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Cryptic diversity in the Hypsiboas semilineatus species group (Amphibia, Anura) with the description of a new species from the eastern Guiana Shield

Authors:
  • Université Montpellier 2

Abstract and Figures

We used molecular and morphological data to investigate the hidden diversity within the Hypsiboas semilineatus species group, and more specifically within H. geographicus, an allegedly widespread species in northern South America. As a result, the identity of H. geographicus was clarified, several candidate species were detected and one of them, from the eastern Guiana Shield, is described herein as a preliminary step to resolve the taxonomy of the group. Hypsiboas diaboli-cus sp. nov. is mainly distinguished from closely-related species by an acuminate snout in lateral view, well-developed webbing between fingers and toes, and unspotted carmine/crimson colouration on the concealed surfaces of legs, feet and hands in life. The tadpole of the new species is described and is characterized by a large A-2 gap, a mostly single row of large marginal papillae, and a dark brown to black colouration. We also describe the advertisement call of the new species, which is defined as a soft call consisting of short clusters of 2-3 chuckles with a dominant frequency ranging between 1.11-1.19 kHz. Hypsiboas diabolicus sp. nov. is currently known only from the eastern Guiana Shield, and is probably endemic to that region. The new species' range overlaps broadly with another candidate species referred to as H. aff. semi-lineatus 1. Our preliminary results stress out a high cryptic diversity in that species group and the need for a formal rede-scription of Hypsiboas geographicus based on more topotypic material than what is currently available to properly sort out the taxonomic status of several lineages in that clade.
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Accepted by V. Orrico: 20 Nov. 2015; published: 24 Feb. 2016
ZOOTAXA
ISSN 1175-5326 (print edition)
ISSN
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Copyright © 2016 Magnolia Press
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http://doi.org/10.11646/zootaxa.4084.1.3
http://zoobank.org/urn:lsid:zoobank.org:pub:26445D9D-AF58-4A8B-9F55-142C169E1F63
Cryptic diversity in the Hypsiboas semilineatus species group (Amphibia, Anura)
with the description of a new species from the eastern Guiana Shield
ANTOINE FOUQUET
1,7
, QUENTIN MARTINEZ
1
, LAUREN ZEIDLER
2
, ELODIE A. COURTOIS
1
,
PHILIPPE GAUCHER
1
, MICHEL BLANC
3
, JUCIVALDO DIAS LIMA
4
, SERGIO MARQUES SOUZA
5
,
MIGUEL T. RODRIGUES
5
& PHILIPPE J. R. KOK
6
1
CNRS Guyane USR3456, Immeuble Le Relais, 2 Avenue Gustave Charlery, 97300, Cayenne, French Guiana
2
Museum of Vertebrate Zoology, University of California, Berkeley, CA, USA
3
Pointe Maripa, RN2/PK35, 97311, Roura, French Guiana
4
Centro de Pesquisas Zoobotânicas e Geologicas (CPZG), Instituto de Pesquisas Científicas e Tecnológicas do Estado do Amapá
(IEPA), Macapá, AP, Brazil
5
Universidade de São Paulo, Instituto de Biociências, Departamento de Zoologia, Caixa Postal 11.461, CEP 05508-090, São Paulo,
SP, Brazil
6
Amphibian Evolution Lab, Biology Department, Vrije Universiteit Brussel, 2 Pleinlaan, B-1050 Brussels, Belgium
7
Corresponding author: e-mail: fouquet.antoine@gmail.com
Abstract
We used molecular and morphological data to investigate the hidden diversity within the Hypsiboas semilineatus species
group, and more specifically within H. geographicus, an allegedly widespread species in northern South America. As a
result, the identity of H. geographicus was clarified, several candidate species were detected and one of them, from the
eastern Guiana Shield, is described herein as a preliminary step to resolve the taxonomy of the group. Hypsiboas diaboli-
cus sp. nov. is mainly distinguished from closely-related species by an acuminate snout in lateral view, well-developed
webbing between fingers and toes, and unspotted carmine/crimson colouration on the concealed surfaces of legs, feet and
hands in life. The tadpole of the new species is described and is characterized by a large A-2 gap, a mostly single row of
large marginal papillae, and a dark brown to black colouration. We also describe the advertisement call of the new species,
which is defined as a soft call consisting of short clusters of 2–3 chuckles with a dominant frequency ranging between
1.11–1.19 kHz. Hypsiboas diabolicus sp. nov. is currently known only from the eastern Guiana Shield, and is probably
endemic to that region. The new species’ range overlaps broadly with another candidate species referred to as H. aff. semi-
lineatus 1. Our preliminary results stress out a high cryptic diversity in that species group and the need for a formal rede-
scription of Hypsiboas geographicus based on more topotypic material than what is currently available to properly sort
out the taxonomic status of several lineages in that clade.
Key words: Anura, conservation, endemism, Guiana Shield, taxonomy
Introduction
Hypsiboas Wagler 1830 is a speciose genus of hylid frogs currently including 90 nominal species (Frost 2015).
These so called “gladiator frogs” form a well-supported monophyletic clade (e.g. Wiens et al. 2010), but without
established morphological synapomorphies (Faivovich et al. 2005). Seven species groups are currently recognized
within the genus (Faivovich et al. 2005). Among these, the H. semilineatus group is strongly supported by
molecular evidence (see Faivovich et al. 2005; Pyron & Wiens 2011), and the presence of a reticulated lower eyelid
represents a putative morphological synapomorphy (Faivovich et al. 2005). The H. semilineatus group comprises
six nominal species: H. semilineatus (Spix, 1824) and H. pombali (Caramaschi, Feio & Pimenta, 2004), which
occur in the Atlantic Forest; H. geographicus (Spix, 1824), which is widely distributed in northern South America;
H. hutchinsi (Pyburn & Hall, 1984), which occurs in western Amazonia; H. boans (Linneaus, 1758), which occurs
in Amazonia, extending to trans-Andean lowlands of Colombia, Ecuador and Panama; and H. wavrini (Parker,
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1936), which occurs in central and northern Amazonia. Among these species, a subgroup containing H.
semilineatus, H. geographicus and H. hutchinsi is characterized by a smaller size, a prepollex not modified into a
projecting spine, the presence of pigmented nuptial excrescences, and a finely granular dorsal skin. Two species of
that subgroup, H. geographicus and H. semilineatus, are taxonomically challenging because morphologically very
similar both in adult and larval stage (d’Heursel & de Sá 1999). Both taxa have large tadpoles unpalatable to fishes
that display schooling behaviour (Duellman & Lescure 1973; Caldwell 1989).
The exact identity of Hypsiboas geographicus remains ambiguous. The holotype, from Tefé, Amazonas, Brazil
(western Amazonia), is lost (Hoogmoed & Gruber 1983), and the only testimonies of it are the succinct description
and illustration in Spix (1824). Recent molecular analyses revealed the existence of distantly related lineages
attributed to H. geographicus in the Guiana Shield (Fouquet et al. 2007) and in Bolivia (Jansen et al. 2011). Gans
(1960) and later Duellman (1973) have already reported a striking geographical variation in the colour of the
webbing of H. geographicus. Duellman (1973) also noted that morphometrics and bioacoustics discriminate
populations displaying differences in webbing colouration in western Amazonia. Additionally, several studies
found conspicuous variation in H. geographicus tadpole teeth rows that were, at the time, partly interpreted as
ontogenetic and only partly considered as of taxonomic value (Bokermann 1963; Kenny 1969; Duellman &
Lescure 1973; d’Heursel & de Sá 1999); differences in tadpole body size were found as well (Caldwell 1989). All
these results converge to suggest the occurrence of several unnamed species erroneously identified as H.
geographicus in Amazonia.
We compared molecular, morphological, and acoustic data attributed to that species, and our analysis reveals
multiple lineages suggestive of the existence of no less that nine confirmed and unconfirmed candidate species in
that group, including two species in the Guiana Shield currently referred to as Hypsiboas geographicus. Based on a
comprehensive sampling we describe one of them as a new species, and closely compare it to the original
description of H. geographicus from Tefé, Brazil, to one recently collected topotypic specimen, and to other
specimens attributable to H. geographicus sensu stricto according to our phylogenetic hypothesis. Pending its
formal description, the second species is herein referred to as H. aff. semilineatus 1 because of its closer
relationship to H. semilineatus than to H. geographicus sensu stricto (see results).
Materials and methods
Molecular analysis. Genomic DNA was extracted using Promega DNA extraction kits from 48 tissue samples,
including 14 of the new species (six from individual tadpoles collected from different schools), all preserved in
95% ethanol. We targeted one mitochondrial locus (16S) that was already available for twelve specimens of the H.
semilineatus group, as well as eight congeneric species used as outgroup (Table 1). Fragments were amplified by
standard PCR techniques using previously described primers (16Sar-5’ and 16Sbr-3’) and PCR conditions (Hillis et
al. 1996). Sequencing was performed using ABI Big Dye V3.1 (ABI Foster City USA) and resolved on an
automated sequencer at Genomic Engenharia corp. (São Paulo Brazil) and Macrogen (Korea). Sequences were
edited and aligned using CodonCode Aligner v.3.5.2 (http://www.codoncode.com/aligner/download.htm). Novel
sequences were deposited in Genbank (Table 1).
The 48 newly generated sequences were collated to 20 available additional sequences from Genbank (totaling
68 sequences), and aligned using MAFFT v6 (Katoh et al. 2013) under default parameters except the use the E-
INS-i strategy, which is adapted to sequences with conserved domains and long gaps. We obtained a final 850 base
pairs (bp) alignment that remained incomplete for the first 290 bp for 42 terminals (all the major lineages except H.
aff. semilineatus 3 & 4 have complete representatives) and the last ca. 100 bp for 24 terminals.
We used the software jModeltest version 0.1.1 (Guindon & Gascuel 2003; Posada 2008) to select the
substitution model that best fits the data under the Bayesian Information Criterion. The resulting model was
employed in a Bayesian analysis (BA) with MrBayes 3.1 (Huelsenbeck & Ronquist 2001). The BA consisted of a
10x10
6
generations run starting with random trees and 10 Markov chains (one cold) sampled every 1000
generations. Adequate burn-in (the first 1000 sampled generations) was determined by examining likelihood scores
of the heated chains for convergence on stationarity as well as the effective sample size of values in Tracer 1.5
(Rambaut & Drummond 2007). We considered relationships to be strongly supported when posterior probabilities
were equal to or higher than 0.95.
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TABLE 1 List of the specimens included in the phylogenetic analysis and GenBank accession numbers. Numbers between parentheses correspond to field numbers; data in bold face correspond to the new species.
Species Locality Country/state Voucher Accession number Latitude Longitude
H. aff. semilineatus 1 Road to Apura Suriname R140 (AF0107) KU168866 5.183333 -55.616667
H. aff. semilineatus 1 Igarapé Camaipi Brazil/Amapá (MTR6216) KU168905 -0.024167 -51.897222
H. aff. semilineatus 1 Road to Apura Suriname R139 (AF0106) KU168865 5.183333 -55.616667
H. aff. semilineatus 1 Pidima French Guiana (CM335) KU168886 3.293856 -54.103300
H. aff. semilineatus 1 Igarapé Camaipi Brazil/Amapá (MTR6214) KU168904 -0.024167 -51.897222
H. aff. semilineatus 1 REBIO Maicurú Brazil/Pará MPEG30285 KU168894 0.828619 -53.931200
H. aff. semilineatus 1 Lourenço Brazil/Amapá (MTR13933) KU168896 2.323611 -51.645278
H. aff. semilineatus 1 Warniabo Creek, SW Dubulay Ranch house Guyana AMNH-A 141054 AY843628 5.620769 -57.856865
H. aff. semilineatus 1 Crique Margot French Guiana (CM140) KU168885 5.466667 -53.950000
H. aff. semilineatus 1 Piste Risquetout French Guiana (BM101) KU168882 4.916731 -52.500064
H. aff. semilineatus 1 Piste Risquetout (tadpole) French Guiana (AF175) KU168867 4.916731 -52.500064
H. aff. semilineatus 1 Serra do Navio Brazil/Amapá (MTR13841) KU168895 0.918056 -52.002778
H. aff. semilineatus 1 Igarapé Camaipi Brazil/Amapá (MTR6217) KU168906 -0.024167 -51.897222
H. aff. semilineatus 1 Nouragues French Guiana R143 (AF1285) KU168875 4.084790 -52.680630
H. aff. semilineatus 1 Crique Bon Espoir, Mana River (tadpole) French Guiana (AF1112B) KU168873 5.099493 -53.800571
H. aff. semilineatus 1 Grand Santi French Guiana (CM033) EF376054 4.333333 -54.250000
H. aff. semilineatus 1 Bagne des Annamites (tadpole) French Guiana (AF1373) KU168876 4.818210 -52.522123
H. aff. semilineatus 1 Mont. Cacao French Guiana (CAAM29) KU168884 2.349156 -53.216013
H. semilineatus Duque de Caxias Brazil/R. Janeiro CFBH5424 AY843779 -22.791375 -43.317947
H. semilineatus unknown Brazil/R. Janeiro unknown KM390786 unknown unknown
H. aff. semilineatus 2 Altamira, UHE Belo Monte Brazil/Pará (BM334) KU168883 -2.950584 -51.936607
H. aff. semilineatus 2 Guaraí Brazil/Tocantins (MRT7584) KU168907 -8.816943 -48.383300
H. aff. semilineatus 3 Juruena Brazil/M. Grosso (AF252) KU168880 -12.849000 -58.925000
H. aff. semilineatus 3 Apiacás Brazil/M. Grosso (968365) KU168863 -9.650846 -57.39366
H. aff. semilineatus 3 Gaúcha do Norte Brazil/M. Grosso (976482) KU168864 -13.235935 -53.15208
H. aff. semilineatus 3 Tapajos, Tocatinzinho Brazil/Pará (JOG179) KU168889 -6.061700 -56.296620
H. aff. semilineatus 3 Itaituba, Mina Palito Brazil/Pará (JOG737) KU168890 -6.317317 -55.798644
H. aff. semilineatus 4 Campo Catuquira Brazil/Amazonas (SMS153) KU168909 -4.9136111 -61.109160
H. aff. semilineatus 5 Rio Icá, comm. cachoeirinha Brazil/Amazonas (MTR36136) KU168899 -2.891870 -68.355180
H. aff. semilineatus 5 Rio Icá, comm. Cuiauá Brazil/Amazonas (MTR36149) KU168900 -2.891870 -68.369280
H. aff. semilineatus 5 Fonte Boa Brazil/Amazonas (MTR36821) KU168902 -2.532115 -66.162602
H. cf. geographicus 1 UHE Jirau, Rio Madeira Brazil/Rondônia (HJ0048) KU168888 -9.576376 -64.923134
H. cf. geographicus 1 FLONA Caxiuanã. Plote PPBIO Brazil/Pará MPEG24822 KU168893 -1.792306 -51.434028
H. cf. geographicus 1 FLONA Caxiuanã. Plote PPBIO Brazil/Pará MPEG24821 KU168892 -1.792306 -51.434028
……continued on the next page
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TABLE 1. (Continued)
Species
Locality
Country/state
Voucher
Accession
number
Latitude
Longitude
H. cf. geographicus1
Rio Ica, São Pedro
Brazil/Amazonas
(MTR36719)
KU168901
-3.028560
-68.882600
H. geographicus
Lago Chaviana, Rio Purus
Brazil/
Amazonas
MZUSP157083
(MTR18569)
KU168897
-4.307750
-61.813833
H. geographicus
Concepcion
Bolivia
MNKA9343
JF790118
-16.351768
-61.975708
H. geographicus
Concepcion (tadpole)
Bolivia
SMF94091
KF723059
-16.359600
-62.000100
H. geographicus
Serra do Divis
or
Brazil/
Acre
MZUSP157090
(MTR28250)
KU168898
-7.434348
-73.660390
H. geographicus
Tefé
Brazil/
Amazonas
MZUSP157060
(MTR36895)
KU168903
-2.890867
-68.361287
H. diabolicus sp. nov
Trinite
French Guiana
R158 (AG196)
EU201106
4.608465
-53.415191
H. diabolicus sp. nov
Mont Saint Marcel
French Guiana
(PG111)
KU168908
2.385833
-53.018889
H. diabolicus sp. nov
Nouragues (Holotype)
French Guiana
R157 (AF1284)
KU168874
4.084790
-52.680630
H. diabolicus sp. nov
Kaw
French Guiana
R152 (AF667)
KU168869
4.627158
-52.307289
H. diabolicus sp. nov
Crique Bon Espoir, Mana River (tadpole)
French Guiana
(AF1111C)
KU168872
5.099493
-53.800571
H. diabolicus sp. nov
French Guiana
(MBT136)
4.462112
H. diabolicus sp. nov
Paracou
French Guiana
R153 (AF0701)
KU168870
5.272546
-52.923596
H. diabolicus sp. nov
French Guiana
(AG406)
4.816926
-54.281875
H. diabolicus sp. nov
Apatou (tadpole)
French Guiana
(AF1788)
KU168877
5.249830
-54.206730
H. diabolicus sp. nov
French Guiana
(AF1800)
5.249830
-54.206730
H. diabolicus sp. nov
Montagne des Singes (tadpole)
French Guiana
(AF1827)
KU168879
5.069670
-52.696800
H. diabolicus sp. nov
Rio Vila Nova
Brazil/Amapá
IEPA5028 (FTA114)
KU168887
0.449335
-52.022137
H. diabolicus sp. nov
Brazil/Amapá
0.909122
-53.228479
H. diabolicus sp. nov
Oiapoque
Brazil/Amapá
R149 (AF1092)
KU168871
3.904047
-51.772270
H. boans
Cano Agua Blanca,
Venezuela
RWM 17746
AY843610
H. polytaenius
Brazil/R. Janeiro
CFBH 5752
H. pulchellus
Entre Rios: Dto. Uruguay: Basavilbaso
Argentina
MACN 37664
AY549351
H. pardalis
USNM 303046
H. sibleszi
Mount Ayanganna
Guyana
ROM 39561
AY843667
H. lanciformis
Pastaza; 5.6 km N Puyo; 1150 m
Ecuador
WED 54081
AY326054
H. raniceps
Santa Fe, Vera, Ea. 'Las Gamas'
Argentina
MACN 37795
AY843657
H. benitezi
Roraima, Vila Pacaraima,
Brazil/Roraima
USNM 302435
AY843606
H. rufitelus
Parque Nacional 'Omar Torrijos'
Panama
KRL 798
AY843662
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FIGURE 1. (A) Map of northern South America showing the distribution of the major lineages recovered from the
phylogenetic analysis. (B) Distribution records of H. diabolicus sp. nov. (red dots) and H. aff. semilineatus 1 (black dots) in the
Eastern Guiana Shield (from specimens, DNA sequences, as well as unambiguously identified individuals from the literature
and various herpetological surveys; other records are ignored). The type locality of Hypsiboas diabolicus sp. nov. is indicated
with a white arrow.
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We also calculated p-distances among major groups recovered from the phylogenetic analysis using a 400 bp
region, where all the sequences overlap, using MEGA 5 (Tamura et al. 2011).
Fieldwork and deposition of specimens. Twenty-two adult specimens of the new species were collected by
hand at night. Nineteen are from eight localities in French Guiana, and three are from distinct localities in Amapá,
Brazil (see below). Nineteen tadpoles from five localities in French Guiana were also collected (six specimens
from five schools were genotyped). Thirteen additional localities of occurrence are based on available molecular
data and direct field observations. In total, the new species is reported from 25 localities in the eastern Guiana
Shield (Appendix 1; Fig. 1).
This material was compared with 22 adult specimens and seventeen tadpoles (three specimens from three
schools were genotyped) of the sympatric H. aff. semilineatus 1, from diverse localities in French Guiana (see
Appendix 2). Additional occurrence records were also gathered from available molecular data and direct field
observations. In total, we provide 33 occurrence records in the Eastern Guiana Shield for that species (Fig. 1).
Hypsiboas aff. semilineatus 1 probably also occurs in Reserva Adolfo Ducke, north of Manaus, Amazonas, Brazil
(Lima et al. 2006). The description of adults, call, and pictures provided by Lima et al. (2006) match with
Hypsiboas aff. semilineatus 1 and none of the other lineages has been recorded north of the Amazon River.
Nevertheless, the status of this population was not assessed in our study, and thus remains tentative.
The new taxon was also compared to one topotypic adult specimen of Hypsiboas geographicus from Tefé
(Amazonas, Brazil). Nine adult specimens from Rio Purus (Amazonas state, Brazil) and Serra do Divisor (Acre
state, Brazil) (Appendix 2) were also unambiguously attributed to that species according to molecular data and
morphology (see results).
Frogs were killed by intraperitoneal injection of Xylocaïne® (lidocaïne chlorhydrate). Tissue samples (a piece
of liver) were removed and stored in 95% ethanol before specimen preservation. All specimens were tagged and
fixed in 10% formalin before being transferred to a solution of 70% ethanol for permanent storage. Type specimens
were deposited in the collections JAGUARS IPG/Kwata FR973A (Cayenne, French Guiana), in the Instituto de
Pesquisas Científicas e Tecnológicas, Estado do Amapá, (Macapá, Brazil), and in the Museum National d’Histoire
Naturelle de Paris (Paris, France).
Morphology. Webbing formulae follow Savage and Heyer (1967), as subsequently modified by Myers and
Duellman (1982). All other terminology follows Duellman (1970). Abbreviations for morphological characters
used throughout the text are: SVL, Snout-Vent Length; TiL, Tibia Length; CL, Calcar Length; ThL, Thigh Length
(from vent to outer edge of flexed knee); TaL, Tarsus Length; FL, Foot Length (from proximal edge of inner
metatarsal tubercle to tip of fourth toe); 4TD, Disc width on Toe IV; FD, Disc width on Finger III; 1FiL, Length of
Finger I (from proximal edge of palmar tubercle to tip of Finger I); 2FiL, Length of Finger II (from proximal edge
of palmar tubercle to tip of Finger II); HaL, Hand Length (from proximal edge of palmar tubercle to tip of Finger
III); ETS, Eye-Tip of Snout distance (straight line between anterior corner of eye and tip of snout); EN, Eye to
Nostril distance (straight line between anterior corner of eye and posterior edge of nostril); HL, Head Length
(straight line from posterior corner of mouth to the tip of snout); HW, Head Width (at widest point); IN, Internarial
Distance; ED, horizontal Eye Diameter; IOD, Interorbital Distance (between the anterior margins of the orbits),
and TYD, Tympanum Diameter. All measurements (rounded to the nearest 0.1 mm) were taken by the same person
(Quentin Martinez, hereafter QM) using electronic digital callipers under a stereomicroscope.
Sex was determined either by the presence or absence of secondary sexual characters (i.e. pigmented nuptial
pads, vocal slits) or by calling activity at the time of collection. Relative length of digits was estimated by
adpressing adjacent digits to one another. Colour pattern in life was taken from field notes and colour photographs
that where compared to the colour definitions proposed by Köhler (2012).
Available tadpoles of the new species range from Gosner stage 27–39 (Gosner 1960), and were closely
compared with tadpoles of the sympatric Hypsiboas aff. semilineatus 1. Gosner stage, Labial Tooth Row Formula
(LTRF) and Total Length were taken on 19 tadpoles of the new species and 16 tadpoles of H. aff. semilineatus 1.
The following measurements were taken on the best preserved larvae (ten tadpoles of the new species and five
tadpoles of H. aff. semilineatus 1) by the same person (Antoine Fouquet, hereafter AF) as summarized in Kok and
Kalamandeen (2008) using calibrated pictures from a Stemi 2000C Zeiss stereomicroscope connected to an
Axiocam ERC 5S: TL, Total Length (from tip of the snout to tip of the tail); BL, Body Length (from tip of snout to
junction of posterior body and tail musculature); TAL, Tail Length (from junction of posterior body and tail
musculature to tip of tail); BW, Body Width (highest width of body); BH, Body Height (highest height of body);
HW, Head Width (at level of eyes); TMH, Tail Muscle Height (at base of tail); UTF, Upper Tail Fin Height (highest
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height of upper fin, from upper margin of tail musculature to upper margin of upper fin); LTF, Lower Tail Fin
Height (highest height of lower fin, from lower margin of lower fin to lower margin of tail musculature); TMW,
Tail Muscle Width (at base of tail); MTH, Maximum Height of Tail; END, Eye-Naris Distance (from anterior
corner of eye to posterior margin of nostril); NSD, Naris-Snout Distance (from anterior margin of naris to tip of
snout); SSD, Snout-Spiracle Distance (from tip of snout to posterior margin of spiracle); IND, Internarial Distance
(distance between the median margins of nares); IOD, Interorbital Distance; ED, Eye Diameter (greatest length of
orbit from anterior margin to posterior margin of eye).
Bioacoustics. Call recordings of the new species were obtained from a vouchered specimen at the Nouragues
biological station (AF1283/MNHN 2014.0109), and from an uncollected specimen at Camp Patawa, Kaw
Mountains, French Guiana; recorded using SONY PCM-M10 and a microphone SENNHEISER ME66 on 15
March 2014 at night (21:20; ~24°C). Unfortunately the quality of the vouchered recording was too low to be
properly analysed. Therefore, we used the unvouchered call, which is unambiguously attributed to a specimen of
the new species because of its characteristic leg colouration (see below). In addition, both recordings display
similar temporal and spectral structures. This recording (four calls analyzed) was compared with a recording of H.
aff. semilineatus 1 (four calls analyzed) from an uncollected specimen from Camp Arataï, Nouragues biological
station, French Guiana, which was recorded using a tape recorder SONY WM-D6C (tape: UX-Pro90) and a
microphone SENNHEISER MKH60 on 21 January 1996 at night (20:32; ~23°C). This individual was
unambiguously identified in the field because of its colouration. Two other recordings of H. aff. semilineatus 1
were obtained from vouchered specimens at the Nouragues biological station and at Chutes Voltaire (AF1288/
R145, and AF1755/MNHN 2014.0119, respectively). These two recordings display similar temporal and spectral
structures, but their quality was too low to be properly analysed. Despite the absence of voucher specimens for the
calls we analysed, we consider that these recordings can be unambiguously attributed to each species. Calls were
also compared to the call of H. geographicus from Bolivia available from Márquez et al. (2002).
Calls were analysed at a sampling rate of 44.1 kHz using Audacity (http://audacity.sourceforge.net/). We
measured call duration (beginning of the first to the end of the last note of a call); number of notes per call (a call is
here defined as a series of notes emitted in groups between longer silent intervals); note duration (beginning of the
note to the end of the note); pulses per second (mean number of pulses/second calculated in 3 notes); internote
silent interval (end of one note to beginning of the next); intercall silent interval (end of one call to the beginning of
the next; as summarized in Kok & Kalamandeen 2008). Peak of the dominant frequency of the note was measured
from a spectral slice taken through each entire call (using the Blackman window function at a 3 dB filter bandwidth
of 120 Hz). Call characteristics of the new species compared to those of H. aff. semilineatus 1 and H. geographicus
are illustrated as spectrograms using the R package SEEWAVE (Sueur et al. 2008).
Results
Phylogenetic analysis. Hypsiboas boans is recovered as the sister species of a clade formed by all the other
representatives of the H. semilineatus group included in this study (i.e. nine main lineages). These lineages display
poorly supported relationships among them (Fig. 2, one of them corresponds to the new species described herein).
Hypsiboas geographicus sensu stricto includes samples from southwestern and central Amazonia: Tefé (Amazonas,
Brazil), Bolivia, Serra do Divisor (Acre, Brazil) and Rio Purus (Amazonas, Brazil); and H. cf. geographicus 1
includes samples from central and eastern Amazonia: Caxiuanã (Pará, Brazil), Jirau (Rondônia, Brazil) and Rio Içá
(Amazonas, Brazil). Genetic distances among these lineages are substantial: > 4.8% in the targeted fragment of 16S
(Table 2). The other six lineages display lower genetic distances (> 2.1% among them, minimum found between H.
semilineatus and H. aff. semilineatus 3) and form a strongly supported clade hereafter referred to as the H.
semilineatus clade (Fig. 2). This clade comprises H. semilineatus from the Atlantic Forest, H. aff. semilineatus 1
from the Guiana Shield, H. aff. semilineatus 2 from Eastern Amazonia, H. aff. semilineatus 3 from Southeastern
Amazonia, H. aff. semilineatus 4 from central Amazonia, and H. aff. semilineatus 5 from central Amazonia.
Hypsiboas geographicus identity. Considering that several species might be involved under the name
Hypsiboas geographicus, the only unambiguous diagnostic characters that can be used to differentiate species
similar to H. geographicus rely so far on the succinct description and the illustration of Spix (1824). We attempted
in vain to find museum specimens from Tefé, and the curator of the Berlin Museum confirmed that the holotype is
lost (M.O. Rödel pers. com.).
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FIGURE 2. Phylogram (50% majority rule with frequencies of all observed bipartition) inferred from Bayesian Analysis of
850 bp of the 16S gene. Posterior probabilities (*100) are indicated on the upper left of the nodes (*=0.99 or 1; not indicated
when <0.5).
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TABLE 2. Mean genetic distances (p-distance, lower diagonal) and sd (upper diagonal, estimated using 100 bootstraps
replicates) among major lineages using pairwise deletion
.
However, a specimen recently collected in Tefé and the specimens from Purus and Serra do Divisor, which
form a clade altogether, are morphologically similar and match well the pattern described by Spix in the original
description of H. geographicus. These specimens are characterized by (1) numerous (8–10) dark grey transversal
bands on the granular dorsal surface of thigh and tibia, extending towards the ventral face of the leg (best visible in
preservative); (2) granular skin on upper thigh covering a broad surface (as broad as the inner and outer smooth
faces of thigh); (3) inner and outer faces of thigh, tibia and flank from dark grey with transversal stripes to black (in
life and in preservative); (4) dark spots on the belly in life and in preservative; (5) reduced hand webbing between
Fingers II–IV; and (6) hand and foot webbing red except between Fingers III–IV and Toes IV–V (grey), fingers and
toes dorsally grey except Finger I and Toes I–II (red). We consider these characters as diagnostic for H.
geographicus sensu stricto, and consider all the specimens belonging to this clade as H. geographicus. The call
from Bolivia provided by Marquez et al. (2002) corresponds to the call of the specimens genotyped by Jansen et al.
(2011; Jansen com. pers.). Sequences from these specimens and from the tadpole described by Schulze et al. (2015)
from Bolivia are included in our phylogenetic analysis. Both call and tadpole can thus be unambiguously identified
as those of H. geographicus sensu stricto. A formal redescription of this taxon is cleary needed, but the available
material from the type locality (one specimen only) is currently insufficient for an accurate description and analysis
of variation. Therefore, we refrain to redescribe this taxon until additional topotypic material is available (see
below).
Candidate species within the H. semilineatus species group. Except the new species described hereafter, all
the other major lineages identified in this study are considered to be candidate species, and their taxonomic status
needs to be clarified. Phylogeography, genetic distances, and overall morphology indicate that some clades
unambiguously correspond to undescribed species whereas the taxonomic status of some lineages remains less
clear (e.g. within the H. semilineatus clade) and deserve further investigation, which is beyond the scope of this
paper. We tentatively grouped samples under the names H. cf. geographicus 1 (given its ambiguous relationship
with any nominal taxon) and H. aff. semilineatus 1–5 (for the lineages related to H. semilineatus), pending
additional data.
Known junior synonyms of Hypsiboas geographicus are all from the Atlantic Forest, except H. appendiculata
(Boulenger, 1882), for which a lectotype from Canelos, Ecuador (BMNH 1947.2.13.1) was designated by Parker
(1933). Hypsiboas appendiculata has vertical blackish lines on flanks, which immediately distinguishes it from the
two species occurring in the Guiana Shield. We conclude that the new species described hereafter unambiguously
differs from both Hypsiboas geographicus and its junior synonym H. appendiculata.
New species description
Hypsiboas diabolicus sp. nov.
Hypsiboas geographicus Fouquet et al., 2007
Hypsiboas aff. geographicus Dewynter et al., 2008
1. 2. 3. 4. 5. 6. 7. 8. 9.
1. H. aff. semilineatus 1 0.006 0.008 0.008 0.01 0.011 0.01 0.012 0.013
2. H. semilineatus 0.023 0.008 0.006 0.009 0.012 0.009 0.012 0.014
3. H. aff. semilineatus 2 0.035 0.031 0.009 0.011 0.012 0.011 0.013 0.014
4. H. aff. semilineatus 3 0.034 0.021 0.046 0.011 0.012 0.01 0.013 0.014
5. H. aff. semilineatus 4 0.04 0.033 0.054 0.044 0.012 0.011 0.012 0.013
6. H. cf. geographicus 1 0.068 0.065 0.069 0.065 0.067 0.014 0.01 0.011
7. H. aff. semilineatus 5 0.051 0.035 0.057 0.038 0.051 0.08 0.013 0.015
8. H. geographicus 0.059 0.06 0.068 0.06 0.062 0.05 0.072 0.01
9. H. diabolicus sp. nov. 0.079 0.083 0.083 0.084 0.084 0.066 0.087 0.048
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Holotype. R157 (AF1284), an adult male collected by AF and QM at Nouragues biological station near “Pont
Ficelle” on Crique Nouragues, (4.08479, -52.68063, 100 m elevation) in the Reserve Naturelle des Nouragues,
municipality of Régina, French Guiana, on 1 June 2013 (Fig. 3).
Paratypes (n=18; numbers between parentheses correspond to field numbers) (Fig. 3). R150 and 151
(AF0594–5), two adult males collected by AF at Piste St Elie (5.341557, -53.03882; 10 m elevation) municipality
of Sinnamary, French Guiana on 1 March 2012; R152 (AF0667) an adult male collected by AF at Chutes
Fourgassié (4.627158, -52.307289, 30 m elevation) municipality of Roura, French Guiana on 7 April 2012; MNHN
2014.0103 (QM459) an adult male collected by QM at « Arlésienne » pond (4.5787333, -52.01965, 200 m
elevation) municipality of Roura; R153 (AF0701), an adult male collected by AF at Paracou (5.272546, -
52.923596, 10 m elevation) municipality of Sinnamary, French Guiana on 29 April 2012; R154 (AF1115), an adult
male collected by AF at “Crique Bon Espoir” near the left margin of the Mana River (5.099493, -53.800571, 50 m
elevation) municipality of St Laurent du Maroni, French Guiana on 1 April 2013; R158, 159 and 155 (AG196,
AG294, AF1185), three adult males, and R160 (AG290) an adult female, collected by Michel Blanc, AF, and
Elodie A. Courtois (EAC) at Aya camp in the Reserve Naturelle de la Trinité (4.608465, -53.415191, 150 m
elevation) municipality of St Elie, French Guiana on 15 January 2007 and 1 May 2013; R156 and MNHN
2014.0109 (AF1283, AF1304), two adult males collected by AF, QM and EAC with the holotype; R161 (AG064),
an adult female collected by Benoit de Thoisy on the Counamy river (5.403682, -53.274515, 10m elevation)
municipality of Iracoubo, French Guiana on 16 July 2001 (this specimen was not measured); MNHN 2014.0104-8
(AF1829, 1828, QM293, 307, 437) an adult female and an adult male collected by Jean-Pierre Vacher and Andy
Lorenzini on 20 March 2014, and three adult males collected by QM on 13 January 2014 at Montagne des singes
(5.06967, -52.6968, 20 m elevation) municipality of Kourou, French Guiana; R149 (AF1092), an adult male
collected by AF near Vila Vitoria (3.904047, -51.77227, 10 m elevation) municipality of Oiapoque, Amapá, Brazil
on 1 March 2013; IEPA5028 (FTA114), an adult male collected by Jucivaldo Dias Lima at Rio Vila Nova within
FLOTA, (0.46966,-52.020493, 100 m elevation) municipality of Mazagão Amapá, Brazil (this specimen was not
measured); IEPA3099 (STD290), an adult male collected by Jucivaldo Dias Lima at Serra Macacoara within
Parque Nacional das Montanhas do Tumucumaque (0.909122, -53.228479, 150 m elevation), municipality of
Laranjal do Jari, Amapá, Brazil (this specimen was not measured).
Etymology. The specific name is a noun in apposition and refers to the “Diables Rouges” (Red Devils),
traditional characters of the carnival in French Guiana who dress in red and black, reminiscent of the black flanks
and the carmine/crimson legs and webbing of the new species (colours 62, 64 in Köhler 2012).
Definition and diagnosis. The new species is morphologically characterized by the following unique
combination of characters: (1) medium size, adult males X=43.5 mm (38.5–48.0 mm, n=17), adult females X=56.3
mm (55.9–56.7 mm, n=2; Table 3); (2) thighs long (ThL/SVL 0.50–0.58); (3) dorsal skin finely granular; (4) dorsal
colour pattern generally consisting of a X-shaped mark on the scapular region; (5) typically 6–8 large dark brown
bands on the granular dorsal surface of tibia and thighs, not extending towards the ventral face of the leg; (6)
granular skin on upper thigh covering a narrow surface (narrower than inner and outer smooth faces of thigh); (7)
flanks black with white speckles, well delimited ventrally; (8) ventral surface immaculate; (9) lower eyelid
translucent with thin brownish reticulations; (10) snout long ETS/EN 0.67–0.89 and slightly acuminate in lateral
view; (11) superelliptical pupils when contracted; (12) hands, feet and concealed surfaces of legs carmine/crimson
(in life) to light grey (in preservative) without white spots; (13) large and rugous dark P-shaped nuptial pad on the
medial surface of Finger I extending onto the dorsal surface in males; (14) prepollex not modified into a projecting
spine; (15) concealed surface of upper arm, axillary region, flanks, and groin black with numerous small bluish
white speckles; (16) fingers fully webbed; (17) feet fully webbed; (18) small calcar on heel, sometimes barely
visible and often coloured with a cream spot.
Morphological comparison with congeners of the semilineatus group. The new species is unambiguously
assigned to the Hypsiboas semilineatus species group based on molecular analyses (Fouquet et al. 2007; this work)
as well as by the presence of a reticulated lower eyelid. The new species is closely related to a subgroup containing
H. semilineatus, H. geographicus and H. hutchinsi that can all be distinguished from other species of the
semilineatus group (H. boans, H. wavrini and H. pombali) by smaller size, prepollex not modified into a projecting
spine, presence of pigmented nuptial excrescences, and finely granular dorsal skin.
We closely compared the new species with the six nominal species of the Hypsiboas semilineatus group (H.
boans, H. geographicus, H. hutchinsi, H. pombali, H. semilineatus, and H. wavrini), and with H. aff. semilineatus 1
since that candidate species occurs in sympatry (other candidate species are phylogenetically distinct and
allopatric). The presence of immaculate red webbing on fingers and toes, and the red concealed surfaces of hind
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limbs immediately distinguish Hypsiboas diabolicus sp. nov. from H. semilineatus and H. aff. semilineatus 1
(webbing brown, dorsoposterior concealed surface of hindlimbs dark grey with white spots, and anterior concealed
surface of hindlimbs cream with dark stripes in H. semilineatus and H. aff. semilineatus 1), from H. geographicus
(red webbing except between Fingers III–IV and Toes IV–V, fingers and toes grey dorsally except Finger I and
Toes I–II, and dorsoposterior and anterior concealed surface of hindlimbs grey with black stripes in H.
geographicus), and from H. hutchinsi (webbing and concealed surfaces of hindlimbs black in H. hutchinsi).
Hypsiboas diabolicus sp. nov. can be further distinguished from H. geographicus by its immaculate venter (vs.
with dark spots in H. geographicus), by its longer snout (ETS/EN 0.67–0.89 vs. 0.53–0.69 in H. geographicus), by
its longer thighs (ThL/SVL 0.50–0.58 vs. 0.44–0.49 in H. geographicus), by its less acuminate snout, and by its
more developed hand and foot webbing. Hypsiboas diabolicus sp. nov. can be further distinguished from H. aff.
semilineatus 1 by a sharp delineation between the dorsal and the flank patterns (vs. dark stripes in H. aff.
semilineatus 1), by its smaller SVL (43.5±2.6 vs. 48.1±2.5 mm in H. aff. semilineatus 1; Table 3, Fig. 5A), and by
its slightly acuminate snout in lateral view (truncate in H. aff. semilineatus 1). The new species is easily
distinguished from H. boans, H. wavrini and H. pombali by its smaller size, red colouration of concealed surface of
hindlimbs and webbing (never red in H. boans and H. wavrini), and absence of a prepollex modified in a projecting
spine.
Description of holotype (Fig. 3). An adult male (48.0 mm SVL). Dorsal skin finely granular, less granular on
head except on its sides. Head as long as wide (HW/HL 0.97), cranial crests absent. Snout slightly acuminate in
lateral view, much longer than eye length (ETS/ED 1.62); canthus rostralis curved and loreal region strongly
concave; eye-naris distance longer than eye length (EN/ED 1.13). Nares directed laterally, visible from frontal and
dorsal views. Lower eyelid finely reticulated, pupil superelliptical. Tympanum round, 3.4 mm long (TD/EL 0.73).
Supratympanic fold inconspicuous, post-rictal tubercles absent. Vocal sac single and subgular, visible. Throat
smooth anteriorly without mental gland, posterior surface of throat, belly, cloacal region, and undersurface of
thighs areolate, undersurface of tibia and tarsus smooth. Dentigerous processes of the vomers oblique, closely set,
each bearing 13 teeth. Vocal slits present. Tongue slightly cordiform.
Hand length/SVL 0.30. Relative length of fingers: I<II<IV<IIII; Finger I/Finger II 0.78; adpressed Finger I
fails to reach proximal edge of finger disc of Finger II; adpressed Finger IV reaches base of disc of Finger III on
both sides. Large and rugose dark P-shaped nuptial pad on medial and dorsal surface of Finger I, prepollex not
modified into a projecting spine. Two lateral fringes on hand and arm, one extending latero-dorsally from the
second segment of Finger IV to the anterior edge of the elbow and one extending latero-ventrally from the disc of
Finger IV to the posterior edge of the elbow forming a metacarpal and an ulnar fold. Fingers fully webbed,
webbing formula I 2
+
—2
-
II 1
-
—2 III 1
-
—1
-
IV. Finger discs broadly expanded, round, as wide as long; disc of
Finger III (1.9 mm) 1.5 times wider that the distal end of the adjacent phalanx. Palmar tubercle inconspicuous;
thenar tubercle indistinct; supernumerary tubercles absent; subarticular tubercles large, round and protuberant, one
tubercle on Finger I and Finger II, two tubercles on Finger III and Finger IV (with the second one much smaller);
many small round accessory palmar tubercles.
Hind limbs long, heels slightly overlap when bent limbs are held at right angles to sagittal plane; TiL/SVL
0.55; FL/SVL 0.39 Relative length of toes I<II<III<V<IV; tip of Toe V extends to the distal edge of the distal
subarticular tubercle on Toe IV; tip of Toe III extends to the proximal edge of the distal subarticular tubercle on Toe
IV. Two lateral fringes along foot and leg, one extending from the proximal edge of the inner metatarsal tubercle to
knee and even further delimiting the concealed part of the leg forming a tarsal fringe, and one extending laterally
from the base of the disc of Toe V to the tarsus, forming a tarsal fold interrupted before the calcar. Toes fully
webbed, webbing formula I 0
-
–1
-
II 0
-
–1
1/3
III 0-–1
-
IV 1
-
–0
-
V. Toe discs slightly smaller than finger discs, broadly
expanded, round. Inner metatarsal tubercle elongate, oval; outer metatarsal tubercle absent; subarticular tubercles
round, large and protuberant; supernumerary plantar tubercles small, round.
Colour of the holotype in preservative (Fig. 3). After two years in 70% ethanol, the dorsal background
colour faded to light brown, with fine dark brown irregular transversal reticulations also present on the dorsal
surface of arms and legs. Five small cream round spots (colour 1 in Köhler 2012) on the posterior half of the body.
A large light cream spot (colour 1 in Köhler 2012) at the tibio-tarsal articulation, extending to the calcar. Hands,
feet and concealed surfaces of legs pale pinkish (colour 3 in Köhler 2012). Lips, throat and chest cream (colour 1 in
Köhler 2012). Belly, ventral surface of arms and thighs, and ventral surface of hands, tarsi and feet pale pinkish
(colour 3 in Köhler 2012). Concealed surface of upper arms, axillary region, flanks, and groin black with numerous
white speckles.
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TABLE 3. Mean and sd of measurements of specimens of H. diabolicus sp. nov, H. aff. semilineatus 1 and H. geographicus; abbreviations are explained in the text.
SVL TiL CL ThL TaL FL 4TD FD 1FiL 2FiL HaL ETS EN HL HW IN ED IOD TYD
H. aff. semilineatus 1 M n=20 48.40 25.20 1.33 25.50 14.50 18.00 1.79 2.12 7.61 10.40 13.90 7.92 5.95 17.29 17.07 3.35 5.28 5.72 4.06
2.23 1.41 0.48 1.42 1.67 1.58 0.27 0.34 0.47 0.55 0.73 0.60 0.47 1.18 1.42 0.26 0.96 0.46 0.28
H. aff. semilineatus 1 F n=3 68.30 34.80 1.93 35.90 20.50 26.20 3.13 3.60 10.60 14.90 19.70 16.30 9.63 23.87 24.43 4.43 6.07 7.40 5.13
3.03 0.78 0.67 0.93 0.66 0.53 0.42 0.26 0.67 0.75 0.64 8.52 2.57 1.76 1.79 0.06 0.59 0.26 0.32
H. diabolicus sp. nov. M n=17 43.50 23.20 0.91 23.50 13.30 16.30 1.61 1.92 6.79 9.20 12.30 7.26 5.39 15.75 15.95 2.98 5.28 5.41 3.55
2.56 1.56 0.25 1.75 1.05 1.40 0.24 0.23 0.63 0.79 1.21 0.76 0.59 1.63 1.03 0.26 0.50 0.50 0.22
H. diabolicus sp. nov. F n=2 56.30 30.30 1.05 29.60 18.10 21.60 2.05 2.35 9.10 12.20 16.50 9.70 6.40 20.50 20.90 3.85 5.60 6.00 4.45
0.57 0.49 0.78 0.57 0.35 1.63 0.21 0.64 0.57 0.35 1.63 0.71 0.57 1.697 1.84 0.64 0.14 0.42 0.35
H. geographicus M n=5 43.00 23.10 0.84 19.70 13.40 17.00 1.96 2.18 6.73 9.45 12.40 7.52 4.68 14.82 15.59 3.11 4.42 8.83 3.11
1.62 0.48 0.16 0.47 0.59 0.90 0.12 0.18 0.53 0.64 0.65 0.41 0.50 0.56 0.88 0.03 0.13 0.24 0.04
H. geographicus F n=5 48.60 26.90 1.03 22.40 15.80 19.50 2.18 2.44 7.65 10.80 14.4 8.29 5.48 16.99 17.84 3.50 4.89 10.00 3.74
2.62 1.68 0.33 1.61 1.42 1.49 0.18 0.22 0.57 0.69 0.93 0.56 0.38 1.136 1.573 0.2 0.29 0.49 0.31
TABLE 4: List of measured tadpoles. A = LTRF on anterior labium, P = LTRF on posterior labium, other abbreviations are explained in the text.
Species Locality Voucher Gosner A P TL BL TAL BW BH HW TMH UTF LTF TMW MTH END NSD SSD IND IOD ED Date Coll.
H. diabolicus sp. nov GaaKaba MBT136D 27 2(2) 4(1) 20.4 8.3 12.3 4.8 4.3 4.2 1.3 1.3 1.3 1.4 4.0 0.9 1.0 5.4 1.7 3 0.9 14 09 2010
H. diabolicus sp. nov GaaKaba MBT136C 27 2(2) 4(1) 21.4 9.2 12.2 5.5 4.7 4.3 1.6 1.3 1.2 1.6 4.1 0.8 1.0 5.9 1.6 2.6 0.9 14 09 2010
H. diabolicus sp. nov GaaKaba MBT136B 28 2(2) 4(1) 23.9 9.9 14.0 5.9 4.6 4.6 1.8 1.5 1.4 1.9 4.7 1.0 1.2 6.4 1.8 3 0.9 14 09 2010
H. diabolicus sp. nov Mont. des singes QM474B 29 2(2) 4(1) 25.2 11.1 14.0 6.2 3.9 5.2 2.0 1.6 1.5 1.3 4.6 1.0 1.1 7.0 1.9 3.1 1.5 20 06 2014
H. diabolicus sp. nov Patawa AF2362I
31 3(1,3) 5(1,5) 35.0 13.8 21.3 7.7 6.8 6.5 2.9 2.5 2.7 2.7 7.0 1.5 1.1 8.9 1.9 3.9 1.5 19 07 2014
H. diabolicus sp. nov Patawa AF2362B
32 3(1,3) 5(1,5) 37.4 13.9 26.7 9.2 8.0 6.8 3.1 2.9 2.8 2.9 8.0 1.4 1.5 9.6 2.3 4.1 1.5 19 07 2014
H. diabolicus sp. nov Patawa AF2362D
36 3(1,3) 5(1,5) 43 14.5 27.7 11.1 10.2 8.1 4.3 3.2 2.9 3.6 9.1 1.5 1.7 10.9 2.6 5.7 1.8 19 07 2014
H. diabolicus sp. nov Patawa AF2362F
34 3(1,3) 5(1,5) 38.8 15.2 25.2 9.4 7.1 6.9 2.9 2.8 2.7 3.0 8.3 1.5 1.6 9.5 2.4 4.4 1.8 19 07 2014
H. diabolicus sp. nov Patawa AF2362C
38 3(1,3) 5(1) 46.4 17.5 29.8 10.8 9.5 8.5 4.1 3.6 3.5 3.3 10.7 1.7 2.0 10.1 2.7 5.5 1.8 19 07 2014
H. diabolicus sp. nov Patawa AF2362E
38 3(1,3) 5(1) 43.7 18.0 26.1 11.9 9.3 9.1 4.5 3.9 3.0 3.9 10.7 1.9 2.0 11.7 2.9 5.9 2.1 19 07 2014
H. aff. semilineatus 1 Sipaliwini AF1996A
29 3(1,3) 5(1,5) 24.8 9.5 15.0 6.0 4.8 4.7 2.1 2.0 1.8 1.7 5.1 0.9 1.3 6.4 1.9 3.2 1.2 18 04 2014
H. aff. semilineatus 1 Crique mirat AF1303C 34 4(1,2,4) 6(1,6) 45.2 16.9 28.5 10.9 9.5 7.0 4.1 3.1 2.8 2.8 9.0 1.2 1.9 11.1 2.7 5.5 1.7 06 01 2005
H. aff. semilineatus 1 Crique mirat AF1303B 35 4(1,2,4) 6(1,6) 48.7 17.0 31.4 10.9 7.9 7.5 3.6 3.0 3.0 2.8 9.4 1.7 1.8 8.1 2.6 4.6 2.1 06 01 2005
H. aff. semilineatus 1 Crique mirat AF1303D 37 4(1,2,4) 6(1,6) 52.7 19.0 37.7 12.6 10 8.0 4.5 2.8 3.6 2.9 10.1 1.9 1.8 11.7 2.8 6.2 2.0 06 01 2005
H. aff. semilineatus 1

AF1112 40 4(1,2,4) 6(1,5) 53.2 20.8 32.4 12.7 10.5 9.5 3.8 4.1 4.3 4.1 12.1 2.2 2.1 12.7 2.9 7.0 2.4 04 04 2013
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FIGURE 3. Holotype R157 (AF1284) of H. diabolicus sp. nov. compared to R143 (AF1285), a specimen of H. aff.
semilineatus 1 (both recently preserved) collected along the same stream at the same time, and H. geographicus [preserved
specimen MZUSP157060 (MTR36895) from Tefé]. a: in life (H. geographicus from Rio Purus active at night); b: dorsal view;
c: ventral view; d: lateral view of the head; e ventral face of right hand and foot.
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FIGURE 4. Intraspecific variation in Hypsiboas diabolicus sp. nov. as shown by dorsal and ventral views of nine specimens of
the type series. Numbers between parentheses correspond to field numbers.
Colour of the holotype in life at night (Fig. 3). Dorsal background colour dark orange rufous (colour 56 in
Köhler 2012), with ill-defined lighter brownish orange spots and ill-defined darker reticulations. Transverse brown
bars on arms and legs. Dorsal surface of tarsi and distal half of feet orange with poorly defined brown bars. Five
small round cream spots (colour 1 in Köhler 2012) on the posterior half of the body. A large cream spot (colour 1 in
Köhler 2012) at the tibio-tarsal articulation, extending to the calcar. Hands, feet and concealed surfaces of legs
carmine/crimson. Lips orange. Throat and chest white. Belly and ventral surface of thighs bright orange. Ventral
surface of hands, tarsi and feet carmine/crimson. Concealed surface of upper arms, axillary region, flanks, and
groin black with numerous bluish white speckles. Iris brownish orange, lighter dorsally, surrounded by a black
circle; eyeball white with a dark blue region posterodorsally, bones white.
Variation (Fig. 4). The most noticeable variation occurs in the dorsal colouration and in the shape of the
calcars. Hypsiboas diabolicus sp. nov. is highly variable in colour and pattern. Background colouration ranges
from dark brown to light brown, and dorsal pattern varies from fine reticulations to large transverse brown
chevrons. A X-shaped brown mark is often present in the scapular region and is generally thin, rarely thick.
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Markings on the dorsal part of the legs range from small dark reticulations to chevrons, which range from cream to
light brown. Individuals may display asymmetrically distributed small to large cream spots on the dorsum. The
bluish white speckles on the black flanks vary in size and number among individuals; some individuals have small
dark spots extending on the belly. In preservative, the red colouration first fades to orange then turn into pale
pinkish (colour 3 in Köhler 2012). Females have similar colouration than males, but are larger. Calcar size ranges
from inconspicuous to prominent, which does not seem to be associated with any sexual dimorphism; calcars are
generally coloured with a cream spot.
FIGURE 5. (A) Boxplots of adult SVL of H. diabolicus sp. nov. and H. aff. semilineatus 1 for each sex. A Student t-test was
performed on males and shows statistically significant differences between species (p<0.001). (B) Tadpole total length as a
function of Gosner stage for both species (H. diabolicus in white H. aff. semilineatus 1 in black). Ontogenetic changes of LTRF
are also indicated.
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FIGURE 6. External and buccal morphology of tadpoles of Hypsiboas diabolicus sp. nov. and H. aff. semilineatus 1. Arrows
highlight some diagnostic characters (upper labium and A2 gaps, marginal papillae).
Description of the tadpole. The following description is based on one individual in Gosner stage 27 (R168
Fig. 5B, Fig. 6, Table 4). Type 4 tadpole (Orton 1953); exotrophic; body skin smooth; TL 21.4 mm; BL/TL 0.43,
BL/BW 1.7, BL/BH 2.0, BW/BH 1.2. Body depressed, oval in dorsal view; snout round in dorsal and lateral views;
eyes positioned and directed dorsolaterally; ED 0.9 mm, ED/IOD 0.35; IOD less than IND; nares positioned and
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directed anterodorsally; narial opening reniform in dorsal view; END 0.8 mm, less than NSD (1.0 mm). Spiracular
tube sinistral, projecting posterodorsally, its base located 64 % of BL from snout. Vent tube not visible, concealed
in a dermal fold. Lateral line system conspicuous. Caudal musculature highest at body-tail junction, tapering
posteriorly, terminating anterior to tail tip; tail tip tapered, rounded; upper fin originating anterior to junction of
body and tail, gradually increasing in height to about midlength of tail, decreasing to tail tip; UTF/TMH 0.81;
comparable ULF/TMH 0.75; lower fin gradually similar in height along the 2/3 of the tail and decreasing to
terminus; MTH/TL 0.34.
Mouth ventral, oral disc strongly emarginated posteriorly, width 2.4 mm. Labial teeth long, in single rows,
LTRF 2(2)/4(1). A-2 consisting of two short rows, separated by a large and deep gap, A-1 slightly shorter than
posterior rows that are of equal length; P-1 medially interrupted by a small gap. Marginal papillae moderately long,
tapered, blunt-tipped, in a single row; broad median gap on upper labium approximately half the length of A-1. A
few submarginal papillae present laterally; jaw sheaths typical, large, serrated, lower jaw sheath broadly V-shaped.
Variation of 17 meristic characters from tadpoles in stages 27–39 is given in Table 4. Considerable variation
occurs in the number of posterior labial teeth rows, ranging from 2(2)/4(1), 3(1,3)/5(1,5) and 3(1,3)/5(1) and in the
number of submarginal papillae laterally; apparently this variation is largely ontogenetic. Body and tail are black to
dark brown.
The tadpole of Hypsiboas diabolicus sp. nov. can be distinguished from that of H. geographicus (described by
Schulze et al. 2015), H. aff. semilineatus 1 [from examined material and previously described by Duellman and
Lescure (1973) from French Guiana] and from that of H. semilineatus [described by Bokermann (1963) and
d’Heursel & de Sá (1999)] by: (1) smaller size [TL 46.4 mm maximum at stage 38 in H. diabolicus vs. TL 48.6 mm
at stage 35 and 59.7 mm at stage 41 in H. geographicus/TL 46.4 mm maximum at stage 38 and >56.3 mm at stage
40 in H. aff. semilineatus 1/TL>65 mm in H. semilineatus (Bokermann 1963)] (Fig. 5B, Table 4); (2) larger upper
labium gap in marginal papillae than in H. aff. semilineatus 1 (0.85 mm in H. diabolicus R168 vs. 0.75 mm in H.
aff. semilineatus 1 AF2362I) (Fig. 6 ; but of similar proportion in H. geographicus); (3) large and mostly single-
rowed marginal papillae (vs. irregularly biseriate laterally and on lower labium in H. geographicus, small and
double-rowed in H. aff. semilineatus 1 and H. semilineatus); and (4) larger A-2 gap (only slightly larger than in H.
geographicus and clearly larger than in H. aff. semilineatus 1; 0.25 mm in H. diabolicus R168 vs. 0.12 mm in H.
aff. semilineatus 1 AF2362I). The tadpole of H. diabolicus can also be distinguished in having more teeth rows at
similar stage than in H. geographicus: 3(1,3)/5(1,5) at stage 30–40 in H. diabolicus vs. 2(2)/4(1) a stage 35 in H.
geographicus, but fewer teeth rows at similar stage than H. aff. semilineatus 1 and H. semilineatus
: at stage 27–29:
2(2)/4(1) vs. 3(1,3)/5(1,5) in H. aff. semilineatus 1 and at stage 30–40 3(1,3)/5(1,5) vs. 3(1,3)/5(1) to 4(1,2,4)/
6(1,6) in H. aff. semilineatus 1 (present data, Table 4); 2(2)/4 in H. semilineatus at stage 36 (Bokermann 1963).
The tadpole of the new species differs from that of Hypsiboas hutchinsi by its black to dark brown tail
(creamish pink in life, sometimes with a dark spot in H. hutchinsi), and lower number of teeth rows (3/5 in H.
diabolicus vs. 4/7 in H. hutchinsi; Pyburn & Hall 1984).
The tadpole of the new species differs from that of Hypsiboas boans and H. pombali by its black to dark brown
colouration [body beige with reddish brown spots and dark brown specks in H. boans and H. pombali (Junca et al.
2012)], upper and lower fins of similar size (upper fin larger in H. boans and H. pombali) and a larger A-2 gap].
The tadpole of Hypsiboas diabolicus differs from that described and attributed to H. geographicus from
Trinidad by Kenny (1969) by smaller body size and LTRF (reported to reach 75.0 mm and to have small and
numerous marginal papillae and lacking an A2 gap in Trinidad), and from that of the species studied by Caldwell
(1989) from Rondônia (Brazil) by smaller size (reported to be >50 mm from stage 37, reaching >90 mm in
Rondônia).
The tadpoles from Reserva Adolfo Ducke examined by d’Heursel and de Sá (1999) and identified as
Hypsiboas geographicus match with the tadpoles of H. aff. semilineatus 1. As mentioned previously, the species
reported by Lima et al. (2006) from this location matches with H. aff. semilineatus 1, none of the other lineages
have been recorded north of the Amazon River and the tadpoles of d’Heursel and de Sá (1999) differ from H.
diabolicus and H. geographicus (see above). Nevertheless, the status of this population was not assessed in our
study, and thus remains tentative.
Advertisement call (Fig. 7). Calling specimens, perched ~1m above ground on vegetation near standing
water, were recorded at a distance of about 1 m. The call of the new species is very soft and consists of short
clusters (X=0.33 s; range=0.24–0.39 s) of 2–3 chuckles (X=0.05 s; range=0.04–0.07 s) with an internote interval of
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X=0.11s (range=0.10–0.13 s) emitted between silent intervals of X=6.01 s (range=3.06–10.72 s; Fig. 7, Table 5).
Each note consists of pulses emitted at X=186.8 pulses/s (range=175.5–200). The call has a fundamental frequency
dominating (X=1.16 kHz, range=1.11–1.19 kHz).
FIGURE 7. Spectrograms of calls of H. diabolicus sp. nov. (bottom), H. aff. semilineatus 1 (middle) and H. geographicus (top,
from Marquez et al. 2002).
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TABLE 5. Call variables of four calls of Hypsiboas diabolicus sp. nov. compared to H. aff. semilineatus 1 and H. geographicus
(recording in Marquez et al. 2002).
The call of Hypsiboas diabolicus sp. nov. is distinguished from that of H. aff. semilineatus 1 (Fig. 7; Table 5)
by shorter notes (X=0.05 s; range=0.04–0.07 s vs. X=0.11 s; range=0.07–0.13 s in H. aff. semilineatus 1), shorter
internote intervals (X=0.11 s; range=0.10–0.13 s vs. X=0.16 s; range=0.14–0.18 s in H. aff. semilineatus 1), and
higher dominant frequency (X=1.16 kHz, range=1.11–1.19 kHz vs. X=0.88 kHz, range=0.81–0.91 kHz in H. aff.
semilineatus 1). Hypsiboas aff. semilineatus 1 also generally produces more notes per call (X=4.5; range 3–7) than
H. diabolicus (X=2.75; range 2–3), and a first note louder than the following ones whereas the notes contain the
same energy across the call of H. diabolicus. A call recorded in Bolivia is available from Marquez et al. (2002) and
corresponds to H. geographicus (same lineage as identified as H. geographicus in this study, Jansen pers. com.).
That call shares many similarities with the call of H. diabolicus, and also matches the call described by Duellman
(1973) from Santa Cecilia, Ecuador. However, the dominant frequency of the call of H. geographicus is lower
(0.94 in H. geographicus vs. 1.16 kHz in H. diabolicus), more notes per call are produced (3–4 in H. geographicus
vs. 2–3 in H. diabolicus), notes are emitted at a faster rate (internote intervals = 0.08 in H. geographicus vs. 0.11 s
in H. diabolicus), and the pulses are emitted faster (216/s in H. geographicus vs. 187/s in H. diabolicus). The new
species’ call is also clearly distinct from the one of H. hutchinsi that consists of more notes (5–7 in H. hutchinsi vs.
2–3 in H. diabolicus), each note being longer (0.10 s in H. hutchinsi vs. 0.04–0.07 s in H. diabolicus), and with a
decrease of intensity of the notes within the call. It also clearly differs from the calls of H. geographicus described
by Duellman (2005) from Pilcopata (dominant frequency = 1.75 kHz) and Tambopata, Peru (dominant frequency =
2.3 kHz).
Distribution and Ecology.
To date Hypsiboas diabolicus sp. nov. has been found throughout French Guiana
(except in the southeast) and in Amapá, Brazil, between 10–150 m elevation. It occurs in sympatry with H. aff.
semilineatus 1 over its entire distribution area, but the latter species seems more widely distributed over the Guiana
Shield.
Both species have been found active at night, sometimes at the very same time and locality. Nevertheless, the
two species seem to display slight differences in reproduction sites. Hypsiboas diabolicus generally breeds in pools
formed at the margin of small streams whereas H. aff. semilineatus 1 usually breeds in larger rivers, generally in
marginal pools formed in regularly flooded parts of the bed. Males of H. diabolicus. were generally found
H. diabolicus sp. nov. H. aff. semilineatus 1
call 1 call 2 call 3 call 4 Mean call 1 call 2 call 3 call 4 Mean
Call duration (s) 0.34 0.24 0.37 0.39 0.33 1.88 1.50 0.64 0.52 1.13
notes/call 32332.7575334.50
Note duration (s) 0.05 0.05 0.06 0.05 0.05 0.13 0.13 0.11 0.07 0.11
Pulses/s NA 200.00 185.00 175.60 186.90 154.40 151.90 177.80 200.00 171.00
Internote silence (s) 0.10 0.13 0.10 0.11 0.11 0.18 0.17 0.14 0.15 0.16
Note dom freq (Hz) 1189 1189 1108 1149 1159 905 870 830 905 877
Intercall silence (s) 3.06 4.24 10.72 NA 6.01 1.60 0.50 0.40 0.60 0.77
H. geographicus
call 1 call 2 call 3 call 4 Mean
Call duration (s) 0.40 0.42 0.36 0.40 0.39
notes/call 34433.50
Note duration (s) 0.05 0.05 0.04 0.05 0.05
Pulses/s 218 226 206 214 216.10
Internote silence (s) 0.10 0,07 0.07 0.10 0.08
Note dom freq (Hz) 883 1023 983 885 943.50
Intercall silence (s) 5.20 6.40 2.90 NA 4.83
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FIGURE 8. (A) Egg clutch of Hypsiboas diabolicus containing 585 eggs (photo by AF from Mitan, AP, Brazil), (B) Tadpoles
of H. diabolicus at early Gosner stage (26) not forming a school (photo by AF from Mitan, AP, Brazil), (C) Tadpoles of H.
diabolicus at a later stage forming a school (photo by D. Baudain from Pedra Branca, AP, Brazil) and (D) Postmetamorphic
juvenile of H. diabolicus (photo by MB from Gaa Kaba, French Guiana). (E) Tadpoles of H. aff. semilineatus 1 at early Gosner
stage (26) forming a loose school (photo by AF from Mitan, AP, Brazil), (F) Older tadpoles of H. aff. semilineatus 1 forming a
tight school (photo by D. Baudain from Crique Gabaret, French Guiana) and (G) Juvenile of H. aff. semilineatus 1 (photo by
AF from Crique Bon Espoir, French Guiana).
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perched on small branches over the water of shallow streams or pools. Reproductively active males were found
during the rainy season (January–June) and at the beginning of the dry season (July), suggesting an extended
breeding period. Tadpoles were found during the end of the rainy season (April) and during the dry season (July
September). Tadpoles of H. diabolicus stay in group, but do not seem to form schools as large and as tight as in H.
aff. semilineatus 1 (Fig. 8). Moreover, they are generally found in shallow stagnant water, often in pools along the
margins of stream, while the tadpoles of H. aff. semilineatus 1 are generally found in the main bed of rivers, where
its large tadpoles can be observed in deep waters. One recently laid clutch contained 585 eggs (Fig. 8). Significant
differences in buccal morphology between the tadpoles of these two species suggest different larval ecology.
Postmetamorphic juveniles of both species are dorsally grey brown; hands and concealed parts of legs are black,
therefore that character does not allow to discriminate between H. diabolicus and H. aff. semilineatus 1 in
postmetamorphic juveniles. Hypsiboas diabolicus does not seem to be rare, but the species is never found in
abundance (1–3 individuals per site).
Discussion
Amphibian diversity in Amazonia. The inaccuracy of our perception of species boundaries and distributions can
dramatically hamper inferences about biodiversity structure and evolution as well as the adequacy of conservation
strategies (Bickford et al. 2007; Angulo & Icochea 2010; Peloso 2010). This is particularly true in Amazonia where
a growing amount of studies reveals that some widely distributed species are in fact diverse species complexes
(Fouquet et al. 2007; Jansen et al. 2011; Funk et al. 2012; Nunes et al. 2012; Fouquet et al. 2014; Peloso et al.
2014). This is obviously the case in the H. semilineatus species group, which currently contains seven described
taxa (including H. diabolicus) and six candidate species. However, our molecular sampling is far from being
exhaustive because no material from Peru, Ecuador or Colombia was included. Therefore, it is plausible that
several additional putative species could be added to that group. Given the numerous threats faced by tropical
forests in general (Laurance et al. 2002; da Silva et al. 2005), and by amphibians in particular (Blaustein & Dobson
2006; Peloso 2010), it is necessary and urgent to describe this diversity.
Neotype designations and species redescriptions. Recurrent problems that thwart the efforts to describe new
species are the lack of precision of many old original descriptions, the frequent poor quality and difficult access to
type-material, and the fact that several morphologically similar species often occur at a same locality (leading to
some ambiguity about the species name-bearers). Redescriptions of these poorly described species, and designation
of neotypes when necessary, are important steps towards a stable taxonomy. However, this task cannot be taken
lightly in order to avoid adding confusion instead of solving issues. Two recent examples exemplify this problem:
the cases of Rhinella margaritifera (Bufonidae) and Scinax x-signatus (Hylidae), two widely recognized species
complexes (Fouquet et al. 2007a,b; Sturaro & Peloso 2014). In the case of the bufonid taxon, a neotype was
designated by Lavilla et al. (2013), but the choice of the type locality was rather arbitrary and the lack of acoustic
and molecular data for the neotypical material impedes further comparisons, especially because several
morphologically similar species may occur sympatrically at the designated type locality. The case of Scinax x-
signatus is rather similar. New species continue to be described when sufficiently diagnosable from Spix’s original
drawings and descriptions (e.g. Sturaro & Peloso 2014), but several undescribed species are more difficult to
diagnose from Spixs description and, thus, remain unnamed. A neotype for Scinax x-signatus is needed as well as
a thorough revision of the group, but the same precaution should be taken i.e. combine molecular, acoustic and
morphological evidence and make sure that diagnostic characters are provided, especially in comparison with
sympatric species. We advise to tackle this task only when adequate sampling is available from—or as close as
possible from —the type locality (reason why we refrain to redescribe Hypsiboas geographicus at this stage).
In the present case, although Hypsiboas diabolicus could be distinguished from H. geographicus by
examination of the original description (and illustration), the recent collection of new topotypical material helped
to provide decisive evidence (morphological and genetic) to discriminate between the two taxa. As noted by
Duellman (1973), striking variations in colouration of the flanks and concealed parts of the legs and arms exist
across species in that group, which will probably prove to be taxonomically useful.
Hypsiboas semilineatus is another species described by Spix (1824), its description consisting in twelve lines
in Latin. The species was synonymised with H. geographicus by Duellman (1973) then revalidated by Silveira and
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Caramaschi (1989) in a congress abstract. Given the actual diversity within this group, thorough redescriptions of
Hypsiboas geographicus and H. semilineatus are necessary. This can only be adequately accomplished by
examining additional material from the type localities of these two taxa. These redescriptions should come before,
or be part of, a revision of the entire species group.
Biogeography and distribution. From a biogeographic point of view, the Hypsiboas semilineatus clade
displays a striking pattern of allopatry throughout Amazonia. This distribution pattern matches well that of other
species groups investigated at this scale (e.g. Nunes et al. 2012; Fouquet et al. 2014). However, the nested position
of the Atlantic Forest H. semilineatus within Amazonian representatives and low genetic distance separating them
is surprising. The origin of this species seems to be the result of a recent dispersal from Amazonia. A similar
pattern is found within the Rhinella margaritifera species group with R. hoogmoedi displaying a nested position
within Amazonian relatives with shallow genetic distances (Fouquet et al. 2007a).
Unlike the pattern of allopatry found within the H. semilineatus clade, the geographic ranges of the lineages
displaying deeper divergence (H. geographicus, H. cf. geographicus 1, H. diabolicus and the H. semilineatus clade
sensu lato) broadly overlap, leaving few doubts about the reproductive isolation of these taxa
Hypsiboas diabolicus seems to have a limited range, likely restricted to the easternmost part of the Guiana
Shield. A total of 25 localities of occurrence have been reported in French Guiana and adjacent Amapá State. Such
a distribution pattern matches that of species endemic to the easternmost part of the Guiana Shield such as
Pristimantis chiastonotus, P. gutturalis, Anomaloglossus baeobatrachus, but also other Hypsiboas such as H.
dentei. This pattern likely originates from historical isolation (Fouquet et al. 2012) and current climatic parameters
such as the distribution of rainfall that concentrates on that part of the Guiana Shield.
Competing interests. We disclose any financial or non-financial competing interests.
Acknowledgements
This work has benefited from an “Investissement d’Avenir” grant managed by Agence Nationale de la Recherche
(CEBA, ref. ANR-10-LABX-25-01), France, from Fundação de Amparo à Pesquisa do Estado de São Paulo
(FAPESP), Brazil, and partially by the Dimensions of BiodiversityProgram [FAPESP (BIOTA, 2013/50297-0),
NSF (DOB 1343578), and NASA]. We thank Marc Gayot (ONF, Reserve Naturelle Trinité), Marguerite Delaval
(ONF, Reserve Naturelle Nouragues). The Nouragues station (CNRS), DEAL Guyane, the DEDD (ONF). We also
thank Kévin Pineau and Christine Poixblanc for sharing thoughts about the choice of the name of the new species.
Molecular data were produced thanks to Institut Pasteur de Guyane (Vincent Lacoste and his team), University of
Canterbury New Zealand (Neil Gemmell) and Université de Provence (André Gilles). We thank the Museu
Paraense Emilio Goeldi, Belém, Brazil (MPEG) and in particular T.C. Avila-Pires, M.S. Hoogmoed and J. Gomes
for the loan of material, R. Montesinos for helping with specimens at USP and M. Jansen and A. Schulze for
sharing information about Bolivian specimens. We thank Paul Ouboter, Rawien Jairam, Maël Dewynter, Antoine
Baglan, Kévin Pineau, Vincent Pelletier, Olivier Chaline, Vincent Rufray, Jean-Pierre Vacher, Agathe Chen, Benoit
Villette, Daniel Baudain, Renato Recoder, José Ghellere, Francisco dal Vechio, Marco Sena, Mauro Teixeira, José
Cassimiro, Francisco Dal Vechio, Ivan Prates and Anthony Cochard for the loan of material or for contributing to
field work during which we collected material. PJRKs work was granted by a postdoctoral fellowship from the
Fonds voor Wetenschappelijk Onderzoek Vlaanderen (FWO12A7614N). Specimens from Brazil were collected
under permit 30309-1 of Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio - Brazil) provided to
Miguel T. Rodrigues.
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APPENDIX 1. Occurrence records of H. diabolicus sp. nov.
APPENDIX 2. Additional material examined.
Hypsiboas aff. semilineatus 1 (field numbers between parentheses)
Locality State Lat Long
St Elie carbet French Guiana 5.341557 -53.038820
Kaw Fourgassié French Guiana 4.627158 -52.307290
Paracou French Guiana 5.272546 -52.923600
Oiapoque Brazil/Amapà 3.904047 -51.772270
Crique Bon Espoir French Guiana 5.099493 -53.800510
Trinite Aya French Guiana 4.608465 -53.415190
Nouragues Camp Inselberg French Guiana 4.084790 -52.680630
Apatou French Guiana 5.249830 -54.206730
Montagne des singes French Guiana 5.069670 -52.696800
Kaw Patawa French Guiana 4.574621 -52.226140
Pedra Branca Brazil/Amapà 0.772970 -51.945700
Mitan D Brazil/Amapà 2.627640 -52.541950
Counamy French Guiana 5.403682 -53.274510
Montagnes Sparouine French Guiana 4.808075 -54.168830
Rio Vila Nova Brazil/Amapà 0.449335 -52.022140
Monts Gaa kaba French Guiana 4.462112 -54.392740
Mont Saint Marcel French Guiana 2.385830 -53.018890
Parna Tumucumaque Brazil/Amapà 0.909122 -53.228480
Réserve Trésor French Guiana 4.548060 -52.151940
Route Nationale 2 French Guiana 4.105350 -52.049440
Pointe Maripa French Guiana 4.676256 -52.354120
Riviere Kourouai French Guiana 4.114492 -52.060250
Carrière Crique Biche French Guiana 4.772883 52.431900
Crique Belle Etoile French Guiana 5.231226 -53.663490
Piste Patagai French Guiana 5.393000 -53.18600
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R138 (AG335) a male from Crique Camopi-Crique Jalbot, French Guiana (3.15, -52.5667) collected by M. Blanc on 26
April 2009, R139-40 (AF0106-7) two males from Road to Apura, Suriname (5.1833333, -55.6166667) collected by A. Fouquet
and M. Blanc on 10 January 2006, R141 (AF0842) a male from Chutes Voltaire camp, French Guiana (05.0526389, -
54.0884444) collected by A. Fouquet, V. Rufray and O. Chaline on 29 December 2012, R142 (AF0939) a male from Chutes
Grégoire, French Guiana (05.0974722, -53.0506667) collected by A. Fouquet and A. Chen on 10 February 2013; R143-5
(AF1285-6, AF1288) three males from Nouragues reserve station “Inselberg”, French Guiana (4.08479, -52.68063) collected
by A. Fouquet and Q. Martinez on 01 June 2013, R146 (AG370) a male from Monts Gaa Kaba, French Guiana (4.462112, -
54.39273) collected by M. Blanc et A. Cochard on 13 September 2010; R147 (AM027) a male from Inini Tolenga, French
Guiana (3.663159, -53.928308) collected by M. Dewynter and K. Pineau on 10 February 2012; R148 (CAAM029) a female
from Montagne Cacao, French Guiana (2.349156, -53.216013) collected by K. Pineau and V. Rufray on 10 July 2012. MNHN
2014.0110 (QM377) a male from Belizon, French Guiana (4.347832, -52.336203) collected by Q. Martinez on 27 May 2014;
MNHN 2014.0111 (AF1825) a male from Mana road, French Guiana (5.55614, 53.59496) collected by J.P. Vacher on 17 March
2014; MNHN 2014.0112-5 (QM310, 403, 417, 428) a female and three males from Montagne de fer, French Guiana (5.318094,
-53.598318) collected by Q. Martinez on 15 January 2014; MNHN 2014.0116 (AF1556) a female from Saül, French Guiana
(3.60654, -53.17625) collected by M. Berroneau, M. Berroneau, L. Barth, P.O. Cochard on 22 January 2014; MNHN
2014.0117-9 (AF1752, 1753, 1755) three males from Camp Voltaire, French Guiana (5.05226, -54.08909) collected by A.
Fouquet and J.P. Vacher on 05 March 2014; MNHN 2014.0120 (AF1861) a male from Waki flat, French Guiana (3.0895, -
53.39846) collected by J.P. Vacher on 01 April 2014.
Hypsiboas geographicus
MZUSP 157083, 157086, 157088, 157089, 157082, 157084, 157087 (MTR 18569, 18763, 18940, 18828, 18771, 18866,
18650) four males and three females from Lago Chaviana, Rio Purus, Municipality of Beruri, Amazonas, Brazil (-4.307750, -
61.813833) collected by M. T. Rodrigues, S. Marques de Souza, A. Fouquet, M. Teixeira Jr, R. Recoder, M.A. Sena, F. Dal
Vechio, J.M.B. Ghellere on 14-24 October 2010; MZUSP 157090, 157091 (MTR 28250, 28249) two females from Serra do
Divisor, Municipality of Mâncio Lima, Acre, Brazil (-7.434348, -73.660390) collected by F. Dal Vechio, I. Prates, P. Peloso on
25 January 2013; MTR36895) a male from Flutuante Mamirauá, municipality of Tefé, Amazonas, Brazil (-2.890867 -
68.361287) collected by M.T. Rodrigues, S.M. Souza, F. Dal Vecchio, R. Recoder, J.M.B. Ghellere, M. Sena, M. Teixeira Jr, I.
Prates, P. Dias on 28 April 2015.
... We decided to keep using this name for Amapá populations until more studies clarify their taxonomic status. In the species group of B. semilineata, two species are known to occur in Amapá, Boana diabolica Fouquet, Martinez, Zeidler, Courtois, Gaucher, Blanc, Lima, Souza, Rodrigues & Kok, 2016 and an unnamed species, B. aff. semilineata (Fouquet et al. 2016). ...
... In the species group of B. semilineata, two species are known to occur in Amapá, Boana diabolica Fouquet, Martinez, Zeidler, Courtois, Gaucher, Blanc, Lima, Souza, Rodrigues & Kok, 2016 and an unnamed species, B. aff. semilineata (Fouquet et al. 2016). Besides these two names, records in Amapá have also been identified as Boana geographica (Spix, 1824) (Lima 2008;Pereira-Júnior et al. 2013;Benício & Lima 2017;Ferreira-Lima et al. 2017) and B. aff. ...
... These records could belong either to B. diabolica or B. aff. semilineata, so we chose to consider in our list only the molecular confirmed records (Fouquet et al. 2016;Vacher et al. 2020). ...
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... The discovery of phenotypically differentiated unnamed species in Amazonia is far from surprising. Most studies that have explored the question of how many species exist in particular groups of amphibians (e.g., Gehara et al., 2014;Fouquet et al., 2016;Kok et al., 2017;Vacher et al., 2017;Jaramillo et al., 2020), including Microhylidae (e.g., Peloso et al., 2014;de S a et al., 2020), have uncovered high numbers of unnamed species. In many cases, the initial recognition of diversity is based on genetic data (commonly based on a single or very few genes), but after closer examination most of the genetic lineages also present conspicuous phenotypic A. Fouquet, K. Leblanc, A.-C. Fabre et al. ...
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