Full Mating Repertoire of Tropidurus Hygomi Reinhardt and Lütken, 1861 on a Coastal Sand Dune Habitat in Bahia, Brazil (Squamata: Tropiduridae)

Herpetology Notes, volume 12: 353-357 (2019) (published online on 07 April 2019)

Full mating repertoire of Tropidurus hygomi Reinhardt and Lütken, 1861 on a coastal sand dune habitat in Bahia, Brazil (Squamata: Tropiduridae)

Luciana Vasconcelos1, Andre C. Bruinjé2,3,*, Felipe E. A. Coelho2, Moacir Santos Tinôco1,4, and Ricardo Marques5

Courtship displays vary greatly among lizard species. Werner, 1978), and for the genus Tropidurus (Wied- It plays an important role on mating success since, apart Neuwied, 1825) (Carpenter, 1977; Coelho et al., 2018), from being species-specific, it should signal and inform occurring in the Caatinga and Amazon Forest biomes. male individual quality to the female (Miles et al., Regarding the reproductive behaviour, there are few 2007). These individual “quality” characteristics can be reports describing the detection and approaching phases in terms of some intrinsic quality (such as better immune of Tropidurus mating, with the male performing head system, physiological condition, and physiological bob displays (Carpenter, 1977; Ávila and Cunha- performance) or in terms of a visually accessible Avellar, 2006; Vaz e Nunes et al., 2008; Vasconcelos quality, such as secondary sexual traits (e.g., increasing et al., 2013; Lima et al., 2017). Copulation, however, showiness of morphological traits, such as colouration, did not occur in any of these reports, not allowing the or the display itself) (Andersson and Simmons, 2006). description of the mating behavioural repertoire, as well Such behaviours are often reported in visually oriented as post-mating behaviours. lizards, such as in Iguania (Schwenk, 1993). Along the coast of Brazil there is the restinga The family Tropiduridae is widely distributed through ecosystem, which is a coastal habitat with sand dunes South America (Frost, 1992). In regard of behavioural that was formed by marine transgressions during the studies within this group, there are some reports for Quaternary. It consists of four types of vegetation, the genus Microlophus (Duméril and Bibron, 1837), which includes beach vegetation, flooded plain, inhabitant of the Galapagos’ Islands and mainland shrub vegetation, and restinga dry forest (Leão and Ecuador (Carpenter, 1966, 1977; Stebbins et al., 1967; Dominguez, 2000; Menezes et al., 2009). Tropidurus hygomi is distributed from the north coast of Bahia to the state of Sergipe, in Brazil (Martins et al., 2010). It inhabits the restinga, being frequently observed in habitats of beach and shrub vegetation. 1 Centro de Ecologia e Conservação Ambiental, Universidade Católica do Salvador, Avenida Professor Pinto de Aguiar Tropidurus hygomi is an heliothermic lizard, considered 2589, Salvador, Bahia 41740-090, Brazil. endangered and endemic to the open habitats of these 2 Departamento de Ecologia, Centro de Biociências, coastal sand dunes (IBAMA, 2014). This lizard is Universidade Federal do Rio Grande do Norte, Natal, Rio a sit and wait forager that feeds on arthropods on the Grande do Norte 59078-900, Brazil. ground and on leaf litter (Travassos et al., 2015). The 3 Departamento de Fisiologia, Instituto de Biociências, behavioural repertoire of T. hygomi, however, remains Universidade de São Paulo, São Paulo, São Paulo 05508- unknown. Here we describe the full court ritual and, for 090, Brazil. 4 Durrell Institute of Conservation and Ecology, School of the first time, the full mating behaviour of T. hygomi. Anthropology and Conservation, University of Kent, Marlowe Building, Canterbury, Kent CT2 7NZ, United Materials and Methods Kingdom. On 6 May 2013 at 1528 h, during field observations 5 Departamento de Sistemática e Ecologia, Centro de Ciências Exatas e da Natureza, Universidade Federal da Paraíba; João towards a behavioural survey, we observed two Pessoa, Paraíba 58051-900, Brazil. individuals of Tropidurus hygomi engaging in * Corresponding author. E-mail: [email protected] interactions towards intercourse behaviour. The 354 Luciana Vasconcelos et al. observation took place at the restinga of Imbassaí remained in that position for 20 seconds. After detaching (12.4816°S, 37.9571°W; datum WGS84; 21 m from the female, the male slowly moved in circles elevation), Municipality of Mata de São João, State around the female until the female moved towards the of Bahia, Northeast Brazil. The observed lizards were right direction, while the male remained in the same at shrub vegetation, on a sandy soil surrounded by location (Fig. 1D). The male kept walking very slowly herbaceous vegetation. Because characteristics of the while performing pelvic rubbing on the substrate, for environment may influence behavioural displays and approximately one minute (Fig. 1E). Shortly after, the reactions in lizards (Herrel et al., 2007), we recorded male moved towards the female’s direction and restarted air temperature (33.7 °C), air humidity (57.4%), and head bobbing (Fig. 1F). The female then proceeded with substrate temperature (42.6 °C). During the whole short sprints while the male chased the female until both observation, the observer (RM) kept a distance of about lizards distanced themselves from the observer among three meters from the two individuals. For the recordings, the bushes. The observation ended at 1532 h. So, the we used a Canon EOS Rebel T4i digital camera. We entire event with the court behaviours, copulation, and conducted the observation under ICMBio permit post-mating behaviours, lasted about four minutes. number 23355-4. For the description of behaviours, we use the terms according to Carpenter and Ferguson Discussion (1977). head bob displays are rapid up-and-down Life-history traits, such as mating repertoire, present movements of the head performed by the lizard, while differences among families, but often present minor tail waving are movements of the lizard’s tail from side variation among phylogenetic related species in lizards to side, often performed with an erect position of the (Brattstrom, 1974). Our report demonstrates that, tail (e.g., Coelho et al., 2018). Both behaviours can be except for lowering the head and arching the body, the signals to conspecifics and are often (e.g., tail waving) mating repertoire of Tropidurus hygomi is similar to related to mating interactions. other species of iguanians (sensu Tonini et al., 2016). Beginning with the perception of the female presence, Results the male approaches and performs courtship displays Prior to their interaction, the lizards were about 1.5 (Clarke, 1963; Carpenter, 1966; Mesquita et al., 2016). meters away from each other. We could only determine Head bob is a social display that varies even among their sex after the copulation because sexual dimorphism populations, according to morphology, life history is not evident in this species and, henceforth, we traits, age, sex, and the context of which it is used (e.g., treat each lizard by their respective sex. The male, in agonistic or mating behaviours) (Labra et al., 2007; bigger and more robust, was steady in its place and Macedonia et al., 2015). The male invited the female for interacting with the female, performing head bobs. courtship by bobbing its own head, which is a common Then, it moved short distances approaching the female. display in other tropidurids, as well as biting the During its locomotion, every time the male stopped, female’s neck before the ritual (Carpenter, 1966). This it performed tail waving and head bobs with its body male behaviour is also reported as a method to pacify the positioned laterally towards the female. This sequence mate and successfully achieve copulation (Crews, 1987). was repeated for approximately one minute until it Our observation showed T. hygomi biting the female’s reached the female when both performed head bobs neck after she accepted the court. For the Galapagoan in front of each other. Before the male approached the tropidurids, biting was done onto the collarbones region counterpart, the female’s tail was still and parallel to the when the courtship was successful, while it was done at ground. The female then lifted its body from the ground the tail when the court was rejected (Carpenter, 1966). while keeping its limbs steady. The male approached In another courtship observation of T. hygomi, even from behind and climbed on the female, keeping the though it was rejected, the male did not bite the female. forelegs around the female’s body and turning its own The female, on the other hand, raised its tail during such body slightly to the side, while biting the female’s neck observation, which is a sign of no receptivity within the (Fig. 1A). Both lizards moved forward together (Fig. species court repertoire (Carpenter, 1966; Vasconcelos 1B), until the female raised the tail, allowing the male to et al., 2013). In our observation, female tail rising assume copulation position, lowering its head, arching was not performed, and the copulation attempt was its body over the female, arranging the cloacal openings, successful, which reinforces the signal of no receptivity and inserting its right hemipenis (Fig. 1C). The lizards emitted by this behaviour. Full mating repertoire of Tropidurus hygomi on a coastal sand dune 355

Figure 1. Court and copulation stages in Tropidurus hygomi: (A) male jumping on top of the female before biting its neck; (B) both individuals moving around the area with the male on top of the female; (C) male and female copulating; (D) female moving away after copulation; (E) the male remained at the copulation location (on the left) while the female distanced itself (on the right); (F) the male (on the left) turned back on following the female (on the right). Photographs taken by Ricardo Marques. Individuals were highlighted and the background was faded due to the cryptic colouration of the species for a better visual perception.

During copulation, the arched position – or “doughnut its dorsum and did not bite it while on arched position. posture” – assumed by the male occurs when the male Possibly, it is a variation within T. hygomi species, protrudes its hemipenis into the mate, ceases biting its which should be verified by further studies. Clarke neck, and then bites its pelvic region, which indicates (1963) and Greenberg (1977) reported copulations ejaculation (Crews, 1987). In our observation, the from two to 20 seconds for Holbrookia maculata male ceased biting the female right after climbing on Girard, 1851, and Sceloporus cyanogenys Cope, 1885, 356 Luciana Vasconcelos et al. respectively. Such reports are similar to our findings Carpenter, C.C. (1977): The aggressive displays of three species of T. hygomi’s 20 seconds-lasting mating, which we of South American iguanid lizards of the genus Tropidurus. believe was a successful copulation. Pelvic rubbing Herpetologica 33 (3): 285–289. Carpenter, C.C., Ferguson, G.W. (1977): Variation and evolution after copulation was not described to the species in the of stereotyped behavior in reptiles. In: Biology of Reptilia: Galapagos Islands, but was reported by Jenssen (1970) Ecology and behaviour, v. 7A, p. 335–554. Gans, C., Tinkle to the iguanians Anolis nebulosus (Wiegmann, 1834), D.W., Eds., London, UK, Academic Press. and by Greenberg (1977) to Sceloporus cyanogenys. Clarke, R.F. (1963): An ethological study of the Iguanid lizard Such behaviour is similar to the behaviour of post- genera Callisaurus, Cophosaurus, and Holbrookia. Unpublished evacuation, and is suggested by the authors as a likely PhD thesis, The University of Oklahoma, Oklahoma, USA. Coelho, F.E.A., Bruinjé, A.C., Costa, G.C. (2018): Ethogram with way of depositing chemical signals. On Ameivula (Spix, the description of a new behavioral display for the striped lava 1825) species (Teiidae), this behaviour occurs before lizard, Tropidurus semitaeniatus. South American Journal of the copulation as an auto-stimulation of the male, or as Herpetology 13 (1): 96–101. intersexual communication (Carpenter, 1962; Ribeiro et Crews, D. (1987): Courtship in unisexual lizards: a model for brain al., 2011). Moving in circles around the female was also evolution. Scientific American 257: 72–77. reported by Lima et al. (2017) in Tropidurus hispidus Frost, D. (1992): Phylogenetyc analysis and taxonomy of the Tropidurus group of lizards (Iguania: Tropiduridae). Americam (Spix, 1825). However, males of T. hispidus performed Museum Novitates 3033: 1–68. this behaviour prior to mounting the female, and not Greenberg, N. (1977): An Ethogram of the Blue Spiny Lizard, after, as we report here for T. hygomi. Sceloporus cyanogenys (Reptilia, Lacertilia, Iguanidae). Journal Our observation on T. hygomi mating repertoire of Herpetology 11 (2): 177–195. shows some similarities with other iguanian families, Herrel, A., James, R.S., Van Damme, R. (2007): Fight versus possibly consisting of phylogenetically shared features. flight: physiological basis for temperature-dependent behavioral This is novel information for the natural history of this shifts in lizards. Journal of Experimental Biology 210 (10): 1762–1767. endangered species with a restricted distribution, and IBAMA, MMA (2014). Listas das Espécies da Fauna Brasileira further contributions should establish a pattern for the ameaçadas de extinção vigentes. Portarias MMA n° 444/2014 sexual behaviour of T. hygomi, as well as other aspects e 445/2014. of its behavioural repertoire. Jenssen, T.A. (1970): The ethoecology of Anolis nebulosis (Sauria, Iguanidae). Journal of Herpetology 4: 1–38. Labra, A., Carozo, P., Desfilis, E., Font, E. (2007): Agonistic Acknowledgements. We thank the collaboration of Herpetofauna interactions in a Liolaemus lizard: Structure of head bob of the North Coast of Bahia research group project and ECOA displays. Herpetologica 63 (1): 11–18. Centre at the UCSAL on fieldwork activities. We also thank the Leão, Z.M.A.N., Dominguez, J.M.L. (2000): Tropical coast of Reserva Imbassaí Institution, the Grand Palladium Resort, the Brazil. Marine Pollution Bulletin 41 (1): 112–122. APA do Litoral Norte Council, and the City Hall of the visited Lima, D.S.S., Siqueira, R.S., Dias, E.J.R., Lira-da-Silva, R.M. municipality for general support. RM thanks Coordenação de (2017): Atividades diárias de Tropidurus hispidus (Squamata: Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the Iguania: Tropiduridae) na Ilha do Monte Cristo, Baía de Todos- current PhD scholarship (Process number 1489596). We also os-Santos, Bahia, Brazil. Revista Brasileira de Zoociências 18 thank an anonymous reviewer and the editor for comments and (2): 55–70. suggestions that significantly improved the manuscript. Macedonia, J.M., Clarck, D.L., Cherry, L.E., Mohamed, N.E., Bartel, B.W. (2015): Comparison of Headbob Displays in Gray- References Dewlapped and Red-Dewlapped Populations of Green Anoles (Anolis carolinensis). Herpetologica 71 (2): 117–124. Andersson, M., Simmons, L.W. (2006): Sexual selection and mate Martins, K.V., Dias, E.J.R., Rocha, C.F.D. (2010): Ecologia e choice. Trends in Ecology and Evolution 21: 296–302. conservação do lagarto endêmico Tropidurus hygomi (Sauria: Ávila, R.W., Cunha-Avellar, L.R. (2006): Tropidurus etheridgei Tropiduridae) nas restingas do Litoral Norte da Bahia, Brasil. (NCN). Courtship. Herpetological Review 37 (4): 473. Biotemas 23 (4): 71–75. Brattstrom, B.H. (1974): The Evolution of Reptilian Social Menezes, C.M., Aguiar, L.G.P.A., Espinheira, M.J.C.L., Silva, Behavior. American Zoologist 14: 35–49. V.I.S. (2009): Florística e fitossociologia do componente arbóreo Carpenter, C.C. (1962): Patterns of behaviour in two Oklahoma do município de Conde, Bahia, Brasil. Revista Biociências 21 lizards. The American Midland Naturalist 67: 132–151. (1): 44–55. Carpenter, C.C. (1966): Comparative behavior of the Galapagos Mesquita, D.O., Costa, G.C., Colli, G.R., Costa, T.B., Shepard, D.B., Lava Lizards (Tropidurus). In: The Galapagos. Proceedings of Vitt, L.J., Pianka, E.R. (2016): Life-History Patterns of Lizards the Symposia of the Galapagos International Scientific Project, of the World. The American Naturalist 187 (6): 689–705. p. 269–273. Bowman, R.I., Ed., California, USA, University of Miles, D.B., Sinervo, B., Hazard, L.C., Svensson, E.I., Costa, D. California Press. (2007): Relating endocrinology, physiology and behaviour Full mating repertoire of Tropidurus hygomi on a coastal sand dune 357

using species with alternative mating strategies. Functional Ecology 21: 653–665. Ribeiro, L.B., Gogliath, M., Sales, R.F.D., Freire, E.M.X. (2011): Mating behavior and female accompaniment in the whiptail lizard Cnemidophorus ocellifer (Squamata, Teiidae) in the Caatinga region of northeastern Brazil. Biota Neotropica 11 (4): 363–368. Schwenk, K. (1993): The evolution of chemoreception in squamate reptiles: A phylogenetic approach. Brain, Behavior and Evolution 41: 124–137. Stebbins, R.C., Lowestein, J.M., Cohen, N.W. (1967): A field study of the lava lizard (Tropidurus albermalensis) in the Galápagos Islands. Ecological Society of America 48 (5): 839–851. Tonini, J.F.R., Beard, K.H., Ferreira, R.B., Jetz, W., Pyron, R.A. (2016): Fully-sampled phylogenies of squamates reveal evolutionary patterns in threat status. Biological Conservation 204: 23–31. Vasconcelos, L., Marques, R., Tinôco, M.S. (2013): Tropidurus hygomi (Reinhardt’s Lava Lizard). Courtship behaviour. Herpetological Review 44 (3): 514–515. Vaz e Nunes, J., Elisei, T., Sousa, B.M. (2008): Tropidurus itambere (Rock lizard). Social Interactions. Herpetological Review 39 (3): 351–352. Travassos, M.L.O., Tinôco, M.S., Marques, R., Delabie, J.H.C. (2015): Lizard prey predilections and resource use in restinga habitats on the north coast of Bahia. Salamandra 51 (2): 171– 181. Werner, D.I. (1978): On the biology of Tropidurus delanonis, Baur (Iguanidae). Ethology 47 (4): 337–395.

Accepted by Pedro Pinna