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A Multi-Level Study with 15 Species of Monkey Tree Frogs (Anura: Phyllomedusidae)

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A Multi-Level Study with 15 Species of Monkey Tree Frogs (Anura: Phyllomedusidae) Canadian Journal of Zoology Variability in anuran advertisement call: a multi-level study with 15 species of monkey tree frogs (Anura: Phyllomedusidae) Journal: Canadian Journal of Zoology Manuscript ID cjz-2020-0018.R1 Manuscript Type: Article Date Submitted by the 10-Mar-2020 Author: Complete List of Authors: Röhr, David; Universidade Federal do Rio Grande do Norte Centro de Biociencias, Ecologia; Faculdade Pitágoras de Medicina de Eunápolis Camurugi, Felipe; Universidade Federal do Rio Grande do Norte, Botânica eDraft Zoologia; Universidade Federal da Paraiba, Centro de Ciências Exatas e da Natureza Paterno, Gustavo ; Universidade Federal do Rio Grande do Norte, Ecologia Gehara, Marcelo; American Museum of Natural History Juncá, Flora; Universidade Estadual de Feira de Santana, Ciências Biológicas Álvares, Guilherme; Universidade de Brasília, Laboratório de Fauna e Unidades de Conservação, Departamento de Engenharia Florestal Brandão, Reuber; Universidade de Brasília, Laboratório de Fauna e Unidades de Conservação, Departamento de Engenharia Florestal Garda, Adrian; Universidade Federal do Rio Grande do Norte, Depto de Botânica, Ecologia e Zoologia Is your manuscript invited for consideration in a Special Not applicable (regular submission) Issue?: acoustic communication, EVOLUTION < Discipline, <i>Pithecopus</i>, Keyword: <i>Phyllomedusa</i>, phylogenetic signal, trait diversification, VARIATION < Discipline https://mc06.manuscriptcentral.com/cjz-pubs Page 1 of 35 Canadian Journal of Zoology Variability in anuran advertisement call: A multi-level study with 15 species of monkey tree frogs (Anura: Phyllomedusidae) David L. Röhr*, Felipe Camurugi, Gustavo B. Paterno, Marcelo Gehara, Flora A. Juncá, Guilherme F. R. Álvares, Reuber A. Brandão, and Adrian A. Garda D.L. Röhr Departamento de Ecologia, Universidade Federal do Rio Grande do Norte, Lagoa Nova, 59072–970, Natal, RN, Brazil, [email protected] F. Camurugi Programa de Pós-Graduação em Ciências Biológicas (Zoologia), Departamento de Sistemática e Ecologia, Centro de Ciências Exatas e da Natureza, Universidade Federal da Paraíba, João Pessoa, 58059–900, PB, Brazil, [email protected] G.B. Paterno Departamento de Ecologia, Universidade Federal do Rio Grande do Norte, Lagoa Nova, 59072–970, Natal, RN, Brazil, [email protected] M. Gehara Rutgers University-Newark, DepartmentDraft of Biological Sciences, 195 University Ave, Newark, NJ 07102, USA, [email protected] F.A. Juncá Departamento de Ciências Biológicas, Universidade Estadual de Feira de Santana, BR 116, Km 03, Campus Universitário, 44031–460, Feira de Santana, BA, Brazil, [email protected] G.F.R. Álvares Laboratório de Fauna e Unidades de Conservação, Departamento de Engenharia Florestal, Universidade de Brasília, 70.910-900, Brasília – DF, Brazil, [email protected] R.A. Brandão Laboratório de Fauna e Unidades de Conservação, Departamento de Engenharia Florestal, Universidade de Brasília, 70.910-900, Brasília – DF, Brazil, [email protected] A.A. Garda Departamento de Botânica e Zoologia, Universidade Federal do Rio Grande do Norte, Campus Universitário, Lagoa Nova, 59072-970, Natal, RN, Brazil, [email protected] Corresponding author: Felipe Camurugi ([email protected]) *Present Address: Faculdade Pitágoras de Medicina de Eunápolis, Centauro, 45821-170, Eunápolis, BA, Brazil 1 https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 2 of 35 Variability in anuran advertisement call: A multi-level study with 15 species of monkey tree frogs (Anura: Phyllomedusidae) D. L. Röhr, F. Camurugi, G. B. Paterno, M. Gehara, F. A. Juncá, G. F. R. Álvares, R. A. Brandão, and A. A. Garda Abstract Understanding the variability of acoustic signals is a first important step for the comprehension of the evolutionary processes that led to current diversity. Herein, we evaluate the variability of the advertisement call of the phyllomedusid species from the genera Phyllomedusa and Pithecopus at different levels: intra-individual, intra-population, inter- population, intra-species, and inter-specific.Draft An analysis of coefficients of variation showed a continuum of variability between the acoustic parameters analyzed, from static to highly dynamic. Most of the variation was attributed to the inter-specific level while call parameters at the intra-individual level varied the least. However, each parameter behaved differently with call interval being the most variable across all levels. Most temporal acoustic parameters were affected by environmental temperature while pulse rate and dominant frequency were strongly influenced by body size. Only pulse rate was correlated to the geographic distance between populations, while all parameters presented a significant phylogenetic signal. Based on these results, we discuss the possible importance of different evolutionary forces and the usage of vocalizations for taxonomic purposes. Key words: acoustic communication, evolution, Pithecopus, Phyllomedusa, phylogenetic signal, trait diversification, variation 2 https://mc06.manuscriptcentral.com/cjz-pubs Page 3 of 35 Canadian Journal of Zoology Introduction Understanding variability is fundamental for the comprehension of evolution (Hallgrimsson and Hall 2011). Darwin´s observations on phenotypic variation were the basis for the development of the concept of natural selection (Darwin 1859), and intra and inter- specific variation were central for the modern evolutionary synthesis (Mayr 1966; Wright 1984). Acoustic signals are important for a large proportion of current fauna, and for most groups it has a predominantly reproductive function (Bradbury and Vehrencamp 1998). There is evidence that acoustic communication may not have increased the diversification rates of terrestrial vertebrates at a macro evolutionary scale (Chen and Wiens 2020). However, because these signals are involved in conspecific recognition, they may have a key role in speciation of highly vocal groups, such as birds and frogs, and their importance as an evolutionary force has been the focus ofDraft many studies (Wilkins et al. 2013). Acoustic signals are the predominant form of communication for the vast majority of anuran species. Although many species present more than one type of call, the advertisement call emitted by males with the main function of attracting females can be considered the most important acoustic signal for this clade (Wells 1977). Since the beginning of bioacoustic studies on anurans, authors report that each species has a distinct advertisement call (Blair 1958, 1964; Duellman and Pyles 1983). Furthermore, it has been shown that females prefer conspecific advertisement calls, even when considering sister taxa with relatively similar calls (Gerhardt 1974; Backwell and Jennions 1993). Thus, this vocalization is considered an important prezygotic reproductive barrier (Gerhardt and Huber 2002) and has been used as an important taxonomic tool, helping overcome the lack of useful external morphological traits in frogs (Padial and De la Riva 2009; Köhler et al. 2017). The anuran advertisement call is considered stereotyped, especially in comparison to other vertebrates such as birds and mammals. Still, there is considerable amount of intra- 3 https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 4 of 35 specific variation at the individual level (Howard and Young 1998), at the population level (Sullivan 1982), and among populations of the same species (Sullivan 1989). Although several studies clearly demonstrate this variation in each level separately, few studies have quantified how different acoustic parameters vary across multiple levels (within and between individuals, populations and species) (Castellano et al. 2002; Bee et al. 2010). Different acoustic parameters from the same call are semi-independent and might encode distinct messages, thus evolving under differing selective pressures (Gerhardt and Huber 2002; Ryan and Kime 2003). Therefore, a broad comprehension of variability at different levels enables the proposition of various hypotheses about the evolutionary mechanisms that led to the present acoustic diversity. In general, variation in acoustic signals can be related to pleiotropic effects (Podos 2001), stochastic processes (GoicoecheaDraft et al. 2010), natural selection (Ryan et al. 1990; Röhr et al. 2020), and sexual selection (Gerhardt 2005). For anurans, pleiotropic effects of morphology and physiology are exemplified by the well-known influence of body size and temperature on acoustic parameters. The size of the vocal apparatus usually affects spectral parameters, while temperature often influences temporal characteristics of the calls (Gerhardt 1994). Such relationships can affect the variability of different acoustic parameters at different levels. For example, acoustic parameters that are more dependent on temperature should vary more, especially intra-individually and in a shorter time scale. At the same time, parameters that are highly dependent on morphology should be more stereotyped, with most of the variation occurring at levels above individuals or ontogenetically. Therefore, it is important to carefully consider the influence of temperature and body size in any bioacoustic study. Stochastic processes also affect the evolution and variability of acoustic signals. For anurans, these effects are tested by evaluating the geographic variation of acoustic parameters (Pröhl et al. 2007) or the effect of phylogeny on inter-specific variation (Goicoechea
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