Herpetology Notes, volume 13: 895-901 (2020) (published online on 22 October 2020)

Assemblage of lizards of a forest fragment in southwest Amazon, Brazil

Jailini da Silva Araújo1, Vinicius Guerra2,3,*, Moises Barbosa de Souza1, and Fabiano Corrêa2,4

Abstract. The Amazon rainforest has one of the greatest diversity of lizards in the world, however there are still many subsampled areas, which underestimate the knowledge about species composition regionally. In this study we present the inventory of lizard species at the Catuaba Experimental Farm (CEF), located in the municipality of Senador Guiomard, Brazil. The field work was carried out monthly between February and September 2016. Through active searches, pitfall traps and occasional encounters, we recorded 54 individuals of lizards, distributed into 15 species and four families. The CEF shelter 10.87% of the lizards that occur in the Brazilian Amazon. The species composition of the studied assemblage is similar to those known for nearby areas also located in southwestern Amazon, State of Acre. Inventory studies increase the knowledge about the occurrence and biology of species, serving as a basis for more elaborate ecological studies.

Keywords. Checklist, conservation, distribution, Squamata, species richness, Reptiles

Introduction activities (Tonini et al., 2016). In lizards the greatest risk of extinction occurs mainly for species of larger The Neotropics shelter the greatest species richness body size and those habitat specialists (Böhm et al., in the world, both in vertebrates and plants, and the 2016). In addition to being important components of Amazon is the rainforest with the greatest biodiversity, natural ecosystems, lizards are considered good model being the main source of biological lineages in America organisms in studies of ecology because they are (Antonelli et al., 2018). Currently, the Amazon has relatively easy to be found and captured in the field, undergone an accelerated deforestation, resulting in the they are abundant, and present different strategies of reduction of more than 20% of its natural vegetation life history, distinct ecomorphological patterns and and loss of its biodiversity and ecosystem services (da ecophysiological variation (Pianka and Vitt, 2003; Cruz et al., 2020). Among vertebrates, squamates are Camargo et al., 2010). one of the groups most threatened by anthropogenic There are 276 species of lizards occurring in Brazil (Costa and Bérnils, 2019), of which 50% (138 species) are recorded in the Brazilian Amazon (Ribeiro-Junior and Amaral, 2016a). Despite the high richness of lizards, there are many subsampled areas in the Amazon, 1 Universidade Federal do Acre, Laboratório de Herpetologia, which evidences a great knowledge gap about species Campus Rio Branco, BR 364 km 04, Distrito industrial, CEP composition regionally (Rodrigues, 2005; Ribeiro- 69915-900, Rio Branco, Acre, Brazil. 2 Universidade Federal do Acre, Laboratório de Ictiologia e Junior and Amaral, 2016a). To fill these gaps, many Ecologia Aquática, Campus Rio Branco, BR 364 km 04, checklists have been published in recent years (e.g., Distrito industrial, CEP 69915-900, Rio Branco, Acre, Brazil. França et al., 2017; Pedroso-Santos et al., 2019; Peixoto 3 Instituto Boitatá de Etnobiologia e Conservação da Fauna, et al., 2019; Freitas et al., 2020), but further studies Goiânia, Goiás, Brazil. are needed to improve the information on this group, 4 Programa de Pós-Graduação em Ecologia e Conservação, especially regarding species living in areas that are Universidade Estadual de Mato Grosso, Campus Nova undergoing anthropogenic changes (Rodrigues, 2005; Xavantina, Av. Dr. Renato Figueiro Varella, Caixa postal 08, CEP 78.690-000, Nova Xavantina, MT, Brazil. Mesquita et al. 2017). * Corresponding author. E-mail: The southwest of the Amazon, where is located the [email protected] state of Acre (Brazil), has a great diversity of lizards 896 Jailini da Silva Araújo et al.

(Ávila-Pires et al., 2009; Ribeiro-Junior and Amaral, tropical forest fragment with palm trees and bamboos, 2016a; Freitas et al., 2020). However, since most with an area of 840 ha, surrounding by pasture matrices studies on lizards are carried out in the northwest of (Medeiros et al., 2013). The climate is hot and humid the state (e.g., Bernarde et al., 2011, 2013), there is a with temperatures ranging from 20.3 to 31.4 °C per year need to better understand the composition of species (Duarte, 2006). from other areas. Among the numerous forest fragments Data Collection.—The field work was carried out in the State of Acre, the Catuaba Experimental Farm monthly between February and September 2016, and (CEF) has been undergoing deforestation because land each campaign last from six to seven days, totalising 50 use of farming in the neighbouring area and predatory days of sampling. The study was carried using RAPELD hunting. Given the limited knowledge about the fauna (see Magnusson et al., 2005) with some modifications. composition of lizards in that region, and to fulfil the RAPELD is an acronym for rapid assessments (RAP) current knowledge gaps, we carried out an inventory of combined with long term ecological research (PELD; the species of lizards in CEF. in Portuguese). Along a transect line of 5 km, we established 10 perpendicular transects of 250 meters Materials and methods long and separated at a distance of 500 meters from Study area.—The CEF is a forest fragment of Terra Firme each other (Fig. 1). Within each perpendicular transects forest (up-land) that belongs to the Federal University we performed Active Searches (AS) and install Pitfall of Acre (UFAC) and is located in the municipality of Traps (PFT) (Heyer et al., 1994). Senador Guiomard, State of Acre, Brazil (10°04’S, The active search was performed by one researcher 67°37’W; Figure 1). The CEF is located 27 km away slowly walking in a zigzag pattern along the straight from Rio Branco downtown area (capital of the State line of the transect (Cortés-Suárez and Díaz-Gutiérrez, of Acre) and 1.5 km away from the intersection of the 2013) and actively searching for lizards during Brazilian highways BR 364 and BR 317. Although mornings (08:00–12:00 h), resulting in an average of 20 the original vegetation consisted of mainly dense hours per month, and totalising 160 hours of searching. ombrophylous forest domain, there are patches of open We sampled all types of microhabitats used by lizards

Figure 1. Location of the Catuaba Experimental Farm (CEF), in the municipality of Senador Guiomard, State of Acre, Brazil. Samplings were performed on 10 perpendicular transects of 250 meters long, separated 500 meters from each other and established along a 5 km transect line. Pitfall traps were installed at the end of each perpendicular transect. Assemblage of lizards of a forest fragment in southwest Amazon, Brazil 897 to forage, rest or reproduce (e.g. burrows, fallen logs, Discussion holes and trees). A total of 10 pitfall traps were installed The richness of 15 species recorded in the Catuaba at the end of each perpendicular transect (Fig. 1). Each Experimental Farm represent 10.87% of the lizards pitfall trap consisted of four plastic buckets (100 litre that occur in the Brazilian Amazon (Ribeiro-Junior and each) buried in the ground, arranged in a “Y” form and Amaral 2016a). Considering the number of species, it interconnected by a barrier of plastic canvas of 65 cm is lower than in other studied areas in the southwest high and 10 meters long (Cechin and Martins, 2000). Amazon, namely: Porto Walter, on the Juruá River The pitfall traps were visited daily and remained open (29 spp., Ávila-Pires et al., 2009), Reserva Extrativista from six to seven days per month for eight months, Riozinho da Liberdade (29 spp., Bernarde et al., 2011), totalising 1,200 hours of sampling. We also obtained Forest of the lower Moa River (17 spp., Bernarde et Occasional Encounters (OE), in which we consider all al., 2013), Reserva Extrativista Chico Mendes (19 individuals registered outside the established transects. spp., França et al. 2017), Estação Ecológica Rio Acre The specimens were identified based on taxonomic (24 spp., Freitas et al., 2020). According to Vitt (1996), keys and descriptions available in Ávila-Pires (1995), between 20 and 30 species of lizards could be found Souza (2009), Bernarde et al. (2011, 2013), and Murphy for most studies in Amazonian Terra Firme forests, et al. (2016). The zoological nomenclature adopted except for the Amazon savannahs, meadows and igapó follows Costa and Bérnils (2019). The endemism was forests, which present fewer species. Differences in assessed by recent studies on Amazon lizards (Ribeiro- richness between studies may occur due to the size of Júnior, 2015a, 2015b; Ribeiro-Junior and Amaral, the sampled areas, variety of phytophysiognomies and 2016b; Ribeiro-Junior and Amaral, 2017). Most of sampling efforts employed during fieldwork (Ramalho the collected specimens were identified and released et al., 2014). in the same place where they were captured. Voucher The species composition of CEF is similar to the nearby specimens were collected, anesthetised and killed in areas in the State of Acre (São Jorge I Farm – Miranda et ether chambers, fixed in 10% formalin solution and al., 2014; RESEX Chico Mendes – França et al., 2017; preserved in 70% alcohol (Bernarde et al., 2012). Estação Ecológica Rio Acre – Freitas et al., 2020). The The vouchers were deposited in the herpetological two most abundant species are terrestrial, diurnal, and collection of the Universidade Federal do Acre (see widely distributed, but G. amazonicus is an endemic of supplementary material). Research permission and the Amazon and A. ameiva occur in most biomes of the collection license was granted by the Instituto Chico Brazil (Ribeiro-Júnior and Amaral, 2016a). All seven Mendes de Conservação da Biodiversidade (ICMBio Amazon endemic species recorded were previously nº49304). known to the State of Acre (Ribeiro-Júnior 2015a, 2015b; Ribeiro-Junior and Amaral, 2016b; Ribeiro- Results Junior and Amaral, 2017). Only Cercosaura sp. were We recorded 54 individuals of lizards, distributed into not identified at a specific level because its morphology 15 species and four families (Table 1, Fig. 2). Ameiva was not compatible with other species of the genus ameiva (Linnaeus, 1758) and Chatogekko amazonicus (Ribeiro and Amaral, 2017). (Andersson, 1918) were the most abundant species, Most species in this study were registered through with 16 and 14 individuals, respectively. The species active search. We also observed that species recorded Cercosaura sp., C. argurlus Peters, 1862, C. eigenmanni by one type of methodology were not obtained by (Griffin, 1917), C. ocellata bassleri Wagler, 1830, others, except for the more generalist ones, such as A. Copeoglossum nigropunctatum (Spix, 1825), Dactyloa ameiva and C. amazonicus. Although the active search punctata (Daudin, 1802), D. transversalis (Duméril has been the most efficient for sampling reptiles in other in Duméril and Duméril, 1851), and Tupinambis studies in the Amazon (e.g., Bernarde et al., 2013), the cuzcoensis Murphy et al., 2016, were represented by use of complementary methods increases the chance of only one individual each (Table 1). Seven species of registering a greater number of species (Heyer et al., lizards are endemic to the Amazon Rainforest (Table 1994), especially those with cryptic habits. 1). None of the sampled species are in some degree The low species richness of the CEF may be related to of threat according to both the IUCN (2020) and the the degree of anthropisation and exploitation of the area, ICMBio (2018). in addition the forest fragment is surrounded by a matrix of pastures used for livestock, which may be isolating 898 Jailini da Silva Araújo et al.

Figure 2. Some lizard species recorded in the Catuaba Experimental Farm, State of Acre, Brazil. (A) Gonatodes humeralis, (B) Dactyloa punctata, (C) Norops fuscoauratus, (D) Cersosaura eigeinmanni, (E) Copeoglossum nigropunctatum and (F) Ameiva ameiva. Photos A – E by Jailini Araújo; Photo F by Daniella França.

the populations of some species. Even so, these areas the Amazon (Bernarde et al., 2013). Inventory studies are important for conservation, as they can sustain are important because they increase knowledge about viable populations or even present a composition of the occurrence and biology of species, serve as a basis different species compared to other forest fragments in for more elaborate ecological studies, and to produce Assemblage of lizards of a forest fragment in southwest Amazon, Brazil 899

Table 1. Abundance of the lizard species recorded at the Catuaba Experimental Farm, municipality of Senador Guiomard, State of Acre, Brazil. PFT =Table Pitfall 1 Traps;. Abundance AS = Active of the lizardSearch, species OE = recorded Occasionally at the Encountered.Catuaba Experimental *Amazon Farm, endemic municipality species. ofIn parentheses is the relative percentageSenador for Guiomard, each species. State of Acre, Brazil. PFT = Pitfall Traps; AS = Active Search, OE = Occasionally Encountered. *Amazon endemic species. In parentheses is the relative percentage for each species.

METHOD TOTAL SPECIES PFT AS OE

Sphaerodactylidae Chatogekko amazonicus (Andersson, 1918)* 3 4 7 14 (25.9) Gonatodes hasemani (Griffin, 1917)* 3 3 (5.6)

Gonatodes humeralis (Guichenot, 1855) 3 1 4 (7.4)

Mabuydae Copeoglossum nigropunctatum (Spix, 1825) 1 1 (1.9) Dactyloidae

Dactyloa punctata (Daudin, 1802) 1 1 (1.9)

Dactyloa transversalis (Duméril in Duméril and Duméril, 1851)* 1 1 (1.9)

Norops fuscoauratus (D’Orbigny, 1837 in Duméril and Bibron, 1837) 3 3 (5.6)

Norops tandai (Ávila-Pires, 1995)* 2 2 (3.7)

Gymnophthalmidae

Iphisa elegans elegans (Gray, 1851)* 3 1 4 (7.4)

Cercosaura argulus (Peters, 1862) 1 1 (1.9)

Cercosaura eigenmanni (Griffin, 1917)* 1 1 (1.9)

Cercosaura ocellata bassleri (Wagler, 1830)* 1 1 (1.9)

Cercosaura sp. 1 1 (1.9)

Teiidae

Ameiva ameiva (Linnaeus, 1758) 12 1 3 16 (29.6) Tupinambis cuzcoensis (Murphy et al., 2016) 1 1 (1.9) Number of specimens 33 8 13 54 Richness 12 5 5 15

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Supplementary material Gonatodes hasemani (HERPUFAC #17, 18, 24, 26), Gonatodes humeralis (HERPUFAC #23), Dactyloa punctate (HERPUFAC #35, 63), Dactyloa transversalis (HERPUFAC #213), Norops fuscoauratus (HERPUFAC #11, 29, 55), Norops tandai (HERPUFAC #212, 241, 242, 243), Iphisa elegans (HERPUFAC #207), Cercosaura argula (HERPUFAC #36, 132, 182, 203, 204), Cercosaura eigenmanni (HERPUFAC #41, 92, 152), Cercosaura ocellata (HERPUFAC #27, 43), Cercosaura sp. (HERPUFAC #81, 97), Ameiva ameiva (HERPUFAC #102, 107, 135, 223, 224).

Accepted by Javier Cortés Suárez