 4679 (2) © 2019 Magnolia Press · 367
morphological characters (e. g. color) from each specimen. The webbing formulae follow Savage & Heyer (1967)
as modified by Myers and Duellman (1982) and Savage & Heyer (1997). We used digital color photographs and
followed Kok & Kalamandeen (2008) to describe color in life and other qualitative characteristics; these images are
deposited at the University of Texas at Arlington digital image collection. All morphological mensural data were
collected from adult specimens by a single observer (GCS).
Acoustic data analysis. Calls were recorded by using a Zoom H4n Handy Recorder® at a sampling rate of
44.1 kHz. For call analyses, we followed the terminology used by Duellman (1970). We performed call analyses by
removing background noise with the sound-editing software Audacity v2.1.2 (Audacity Team 2016). To produce
oscillograms and spectrograms we used RAVEN LITE 2.0.0 (Bioacoustics Research Program 2016). We calculated
the time between notes, the time between pulses, fundamental frequency, and dominant frequency using SOUN-
DRULER version 0.9.6.0 (Gridi-Papp 2007).
Taxon sampling and DNA sequencing. To isolate genomic DNA we used Serapure beads following the Agen-
court protocol (Beckman Coulter Co., Fort Collins, CO, USA) after Rohland & Reich (2012). We amplified one
mitochondrial (16S) gene using the forward primer 16SH (5’ CGC CTG TTT ATC AAA AAC AT 3’) and the reverse
primer 16SL (5’ CCG GTC TGA ACT CAG ATC ACG T 3’), after Vences et al. (2005), using the thermocycler PCR
protocol provided by Van Bocxlaer et al. (2009), and the Go Taq® Flexi DNA polymerase (Promega Corporation,
Madison, Wisconsin, USA), on a GeneAmp® PCR System 9700 (Applied BioSciences, Foster City, CA, USA).
PCR success was visually assessed on a 1% agarose gel, and PCR products were purified with Serapure beads (fol-
lowing the Agencourt protocol, Beckman Coulter Co., Fort Collins, CO, USA). The Genomic Core Facility at the
University of Texas at Arlington completed the sequencing reactions with an ABI PRISM 3100xl Genetic Analyzer
(Applied Biosystems, Foster City, CA, USA).
We used 32 sequences for phylogenetic inference, including 17 sequences from GenBank. All sequences gener-
ated for this project were submitted to GenBank (Table 1). Our taxon sampling included at least one representative
from each extant Southeast Asian bufonid genus. We included one New World bufonid—Cayenne stubfoot toad
(Atelopus flavescens), and one hylid—Canyon Treefrog (Dryophytes arenicolor) as outgroups.
Sequence alignment and phylogeny inference. We assembled and cleaned raw gene fragment sequences
using Sequencher v 5.3 (Gene Codes, Ann Arbor, MI, USA) and aligned the sequences using the Muscle (Edgar
2004) algorithm in MEGA (v6.0; Tamura et al. 2013). We used the Gblock server (Castresana 2000) to identify
poorly resolved regions of the alignment, using a less stringent selection of blocks, which is more appropriate for
short alignments (Castresana 2000; Talavera & Castresana 2007). We removed these poorly aligned regions from
subsequent analyses.
To examine the phylogenetic relationships of Sigalegalephrynus we used maximum likelihood (ML) and Bayes-
ian inference (BI) methods. PartitionFinder v1.10 (Lanfear et al. 2012) was used to determine the best partitioning
schemes and respective nucleotide substitution models. We employed the corrected Akaike Information Criterion
(AICc) model to find selection parameters and the ‘greedy’ search algorithm for finding the best models for Bayes-
ian analysis.
The GTR+I+G model was suggested for Bayesian analysis, but following Stamatakis (2006), we used GTR+G
instead. We performed ML analysis employing a rapid bootstrapping algorithm using the program RAxML-HPC
BlackBox (v8.2.10; Stamatakis 2014) on the CIPRES gateway server (Miller et al. 2010). We considered nodes to
be strongly supported when having bootstrap value were above 70% (Hillis & Bull 1993).
We conducted Bayesian Markov chain Monte Carlo (MCMC) phylogenetic analyses using MrBayes (v3.2.3;
Ronquist et al. 2012), employing two simultaneous runs of four MCMC analyses, consisting of one cold and three
incrementally heated chains, with random trees for a total of 10 × 106 generations (sampling every 500 genera-
tions). We set the burn-in to the default value of 25%, hence discarding the initial 5000 generations. To examine
stationarity, we used trace plots and ESS values (> 200) on TRACER v1.6 (Rambaut et al. 2014). We constructed
a 50% majority consensus tree with estimates of Bayesian support using the remaining sampled trees and posterior
probabilities (PP). We considered nodal support with PP values ≥ 0.95 as significant (Huelsenbeck & Rannala 2004;
Mulcahy et al. 2011). We used FigTree (v1.4.2; Rambaut, 2012) for graphical visualization of the resulting ML and
Bayesian trees.
Niche modeling and habitat suitability. Because there are many highland forests we could not explore dur-
ing our Sumatran expedition, we used species distribution modeling techniques to identify suitable habitat for the
most probable occurrence of additional new species of this genus. We used MaxEnt v.3.4.1 (Phillips et al. 2017), a
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368 · Zootaxa 4679 (2) © 2019 Magnolia Press
maximum entropy model implementation, because it performs best among all other available species distribution
modeling programs (Pearson et al. 2007; Tarkesh & Jetschke 2012, Remya et al. 2015). Several studies (Galante
et al. 2018, Pearson et al. 2007, Shcheglovitova & Anderson 2013) have shown that MaxEnt can have a biologi-
cally meaningful model performance with as low as five occurrence data points. For a very narrow-ranged species,
this minimum number of occurrence data points can be as low as three (Proosdij et al. 2016) since MaxEnt is less
sensitive to sample size (Wisz et al. 2008). Sigalegalephrynus species are micro-endemics (Smart et al. 2017) and
occurrence data of these is limited, in fact we have no more than two useful occurrence data points for a single spe-
cies. Thus, for finding suitable habitats for potential new populations or species, instead of modeling each species
individually we collectively modeled our nine GPS data points for the five Sigalegalephrynus species.
For environmental variables, we used the 19 environmental variables representing seasonality, extremity, and
annual trend available from the WorldClim v2.0 (http://worldclim.org/version2) datasets (Fick & Hijmans 2017),
30 arc seconds land cover data (http://www.diva-gis.org/gdata), and 30 arc-second digital elevation modeling data
(DEM) from Southeast Asia (downloaded using ArcGIS online extension (ArcGIS v10.5; ESRI, Redlands, CA).
Correcting for autocollinearity and excluding highly correlated variables is important in predicting future range
shift of a species under climate change scenario (Braunisch et al. 2013). But, autocollinearity is not a problem for
predicting the current range of a taxon (Braunisch et al. 2013, Brown et al. 2017).
Inclusion of all of the environmental variables do not affect the overall predictive quality of the MaxEnt model
(Brown et al. 2017). On the other hand, exclusion of correlated environmental variables from the model needs a
good understanding of the ecology and natural history of the species (Dufresnes et al. 2018; Spear et al. 2018).
Also, the exclusion of environmental variables from the model could underperform and fail to predict the actual
species occurrence data points too (Tan et al. 2017). Moreover, correcting for autocollinearity and deciding variable
importance in modeling is not difficult for the machine learning algorithm of MaxEnt (Elith et al. 2011; Shaney et
al. 2017) which can be performed though jackknifing (Shaney et al. 2017). Many recent studies have used all of the
19 bioclimatic variables in species distribution modeling for predicting current distribution of species (e. g. for—ar-
thropods: Perger et al, 2017, Bagheri et al. 2018; fish: Jarić et al. 2018; amphibians: Dufresnes et al. 2018, Neal et
al. 2018; reptiles: Brothers & Lohman 2018, Shaney et al. 2017; birds: Berzaghi et al. 2018; mammals: Regmi et
al. 2018; plants: Kodis et al. 2018, Karrenberg et al. 2018, Kim et al. 2018).
Given that multicollinearity is not a problem for predicting current distribution, we do not have a good under-
standing of the ecology and natural history of all the species of Sigalegalephrynus and aim of this modeling is not
to predict future range shift under climate change scenario, we decided to include all 19 bioclimatic variables in our
model following Spear et al. (2018). We jackknifed our model to assess best for predictor variables the distribution
of Sigalegalephrynus (Merow et al. 2013, Brown 2014, Remya et al. 2015, Shaney et al. 2017). We used 75% of the
data for training and 25% for testing following Hu et al. (2016). We used default regularization since it performs bet-
ter in choosing reasonable predictors (Phillips et al. 2006). Four replicates were performed using subsample replica-
tion run type and maintaining 1000 iterations. We followed Hu and Jiang (2018) in using a 10th percentile training
threshold for creating a binary presence/absence map from the continuous suitability map output. We reported the
area under the receiver operating characteristic (ROC) curve (AUC value). AUC value closer to 1.0 indicates high
performance of the predictive model (Phillips and Dudík 2008, Walden-Schreiner et al. 2018), for each replication.
We reported the average AUC value under the ROC curve of all replicates. Since sometimes AUC score itself under
the ROC curve might be misleading (Lobo et al. 2008, Ramírez-Gíl et al. 2018), we assessed our model prediction
performance by using functions available in NicheToolBox (http://shiny.conabio.gob.mx:3838/nichetoolb2/) (Os-
orio-Olvera et al. 2018). We used similar parameters in NichToolBox that were used by Ramírez-Gíl et al. (2018)
for assessing model prediction performance.
Geospatial conservation assessment. The extinction risks of all the species of Sigalegalephrynus were evalu-
ated following the criteria and guidelines for the IUCN Red List Categories (IUCN Standards and Petitions Sub-
committee, 2017). We also used the program GeoCAT (Bachman et al. 2011) for measuring Area of Occupancy
(AOO) and Extent of Occupancy (EOO) by using IUCN recommended default values of the cell grid, and less
stringent cell grid values (by doubling the IUCN default values).
Results
SIGALEGALEPHRYNUS, THE PUPPET TOADS OF SUMATRA Zootaxa 4679 (2) © 2019 Magnolia Press · 369
TABLE 1. GenBank Accession numbers of specimens used in molecular analysis.
Species Location Field Number Voucher Number GenBank Accession No. (16S) Source
INGROUP
Ansonia hanitschi Malaysia; Borneo VUB 0615 FJ882794 Van Bocxlaer et al. 2009
Ansonia leptopus Malaysia; Borneo VUB 0632 FJ882795 Van Bocxlaer et al. 2009
Ansonia sp. Indonesia; Sumatra ENS 19207 UTA A-65475 MH560504 This study
Ansonia spinulifer Malaysia; Borneo VUB 0647 FJ882798 Van Bocxlaer et al. 2009
Duttaphrynus melanostictus Indonesia; Java ENS 13607 UTA A-65510 MH560505 This study
Duttaphrynus melanostictus Indonesia; Java ENS 15036 UTA A-63417 MH560506 This study
Duttaphrynus melanostictus Indonesia, Lampung ENS 13762 UTA A-65511 MH560507 This study
Ingerophrynus biporcatus Indonesia; Sumatra ENS 7529 UTA A-53730 KX192090 Smart et al. 2017
Ingerophrynus divergens Indonesia; Sumatra ENS 18497 UTA A-65486 MH560508 This study
Leptophryne borbonica Indonesia; Sumatra ENS 14099 UTA A-62486 KX192095 Smart et al. 2017
Leptophryne cruentata Indonesia; Java ENS 15955 UTA A-62523 MH560509 This study
Pelophryne misera Malaysia; Borneo VUB 0641 FJ882800 Van Bocxlaer et al. 2009
Pelophryne signata Malaysia; Borneo VUB 0583 FJ882801 Van Bocxlaer et al. 2009
Pelophryne sp. Indonesia; Sumatra ENS 16092 UTA A-65485 MH560510 This study
Phrynoidis asper Indonesia; Sumatra ENS 15172 UTA A 63413 MH560511 This study
Phrynoidis asper Indonesia; Java ENS 16138 UTA A 63410 MH560512 This study
Phrynoidis juxtasper Malaysia; Borneo VUB 0649 FJ882805 Van Bocxlaer et al. 2009
Pseudobufo subasper Indonesia; Sumatra ENS 17047 UTA A-63763 KX192096 Smart et al. 2017
Pseudobufo subasper Indonesia; Sumatra ENS 17052 UTA A-63764 KX192093 Smart et al. 2017
Rentapia hosii Malaysia; Borneo BORNEENSIS 22088 AB331717 Matsui et al. 2007
Sabahphrynus maculatus Malaysia; Borneo BORNEENSIS 08425 AB331718 Matsui et al. 2007
Sigalegalephrynus burnitelongensis Indonesia; Sumatra ENS 18883 UTA A-65492 MH560517 This study
Sigalegalephrynus burnitelongensis Indonesia; Sumatra ENS 18884 MZB.Amph.30413 MH560518 This study
Sigalegalephrynus gayoluesensis Indonesia; Sumatra ENS 19525 UTA A-65490 MH560515 This study
Sigalegalephrynus gayoluesensis Indonesia; Sumatra ENS 19527 MZB.Amph.30411 MH560516 This study
Sigalegalephrynus harveyi Indonesia; Sumatra ENS 18377 MZB.Amph.30412 MH560513 This study
Sigalegalephrynus harveyi Indonesia; Sumatra ENS 18406 UTA A-65474 MH560514 This study
Sigalegalephrynus mandailinguensis Indonesia; Sumatra ENS 16936 UTA A-63562 KX192092 Smart et al. 2017
Sigalegalephrynus mandailinguensis Indonesia; Sumatra ENS 15697 MZB.Amph.25736 KX192094 Smart et al. 2017
Sigalegalephrynus minangkabauensis Indonesia; Sumatra ENS 16028 MZB.Amph.25738 KX192091 Smart et al. 2017
OUTGROUP
Atelopus flavescens French Guiana, S Kaw BPN 726 (UTA) DQ283259 Frost et al. 2006
Dryophytes arenicolor USA; Mississippi DCC 0343 TNHC 61118 (VUB 1052) FJ882776 Van Bocxlaer et al. 2009
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370 · Zootaxa 4679 (2) © 2019 Magnolia Press
Phylogenetic analyses. Our Bayesian and Maximum Likelihood analyses recovered monophyly and identical to-
pologies for Sigalegalephrynus, with high support values (Fig. 1). Our phylogenetic analyses recovered two distinct
clades, a northern clade that contains two undescribed new species, and a southern clade containing S. mandai-
linguensis, S. minangkabauensis, and a third undescribed species. Uncorrected pairwise interspecific distances in
the mitochondrial ribosomal gene 16S rRNA fragment range from 4.0 to 10.4%, with significant divergence be-
tween the northern and southern clades, 8.2–10.4%, and moderate divergence within clades, 4.0–6.0% (Table 2).
Morphological characters also support a north/south clade division. Characters that define the southern clade in-
clude: (1) moderately mucronated (presence of rostral keel) snout in dorsal profile (vs truncated in northern clade),
(2) body and limbs lanky (vs stocky in northern clade), (3) presence of distinct hourglass shape marking on dorsum
(vs absent in northern clade), (4) body tubercles spinose (vs round in northern clade), (5) large tubercles on posterior
of tympanum spinose (vs round in northern clade), (6) tympanum without elevated annulus (vs elevated annulus in
northern clade), and (7) lore with distinct white marking at sides (vs absent white bordering markings in northern
clade).
FIGURE 1. Estimated phylogeny of Sigalegalephrynus based on 16S mitochondrial rRNA, depicted as a maximum-likelihood
tree with bufonid outgroups. The non-bufonid outgroup—Dryophytes arenicolor is not shown.
Systematics
Sigalegalephrynus burnitelongensis sp. nov.
Figs. 2A–C, 4A, 5A, 6A
Holotype. Museum Zoologicum Bogoriense of Amphibian Collection, MZB.Amph.30413 (field number ENS
18884), an adult male. Collected from a stream of Gunung Burni Telong near Desa (Village) Rambune, Keca-
matan (Subdistrict) Timang Gajah, Kabupaten (Regency) Bener Meriah, Province of Aceh, Indonesia. 4.76455ºN,
96.80138ºE, 1519 m a.s.l (Fig. 3). Collected by Goutam C. Sarker, Irvan Sidik, Syaripudin and Muhammad Ikhsan
on 9 August 2015 at 00:30h.
SIGALEGALEPHRYNUS, THE PUPPET TOADS OF SUMATRA Zootaxa 4679 (2) © 2019 Magnolia Press · 371
TABLE 2. Uncorrected P-distances between sequences based on 608 bp of 16S rRNA gene (percentages of base differences per site) (shaded regions represent intra-Group di-
vergence and bold cells represent divergence between the southern and northern Groups).
1234567891011
1Ansonia hanitschi (VUB 0615)
2Ansonia leptopus (VUB 0632) 9.2
3Ansonia sp. (UTA A-65475) 8.5 2.8
4Ansonia spinulifer (VUB 0647) 9.5 10.0 11.0
5Duttaphrynus melanostictus (UTA A-65510) 10.0 10.6 11.1 12.6
6Duttaphrynus melanostictus (UTA A-63417) 10.0 10.6 11.1 12.6 0.0
7Duttaphrynus melanostictus (UTA A-65511) 10.0 10.6 11.1 12.6 0.0 0.0
8Ingerophrynus biporcatus (UTA A-53730) 9.8 11.2 11.5 11.8 10.3 10.3 10.3
9Ingerophrynus divergens (UTA A-65486) 12.6 12.8 12.4 13.7 10.5 10.5 10.5 8.2
10 Leptophryne borbonica (UTA A-62486) 12.3 13.3 12.1 13.0 11.8 11.8 11.8 11.5 13.4
11 Leptophryne cruentata (UTA A-62523) 14.4 16.0 15.8 15.2 13.4 13.4 13.4 13.6 13.9 12.2
12 Pelophryne misera (VUB 0641) 10.5 11.8 11.6 13.3 9.4 9.4 9.4 11.5 13.8 13.2 16.1
13 Pelophryne signata (VUB 0583) 10.2 10.5 10.5 12.0 10.7 10.7 10.7 11.1 14.0 10.2 15.7
14 Pelophryne sp. (UTA A-65485) 10.7 12.3 12.1 12.5 12.2 12.2 12.2 11.2 14.1 11.5 15.8
15 Phrynoidis asper (UTA A 63413) 12.2 10.6 11.1 11.3 9.0 9.0 9.0 10.8 11.6 11.7 12.5
16 Phrynoidis asper (UTA A 63410) 11.7 10.8 11.4 11.5 9.5 9.5 9.5 11.2 11.8 12.5 13.3
17 Phrynoidis juxtasper (VUB 0649) 8.5 9.0 9.1 11.0 8.0 8.0 8.0 9.9 10.0 10.9 11.8
18 Pseudobufo subasper (UTA A-63763) 10.7 11.5 11.7 13.0 9.5 9.5 9.5 10.2 11.5 10.7 14.5
19 Pseudobufo subasper (UTA A-63764) 10.7 11.5 11.7 13.0 9.5 9.5 9.5 10.2 11.5 10.7 14.5
20 Pedostibes hosii (BORNEENSIS 22088) 8.0 11.3 10.8 11.4 9.0 9.0 9.0 10.7 13.3 10.2 13.0
21 Sabahphrynus maculatus (BORNEENSIS 08425) 9.8 12.1 10.9 11.3 8.8 8.8 8.8 9.2 9.1 10.5 12.4
22 Sigalegalephrynus burnitelongensis sp. nov. (UTA A-65492) 12.8 14.2 15.1 13.3 11.6 11.6 11.6 13.1 12.7 12.7 14.3
23 Sigalegalephrynus burnitelongensis sp. nov. (MZB.Amph.30413) 12.8 14.2 15.1 13.3 11.6 11.6 11.6 13.1 12.7 12.7 14.3
24 Sigalegalephrynus gayoluesensis sp. nov. (UTA A-65490) 12.6 12.9 14.0 13.6 12.3 12.3 12.3 12.6 13.8 14.0 15.1
25 Sigalegalephrynus gayoluesensis sp. nov. (MZB.Amph.30411) 12.6 12.9 14.0 13.6 12.3 12.3 12.3 12.6 13.8 14.0 15.1
26 Sigalegalephrynus harveyi sp. nov. (MZB.Amph.30412) 9.7 11.0 9.8 11.4 8.7 8.7 8.7 10.0 11.3 9.2 11.7
27 Sigalegalephrynus harveyi sp. nov. (UTA A-65474) 9.7 11.0 9.8 11.4 8.7 8.7 8.7 10.0 11.3 9.2 11.7
28 Sigalegalephrynus mandailinguensis (MZB.Amph.25736) 11.4 10.7 11.0 11.6 9.0 9.0 9.0 10.2 10.8 9.3 12.2
29 Sigalegalephrynus mandailinguensis (UTA A-63562) 11.4 10.7 11.0 11.6 9.0 9.0 9.0 10.2 10.8 9.3 12.2
30 Sigalegalephrynus minangkabauensis (MZB.Amph.25738) 12.4 12.8 11.8 13.2 10.5 10.5 10.5 12.9 13.3 10.1 13.3
31 Atelopus flavescens (BPN 726) 16.0 13.8 13.0 15.1 15.4 15.4 15.4 13.5 16.1 15.3 17.3
32 Dryophytes arenicolor (TNHC 61118 (VUB 1052) 14.5 17.1 17.2 15.6 12.6 12.6 12.6 12.6 15.6 16.3 17.3
......continued on the next page
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TABLE 2. (Continued)
12 13 14 15 16 17 18 19 20 21
1Ansonia hanitschi (VUB 0615)
2Ansonia leptopus (VUB 0632)
3Ansonia sp. (UTA A-65475)
4Ansonia spinulifer (VUB 0647)
5Duttaphrynus melanostictus (UTA A-65510)
6Duttaphrynus melanostictus (UTA A-63417)
7Duttaphrynus melanostictus (UTA A-65511)
8Ingerophrynus biporcatus (UTA A-53730)
9Ingerophrynus divergens (UTA A-65486)
10 Leptophryne borbonica (UTA A-62486)
11 Leptophryne cruentata (UTA A-62523)
12 Pelophryne misera (VUB 0641)
13 Pelophryne signata (VUB 0583) 6.5
14 Pelophryne sp. (UTA A-65485) 7.0 4.7
15 Phrynoidis asper (UTA A 63413) 12.0 13.2 13.3
16 Phrynoidis asper (UTA A 63410) 12.7 14.2 14.1 1.5
17 Phrynoidis juxtasper (VUB 0649) 11.4 11.6 11.7 5.8 5.1
18 Pseudobufo subasper (UTA A-63763) 13.8 13.7 14.1 9.7 9.4 9.9
19 Pseudobufo subasper (UTA A-63764) 13.8 13.7 14.1 9.7 9.4 9.9 0.0
20 Pedostibes hosii (BORNEENSIS 22088) 10.2 11.6 12.4 10.9 10.9 9.9 10.2 10.2
21 Sabahphrynus maculatus (BORNEENSIS 08425) 11.0 11.4 11.0 11.3 11.9 9.3 9.2 9.2 9.5
22 Sigalegalephrynus burnitelongensis sp. nov. (UTA A-65492) 12.2 12.2 12.8 11.2 11.7 12.0 12.3 12.3 11.4 13.1
23 Sigalegalephrynus burnitelongensis sp. nov. (MZB.Amph.30413) 12.2 12.2 12.8 11.2 11.7 12.0 12.3 12.3 11.4 13.1
24 Sigalegalephrynus gayoluesensis sp. nov. (UTA A-65490) 12.6 14.1 14.2 10.7 11.3 11.3 11.8 11.8 12.0 13.1
25 Sigalegalephrynus gayoluesensis sp. nov. (MZB.Amph.30411) 12.6 14.1 14.2 10.7 11.3 11.3 11.8 11.8 12.0 13.1
26 Sigalegalephrynus harveyi sp. nov. (MZB.Amph.30412) 10.7 12.1 12.2 7.8 8.0 8.2 9.2 9.2 7.5 8.8
27 Sigalegalephrynus harveyi sp. nov. (UTA A-65474) 10.7 12.1 12.2 7.8 8.0 8.2 9.2 9.2 7.5 8.8
28 Sigalegalephrynus mandailinguensis (MZB.Amph.25736) 11.1 11.3 11.7 7.3 8.2 7.0 10.1 10.1 9.6 10.4
29 Sigalegalephrynus mandailinguensis (UTA A-63562) 11.1 11.3 11.7 7.3 8.2 7.0 10.1 10.1 9.6 10.4
30 Sigalegalephrynus minangkabauensis (MZB.Amph.25738) 11.9 12.6 12.9 8.5 9.0 9.2 10.7 10.7 9.6 11.0
31 Atelopus flavescens (BPN 726) 17.9 16.7 16.7 13.0 13.8 12.5 17.1 17.1 16.2 13.8
32 Dryophytes arenicolor (TNHC 61118 (VUB 1052) 16.7 16.0 15.8 12.9 14.3 14.1 12.9 12.9 14.8 14.3
......continued on the next page
SIGALEGALEPHRYNUS, THE PUPPET TOADS OF SUMATRA Zootaxa 4679 (2) © 2019 Magnolia Press · 373
TABLE 2. (Continued)
22 23 24 25 26 27 28 29 30 31
1Ansonia hanitschi (VUB 0615)
2Ansonia leptopus (VUB 0632)
3Ansonia sp. (UTA A-65475)
4Ansonia spinulifer (VUB 0647)
5Duttaphrynus melanostictus (UTA A-65510)
6Duttaphrynus melanostictus (UTA A-63417)
7Duttaphrynus melanostictus (UTA A-65511)
8Ingerophrynus biporcatus (UTA A-53730)
9Ingerophrynus divergens (UTA A-65486)
10 Leptophryne borbonica (UTA A-62486)
11 Leptophryne cruentata (UTA A-62523)
12 Pelophryne misera (VUB 0641)
13 Pelophryne signata (VUB 0583)
14 Pelophryne sp. (UTA A-65485)
15 Phrynoidis asper (UTA A 63413)
16 Phrynoidis asper (UTA A 63410)
17 Phrynoidis juxtasper (VUB 0649)
18 Pseudobufo subasper (UTA A-63763)
19 Pseudobufo subasper (UTA A-63764)
20 Pedostibes hosii (BORNEENSIS 22088)
21 Sabahphrynus maculatus (BORNEENSIS 08425)
22 Sigalegalephrynus burnitelongensis sp. nov. (UTA A-65492)
23 Sigalegalephrynus burnitelongensis sp. nov. (MZB.Amph.30413) 0.0
24 Sigalegalephrynus gayoluesensis sp. nov. (UTA A-65490) 5.1 5.1
25 Sigalegalephrynus gayoluesensis sp. nov. (MZB.Amph.30411) 5.1 5.1 0.0
26 Sigalegalephrynus harveyi sp. nov. (MZB.Amph.30412) 9.2 9.2 8.2 8.2
27 Sigalegalephrynus harveyi sp. nov. (UTA A-65474) 9.2 9.2 8.2 8.2 0.0
28 Sigalegalephrynus mandailinguensis (MZB.Amph.25736) 9.3 9.3 8.9 8.9 4.0 4.0
29 Sigalegalephrynus mandailinguensis (UTA A-63562) 9.3 9.3 8.9 8.9 4.0 4.0 0.0
30 Sigalegalephrynus minangkabauensis (MZB.Amph.25738) 10.4 10.4 10.4 10.4 4.7 4.7 6.0 6.0
31 Atelopus flavescens (BPN 726) 17.4 17.4 18.0 18.0 14.3 14.3 13.5 13.5 16.8
32 Dryophytes arenicolor (TNHC 61118 (VUB 1052) 15.9 15.9 14.9 14.9 13.7 13.7 14.5 14.5 15.6 15.5
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FIGURE 2. Lateral, dorsal, and ventral views of specimens of Sigalegalephrynus in life. Holotypes of S. burnitelongensis sp.
nov. (A–C, MZB.Amph.30413, SVL 22.18 mm), S. gayoluesensis sp. nov. (D–F, MZB.Amph.30411, SVL 26.49 mm), S. man-
dailinguensis (G–I, MZB.Amph.25736, SVL 38.01 mm), S. minangkabauensis (J–L, MZB.Amph.25738, SVL 19.32 mm), and
S. harveyi sp. nov. (M–O, MZB.Amph.30412, SVL 26.36 mm).
SIGALEGALEPHRYNUS, THE PUPPET TOADS OF SUMATRA Zootaxa 4679 (2) © 2019 Magnolia Press · 375
Paratypes (2). The University of Texas at Arlington Amphibian collection numbers UTA A-65788 and UTA
A-65492, adult males. Collected from near to the collection locality of the holotype, 4.76455ºN, 96.80138ºE, 1519
m a.s.l. (Fig. 3). Collected by Goutam C. Sarker, Irvan Sidik, Syaripudin and Muhammad Ikhsan on 8 August 2015
at 23:50h.
Referred specimens (33). All juveniles, UTA A−65493−509 (17), and MZB.Amph.26016−031 (16), same col-
lection information as the types.
Etymology. The specific epithet is an adjective in Aceh language derived from Burni, meaning Mountain
(Gunung in Indonesian) and Telong, meaning burning (Bakar in Indonesian), or in Sanskrit Borni Təloŋ, meaning
“burning mountain”. This is the local name for the volcano that is the type-locality of this new species, and the Latin
suffix –ensis, denoting place.
Suggested Common Name. Burning Mountain Puppet Toad, in English; Kodok-wayang burnitelong, in Indo-
nesian.
Diagnosis. Sigalegalephrynus burnitelongensis sp. nov. can be diagnosed from its congeners by a unique com-
bination of characters: (1) small-size (males 21.73–23.06 mm SVL); (2) lacking parotoid glands; (3) tympanum
visible, with elevated annulus not encircled by sharply raised spinose tubercles; (4) naris closer to tip of snout than
to eye; eye-naris distance 6.3% (8.3%, 6.9%) of SVL; naris-snout distance 1.1 % (1.2% 1%) of SVL, (5) fingertips
truncated but not expanded (except finger I); (6) tips of toe I, II and III rounded, truncated but not expanded on toe
IV and V; (7) rudimentary webbing in hands, moderate in feet; (8) dorsum brown without any marking; (9) medial
dorsal dark band absent; (10) lacking alternate dark brown and white markings on upper lip, or not prominent; (11)
flanks lacking stroke of different color; (12) dorsum lightly tuberculate, tubercles round; (13) venter pinkish–yel-
low, without maculation and uniformly tuberculate, (14) interocular distance 44% (43%) of head width; (15) nuptial
pads dark brown, with black–tipped spicules; (16) finger IV tip not reaching distal phalangeal articulation of finger
III (when adpressed); (17) inner metacarpal tubercle ¾ of outer metacarpal tubercle in length.
Description of holotype and variation of paratypes (in parenthesis). Body moderately robust; head slightly
longer than wide, HL/HW = 1.03 (1.10, 1.02); head length 32% (32%, 31%) of SVL; head width 31% (29%,
31%) of SVL; snout length 11% (10, 11%) of SVL; canthus rostralis concave; loreal area slightly tuberculate and
concave; eye length 10% (9%, 10%) of SVL; pupil circular; snout truncate in dorsal view and protruding (slightly
sloping back towards mouth) in lateral view; tympanum round with distinct annulus; interorbital space flat; cranial
crests absent; no teeth in jaws; tongue tip oval shaped and longer than wide; skin of dorsal surfaces slightly rough
to finely shagreen, with few large, scattered, round tubercles; most tubercles small, almost without keratinization;
no dorsolateral, paravertebral, or occipital folds; skin on venter smoother, with very small and round tubercles;
circumcloacal region golden yellow.
Arms robust, with moderately developed axillary membrane; forearm length 27% (27%, 26%) of SVL; hand
length 27% (24%, 26%) of SVL; relative length of fingers: I < II < IV < III; fingers bearing large expanded pads;
webbing formula for hand: I11/2-2II11/2-23/4III23/4-22/3IV (I1-1II3-23/4III 21/2-2IV); skin of forearm with tu-
bercles; finger I with elongate inner metacarpal tubercle, smaller than the outer metacarpal tubercle; each finger
with one poorly developed round subarticular tubercle; nuptial pads brownish-dark, glandular, and dorsomedially
extended with black keratinized spicules present at the base of finger I.
Thigh length 44% (43%, 43%) of SVL; tibia length 41% (41%, 40%) of SVL; tarsal length 21% (21%, 24%)
of SVL; foot length 41% (37%, 41%) of SVL; relative lengths of toes—I< II< III<V< IV; toes bearing large pads;
feet with moderate webbing (Fig. 6A), webbing formula for the feet: I0-11/2II0-2III11/2-3IV3-2V (I1-11/2II2-
2III3-3IV2-11/2V); heels without tubercles; inner metatarsal tubercle moderately developed and elongate; outer
metatarsal tubercle distinct; one moderate subarticular tubercle present at the base of first phalanx on each toe; toes
with toe pads.
Measurements (in mm). Holotype followed by paratypes in parenthesis. Finger III of right hand of paratype
deformed, finger measurements of this specimen taken on left hand. SVL 22.18 (21.73, 23.06); HL 7.06 (6.96,
7.20); HW 6.84 (6.31, 7.04); SNL 2.40 (2.20, 2.45); ICD 3.70 (3.50, 3.80); IND 1.89 (1.91, 1.93); END 1.4 (1.80,
1.6); NSD 0.25 (0.26, 0.23); IOD 3.00 (3.10, 3.00); EL 2.20 (2.00, 2.25); TML 1.4 (1.45, 1.2); FAL 6.04 (5.90,
6.10); HAL 6.00 (5.30, 6.00); THL 9.70 (9.28, 9.82); TBL 9.09 (8.97, 9.24); TRL 4.55 (4.50, 5.51); FTL 9.00 (7.98,
9.34); OMCL 1.00 (1.00, 1.00); OMCW 1.00 (1.00, 1.00); IMCL 0.55 (0.50, 0.50); IMCW 0.75 (0.75, 0.75); IMTL
1.5(1.00, 0.90); IMTW 1.0(0.70, 0.80); F1L 0.80 (1.00, 1.00); F2L 1.60 (2.00, 2.00); F3L 3.15 (3.50, 3.50); F4L 2.10
(2.50, 2.50); T1L 1.00 (1.00, 1.00); T2L (1.40, 1.40); T3L 1.80 (2.00, 2.00); T4L 5.00 (4.00, 4.60); T5L 3.50 (3.0,
3.00); F3PD 0.90 (0.80, 1.00); F3PB 0.80 (0.60, 0.75).
SARKER ET AL.
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Color of holotype in life. Adult male holotype (Figs. 2A, 2B, 2C): dorsum predominantly light brown, lack-
ing distinct markings; flanks brown, lacking oblique stripes; infraorbital part of maxilla with light-brown marking;
lore light brown, with small dark-brown spot between orbit and naris; dorsum of limbs brown, lacking distinctive
crossbar markings; moderately large white tubercles at posterior mandibular articulation; abdominal surface pink,
with many yellow blotches; gular region, clavicular, and ventral surface of limbs pink, without yellow blotches; tips
of fingers and toes blackish, with golden yellow blotches; iris golden yellow, with heavy black reticulations.
Color of holotype in preservative. Differing slightly from that in life, pinkish coloration turned grey, and
venter has turned whitish grey.
Comparisons. Sigalegalephrynus burnitelongensis sp. nov. is restricted to Gunung Burni Telong, a volcano in
Bener Meriah regency, Sumatra. Sigalegalephrynus burnitelongensis sp. nov. can be easily distinguished from all
other congeners (including S. gayoluesensis sp. nov. from Gayo Lues Regency) by the lack of crossbar markings on
the dorsal surface of the limbs. It differs from S. mandailinguensis, S. minangkabauensis and S. harveyi sp. nov. by
its truncate (vs. mucronate) shaped snout in dorsal profile, stocky limbs (vs. lanky) smooth tubercles (vs. warty with
sharp tips), and lacking an hourglass mark on the dorsum (vs. hourglass present).
FIGURE 3. Map of Sumatra showing the known distribution of Sigalegalephrynus species.
SIGALEGALEPHRYNUS, THE PUPPET TOADS OF SUMATRA Zootaxa 4679 (2) © 2019 Magnolia Press · 377
Distribution and natural history. Sigalegalephrynus burnitelongensis sp. nov. is known only from forest
patches associated to small streams and surrounded by coffee plantations, at Gunung Burni Telong, near the village
of Rambune in the province of Aceh, from 1519 m a.s.l. (Fig. 3). The holotype and paratype were found sitting on
small leaves of shrubs 20 cm above ground. The holotype weighed 0.76 g, and the paratype 0.69 g. The smallest
juvenile collected (UTA A-65505) was 9.6 mm in SVL and 0.06 g in weight.
Sigalegalephrynus gayoluesensis sp. nov.
Figs. 2D–F, 4B, 5B, 6B
Holotype. Museum Zoologicum Bogoriense of Amphibian Collection, MZB.Amph.30411 (field number ENS
19527). An adult male from above the Desa (Village) Kenyaran Pantan Cuaca, Kabupaten (Regency) Gayo Lues,
Provinsi Aceh, Indonesia, 4.22588ºN, 97.18915ºE, 1850 m. a.s.l. (Fig. 3). Collected by Elijah Wostl, Ahmad Muam-
mar Khadafi, and Syaripudin on 9 August 2015 at 21:20h.
Paratypes (3). The University of Texas at Arlington Amphibian collection number UTA A-65490, Museum
Zoologicum Bogoriense of Amphibian Collections, MZB.Amph.26035, adult males; MZB.Amph.26037, adult fe-
male. Collected from near to the collection locality of the holotype, 4.22580ºN, 97.1886º1E, 1844 m. a.s.l. (Fig. 3).
Collected by Elijah Wostl, Ahmad Muammar Khadafi, and Syaripudin on 9 August 2015 at 21:05h.
Referred specimens (8). Collection locality very close to the types. UTA A-65488−489, 65789 (subadult and
two juveniles, respectively, 1827 m. a.s.l., 4.2239ºN, 97.18718ºE); 65790 (subadult, 1826 m. a.s.l., 4.22487ºN,
97.18769ºE); and MZB.Amph. 26032 (juvenile, 1827 m. a.s.l., 4.22357ºN, 97.186551º E); 26033 (juvenile,1827 m.
a.s.l., 4.2239ºN, 97.18718ºE); 26034, 26036 (two juveniles,1826 m. a.s.l., 4.22487ºN, 97.18769ºE).
Etymology. The specific epithet refers to the Gayo Lues Highlands, where this new species was found.
Suggested Common name. Gayo Lues Highland’s Puppet Toad; Indonesia name: Kodok-wayang gayolues
Diagnosis. Sigalegalephrynus gayoluesensis sp. nov. can be identified from its congeners by a unique combi-
nation of characters: (1) medium-size (adult males 25.65–26.49 mm SVL); (2) lacking parotoid glands; (3) tympa-
num visible, with elevated annulus, and not encircled by sharply raised spinose tubercles; (4) naris closer to tip of
snout than to eye; eye-naris distance 6.4.0% (7%) of SVL; naris-snout distance 1% (1.9%) of SVL; (5) fingertips
truncated and expanded (except finger I); (6) tips of toe I, II and III are rounded; tips of toes IV and V truncated but
not expanded; (7) rudimentary webbing in hands, moderate in feet; (8) adult male dorsal coloration dark brown,
with prominent whitish diamond shaped suprascapular marking; (9) dorsum lacking medial dark band; (10) upper
lip with prominent alternating dark brown and white marks; (11) flanks with stroke of dark brown (demarcated by
thin white lines on top and bottom), extending from orbit to inguinal area; (12) dorsal surface lightly tuberculate,
with round tubercles; (13) venter pinkish–white, with black maculation; (14) interocular distance 43% (44%) of
head width; (15) nuptial pads dark brown, with black–tipped spicules; (16) finger IV tip extending beyond distal
(terminal) phalangeal articulation of finger III (when adpressed); (17) inner metacarpal tubercle ¾ length to outer
metacarpal tubercle.
Description of holotype and variation of paratypes (in parenthesis). Body moderately robust; head longer
than wide, HL/HW =1.14 (1.11, 1.07, 1.02); head length 33% (34%, 31%, 34%) of SVL; head width 29% (31%,
29%, 33%) of SVL; snout length 10% (10%, 10%, 11%) of SVL; canthus rostralis concave; loreal area without tu-
bercles, concave; eye length 10% (12%, 10%, 9%) of SVL; pupil circular; snout truncate in dorsal view, protruding
in lateral view, sloping back towards mouth; tympanum distinct and rounded, with annulus, but not surrounded by
large tubercles; interorbital space flat; cranial crests absent; no teeth in jaws; tongue tip oval shaped and longer than
wide; skin of dorsum finely shagreened, with few large and scattered tubercles; tubercles rounded, without kerati-
nization; no dorsolateral, paravertebral, or occipital folds; skin on venter smooth with anastomosis; circumcloacal
region is golden yellow.
Arms robust; forearm length 31% (33%, 25%, 26%) of SVL; hand length 30% (31%, 26%, 27%) of SVL;
relative length of Finger—I<II<IV<III; fingertips truncated and dilated; hands rudimentary webbed, hand webbing
formula: I0-11/2II1-21/2III21/2-21/3IV (I[0]-[12/3–2]II[1–11/2]-[2–21/2]III[2–21/2]-[2–21/2]IV); skin of forearm
with moderately developed tubercles; finger I with moderately developed inner metacarpal tubercle, smaller than
the outer metacarpal tubercle; each finger with one poorly developed round subarticular tubercle; nuptial pads
brownish-dark, glandular, dorsomedially extended; spicules of nuptial pads with black keratinized spicules.
SARKER ET AL.
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Thigh length 45% (44%, 44%, 44%) of SVL; tibia length 40% (43%, 39%, 41%) of SVL; tarsal length 25%
(25%, 21%, 20%) of SVL; foot length 41% (42%, 42%, 39%) of SVL; relative lengths of toes—I< II< III<V<IV;
toes bearing large pads; feet with moderate webbing (Fig. 6B), webbing formula for the feet: I0-1/2II0-1III1-
21/2IV23/4-2V (I[0]-[0–1/2]II[0]-[1]III[0–1/2]-[21/2]IV[21/2]-[12/3–2]V); heels without tubercles; inner and outer
metatarsal tubercle moderately developed and elongate.
Measurements (in mm). Holotype followed by paratype in parenthesis: SVL 26.49 (25.65, 26.07, 27.36); HL
8.72 (8.84, 8.06, 9.20); HW 7.67 (7.98, 7.53, 9.0); SNL 2.75 (2.5, 2.55, 3.0); ICD 4.30 (4.50, 4.50, 4.56); IND 2.20
(1.80, 2.0, 2.0); END 1.7 (1.8, 1.55, 2.12); NSD 0.25 (0.5, 0.5, 0.7); IOD 3.0 (3.5, 3.5, 4.0); EL 2.70 (3.0, 2.55, 2.55);
TML 1.50 (1.55, 1.6, 1.47); FAL 8.24 (8.40, 6.5, 6.5); HAL 7.89 (7.86, 6.67, 7.5); THL 11.83 (11.34, 11.53, 12.07);
TBL 10.68 (10.95, 10.29, 11.23); TRL 6.63 (6.48, 5.50, 5.50); FTL 10.83 (10.86, 10.90, 10.80); OMCL 1.0 (1.0,
10, 1.0); OMCW 1.0 (1.0, 1.0 1.0, 1.0); IMCL 0.75 (0.75, 0.65, 0.60); IMCW 0.50 (0.50, 0.50); IMTL 1.0 (1.0, 1.0,
1.0); IMTW 1.0 (1.0, 1.0, 1.0); F1L 1.5 (1.5, 1.5, 1.5); F2L 2.30 (2.25, 2.35 2.45); F3L 4.0(3.5, 3.5, 3.2); F4L 3.5
(3.0, 2.6, 2.55); T1L 2.0 (1.5, 1.5, 1.6); T2L 2.5 (2.0, 2.0, 2.0); T3L 3.2 (3.0, 3.3, 2.5); T4L 5.5 (5.0, 5.0, 4.5); T5L
4.0 (3.5, 3.5, 3.3); F3PD 1.25 (1.2, 1.0, 1.3); F3PB 1.0 (1.0, 0.9, 1.0 ).
FIGURE 4. Dorsal (top) and ventral (bottom) aspects of Sigalegalephrynus specimens in alcohol (Scale bar = 5 mm). Holotypes
of Sigalegalephrynus burnitelongensis sp. nov. (A, MZB.Amph.30413), S. gayoluesensis sp. nov. (B, MZB.Amph.30411), S.
mandailinguensis (C, MZB.Amph.25736), S. minangkabauensis (D, MZB.Amph.25738), and S. harveyi sp. nov. (E, MZB.
Amph.30412).
Color of holotype in life. (Figs. 2D, 2E, 2F). Dorsum predominantly brown, with suprascapular dark brown
diamond-shaped marking encircled by light brown; flanks with alternate wide dark brown and narrow white stripes;
wide whitish light-brown spot below eye; lore dark brown, with small light brown spot adjacent to anterior of or-
bit; iris golden yellow, heavily reticulated; dorsum of limbs dark brown, with dark-brown crossbars; large white
tubercles present at point of posterior mandibular articulation; abdominal surface pink, with dark brown maculation;
throat pinkish, with no maculation; underside of limbs pink, with dark brown maculation; iris golden yellow, with
black reticulations.
Color of holotype in preservative. In alcohol, pinkish coloration turned grey and venter whitish grey, macu-
lated with dark brown blotches.
Advertisement call. The call of the male holotype was recorded in the field and before collection. Ambient
temperature at the time of recording was 17.2 ºC. The call is composed of 179 highly modulated notes given 0.245
seconds apart, on average (range, 0.140–0.907 seconds, SD ± 0.148 seconds). On average, each note is 0.049 sec-
onds (range, 0.24–0.93, SD ± 0.18 seconds) in length and is composed of one distinct pulse. The average fundamen-
tal and dominant frequencies of the vocalization are 2474.361 (range, 2368.652–2627.051 Hz, SD ± 85.86 Hz) Hz
and 4948.722 Hz (range, 4737.305–5254.102 Hz, SD ±171.7309 Hz) respectively (Fig. 7).
Comparisons. Sigalegalephrynus gayoluesensis sp. nov. is likely restricted to the mountains of the Gayo Lues
Regency of Aceh, Sumatera, and does not exist in sympatry with any other congener. Sigalegalephrynus gayolue-
sensis sp. nov. can be easily distinguished from S. mandailinguensis, S. minangkabauensis and S. harveyi sp. nov.
SIGALEGALEPHRYNUS, THE PUPPET TOADS OF SUMATRA Zootaxa 4679 (2) © 2019 Magnolia Press · 379
by its smooth tubercles on the body (vs. sharp-tipped warty tubercles) and a diamond shaped marking on the dorsum
(vs. hourglass in S. mandailinguensis, S. minangkabauensis and S. harveyi sp. nov., no hourglass or diamond shape
mark in S. burnitelongensis sp. nov.). Sigalegalephrynus gayoluesensis sp. nov. can also be distinguished from S.
burnitelongensis sp. nov. by its black anastomotic maculated throat and abdomen (vs immaculate throat and abdo-
men).
Acoustic data is limited for Sigalegalephrynus species, the call of the holotype of S. gayoluesensis sp. nov., dif-
fers from that of S. mandailinguensis in duration (46.448 s vs 17.27 s), total number of notes (179 vs 62), notes per
second (4 vs 6–7), average note length (0.49 s vs 0.029 s), average pause length between notes (0.245 s vs 0.012 s),
and dominant frequency (4948.722 Hz vs 3400 Hz) (Fig 5).
Distribution and natural history. Sigalegalephrynus gayoluesensis sp. nov. is known only from rain for-
est flanking a stream adjacent to the Takengon-Blangkejeren road above the village Kenyaran Pantan Cuaca, in
the Gayo Lues Regency of the province of Aceh, between 1787 and 1796 m a.s.l. (Fig. 3). Both the holotype and
paratype were found calling on broad smooth leaves, at 1.6 m and 3.8 m above ground, respectively. The call of
the holotype was recorded. The call sounded similar to that of S. mandailinguensis at the time of recording. Both
the holotype and paratype weighed 1.27 g. Our smallest juvenile of this species (UTA A-65789) was less than 1 cm
(SVL 8.0 mm) in SVL and weighed 0.05 g.
FIGURE 5. Dorsal (top) and lateral (middle) profiles of Sigalegalephrynus specimens in alcohol (Scale bar = 5 mm). Head,
and upper surface of hand (bottom) of holotypes of Sigalegalephrynus burnitelongensis sp. nov. (A, MZB.Amph.30413), S.
gayoluesensis sp. nov. (B; MZB.Amph.30411), S. mandailinguensis (C, MZB.Amph.25736), S. minangkabauensis (D, MZB.
Amph.25738), and S. harveyi sp. nov. (E, MZB.Amph.30412).
Sigalegalephrynus harveyi sp. nov.
Figs. 2M–O, 4E, 5E, 6E
Holotype. Museum Zoologicum Bogoriense of Amphibian Collection, MZB.Amph.30412 (field number ENS
18377). An adult male from Gunung Dempo above the Desa (Village) Kampung Empat, Kabupaten (Regency)
Pagar Alam, Provinsi Sumatera Selatan, Sumatra, Indonesia, 4.040980ºS, 103.1481ºE, 1826 m a.s.l. (in all cases,
datum = WGS84) (Fig. 3). Collected by Michael B. Harvey, Farits Alhadi, and Panupong Thammachoti on 8 July
2015, at 21:35h.
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Paratype. The University of Texas at Arlington Amphibian Collection UTA A-65474, an adult male. Collected
from near to the collection locality of the holotype, 4.03923ºS, and 103.1473ºE, 1878 m a.s.l (Fig 3). Collected by
Michael B. Harvey, Panupong Thammachoti, and Gilang Pradana on 10 July 2015, at 20:55h.
Etymology. The specific epithet is a patronym in honor of Michael B. Harvey, one of the collectors of this new
species, a friend, an outstanding herpetologist, and the co-Principal Investigator of the National Science Foundation
(NSF) project that has contributed this and a significant number of other papers on the herpetofauna of Sumatra.
Suggested Common Name. Harvey’s Puppet Toad, in English; Kodok-wayang Harvey, in Indonesian.
Diagnosis. Sigalegalephrynus harveyi sp. nov. can be identified from its congeners by a unique combination of
characters: (1) medium-sized (adult males 26.36–28.09 mm SVL) Sigalegalephrynus; (2) lacking parotoid glands;
(3) tympanum visible, with elevated annulus encircled with sharply raised spinose tubercles; (4) naris closer to tip of
snout than to eye; eye-naris distance 8.0% (9.3%) of SVL; naris-snout distance 2.8 % (2.1%) of SVL; (5) fingertips
truncated (except finger I), but not expanded; (6) tips of toes I, II, III and V rounded, toe IV tip truncated, but not
expanded; (7) webbing rudimentary in hands, moderate in feet; (8) dorsal coloration in adult males light brown,
with a prominent hourglass shaped marking; (9) dorsum, lacking medial dark band; (10) prominent alternate dark
brown and white marks on upper lip; (11) flanks with dark brown strokes (demarcated by thin white lines on top
and bottom), extending from orbit to inguinal area; (12) dorsal surface very lightly tuberculate, with white tipped
spinose tubercles; (13) venter golden–yellow, without dark maculation; (14) interocular distance 48% (52%) of head
width; (15) nuptial pads white, with white–tipped spicules; (16) finger IV tip touches distal phalangeal articulation
of finger III (when adpressed); (17) inner metacarpal tubercle equal in length to outer metacarpal tubercle.
FIGURE 6. Palmar and plantar surfaces of Sigalegalephrynus specimens in alcohol (Scale bar = 5 mm). Holotypes of Sigalega-
lephrynus burnitelongensis (A, MZB.Amph.30413), S. gayoluesensis sp. nov. (B, MZB.Amph.30411), S. mandailinguensis (C,
MZB.Amph.25736), S. minangkabauensis (D, MZB.Amph.25738), and S. harveyi sp. nov. (E, MZB.Amph.30412).
Description of holotype and variation in paratype (in parenthesis). Body slender; head longer than wide,
HL/HW 1.11 (1.14); head length 30% (33%) of SVL; head width 27.0% (29%) of SVL; snout length 13% (14%)
of SVL; canthus rostralis concave; loreal area smooth and concave; eye length 10% (10%) of SVL; pupil circular;
snout slightly sloping back, towards mouth; snout mucronate, with prominent median keel, protruding in lateral
view; tympanum distinct, rounded, with moderately developed annulus; interorbital space flat; cranial crests absent;
jaws toothless; tongue tip oval shaped and longer than wide; dorsal skin tuberculate and rough, with mostly small
and white tipped tubercles, lacking black keratinization; tympanum with elevated and distinct annulus, circled by
SIGALEGALEPHRYNUS, THE PUPPET TOADS OF SUMATRA Zootaxa 4679 (2) © 2019 Magnolia Press · 381
large tubercles; no dorsolateral, paravertebral, or occipital folds; throat golden yellow; venter pinkish and golden-
yellow, areolate in texture; circumcloacal region brownish yellow.
Arms lanky, with poorly developed axillary membranes; forearm length 28% (28%) of SVL; hand length 27%
(28%) of SVL; relative length of fingers I < II < IV < III; fingertips truncated but not expanded; fingers bearing
moderate pads; hands rudimentary webbed, hand webbing formula: I13/4-2II13/4-3III3-3IV (I13/4-2II13/4-3III3-
3IV); flanks and dorsal surface of forearms tuberculate; inner metacarpal tubercle elongate, as large as outer meta-
carpal tubercle; fingertips truncated but not dilated; finger I and II with moderately developed basal round subar-
ticular tubercles; subarticular tubercle on finger I is equal in size to the inner metacarpal tubercle; fingers III and IV
with poorly developed basal round subarticular tubercles; nuptial pads white, glandular, dorsomedially extended;
spicules of nuptial pads white tipped.
FIGURE 7. Spectral graphs of known calls for species of Sigalegalephrynus, S. gayoluesensis sp. nov. (MZB.Amph.30411)
and S. mandailinguensis (MZB.Amph.25736). Oscillograms (A and C, S. gayoluesensis sp. nov.; F and H, S. mandailinguensis);
spectrograms (B and D, S. gayoluesensis sp. nov.; G and I, S. mandailinguensis); oscillograms of a single pulse within call (E,
S. gayoluesensis sp. nov.; J, S. mandailinguensis).
Thigh length 41% (43%) of SVL; tibia length 38% (41%) of SVL; tarsal length 24% (23%) of SVL; foot length
42% (41%) of SVL; relative lengths of toes I < II < III< V< IV; feet moderately webbed (Fig. 6E), foot webbing
formula: I0-2II0-2III13/4-3IV3-2V (I0-1II0-2III11/2-3IV3-2V); heels without tubercles; inner metatarsal tubercles
oval and well developed; inner metatarsal tubercle round and larger than the outer metatarsal tubercle.
Measurements (in mm). Holotype followed by paratype in parentheses: SVL 26.36 (28.09); HL 8.0 (9.41);
HW 7.18 (8.25); SNL 3.4 (3.8); ICD 4.2 (4.5); IND 2.0 (2.60); END 2.6 (12.1); NSD 0.06 (0.75); IOD 3.7 (4.0); EL
2.55 (2.70); TML 1.3 (2.1); FAL 7.25 (7.95); HAL 7.09 (7.80); THL 10.72 (11.96); TBL 10.11 (11.45); TRL 6.20
(6.41); FTL 10.96 (11.62); OMCL 1.0 (1.0); OMCW 1.0 (1.0); IMCL 1.0 (1.0); IMCW 0.38 (0.50); IMTL 1 (1);
IMTW 1 (1); F1L 1.5 (1.8) ; F2L 2.25 (2.30); F3L 3.65 (3.98); F4L 2.75 (3.40) ; T1L 1.0 (1.5); T2L 1.5 (2); T3L 3.0
(3.0); T4L 5.0 (5.5); T5L 3.5 (4.0).; F3PD 0.75 (1.0); F3PB 0.75 (1.0).
Color of holotype in life. Adult male holotype (Figs. 2M, 2N, 2O): dorsum predominantly brown, with an hour-
glass marking with whitish brown halo; iris brownish-yellow; flanks with alternate wide dark-brown and thin white
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oblique stripes, extending from post-ocular to inguinal areas; a very dark brown triangular blotch below anterior half
of eye, with thin posterior white border that extends posteriorly on subocular rim; loreal region brown; dorsum of
limbs darker than body dorsum, humeral and femoral segments without crossbars, distal segments with crossbars;
area of posterior mandibular articulation with a whitish-yellow spot; lower flanks, inguinal, and circumcloacal
regions golden-yellow; underside of body and head yellowish, with heavily melanized chest; ventral limb surfaces
brown-salmon color; finger and toe tips pale salmon color, not melanized; iris bronze with black reticulations.
Color of holotype in preservative. Differing slightly from that in life, specimens have lost the golden yellow
and pinkish coloration, which has turned grey.
Comparisons. Sigalegalephrynus harveyi sp. nov. differs from all congeners by the combination of possess-
ing truncated but not expanded fingertips (except finger I) (vs truncated and highly expanded in S. gayoluesensis
sp. nov. and S. burnitelongensis sp. nov.; truncated and moderately expanded in S. mandailinguensis; round in S.
minankabauensis), and white tipped tubercles on the body (vs black tipped in S. mandailinguensis and S. minangk-
abauensis). Additionally, Sigalegalephrynus harveyi sp. nov. has a prominent hourglass shaped marking on the dor-
sum (vs missing in adult males of S. burnitelongensis sp. nov.), white-spiculed nuptial pads in adult males (vs black
or dark brown tipped in S. mandailinguensis, S. gayoluesensis sp. nov., S. burnitelongensis sp. nov., unknown in S.
minangkabauensis), an indistinct white loreal spot (vs very distinct in S. mandailinguensis and S. minangkabauen-
sis, absent in S. gayoluesensis sp. nov. and S. burnitelongensis sp. nov.), inner and outer metacarpal tubercles of
equal size (vs inner metacarpal tubercle larger in S. mandailinguensis and S. minangkabauensis, and smaller in S.
gayoluesensis sp. nov. and S. burnitelongensis sp. nov., with respect to outer metacarpal tubercle), and Finger IV tip
(when adpressed) not touching the terminal (distal) phalangeal articulation of Finger III (vs touching in S. mandai-
linguensis S. minankabauensis, and going beyond the articulation in S. gayoluesensis sp. nov.) (Fig. 6E).
Distribution and natural history. Sigalegalephrynus harveyi sp. nov. is only known from montane cloud-for-
est on the south-eastern slopes of Gunung Dempo, from 1826 and 1878 m a.s.l. (Fig. 3), and does not exist sym-
patrically with any other congener. The holotype was found calling on a leaf about 2 m above ground. Call was not
recorded. The paratype was inactive on a leaf, 10 cm above ground. The holotype was not weighed, the paratype
was 1.09 g.
FIGURE 8. A) Elevational distribution of Sigalgalephrynus species in Sumatra. B) Map showing probability of presence of
Sigalegalephrynus species. C) Map showing suitable habitats of Sigalegalephrynus species (according to 10 percentile rule in
MaxEnt).
Key to the species of Sigalegalephrynus
1 Adult males have a stout body with stocky limbs, and dorsum with a white diamond shaped mark or unmarked (Figs. 4A–B);
snout truncated in dorsal profile, and tympanic annulus well developed and covered with sharply raised tubercles (Figs. 5A–
B) .................................................................................................2
- Adult males and juveniles with a gracile body and lanky limbs, and dorsum with an hourglass shaped mark (Figs. 4C–E); snout
SIGALEGALEPHRYNUS, THE PUPPET TOADS OF SUMATRA Zootaxa 4679 (2) © 2019 Magnolia Press · 383
moderately mucronated in dorsal profile, and tympanic annulus not covered by sharply raised tubercles (Figs. 5C–E) . . . . . . 3
2 Adult males >24 mm in SVL, a white diamond shaped mark present on dorso-scapular region, and venter maculated in adult
males (Fig. 4B); subarticular tubercle of finger I as wide as width of inner metacarpal tubercle, tip of finger IV extending be-
yond distal phalangeal articulation of finger III, when addpressed (Fig. 6B) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
.......................................................................................S. gayoluesensis
- Adult males <24 mm in SVL, dorsum without marking, and venter without maculation (Fig. 4A); inner metacarpal tubercle
wider than long, subarticular tubercle of finger I as wide as inner metacarpal tubercle, and tip of finger III not extending beyond
distal phalangeal articulation of finger III, when addpressed (Fig. 6A) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . S. burnitelongensis
3 Venter in adult males maculated or blotched (Figs. 4C, 4E); webbing between toes I and II not complete (Figs. 6C, 6E); poste-
rior mandibular articulation with a white spot on each side, and post-tympanic region with black and white large tubercles (Figs.
5C, 5E) .............................................................................................4
- Venter in juveniles yellow with black blotches (Fig. 4D); webbing between toes I and II complete (Fig. 6D); posterior mandibu-
lar articulation without a white spot on each side, and post-tympanic region with only white large tubercles; fingertips rounded
(Fig. 5D) ........................................................................... S. minangkabauensis
4 Adult males >30 mm in SVL, venter in adult males maculated and anastomotic, and tubercles on body with dark brown or black
keratinized tips (Fig. 4C); nuptial pads in adult males with black-tipped spicules (Fig. 5C); finger tips truncated and expanded
(Fig. 6C) ............................................................................ S. mandailinguensis
- Adult males <30 mm in SVL, venter in adult males not maculated and anastomotic, but slightly spotted, and tubercles on body
round and white-tipped (Fig. 4E); nuptial pads in adult males with white-tipped spicules (Fig. 5E); fingertips truncated but not
expanded (Fig. 6E) .............................................................................S. harveyi
Niche modeling, distribution, and conservation status of Sigalegalephrynus
All known Puppet Toads are found in the highland forests of Sumatra between 1200 and 1900 m a.s.l. (Fig. 8A).
Our logistic output for habitat suitability distribution of Sigalegalephrynus species had a very high success rate.
Our average test AUC score for the replicate runs was 0.945, with a standard deviation of 0.027. Jackknife variable
contribution test revealed that among the variables used for the modeling, elevation contributed most significantly
(64.5%) to the habitat suitability, followed by land cover (7.1%). Our model identified many additional isolated
mountain tops as suitable habitat for Sigalegalephrynus species (Fig. 8B). The total area of all suitable habitat in
Sumatra equaled 445 km2 which is only 1.78% of the total montane forests of Sumatra (Margono et al. 2014). All
the suitable habitats are highland forests above 1200 meters in elevation (Fig. 8C).
Our GeoCAT analysis revealed that extent of occurrence (EOO) of each species of Sigalegalephrynus is less
than 1 km2 and area of occupancy (AOO) is between 4 and 8 km2, suggesting all species are Critically Endangered
(CR), based on both EOO and AOO status. Doubling the IUCN default grid values in GeoCAT, we found that area
of occupancy (EOO) is between 4 and 36 km2 suggesting Critically Endangered (CR) category but the AOO status
suggesting Endangered (EN) category for all of the Sigalegalephrynus species (Table 3).
TABLE 3. Area of occupancy (AOO) and extent of occurrence (EOO) output with suggested IUCN Red List Status from
GeoCAT analysis.
Species IUCN default value Default IUCN value*2
EOO
(km2)
AOO
(km2)
EOO
Status
AOO
Status
EOO
(km2)
AOO
(km2)
EOO
Status
AOO
Status
S. harveyi sp. nov. 0 4 CR CR 0 16 CR EN
S. minangkabauensis 0 4 CR CR 0 4 CR EN
S. mandailinguensis 0.067 8 CR CR 0.067 32 CR EN
S. gayoluesensis sp. nov. 0.017 8 CR CR 0.017 16 CR EN
S. burnitelongensis sp. nov. 0 8 CR CR 0 32 CR EN
Discussion
Sigalegalephrynus is one of the four enigmatic bufonid genera in South and Southeast Asia and one of the key
components to understand biodiversity of the region (Chan and Grismer 2019) that needs more studies. This is
only the second study on the genus Sigalegalephrynus, and with this discovery of three new species, the genus Si-
galegalephrynus becomes the most diverse endemic bufonid in Indonesia. These are micro-endemic frogs that are
restricted to the mountain tops of the Barisan Range of Sumatra. The inter-specific divergence of the mitochondrial
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384 · Zootaxa 4679 (2) © 2019 Magnolia Press
16S rRNA gene between S. harveyi sp. nov. and S. mandailinguensis is 4.2%, which exceeds the conventional
threshold values considered by many anuran phylogeny studies for recognizing distinct species—3% in Fouquet et
al. (2007) and Vieites et al. (2009), 1.6% in Bell (2016), 2–2.5% in Zimkus et al. (2017), and 2.3% in Tapley et al.
(2017). Our phylogenetic data shows a deep divergence (8.2%-10.4%) (Table 2) between the clades north and south
of Lake Toba. A similar divergence pattern is also identified in the highland agamid lizards of the genus Dendro-
gama (Harvey et al. 2017b) and in the frogs of the genus Rhacophorus (O’Connell et al. 2018).
Crow (2005) suggested continuous volcanic activity through the Bukit Barisan mountain range of Sumatra
until the late Miocene, with reduced volcanic eruptions afterward, and according to Setyaningsih et al. (2018) that
active volcanism greatly affected the ecosystem and biodiversity of the region. Lohman et al. (2011) suggested that
the inundation of lowlands due to rising of sea level during the Pliocene and Pleistocene, formed isolated highland
refugia throughout the Barisan Range, having a great influence on Sumatran biodiversity. Thus, the deep divergence
between the northern and southern clades might be the result of ancient volcanic eruptions in the late Miocene. Fur-
ther diversification within the group might be a result of more recent volcanic orogeny and glacial cycles and related
sea level fluctuations during the late Pliocene and early Pleistocene.
Proper estimation of biodiversity is the key component for conservation. Conservation and management ef-
forts become more challenging where the vast majority of species of an area—for example, Sumatra—is yet to be
discovered (Grismer et al. 2013). New species are most likely to be found on each isolated mountain top within the
distribution of a genus containing species generally small sized, secretive, and with special habitat requirements
(Grismer 2006). Given the arboreal nature with close ties to the stream systems of montane forests of Sumatra, it is
highly likely that there are many more Sigalegalephrynus species awaiting discovery in unexplored mountain tops
in Sumatra. With a high average AUC test score for replicates (0.945±0.027) our MaxEnt output presents a high
level of accuracy in model prediction, and our partial model validation test for ROC was also significant (P<0.001).
Since the MaxEnt modeling output with 10th percentile threshold rule for suitable habitat (Hu & Jiang 2018) recov-
ered at least 17 mountains with montane forests that are more than 1100 m a.s.l., isolated, and forested (Fig.8B and
8C), it would not be surprising to find as many as 12 more new populations of Sigalegalephrynus in Sumatra. Given
the microendemicity observed in Sigalegalephrynus, all of these could represent distinct species. Despite recent
discoveries of other anurans in Sumatra (Teynie et al. 2010, Matsui et al. 2012, Streicher et al. 2014, Hamidy &
Kurniati 2015, Wostl et al. 2017, Arifin et al. 2018), anuran diversity in the island still remains significantly under-
estimated (Stuart et al. 2006, Inger et al. 2009, Arifin et al. 2018). Intensive surveying for new amphibian species
on individual mountains of Sumatra is imperative for documenting underrepresented anuran diversity.
About 32% of amphibian species are threatened globally, the highest percentage among all threatened quadru-
ped vertebrate classes (IUCN 2017). Southeast Asian amphibians are no exception to the threats, and they are facing
a grave conservation crisis (Rowley et al. 2009, Coleman et al. 2019), compounded day by day by global climate
change (Bickford et al. 2010, Kusrini et al. 2017), overexploitation (Natusch & Lyons 2012), habitat loss and de-
forestation (Daszak et al. 2003), chytrid fungus infestation (Kusrini et al. 2017, Hamidy et al. 2018), and lack of
information on conservation status (Tapley et al. 2018). In Indonesia, 41.4% of amphibians are endemic (Sodhi et
al. 2004), and 65.6% of these are threatened (IUCN 2017). The Puppet Toads face threats to their survival, all have
been discovered at forest edges, less than 1 km away from tea and/or coffee plantations, or mining pits. All of the
Sigalegalephrynus species occur in isolated mountain tops where deforestation pressure is very high.
Deforestation rate in the provinces where Sigalegalephrynus toads are discovered is significantly high (Aceh
6.72%, Jambi 30.70%, West Sumatra 11.9% and South Sumatra 15.94%; Suprianta et al. 2017). These toads are
under the direct and imminent threat of habitat destruction that warrant an immediate and strong conservation
initiative. It is suggested to update the IUCN Red List status of the new species, given new information provided
herein and IUCN Red List of Threatened Species category and criteria to at least Endangered, EN B1ab(iii) (IUCN
Standards and Petitions Subcommittee 2017). Future research should focus on finding new species in areas with
high presence probability and habitat suitability derived from our niche modeling analysis, as well as determining
the distributional range of the identified species.
Acknowledgments
All specimens were collected and euthanized following approved protocols (UTA IACUC A12.004). Research in
Indonesia was conducted under research permits 149/SIP/FRP/SM/V/2013 (E.N. Smith). We are grateful to the
SIGALEGALEPHRYNUS, THE PUPPET TOADS OF SUMATRA Zootaxa 4679 (2) © 2019 Magnolia Press · 385
Ministry of Research and Technology of the Republic of Indonesia (RISTEK) for coordinating and granting re-
search permission. S. Wahyono (RISTEK) provided valuable assistance throughout the permit approval process.
We are grateful to past and present representatives of LIPI at the Museum Zoologicum Bogoriense for facilitating
the in-house study of specimens and export and field research permits, namely Boeadi, M. Amir, R. Ubaidillah,
R.M. Marwoto, and H. Sutrisno. Both RISTEK and LIPI reviewed and approved our fieldwork in Indonesia and
provided export permits for specimens to the United States for study and deposition at UTA. A. Riyanto, Syaripu-
din and W. Tri Laksono kindly provided laboratory assistance at MZB, and N. Widodo and Mr. Marwoto from the
Faculty of Mathematicas and Natural Sciences of Universitas Brawijaya (UB) kindly provided logistical support.
Dr. E. Harnelly and Dr. Suwarno (Biology Department, Syiah Kuala University [SKU], Banda Aceh, Indonesia)
kindly provided logistical support to our team while in Aceh. For their hard work under often difficult field condi-
tions, we thank members of the summer 2015 expedition to Sumatra: M. Ikhsan and I. Fonna (SKU), F. Akhsani, F.
Alhadi, S. Sianturi, Syaripudin, W. Tri Laksono, and G. Pradana (MZB), A.M. Kadafi (UB), and U. Smart, (UTA).
We thank Dr. Sophia Passy (UTA) for providing critical comments suggesting substantial improvement on an earlier
draft of the manuscript. Helpful comments by Dr. Bryan Stuart (NCMNS) and one anonymous reviewer greatly
improved the manuscript. A National Science Foundation (NSF) grant (DEB-1146324) to ENS and MBH funded
this research.
Author contributions
GCS conducted analyses and wrote the manuscript. GCS, EW, PT, IS, & ENS conducted fieldwork and collected
specimens. ENS, AH & NK obtained permission for conducting fieldwork in Indonesia. All authors have equal posi-
tion in authorship, they also discussed, corrected and approved the final version of the manuscript.
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APPENDIX I. Additional Specimens Examined.
Sigalegalephrynus mandailinguensis (4).—INDONESIA: Sumatera Utara: Kabupaten Mandailing Natal: Gunung Sorikmarapi
(W side), 1383 m. a.s.l., 0.701648ºN, 99.552628ºE, MZB.Amph.25736—Holotype (male); trail between the Tano Bato to Sapo
Tinjak road and Lake Saba Begu, Batang Gadis National Park, 1297 m. a.s.l., 0.708668ºN, 99.519538ºE, MZB.Amph.25737—
Paratype (male); 1299 m. a.s.l., 0.708668ºN, 99.519538ºE, UTA A63562—Paratype (male), UTA A63561—Paratype (male).
Sigalegalephrynus minangkabauensis (1).—INDONESIA: Jambi: Kabupaten Kerinci: Gunung Kunyit, 1428 m. a.s.l.,
2.260138ºS, 101.495128ºE, MZB.Amph. 25738—Holotype.
... Herpetofauna discoveries began primarily in Java in the 19th century (Boulenger 1890;de Rooij 1917;van Kampen 1923;Kopstein 1930;de Haas 1941) and expedited our understanding of Indonesia's species diversity. Recent decades have seen a rapid increase in the number of newly described herpetofauna species, particularly for amphibians, e.g., Megophrydae (Hamidy & Matsui 2010;Hamidy et al. 2012;Eto et al. 2018;Munir et al. 2018;2021b), Rhacophoridae (Matsui et al. 2014;Hamidy & Kurniati 2015;Wostl et al. 2017b;Mediyansyah et al. 2019;Munir et al. 2021a), Microhylidae (Matsui et al. 2013;Atmaja et al. 2019;Munir et al. 2020;Eprilurahman et al. 2021), Bufonidae (Smart et al. 2017;Hamidy et al. 2018;Sarker et al. 2019), Ranidae (Matsui & 92 Hamidy 2012;Arifin et al. 2018), Dicroglossidae (Iskandar et al. 2011a;Mcleod et al. 2011); and reptiles, e.g., Gekkonidae including Cyrtodactylus (Iskandar et al. 2011b;Riyanto et al. 2018a;2018b;, Cnemaspis (Amarasinghe et al. 2015a;Riyanto et al. 2017;Iskandar et al. 2017), Hemiphyllodactylus (Grismer et al. 2014), and Lepidodactylus (Stubbs et al. 2017); Agamidae (Harvey et al. 2014;2018;, Colubridae (Vogel et al. 2014;Amarasinghe et al. 2015b;Wostl et al. 2017a), and Cylindrophiidae ; which highlight the fact that many enigmatic, elusive, and cryptic species are waiting to be discovered. Although the region of Sumatra, Borneo, Celebes, Moluccas and Java has been extensively surveyed (David & Vogel 1996;Inger et al. 2005;de Lang & Vogel 2006;Kurniawan et al. 2021;Kusrini et al. 2021), the primary focus has been on areas with relatively high diversity. ...
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