Herpetology Notes, volume 14: 27-30 (2021) (published online on 08 January 2021)

Natural history note of the endangered psammophilous Eurolophosaurus amathites (: ) from Caatinga domain,

Maria Aldenise Xavier1,2,*, Tainara Lima da Silva2,3, Gabriel Deyvison dos Santos Carvalho2, and Eduardo José dos Reis Dias1,2,3

The Eurolophosaurus genus is a monophyletic 1984, 1986, 1996; Leal et al., 2003), such as E. group, which previously were part of the amathites. However, the progressive anthropisation of nanuzae group (Frost et al., 2001; Passoni et al., the natural habitats of this rich biome (e.g. trampling, 2008). It is composed of three : E. amathites deforestation, agriculture and sand exploration) results (Rodrigues, 1984), E. divaricatus (Rodrigues, 1986) in a continuous loss of habitat quality for such species and E. nanuzae (Rodrigues, 1981) (Passoni et al., 2008). (Leal et al., 2003; Van Sluys, 2010; Brazil, 2018). Many Eurolophosaurus amathites (Fig. 1) is an endemic of these species can disappear even before they have species of Caatinga domain, occurs in sand dunes and been studied, so it is necessary to make efforts to reduce is restricted to the right bank of the São Francisco the lack of knowledge about the biological diversity of River (Fig. 2) (Rodrigues, 1996; Passoni et al., 2008). this region. Eurolophosaurus amathites was described It is a diurnal and psammophilous species, with a three decades ago, but little is known about this species, highly restricted geographic distribution, from the especially its biology and ecology. The goal of this study municipalities of Santo Inácio, Gameleira do Assuruá was to describe some aspects of the natural history of and Lagoa de Itaparica (Rodrigues, 1984, 1996; Passoni the E. amathites lizard. et al., 2008). According to the International Union for The capture of specimens was done in region Caatinga, Conservation Nature (IUCN) this species presents data in Serra de Santo Inácio (42.73719°W, 11.12089°S; deficient (DD), however it has been categorised as Datum WGS 84; 364 m a.s.l.), municipality of Gentio endangered (EN) [EN B1ab (iii)] in Brazilian red list, do Ouro, State of Bahia, Brazil (Fig. 2). This region is due to the progressive anthropisation in their natural characterised for a short period of rains (about 687 mm/ habitats causing a destabilisation of the dunes and a annual – http://pt.climate-data.org/) and predominant continuous decline at habitat quality (Brazil, 2018). larges rock outcrops and white sandy soils, result The Caatinga refuges some endemic species, including species strictly adapted to life in sandy soils (Rodrigues,

1 Programa de Pós-Graduação em Biodiversidade e Evolução, Instituto de Biologia, Universidade Federal da Bahia, Campus de Ondina, Rua Barão de Jeremoabo, 147 - CEP: 40170-290 - Salvador, Brazil. 2 Laboratório de Biologia e Ecologia de Vertebrados, Departamento de Biociências, Universidade Federal de Sergipe, Campus Prof. Alberto Carvalho, Av. Vereador Olímpio Grande, s/n - CEP: 49500-000 - Itabaiana, Brazil. 3 Programa de Pós-Graduação em Ciências Naturais, Universidade Federal de Sergipe, Campus Prof. Alberto Carvalho, Av. Vereador Olímpio Grande, s/n - CEP: 49500- 000 - Itabaiana, Brazil. * Corresponding author. E-mail: [email protected] Figure 1. Specimen of Eurolophosaurus amathites at Caatinga © 2020 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. domain of Santo Inácio, in northeastern Brazil. 28 Maria Aldenise Xavier������� et al. from rock intemperism, with herbaceous and arbustive We collected four individuals (LABEVL787, vegetation and cactaceous (Arias et al., 2011). LABEVL788, LABEVL789, LABEVL803) of E. We collected the by stunning them with amathites (one male with 64.1 mm of snout-vent elastic bands in June and November 2016, and April length (SVL) and three females with SLV of 52.9 mm, 2017, euthanised with a lethal dose of lidocaine 50.3 mm and 51.6 mm). The diet of this species was hydrochloride®, and next measured the snout-vent length composed of 124 items, we were able to identify eight (SVL) using a digital calliper (precision of to 0.01 mm). prey categories that included arthropods and material The individuals of E. amathites were dissected and their plant. The items most representative in terms of number stomach contents were analysed. The length and width were Hymenoptera “” (86.3%), leaf (5.6%) and of each item were measured using a digital calliper Blattodea “” (3.2%), in terms of volume were (precision of to 0.01 mm), to estimate volume (mm3) larvae of Lepidoptera (42.5%), Hymenoptera “ants” using the formula ovoid-spheroid (Dunham, 1983): V = (41.8%) and leaf (4.8%), and the most frequent were 4/3π (L/2) (W/2)2, where: “L” is the length and “W” is Hymenoptera “ants” (100%) (Table 1). the width of each prey. The diet of Eurolophosaurus amathites was composed We measured the length and width of male’s testes of arthropods (termites, ants and larvae) and plant using a digital calliper (precision of to 0.01 mm) and material, indicating that this species is possibly a estimated volume using the ellipsoid formula v = π. l. generalist predator, similar to other species of the family (w²)/6, where v = gonads volume, l = gonads length and Tropiduridae (Ribeiro and Freire, 2011; Gomides et w = gonads width (Ribeiro et al., 2010). Left testis was al., 2013; Siqueira et al., 2013; Alcantara et al., 2018). removed, fixed in 10% formalin, dehydrated in a graded However, his diet was predominantly composed of series of ethanol, cleared in xylol, embedded in paraffin, plant material and ants, similar to other tropidurids, sectioned at 5 µm, mounted on slides and stained with such as Tropidurus psammonastes and E. divaricatus haematoxilin-eosin staining technique. The clutch size (Rocha and Rodrigues, 2005). The consumption of was estimated by the number of vitellogenic follicles. plant material (e.g. flowers, leaves, fruits and seeds) The lizards were deposited in the herpetological and larvae may be associated with its high energy collection of the Laboratório de Biologia e Ecologia and nutrient levels and water contents, especially dos Vertebrados (LABEV), Universidade Federal de in semiarid environments, such as Caatinga, where Sergipe. resources may otherwise be limited (Fialho et al., 2000; Ribeiro et al., 2008; Sales et al., 2012; Passos et al., 2013; Xavier et al., 2019). In addition, the consumption of plant material demonstrates the role of seed dispersal, especially in dry environments (Ribeiro et al., 2008; Passos et al., 2013; Xavier and Dias, 2015, 2017). The myrmecophagy recorded in E. amathites may be due to the plesiomorphic features of Tropidurinae (Frost et al., 2001; Rocha and Rodrigues, 2005). The microhabitat used by this species was on leaf litter under shrub and vegetation height less than 2.0 m. The specimens were collected between 10:00 and 16:00 hours. The microhabitat used by E. amathites was similar to that reported for the psammophilous species T. hygomi (Lima-Silva et al., 2019). The E. amathites male was not in the reproductive mode; the volume of the testicles was 0.63 mm³ (right) and 0.91 mm³ (left) without spermatozoa. The smallest reproductive female in this study was 50.3 mm captured in November. Three reproductive females had each two Figure 2. Sampling locality in dune fields in the lower-mid vitellogenic follicles, which is similar to what is known São Francisco River valley at Santo Inácio, municipality of for other tropidurid species, such as E. nanuzae (Galdino Gentio do Ouro, Bahia State, Brazil. SF River: São Francisco et al., 2003; Galdino and Van Sluys, 2011), T. torquatus River. (Kiefer et al., 2008) and T. hygomi (Lima, 2016). Natural history note of the endangered Eurolophosaurus amathites3 , Brazil Table 1. Number (N), volume (V, in mm ) and frequency (F) of each food item in the 29 diet of Eurolophosaurus amathites (N = 4) in Caatinga domain of Santo Inácio, 3 Table 1. Numbermunicipality (N), volume (V, of inGentio mm ) and do frequency Ouro in (F)Bahia of each State, food Brazil. item in thePercentage diet of Eurolophosaurus values (%) inamathites (N = 4) in Caatinga domainbrackets. of Santo Inácio, municipality of Gentio do Ouro in Bahia State, Brazil. Percentage values (%) in brackets.

Prey type N (%) V (%) F (%) ARTHROPODA Insecta Hymenoptera (Ants) 107(86.3) 21(41.8) 4(100.0) Hemiptera 2(1.6) 1.8(3.6) 1(25.0) Coleoptera 1(0.8) 0.1(0.2) 1(25.0) Blattodea (Termites) 4(3.2) 2(4.0) 1(25.0) Lepidoptera (Unidentified larvae) 1(0.8) 21.3(42.5) 1(25.0) Arachnida Araneae 2(1.6) 0.2(0.4) 2(50.0) Arthropoda Remains - 1.4(2.8) 1(25.0) PLANTS Leaves 7(5.6) 2.4(4.8) 2(50.0) Total 124(100.0) 50.2(100.0) 4(100.0)

The clutch size among is positively correlated References with the female body size (e.g. Vitt, 1981; Wiederhecker Alcantara, E.P., Ferreira-Silva, C., Sousa, J.G.G., Ávila, R.W., et al., 2002; Du et al., 2005; Kiefer et al., 2008; Galdino Morais, D.H. (2018): Ecology and of the lizard and Van Sluys, 2011). In E. nanuzae, for example, the Tropidurus jaguaribanus (Squamata: Tropiduridae) from clutch size does not have a fixed number (normally two northeastern Brazil. Phyllomedusa 17: 195–210. eggs), but larger (older) females are able to produce Arias, F., Carvalho, C.M., Rodrigues, M.T., Zaher, H. (2011): Two larger clutches (three eggs) (Galdino and Van Sluys, new species of Cnemidophorus (Squamata: Teiidae) of the C. 2011). In addition, lizard species with psammophily ocellifer group, from Bahia, Brazil. Zootaxa 3022: 1–21. habits tend to produce smaller clutches compared to Brazil. (2018): Livro Vermelho da Fauna Brasileira Ameaçada de Extinção. Instituto Chico Mendes de Conservação da terrestrial and saxicolous species (Dunham et al., 1988), Biodiversidade. Available at: http://www.icmbio.gov.br/portal/ such as T. torquatus in restinga environments (Kiefer et images/stories/comunicacao/publicacoes/publicacoes-diversas/ al., 2008). Reduced clutch size favours sand movement livro_vermelho_2018_vol4.pdf. Accessed on 1 March 2020. and the rapid predator escape (Shine, 1980). In this Du, W., Ji, X., Shine, R. (2005): Does body-volume constrain context, we believe that E. amathites might have the reproductive output in lizards? Biology Letters 1: 98–100. same biological pattern. Dunham, A.E. (1983): Realized niche overlap, resource abundance This study brought important information about the and intensity of interspecific competition in lizard ecology. In: natural history of E. amathites. We hope that these natural Lizards ecology: studies of model organism. R.D. Huey, E.R. histories notes can contribute for more knowledge about Pianka and T.W. Schoener (eds.). Harvard University Press, pp. 261–280. this lizard, because this species is little known and the Dunham, A.E., Miles, D.B., Reznick, D.N. (1988): Life history progressive anthropisation of the Caatinga has led patterns in squamate reptiles. In: Biology of the Reptilia. Grans, to high rates of habitat loss. Therefore, more detailed C., Huey, R.B. (eds.). Alan R. Liss, Inc, New York, pp. 441– studies on the biology and ecology of this species are 522. necessary for an adequate conservation plan. Fialho, R.F., Rocha, C.F.D., Vrcibradic, D. (2000): Feeding ecology of Tropidurus torquatus: Ontogenetic shift in plant Acknowledgements. The Fundação de Amparo à Pesquisa do consumption and seasonal trends in diet. Journal of Herpetology Estado da Bahia (FAPESB) for a graduate fellowship to the first 34: 325–330. author (Process - BOL2531/2016). The samples were authorised Frost, D.R., Rodrigues, M.T., Grant, T., Titus, T.A. (2001): by the Instituto Chico Mendes de Conservação da Biodiversidade Phylogenetics of the lizard genus Tropidurus (Squamata: (SISBio\ICMBio — licence 20788 (nº 8072-1)). We thank D. Tropiduridae: Tropidurinae): direct optimization, descriptive Passos for helpful suggestions. efficiency, and sensitivity analysis of congruence between 30 Maria Aldenise Xavier������� et al.

molecular data and morphology. Molecular phylogenetics and Rodrigues, M.T. (1984): Uma nova espécie brasileira de Tropidurus evolution 21: 352–371. com crista dorsal (Sauria, Iguanidae). Pápeis Avulsos de Galdino, C.A.B., Van Sluys, M. (2011): Clutch size in the small- Zoologia 35: 169–175. sized lizard Eurolophosaurus nanuzae (Tropiduridae): does it Rodrigues, M.T. (1986): Um novo Tropidurus com crista dorsal vary along the geographic distribution of the species? Iheringia do Brasil, com comentários sobre suas relações, distribuição 101: 61–64. e origem (Sauria, Iguanidae). Pápeis Avulsos de Zoologia 36: Galdino, C.A.B., Assis, V.B., Kiefer, M.C., Van Sluys, M. (2003): 171–179. Reproduction and fat body cycle of Eurolophosaurus nanuzae Rodrigues, M.T. (1996): Lizards, snakes, and amphisbaenians from (Sauria; Tropiduridae) from a seasonal montane habitat of the quaternary sand dunes of the middle Rio São Francisco, Southeastern Brazil. Journal of Herpetology 37: 687–694. Bahia, Brazil. Journal of Herpetology 30: 513–523. Gomides, S.C., Ribeiro, L.B., Peters, V.M., Sousa, B.M. (2013): Sales, R.F.D., Ribeiro, L.B., Jorge, J.S., Freire, E.M.X. (2012): Feeding and reproduction ecology of the lizard Tropidurus Feeding habitats and predator-prey size relationships in the torquatus (Squamata: Tropiduridae) in a rock outcrop area in whiptail lizard Cnemidophorus ocellifer (Teiidae) in the semiarid southeastern Brazil. Revista Chilena de Historia Natural 86: region of Brazil. South American Journal of Herpetology 7: 137–151. 149–156. Kiefer, M.C., Van Sluys, M., Rocha, C.F.D. (2008): Clutch and egg Shine, R. (1980): “Costs” of Reproduction in Reptiles. Oecologia size of the tropical lizard Tropidurus torquatus (Tropiduridae) 46: 92–100. along its geographic range in coastal eastern Brazil. Canadian Siqueira, C.C., Kiefer, M.C., Van-Sluys, M., Rocha, C.F.D. (2013): Journal of Zoology 86: 1376–1388. Variation in the diet of the lizard Tropidurus torquatus along its Leal, I.N., Tabarelli, M., Silva, J.M.C. (2003): Ecologia e coastal range in Brazil. Biota Neotropica 13: 93–101. conservação da Caatinga. Ed. Universitária da UFPE – Recife, Van Sluys, M. (2010): Eurolophosaurus amathites. The IUCN pp. 822. Red List of Threatened Species 2010: e.T178588A7576237. Lima, J.O. (2016): Efeito de gradientes ambientais sobre a Available at: https://dx.doi.org/10.2305/IUCN.UK.2010 distribuição espacial, atividade, dieta e reprodução de lagartos 4.RLTS.T178588A7576237.en. Accessed on 02 March 2020. do gênero Tropidurus (Squamata: Tropiduridae) na Serra Vitt, L.J. (1981): Lizard reproduction: habitat specificity and de Itabaiana, Sergipe. Dissertação (Mestrado em Zoologia) constraints on relative clutch mass. The American Naturalist Universidade Federal da Bahia, pp. 64. 117: 506–514. Lima-Silva, T.L., Xavier, M.A., Dias, E.J.R. (2019): Período de Wiederhecker, H.C., Pinto, A.C.S., Colli, G.R. (2002): Reproductive recrutamento e uso de recursos espaciais por Tropidurus hygomi Ecology of Tropidurus torquatus (Squamata: Tropiduridae) in (Sauria: Tropiduridae) emu ma área de ecótono, Nordeste, the Highly Seasonal Cerrado Biome of Central Brazil. Journal Brasil. Oecologia Australis 23: 280–291. of Herpetology 36: 82–91. Passoni, J.C., Benozzati, M.L., Rodrigues, M.T. (2008): Phylogeny, Xavier, M.A., Dias, E.J.R. (2015): First record of the Brazilian species limits, and biogeography of the Brazilian lizards of the restinga lizard Tropidurus hygomi ingesting a fruit of Melocactus genus Eurolophosaurus (Squamata: Tropiduridae) as inferred violaceus (Cactaceae). Herpetology Notes 8: 437–438. from mitochondrial DNA sequences. Molecular Phylogenetics Xavier, M.A., Dias, E.J.R. (2017): Ecology of the endemic and and Evolution 46: 403–414. saxicolous lizard Tropidurus pinima (Rodrigues, 1984) from Passos, D.C., Zanchi, D., de Souza, I.H.B., Gallão, M.I., Borges- Caatinga domain, Brazil. Herpetology Notes 10: 491–492. Nojosa, D.M. (2013): Frugivory of Momordica charantia Xavier, M.A., Lima-Silva, T., Dias, E.J.R. (2019): Habitat use (Cucurbitaceae) by Ameivula ocellifera (Squamata: Teiidae) in a and diet of the endemic lizard Ameivula nigrigula (Squamata: coastal area of northeastern Brazil. Salamandra 49: 234–236. Teiidae) in Caatinga domain, Northeastern Brazil. Journal of Ribeiro, L.B., Freire, E.M.X. (2011): Trophic ecology and foraging Natural History 53: 1787–1797. behavior of Tropidurus hispidus and Tropidurus semitaeniatus (Squamata, Tropiduridae) in a Caatinga area of northeastern Brazil. Iheringia 101: 225–232. Ribeiro, L.B., Gogliath, M., Freire, E.M.X. (2008): Tropidurus semitaeniatus (Squamata: Tropiduridae) as a seed disperser of the plant Commiphora leptophloeos (Burseraceae) in the Caatinga of Northeastern Brazil. Cuadernos de Herpetología 22: 91–94. Ribeiro, L.B., Kolodiuk, M.F., Freire, E.M.X. (2010): Ventral colored patches in Tropidurus semitaeniatus (Squamata, Tropiduridae): sexual dimorphism and association with reproductive cycle. Journal of Herpetology 44: 177–182. Rocha, P.L., Rodrigues, M.T. (2005): Electivities and resource use by an assemblage of lizards endemic to the dunes of the Accepted by Anamarija Žagar São Francisco River, northeastern Brazil. Papéis Avulsos de Zoologia 45: 261–284.