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Herpetology Notes, volume 14: 345-348 (2021) (published online on 14 February 2021)

First record of semitaeniatus (: ) ingesting a fruit of the catingicola in northeastern

Tainara Lima da Silva1,*, Gabriel Deyvison dos Santos Carvalho1, Maria Aldenise Xavier1, Jefferson Oliveira Lima1, and Eduardo José dos Reis Dias1

Saurochory is a mutualistic relationship, in which 2017), T. semitaeniatus (Fonseca et al., 2012; Gomes promote seed dispersal (Valido and Olesen, et al., 2013, 2016, 2017) and T. torquatus (Figueira et 2007; Ricklefs, 2010). This process has been well al., 1994). documented for some (Valido et al., Tropidurus semitaeniatus (Spix, 1825) is diurnal and 2003; Rodríguez-Pérez et al., 2005; Valido and Olesen, saxicolous with a generalist diet that includes arthropods 2007, 2019; Casado and Soriano, 2010; Fonseca et al., as well as material (Kolodiuk et al., 2009; Ribeiro 2012; Gomes et al., 2014; Aximoff and Felix, 2017). and Freire, 2011). This species is widely distributed in Under certain ecological conditions, the reproduction northeastern Brazil, occurring in the states of , of some plant species is directly influenced by the role , Ceará, Paraíba, , Piauí, Rio Grande that lizards play, either in dispersal or in the breaking of do Norte and (Rodrigues, 2003; Uetz et al., seed dormancy after passage through a lizard’s digestive 2020). Previous studies on the diet of T. semitaeniatus tract (Traveset and Verdú, 2002; Celedón-Neghme et reported the consumption of Melocactus ernestii al., 2008). (Gomes et al., 2013), M. glaucescens (Fonseca et al., The phenomenon of saurochory has been documented 2012), and Pilosocereus gounellei (Gomes et al., 2016, previously for the Cactaceae family (Fonseca et al., 2012; Nascimento et al., 2015; Xavier and Dias, 2015a,b, 2017; Gomes et al., 2016). In arid and semiarid environments, cacti provide different resources to pollinators and dispersers (such as pollen, nectar, and fruits), attracting them with varied shapes, scents, or colours and presenting fleshy fruits with high numbers of seeds (Pimienta-Barrios and Del Castillo, 2002; Taylor and Zappi, 2004; Gomes et al., 2014, 2016). In addition, herbivory is well documented for tropidurid lizards (Santos et al., 2012), with some species being considered as important dispersers of cactus seeds, including Tropidurus cocorobensis (Fonseca et al., 2012), T. hispidus (Ferreira et al., 2017), T. hygomi (Xavier and Dias, 2015a), T. pinima (Xavier and Dias,

1 Laboratório de Biologia e Ecologia de Vertebrados, Departamento de Biociências, Universidade Federal de Figure 1. Location of Parque Nacional Serra de Itabaiana, Sergipe, Campus Prof. Alberto Carvalho, Avenida Vereador Areia Branca Municipality, Sergipe State, Brazil, where Olímpio Grande, s/n, Itabaiana, Sergipe 49500-000, Brazil. Tropidurus semitaeniatus was observed feeding on fruits of * Corresponding author. E-mail: [email protected] Pilosocereus catingicola. SF River: São Francisco River; AL: © 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. Alagoas; BA: Bahia; SE: Sergipe. 346 Tainara Lima da Silva������� et al.

2017). In the present study, we describe a new record of demonstrating a great adaptation to semiarid conditions saurochory for T. semitaeniatus. (Medeiros et al., 2015). On 20 March 2015, a young T. semitaeniatus Saurochory records for the cactus Pilosocereus (snout–vent length = 49.3 mm) was captured in are scarce in the literature (Gomes et al., 2016, 2017), Parque Nacional Serra de Itabaiana, Sergipe State, and ornithochory is its main means of dispersion Brazil (10.4208°S, 37.4208°W; WGS 84; Fig. 1). (Silvius, 1995; Soriano et al., 1999; Godínez-Alvarez The unequivocal identification was made from et al., 2002; Rengifo et al., 2007; Gomes et al., 2014, morphological information of the species according 2017; Santos et al., 2019), which includes P. catingicola to Vanzolini et al. (1980): very flattened body, greyish (Medeiros et al., 2015). Meiado et al. (2012) suggested brown dorsal colour with a median light band, which that the funicular pulp of Pilosocereus inhibits seed runs from the tip of the snout to the base of the tail. germination, and its removal by that feed on its After the lizard was captured, a faecal sample was fruit facilitates seed germination. obtained by light ventral pressure. In the laboratory, The presence of P. catingicola seeds in faeces of T. the sample was analysed using a stereomicroscope, semitaeniatus indicate that likely this lizard is a seed and the cactus material in the sample was identified disperser. Passing of seeds through the digestive tract of as seeds of Pilosocereus catingicola (Gürke) Byles & may increase the germination rate (Figueira et al., Rowley subsp. salvadorensis (Werderm.) Zappi (Fig. 1994) or may not influence seed germination (Fonseca 2). This cactus is widely distributed in the northeastern et al., 2012). In addition, through dispersion the seeds Brazilian semiarid area, popularly known as facheiro, are transported away from the mother plant, avoiding

Figure 2. Pilosocereus catingicola in its fruiting state, observed in an area of rocky outcrops in Parque Nacional Serra de Itabaiana, Sergipe State, northeastern Brazil. (A) Fruit of P. catingicola. (B) Pulp fruit of P. catingicola impaled on part of the cactus closer to the ground. (C) Captured individual of T. semitaeniatus emitting faeces with pulp and seeds of P. catingicola. Photos by Jefferson O. Lima. First record of Tropidurus semitaeniatus ingesting a fruit Pilosocereus catingicola 347 competition (Valido and Olesen, 2007), and these seeds Gomes, V.G.N., Meiado, M.V., Quirino, Z.G.M., Araújo, H.F.P., can be favoured when they are released in a potentially Machado, I.C. (2017): Synchronous fruiting and common seed more suitable and safer places for recruitment (Hughes dispersers of two endemic columnar cacti in the Caatinga, a dry forest in Brazil. Plant Ecology 228: 1325–1338. et al., 2011; Fonseca et al., 2012). Hughes, F.M., Rot, M.L.C., Romão, R.L., Castro, M.S. (2011): This study adds relevant information about saurochory. Dinâmica espaço-temporal de Melocactus ernestii subsp. We hope that this note can contribute to future studies, as ernestii (Cactaceae) no nordeste do Brasil. Revista Brasileira de lizards have been increasingly considered as good seed Botânica 34: 389–402. dispersers. Therefore, further studies can be performed Kolodiuk, M.F., Ribeiro, L.B., Freire, E.M.X. (2009): The effects to demonstrate the efficiency of T. semitaeniatus in the of seasonality on the foraging behavior of Tropidurus hispidus germination of P. catingicola seeds. and Tropidurus semitaeniatus (Squamata: Tropiduridae) living in sympatry in the Caatinga of northeastern. Brazil. Zoologia Acknowledgements. We thank Marcos Vinícius Meiado for 26: 581–585. identifying the species of cactus and Annelise Batista D’Angiolella Meiado, M.V., Silva, F.F.S., Barbosa, D.C.A., Siqueira-Filho, for helpful suggestions. The samples were authorised by the J.A. (2012): Diásporos da Caatinga: uma revisão. In: A Flora Instituto Chico Mendes de Conservação da Biodiversidade das Caatingas do Rio São Francisco – História Natural e (Licence SISBIO/ICMBio, n° 45723-1). Conservação, p. 306–365. Siqueira-Filho, J.A., Ed., Rio de Janeiro, Brazil, Andrea Jakobsson Estúdio. Medeiros, R.L., Souza, V.C., Azeredo, G.A., Pereira, E.M., Barbosa References Neto, M.A., Medeiros, V.S., Barbosa, A.S. (2015): Germinação Aximoff, I., Felix, E. (2017): Natural history notes. Lygodactylus e vigor de sementes de Pilosocereus catingicola (Gürke) Byles klugei. Diet. Herpetological Review 48: 439. & Rowley subsp. salvadorensis (Werderm.) Zappi (Cactaceae) Casado, R.B., Soriano, P.J. (2010): Frutificación, frugivoría da Caatinga Paraibana. Gaia Scientia 9: 61–66. y dispersión en el cactus globular Melocactus schatzlii em Nascimento, J.P.B., Meiado, M.V., Nicola, P.A., Pereira, L.C.M. el enclave semiárido de Lagunillas, Mérida, Venezuela. (2015): Germinação de sementes de Tacinga inamoena (K. Ecotropicos 23: 18–36. Schum.) n. p. Taylor & Stuppy (Cactaceae) após endozoocoria Celedón-Neghme, C., Martins, L.A.S., Victoriano, P.F., Cavieres, por Chelonoidis carbonaria (Spix, 1824) (Reptilia: Testudinidae). L.A. (2008): Legitimate seed dispersal by lizards in an alpine Gaia Scientia 9: 9–14. habitat: the case of Berberis empetrifolia (Berberidaceae) Pimienta-Barrios, E., Del Castillo, R.F. (2002): Reproductive dispersed by Liolaemus belii (Tropiduridae). Acta Ecologica biology. In: Cacti and Uses, p. 163–183. Nobel, P.S., Ed., Sínica 33: 265–271. California, Los Angeles, University of California. Ferreira, A.S., Silva, A.D.O., Conceição, B.M., Faria, R.G. (2017): Rengifo, C.G., Naranjo, M.E., Soriano, P.J. (2007): Fruit The diet of six species of lizards in an area of Caatinga, Brazil. consumption by birds and bats on two species of columnar cacti Herpetological Journal 27: 151–160. in a semi-arid Andean enclave of Venezuela. Caribbean Journal Figueira, J.E.C., Vasconcellos-Neto, J., Garcia, M.A., Souza, of Science 43: 254–259. A.L.T. (1994): Saurocory in Melocactus violaceus (Cactaceae). Ribeiro, L.B., Freire, E.M. (2011): Trophic ecology and foraging Biotropica 26: 295–301. behavior of Tropidurus hispidus and Tropidurus semitaeniatus Fonseca, R.B.S., Funch, L.S., Borba, E.L. (2012): Dispersão (Squamata, Tropiduridae) in a caatinga area of northeastern de sementes de Melocactus glaucescens e M. paucispinus Brazil. Iheringia 101: 225–232. (Cactaceae), no Município de Morro do Chapéu, Chapada Ricklefs, R.E. (2010): A Economia da Natureza. Sixth Edition. Rio Diamantina – BA. Acta Botânica Brasílica 26: 481–492. de Janeiro, Brazil, Guanabara Koogan. Godínez-Alvarez, H., Valiente-Banuet, A., Rojas-Martínez, A. Rodrigues, M.T. (2003): Herpetofauna da Caatinga. In: Ecologia (2002): The role of seed dispersers in the population dynamics e Conservação da Caatinga, p. 181–236. Leal, I.R., Tabarelli, of the columnar cactus Neobuxbaumia tetetzo. Ecology 83: M., Silva, J.M.C., Ed., Recife, Brazil, Universidade Federal de 2617–2629. Pernambuco. Gomes, V.G.N., Quirino, Z.G.M., Machado, I.C. (2013): Pollination Rodríguez-Pérez, J., Rieira, N., Traveset, A. (2005): Effect of and seed dispersal of Melocactus ernestii Vaupel subsp. ernestii seed passage through birds and lizards on emergence rate (Cactaceae) by lizards: an example of double mutualism. Plant of Mediterranean species: differences between natural and Biology 16: 315–322. controlled conditions. Functional Ecology 19: 699–706. Gomes, V.G.N., Quirino, Z.G.M., Araujo, H.F.P. (2014): Frugivory Santos, N.E.F., Dias, U.N.S., Bezerra, J.K., Silva, C.D.A., Ribeiro, and seed dispersal by birds in Cereus jamacaru DC. ssp. L.B. (2012): Frugivoria e dispersão de sementes por lagartos em jamacaru (Cactaceae) in the Caatinga of northeastern Brazil. ecossistemas brasileiros: uma revisão. Revista Nordestina de Brazilian Journal of Biology 74: 32–40. Zoologia 6: 74–102. Gomes, V.G.N., Meiado, M.V., Quirino, Z.G.M., Machado, I.C. Santos, L.D.N., Pereira, I.M.S., Ribeiro, J.R., Las-Casas, F.M.G. (2016): Seed removal by lizards and effect of gut passage on (2019): Frugivoria por aves em quatro espécies de Cactaceae na germination in a columnar cactus of the Caatinga, a tropical dry Caatinga, uma floresta seca no Brasil. Inheringia 109: 1–10. forest in Brazil. Journal Arid Environments 135: 85–89. Silvius, K.M. (1995): Avian consumers of cardón fruits (Stenocereus 348 Tainara Lima da Silva������� et al.

griseus: Cactaceae) on Margarita Island, Venezuela. Biotropica Valido, A., Olesen, J.M. (2019): Frugivory and seed dispersal by 27: 96–105. lizards: a global review. Frontiers in Ecology and Evolution 7: Soriano, P.J., Naranjo, M.E., Rengifo, C., Figuera, M., Rondón, M., 1–85. Ruiz, L. (1999): Avian consumers of columnar cacti fruits in the Valido, A., Nogales, M., Medina, F.M. (2003): Fleshy fruits in the semiarid enclave of Lagunillas, Merida, Venezuela. Ecotropicos diet of Canarian lizards Gallotia galloti () in a xeric 12: 91–100. habitat of the island of Tenerife. Journal of Herpetology 37: Taylor, N.P., Zappi, D.C. (2004): Cacti of Eastern Brazil. Richmond, 741–747. United Kingdom, Royal Botanic Gardens, Kew. Vanzolini, P.E., Ramos-Costa, A.M., Vitt, L.J. (1980): Répteis Traveset, A., Verdú, M. (2002): A meta-analysis of the effect das Caatingas. Rio de Janeiro, Brazil, Academia Brasileira de of gut treatment on seed germination. In: Seed Dispersal and Ciências. Frugivory: Ecology, Evolution and Conservation, p. 339–350. Xavier, M.A., Dias, E.J.R. (2015a): First record of the Brazilian Levey, D.J., Silva, W.R., Galetti, M., Eds., Wallingford, United restinga lizard Tropidurus hygomi ingesting a fruit of Melocactus Kingdom, CABI Publishing. violaceus (Cactaceae). Herpetology Notes 8: 437–438. Uetz, P., Freed, P., Hošek, J. (2020): The Database. Xavier, M.A., Dias, E.J.R. (2015b): Natural history notes. Ameivula Available at: http://www.reptile-database.org. Accessed on 01 abaetensis. Saurochory. Herpetological Review 46: 430–431. March 2019. Xavier, M.A., Dias, E.J.R. (2017): Natural history notes. Tropidurus Valido, A., Olesen, J.M. (2007): The importance of lizards as pinima. Saurochory. Herpetological Review 48: 202–203. frugivores and seed dispersers. In: Seed Dispersal: Theory and Application in a Changing World, p. 124–147. Dennis, A.J., Schupp, E.W., Green, R., Westcott, D.A., Eds., Wallingford, United Kingdom, CABI Publishing.

Accepted by Aldemar Acevedo