Use of a Rostral Appendage During Social Interactions in the Ecuadorian Anolis Proboscis
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Journal of Natural History ISSN: 0022-2933 (Print) 1464-5262 (Online) Journal homepage: https://www.tandfonline.com/loi/tnah20 Use of a rostral appendage during social interactions in the Ecuadorian Anolis proboscis Diego R. Quirola, Andrés Mármol, Omar Torres-Carvajal, Andrea E. Narváez, Fernando Ayala-Varela & Ignacio T. Moore To cite this article: Diego R. Quirola, Andrés Mármol, Omar Torres-Carvajal, Andrea E. Narváez, Fernando Ayala-Varela & Ignacio T. Moore (2017) Use of a rostral appendage during social interactions in the Ecuadorian Anolisproboscis, Journal of Natural History, 51:27-28, 1625-1638, DOI: 10.1080/00222933.2017.1332790 To link to this article: https://doi.org/10.1080/00222933.2017.1332790 View supplementary material Published online: 02 Jun 2017. Submit your article to this journal Article views: 409 View Crossmark data Citing articles: 1 View citing articles Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=tnah20 JOURNAL OF NATURAL HISTORY, 2017 VOL. 51, NOS. 27–28, 1625–1638 https://doi.org/10.1080/00222933.2017.1332790 Use of a rostral appendage during social interactions in the Ecuadorian Anolis proboscis Diego R. Quirola a, Andrés Mármola, Omar Torres-Carvajal a, Andrea E. Narváez b, Fernando Ayala-Varelaa and Ignacio T. Moore c aMuseo de Zoología, Escuela de Ciencias Biológicas, Pontificia Universidad Católica del Ecuador, Quito, Ecuador; bDepartment of Ecology, Environment and Evolution, La Trobe University, Bundoora, Australia; cDepartment of Biological Sciences, Virginia Tech, Blacksburg, VA, USA ABSTRACT ARTICLE HISTORY The use of sexually selected characters in inter- and intra-sexual Received 28 January 2017 interactions has long been of interest to evolutionary biologists. Accepted 11 May 2017 Recently, a distinction between sexually selected traits as ornaments Online 2 June 2017 versus weapons has been advanced. We investigated the behaviour KEYWORDS of an enigmatic lizard with a prominent sexually dimorphic trait in an Behaviour; exaggerated trait; effort to describe whether the trait was the product of sexual selec- Anolis; sexual selection tion and further whether it functioned as a weapon or an ornament. The subject of our study was the Ecuadorian proboscis anole (Anolis proboscis), a slow-moving cryptic species endemic to the north-wes- tern slopes of the Andes in Ecuador. Males, but not females, of this species bear a rostral appendage that has been described as an exaggerated trait resulting from sexual selection. However, a thor- oughdescriptionoftheuseoftherostralappendageinsocialinter- actions is lacking. Here, we describe social interactions of this species during 11 male–female courtships and mating interactions, as well as three male–male agonistic interactions. We describe four types of displays by males, many involving the rostral appendage. We found that the rostral appendage is used as an ornament in social displays but not as a weapon in combat. We also show that, unlike other lizards with rostral appendages, male A. proboscis hatchwiththis structure already developed. Introduction Sexual selection has resulted in numerous examples of exaggerated morphological traits. These traits are typically used in intersexual selection (e.g. mate choice) and/or intra-sexual selection (e.g. male–male competition), such as spines in stickleback fish, or conspicuous plumage in birds (Andersson 1994). In males, exaggerated secondary sexual characters may be honest indicators of individual fitness (Lailvaux and Irschick 2006; Irschick et al. 2007a, 2007b; Karsten et al. 2009a). For example, there are some functional correlations of exaggerated traits, such as dewlap and head size with bite force in lizards (Vanhooydonck et al. 2005a, 2005b; Irschick et al. 2006; Karsten et al. 2009a). Thus, CONTACT Andrea E. Narváez [email protected] Supplemental material for this article can be accessed here. © 2017 Informa UK Limited, trading as Taylor & Francis Group Published online 02 Jun 2017 1626 D. R. QUIROLA ET AL. exaggerated traits may be honest signals of performance and benefit the males in intra- sexual selection, inter-sexual selection, or both (Karsten et al. 2009a). Finally, exagger- ated traits may function as either weapons or ornaments, or both. Recent arguments have suggested caution in interpretation of exaggerated traits, as combat and mating functions are not easily distinguished based on morphology alone (McCullough et al. 2016). Lizards of the genus Anolis have long been used as model systems for investigating sexually selected traits. One such exaggerated morphological trait is the dewlap, an extensible flap of skin under the throat that varies among species in size and colour pattern (Losos 2009). There is also individual variation in the dewlap that is important in intra-specific communication (Greenberg and Noble 1944; Losos 1985; Decourcy and Jenssen 1994). The dewlap is used in stereotyped visual displays that usually involve other body movements such as head-bobs and push-ups (Greenberg and Noble 1944; Jenssen 1977; Losos 2009; Fleishman and Pallus 2010). Three Anolis species possess another exaggerated trait, a rostral appendage (Williams 1979). One of them is Anolis proboscis (Peters and Orcés 1956); it was long thought extinct but was recently rediscovered (Almendáriz and Vogt 2007). Anolis proboscis is a slow-moving cryptic species, endemic to the western slope of the Andes in northern Ecuador (Yánez-Muñoz et al. 2010; Losos et al. 2012; Poe et al. 2012). The rostral appendage of A. proboscis is soft, fleshy, flexible, and compressed laterally. The presence of such appendage has granted this group of lizards several common names, such as horned anoles. However, this is not a rigid structure (horn like), but is at least somewhat mobile (Yánez-Muñoz et al. 2010; Losos et al. 2012; Poe et al. 2012). Therefore, we will refer hereafter to the species as proboscis anole. While the rostral appendage in A. proboscis has been previously described, its function in social displays remains unclear. The presence of the rostral appendage only in males has led to the suggestion that it is a product of sexual selection (Williams 1979; Yánez-Muñoz et al. 2010; Losos et al. 2012). As such, it could be used in male–male competition, female mate choice, or both. In this study, we hypothesized that the rostral appendage would be used during male–female interac- tions as an ornament rather than used in male competition as a weapon (sensu McCullough et al. 2016). We provide new insights on the social behaviour of A. proboscis, by reporting, for the first time, observations of how males use the rostral appendage during both agonistic and courtship encounters. In addition, we provide general data on the ontogeny of this structure. Materials and methods Reproduction in captivity To learn more about the ontogeny of the rostral appendage in Anolis proboscis,we captured and housed a gravid adult female (QCAZ 12725) at Museo de Zoología QCAZ, Pontificia Universidad Católica del Ecuador in Quito. The eggs were incubated under an ambient temperature that varied from ca. 28°C during the day to ca. 17°C during the night, and relative humidity was between 80% and 90%. JOURNAL OF NATURAL HISTORY 1627 Table 1. Mating behaviour in Anolis proboscis. Duration of courtship (COU), chasing (CHA), stimulation (STI), copulation (COP), and total time (TT) is shown in seconds. Information on bitings (BIT), copulation substrate (SUB), and hemipenis used (HEM) is also shown. Asterisks indicate cases in which males failed to perform head movements in chasing. A numbered code (MIN) was assigned to each individual. Mating individuals female–male Date of trial (2014) COU CHA STI COP TT BIT SUB HEM 1 MIN2–MIN5 28 February 154 - - - - No Branch Right 2 MIN2–MIN5 1 March 19 22 33 191 305 No Leaf Left 3 MIN2–MIN5 2 March 9 32* 28 220 332 No Branch Right 4 MIN12–MIN13 26 May - 33 95 363 - Yes Branch Left 5 MIN14–MIN13 26 May 47/23 41 43 251 370 Yes Branch Right 6 MIN12–MIN13 28 May 3 23* 82 413 536 Yes Branch Left 7 MIN14–MIN13 29 May 11 - * - 298 442 Yes Araceae petiole Right 8 MIN24–MIN21 15 September - - 75 251 353 No Branch Right 9 MIN24–MIN22 17 September 13 - * - 148 - No Trunk Right 10 MIN28–MIN27 17 September 3 14 39 183 249 Yes Araceae petiole Left 11 MIN28–MIN27 18 September 17 30* 76 304 433 Yes Leaf Right Behaviour trials To investigate the social behaviour and use of the rostral appendage, we conducted behavioural trials with male and female Anolis proboscis.WesearchedforA. proboscis in the area surrounding the town of Mindo, Pichincha Provence, Ecuador, located at ~1270 m of elevation on the western slopes of the Andes (exact locations withheld to avoid poach- ing). Upon visually locating an individual, we captured them by hand or by noosing. Each captured lizard was assigned a code that was written on its abdomen with a marker. Lizards were kept in captivity for a maximum of three days, after which they were released at their original capture locations. Behaviour trials were conducted in an outdoor set-up, under natural environmental conditions, located approximately 5 km away from the collecting sites. A solitary tree in an open area was selected to allow observation of the animals from multiple perspectives. We selected a bushy tree, big enough to allow the animals to move freely. For each trial, two lizards (two males, or one male and one female) were placed facing to each other on different branches, or on the same branch, separated by at least 45 cm. Two video cameras were used to record lizards’ behaviours from a distance that varied between 3 and 7 m. All trials were conducted between 09:00 h and 12:00 h from 28 February until 18 September 2014 (Tables 1 and 2), following previous observations of activity patterns of A. proboscis (Losos et al.