Published in the United States of America 2020 * VOLUME 14 « NUMBER 3
AMPHIBIAN & REPTILE
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ISSN: 1083-446X eISSN: 1525-9153
Official journal website: amphibian-reptile-conservation.org
Amphibian & Reptile Conservation 14(3) [Taxonomy Section]: 1-30 (e250).
urn:lsid:zoobank.org:pub:CDB4001E-16D3-421D-B68B-314A89BB0924
Some color in the desert: description of a new species of Liolaemus (Iguania: Liolaemidae) from southern Peru, and its conservation status
‘Ling Huamani-Valderrama, ‘Aaron J. Quiroz, Roberto C. Gutiérrez, °*Alvaro Aguilar-Kirigin, 5Wilson Huanca-Mamani, *Pablo Valladares-Fauindez, 7José Cerdena, ”**Juan C. Chaparro, ?Roy Santa Cruz, and *"°Cristian S. Abdala
'Universidad Nacional de San Agustin de Arequipa, Escuela Profesional de Biologia, Ay. Alcides Carrion s/n, Arequipa, PERU *Universidad Nacional de San Agustin de Arequipa, Museo de Historia Natural, Av. Alcides Carrion s/n, Arequipa, PERU *Red de Investigadores en Herpetologia, La Paz, Estado Plurinacional de Bolivia, BOLIVIA *Area de Herpetologia, Coleccion Boliviana de Fauna, La Paz, Estado Plurinacional de BOLIVIA *Departamento de Produccioén Agricola, Facultad de Ciencias Agronomicas, Universidad de Tarapaca, Arica, CHILE °Departamento de Biologia, Facultad de Ciencias, Universidad de Tarapacd. Velasquez 1775, Arica, CHILE ‘Museo de Biodiversidad del Peru, Urbanizacion Mariscal Gamarra A-61, Zona 2, Cusco, PERU *Museo de Historia Natural de la Universidad Nacional de San Antonio Abad del Cusco, Paraninfo Universitario (Plaza de Armas s/n), Cusco, PERU °Consejo Nacional de Investigaciones Cientificas y Técnicas (CONICET)—Unidad Ejecutora Lillo (UEL), San Miguel de Tucuman, ARGENTINA '°Facultad de Ciencias Naturales e Instituto Miguel Lillo (IML), Universidad Nacional de Tucuman, San Miguel de Tucuman, ARGENTINA
Abstract.—The desert of southern Peru and northern Chile is an area with a high degree of endemism in squamate reptiles. In this work, an endemic new species is described in the genus Liolaemus with a restricted geographical distribution on the western slopes of the La Caldera batholith in the Department of Arequipa, southern Peru, that inhabits the Desert province of southern Peru, between 1,800 and 2,756 m asl. The new species is characterized by a unique combination of morphological and molecular characters that distinguish it from all other Liolaemus species, and it is included in the L. reichei clade within the L. montanus group. Evidence presented shows that the category of threat corresponds to Endangered under the IUCN Red List criteria.
Keywords. Arequipa, coastal desert, Endangered, La Caldera batholith, Liolaemus insolitus, lizard, Reptilia
Citation: Huamani-Valderrama L, Quiroz AJ, Gutiérrez RC, Aguilar-Kirigin A, Huanca-Mamani W, Valladares-Faundez P, Cerdefia J, Chaparro JC, Santa Cruz R, Abdala CS. 2020. Some color in the desert: description of a new species of Liolaemus (Iguania: Liolaemidae) from southern Peru, and its conservation status. Amphibian & Reptile Conservation 14(3) [Taxonomy Section]: 1-30 (e250).
Copyright: © 2020 Huamani-Valderrama et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribution 4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Accepted: 15 July 2020; Published: 2 September 2020
Introduction
The Desert province of the South American Transition Zone (sensu Morrone 2014), a biogeographic area that corresponds to a narrow strip along the Pacific Ocean coast from northern Peru to northern Chile (Fig. 1), is located in southern Peru near the Chilean border. This desert contains one of the most hyper-arid deserts in the world, the La Joya desert, which includes areas with zero annual rainfall (Valdivia-Silva et al. 2012) and soils with characteristics like the surface of Mars (Valdivia-Silva et al. 2011). The southern portion of the Desert province harbors a distinctive biota characterized by many endemic plants and animals (e.g., Gutiérrez et al. 2019; Malaga et
al. 2020). The knowledge of the amphibians and reptiles in this area remains scarce compared to the desert areas in Chile and Argentina (Escomel 1929; Dixon and Wright 1975; Péfaur et al. 1978a,b; Cei and Péfaur 1982; Frost 1992; Carrillo and Icochea 1995; Zeballos et al. 2002; Gutiérrez et al. 2010; Abdala y Quinteros 2014); although in recent years three species of Liolaemus lizards were described from this region (Aguilar-Puntriano et al. 2019; Villegas-Paredes et al. 2020).
The South American genus Liolaemus comprises more than 270 formally described species (Abdala and Quinteros 2014; Gutiérrez et al. 2018; Abdala et al. 2019; Villegas-Paredes et al. 2020; Chaparro et al. 2020). These lizards occupy habitats ranging from hot areas, such as
Correspondence. *jchaparroauza@yahoo.com, juan.chaparro@mubi-peru.org
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A new species of Liolaemus from Peru
70°0'O"W
5°0'0"S
10°0'0"S
Rond6nia province
15°0'0"S
PACIFIC OCEAN
20°0'0"S
25°0'0"S
6,000 km /
J
i eS Prepuna pra
80°0'O"W 75°0'O"W 70°0'O"W
65°0'0"W
65°0'0"W
Madeira province
10°0'0O"S
Legend
@ La Caldera batholith Atacaman province (| Cerrado province
(| Chacoan province Desert province
(| Ecuadorian province @ Madeira province Monte province
(J Paramo province
(4 Prepuna province
[ Puna province Rondénia province (| Ucayali province
Gi Yungas province
72] f=) o °
it) me
20°0'0"S
25°0'0"S
60°0'0"W
Fig. 1. Biogeographic regionalization proposed by Morrone (2014), showing the limits of the Desert province and Atacama prov- ince. The geoform La Caldera batholith, adapted from Ramos (2008), is also shown.
the Atlantic coast of southern Brazil and the continental deserts in Chile, Peru, and Argentina, to very cold regions such as Patagonia in Argentina or the high Central Andes in Peru and Bolivia, and reaching elevations greater than 5,000 m asl (Abdala and Quinteros 2014; Gutiérrez et al. 2018; Abdala et al. 2020; Ruiz et al. 2019; Quinteros et al. 2020).
The great diversity within Liolaemus includes a few species with a wide distribution range, such as L. darwinii (Abdala 2007), L. multicolor (Abdala et al. 2020), and L. wiegmannii (Villamil et al. 2019), in addition to a large number of species with very restricted distributions, e.g., L. halonastes (Lobo et al. 2010), L. rabinoi (Abdala et al. 2017), and L. balagueri (Villegas-Paredes et al. 2020). Liolaemus is divided into the subgenera Eulaemus and Liolaemus sensu stricto (Laurent 1983, 1985; Schulte et al. 2001). Within these subgenera, a large number of monophyletic groups have been named (Etheridge 1995; Lobo 2005; Avila et al. 2006; Abdala 2007; Quinteros 2013; Breitman et al. 2011; Abdala et al. 2020).
One of the large groups within Eulaemus is the L. montanus group (Etheridge 1995; Abdala et al. 2020), which is made up of more than 60 described species, and several unnamed species (Abdala et al. 2020). In general, the L. montanus group has been studied in recent years from various branches of biology (Halloy et al. 2013;
Amphib. Reptile Conserv.
Troncoso-Yafiez 2013; Riveros-Riffo and Torres-Murua 2015; Ruiz de Gamboa and Ortiz-Zapara 2016; Aguilar- Kirigin and Abdala 2016; Aguilar-Kirigin et al. 2016; Quipildor et al. 2018), however the taxonomy (Abdala et al. 2008, 2009, 2013; Lobo et al. 2010; Quinteros and Abdala 2011; Gutiérrez et al. 2018; Ruiz de Gamboa et al. 2018; Aguilar et al. 2017; Aguilar-Puntriano et al. 2019; Abdala et al. 2019), and the phylogenetic hypotheses (Aguilar et al. 2017; Abdala et al. 2020; Chaparro et al. 2020), are the areas that have been most developed, providing essential information for understanding the distribution and diversity of the group. However, essential knowledge gaps remain, including sensitive and important issues such as conservation and natural history. In total, 17 species of L. montanus group have been reported for Peru (Chaparro et al. 2020), with six species recorded in the last three years (Gutiérrez et al. 2018; Aguilar-Puntriano et al. 2019; Chaparro et al. 2020; Villegas-Paredes et al. 2020). Additionally, in recent integrative taxonomy studies (Aguilar et al. 2017; Abdala et al. 2020), several populations of unnamed species representing independent lineages have been proposed.
While the Z. montanus species group largely inhabits cold and high-altitude environments, the species of the L. reichei clade (sensu Abdala et al. 2020) occupy coastal habitats of northern Chile and southern Peru (e.g., Aguilar-
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Table 1. Species list of Liolaemus reichei clade.
Species name Author(s)
Liolaemus audituvelatus Villegas et al. 2020 Aguilar et al. 2019 Cei y Péfaur 1982 Aguilar et al. 2019
Valladares 2004 (Werner 1907)
(Steindachner 1891)
(Nufiez et al. 1891)
Liolaemus balagueri Liolaemus chiribaya Liolaemus insolitus Liolaemus nazca Liolaemus poconchilensis Liolaemus reichei Liolaemus stolzmanni
Liolaemus torresi
Puntriano et al. 2018; Villegas-Paredes et al. 2020). The known diversity of the L. reichei clade (Table 1) has increased considerably in recent years with the description of L. balagueri (Villegas-Paredes et al. 2020), as well as L. chiribaya and L. nazca (Aguilar-Puntriano et al. 2019). Various taxonomic and phylogenetic hypotheses have been proposed recently for the L. reichei group (Langstroth 2011; Aguilar-Puntriano et al. 2018; Ruiz de Gamboa et al. 2018; Valladares et al. 2018; Abdala et al. 2020; Villegas- Paredes et al. 2020; Chaparro et al. 2020). Abdala et al. (2020) recovered seven candidate species within their L. reichei clade which are all very close phylogenetically to L. insolitus, a species with a distribution restricted to its type locality in the coastal desert of the Department of Arequipa. In the present study, the taxonomic hypothesis of one of these unnamed populations is evaluated using the general or unified concept of species (De Queiroz 1998, 2007). This concept defines a species as an entity that represents independent historical lineages or divergent lineages of metapopulations. Our criteria to determine the independence of this lineage is based on Total Evidence, such as phylogenetics (molecular and morphological), multivariate statistical analysis, and the description of unique morphological characters; and the results provide decisive evidence to describe it as a new species of Liolaemus.
Materials and Methods
Images and maps. Photographs of live specimens were taken using a digital camera Canon sx50 hs. Close- up photographs of the holotype (preserved) were taken with a digital camera Canon EOS Rebel T5. Maps were elaborated using ArcMap 10.3, and use coordinates previously cited by Aguilar et al. (2016), Gutiérrez et al. (2018), and Chaparro et al. (2020). Type localities were taken from the original manuscripts of the species descriptions. Coordinates of the records reported here were obtained with a GPS device (datum WGS84), Garmin Etrex 30. The regionalization map was elaborated using shape files design from Lowenberg-Neto, which follows Morrone (2014).
Amphib. Reptile Conserv.
(Nufiez and Yafiez 1983)
Distribution Chile: Antofagasta/ Atacama Regions
Peru: Arequipa Department
Peru: Moquegua Department Peru: Arequipa Department Peru: Arequipa Department
Peru: Tacna Department, Chile: Arica Region Chile: Tarapaca Region
Chile: Antofagasta Region Chile: Antofagasta Region
Material examined. Specimens of Liolaemus examined were from the Museo de Historia Natural de la Universidad Nacional de San Agustin de Arequipa, Pert (MUSA); Museo de Biodiversidad del Pert, Cusco, Peru (MUBI); Fundacion Miguel Lillo, Tucuman, Argentina (FML); and Museo de Historia Natural de la Universidad Nacional Mayor de San Marcos, Lima, Peru (MUSM). Collected specimens of Lio/aemus were captured by hand within the locality of La Caldera batholith, District of Uchumayo, Province of Arequipa, Department of Arequipa, Peru. Specimens were euthanized with a 1% Halatal solution, fixed with 10% formaldehyde, and stored in 70% alcohol. Prior to fixation, a sample of muscle was collected for DNA extraction and fixed in 96% ethanol. Collected specimens are deposited in the collections of MUSA and MUBI. Appendix I details the specimens used for the first time here, as well as those reanalyzed for the present work but previously examined in Abdala and Quinteros (2008), Abdala et al. (2008, 2009, 2013), Quinteros et al. (2008), Quinteros and Abdala (2011), Gutiérrez et al. (2018), and Abdala et al. (2020). Additional data were obtained from the literature for L. erroneous (Nufiez and Yafiez 1984), L. omorfi (Demangel et al. 2015), and L. stolzmanni (Langstroth 2011).
Conservation status and endemism. The [UCN (2001, 2020) criteria were used to categorize the new species. The extent of occurrence (EOO), and area of occupancy (AOO), were obtained using the GeoCat tool (http:// geocat.kew.org/), which is a tool that follows IUCN criteria. The endemic concept and restricted range of distribution followed Bruchmann and Hobohm (2014), IUCN (2016), Kier and Barthlott (2001), and Noguera- Urbano (2017).
Morphological data. Morphological characters utilized in taxonomic studies of Liolaemus were studied here, mainly those described or cited by Laurent (1985), Etheridge (1995, 2000), Abdala (2007), Abdala and Juarez (2013), Gutiérrez et al. (2018), Aguilar-Puntriano et al. (2018), Villegas-Paredes et al. (2020), and Abdala et al. (2020). The coloration description was based on live specimens and digital photographs taken in the field. Color
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A new species of Liolaemus from Peru
pattern terminology follows Lobo and Espinoza (1999), Abdala (2007), and Abdala et al. (2020). Examination of scalation or pholidosis was performed using a binocular stereoscope (10—40x), and morphometric measurements were made with a Mitutoyo caliper with precision of 0.01 mm. The morphometric variables were measured three times on the same individual, and the mean value for each species was used in the statistical analyses. Only adult males were used in the multivariate analysis to avoid confounding effects of intraspecific allometric variation, and to avoid confusion in the multivariate analyses due to possible sexual dimorphism (Losos 1990; Abdala et al. 2019). All bilateral characters were measured on the right side. The measured morphometric traits and meristic characters counted follow Abdala et al. (2019) [Appendix IT].
DNA _ extraction, amplification, and sequencing. Total genomic DNA was extracted from samples of muscle using the GenElute mammalian genomic DNA miniprep kit (Sigma-Aldrich), according to the manufacture’s instructions. A fragment of approximately 1,174 base pairs of the mitochondrial gene cytochrome b (cyt-b) was amplified by polymerase chain reaction (PCR), using the primers IguaCytob_ F2 (5'-CCACCGTTGTTATTCAACTAC-3') and IguaCytob_R2 (5'-GGTTTACAAGACCAATGCTTT-3') [Corl et al. 2010]. Each reaction contained 1x PCR buffer (KCI), 2.5 mM MgCl, 0.25 mM each dNTP, 0.1 uM each primer, 1 unit of Taq DNA polymerase (Thermo Scientific), and 1 uL DNA extract. PCR cycling consisted of a 5 min initial denaturation at 94 °C, 35 cycles of 30 sec at 94 °C; 30 sec at 55 °C; 60 sec at 72 °C, anda final elongation step of 2 min at 72 °C. The PCR product was visualized on 1.5% agarose gel stained with Gel-Red (Biotium, Inc.), and subsequently sent to Macrogen, Inc. (Seoul, Republic of Korea) for purification and direct sequencing. The nucleotide sequence was visualized and edited using 4 Peaks software (http://nucleobytes. com/4peaks/) and checked manually, and nucleotides with ambiguous positions were clarified. The sequences newly obtained in this study are publically available in GenBank (see Table 2).
Statistical analysis. A Principal Component Analysis (PCA) was employed to analyze morphological variation, and discriminant function analyses (DFA) were used to verify morphological variation between and within each Liolaemus species employing a jackknife classification matrix (Manly 2000; McCune and Grace 2002; Quinn and Keough 2002; Zar 2010). Based on the existing phylogenetic results (Abdala et al. 2020) and those obtained, four species of L. reichei clade distributed in Peru (L. balagueri, L. chiribaya, L. insolitus, and L. nazca), and the new species proposed here were used as comparative groups for building the PCA and the DFA. Normal distributions of the morphometric data were
Amphib. Reptile Conserv.
examined using the Kolmogorov-Smirnov test (P < 0.05), and homoscedasticity was evaluated with Levene’s test. To reduce the effect of non-normal distributions of the morphological data, all continuous variables were log,, transformed and meristic variables were square root transformed (Irschick and Losos 1996; Sokal and Rohlf 1998; Peres-Neto and Jackson 2001).
All operational taxonomic units were analyzed by two distinct treatments. The PCA analysis was performed to evaluate the distribution of individuals corresponding to the five species (L. balagueri, L. chiribaya, L. insolitus, L. nazca, and Liolaemus sp. nov.) in the multivariate space. The PCA was based on the correlation matrices of the morphological variables to reduce dimensionality of the data (Quinn and Keough 2002; Lovett et al. 2000). The PCA and DFA were evaluated separately for continuous and meristic characters, following the recommendations of certain authors not to join both matrices in the multivariate analyses, although there is no mathematical consensus on this approach (McGarigal et al. 2000). The PCA evaluates relationships within a single group of interdependent variables regardless of any relationships that they may have outside of that group of variables. After the PCA was performed, and the lineal combinations that explained the highest variation were extracted, DFA was performed independently for continuous and meristic morphological characters, to identify the combination of morphological characters that best differ between the groups identified by the PCA. The DFA produces a linear combination of variables that maximizes the probability of correctly assigning observations to predetermined groups, and simultaneously, new observations can be classified into one of the groups, providing likelihood values of such classification (McGarigal et al. 2000; Van den Brink et al. 2003). All statistical analyses were performed using Statistica software, version 7.0 (http://www.statsoft.com).
Phylogenetic analysis. Three matrices were constructed, including: (1)morphological data; (2) molecular characters (cyt-b); and (3) both morphological and molecular data. Total Evidence and morphological phylogenetic analysis were performed using the matrix of Abdala et al. (2020). The morphological matrix includes 306 characters and 105 terminals (with Crenoblepharys adspersa and Phymaturus palluma as an “outgroup” and 96 terminals of L. montanus group). The Total Evidence matrix included 105 terminals and 3,390 characters. Parsimony was used as the optimality criterion, only selecting the shortest trees or those with the fewest homoplasies. TNT version 1.5 (Tree Analysis Using New Technology; Goloboff et al. 2003) was employed to generate the phylogenetic hypotheses. Continuous characters were analyzed following Goloboff et al. (2006), and were standardized using the function mkstandb.run. For this analysis, the value of two was considered as the highest transformation cost. Heuristic searching was used to find the shortest trees or those with the smallest number of steps. The matrix was analyzed
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Huamani-Valderrama et al.
Table 2. GenBank codes and voucher information of Liolaemus and outgroup specimens sequenced for this study.
Ctenoblepharys adspersa (outgroup) Ls i Bs
tS
L. poconchilensis L. poconchilensis L. poconchilensis
L. poconchilensis
Amphib. Reptile Conserv.
co
annectens
annectens
. annectens . annectens “Lampa” . balagueri . balagueri . chiribaya . etheridgei . etheridgei . etheridgei . etheridgei . etheridgei . etheridgei . Stolzmanni
. Stolzmanni
torresi torresi
torresi
. insolitus
. insolitus
. dorbignyi
. eleodori
. audituvelatus . audituvelatus . audituvelatus . audituvelatus . audituvelatus . audituvelatus .vallecurensis . nazca (L. “Nazca’’) . nazca (L. “Nazca’’) nazca (L. “Nazca’”’) . nazca (L. “Nazca’’) nazca (L. “Nazca’’) . ortiz . ortiz
L. aff. poconchilensis
Species names
Voucher code BYU 50502 BYU 50489 BYU 50486 BYU 50491
MUSM 31433 MUSA 5575 MUSA 5576 BYU 51568 BYU 50494 BYU 50495 BYU 50497 BYU 50493 BYU 50499
MUSM 31494
LNC 138 MR 213 LNC 146 LNC 134 LNC 133
MUSM 31490
BYU 50462
LJAMMCNP 5002 LJAMMCNP 2709
LNC 136 LNC 86 ERI MUAP104 SSUC-Re760 LNC 135
LJAMMCNP 650
BYU 50472
BYU 50507
BYU 50508 MUSM 31523 MUSM 31524 MUSM 31513 MUSM 31514 MUSM 31545 MUSM 31543 MUSM 31544 MZUC43498 MZUC43497
cyt-b MH981364 KX826616 KX826615 KX826617 KX826618 MK568539 MK568538 MH981365 KX826620 KX826621 KX826622 KX826619 KX826623 KX826625 MH184793 MH184794 MH184797 MH184795 MH184796 KX826627 KX826626 KF968848 KF968850 MH184785 MH184779 MH184780 MH184782 MH184783 MH184784 KF968960 KX826673 KX826674 KX826675 KX826676 KX826677 KX826633 KX826634 KX826637 KX826635 KX826636 MH184798 MH184799
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Source Aguilar-Puntriano et al. 2018 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Villegas-Paredes et al. 2020 Villegas-Paredes et al. 2020 Aguilar-Puntriano et al. 2018 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Ruiz De Gamboa et al. 2018 Ruiz De Gamboa et al. 2018 Ruiz De Gamboa et al. 2018 Ruiz De Gamboa et al. 2018 Ruiz De Gamboa et al. 2018 Aguilar et al. 2016 Aguilar et al. 2016 Olave et al. 2014 Olave et al. 2014 Ruiz De Gamboa et al. 2018 Ruiz De Gamboa et al. 2018 Ruiz De Gamboa et al. 2018 Ruiz De Gamboa et al. 2018 Ruiz De Gamboa et al. 2018 Ruiz De Gamboa et al. 2018 Olave et al. 2014 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Ruiz De Gamboa et al. 2018 Ruiz De Gamboa et al. 2018
Table 2 (continued). GenBank codes and voucher information of Liolaemus and outgroup specimens sequenced for this study.
L. polystictus L. polystictus
Species names
E. sik i
co
qalaywa qalaywa
“Apurimac”
. robustus . robustus . robustus
. robustus
thomasi thomasi thomasi thomasi
thomasi
. signifer . signifer . signifer . signifer . signifer . signifer . signifer . signifer . signifer
melanogaster melanogaster
melanogaster
. melanogaster
. victormoralesii (L. . victormoralesii (L. . victormoralesii (L. . victormoralesii (L. . victormoralesii (L. . victormoralesii (L. . victormoralesii (L. . victormoralesii (L. . victormoralesii (L. . victormoralesii (L. . victormoralesii (L. . victormoralesii (L. . williamsi
. Williamsi
. williamsi
“AbraToccto’) “AbraToccto’) “AbraToccto’) “AbraToccto’) “AbraToccto’) “AbraToccto’”) “AbraToccto’”) “AbraToccto’) “AbraToccto’) “AbraToccto’”) “AbraToccto’”) “AbraToccto’)
Amphib. Reptile Conserv.
Voucher code MUSM 31451 MUSM 31446 MUBI 12081 MUBI 12099 MUSM 27694 MUSM 31504 MUSM 31508 MUSM 31505 BYU 50483 BYU 50469 BYU 50466 MUSM 31516 BYU 50467 MUBI 5925 MUSM 31443 MUSM 31434 BYU 50444 BYU 50357 BYU 50350 MUSM 31437 BYU 50355 MUSM 31447 MUSM 29110 BYU 50151 MUSM 31472 MUSM 31475 BYU 50154 MUSM 31371 MUSM 31374 MUSM 31373 BYU 50426 MUSM 31461 BYU 50430 MUSM 31462 BYU 50431 BYU 50428 MUSM 31464 MUSM 31465 MUSM 31468 BYU 50463 MUSM 31485 BYU 50143
A new species of Liolaemus from Peru
cyt-b KX826642 KX826641 MT366061 MT366062 MH98 1371 KX826646 KX826648 KX826647 KX826643 KX826680 KX826678 KX826681 KX826679 MT366060 KX826656 KX826654 KX826652 KX826651 KX826649 KX826655 KX826650 KX826657 KX826653 KX826628 KX826630 KX826631 KX826629 KX826665 KX826667 KX826666 KX826661 KX826668 KX826663 KX826669 KX826664 KX826662 KX826670 KX826671 KX826672 KX826684 KX826687 KX826682
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Source
Aguilar et al. 2016 Aguilar et al. 2016 Chaparro et al. 2020 Chaparro et al. 2020
Aguilar-Puntriano et al. 2018
Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Chaparro et al. 2020 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016 Aguilar et al. 2016
Table 2 (continued). GenBank codes and voucher information of Liolaemus and outgroup specimens sequenced for this study.
Huamani-Valderrama et al.
Species names Voucher code cyt-b Source L. williamsi BYU 50464 KX826685 Aguilar et al. 2016 L. williamsi BYU 50144 KX826683 Aguilar et al. 2016 L. williamsi MUSM 31486 KX826688 Aguilar et al. 2016 L. williamsi BYU 50465 KX826686 Aguilar et al. 2016 L. “AbraApacheta” MUSM 31481 KX826660 Aguilar et al. 2016 L. “AbraApacheta” BYU 50145 KX826658 Aguilar et al. 2016 L. “AbraApacheta” BYU 50148 KX826659 Aguilar et al. 2016 L. polystictus “Castrovirreyna” MUSM 31454 KX826639 Aguilar et al. 2016 L. polystictus “Castrovirreyna” BYU 50630 KX826638 Aguilar et al. 2016 L. polystictus “Castrovirreyna” BYU 31455 KX826640 Aguilar et al. 2016 L. robustus “MinaMartha” BYU 50438 KX826644 Aguilar et al. 2016 L. robustus “MinaMartha” MUSM 31439 KX826645 Aguilar et al. 2016 L. annectens LDHV 73 MT773391 This study L. aff. annectens LECG 078 MT773392 This study L. “Cotahuasi” RGP 6031 MT773393 This study L. “Cotahuasi” MDUM 006 MT773394 This study L. “Cotahuasi” MDUM 005 MT773395 This study L. “Cotahuasi” MDUM 004 MT773396 This study L. aff. galaywal MDUM 001 MT773397 This study L. aff. galaywal MDUM 002 MT773398 This study L. aff. galaywa MDUM 017 MT773399 This study L. aff. galaywa MDUM 014 MT773400 This study L. aff. galaywa MDUM 007 MT773401 This study L. aff. galaywa VOI 009 MT773402 This study L. aff. galaywa VOI 006 MT773403 This study L. chiribaya AQR 003 MT773404 This study L. chiribaya AQR 004 MT773405 This study L. aff. insolitus4 RGP 6249 MT773406 This study L. sp. nov. (described herein) MUSA 1766 MT773407 This study L. sp. nov. (described herein) MUBI 13522 MT773408 This study L. sp. nov. (described herein) MUBI 14417 MT773409 This study L. aff. insolitus6 MUSA 1769 MT773410 This study L. aff. insolitus6 MUSA 1770 MT773411 This study L. aff. insolitus6 MUSA 1771 MT773412 This study L. insolitus AQR 001 MT1T773413 This study L. insolitus AQR 002 MT1T773414 This study L. aff balagueri LDHV 005 MT771288 This study L. aff. insolitus2 RGP 6147 MT1T773415 This study L. aff. insolitus8 RGP 6154 MT773416 This study
using the “implied weights” method (Goloboff 1993). The value of the constants K = 14 (morphological analysis) and K = 19 (Total Evidence analysis) were used as in the analysis of Abdala et al. (2020). One thousand replications
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were performed for each search. Symmetric resampling was used to obtain support values for the results obtained, with 500 replications with a deletion probability of 0.33. To construct the cyt-b tree, sequences from this study
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A new species of Liolaemus from Peru
(13 species) were combined with a published dataset of 24 species, and five undescribed lineages of Liolaemus (Aguilar et al. 2016; Aguilar-Puntriano et al. 2018, 2019; Chaparro et al. 2020; De Gamboa et al. 2018; Olave et al. 2014; Villegas-Paredes et al. 2020) [Table 2]. A maximum likelihood phylogenetic analysis was carried out with MEGA X (Kumar et al. 2018). Heuristic tree searches were performed with the GTR + G + I substitution model (determined based on the Akaike information criterion), and 1,000 bootstrap replications.
Results and Discussion
The independent taxonomic status of the population of Liolaemus studied here was validated using morphological and molecular evidence. The results of the phylogenetic and statistical analyses described below suggest that the population can be considered as distinctive from all other described species of Liolaemus. In accordance with best practices in zoological nomenclature, the results of statistical, morphological, and molecular phylogenetic analyses are provided following the formal presentation of the new proposed species.
Taxonomy
Liolaemus anqapuka WHuamani-Valderrama, Quiroz, Gutiérrez, Aguilar-Kirigin, Chaparro, Abdala sp. nov. (Figs. 2—5).
urn:lsid:zoobank.org:act: EF6A BFF4-97 BC-4C8F-83 E7-79D2B3FE7171
1885 Ctenoblepharis adspersus—Boulenger, Catalogue of the Lizards in the British Museum (Natural History). Second Edition 2: 136-137.
1978b “Ctenoblepharus sp.” Péfaur et al. Bulletin de l'Institut Francais d'Etudes Andines VII (1-2): 129-139. 1982 Liolaemus insolitus Cei and Péfaur, In Actas 8vo Congreso Latinoamericano de Zoologia. Pp. 573-686. 1995 Ctenoblepharys adspersa—Etheridge, American Museum Novitates 3142: 1-34.
2004 Phrynosaura [sp.| Nufiez, Noticiario Mensual Museo de Historia Natural 353: 28-34.
2010 Liolaemus cf. insolitus, Gutierrez and Quiroz, Herpetofauna del Sur del Pert, Available: http:// herpetofaunadelsurdelperu. blogspot.com [Accessed: 13 June 2020].
2011 Liolaemus species 2, Langstroth, Zootaxa 2809: 32. 2020 Liolaemus aff. insolitus7, Abdala et al., Zoological Journal of the Linnean Society 189: 1-29.
Holotype. MUSA 5573, an adult male (Figs. 2-3), from between Quebrada San Jose and Quebrada Tinajones, District of Uchumayo, Province of Arequipa, Department of Arequipa, Peru (16°31’47”S, 71°39°04’W) at 2,460 m asl, collected on 10 November 2013, by C.S. Abdala, R. Gutiérrez, A. Quiroz, L. Huamani, and J. Cerdefia.
Amphib. Reptile Conserv.
Paratypes. Six adult females: MUSA 5574-75, same data as holotype. MUSA 1766, from Quebrada Tinajones, 300 m southeast of holotype (16°31754.29’S, 71°38°57.547°W) at 2,492 m asl, collected on 9 October 2010, by A. Quiroz and J. Cerdefia. MUBI 13522, MUSA 1767, from Quebrada Tinajones, 600 m southeast of holotype (16°31°54.207"S, 71°38’46.187°W) at 2,528 m asl, collected on 9 October 2010, by A. Quiroz and J. Cerdefia. MUBI 14680, from Quebrada Tinajones (16°31°22.705”S, 71°37°35.666"W) at 2,561 m asl, collected on 27 July 2007, by R. Gutiérrez and A. Quiroz. Two adult males: MUBI 13521, from Quebrada Tinajones, 300 m southeast of holotype (16°317°54.29”S, 71°38°57.547°W) at 2,492 m asl, collected on 9 October 2010, by A. Quiroz and J. Cerdefia. MUBI 14417, from Quebrada Tinajones (16°31’22.705”S, 71°37°35.666”W) at 2,561 m asl, collected on 27 July 2007, by R. Gutiérrez and A. Quiroz.
Diagnosis. We assign Liolaemus angapuka sp. nov. to the L. montanus group because it presents a blade-like process on the tibia, associated with the hypertrophy of the tibial muscle tibialis anterior (Abdala et al. 2020; Etheridge 1995) and its placement in the morphological and molecular phylogenies (Fig. 11). Within the L. montanus group, Liolaemus angapuka sp. nov. differs from L. andinus, L. annectens, L. aymararum, L. cazianiae, L. chlorostictus, L. dorbignyi, L. fabiani, L, forsteri, L. foxi, L. gracielae, L. huayra, L. inti, L. jamesi, L. melanogaster, L. multicolor, L. nigriceps, L. orientalis, L. pachecoi, L. pantherinus, L. patriciaiturrae, L. pleopholis, L. polystictus, L. puritamensis, L. qalaywa, L. robustus, L. scrocchii, L. signifer, L. vallecurensis, L. victormoralesii, L. vulcanus, and L. williamsi, for being species of larger size (SVL greater than 75 mm) unlike L. angapuka sp. nov., which has a maximum SVL of 73.5 mm. Liolaemus angapuka sp. nov., has between 58 and 72 (mean = 64.8) scales around the body, which differentiates it from species of the group with more than 80 scales, such as L. cazianiae, L. duellmani, L. eleodori, L. erguetae, L. forsteri, L. gracielae, L. molinai, L. multicolor, L. nigriceps, L. patriciaiturrae, L. pleopholis, L. poecilochromus, L. porosus, L. pulcherrimus, L. robertoi, L. rosenmanni, L. ruibali, and L. vallecurensis; and also from species with less than 55 scales, like L. aymararum, L. jamesi, L. pachecoi, and L. thomasi. Liolaemus angapuka sp. nov. have 60—72 dorsal scales (mean = 65.5), and differs from L. andinus, L. cazianiae, L. eleodori, L. erguetae, L. forsteri, L. foxi, L. gracielae, L. halonastes, L. molinai, L. multicolor, L. nigriceps, L. patriciaiturrae, L. pleophlolis, L. poecilochromus, L. porosus, L. pulcherrimus, L. robertoi, L. rosenmanni, L. ruibali, L. schmidti, and L. vallecurensis, which have between 75-102 dorsal scales. The number of ventral scales between 73-87 (mean = 81.3) differentiates it from species with more than 90 ventral scales, such as L. andinus, L. cazianiae, L. erguetae, L. eleodori, L. foxi, L.
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Fig. 2. Details of the holotype of Liolaemus angapuka sp. nov. (MUSA 5573; SVL = 73.5 mm, Tail = 63.9 mm): (A) dorsal and (B) ventral views of body; (C) ventral, (D) dorsal, and (E) lateral views of head; (F) ventral view of precloacal pores. Scale = 10 mm.
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Fig. 3. Adult male of the holotype, Liolaemus anqapuka sp. nov. (MUSA 5573; SVL =
ment of Arequipa, 2,460 m asl. Photos by C.S. Abdala.
gracielae, L. halonastes, L. hajeki, L. molinai, L. nigriceps, L. patriciaiturrae, L. pleopholis, L. poecilochromus, L. porosus, L. robertoi, L. rosenmanni, and L. vallecurensis. Liolaemus anqapuka sp. nov. has juxtaposed or subimbricate dorsal scales, without keel or mucron, this differentiates it from species with conspicuous keel and mucron, as L. aymararum, L. etheridgei, L. famatinae, L. fittkaui, L. griseus, L. huacahuasicus, L. montanus, L. orko, L. ortizi, L. polystictus, L. pulcherrimus, L. galaywa, L. signifer, L. tajzara, L. thomasi, L. victormoralesii, and L. williamsi. Females of L. angapuka sp. nov. present 14 (mean = 2.6) precloacal pores, this character differentiates it from species like L. andinus, L. balagueri, L. fittkaui, L. multicolor, L. ortizi, L. polystictus, L. puritamensis, L. robertoi, L. robustus, L. rosenmanni, L. ruibali, L. thomasi, and L. vallecurensis, because they do not present precloacal pores in females.
Liolaemus angapuka sp. nov. belongs to the clade of Liolaemus reichei sensu Abdala et al. (2020). The color pattern of Liolaemus angapuka sp. nov. has a combination of characteristics in males and females that distinguish it from the rest of the Liolaemus of the group. The number of scales around the body is between 58—72 (mean = 64.8), which differentiates it from L. audituvelatus, L. balagueri, L. insolitus, and L. reichei (Table 3). The number of dorsal scales varies between 60—72 (mean = 65.5), which is lower than the number in L. audituvelatus, higher than in L. nazca, and has a variation in range of scales different than L. chiribaya, L. reichei, and L. torresi (Table 3). The numbers of ventral scales of Liolaemus angapuka sp.
Amphib. Reptile Conserv.
Se
73.5 mm, Tail = 63.9 mm), from the Depart-
nov. vary between 73—87 (mean = 81) which are different from L. audituvelatus, L. nazca, and L. torresi (Table 3). The presence of precloacal pores in females 1—4 (mean = 2.6), is different from L. audituvelatus, L. balagueri, and L. reichei, whose females do not have precloacal pores (Table 3). Coloration patterns on lateral sides have light blue scales, which are different from L. audituvelatus, L. balagueri, L. nazca, L. torresi, and L. reichei (Table 3). The existence of dorsal body scales with a keel differentiate it from L. nazca which have dorsal body scales without keel. Ventral thigh scales with keel are present in 100% of individuals of L. angapuka sp. nov. but they are less evident than those present in L. chiribaya, where only 35% of individuals present this character (Table 3). The maximum SVL is greater than in L. audituvelatus, L. poconchilensis, L. reichei, L. stolzmanni, and L. torresi (Table 3).
Description of the holotype (Figs. 2-3). Adult male (MUSA 5573), SVL 73.53 mm. Head 1.20 times greater in length (16.47 mm) than width (13.74 mm). Head height 10.48 mm. Neck width 14.37 mm. Eye diameter 3.67 mm. Interorbital distance 10.96 mm. Orbit-auditory meatus distance 6.55 mm. Auditory meatus 2.0 mm high, 0.97 mm wide. Orbit-commissure of mouth distance 5.77 mm. Internasal width 1.58 mm. Subocular scale length 4.09 mm. Trunk length 31.81 mm, width 24.37 mm. Tail length 63.91 mm. Femur length 14.65 mm, tibia 14.47 mm, and foot 18.01 mm. Humerus length 11.01 mm. Forearm length 9.31 mm. Hand length 10.82 mm. Pygal
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ee ee
OS PT the Liolaemus anqapuka
Fig. 4. Male specimens of region length 5.95 mm, and cloacal region width 7.97 mm. Dorsal surface of head rough, with 17 scales, rostral 3.09 times longer (2.78 mm) than wide (0.9 mm). Mental as long (2.78 mm) as rostral, trapezoidal, surrounded by four scales. Nasal separated from rostral by one scale. Two internasals slightly longer than wide. Nasal surrounded by eight scales, separated from canthal by two scales. Nine scales between frontal and rostral. Frontals divided into three scales. Interparietal smaller than parietal, in contact with six scales. Preocular separated from lorilabials by one scale. Five superciliaries and 15 upper ciliaries scales. Three differential scales at anterior margin of auditory
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ee Bee
sp. nov. Photos by A.
11
nd C.S. Abdala (E). meatus. Ten temporary scales. Four lorilabials scales, in contact with subocular. Seven supralabials, which are not in contact with subocular. Five supraocular. Eight lorilabials. Six infralabials. Five chin shields, 4" pair separated by five scales. Seventy scales around half a body.
Sixty-two rounded dorsal body scales, juxtaposed, and without a keel or mucron; laminar anterior on members, imbricate and slightly keeled; laminar on hind limbs, imbricate and slightly keeled; tail with dorsal scales in the first third juxtaposed, and the remaining two-thirds imbricate, presence of some scales keeled. Eighty-six
& ‘Sete ee Quiroz (A—D) a
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A new species of Liolaemus from Peru
“ue . 4 ote . .
Fig. 5. Female specimens of the Liolaemus angapuka Sp. nov. Photos by A. Quiroz.
ventral scales, from the mental to the cloacal region, following the ventral midline of the body, laminar, imbricated. Thirty-two imbricate gulars, smooth. Neck with longitudinal fold with 36 granular, not keeled scales, ear fold and antehumeral fold present. Gular fold incomplete. Forelimbs ventrally laminar, subimbricate to imbricate, not keeled; hind legs laminar, imbricate, with some keeled scales (Figs. 2-3). Seventeen subdigital lamellae on the 4" finger of the hand. Twenty-one subdigital lamellae of the 4" toe, with four keels, plantar scales with keels and mucrons. Lamellar ventral scales on tail, imbricate, not keeled. Five precloacal pores. Supernumerary pores absent.
Color of holotype in life (Fig. 3). Dorsal and lateral color of the neck is light gray with few light blue scales, with dull orange scales, and spots on side. Dorsum, limbs, and tail light gray. Vertebral region delimited, vertebral line and spots absent, but dotted with sky blue scales. Paravertebral and dorsolateral region of the body, large orange spots of irregular shape and size stand out. These orange spots are surrounded and dotted with numerous sky-blue scales, with thin design or undulating edges. The orange spots with light white irregular spots. There are no dorsolateral bands, antehumeral arch, or scapular spots. On the sides of the body the pattern of orange spots and
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12
light blue scales is repeated, but the gray color of the body is darker. This design extends to the first third of the tail. Tail with dark semi-complete rings with white back spots. Midline of the body with orange scales and spots. Back of the limbs with numerous light white spots unevenly distributed. Hands and feet dorsally white. Ventrally white from mental region to the tail. Gular and femoral regions light yellow. Flanks of the body with a thin orange border from the armpits to the groin.
Morphological variation. Twenty-two specimens (six males and 16 females). Dorsal surface of head rough with 14-21 scales (mean = 16.82; STD = 1.71). Nasal surrounded by 6—9 scales (mean = 7.41; STD = 0.73). Supralabials 7-10 scales (mean = 8.18; STD = 0.8), lorilabials 8-11 scales (mean = 9.32; STD = 0.89). A line of lorilabial scales. Supraoculars 4—6 (mean = 5.45; STD = 0.6). Interparietals smaller than parietals, surrounded by 4-8 scales (mean = 6.32; STD = 1.09). Infralabials 6-9 (mean = 7.14; STD = 0.77). Gulars 28—39 (mean = 33.41; STD = 2.99). Temporals smooth, 7-10 scales (mean = 9.09; STD = 0.97). Meatus auditory higher 1.37—2.47 mm (mean = 2.05; STD = 0.26), than wide 0.20—1.20 (mean = 0.81; STD = 0.25). Head longer 12.32—17.20 (mean = 14.91; STD = 1.31) than wide 9.15—15.92 (mean = 12.77; STD = 2.03). Head height 6.84—10.48 (mean = 8.38; STD
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Amphib. Reptile Conserv.
conspicuous spots
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absent
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spots
A new species of Liolaemus from Peru
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Precloacal pores in
males
= 0.87). Underarm to groin length 21.61—32.8 (mean = 28.58; STD = 2.76). SVL males 56.23—73.53 mm (mean = 65.05 mm; STD = 7.08) and females 52.15—71.10 mm (mean =62.9mm; STD =4.61). Femur length 10.11—14.65 mm (mean = 12.31 mm; STD = 1.06). Humerus length 7.56—11.01 mm (mean = 8.86 mm; STD = 0.99). Forearm length 7.65—11.56 mm (mean = 9.59 mm; STD = 1.06). Hand length 8.03-11.25 (mean = 10.25; STD = 0.86). Scales around midbody 58—72 (mean = 65.09; STD =3.7). Dorsal 60—72 (mean = 65.59; STD = 3.5), juxtaposed to sub-juxtaposed, and smooth scales. Infradigital lamellae of the 4" finger of the hand 15—21 (mean = 17.73; STD = 1.45) and of the 4" toe 20-26 (mean = 21.67; STD = 1.5). Ventral 73-87 (mean = 81.32; STD = 3.37) larger than dorsal scales. Tail length 46.77-67.16 mm (n = 17, mean = 56.83 mm; STD = 5.91). Males with 4-6 (mean = 4.67; STD = 0.82) precloacal pores, and females with 3-5 (mean = 4.22; STD = 0.83) precloacal pores. Body measurements, males (mean = 66.62 mm) slightly larger than females (mean = 62.90 mm), tail length in males slightly larger (mean = 61.74 mm) than females (mean = 54.80 mm) [Table 4].
Color variation in life (Figs. 4-5). Liolaemus angapuka sp. nov. shows evident sexual dichromatism. In males, head is darker than the gray body. In some specimens, supralabial and infralabial scales are generally lighter gray than the rest of the head. The subocular is generally white with irregular dark spots. The dorsal color of the neck is gray, varying in its hue, and may be dotted with some light blue scales and orange spots. The body color is always gray. The vertebral region in most males is well delimited with some light blue scales. No vertebral line, dorsolateral bands, antehumeral arch, or scapular spots. Few specimens have diffuse gray paravertebral spots, and rounded shape. As in the holotype, in the paravertebral, dorsolateral, and lateral regions of the body, irregular orange spots stand out, surrounded and dotted with celestial scales. Orange spots can vary in intensity and size, as light blue scales that can form thin irregular lines or clump together to form more conspicuous spots. In some specimens the amount of light blue scales is so remarkable that they cover the orange spots. Orange spots and light blue scales are distributed on the sides of the tail. In some individuals, the celestial scales reach the distal end of the tail. In some specimens, light blue scales are replaced by dark, bluish-green scales. In some, irregularly shaped white spots are distributed among the orange spots. The fore and hind limbs, as well as the tail, have the same design as the body. In the tail, incomplete rings of dark spots with light edges are formed. Ventrally, the majority of males are similar. The predominant color is white, some have faint yellow and a yellow hue that can vary in intensity, highlighted in the gular region and the hind limbs. On the sides of the belly, a thin orange longitudinal line protrudes from the armpit to the groin
(Fig. 4).
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Table 4. Differences in morphological characters between males and females of Liolaemus anqapuka sp. nov.
Morphological characters te ied & Snout-vent length 66.62 6.05 Tail length 61.74 3.74 Head length 15:9 0.85 Head width 13.94 1.46 Forelimb length 30.45 0.77 Hind limb length 44.03 2.33 Head length/snout-vent length 0.24 0.02 Head length/head width Ls 0.09 Trunk width/trunk length 0.7 0.06 Tympanum height/tympanum width 2.74 1.07 Auditory meatus scales 135 0.55 Neck scales 39.33 3.5 Scales around midbody 65.67 4.59 Dorsal scales 67.17 4.58 Ventral scales 83.5 251 Pygal scales 6.5 2.07 Precloacal pores 4.67 0.82
Females have a totally different coloring pattern than males (Fig. 5). The color of the head varies from brown to gray, with some dark red spots and scales. The supralabial, infralabial, and lorilabial scales are lighter in color than the dorsal surface of the head. The back of the body can be light gray or brown; with small paravertebral spots, gray or dark brown, and circular or sub-quadrangular; with a small white spot on the back which can be the same size as the paravertebral; and with meager orange spots between the paravertebrals. A few females have light blue scales on paravertebral spots. On the sides of the body, there may be lateral spots of the same design as the paravertebral ones. The tail and hind limbs have the same design and color as the body, without dorsolateral bands. Ventrally they are white or faint yellow immaculate throughout the body. In some females, the tail has more intense yellow throughout its extension (Fig. 5).
Etymology. The specific name refers to the coloration patterns of males. The word “anqapuka” is an original word in the Quechua language (spoken currently in the Peruvian Andes), corresponding to a complex word between “anqa” assigned to the blue color, and “puka” which means orange or red color.
Distribution and natural history. Liolaemus anqapuka sp nov. is restricted to the western slopes of the La Caldera batholith, Arequipa, Peru, between 1,800 and 2,756 m asl, which includes the upper altitude limit of the La Joya desert (Fig. 6). The distribution is within the Desert biogeographic province (sensu Morrone 2014). Liolaemus anqapuka sp. nov. inhabits arid
Amphib. Reptile Conserv.
Variation in Mean in STD Variation in males females females females (56.23—73.53) 62.91 4.61 (52.15—71.10) (58.08-67.16) 54.78 5.49 (46.77-66.88) (14.87-17.2) 14.53 1.27 (12.32-16.79) (11.5-15.92) 12.33 2.08 (9.15—15.38) (29.41—31.53) 28.05 1.58 (25.68—31.36) (39.99-47.13) 40.25 29 (36.02-45.04) (0.22—0.26) 0.23 0.01 (0.21-0.25) (1.04—1.29) 12 0.13 (1.02-1.37) (0.64—0.78) 0.69 0.1 (0.53—-0.97) (2.06-4.9) 3.08 p> (1.57-10.7) (1-2) 1.56 0.63 (1-3) (34-42) 38.7 3.91 (32-43) (60-72) 64.9 3.46 (58-72) (61-72) 65 2.97 (60-72) (81-87) 80.5 3.35 (73-84) (5-10) 6.75 1.69 (5-10) (4-6) 3.64 1.15 (2-5)
environments, characteristic of the desert of southern Peru, with sandy-stony substrates and little slope, seasonal herbaceous vegetation, and columnar and prostrate cacti. This species also inhabits sectors without vegetation (Fig. 7). It takes refuge mainly under stones, and in burrows that surround the roots of small bushes, prostrate cacti, and in cavities underground or in hardened sand. Some specimens of Liolaemus anqapuka sp. nov. were observed feeding on coleopteran larvae, as well as larvae and notably adults of Lepidoptera belonging to the Sphingidae family (Fig. 8). Feeding on beetles is very similar to that reported for the closely- related species Liolaemus insolitus, which is specialized in feeding on so-called “flea beetles” of the subfamily Halticinae (Coleoptera: Chrysomelidae) [Cei and Péfaur 1982]. The adults and larvae of the family Sphingidae are most abundant in the summer months, when the local rainfall is complemented by abundant ephemeral surface watercourses whose flow is derived from rainfall on the western slopes of the Andes, and these insects can display unusual and explosive development. During years when there is exceptionally high accumulated rainfall, a biological phenomenon known as a “blooming desert” can occur (Chavez et al. 2019), and some phytophagous insects would be expected to be able to use the abundant plant resources that suddenly become available in these events, as reported for Sphingidae in northern Chile (Vargas and Hundsdoerfer 2019). Liolaemus anqapuka sp. nov. was found in syntopy with other reptile species, such as Microlophus sp. and Phyllodactylus gerrhopygus.
Endemism, threats, and conservation status. Liolaemus anqapuka sp. nov. is considered as an endemic species
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A new species of Liolaemus from Peru
75°0'O"W 72°0'0"W
12°0'0"S
15°0'0"S
PACIFIC OCEAN
18°0'0"S
0 250 500 1,000 km
75°0'O"W 72°0'0"W
69°0'0"W
12°0'0"S
Legend | w @ L. polystictus * L. signifer LS @ L. robustus ime fe L. th i | = @ L. victormoralesii paar @ L. "A. Apacheta" i) L. annectens ©) L. "Castrovirreina” cn L. evaristoi @ L. "Minas Martha” op L. anqapuka sp. nov. AL. balagueri (*) Type localities A L. chiribaya /\ Type localities 2s Linsolitus xk Type localities L. A eae oa Type localities L. poconchilensis x . [__]o-1,000 L. williamsi [I 1.001 - 2,000 8 * L. etheridgei 2.001 - 3,000 & : 4 * L. melanogaster | au ae | | 4,001 - 5,000 * L. ortizi BBB 5.001 - 6,301 * L. qalaywa
69°0'0"W
Fig. 6. Geographic distribution of Liolaemus montanus group species from Peru. Symbols with a black dot in the middle represent the type locality of each species. Species with quotation marks in the names belong to the candidate species listed in Aguilar et al.
(2016).
with a restricted-range of geographical distribution, because the species occupancy is less than 10,000 km? (Bruchmann and Hobohm 2014; IUCN 2016; Kier and Barthlott 2001; Noguera-Urbano 2017). Using the Geocat tool, and based on records of the species, we estimate the extent of occurrence (EOO) at 147.2 km? and the area of occupancy (AOO) at 80.0 km”. The restricted range might be caused by their climatic tolerance, and the ecological adaptation to extreme environmental conditions found on the Desert biogeographic province. The main threats are the loss of habitat, because of the large-scale mining activities, urban expansion, and contamination by chemicals and metals; and also because of the presence of highways that cut through their natural habitat, and the opening of new secondary roads. Following the IUCN (2020) criteria, and using the actual knowledge of the new species, we evaluated the conservation status of L. anqapuka sp. nov. to be in the category of endangered iv)|, based on the area of occupancy (AOO) < 500 km”, the extent of occurrence (EOO) < 5,000 km?, the number of localities are < 5; and we consider it as a species with restricted range because L. angapuka sp. nov. has a global range size less than or equal to 10,000 km? (IUCN 2016).
Amphib. Reptile Conserv.
Statistical analysis (Figs. 9-10). The summary statistics for all the non-transformed, continuous, and meristic characters taken from five species of Liolaemus are shown in Appendix II. The homogeneity of variance was not supported for either continuous or meristic characters by the Levene’s test in some groups. Therefore, the results of the Principal Component Analyses (PCA) should be preferred for deriving linear combinations of the variables that summarize the variation in the data set. The results of the PCA for continuous and meristic characters are presented separately (Tables 5-6).
The first four components of continuous characters explained 55.51% of the variation, and a screen plot test of the PCs indicated that only the first three components contained nontrivial information. The first axis represents body size, loading negatively for most variables, and accounts for 23.46% of the variation, with strong loading for width of the base of the tail. The second axis represents morphological variation and accounts for most of the remaining variation, with strong loadings for mental scale width, length of the 4" supralabial scale, and upper width of the pygal area. The next axes account for the remaining variation.
The first four components of meristic characters explained 54.59% of the variation, and a screen plot
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Table 5. Principal component (PC) axes loadings of continuous characters for L. balagueri (n = 12), L. chiribaya (n = 10), L. insolitus (n= 15), L. nazca (n=7), and Liolaemus angqapuka sp. nov. (n = 7). Eigenvectors, eigenvalues, and percentage of variance explained for the first four principal components from transformed data in the five putative species of Liolaemus.
Loadings PCI PC2 PC3 PC4 Percentage variation accounted for 23.46 14.84 10.97 6.24 Eigenvalue D2 46 3.4 1.93 Snout-vent length —0.85 —0.06 0.09 0.16 Minimum distance between the nasal scales —0.13 0.48 0.67 —0.02 Snout width at the edge of the flake canthal —0.04 0.2 0.54 0.2 Distance from the nose to the back edge of the flake canthal —0.68 —0.08 —0.15 0.08 Distance between the posterior edge of the series superciliary —0.67 0.56 0.01 0.23 Length of the interparietal —0.48 0.08 —0.44 —0.29 Length of the parietal —0.51 0.43 —0.20 —0.27 Mental flake width 0.13 0.73 0.49 0.05 Length of the mental scale —0.50 —0,33 —0.68 —0.16 Distance from nostril to the mouth —0.55 —0.43 0.28 0.01 Rostral height —0.51 —0.19 0.16 0.05 Length of the subocular scale —0.41 —0.19 0.01 0.06 Ear height —0.16 —0.23 0.22 —0.49 Ear width 0.11 0.29 0.67 —0.32 Length of the preocular scales —0.11 —0.56 0.19 0.14 Preocular width —0.26 —0.46 G32 0 Length of the fourth supralabial flake —0.25 —0.71 0.17 —0.17 Length of the fourth lorilabial flake —0.50 —0.46 0.04 0.04 Length between orbits —0.61 0.37 —0.05 0.46 Length of the first finger of the forelimb, without the claw —0.54 0.41 —0.16 —0,29 Length of the claw of the fourth finger of the forelimb —0.15 0.32 —0.56 0.29 Length of the fifth finger of the forelimb, without the claw —0.19 0.17 0.23 —0.68 Humerus width —0.62 0.06 —0.03 0.24 Distance from the insertion of the forelimb in the body toward the elbow —0.67 0.17 0.29 0.12 Thigh width —0.66 —0.50 —0.01 —0.23 Length of the first finger of the hind limb, without the claw —0.24 0.35 —0.21 —0.38 Length of the claw of the fourth finger of the hind limb —0.54 Q-19 —0.15 —0.26 Body width —0.62 —0.12 0.53 —0.02 Width of the base of the tail —0.75 —0.12 0.22 0.19 Upper width of the pygal area —0.19 0.7 —0.11 —0.13 Length of the pygal area —0.62 0.4 —0.17 0.01
test of the PCs indicated that only those components contain relevant information. The four axes represent morphological variation, loading strongly for number of paravertebral spots in the right side, number of scales around midbody, number of ventral scales, and number of gular scales. The four axes account for the remaining variation, albeit with values below 0.70 for subdigital lamellae of the 4" finger of the forelimb, number of auricular scales, projecting scales on anterior edge of auditory meatus, and number of organs in the postrostral scales.
The positions of species based on their scores for the two morphological principal components axes are illustrated
Amphib. Reptile Conserv.
in Figs. 9-10. The spatial distribution of the continuous characters indicates that they are sufficient to virtually separate the five Peruvian Liolaemus species of the L. reichei group. These species can also be distinguished by their position in the analysis of meristic characters only. In both analyses, Liolaemus angapuka sp. nov. can be differentiated from other phylogenetically related species by its body size and morphological variation.
To further clarify the position of the Liolaemus species in the morphospace of both continuous and meristic characters, a DFA was carried out, where the group membership was determined a priori. The result obtained through the DFA for the five species of Liolaemus was
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A new species of Liolaemus from Peru
Table 6. Principal component (PC) axes loadings of meristic characters for L. balagueri (n = 12), L. chiribaya (n= 10), L. insolitus (n = 15), L. nazca (n = 7), and Liolaemus angapuka sp. nov. (n = 7). Eigenvectors, eigenvalues, and percentage of variance explained for the first four principal components from transformed data in the putative species of Liolaemus.
Loadings
Percentage variation accounted for
Eigenvalue
Number of scales around the interparietal scale Supralabials number on the right side
Supralabials number on the left side
Infralabials number on the right side
Infralabials number on the left side
Number of scales around mental scale
Number of scales around the rostral scale
Number of lorilabials
Hellmich index
Subdigital lamellae of the first finger of the forelimb Subdigital lamellae of the second finger of the forelimb Subdigital lamellae of the third finger of the forelimb Subdigital lamellae of the fourth finger of the forelimb Subdigital lamellae of the fifth finger of the forelimb Subdigital lamellae of the first toe of the hind limb Subdigital lamellae of the second toe of the hind limb Subdigital lamellae of the third toe of the hind limb Subdigital lamellae of the fourth toe of the hind limb Subdigital lamellae of the fifth toe of the hind limb
Number of dorsal scales between the occiput and the level of the anterior
edge of the thigh
Precloacal number of pores
Number of scales between canthal and nasal Number of scales around the nasal scale Supraoculars number enlarged scale in the right side Supraoculars number enlarged scale in the left side Number of scales between canthal and nasal scales
Number of organs in the third lorilabial scale
Number of organs above the row of lorilabials scales and below the canthal
and preocular scales
Gular number of scales
Number of scales around the middle body Number of ventral scales
Number of auricular scales
Number of paravertebral spots in the right side
not significant for continuous morphological characters (Wilk’s Lambda = 0.85, F = 0.71, P = 0.60), and the jackknife classification was 100% satisfactory. The DFA of operational taxonomic units for meristic characters was not significant either (Wilk’s Lambda = 0.69, F = 1.58, P = 0.23); however, the jackknife satisfactory classification was developed at a 100% rate. These results show L. anqapuka sp. nov. can be reliably distinguished from
Amphib. Reptile Conserv.
PCI PC2 PC3 PC4 26.62 10.3 9.63 8.04 8.78 3.4 3.18 2.65 —0.06 —0.36 —0.03 0.05 —0.04 —0.52 —0.27 0.18 0.17 —0.51 —0.47 0.42 0.39 —0.30 —0.44 —0.01 0.25 —0.55 —0.47 —0.07 0.37 —0.09 0) —0.11 0.56 0.31 —0.26 —0.40 —0.16 —0.56 0.07 —0.45 0.32 —0.10 —0.39 0.4 —0.09 —0.59 0.48 —0.04 0.06 —0.35 0.47 0.44 —0.31 —0.07 0.55 0.2 —0.74 —0.12 —0.14 0.24 —0.61 0.12 0.38 —0.22 —0.43 —0.37 0.04 0.14 —0.56 —0.40 0.46 —0.16 —0.47 —0.26 0.14 —0.13 —0.08 —0.55 0.23 —0.48 —0.19 0.22 0.19 0.52 0.43 —0.51 —0.40 —0.18 0.29 —0.24 0.11 0.5 —0.60 —0.41 —0.15 0.36 —0.20 —0.12 —0.05 —0.09 0.67 —0.22 0.2 —0.27 0.48 —0.23 0.05 —0.48 0.7 —0.26 0.15 —0.09 —0.08 —0.18 0.58 0.2 0.66 0.02 0.34 —0.13 —0.88 0.01 0.27 —0.25 —0.92 0 —0.27 —0.09 —0.92 0.03 —0.26 —0.15 —0.73 0.04 —0.02 —0.31 —0.93 —0.02 —0.23 —0.10
the other species by a combination of morphological characters.
Phylogenetic analysis (Fig. 11). The objective of the phylogenetic analyses carried out (morphological, molecular, and Total Evidence) is not to resolve the relationships of the LZ. montanus group, which 1s far beyond the scope of this study. The main objective of
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these analyses is to obtain some approximation of the phylogenetic relationships of L. angapuka sp. nov. and the rest of the L. reichei group sensu Abdala et al. (2020). The new taxon was recovered in three analyses, within the L. montanus group. In the morphological and Total Evidence analyses, under parsimony methodology, the L. reichei group is monophyletic; within this, L. angapuka sp. nov., through molecular analysis of ML, the L. reichei group 1s paraphyletic.
Molecular analysis. The three DNA (cyt-b) obtained for L. anqapuka sp. nov. fall within the same clade, supporting the identification of the new species. The nearest terminal is L. aff. insolitus4, a population innominate from Department of Arequipa, and it is grouped in the same clade with L. chiribaya, a species from Department of Moquegua, with node support (BS = 99). The clade that contains these three species is deeply separated from its sister clade, (L. poconchilensis + L. aff. insolitus8). The analysis does not recover the clade of L. reichei group sensu Abdala et al. (2020) as monophyletic.
Morphological analysis. The result of the morphological phylogenetic hypothesis shows that Liolaemus anqapuka sp. nov. belongs to the group of L. montanus, within the clade of L. reichei sensu Abdala et al. (2020), together with L. audituvelatus, L. balagueri, L. chiribaya, L. insolitus, L. nazca, L. poconchilensis, L. reichei, L. torresi, and eight unnamed populations so far. Liolaemus reichei sensu Abdala et al. (2020), is supported by 13 synapomorphies, of which four are continuous characters (lower number of scales from rostral to occiput, lower number of scales around midbody and lower ratio of tail length/SVL) and eight are discrete (ventral scales of the body equal to, or slightly larger than the dorsal; sides of the body not conspicuously colored, with little or no ventral sexual dichromatism; absence of white line in the temporal region; diameter of the eye, larger than the distance between the anterior margin of the eye, and the rostral scale; isognathic profile, substrate where they occur predominantly sandy).
Amphib. Reptile Conserv.
Fig. 7. Habitat of Liolaemus anqapuka sp. nov. in (A) dry season and (B) wet season. Photos by A. Quiroz (A), C.S. Abdala (B).
—_
This clade is divided into two large subclades, one with unnamed species and populations from Chile (L. audituvelatus, L. poconchilensis, L. reichei, and L. torresi) and the other with species and populations from central and southern Peru (L. balagueri, L. chiribaya, L. insolitus, and L. nazca). This last subkey is where the new species is recovered, supported by 19 synapomorphies, several of which stand out: ratio of auditory meatus height/head height, number of pygals, number of lorilabials contacting the subocular, number of supraoculars, dorsal surface of head (rugouse), scales on external edge of forelimbs (subimbricate), scales of dorsal hind limbs (subimbricate), with notch in edge of scales of gular fold, scales of pygal region (subimbricate), with dark line through the eye; white posterior edge of paravertebral spots in both sex (present), black dots scattered on dorsal region of hind limbs in males (absent), and dark line through the eye in females (present). Liolaemus anqapuka sp. nov. have populations of close relatives which also occur in Department of Arequipa, Peru, with particular morphological characteristics, and these are currently under description. Liolaemus anqapuka sp. nov. is recovered as a sister species of L. aff. insolitus4, a population related to L. insolitus near the
ss = ATR aire METS S TPT I 1 : . " i Wi eco PR Aa ; ¥ 7 § Srey * 4 vin Ps
Fig. 8. Liolaemus anqapuka sp. nov. eating a moth of the Sphingidae family. Photo by A. Quiroz.
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A new species of Liolaemus from Peru
*
? +X fons | i = t : Pere “a aa“ = Vv ey A 5 0 Vv. @ S ree Ba A & e es Vee Bl Vy A &
Principal Component 1
Fig. 9. Plot of principal component scores for continuous characters for L. balagueri (yellow stars, n = 12), L. chiriba- ya (purple circles, n = 10), L. insolitus (red triangles, n = 15), L. nazca (sky blue triangle, n = 7), and L. angapuka sp. nov. (green squares, n = 7). Eigenvectors, eigenvalues, and percent of variation explained for the first two principal components are summarized in Table 5.
coasts of the Department of Arequipa, which occupies elevations of 1,000 m asl. This relationship is supported by six synapomorphies. Liolaemus anqapuka sp. nov. is supported by seven autopomorphies in the phylogenetic tree (Fig. 11).
Total Evidence analysis (Fig. 11). The L. reichei clade is recovered as monophyletic, and L. angapuka sp. nov. belongs to this clade, as do the sister species of L. aff. insolitus4, as well as in the morphological and molecular phylogenetics analyses. This relationship is supported by 14 synapomorphies, six of which are continuous characters and the support of this relationship is high (89%). This relationship is recovered within the clade (L. aff. insolitus5 (L. aff. insolitus4 + L. anqapuka sp. nov.)), and is supported by three morphological and 11 molecular synapomorphies. Likewise, a total of seven autopomorphies support the new species of Liolaemus. In this hypothesis, as in the morphological one, two sub clades are recovered within the L. reichei clade—on the one hand are the species that are distributed in northern Chile, and on the other are those in southern Peru.
Taxonomic history. Boulenger (1885) identified a male specimen (BMNH 65-—5-—3-3) from “Arequiba, 7,500 ft” as Ctenoblepharis adspersus (an unjustified emendation of Ctenoblepharys adspersa Tschudi 1845) in his catalogue of the lizards in the British museum. Péfaur et al. (1978b) mentioned the distribution and classification of the reptiles from Department of Arequipa, noting that the specimens collected by Duellman (1974) from the “La Caldera batholith” located approximately 10 km southwest of Uchumayo town would be “Crenoblepharus sp.” (= Ctenoblepharys). But this was not the only mistake. Years later, Cei and Péfaur (1982) wrote the
Amphib. Reptile Conserv.
20
Principal Component 3
Principal Component 2
Fig. 10. Plot of principal component scores for meristic char- acters for L. balagueri (yellow stars, n = 12), L. chiribaya (purple circles, n = 10), L. insolitus (red triangles, n = 15), L. nazca (sky blue triangle, n = 7), and L. angapuka sp. nov. (green squares, n = 7). Eigenvectors, eigenvalues, and percent of variation explained for the first two principal components are summarized in Table 6.
original description of Liolaemus insolitus, considered to be a widely distributed coastal species which reached altitudes above 2,000 m asl, including the populations of the “La Caldera batholith” from Department of Arequipa. Etheridge (1995), from the specimens considered by Boulenger (1885), identified the possible existence of a different species of Liolaemus from Department of Arequipa, which shows the characteristics of the specimens collected by Duellman (KU 163589, 3 km SW Uchumayo, at 2,150 m asl). During the following years, the regional museums of Peru considered the population from “La Caldera batholith” as an undescribed form associated with Liolaemus insolitus (Zeballos et al. 2002), which they called Liolaemus cf. insolitus. Nufiez. (2004) identified the specimen considered by Boulenger (1885) as a new species of the genus Phrynosaura (synonym of Liolaemus). Gutiérrez and Quiroz (2010), based on photographic material, presumed that the population belonged to L. cf. insolitus. Later, Langstroth (2011) reviewed the field notes written by Duellman, Simmons, and Pefaur (unpublished) and their specimens cataloged as Phrynosaura stolzmanni from the University of Kansas (KU 163589, KU 163592, and KU 163594; collected from “10 km SE of the town of Uchumayo, in the La Caldera batholith”), and indicated that these lizards are not Liolaemus stolzmanni. Based on fieldnotes, which indicate that these specimens are individuals found in habitats of gray sand with granitic rocks and the coloration is cryptic with the habitat, he also highlights the mottled black, orange, and metallic blue back, and the lateral sides of the belly are orange; and these characters are corroborated with the photography of the individual KU163589; citing this population in his work as Liolaemus species 2 (KU 163589, KU 163592, and KU 163594). Finally, Abdala et al. (2020) corroborate through
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Liolaemus montanus
group
Liolaemus montanus
group
Morphology
C
Total Evidence
A
49
Liolaemus chlorostictus clade
Liolaemus dorbignyi clade
47
Liolaemus chlorostictus clade
Liolaemus andinus clade
Liolaemus dorbignyi clade
L.poconchilensis
Liolaemus reichei clade 89
Liolaemus reichei clade
Huamani-Valderrama et al.
L.reichei L.torrestRioLoa L.audituvelatus L.afftorresi1 L.torrest
67 L. nazca
L.balagueri
L.aff.insolitus6
L.insolitus
L.aff.poconchilensis L.aff.insolitus2
L.aff.insolitus3
L. chirtbaya
L.aff.insolitus5 L.angapuka sp. nov. Laflinsolitued
50
Liolaemus andinus clade
L.poconchilensis
L.reichei L.audituvelatus L.torresi L.torresikioLoa L.aff.torresi1
92 L.balagueri L. nazea L. chiribaya L.aff.insolitus2 L.aff.insolitus3 L.aff.poconchilensis L.insolitus L.aff.insolitus6 Le lier
an uUKA Sp. NOV. Lat eolineA
69 40 78
Liolaemus victormoralestt Liolaemus victormoralesti
Liolaemus victormoralesti Liolaemus victormoralesii Liolaemuts victormoralesit Liolaemus victormoralesit Liolaemus victormoralesii Liolnemus victormoralesti Liolaemus victormoralesit Liolaenius victormoralestt Liolaemus victormoralesit
AL jolaemus victormoralesii Liolaentus melanogaster Liolaemus melanogaster Liolaemus melanogaster Liolaemus melanogaster Liolaemus williamsi
97) 86h Liolaemus williamst
38F Liolaemus williamsi
93
Liolaemus williamsi Liolaemus williansi Liolaemus willianst Liolaemus williams 707 Liolaemus “ AbraApacheta” $4" Liolaemus “AbraApacheta” 1} "Liolaemus “ AbraApacheta”’ Liolaemus palystictus 9 Liolaentus polystictus 52r Liolaemus polystictus 9 ET olaemus polystictus Liolaenius polystictus 99 _fLiolaentus robustus Liolaemus robustus Liolaemus robustus Liolaentus robustus 99 |Liolnenius robustus 99 "Liolaemus robustus 59 rLiolaentus signifer Liolaentus signifer 87 JLiolnenus signifer Liolaemus signifer Liolaemus signifer Liolacnits sigitifer 99 “Liolaemus signifer Liolaemus stgnifer Liolaemus ethertdget ‘Liolaemus etheridget 99 [Liolaemus etheridge Liolaemus etheridger Liolaemus ethertdget Liolaemus etheridget ‘Liolaenius annectens gq |Ltolnentus annectens pif Liolnenius arnmecterns 6l Liolaemus annectens Liolaemus aff.annectens Liolaentus annectens Liolaemus signifer 50 FLiolaemus “Cotahuasi” Liolaemus “Cotahuasi” Liolaemus “Cotahuasi” Liolaemus “ Cotahuasi” Ltolaentus qalaywa
$2
40
173° Liolaemus qalayewn gop Lrolaentus att.qalaywal
Liolaemus aft.qalaywa ® FLiolaemus aff.qalaywa
Liolaemus aff.qalaywa 99 |Ltolaemus stolzmanna Liolaemus stolzmanni 99 Liolaemus torresi 99 [ Liolaentius toriesi 65 ‘Liolaemus torrest =| 33 Liolaemus tmsohi tus 87 IT iolaemus insolitus * Liolnenus insolitus Liolaemus insolitus Liolnenius aft.insolitus6
Liolnentus aff.insolitus6 Liolaenius aff.ansolitus6
24) Liolaemus dorbignyt
Liolaemus eleodori
Liolaemus audituvelatus Liolaentus audituvelatus Liolaemus audituvelatus Liolaemus audituvelatus Liolaemus audituvelatus
Molecular
B :
52
84' Liolaemus audituvelatus Liolnemus nazea
86 Liolaemus nazea
2 Fhiolaenus nazca Liolaemus nazca 82 ‘Liolaemus nazca Liolaemus aft.balaguert Liolaentus balaguert 99 “Liolaemus balaguert Liolaemus aff.insolitus2 ‘Liolaenuts att.poconchilensis 96 |Liolaentus poconclulensis °8 1'Liolaentus poconclulensis 99 = s Liolaemus poconchalensts
Liolaentus poconchilensts Liolaeius aff.insoli tus
74 (Liolaemus cluribaya 22 Liolaemus chit tbaya Liolaemus chiribaya 99 |F-Liolaenus aff.insolitus4
85
99
32
40 J5]] 29
Liolaemus 93, |[ Ltolaentus anqapuka sp. nov. Montanus 93 [|p Liolaenius angapuka sp. nov. group 97 !Liolnemus anqapuka sp. nov. 99 Liolaemus ortizi Liolaentus ortizt Liolaemus thonust ° | TLiolaemus thomasi Liolaemus thomuasi Liolaemus tonusi Liolaemus thonust Liolaemus vallecurensis
Fig. 11. Phylogenetic trees showing the relationships between Liolaemus anqapuka sp. nov. and species within the L. montanus group by (A) Total Evidence analysis, (B) molecular phylogenetic analysis, and (C) morphological phylogenetic analysis. The values correspond to the support measure with symmetric resampling.
Amphib. Reptile Conserv.
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Ctenoblepharys adspersa
A new species of Liolaemus from Peru
analysis of Total Evidence of the L. montanus group that the population from “La Caldera batholith” (Z. aff. insolitus7) is an independent terminal, because it presents morphological characteristics different from the rest of the known species of Liolaemus. Therefore, we corroborate the hypothesis presented by Abdala et al. (2020), based in morphological and molecular phylogenetic evidence, which they named as L. aff. insolitus’7.
Acknowledgments.—We are grateful to Evaristo Lopez [Museo de Historia Natural, Universidad Nacional San Agustin, Arequipa, Peru (MUSA)], the staff of the Museo de Biodiversidad del Pert (MUBI, Cusco, Pert), Sonia Kretzschmar and Esteban Lavilla [Fundacion Miguel Lillo, Tucuman, Argentina (FML), César Aguilar-Puntriano y Alejandro Mendoza (Museo de Historia Natural, Universidad Nacional Mayor de San Marcos, Lima, Peru (MUSM)], for allowing the review of specimens from their museum collections and for facilitating access to the collection under his care. Comments of Roberto Langstroth, Emma Steigerwald, Matt King, and one anonymous reviewer improved our manuscript considerably. Collection permits for specimens were issued by Ministerio de Agricultura, through Resolucion Directoral N° 0399-2013—MINAGRI-DGFFS/DGEFFS and Resolucion Directoral N°0112-2012-AG-DGFFS- DGEFFES; and additionally, the Resolucion de Direccion General N° 509-2018-MINAGRI-SERFOR-DGGSPFFS. We are grateful to Yovana Mamani Ccasa, from Cusco, for the support of the epithet in the original language of the Incas. LHV thanks Luis Arapa and Jeitson Zegarra for their help, in part, in obtaining morphological data; Mg. Sandro Condori and Dr. Sebastian Quinteros for their comments on the sequence alignment process; Dra. Maria Valderrama for access to the environments of the Genetics Laboratory of the National University of San Agustin; and finally, he especially thanks the researchers and others who help him during his stay on his trip to Argentina: Romina Sehman, AnaLu Bulacios, Marco Paz, the Abdala family in Mendoza, Lisseth Montes and family in Tacna, Valladares family in Chile, Carlos Valderrama and family in Lima. CSA thanks the Cerdefia family and the Hotel Princess from Arequipa. Thanks to CONICET and the Agencia y Técnica (PICT 2015- 1398, Argentina) and “Convenio de Desempefio Regional UTA-1795.”
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Ling Huamani-Valderrama is a Biologist from the Universidad Nacional San Agustin de Arequipa, Peru. For her thesis degree (obtained in 2018), Ling studied the morphological and molecular characterization, and establishment of an ecological niche of a species of the genus Liolaemus. Her interest is the systemat- ics, taxonomy, ecology, and conservation of reptiles, focusing on lizards of coastal and highland areas.
Aaron J. Quiroz graduated in Biological Science, and is currently a Research Associate of the Museum of Natural History, National University of San Agustin, Arequipa, Peru. Aaron is a co-author and collaborator on publications which focus on the taxonomy and conservation of amphibians and reptiles in Peru. He is currently developing a career as an independent professional in the direction and design of amphibian and reptile research and conservation projects.
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A new species of Liolaemus from Peru
Roberto C. Gutiérrez is a Biologist who graduated from the National University of San Agustin de Arequipa of Peru. Roberto is currently the Curator and Principal Researcher of the Herpetological Collection, Museum of Natural History, National University of San Augustin de Arequipa, Peru, and Vice President and Founding Member of the Herpetological Association of Peru (AHP). He is interested in the herpetofauna of the tropical =. Andes and the coastal desert, with a special focus on lizards of genus Liolaemus, and is developing studies in the systematics of amphibians and reptiles, ecology, and conservation. Roberto has conducted several biodiversity inventories, biological assessments, and biodiversity monitoring programs, and is currently working at the Natu- ral Protected Areas Service of the Peruvian Ministry of Environment.
' Alvaro Aguilar-Kirigin is a Bolivian Biologist who graduated from the Universidad Mayor de San Andrés, .A La Paz, has been a researcher at the Coleccion Boliviana de Fauna specializing in herpetology since 2002, and = is a member of the Bolivian Network Researchers in Herpetology. He carried out two research internships in “ Argentina and Uruguay, focusing on the systematics and phylogeny of Liolaemus and the latitudinal patterns of seasonal changes in fat body size in 59 species of lizards. He has authored over 35 publications (18 of which were peer-reviewed), 10 book chapters, and seven technical cards as part of book chapters, including the descriptions _ of three species of Liolaemus. Alvaro is interested in integrative taxonomy, especially in the genus Liolaemus, _ because of its phenotypic plasticity in the Andean region. As a line of research, he is making progress with linear »- models in the study of classical comparative morphometry. Likewise, he is linked to the conservation of the ~~ £ wildlife that inhabit the Amazonian forest in the Department of Beni in Bolivia.
Wilson Huanca-Mamani is a Biologist from the Universidad de Concepcion (Concepcion, Chile), with a Doc- torate in Plant Biotechnology from Centro de Investigacion y de Estudios Avanzados del IPN (CINVESTAV), Unidad Irapuato, Mexico. Wilson is currently a researcher at the Universidad de Tarapaca (Arica, Chile). One of his research interests focuses on the population genetics of desert plants.
Pablo Valladares-Fatndez is a Biologist who graduated from the Austral University of Chile and obtained his Ph.D. from the University of Chile. Pablo is currently an academic in the Department of Biology, Science Faculty, University of Tarapaca, in northern Chile. He is interested in the study of vertebrates from arid and high * Andean ecosystems, particularly lizards of the genera Liolaemus and Microlophus, and is developing studies on 4 their taxonomy, systematics, ecology, and conservation. Pablo is also developing a herpetological collection of | northern Chile.
José Cerdeiia is a Biologist who graduated from the Universidad Nacional de San Agustin de Arequipa (Peru), and is a researcher at Museo de Historia Natural de la Universidad Nacional de San Agustin de Arequipa (MUSA) in Peru. José’s research includes the systematics, taxonomy, and biogeography of Lepidoptera, but with a recent ' interest in the taxonomy and ecology of the genus Liolaemus in southern Peru.
Juan C. Chaparro is a Peruvian Biologist with extensive experience in studying the fauna of all the traditional geographic regions of Peru. Juan graduated in Biological Sciences from Universidad Nacional Pedro Ruiz Gallo, Lambayeque, Peru; received a Master’s degree in Biodiversity in Tropical Areas and Conservation in 2013, from an institutional consortium of the International University of Menendez Pelayo (UIMP-Spain), Universidad Tec- noldgica Indoamérica (UTI-Ecuador), and Consejo Superior de Investigaciones Cientificas (CSIC-Spain). He is currently the president of the Herpetological Association of Peru (AHP), director and curator of the Herpetological Collection of the Museo de Biodiversidad del Peru (MUBL, https://mubi-peru.org/herpetologia/p-mub1), and he also works as a consultant in environmental studies. Juan has authored or co-authored 51 peer-reviewed scientific pa- - pers, notes, book chapters, and books on various fauna (especially in herpetology and arachnology), on topics such wey as their taxonomy, biodiversity, systematics, phylogeny, conservation, and biogeography in South America. He is Ey interested in those topics, as well as life history, distributional patterns, and evolution using amphibian and reptiles as biological models. Four species have been named in his honor: Phyllomedusa chaparroi (Amphibia), Phrynopus chaparroi (Amphibia), Hadruroides juanchaparroi (Arachnida), and Chlorota chaparroi (Insecta).
Roy Santa Cruz is a Research Associate at Area de Herpetologia del Museo de Historia Natural (MUSA), Uni- versidad Nacional de San Agustin de Arequipa, Peru. His current research interests include the taxonomy, natural history, and conservation of amphibians and reptiles. He currently coordinates several research projects which focus on threatened species of Andean frogs.
Cristian S. Abdala is an Argentinian Biologist, a researcher at CONICET, and a professor at the Universidad Nacional de Tucuman (UNT) in Argentina. Cristian received his Ph.D. degree from UNT, and is a herpetologist with extensive experience in the taxonomy, phylogeny, and conservation of Liolaemus lizards. He has authored or co-authored over 70 peer-reviewed papers and books on herpetology, including the descriptions of 50 recog- nized lizard species, mainly in genus Liolaemus. One species, Liolemus abdalai, has been named in his honor. He has conducted several expeditions through Patagonia, the high Andes, Puna, and the salt flats of Argentina, Chile, Bolivia, and Peru. Since 2016, Christian has been the president of the Argentine Herpetological Association.
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Huamani-Valderrama et al.
Appendix I. Specimens examined.
Liolaemus anqapuka sp. nov. (n = 22): PERU. Arequipa: Arequipa, Uchumayo: MUBI 13521—22, MUSA 4131, 4133-34; Arequipa, Uchumayo, Quebrada Tinajones, MUSA 1766-67, MUSA 4546, 5207-12, 5214, MUBI 14417, MUBI 14680, LSF 001, LSF 002; Arequipa, Uchumayo, between Quebrada Tinajones and Quebrada San Jose, MUSA 5573-75.
Liolaemus balagueri (n= 18): PERU. Arequipa: Camana, Quilca, Lomas de Quilca, MUSA 1772-74, MUSA 5575-78, MUBI 13206-09, MUBI 16483-84, MUSM 3919395; Camana, Camana, Lomas de La Chira, MUSM 39192, MUSA 5579.
Liolaemus chiribaya (n= 11): PERU. Moquegua: Mariscal Nieto, Torata, Jaguay Chico, MUSM 31548-50, MUSM 31553; Mariscal Nieto, Torata, Cerro los Calatos, MUSM 31547, MUSM 31386, MUSM 31388-91; Mariscal Nieto, between Moquegua and Torata, MUSM 31387.
Liolaemus etheridgei (n = 17): PERU. Arequipa: Cabrerias, Cayma, MUSA 501; Cerro Uyupampa, Sabandia, MUSA 549- 54; Monte Riberefio de la Quebrada de Tilumpaya Chiguata. Pocsi, MUSA 1113-14, 1116, 1264-68, 1353; Anexo de Yura Viejo, Yura, MUSA 1229.
Liolaemus evaristoi (n= 16): PERU. Huancavelica: Los Libertadores, Pilpichaca, Huaytara, MUSA 2841 (holotype), 2781- 85, 2840, 2842-45, MUBI 10474—78 (paratypes).
Liolaemus insolitus (n = 10): PERU. Arequipa: Lomas de Mejia, Dean Valdivia, MUSA 346, MUSA 1741, MUSA 2187-90; Alto Inclan, Mollendo MUSA 4787-88, MUSA 4812, MUSA 4815.
Liolaemus nazca (n= 7): PERU. Ica: Nazca, MUSM 31520—21, MUSM 31523, MUSM 31525—26, MUSM 31541, MUSM 16100.
Liolaemus poconchilensis (n = 2): PERU. Tacna: Morro Sama, Las Yaras, MUSA 1638-39.
Liolaemus polystictus (n = 13): PERU. Huancavelica: Mountain near Rumichaca, Pilpichaca, MUSA 1337-1338; Santa Inés, Castrovirreyna, MUSA 2448-2457; Santa Inés, FML 1683 (paratype).
Liolaemus robustus (n= 11): PERU. Lima: Surroundings of Huancaya, Reserva Paisajistica Nor Yauyos Cochas, MUSA 1693-1702; Junin: Junin, FML 1682 (paratype).
Liolaemus signifer (n = 12): PERU. Puno: Titicaca Lake, 3,840 m, FML 1434; Titicaca Lake, road to Puno, FML 1557; near Tirapata, MUSA 1415; Huancané, Comunidad Taurahuta, MUSA 1441-43; Huerta Huayara community, 3 km before Puno,
MUSA 1483-87.
Appendix II. Measured morphometric traits and meristic characters.
Morphological L. balagueri L. chiribaya L. insolitus L. nazca L. angapuka sp. nov. characters n=12 n=10 n=15 n=7 n=7 SVL 51.08-64.96 49 28-68.25 47.35-65.77 53.51-64.34 52.15—73.53 58.82 + 4.68 59.60 + 6.59 56.79 +5.41 59.35+4.98 60.14+6.71 DN 1.03—2.04 1.96-3.00 0.91-1.96 0.63-1.81 0.96—-1.68 1.31+0.28 2.47 + 0.30 1.53 + 0.36 1.47+0.42 1.36 + 0.24 AH 3.59-5.61 3.71-5.67 3.21-5.06 1.96—4.85 4.16—-5.43 4.45+0.54 4.73+0.66 4.23 + 0.53 3.92 + 0.93 4.70 + 0.42 NC 1.65-2.91 1.07—2.57 1.52-2.85 2.10-3.14 2.10—2.73 2.09 + 0.36 2.09 + 0.52 2.09 + 0.33 2.49 + 0.38 2.47 +0.27 EO 6.11-8.96 7.01-9.26 7.12-8.88 6.16—8.25 7.00-9.62 7.49 + 0.74 8.244 0.72 7.90 + 0.49 7.11 £0.80 8.54 + 0.90 LEI 0.89-1.69 0.88-1.28 0.66-1.58 0.47—2.06 1.23—-1.76 1.28 + 0.26 1.09+0.14 1.12+0.26 1.31+0.48 1.54+40.21 PA 0.85—1.74 1.31-1.72 0.90-1.82 0.51-1.91 1.45-1.99 1.34+ 0.26 1.43+0.14 1.25 + 0.26 1.244 0.47 i eae Oe | AM 1.05-1.76 2.00—2.86 1.32-2.41 0.46-1.31 1.06-1.49 1.28 + 0.20 2.46 + 0.28 1.94+ 0.47 1.06 + 0.30 1.26+ 0.18
Amphib. Reptile Conserv.
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Appendix II (continued). Measured morphometric traits and meristic characters.
Morphological
characters
LM
NB
HR
ES
hTy
aly
LPO
LPOT
LCSP
LCLB
DEO
1D
G4D
5D
AHU
LEA1
AMU
IP
4U
AL
WTB
ASPI
Amphib. Reptile Conserv.
L. balagueri n=12 2.05-3.13 2.53 + 0.34 1.11-1.92 1.41 40.23 0.40-1.04 0.80 + 0.17 2.83-4.58 3.72+0.49 1.69-2.63 2.16 + 0.26 0.47-1.54 0.97 + 0.26 0.91-1.67 1.20 + 0.23 0.43-0.85 0.61+0.13 1.01—2.00 1.52 + 0.34 0.68-1.56 1.15+0.25 6.80-8.83 7.83 + 0.67 1.86-3.21 2.51 40.39 1.10-1.59 1.304 0.16 2.89-3.84 3.29 + 0.33 1.98-3.63 2.81 40.51 6.94-11.83 8.89 + 1.40 3.76—-5.28 454+ 0.47 2.87-3.68 3.19+0.29 0.93—2.06 1.45 + 0.32 16.19—20.03 17.43 + 1.06 6.32-8.63 7.49 + 0.76 5.39-6.80 6.08 + 0.44
L. chiribaya n=10 0.84—-1.55 1.20 + 0.22 1.19-1.63 1.42+0.12 0.64—1.22 0.86 + 0.19 3.20-4.06 3.57+£0.27 1.68—2.30 1.91+40.21 1.18-1.65 1.37+£0.17 0.57-1.54 102032 0.48-0.80 0.60+ 0.11 0.83-1.42 1.1440.19 0.86-1.28 0.99 + 0.12 7.31-9.32 8.26 + 0.68 1.84-3.12 2.52 + 0.44 0.74-1.38 1.01+0.21 2.41-4.41 3.31 40.56 1.99-4.58 3.03 0.78 8.65-10.81 9.75+0.71 3.33-4.98 4.18+0.60 1.66—-4.30 3.20 + 0.86 0.74-2.32 1.33 + 0.45 19.64—33.02 25.76 + 4.97 6.19-9.15 7.76 + 1.21 4.37-7.80 6.45+1.17
28
A new species of Liolaemus from Peru
L. insolitus n=15 1.08—2.92 1.69 + 0.66 0.96-1.56 1.26+0.18 0.53-1.01 0.77+0.11 1.90-4.16 3.52 + 0.53 1.02—2.09 1.72 + 0.25 0.65-1.22 0.94 + 0.20 0.53-1.49 1.17+0.24 0.37-0.72 0.52+0.11 0.54-1.52 1.03 + 0.25 0.55-131 0.97 + 0.20 7.48-9.17 8.36 + 0.55 1.63-2.95 2.32 + 0.31 1.17—2.04 1.53 40.22 2.44—3.40 2.84 + 0.25 2.24—3.46 2.77 0.38 6.34-9.45 8.19 + 0.86 2.67-4.68 3.71 0.73 2.50-3.78 3.15+0.37 0.98-1.77 1.30 + 0.22 12.12-19.74 15.99 + 2.40 4.91-8.44 6.98 + 1.07 5.57—7 84 6.43 + 0.69
L. nazca n=7 1.23-2.64 2.16+0.54 1.16—1.87 1.56 + 0.28 0.69-1.54 0.93 + 0.31 2.93-6.62 3.93 + 1.26 1.72—2.49 1.95 + 0.26 0.67-1.13 0.94+0.14 0.75—2.35 1.43 + 0.50 0.48-0.92 0.69 + 0.15 1.39-3.36 2.01 + 0.67 0.85-2.14 1.29 + 0.46 6.90-8.67 Pose OTA 1.61-2.82 2.13+0.41 0.67-1.35 1.00 + 0.23 2.33-3.93 2.93 + 0.52 2.01-3.93 3.06 + 0.54 7.01-8.95 8.17 + 0.80 4 82-7.19 5.96 + 0.79 1.73-4.08 2.92 + 0.72 0.75-1.72 1.33 + 0.36 19.61—27.88 24.85 + 2.70 6.249 20 7.46 + 0.88 2.70-7.20 4.55 + 1.35
L. angapuka sp. nov.
n=7 2.30-2.78 2.55+0.21 0.97-1.51 1.3140.17 0.55—1.04 0.82 + 0.15 3,244.73 3.81 £0.49 1.37—2.02 1.78 0.23 0.57—1.10 0.85+0.18 0.60—1.07 0.89 40.19 0.33-0.82 0.55+0.18 0.66—1.37 1.03+0.31 0.57—1.30 1.03 + 0.28 8.17-10.95 9.45 + 1.03 2.56-3.31 2.88 + 0.30 1.29-2.11 1.544 0.32 2.28-3.41 3.00 + 0.44 2.59-4.36 3.45 + 0.60 9.03-11.01 9.96 + 0.68 3.60—5.80 4.43 + 0.78 2.51-3.42 3.08 + 0.29 0.97-1.87 1.45 + 0.32 15.27-24.37 19.85 + 3.27 6.50—10.07 7.46 + 1.20 4.76-6.66 5.56 + 0.64
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Appendix II (continued). Measured morphometric traits and meristic characters.
Morphological
characters
LPI
All
Al2
Al5
Al3
Al9
Al4
Al6
Al7-l
Al18
A20-1
A20-2
A20-3
A204
A20-5
A21-1
A21-2
A21-3
A214
A21-5
A22
A26
Amphib. Reptile Conserv.
L. balagueri
n=12 4.01-6.12 5.07 + 0.62 4-8 6.33 + 0.98 6-8 7.08 + 0.79 6-8 6.67 + 0.89 5-7 6.08 + 0.51 5-7 5.67 + 0.65 4 4.00 + 0.00 6-8 6.67 + 0.65 7-9 7.50 + 0.67 12-16 13375 1:29 7-8 7.33 £0.49 9-11 10.17 + 0.83 14-16 14.67 + 0.65 12-18 15.33 + 1.67 8-11 9.58 +0.79 5-10 8.17+ 1.53 10-13 11.83 + 0.94 9-18 15.00 + 2.37 19-24 20.33 + 1.50 10-14 11.58+ 1.16 52-56 53.50 + 1.62 0-7 3.00 + 2.80
Huamani-Valderrama et al.
L. chiribaya n=10 4.71-6.75 5.75 + 0.76 5-7 6.20 + 0.63 7-9 7.60 + 0.70 7-10 8.60 + 0.97 5-7 6.10 + 0.57 5-7 6.10 + 0.57 46 4.20 + 0.63 6-7 6.10 + 0.32 5-8 6.40 + 1.07 14-18 15.90 + 1.20 7-8 7.30 + 0.48 11-13 12.60 + 0.84 14-16 15.30 + 0.67 17-19 18.20 + 0.92 8 8.00 + 0.00 9-10 9.20 + 0.42 11-12 1.200.423 14-16 15.40 + 0.70 18-21 19.50 + 0.85 11-13 12.50+0.71 52-63 57.40 + 3.50 2-5 3.80 + 1.03
L. insolitus n=15 3.73-6.40 5.03 + 0.82 5-9 6.27 + 1.16 7-8 7.47 + 0.52 7-9 7.80 + 0.56 5-8 6.40 + 0.74 5-8 6.27 0.70 46 467+ 0.82 6-8 7.07 + 0.59 7-8 7.20 + 0.41 14-18 15.07 + 1.03 6-9 7.67+ 1.11 8-16 12.07 + 2.49 12-16 14.40 + 1.30 10-17 (2-73 2,02 6-10 FAISELAO 6-11 7.80 + 1.15 10-12 10.93 + 0.88 12-16 14.00 + 1.25 20-22 20.67 + 0.62 10-12 11.27+0.88 58-69 63.40 + 3.48 0-8 4.20 + 2.83
L. nazca n=7 3.23-6.16 4.90 + 0.87 5-8 6.14 + 1.07 6-9 7.43 + 0.98 6-8 6.57 + 0.98 5-6 5.57 + 0.53 5-6 5.71+0.49 4—5 4.14+0.38 5-6 5.86 + 0.38 7-10 8.43 + 0.98 11-14 | ay a I ol 7-10 8.71+1.11 12-13 12.86 + 0.38 15-19 15.86 + 1.57 17-20 18.57 + 1.13 9-10 9.71 +0.49 8-10 8.86 + 0.90 12-13 12.71 + 0.49 15-18 16.14+ 1.21 20-23 21.57 + 0.98 10-13 | eo =e [i 53-56 54.144 1.35 1-6 3.43 + 1.51
L. angapuka sp. nov.
n=7 5.20-9.22 6.33 + 1.41 6-8 7.00 + 0.58 7-10 8.43 + 0.98 8-10 9.00 + 0.82 6-8 6.86 + 0.69 7-8 7.14+0.38 4—5 414+0.38 6-7 6.14+ 0.38 8-10 9.00 + 0.82 13-17 14.29 + 1.50 7-9 8.29 + 0.76 9-13 11.29 + 1.38 11-15 13.57+ 1.62 15-18 17.00 + 1.15 7-10 8.71+1.11 7-11 9.29 + 1.50 11-14 12.00 + 1.00 12-18 15.14+ 1.86 20-23 21.434 1.13 9-13 10.86 + 1.35 60-76 67.29 + 5.59 2-6 3.43 + 1.62
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Appendix II (continued). Measured morphometric traits and meristic characters.
Morphological L. balagueri L. chiribaya L. insolitus L. nazca L. angapuka sp. nov. characters n=12 n=10 n=15 n=7 n=7 M2 1-2 2 1 1-3 1-2 1.33 + 0.49 2.00 + 0.00 1.00 + 0.00 1.86 + 0.69 1.86 + 0.38 M3 6-9 7-8 5-9 6-9 7-8 7.50 + 0.80 7.20 + 0.42 7.07 + 1.28 7.57+1.13 7.43 £0.53 M5 3-5 3-5 4-8 46 5-6 4.25+0.62 4.00 + 0.47 6.73 + 0.96 4.71+0.76 5.29 + 0.49 M4 3-6 3-5 3-8 3-6 4—7 4.75 +0.87 3.80 + 0.63 6.47 + 1.30 486+ 1.07 5.71 £0.95 M13 1-6 2-6 5—16 4—]] 3-8 3.92 + 1.68 420+ 1.40 10.00 + 3.21 6.57 + 2.64 5.29 + 1.80 M14 2-6 3-7 2-8 3-11 1-6 3:75 1:29 440+ 1.07 4.27+1.71 7.86 £2.97 3.86 + 1.95 M15 1-6 1-8 5—24 1-12 1-4 3.50 + 1.51 460+ 2.67 12.53 + 5.05 5.86 + 3.72 2.29 + 1.25 M23 26-30 19-25 26-32 21-25 28-36 27.17 + 1.34 21.70 + 1.89 28.80 + 2.48 23.86 + 1.46 30.86 + 3.02 M26 52-60 55-66 52-60 54-59 63-72 56.50 + 2.28 61.80 + 3.68 55.80 + 2.27 56.86 + 1.95 67.29 + 3.15 M32 65-79 67-77 69-80 65-74 73-87 73.17 + 3.69 72.70 + 2.95 73.53 + 3.36 70.57 + 2.88 82.43 + 4.72 M34 | 1 2-4 1-2 1 1.00 + 0.00 1.00 + 0.00 2.87 + 0.52 1.86 + 0.38 1.00 + 0.00 D6 6-8 6-8 6-8 7-10 7-9 6.92 + 0.67 7.30 + 0.67 6.47 + 0.74 P71 SAM 8.14 +0.69
A new species of Liolaemus from Peru
Note: Range in the first line; mean + standard deviation (mm) for quantitative characters in the second line.
Legend: Snout-vent length (SVL); minimum distance between the nasal scales (DN); snout width at the edge of the canthal scale (AH); distance from the nose to the back edge of the canthal scale (NC); distance between the posterior edge of the superciliary series (EO); length of the interparietal (LEI); length of the parietal (PA); mental scale width (AM); length of the mental scale (LM); distance from nostril to mouth (NB); rostral height (HR); length of the subocular scale (ES); auditory meatus height (hTy); auditory meatus width (aTy); length of the preocular scale (LPO); preocular width (LPOT); length of the fourth supralabial scale (LCSP); length of the fourth lorilabial scale (LCLB); length between orbits (DEO); length of the first finger of the forelimb, without claw (1D); length of the claw of the fourth finger of the forelimb (G4D); length of the fifth finger of the forelimb without claw (5D); humerus width (AHU); distance from the insertion of the forelimb in the body toward the elbow (LEA1); thigh width (AMU); length of the first toe of the hind limb without claw (1P); length of the claw of the fourth toe of the hind limb (4U); length of the five dorsal scales in a row in the middle of the body (ED); cloacal opening width, measured distance between the corners of the cloaca (PP); body width (AL); width of the base of the tail (WTB); upper width of the pygal area (ASPI); length of the pygal area (LPI). Number of scales around the interparietal scale (A11); number of supralabials on the right side (A12); number of supralabials on the left side (A15); number of infralabials on the right side (A13); number of infralabials on the left side (A19); number of scales around the mental scale (A14); number of scales around the rostral scale (A16); number of lorilabials (A17—1); Hellmich index (A18); subdigital lamellae of the first finger of the forelimb (A20-1); subdigital lamellae of the second finger of the forelimb (A20—2); subdigital lamellae of the third finger of the forelimb (A20-3); subdigital lamellae of the fourth finger of the forelimb (A20-4); subdigital lamellae of the fifth finger of the forelimb (A20—5); subdigital lamellae of the first toe of the hind limb (A21—1); subdigital lamellae of the second toe of the hind limb (A21—2); subdigital lamellae of the third toe of the hind limb (A21-—3); subdigital lamellae of the fourth toe of the hind limb (A21-—4); subdigital lamellae of the fifth toe of the hind limb (A21—5); number of dorsal scales between the occiput and the level of the anterior edge of the thigh (A22); number of precloacal pores (A26); number of scales between canthal and nasal scales (M2); number of scales around the nasal scale (M3); number of supraocular enlarged scales in the right side (M5); number of supraocular enlarged scales in the left side (M4); number of organs in the postrostral scales (M13); number of organs in the third lorilabial scale (M14); number of organs in the scale above the row of the lorilabial scales and below the canthal and preocular scales (M15); number of gular scales (M23); number of scales around midbody (M26); number of ventral scales (M32); number of auricular scales, projecting scales on anterior edge of auditory meatus (M34); and number of paravertebral spots in the right side (D6).
Amphib. Reptile Conserv. 30 September 2020 | Volume 14 | Number 3 | e250
Official journal website: amphibian-reptile-conservation.org
Amphibian & Reptile Conservation 14(3) [Taxonomy Section]: 31-45 (e251).
urn:lsid:zoobank.org:pub:BC39D736-FFFC-481D-B5FA-6CB84EA4E7AA
A new cryptic species of Cnemaspis Strauch, 1887 (Squamata: Gekkonidae), in the C. /ittoralis complex, from Anakkal, Palakkad, Kerala, India
‘*TAmit Sayyed, *'Vivek Philip Cyriac, and *Raveendan Dileepkumar
'Wildlife Protection and Research Society, Maharashtra, INDIA *IISER-TVM Centre for Research and Education in Ecology and Evolution (ICREEE), School of Biology, Indian Institute of Science Education and Research, Thiruvananthapuram, Kerala 695551, INDIA *YIPB Department of Biotechnology, University of Kerala, INDIA
Abstract.—A new cryptic species of the gekkonid genus Cnemaspis is described from the Central Western Ghats of Kerala, India. Cnemaspis palakkadensis sp. nov. is a small-sized (snout-vent length less than 35 mm) Cnemaspis in the littoralis clade. Although the new species superficially resembles C. littoralis, it shows moderate levels of genetic divergence in the 16S rRNA gene, and can be differentiated from all other Indian congeners by a Suite of distinct morphological characters: dorsal scales homogenous, small, smooth; absence of conical or spine-like tubercles on flanks; ventral scales smooth, imbricate; dorsal scales of limbs smooth; 15 or 16 femoral pores on each side separated by 14 poreless scales; lamellae under fourth digit of manus 12-15 and pes 14—17; absence of whorls of pointed tubercles on tail; median subcaudals enlarged, imbricate, smooth.
The species is found in an ignored low-lying forest habitat in parts of the Anakkal reserve forest in Kerala.
Keywords. Asia, description, dwarf gecko, mountains, Reptilia, southern Western Ghats
Citation: Sayyed A, Cyriac VP, Dileepkumar R. 2020. A new cryptic species of Cnemaspis Strauch, 1887 (Squamata: Gekkonidae), in the C. /ittoralis complex, from Anakkal, Palakkad, Kerala, India. Amphibian & Reptile Conservation 14(3) [Taxonomy Section]: 31-45 (e251).
Copyright: © 2020 Sayyed et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribution 4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Accepted: 15 July 2020; Published: 8 September 2020
Introduction
The genus Cnemaspis Strauch, 1887 is among the most speciose of the Old World gekkotan genera, with at least 168 known species, ranking as the second most diverse gecko genus in the world after Cyrtodactylus (Uetz et al. 2020). Although large-scale molecular phylogenetic analyses have recently shown the genus to be polyphyletic (Gamble et al. 2012; Pyron et al. 2013; Zhang and Wiens 2016), there has been limited effort to resolve these issues, probably due to the lack of wide- spread sampling, specifically in the Indian region. With 48 species in mainland India, Cnemaspis represents the largest group of geckos in the country, with a large majority of the species restricted to the Western Ghats. The Western Ghats, a long north-south orientated mountain chain extending from Gujarat in the north (21.00°N) to the southern tip of peninsular India in Tamil Nadu (08.25°N), is one of the 36 global biodiversity hotspots (Myers et al. 2000). Its historical isolation from
neighboring regions, complex topography, and humid tropical to subtropical climate have resulted in a high level of generic endemism, which 1s specifically accentuated in many amphibians and reptiles (Vijayakumar et al. 2014; Cyriac and Kodandaramaiah 2017). Widespread exploration in the higher reaches of the Western Ghats has rapidly increased the number of reptile and amphibian species in India (e.g., Zacharyah et al. 2011; Byu et al. 2014; Viyayakumar et al. 2014; Zacharyah et al. 2016; Sayyed et al. 2018; Chaitanya et al. 2019). However, recent surveys in the low-lying regions of the Western Ghats and several isolated hillocks in peninsular India are revealing a great amount of undocumented lizard diversity, especially among members of the genus Cnemaspis (Khandaker et al. 2019; Agarwal et al. 2020; Cyriac et al. 2020). In light of this, field surveys were conducted in the lowland forests bordering the Palghat gap in Kerala and Tamil Nadu, the largest geographical break in the long Western Ghats chain of mountains. These explorations revealed a new undescribed species
Correspondence. !:*amitsayyedsatara@gmail.com, ? vivek.cyriac@gmail.com, * dileepkamukumpuzha@gmail.com, ‘Authors contributed
equally to this work.
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which resembles the widespread C. J/ittoralis (Jerdon) and 1s described here based on its genetic distinctiveness and a suite of distinct morphological characters.
Materials and Methods
Field sampling and specimens. Field surveys were conducted during May 2019, in parts of Anakkal, Palakkad District, Kerala, India. Specific sampling locations were chosen based on previous observations. All adult specimens were collected by hand, photographed in life, and then euthanized using halothane. Thigh muscles were collected as tissue samples for further genetic analysis, after which specimens were fixed in 4% formaldehyde for ~24 hours, washed in water, and transferred to 70% ethanol for long-term storage. Scalation and other morphological characters were recorded using a Lensel stereo microscope. The materials referred to in this study are deposited in the collection of the Bombay Natural History Society (BNHS), Mumbai, and were collected under the permits issued by the Kerala Forest and Wildlife Department (permits to RD, numbers WL10- 41691/2014 and 94/2009).
Phylogenetic analysis. Total genomic DNA _ was extracted from the tissue samples using protocols as per Sayyed et al. (2016). The 16S rRNA mitochondrial gene was amplified using the primers designed by Palumbi et al. (1991) following standard 3-step PCR protocols (Palumbi 1996). The amplicons were then Sanger sequenced using the primers. The resulting sequences were manually checked for sequencing artifacts, and then added to the 16S rRNA sequence matrix generated by Cyriac et al. (2020) for the Indian Cnemaspis. However, C. nilagirica was removed from the matrix generated by Cyriac et al. (2020), since we found that the sample used was contaminated. The sequences were aligned using the MAFFT algorithm (Katoh and Standley 2013). The pair-wise uncorrected p-distances between and within species for the 16S rRNA gene were then calculated after removing all ambiguous positions for each sequence pair using MEGAX (Kumar et al. 2018). For the downstream phylogenetic analysis, multiple sequences of the same species were removed, except for the two sequences of C. /ittoralis. The best-fit substitution model was determined using PartitionFinder 2 (Lanfear et al. 2016) on the final 596 bp dataset and then a Maximum Likelihood analysis was performed using IQ-TREE (Nguyen et al. 2015) under the GTR+I+G substitution model with 1,000 standard bootstrap replicates. The MAFFT alignment, Partition Finder analysis, and Maximum Likelihood analysis were carried out using the phylogenetic workflow implemented in the PhyloSuite platform (Zhang et al. 2020). Following Cyriac et al. (2020), the tree was rooted by including three species of Lygodactylus and three species of Phelsuma as outgroups for the phylogenetic reconstruction (see Appendix 1).
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Morphological and meristic data. For the specimens listed in Appendix 2, the following measurements were taken using a Yamayo digimatic calliper, a Mitutoyo 500, or a Tesacalip 64 (to the nearest 0.1 mm): snout- vent length (SVL), from tip of snout to anterior edge of cloacal opening; trunk length (TL), distance from axilla to groin measured from posterior edge of the forelimb insertion to the anterior edge of the hind limb insertion; trunk width (TW), maximum width of body; tail length (TAL), from vent to tip of tail; tail width (TLW), measured at widest point of tail; head length (HL), distance from tip of snout to posterior edge of mandible; head width (HW), maximum width of head; head depth (HD), maximum depth of head, from occiput to underside of jaws; upper arm length (UAL), distance from axilla to elbow; forearm length (FAL), from base of palm to elbow; femur length (FEL), distance from groin to the knee; tibia length (TBL), knee to tarsus; toe length (TOL), distance from tip of toe to the nearest fork; palm length (PAL), distance between posterior-most margin of palm and tip of fourth digit; finger length (FL), distance from the tip of the finger to the nearest fork; eye to nares distance (E-N), distance between anterior- most point of eye and nostril; eye to snout distance (E-S), distance between anterior-most point of eye and tip of snout; eye to ear distance (E-E), distance from anterior edge of ear opening to posterior corner of eye; tympanum diameter (EL), maximum distance end-to-end (height) of ear opening; distance between nares (IN), right to left nare; orbital diameter (OD), greatest diameter of orbit; interorbital snout distance (IO), distance between orbit and snout on frontal bone.
Meristic data recorded for all specimens were number of supralabials (SupL) and infralabials (InfL) on left (L) and right (R) sides; number of interorbital scales (InO); number of postmentals (PoM); number of posterior postmentals (PoP), scales that are surrounded by the posterior-postmentals and between infralabials; number of supranasals (SuN), excluding the smaller scales between the larger supranasals; number of the postnasals (PoN), all scales posterior to the naris; number of supraciliaries (SuS); number of scales between eye and tympanum (BeT), from posterior-most point of the orbit to anterior-most point of the tympanum; number of canthal scales (CaS), number of scales from posterior- most point of naris to anterior-most point of the orbit; number of dorsal paravertebral scales (PvS), between pelvic and pectoral limb insertion points along a straight line immediately left of the vertebral column; number of mid-dorsal scales (MbS), from the center of mid-dorsal row diagonally towards the ventral scales; number of midventral scales (MvS), from the first scale posterior to the mental to the last scale anterior to the vent; number of mid-body scales (BIS), across the ventral between the lowest rows of dorsal scales; femoral pores (FPores), the number of femoral pores; lamellae under digits of manus (MLam) and pes (PLam) on right (R) side, counted from
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BNHS 2458 Cnemaspis amboliensis ZS] R 1049 Cnemaspis sp : a4 ZSI R 1050 Cnemaspis sp goaensis clade ZSI R 1045 Cnemaspis goaensis . : , _ mysoriensis 22 - BNHS 2510 Cnemaspis peer daite 45 BNHS 2512 Cnemaspis otai BNHS 2465 Cnemaspis adii BNHS 2514 Cnemaspis gracilis BNHS 2446 Cnemaspis girii ZS! R 1053 Cnemaspis limayei ZSI R 1048 Cnemaspis mahabali ZSI R 1058 Cnemaspis ajijae ————- ZS] WRC 1043 Cnemaspis flaviventralis BNHS 2516 Cnemaspis indica BNHS 2517 Cnemaspis littoralis 400 BNHS 2518 Cnemaspis littoralis Cnemaspis palakkadensis sp. nov. = VPCGK 014 Cnemaspissp 1 pepara 95 VPCGK 021 Cnemaspis sp 2 vagamon VPCGK 016 Cnemaspis anamudiensis BNHS 2466 Cnemaspis cf heteropholis VPCGK 050 Cnemaspis cf heteropholis
42 2
giri clade
87
southern WG clade
32
26
BNHS 2520 Cnemaspis wynadensis
79 27
UP W 007 Cnemaspis chengodumalaensis
wynadensis clade
70 VPCGK 051 Cnemaspis kottiyoorensis
83 UP W 001 Cnemaspis zacharyi
BNHS 2448 Cnemaspis kolhapurensis
Fig. 1. 16S rRNA tree of the Indian Cnemaspis obtained from the Maximum Likelihood analysis in IQ-TREE. Node values indicate bootstrap support with values < 70 indicating low support, values between 70—90 indicating moderate support, and values > 90 indicating strong support. The blue and yellow circles represent the branches leading to C. /ittoralis and C. palakkadensis sp. nov., respectively, along with representative images of the two species indicated by their blue (C. /ittoralis) and yellow (C. palakkadensis
sp. nov.) borders.
first proximal enlarged scansor greater than twice width of the largest palm scale, to distal-most lamella at tip of digits; and lamellae under fourth digit of pes (LampIV). For the geographical coordinates, altitude, and temperature readings, a Kestrel 4500 receiver was used. Opportunistic observations on the ecology of the species were also made during field work. Since the specimens from Palakkad most closely resembled Cnemaspis littoralis, specimens were compared with the neotype of C. littoralis and other associated material deposited at the Zoological Survey of India Western Ghats Regional Center (ZSI-WGRC), Kozhikode, India.
Morphometric analysis. The morphometric analysis was performed in R V. 3.5.2 (R Core Team 2016). A multivariate analysis was carried out on 25 morphometric variables. This analysis included only 25 variables for the analysis out of the 29 variables collected because some variables were unavailable for a few specimens due to missing tails or digits (see Table 3). A Principal Component Analysis (PCA) was performed on the 25 variables to identify the variables that contributed to the observed variation in the data. Plots were generated for the first and second, and the first and third principal components to visually examine the morphospace of
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the new species and the morphologically similar C. littoralis.
Results Phylogenetic Relationships
The topology recovered by the Maximum Likelihood analysis indicated well-supported deeper nodes but showed low support for many shallower nodes (Fig. 1). The topology was mostly consistent with the topology recovered by Sayyed et al. (2018) and Cyriac et al. (2010), except for the position of Cnemaspis indica where C. indica was sister to members of the giri, gracilis, mysoriensis, goaensis, and amboliensis clades. The new species was recovered as being sister to C. /ittoralis with very strong support (Fig. 1). The Jittoralis clade was sister to the (indica + (giri + ((((adii + mysoriensis) + gracilis) + goaensis) + amboliensis))) clade. Uncorrected pairwise sequence divergence for the 16S rRNA gene indicated that the /ittoralis clade was deeply divergent from the rest of the species (Sequence divergence > 10). However, there was only a moderate level of genetic divergence between C. /ittoralis and C. palakkadensis sp. nov., which ranged between 2.5—2.7%.
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Table 1. Loadings obtained from the Principal Component Analysis of the 25 morphometric variables. Bold values indicate strong
loading with correlation > 0.5.
Character Description
SVL Snout-vent length TL Axilla-groin distance TW Trunk width
OD Eye diameter
E-N Eye-to-nasal distance E-S Snout length
E-E Eye-to-ear distance IN Inter-nasal distance EL Horizontal diameter of ear opening HL Head length
HW Head width
HD Head depth
IO Inter-orbital distance UAL Upper arm length FAL Lower arm length PAL Palm length
FL1 Length of 1* finger FL3 Length of 3" finger FL4 Length of 4" finger FL5 Length of 5" finger FEL Femur length
TBL Tibia length
TOLI Length of 1* toe TOL2 Length of 2" toe TOL4 Length of 4" toe Eigenvalue
Standard deviation Proportion of variance
Cumulative proportion
Morphometric Analysis
Principal Component Analysis indicated that the first three PCs explained 77.7% of the variation in morphology. PC1 explained ca. 48.9% of the variation and described a shorter, slender body form with a shorter head, shorter snout, larger eyes, and short limbs (Table 1). PC2 explained ca. 20.2% of the variation and is described mostly by smaller eyes, shorter eye-to-ear distance, smaller ear opening, and shorter forelimbs (Table 1). PC3 explained ca. 8.1% of the variation and described a less depressed head and narrower interorbital region (Table 1). Plots of PC1 with PC2 and PC1 with PC3 indicated considerable differences in the morphospace between the new species and C. /ittoralis, with the differences being along PC1 (Fig. 2A—B).
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PCI PC2 PC3 -0.8278 -0.3045 -0.2238 -0.8229 -0.2799 -0.2737 -0.7241 -0.4259 -0.3070 0.6453 -0.6311 -0.0557 -0.9000 0.2800 0.0950 -0.7350 -0.3478 -0.0852 -0.3239 -0.5513 0.4186 -0.9745 0.1924 -0.0163 0.4675 -0.7923 -0.1568 -0.6952 -0.5014 0.2935 -0.8603 -0.3320 0.2034 -0.3677 -0.2852 0.5858 -0.6162 -0.0902 -0.5711 -0.4407 -0.7307 0.1714 -0.6657 -0.4920 0.3509 -0.7949 0.2111 -0.2336
0.5045 -0.5947 0.0675 0.6421 -0.0028 0.3832 0.7575 -0.4670 0.0566 0.6749 -0.5265 -0.3075 -0.9383 -0.2243 0.0515 -0.6979 -0.1892 0.2162 0.7920 -0.5161 -0.0054 0.6670 -0.6226 -0.1914 -0.4037 -0.5158 -0.4972 12.2328 5.0454 2.0250 3.4976 2.2462 1.4230 0.4893 0.2018 0.0810 0.4893 0.6911 0.7721 Systematics
Cnemaspis palakkadensis sp. nov. Figs. 3-7; Tables 2-4.
urn: lsid:zoobank.org:act:4A854A 91-206D-41E0-959 E-5761F3040380
Holotype. BNHS 2790, an adult male, 32.2 mm SVL, from Anakkal (10°52’50”N, 76°39’23”E; ca. 140 m asl), Palakkad District, Kerala, south-western India (Fig. 1), collected by Amit Sayyed, 18 May 2019.
Paratype. BNHS 2791, an adult male, 31.5 mm SVL, and BNHS 2792, an adult female, 34.1 mm SVL; collected from same locality as holotype by Vivek Vaidyanathan and Abhijit Nale, 19 May 2019.
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72.5°E
Species (@|C. littoralis
Dim2 (20.2%) Oo
Dim3 (8.1%) oOo
! \ \ \ ' 1 \ \ -------- + ' \ \ \ \ ' 1 \ \ T +
72.5°E
4 0 Dim1 (48.9%)
_75.0°E
77.5°E
77.5°E
Fig. 2. Results of the morphometric analysis comparing the morphospace occupied by Cnemaspis littoralis and C. palakkadensis sp. nov. (A) Morphospace occupied by the two species as indicated by the first two dimensions (PC1 and PC2); (B) morphospace occupied by the two species as indicated by the first and third dimensions (PC1 and PC3); and (C) map showing the distributions of C. littoralis and C. palakkadensis sp. nov. The blue and yellow points in the morphospace and the map correspond to C. /ittoralis
and C. palakkadensis sp. nov., respectively.
Diagnosis and comparison with Indian congeners. A small-sized Cnemaspis, SVL < 35 mm; dorsal pholidosis homogenous with small, smooth, granular scales in the vertebral and paravertebral regions; conical or spine- like tubercles absent on flank; ventral scales smooth, imbricate; males with 15-16 femoral pores on each thigh and no pre-cloacal pores; supralabials to angle of jaw 7-8, infralabials to angle of jaw 6—8; lamellae under fourth digit of manus 12—15, and pes 14-17; tail without whorls of enlarged tubercles; median subcaudals enlarged, imbricate, smooth, post cloacal spur absent in both sexes.
Cnemaspis palakkadensis sp. nov. can be distinguished from all other Indian congeners on the basis of the following differing or non-overlapping characters: Spine-like tubercles absent on flanks [versus spine-like tubercles present on flank in C. amboliensis Sayyed, Pyron, and Dileepkumar, C. assamensis Das and Sengupta, C. anandani Murthy, Nitesh, Sengupta, and Deepak, C. flaviventralis Sayyed, Pyron, and Dahanukar, C. goaensis Sharma, C. gracilis (Beddome), C. jerdonii (Theobald), C. koynaensis Khandekar, Thackery, and Agarwal, C. monticola Manamendra-Arachchi, Batuwita, and Pethiyagoda, C. mysoriensis (Jerdon), C. monticola Manamendra-Arachchi, Batuwita, and Pethiyagoda, C. nilagirica Manamendra-Arachchi, Batuwita, and Pethiyagoda, and C. otai Das and Bauer]. Dorsal scales on midbody homogenous [versus heterogeneous in C. aaronbaueri Sayyed, Grismer, Campbell, and
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Dileepkumar, C. agarwali Khandekar, C. ajijae Sayyed, Pyron, and Dileepkumar, C. amba Khandekar, Thackery, and Agarwal, C. amboliensis, C. anamudiensis Cyriac, Johny, Umesh, and Palot, C. anandani, C. andersonii (Annandale), C. australis Manamendra-Arachchi, Batuwita, and Pethiyagoda, C. avasabinae Agarwal, Bauer, and Khandekar, C. bangara Agarwal, Thackeray, Pal, and Khandekar, C. beddomei (Theobald), C. chengodumalaensis Cyriac, Palot, and Deutiand Umesh, C. flaviventralis, C. girii Mirza, Pal, Bhosale, and Sanap, C. goaensis, C. gracilis, C. graniticola Agarwal, Thackeray, Pal, and Khandekar, C. heteropholis Bauer, C. kottivoorensis Cyriac and Umesh, C. koynaensis, C. limayei Sayyed, Pyron, and Dileepkumar, C. maculicollis Cyriac, Johny, Umesh, and Palot, C. mahabali Sayyed, Pyron, and Dileepkumar, C. monticola Manamendra- Arachchi, Batuwita, and Pethiyagoda, C. nairi Inger, Marx, and Koshy, 1984, C. ornata (Beddome), C. shevaroyensis (Khandekar, Gaitonde and Agarwal, C. sisparensis (Theobald), C. thackerayi Khandekar, Gaitonde, and Agarwal, C. wicksii (Stoliczka), C. yelagiriensis Agarwal, Thackeray, Pal, and Khandekar, and C. yercaudensis Das and Bauer]. Presence of a series of 15-16 femoral pores on each side and the absence of pre-cloacal pores in males [versus absence of femoral pores in C aaronbaueri, C. anamudiensis, C. avasabinae, C. assamensis, C. beddomei, C. boiei (Gray), C. maculicollis, C. nairi, and C. ornata; presence of both pre-cloacal and femoral pores in C. adii, C.
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Table 2. Measurements (to the nearest 0.1 mm) of the type series of Cnemaspis palakkadensis sp. nov. Measurement abbreviations
are defined in the text.
Measurement Holotype BNHS 2790 Sex male SVL 32.2 TL 15.6 TW 6.4 TAL a5 TLW 3.4 HL 8.9 HW 52 HD 3.3 UAL 4.5 FAL 5.5 FEL 5.8 TBL 5.9 PAL 3.7 E-N 4.0 E-S 4.1 E-E 2.5 EL 0.3 IN 1.6 OD 2 IO 3.3
agarwali, C. amboliensis, C. andersonii, C. australis, C. bangara, C.gracilis, C. goaensis, C. graniticola, C. mysoriensis, C. otai, C. shevaroyensis, C. thackerayi, C. wicksii, C. yelagiriensis, and C. yercaudensis|; and from the following species by presence large number of femoral pores [versus < 10 femoral pores on each side in C. ajijae, C. amba, C. anandani, C. chengodumalaensis, C. flaviventralis, C. girti, C. heteropholis, C. indica, C. Jerdonii, C. kottiyoorensis, C. koynaensis, C. limayei, C. mahabali, C. nilagirica, C. sisparensis, C. wynadensis, and C. zacharyi Cyriac, Palot, and Deutiand Umesh; and a continuous series of precloacal-femoral pores in C. kolhapurensis|. Median subcaudals enlarged [versus small median subcaudals in C. adii, C. ajijae, C. amba, C. andersonii, C. flaviventralis, C. girii, C. gracilis, C. koynaensis, and C. limayei].
Cnemaspis palakkadensis sp. nov. could be confused with the morphologically similar C. /ittoralis (Jerdon), but can be distinguished by its longer trunk length (AG 46-49% of SVL versus AG 37-46% of SVL in C. littoralis), much smaller eyes (ED 13-14% of HL versus ED 16-21% of SVL in C. Jittoralis),; absence of conical or spine-like tubercles on flanks (versus small spine-like tubercles present on flanks in C. /ittoralis), supralabials to angle of jaw 7-8 (versus 9-10 supralabials in C. littoralis),; number of scales between eye and tympanum 18-19 (versus 17); mid-dorsal scales 54—57 (versus 52);
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Paratypes BNHS 2791 BNHS 2792 male female 31.5 34.0 14.6 16.7 52 6.8 32.6 33.3 27 2.8 8.7 9.1 S| 5.2 3.3 3.5 3.8 4.6 5.3 5.6 St 59 5.9 6.0 3.6 3.9 4.0 4.2 4] 43 pies: 25 0.2 0.3 1.6 1.6 1.2 be 322 3.4
midventral scales 130-134 (versus 122); number of mid-body scales 32—38 (versus 26); absence of a small post-cloacal spur on both sides of the tail and absence of whorls of enlarged tubercles on the tail (versus a single post-cloacal spur present on each side of the tail and whorls of small but enlarged tubercles on the dorsal side of the tail in C. Jittoralis).
Description of holotype. An adult male of SVL 32.2 mm (Fig. 3A—B); head moderately short (HL 17.6% of SVL), narrow (HW 15.9% of SVL), flat CHD 59.4% of HL), distinct from neck; snout short (E-S 78.6% of HL), slightly curved laterally; scales on snout granular, smooth, larger than those on the forehead and interorbital region (Fig. 4A); eye small (OD 21.8% of HL); pupil rounded; 13 supraciliaries; 30 interorbital scales; ear opening small (EL 5.7% of HL), longer than broad; 18 scales between eye and tympanum. Rostral wider than long, partially divided by a deep median groove; nostrils small, bordered posteriorly by two small, granular, postnasal scales; single enlarged supranasal on each side separated by an elongated intermediate scale. Mental large, triangular, not pointed posteriorly, broader than long, bordered posteriorly by two postmentals and a single intermediate chin shield broadly separated the postmentals, eight scales surrounded posteriorly by the posterior postmentals, infralabials, and the mental;
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Fig. 3. Holotype (BNHS 2790) of Cnemaspis palakkadensis sp. nov. (A) Dorsal view and (B) ventral view of full-body. Photos by Amit Sayyed.
three smooth, large scales posteriorly surrounded by intermediate chin shield; gular scales granular, smooth, larger than those on throat (Fig. 4B). Seven supralabials to angle of jaw on each side, supralabial I largest, decreasing in size posteriorly; six infralabials to angle of jaw on each side, infralabial I largest, decreasing in size posteriorly (Fig. 4C).
Fig. 4. Holotype (BNHS 2790) of Cnemaspis palakkadensis sp. nov. (A) Dorsal, (B) ventral, and (C) lateral views of the head. Photos by Amit Sayyed.
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Body slender, short (TL 40%) without conical or spine-like tubercles on flanks (Fig. 5A, C). Dorsal scales of the body and flank homogenous, small, granular, smooth; scales on forehead, neck, and dorsal body equal in size; paravertebral scales 112; number of mid-dorsal scales 54; scales arranged in 33-35 longitudinal rows at midbody, number of midventral scales 131, smooth, imbricate, larger than dorsals (Fig. 5B). Fore and hind limbs relatively long, slender (FL 16.8%; TBL 16.4%); dorsal scales of brachium granular, smooth, larger than forearm; dorsal scales of forearm small, granular; ventral scales of brachium and forearm small, smooth; dorsal scales on palm, foot and fingers granular, smooth; scales on palmar and plantar surfaces smooth; subdigital lamellae entire, few fragmented; series of unpaired lamellae on basal portion of digits, separated from fragmented distal lamellae by a single large scale at the inflection; proximal lamellae series: 1-3-4-4-3 (right manus), 1-4-5-6-3 (right pes); distal lamellae series: 9-11-14-14-12 (right manus), 9-13-15-17-11 (right pes). Relative lengths of digits, fingers: IV (2.71 mm) > III (2.53 mm) > II (2.42 mm) > V (1.87 mm) > I (1.18 mm); toes: IV (3.68 mm) > III (3.16 mm) > II (1.99 mm) > V (1.75 mm) > 1 (0.85 mm) [Fig. 6A—B]. Femoral pores 15; 14 poreless scales between right and left femoral pore series; three rows of enlarged, roughly hexagonal scales above the femoral pores, larger than those on precloacal region; no precloacal pores; precloacal scales equal in size to the belly scales (Fig. 6C).
Tail long (TAL 111%), cylindrical, base swollen; post-cloacal spur absent on each side of lateral surface of hemipenal bulges at base of tail; dorsal scales of tail homogenous, smooth, granular, without enlarged, conical tubercles forming whorls, ventral scales imbricate, smooth; median subcaudals enlarged, smooth; those at the base are moderately smaller and imbricate (Fig. 6D-F).
Coloration in life (Fig. 6A—C). Male and female of the new species are the same in dorsal appearance. Dorsum of head mottled with brown and yellow; ventral side of head bright orange-yellow in males but white in females, bordered by a dark brown line up to the throat; nape with a small, black ocelli-like marking. Iris yellow with thin dark yellow line bordering pupil; pupil circular, black; supraciliaries yellow; supralabials and _ infralabials yellow. Dorsum of the body and limbs dull grey with brown and pale yellowish mottling; vertebral region pale yellow with 6-7 dark-edged lighter markings. Tail dull brown dorsally, with irregular faded yellow spots. Ventral side of body and tail white.
Coloration in preservative. Dorsum of the body and limbs with brown which turns into dark brown and pale yellow mottling and into grey; ventral side of body and tail greyish white; ventral side of head in males grey with slight yellowish tinge.
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Table 3. Meristic data for the type series of Cnemaspis palakkadensis sp. nov. The symbol “?” indicates a broken finger, and “—”
indicates pores not present.
Character Holotype (BNHS 2790) Paratype (BNHS 2791) Paratype (BNHS 2792) Sex male male female SupL R/L 7/7 8/8 8/8
InfL R/L 6/6 8/8 8/7
SuS 13 13 13
InO 30 32 31
BeT 18 18 19
PoN 2
PoM 2
PoP 10
SuN 1 1 1
CaS 14 15 14
PvS 112 109 113
MbS 54 54 57
MvS 131 130 134
BIS 33-35 32-34 35-38 FPores 15/15 16/16 — MLam R 9-11-14-14-12 7-10-12-12-11 9-?-13-15-13 PLam R 9-13-15-17-11 7-12-9-14-13 9-14-16-17-15
Variation of the type series (Tables 1-3). The SVL of adult specimens in the type series of Cnemaspis palakkadensis sp. nov. (n = 3) ranges from 31.5 to 34.1 mm; number of posterior postmentals, 8—10; scales between eye and tympanum,18—19; number of interorbitals, 30-32; number of canthal scales, 14—15; number of dorsal paravertebral scales, 109-113; number of mid-dorsal scales, 54-57; number of midventral scales from mental to cloaca, 130—134; number of mid-body scales across belly, 32-38; lamellae under fourth digit of manus (MLamIV) and pes (PLamIV), 12—15 and 14— 17, respectively. Male and female paratypes match the holotype in overall coloration, except for the coloration on the throat.
Etymology. The specific epithet palakkadensis refers to the Palakkad district, from which the type series was collected.
Suggested Common Name. Palakkad Dwarf Gecko.
Distribution. At present, the new species is only known from the type locality in Anakkal reserve forest (10°52’50”N 76°39’23”E) in Palakkad District of Kerala state (Fig. 1C), which is a low-land moist deciduous to riparian forest at an elevation of 84-170 m asl on the northern border of the Palghat gap, a ca. 30-km gap separating the central and southern Western Ghats. However, it is possible that the range of this species may extend to other low-land forests in the Palakkad region of Kerala and Coimbatore of Tamil Nadu.
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Natural history. The species is found in low-land moist deciduous to semi-evergreen forest habitat of Palakkad hills of the Central Western Ghats. The climate of the region 1s moist and humid, and the area is rich in natural forest. All the specimens were found active during the day on the trunks, branches, and exposed roots of large trees around small streams (Fig. 8A—B), suggesting that this species is arboreal and diurnal. Single eggs or pairs of eggs were observed in several tree holes during the field survey (Fig. 7D). Two eggs that were collected measured 5.1 x 4.9mm and 5.2 x 5.0 mm. The types were found sympatrically with Ophiophagus hannah (Cantor), Trimeresurus gramineus (Shaw), Naja naja (Linnaeus), Hypnale hypnale (Merrem), Ahaetulla nasuta Lacepede, Amphiesma_ stolatum (Linnaeus), Lycodon aulicus (Linnaeus), Dendrelaphis tristis (Daudin), Cnemaspis gracilis, Cnemaspis sp., Psammophilus dorsalis (Gray), and Psammophilus sp. (Stoliczka).
Discussion
The phylogenetic analysis recovered a topology mostly concordant with previous studies employing the 16S rRNA gene (Sayyed et al. 2018; Cyriac et al. 2020), even after the removal of Cnemaspis nilagirica from the sequence matrix. However, there was a difference in the phylogenetic placement of Cnemaspis indica. While this analysis recovered moderate support for a sister relationship between C. indica and members of the giri, gracilis, mysoriensis, goaensis, and amboliensis clades (Fig. 1), Sayyed et al. (2018) and Cyriac et al. (2020)
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Fig. 5. Holotype (BNHS 2790) of Cnemaspis palakkadensis sp. nov. (A) Dorsal pholidosis at midbody, (B) ventral scales at midbody, (C) scales on lateral surface of trunk. Photos by Amit Sayyed.
recovered a sister relationship between C. indica and members of the gracilis, mysoriensis, goaensis, and amboliensis clades, albeit with very low support. Such discordance could be due to the removal of C. nilagirica from the analysis or the differences in our analytical approach. Nonetheless, our analysis indicates slightly improved support values for deeper nodes compared to earlier 16S rRNA trees.
The analysis clearly indicated that Cnemaspis palakkadensis sp. nov. was sister to C. /ittoralis, and showed moderate levels genetic divergence (2.5- 2.7%) from the latter. Although genetic divergences of 24% are considered low for the 16S rRNA gene, morphologically distinct species have been shown to exhibit shallow genetic divergence (ca. 1%) for the 16S rRNA gene (Shanker et al. 2017). The specimens described here as C. palakkadensis sp. nov. occupy a distinct morphospace compared to C. Jittoralis, despite the superficial morphological resemblance and shallow genetic divergence with C. /ittoralis. Further, the genetic divergence between C. palakkadensis sp. nov. and C. littoralis was greater than the average intraspecific genetic divergence estimated for 16 Cnemaspis species based on the 16S rRNA gene of only 0.4 + 0.42%, with the maximum intraspecific genetic divergence recorded
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A
Fig. 6. Holotype (BNHS 2790) of Cnemaspis palakkadensis sp. nov. (A) Lamellae on manus, (B) lamellae on pes, (C) femoral pores, (D) dorsal scalation of tail, (E) subcaudals, (F) lateral side of tail. Photos by Amit Sayyed.
being 1.7% (see Appendix 3). The two species are also morphologically distinct and can be distinguished based on several non-overlapping diagnostic characters. Interestingly, C. palakkadensis sp. nov. was found in low-land moist deciduous to semi-evergreen forests in the northern border of the Palghat gap. This gap forms a major dispersal barrier and biogeographic divide to many groups of animals which are distributed on the higher reaches of the Western Ghats (Robin et al. 2010; Van Bocxlaer et al. 2012; Vijayakumar et al. 2014). However, our understanding of what biogeographic barriers influence the distribution of low-land habitat- Specialist species remains poor, mostly due to the lack of systematic exploration of low-lying regions. The discovery of C. palakkadensis sp. nov. from the low-land forests in the Palghat gap further highlight the presence of unknown diversity within the species C. Jittoralis, which is thought to have a wide distribution in the littoral regions of Kerala (Cyriac and Umesh 2013). However, widespread systematic explorations in these low-land forests will be necessary to determine the distributional range of this species. Cyriac and Umesh (2013) designated a neotype for C. /ittoralis based on specimens
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Fig. 7. Color in life of Cnemaspis palakkadensis sp. nov. (A) Holotype male (BNHS 2790), (B) paratype female (BNHS 2792), (C)
= Se. * Sr
holotype male (BNHS 2790) showing the coloration of throat, (D) egg. Photos by Amit Sayyed.
collected from Chaliyam coast in Kozhikode, Kerala, and reported additional specimens from Narayamkulam (= Chengodumala) in Kozhikode district, Nellikuth in Malapuram district, and Kapprikkad in Ernakulam district of Kerala. They also reported observations of C. littoralis from Kannur, Thrissur, Palakkad, Ernakulam, and Thiruvananthapuram in Kerala. However, given the possibility of cryptic species within this group, the true distribution of C. /ittoralis will need further evaluation.
Recent and current explorations in the high and low mountains of the Western Ghats of India have led to the discovery of several unique species of the genus Cnemaspis. Although most of them are from isolated humid forest (Giri et al. 2009b; Srinivasulu et al. 2015; Cyriac et al. 2018; Khandekar et al. 2019a; Sayyed et al. 2019), ongoing studies are showing that Cnemaspis can also be found in drier regions. With the discovery of C. palakkadensis sp. nov., the number of Cnemaspis species in the Indian mainland increases to 43, yet the true diversity within this group is clearly far from being totally uncovered. Recent studies have also hinted at the presence of cryptic diversity within the south Asian Cnemaspis (Agarwal et al. 2017; Cyriac et al. 2020). The current study further calls attention to cryptic diversity within the Western Ghats and adjacent low-lying regions. Thus, widespread fine-scale sampling will be critical for uncovering species richness and distributional patterns within the group.
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Fig. 8. Habitat of Cnemaspis palakkadensis sp. nov. Photos by Amit Sayyed.
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Acknowledgments.—The authors are thankful to the Forest Departments of Kerala for issuing collecting permits, and for their support during field surveys. Deepak Apte (Director) and Rahul Khot (museum curator) of the Bombay Natural History Society, Mumbai, provided access to specimens and registration of the type specimens. We also thank Vithoba Hegde, Umesh P.K, Vivek Vidyanathan, Abhiit Nale, Kiran Ahire, Vikas Jagtap, Mahesh Bandgar, Ayaan Sayyed, and Masum Sayyed for help during fieldwork and for their support.
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Amit Sayyed is a herpetologist, and the founder and director of the Wildlife Protection and Research Society, India. Amit is working on the faunal diversity and conservation of reptiles, and his main interests have been in the taxonomy of snakes, geckos, and frogs. He has published several papers on natural history and faunal diversity, and thus far he has described eight new species. Amit is the author of three books: Amazing Creatures of the Earth (Snakes of Maharashtra, Goa and Karnataka), Butterflies and Spiders of The Western Ghats, and Dangerous Bite and First Aid. His Ph.D. focused on wildlife conservation, and he plans to pursue further studies on the phylogenetic systematics, taxonomy, and natural history of the Indian species of the genus Cnemaspis.
Vivek Cyriac is an evolutionary ecologist from India with broad interests in the ecological and evolutionary mechanisms that generate biodiversity patterns. His work is centered around understanding how environmental factors and biotic interactions influence species diversification and create macro-evolutionary patterns. Vivek uses reptiles and amphibians as model systems to explore diverse questions in ecology, evolution, and behavior. Thus far, he has predominantly worked on fossorial uropeltid snakes and geckos of the genus Cnemaspis.
Raveendan Dileepkumar is currently a Principal Investigator under the Young Investigator’s Program in Biotechnology in the Centre for Venom Informatics, University of Kerala, India. He is also co-investigating projects in the area of venomics supported by KSCSTE, Government of Kerala. His research broadly encompasses the venomics, venom gland transcriptomics, and genomics of venomous snakes; with ongoing projects centered on understanding the venom composition of venomous species in the animal kingdom. His publications, including book chapters, have focused on snake taxonomy, venomics, and venom applications in medical technologies.
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Appendix 1. GenBank accession number and voucher information for Indian Cnemaspis and outgroups used in the phylogenetic analysis. The line highlighted in bold indicates a new sequence generated for C. palakkadensis sp. nov. * indicates accession number of C. kottivoorensis which was misprinted as MT217042 in Cyriac et al. (2020).
No Species Locality Voucher 16s rRNA l Cnemaspis mahabali Pune, Maharashtra ZSI/R/1048 KX753643 2 Cnemaspis amboliensis Sindhudurg, Maharashtra BNHS 2458 MH174358 3 Cnemaspis ajijae Satara, Maharashtra ZSI WRC R/1058 KX753653 4 Cnemaspis limayei Sindhudurg, Maharashtra ZSI WRC R/1053 KX753647 5 Cnemaspis yercaudensis Salem, Tamil Nadu BNHS 2510 MH174360 6 Cnemaspis otai Vellore, Tamil Nadu BNHS 2512 MH174362 si Cnemaspis gracilis Palakkad, Kerala BNHS 2514 MH174370 8 Cnemaspis indica Nilgiris, Tamil Nadu BNHS 2516 MH174366 9 Cnemaspis littoralis Kozhikode, Kerala BNHS 2517 MH174367 10 Cnemaspis littoralis Kozhikode, Kerala BNHS 2518 MH174368 11 Cnemaspis kottiyoorensis Kannur, Kerala BNHS 2519 MH174363 12. = Cnemaspis wynadensis Wayanad, Kerala BNHS 2520 MH174364 13. Cnemaspis goaensis Goa ZSI WRC R/1045 KX269826 14. Cnemaspis flaviventralis Sindhudurg, Maharashtra ZSI WRC R/1043 KX269820 15 = Cnemaspis girii Satara, Maharashtra BNHS 2446 KX269824 16 Cnemaspis kolhapurensis Sindhudurg, Maharashtra BNHS 2448 KX269822 17. Cnemaspis heteropholis Shimoga, Karnataka BNHS 2466 KX753660 18 = Cnemaspis adii Ballari, Karnataka BNHS 2465 KX753655 19. Cnemaspis goaensis Goa ZSI WRC R/1044 KX269825 20 Cnemaspis zacharyi Lakkadi, Wayanad, Kerala BNHS 2735 MT217042 Chengodumala, Kozhikode, 21 Cnemaspis chengodumalaensis Kerala BNHS 2741 MT217043 22 Cnemaspis sp. (Pepara) Pepara WLS, Trivandrum, Kerala VPCGK_014 MT217033 23. =~ Cnemaspis anamudiensis Anamudi RF, Idukki, Kerala VPCGK_016 MT217034 24 Cnemaspis sp. (Vagamon) Vagamon, Kerala VPCGK_021 MT217035 Devarakolli, Madikeri, 25. Cnemaspis heteropholis Karnataka BNHS 2745 MT217039 Devarakolli, Madikeri, 26 Cnemaspis kottiyoorensis Karnataka BNHS 2747 MT217038 27 — Cnemaspis kottiyoorensis Paithalmala, Kannur, Kerala VPCGK_052 MT217037* 28 Cnemaspis palakkadensis sp. nov. Anakkal, Palakkad, Kerala BNHS 2790 MT762366 Outgroups 29 Phelsuma lineata Madagascar ZCMV_2029 KC438463 30 ~—- Phelsuma v-nigra Moheli, Comoros MH10 FJ829967 31 ~=Phelsuma ornata Reunion Sound _P7 DQ270577 32. ~— Lygodactylus picturatus Tanzania LYG 4 HQ872462 33. —- Lygodactylus miops Madagascar LUS8 LN998673 34. ~=— Lygodactylus madagascariensis Madagascar LMIA LN998665 Amphib. Reptile Conserv. 44 September 2020 | Volume 14 | Number 3 | e251
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Appendix 2. Specimens examined. Cnemaspis aaronbaueri. BNHS 2607, BNHS 2608, and BNHS 2609 (females), from Thenmala, Kollam District, Kerala, India.
Cnemaspis beddomei: collection of the Natural History Museum, London (NHMUK), NHMUK 1946.9.4.83 (male), from South Tinnevelly, Tirunelveli, southern Tamil Nadu State, India.
Cnemaspis gracilis: NHMUK 74.4.29.393 (male), from “Palghat Hills” (Kerala State, India), and BNHS 2513 and BNHS 2514, collected from the Palakkad, Kerala, used for examination and genetic analysis.
Cnemaspis indica. NHMUK 46.11.22.22b (male), BNHS 1252-10 (male), Nilgiris, Tamil Nadu, India.
Cnemaspis kolhapurensis: BNHS 1855 (male), Dajipur, Kolhapur district, Maharashtra; and BNHS 2447 and BNHS 2448, from Amboli, Sindhudurg district, Maharashtra, India.
Cnemaspis kottiyoorensis. BNHS 2519 from Kannur, Kerala state, India.
Cnemaspis littoralis: Neotype ZSI/WGRC/IR/V/2377 (male) from Chaliyam, Kozhikode, Kerala; ZSI/WGRC/IR/V/2378a and ZSI/WGRC/IR/V/2378b (males) from Narayamkulam (= Chengodumala), Kozhikode, Kerala; ZSI/WGRC/IR/V/2379a (male) and ZSI/WGRC/IR/V/2379b (female) from Kapprikad, Ernakulam, Kerala; ZSI/WGRC/IR/V/2380 (male) from Chaliyam, Kozhikode, Kerala; ZSI/WGRC/IR/V/2381a and ZSI/WGRC/IR/V/2381b (males) from Nellikuth, Mallapuram, Kerala; BNHS 1150 (male), from Nilambur, Malabar, Kerala state, India. BNHS 2517 and BNHS 2518 from the Kozhikode, Kerala state, India.
Cnemaspis maculicollis: ZS1/WGRC/IR/V/2704 (male), from Pandimotta, Shendurney Wildlife Sanctuary, Kollam District, Kerala, India.
Cnemaspis nilagirica. NHMUK 74.4.29.729 (female), Nilgiries, Nilgiri District, Tamil Nadu State, south-western India. Cnemaspis ornata: Lectotype NHMUK 74.4.29.400 (male), paralectotype NHMUK 74.4.29.401 (male), NHMUK 74.4.29.404 (female), NHMUK 74.4.29.405 (female), NHMUK74.4.29.406 (female), NHMUK 74.4.29.407 (female), NHMUK 74.4.29.408 (female), and NHMUK 74.4.29.409 (female), from South Tinnevelly Hills, Tirunelveli, Tamil Nadu State, India.
Cnemaspis sisparensis: NHMUK 74.4.29.383 (male), from Sholakal, the foot of SisparaGhat, Kerala, India.
Cnemaspis wynadensis. BMNH 74.4.29.355 (male), from Wynaad, Kerala, and BNHS 1042, BNHS 1043 (male), Mannarghat, Palghat, Kerala, India.
Amphib. Reptile Conserv. 45 September 2020 | Volume 14 | Number 3 | e251
Official journal website: amphibian-reptile-conservation.org
Amphibian & Reptile Conservation 14(3) [General Section]: 46—56 (e252).
Amphibian diversity and conservation along an elevational gradient on Mount Emei, southwestern China
12Xiaoyi Wang, '*Shengnan Yang, '?Chunpeng Guo, ‘Ke Tang, ‘*Jianping Jiang, and ‘**Junhua Hu y
'Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, CHINA *University of Chinese Academy of Sciences, Beijing 100049, CHINA ?*Key Laboratory of Southwest China Wildlife Resource Conservation (China West Normal University), Ministry of Education, Nanchong 637009, CHINA
Abstract.—Understanding the diversity, distribution, and threat status of species serves an important role in biodiversity conservation, particularly in regions with high species richness. Being a well-known Natural and Cultural World Heritage site, Mount Emei is seated on the transition zone between Qinghai-Tibetan Plateau and Sichuan Basin in southwestern China, and is of special significance to conservation and science due to its high biodiversity. Based on data from extensive field expeditions, the published literature, and museum specimens, this study documented a total of 35 species, belonging to 22 genera and nine families, along a 2,600 m elevational gradient on Mount Emei. Almost one-third of these species are in IUCN threatened categories. A majority of species occupied a narrower local elevation range size compared with their overall elevation range size, especially those that are threatened. Along the elevational gradient, both the total and threatened species richness showed hump-shaped patterns. These results provide insight into the species diversity, elevational distribution, and threat status for the amphibians on Mount Emei. These findings highlight the significance and urgent need to protect the amphibians in the focal region, provide support for further ecological studies, and will contribute to the conservation of this biodiverse region in the future.
Keywords. Anura, biodiversity, Caudata, hump-shaped pattern, species richness, threatened species, World Heritage site
Citation: Wang X, Yang S, Guo C, Tang K, Jiang J, Hu J. 2020. Amphibian diversity and conservation along an elevational gradient on Mount Emei, southwestern China. Amphibian & Reptile Conservation 14(3) [General Section]: 46-56 (e252).
Copyright: © 2020 Wang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribution 4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are
as follows: official journal title Amphibian & Reptile Conservation; official journal website: amphibian-reptile-conservation.org.
Accepted: 4 April 2020; Published: 20 September 2020 Introduction
Elevational gradients provide one of the most powerful natural experiments for exploring the ecological and evolutionary responses of biota to the complex influences of geophysical and climatic changes (Korner 2007). In mountain regions, elevational gradients yield a large amount of environmental variation (e.g., in temperature and humidity) over a short spatial distance, and play a prominent role in shaping vertical species distribution (Korner 2007; Perrigo et al. 2019). Following in von Humboldt’s footsteps, the importance of elevational gradients to biodiversity has motivated growing scientific interest in them over the last two centuries (Aynekulu et al. 2012; Frishkoff et al. 2019; Lomolino 2001). Along elevational gradients, a multitude of studies have focused on species diversity-elevation relationships across many different taxa worldwide (e.g., Frishkoff et al. 2019; Hu et al. 2011; Longino and Branstetter 2019; Peters et al. 2016; Quintero and Jetz 2018), often revealing monotonic decreasing, hump-
Correspondence. *jiangjp@cib.ac.cn (JJ), hujh@cib.ac.cn (JH)
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shaped patterns or plateaus (Rahbek 2005). While varying degrees of evidence have supported different patterns, understanding the elevational patterns in biodiversity remains crucial for conservation in specific key biodiversity areas and in some taxa which are not well documented.
Among amphibians, the distribution range of a species is highly related to its adaptation to environmental variations and extinction risk (Chen et al. 2019; Cooper et al. 2008). Amphibians with a small geographic (e.g., latitudinal or elevational) range size may face higher extinction risk, since they are relatively less abundant, less mobile, and more easily influenced by local environment changes, compared with those with broad ranges (Botts et al. 2013; Chen et al. 2019; Cooper et al. 2008). Since each species has a unique ecological extension and environmental tolerance (Wells 2007), range size and its shifts along elevational gradients can be regarded as adaptive responses to environmental changes (Chen et al. 2009; Kusrini et al. 2017). Consequently, determining elevational range size
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85°F 90°F
te
Elevation(m)
=
3300 7800
29°30'N
| s
103°20'E
103°15’E
103°2S’E
95°E
40°N
25°N
Fig. 1. (A) Geographic location of Mount Emei; (B) topographic overview of sample sites; and dominant vegetation types and typical habitats along the elevational gradient at (C) 500 m, (D) 1,300 m, and (E) 3,050 m. Sampling sites are indicated with red
stars (see Appendix | for details).
under various environmental conditions is important for contributing to the conservation of amphibians with a narrow range (Chan et al. 2016).
Mount Emei (Omei Shan) is located tn the transitional zone between the Sichuan Basin and Qinghai-Tibetan Plateau in southwestern China (Fig. 1A). It possesses various landscapes and a diversity of natural biological zones with high biodiversity (Li and Shi 2007; Zhao and Chen 1980). Mount Emei, together with the Leshan Giant
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Buddha Scenic Area, constitutes a Natural and Cultural World Heritage site due to the striking scenic beauty, and its exceptional spiritual and cultural significance in Chinese Buddhism (http://whc.unesco.org/en/list/779). In addition, the high biodiversity highlights its special significance to conservation and science (Zhao and Chen 1980). For amphibians, increasing attention has been paid to this region in the past several decades. Liu (1950) had conducted field surveys since 1938, and Fei et al.
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(1976) roughly delineated the elevational distributions for 32 species. However, there were no scientific reports concerning amphibians on Mount Emei for nearly 40 years after these early studies, except for some scattered sightings and samplings. By recording 24 species, Zhao et al. (2018) recently documented the idiosyncratic contributions of individual species to the taxonomic, functional, and phylogenetic diversity on Mount Emel. While these studies presented different facets of diversity, efforts to provide acomprehensive inventory by integrating amphibian species diversity, distribution, and threat status on Mount Emei have remained severely limited.
This study aims to summarize and update data on amphibian species richness on Mount Emei, and also to delineate the distribution and threat status of each species based on extensive field expeditions, supplemented with data from the literature (Fei et al. 1976; Liu 1950; Zhao et al. 2018) and specimen records in the Herpetological Museum, Chengdu Institute of Biology (CIB), Chinese Academy of Sciences (CAS). This study will be helpful in the development of effective conservation strategies for the amphibians on Mount Emei and the surrounding areas.
Materials and Methods Study Area
Mount Emei, a mountain in southwestern China which is known worldwide, was formed on the southwestern edge of Sichuan Basin, China, and dates from the late Cretaceous Period around 70 million years ago (Zhao and Chen 1980). From the base at about 500 m asl, the mountain rises to an altitude of 3,099 m (Fig. 1B). It is made up of deep canyons and narrow gorges (Tang 2006), which results in a variety of attractive landscapes and complex environments to support exceptionally rich flora and fauna (Li and Shi 2007; Zhao and Chen 1980). Mount Emei is characterized by a subtropical monsoon climate. The annual average temperature drops from 17 °C to 3 °C with the increasing elevation. The rainfall is abundant and concentrated during May—September, without a dry season (Tang 2006), and the highest rainfall occurs in the middle and high mountain areas (L1 1990).
The parent rocks in this region mainly include shale, dolomite, limestone, basalt, sandstone, and mudstone (Zhao and Chen 1980); and the following natural vertical soil zones have been described: yellow soil and mountain yellow soil sandwich a purple soil zone (below 1,800 m), mountain yellow-brown soil zone (1,800—2,200 m), mountain dark brown soil zone (2,200—2,600 m), and podzolic soil and meadow soil zone (above 2,600 m) [Li 1990; Tang 2006]. Additionally, Mount Emei is situated at the junction between the tropical and temperate zonation types in eastern Asia (Tang and Ohsawa 1997). There are three major vegetation types along the elevational gradient (from low to high): evergreen broad-
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leaved forest, evergreen deciduous broad-leaved mixed forest, and coniferous forest (Li and Shi 2007; Tang and Ohsawa 1997) [Fig. 1C—E].
Species Data
The field surveys included 23 line transects and three sampling points along the elevational gradient to comprehensively investigate the amphibian species composition on Mount Emei during the breeding seasons in 2017 and 2018 (Fig. 1B; Appendix 1). During the field surveys, line transects and sampling points were mainly placed near water resources according to habitat conditions, and locations were recorded by a global positioning system (GPS) app (Shenzhen 2bulu Information Technology Company). Observers (at least two persons) intensively searched for amphibians with an electric torch and searched systematically at a relatively steady pace (about 2.0 km h') at night (1900-2400 h), with the locations of observed individuals being recorded by the GPS.
Complementary information was also collected from the literature (Fei et al. 1976; Liu 1950; Zhao et al. 2018), with useful information extracted on the taxonomy, Species composition, and elevational distribution of amphibians. Species data were also supplemented with records from museum specimens in the CIB/CAS. The preserved specimen and recorded information were carefully authenticated and crosschecked, and records possibly representing missing species detections and/ or misidentifications during sampling or secondary information compilation were removed. In total, there were 35 amphibian species scientifically recorded, with available elevation information for 34 of the species (all except Amolops granulosus).
Data Compilation and Analysis
Species nomenclature followed Amphibian Species of the World (Frost 2019). Referring to both the IUCN Red List (IUCN 2018) and the China Biodiversity Red List (MEP and CAS 2015), the threat status levels for each species were compared at the global and national scales. A database was generated with the species components, elevational distribution data (minimal and maximal elevations of occurrence), and threat status of each species.
The overall elevational range spanning 500-3,099 m was divided into 200 m band widths, and areas with elevation ranges between 500—1,299 m were defined as low elevations, ranges between 1,300—2,099 m as middle elevations, and ranges between 2,100-3,099 m as high elevations. For each species, the elevational distribution was assumed to cover a continuous range between the minimum and maximum documented elevations (Hu et al. 2011; Rahbek 1997). For example, a species with recorded elevation limits between 1,235 and 1,450 m can be classified into both the 1,100-—1,299 m and 1,300—
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1,499 m bands. Species richness was calculated from the total (cumulative) number in each band and each species’ threat status was assessed for the different bands. In addition, three polynomial regressions (richness as a function of elevation, elevation’, and elevation*) were used to investigate the richness-elevation relationships for total species and threatened species (at both global and national scales) based on the smallest corrected Akaike information criterion (AICc) value.
Next, the overall range size (i.e., elevational range covering the whole distribution range of a species) was collected from the literature (Fei et al. 2006, 2009a,b, 2012) and the online database (Amphibian Species of the World, Frost 2019). Local elevational range size (maximal minus minimal elevation) observed on Mount Emei was plotted and compared with the overall range size for each species. The elevational range size values below the median value (1.e., 1,300 m) were considered “small,” and they were considered “large” for those that were not less than the median.
Results
The 35 species belonged to 22 genera and nine families. Of special note, Mount Emei was the type locality of 14 species, including one endemic species (Rana chevronta, Table 1). At the family level, Megophryidae and Ranidae were the two most abundant families (each with 11 species) and they contributed approximately 63% of all amphibian species on this mountain; followed by Rhacophoridae (four species); Microhylidae, Dicroglossidae, and Hynobiidae (each with two species): and the other three families (Bufonidae, Hylidae, and Cryptobranchidae) were each represented by a single species (Table 1). According to the IUCN Red List, 13 of the 35 species were categorized as threatened, including two Critically Endangered (CR), five Endangered (EN), three Vulnerable (VU), and three Near Threatened (NT) species; while according to the China Biodiversity Red List, 16 of the 35 species were categorized as threatened, including one CR, three EN, nine VU, and three NT species (Table 1).
Along the elevational gradients, a cubic relationship was Statistically favored over either a quadratic or linear relationship for the total species richness, while a quadratic relationship was favored over cubic or linear for the threatened species richness at the two scales (Fig. 2; Table 2). Both species richness and threatened species richness showed mid-elevation peak patterns (Fig. 2). Low and middle elevations (500—2,099 m) were found to harbor a majority of species with a maximum richness at the two elevational bands of 700-899 m and 1,500-1,699 m (Fig. 2). There was a sharp decrease between 1,900-— 2,099 m and 2,100—2,299 m, while species richness changed only slightly for elevations above 2,100 m (Fig. 2). Similar patterns were found for the threatened species, with a maximum in the band at 1,700—1,899 m (Fig. 2:
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A 204 DD LC “ ZZ NT VU 164 faa) EN Mg cr wa & i total species = 124 2 threatend species g ” “i 44 Yi, Y, | 0 B 20 wn 16 é S a = a 12 é te) vo n 8 4 ial oo wo oo To oe 0 Geee} EE ESR eer
600 800 1,000 1,200 1,400 1,600 1,800 2,000 2,200 2,400 2,600 2,800 3,000
Elevation (m) Fig. 2. The numbers of total and threatened species (bars) and elevational patterns of species richness (curves). Regression lines show total species richness (black) and threatened species richness (red) based on the polynomial regression models, with threatened status counts referring to the IUCN Red List (A) and the China Biodiversity Red List (B).
Table 1). Referring to the IUCN Red List, 12 threatened Species occurred in low and middle elevations, while three threatened species occurred in high elevations (Fig. 2A; Table 1); referring to the China Biodiversity Red List, 14 threatened species were in low and middle elevations, and four threatened species were in high elevations (Fig. 2B; Table 1).
Although the upper elevational limits of three species (i.e., Scutiger chintingensis, Batrachuperus pinchonii, and Rhacophorus dugritei) were higher than 3,000 m, and four species (1.e., Xenophrys omeimontis, X. minor, Oreolalax omeimontis, and O. major) were found to exceed the overall range size, 26 of the species have a small range size (<< 1,300 m) on Mount Emei (Fig. 3; Table 1). In total, ten of the threatened species have a small range size on Mount Emei (Table 1). Notably, the Critically Endangered species (Andrias davidianus) and the endemic (R. chevronta) were each restricted to an extremely narrow range. The local range size was relatively wider than the overall range size for some of the threatened species (e.g., B. londongensis, R. chevronta, O. omeimontis), but the range size of these species were reasonably small (Fig. 3; Table 1).
Discussion
Knowing where the individual species occur and identifying which ones are threatened and_ their
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Table 1. Amphibian species on Mount Emei, China, with their elevational distribution (minimal and maximal elevations of occurrence) and threat status.
Lower limit Upper limit
Species IUCN Red List China Red List (m) (m) I. Hynobiidae Batrachuperus londongensis' EN VU 1,200 1,400 Batrachuperus pinchonii VU VU 1,400 3,050 II. Cryptobranchidae Andrias davidianus CR CR — 500 III. Megophryidae Oreolalax major' VU VU 1,500 2,000 Oreolalax schmidti' NT NT 1,580 2,340 Oreolalax multipunctatus' VU VU 1,800 1,920 Oreolalax omeimontis' EN VU 740 2,060 Oreolalax popei Le VU 950 2,010 Scutiger chintingensis' EN EN 2,890 3,050 Leptobrachium boringii' EN EN 650 1,650 Leptobrachella oshanensis' Le Le 760 1,810 Atympanophrys shapingensis 1S LC = 2,120 Xenophrys omeimontis' NT VU 610 1,920 Xenophrys minor LC LC 680 1,600 IV. Bufonidae Bufo gargarizans LC Le 500 1,910 V. Hylidae Hyla annectans LC LC 1,200 1,298 VI. Ranidae Rana chevronta'* CR EN 1,750 1,850 Rana omeimontis' |i LC 500 2,080 Pelophylax nigromaculatus NT NT 500 1,300 Boulengerana guentheri LC LC — 500 Nidirana daunchina!' EC LC 750 1,660 Odorrana graminea DD Le 530 710 Odorrana schmackeri LC LG 530 790 Odorrana margaretae LC LC 500 1,810 Amolops chunganensis LE Le 720 1,600 Amolops granulosus 1S NT — — Amolops mantzorum Le Le 800 1,660 VII. Dicroglossidae Quasipaa boulengeri EN VU 500 1,900 Fejervarya multistriata DD EC 500 850 VUI. Rhacophoridae Polypedates megacephalus LC LC 740 1,600 Rhacophorus chenfui' ne EC 800 1,660 Rhacophorus omeimontis' Le Le 680 1,810 Rhacophorus dugritei Le VU 1,520 3,050 IX. Microhylidae Microhyla fissipes LC LC 500 530 Kaloula rugifera BS LC 700 900
'Species type locality is Mount Emei; "endemic species on Mount Emei. The threat status abbreviations refer to the [UCN Red List of Threatened Species and the China Biodiversity Red List: Data Deficient (DD), Least Concern (LC), Near Threatened (NT), Vulnerable (VU), Endangered (EN), and Critically Endangered (CR).
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Table 2. Results of polynomial regression models for assessing the total species and threatened species patterns along the elevational
gradient.
Polynomial regressions Total species richness
First-order R? OOF AICc 78.63
Second-order R? 0.81*** AICc 79.90
Third-order R? 0.95*** AICc 68.64
Threatened species (IUCN)
Threatened species (China)
0.22 0:39* 67.69 61.27 0.57* 0.62** 64.20 59.47 0.66* 0.70** 66.66 61.88
Tested effects were significant at: * P < 0.05; ** P< 0.01; *** P< 0.001. Bold numbers indicate the models which best accounted for variation in
the richness along the elevation gradient based on the smallest AICc value.
conservation status are critical for optimizing the conservation of species and communities in a given region. This study documented the species component, distribution, and threat status of amphibians along a 2,600 m elevational gradient on Mount Emei in China. Although Mount Emei is a Natural and Cultural World Heritage site with high richness in amphibians, their threat status is really severe overall, particularly since a majority of the species possess relatively narrow local range sizes. Taken together, these results can contribute to a better understanding and more effective conservation of the amphibian diversity on this mountain.
The higher amphibian diversity on Mount Emei documented in this study, relative to the published records in this region (Fei et al. 1976; Liu 1950; Zhao et al. 2018) and the neighboring regions (e.g., Mount Gongga and Mount Erlang; Xie et al. 2007), underlines its great significance in conservation and scientific studies. Megophryidae and Ranidae are the two most species- rich families, accounting for 63% of all species in the region (Table 1); and the extremely adaptable capacities and enhanced environmental tolerances of some species may contribute to the dominance of these two families (Fei et al., 2009a,b; Wells 2007). At the species level, the endemic species (R. chevronta) with a narrowly specified range is actually rare and threatened, and it should be urgently targeted for conservation (Hu et al. 2012). Although the data in this study were obtained from extensive field surveys combined with comprehensive data collection, the results provided here may be missing certain information. Anecdotal observations of Odorrana hejiangensis on Mount Emei have been reported (K. Jiang, pers. comm.), but they were not verified from any scientific publication or field expedition. Therefore, further surveys in the region are still necessary.
Elevation is often regarded as a surrogate for temperature and moisture, and is widely used to investigate distributional patterns of species richness in mountainous regions (Khatiwada et al. 2019; Peters et al. 2016; Rahbek 1995). Variations of climatic variables, land surface area, and geography along elevational gradients are among the hypothesized causal factors influencing species composition and _ distribution (Lomolino 2001). Amphibians, which tend to have
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complex life histories and relatively low mobility, are strongly restricted by the external environment (Hof et al. 2011; Wake and Vredenburg 2008). Climatic factors (mainly temperature and precipitation) are widely recognized as the key determinants that influence various aspects of amphibian biology, such as physiology, behavior, and ecological performance (Wells 2007). A habitat with a lower temperature and higher elevation is prone to support more species (Navas et al. 2013), and more abundant precipitation can support higher species richness and abundance (Rahbek 2005; Wells 2007). Under the influences of climatic, edaphic, and vegetation zones (Tang 2006; Tang and Ohsawa 1997), the vertical distribution pattern of amphibians on Mount Emeti is obvious (Fig. 2). Indeed, low and middle elevations with higher temperatures (Tang 2006) and rainfall (Li 1990) are so suitable for amphibians that they support more species (Fig. 2). Additionally, it is well known that conserving a large number of species can provide the opportunity to conserve rare species and other undetected species (Aynekulu et al. 2012). That is, more conservation investment in the areas below 2,100 m on this mountain is needed because most of the amphibians and threatened species are restricted to the elevations below 2,100 m (Fig. 2). Even so, several species in high elevations (2,100-—3,099 m) should also attract a great deal of attention because they can be considered as the indicators of environmental adaptation in the high elevations.
Range size is a critical factor that reflects the local assemblage structure (Gaston 1996) and a species’ environmental niche (Pearson et al. 2006). It is recognized that species with different range sizes should be conserved with different strategies (Chen et al. 2019; Di Marco and Santini 2015). A small range size may be one of the strongest predictors of extinction risk (Chen et al. 2019; Rosenzweig 1995). In this study, some species have a larger local range size compared with the overall elevational range size but most species have a smaller local range size, especially among the threatened species (Fig. 3; Table 1). For instance, the range size is extremely narrow for A. davidianus (CR). Therefore, conservation priority should be given to these species with small range sizes (Chen et al. 2019). Range size can be influenced
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Rhacophorus omeimontis Rhacophorus dugritei Rhacophorus chenfui
Polypedates megacephalus Rana omeimontis
Rana chevronta Pelophylax nigromaculatus Odorrana schmackeri Odorrana margaretae Odorrana graminea Boulengerana guentheri Nidirana daunchina Amolops mantzorum Amolops chunganensis Microhyla fissipes Kaloula rugifera Xenophrys omeimontis Xenophrys minor
Scutiger chintingensis Oreolalax schmidti Oreolalax popei
Oreolalax omeimontis Oreolalax multipunctatus Oreolalax major Leptobrachella oshanensis Leptobrachium boringii Atympanophrys shapingensis Andrias davidianus Batrachuperus pinchonii Batrachuperus londongensis Ayla annectans
Quasipaa boulengeri Fejervarya multistriata Bufo gargarizans
500
1,000
Re sa Re _ J - = _] iy |Re=—______ |}————.__- P| =—_ HK—__+——__ —————— ooo |I————_ ] HK—_—_+—_——— + =—
[—_™—_+ =
1,500 2,000 2,500 3,000 3,500 4,000
Elevation (m)
Fig. 3. Local and overall elevational ranges for each amphibian species. For each species, the local elevational range is the maximum minus minimum elevation on Mount Emei (gray box or vertical line), and the overall elevational range size is the published elevational range covering the whole distribution range (the horizontal line).
by environmental modification, as well as life-history and evolutionary traits (Gaston 1996). For example, increasing human activities and climate changes may lead to a range shift along the elevation (Chen et al. 2009; Kusrini et al. 2017). As a famous tourist attraction, the tourist season on Mount Emei overlaps with the breeding season of most amphibians, resulting in changes of the species’ range size (Fei et al. 2009a,b; Liu and Yang
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2012). On the other hand, individual intrinsic traits, such as dispersal abilities, habitat selection, and environmental tolerance, may indirectly contribute to a range shift under environmental changes (Fei et al. 2006, 2009a,b; Gaston 1996). For example, tadpoles and some stream- dwelling adults may be flushed downstream in running water, leading to a lower minimal elevation. Of course, one caveat must be applied to the results. Although
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this survey illustrated that a species’ range size may be related to its threat status, it did not examine the extent of that correlation based on any statistical support. There is a need to further explore the influences of intrinsic traits (e.g., range size, body size, and clutch size) on extinction risk with more detailed data.
Amphibians are a major group that is currently at risk globally (Jiang et al. 2016; Wake and Vredenburg 2008), with declines which far exceed those of other vertebrate taxa (Hoffmann et al. 2010). Accumulating evidence indicates that amphibians are threatened by anthropogenic land-use changes, fatal chytridiomycosis, climatic changes, and over-exploitation (Blaustein and Kiesecker 2002; Hof et al. 2011). Mount Emei suffers from intense human disturbance (e.g., cultivation and tourism), and nearly one-third of the amphibian species are severely at risk as indicated by their currently threatened status (Table 1). As such, urgent conservation actions are necessary for amphibians. Although biodiversity conservation and environmental management awareness among_ local governments and the public have been strengthened, the conflict between conservation and socioeconomic development continues to make biodiversity conservation exceptionally difficult to achieve. In this context, understanding how species respond to human-disturbances and survive in the human-dominated landscape 1s critical to the conservation of amphibians in mountain systems. This study can be helpful for scientifically-based policy making and for implementing the regulatory measures to mitigate the potential disturbances on biodiversity caused by mass-tourism.
Conclusion
In summary, this study presents data on the species richness, distribution, and threat status for 35 amphibian species in a tourist attraction, Mount Emei in China, which 1s a site of special significance to conservation and to science. The results highlight the urgent need to manage and preserve the amphibians, especially the threatened species, and will be helpful in assisting with sustainable management and the development of effective conservation strategies. These findings can also provide a basis for further ecological studies, such as exploring intraspecific and/or interspecific responses to biotic and abiotic influences (Hu et al. 2019; Huang et al. 2020; Wang et al. 2019), not only for the focal mountain but also for other similar regions or high-profile areas of concern.
Acknowledgements.—We would like to thank Liang Fei and Changyuan Ye for their valuable suggestions and guidance in the identification of species and obtaining key information. We thank Tian Zhao, Chunlin Zhao, Shengchao Shi, and Bin Wang for their help in the fieldwork. Many thanks to the Herpetological Museum of Chengdu Institute of Biology, Chinese Academy of Sciences, for the support of specimens. This study was
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supported by National Key Research and Development Plan (2016YFC0503303), the National Natural Science Foundation of China (31770568, 31572290), the ‘Light of West China’ Program of the Chinese Academy of Sciences, and China Biodiversity Observation Networks (Sino BON).
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Xiaoyi Wang is a Ph.D. candidate at Chengdu Institute of Biology, Chinese Academy of Sciences, whose work focuses on species diversity and community assembly mechanisms along environmental gradients, responses of traits to environmental changes, and the conservation of endangered species. Specifically, she aims to link biodiversity conservation with multidimensional insights, such as species function in the ecosystem, evolution and adaptation, to assess how biodiversity responds to environmental changes.
Shengnan Yang entered the laboratory at Chengdu Institute of Biology, Chinese Academy of Sciences and began her amphibian and reptile studies during her undergraduate work. She is interested in the ecology and conservation of amphibians and reptiles. Her current research topics include the impact of habitat transformation on these groups and the potential adaptability and plasticity of species.
Chunpeng Guo is a postgraduate student at Chengdu Institute of Biology, Chinese Academy of Sciences. His research interests include the road ecology, conservation biology, and natural history of reptiles and amphibians. His current studies focus on assessing the impacts of roads on amphibian and reptile assemblages
Ke Tang is a postgraduate student at Chengdu Institute of Biology, Chinese Academy of Sciences. He studies the population ecology of amphibians and reptiles, and his current research focuses on the effects of environmental heterogeneity on amphibians and reptiles in the Three-River-Source (Sanjiangyuan) National
Jianping Jiang is a herpetologist at Chengdu Institute of Biology, Chinese Academy of Sciences, with more than 25 years of professional wildlife and research experience. Currently, he is focusing on the taxonomy, systematics, ecology, evolution, and conservation of reptiles and amphibians.
Junhua Hu is a full professor at Chengdu Institute of Biology, Chinese Academy of Sciences. His research focuses on animal ecology and the conservation of endangered species in a changing world.
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Appendix. Locations of sampling sites and the numbers of line transects (N) at each site along the elevational gradient on Mount Emei, China.
Sampling site Longitude (°E) Latitude (°N) Elevation (m) N
Line Huangwan Village 103.43 29.58 500 e
Hranisects Baoguo Temple 103.44 29,57 530 2
Lianghekou 103.41 29.59 650 l
Qingyin Pavilion 103.39 29.57 730 1
Shenshui Pavilion 103.41 29.56 800 2
Baiguo Village 103.34 29.43 860 1
Chadi Village 103.36 29.59 914 1
Weigan Village 103.31 29.60 1,100 1
Longdong Village 103.28 29.58 1,250 2
Qiliping 103.25 29,57 1,280 1
Linggongli 103.29 2958 1,340 2
Kuhaoping 103.27 29.45 1,470 2
Changshou Bridge 103.35 29.56 1,540 1
Jinchuan Village 103.24 29.44 1,560 2
Longqiaogou 103.35 29.55 1,900 1
Jingding 103.33 29.52 3,050 1 Sampling Shouxing Bridge 103.37 29.55 1,280 points Shuangshuijing 103.32 29.55 2,230 Leidongping 103.33 29.55 2,433
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Official journal website: amphibian-reptile-conservation.org
Amphibian & Reptile Conservation 14(3) [General Section]: 57—61 (e253).
New record of Adelphicos daryi (Serpentes: Dipsadidae) after 19 years, and additional record of Ptychohyla euthysanota (Anura: Hylidae) in Guatemala 12*J. Renato Morales-Mérida and *Fred Muller ‘Escuela de Biologia, Universidad de San Carlos de Guatemala, Ciudad Universitaria, zona 12, Guatemala, GUATEMALA *Red Mesoamericana y del Caribe para la Conservacion de Anfibios y Reptiles (Red MesoHerp Network, https://redmesoherp.wixsite.com/red-mesoherp) *26 Avenida
32-56 Hacienda Real, Zona 16, Guatemala City, GUATEMALA
Abstract.—New records of the Endangered Adelphicos daryi (Serpentes: Dipsadidae) and Near Threatened Ptychohyla euthysanota (Anura: Hylidae) are reported for the Department of Guatemala, Guatemala City. Brief
comments on local conservation concerns for these two species are presented.
Keywords. Amphibia; Central America; Endangered; new records; Reptilia
Citation: Morales-Mérida J, Muller F. 2020. New record of Adelphicos daryi (Serpentes: Dipsadidae) after 19 years, and additional record of Ptychohyla euthysanota (Anura: Hylidae) in Guatemala. Amphibian & Reptile Conservation 14(3) [General Section]: 57-61 (e253).
Copyright: © 2020 Morales-Mérida and Muller. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribution 4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. The official and authorized publication credit sources, which will be duly enforced, are as