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Distinguishing females of capuchino seedeaters: call repertoires provide evidence for species-level diagnosis

Distinguishing females of capuchino seedeaters: call repertoires provide evidence for... Revista Brasileira de Ornitologia 27(2): 70–78. ARTICLE June 2019 Distinguishing females of capuchino seedeaters: call repertoires provide evidence for species-level diagnosis 1,2 1 Márcio Repenning & Carla Suertegaray Fontana Laboratório de Ornitologia, Museu de Ciências e Tecnologia, Programa de Pós-graduação em Ecologia e Evolução da Biodiversidade, Pontifícia Universidade Católica do Rio Grande do Sul, PUCRS, Porto Alegre, RS, Brazil. Corresponding author: mrepenning@gmail.com Received on 17 September 2018. Accepted on 03 May 2019. ABSTRACT: Reliable identification of cryptic Neotropical capuchino seedeater females remains as a recurrent and non-trivial issue in field ornithology. Even in the hand, capuchino females cannot be accurately diagnosed to the species level based solely on visual plumage examination, which may present a problem for future research on this group. During 10 years of field resear ch on this group, we observed subtle vocal differences. We studied females of two parapatric species that may bree d in syntopic upland grassland areas in southern Brazil: Tawny-bellied Seedeater Sporophila hypoxantha and Black-bellied Seedeater Sporophila melanogaster. Our main aim was to measure dissimilarities between inter-specific and intersexual repertory calls. We found unequivocal inter-specific divergences in call type repertoires revealed by cluster analysis, and no intersexual differences in the co-specific repertoire calls. These combined results enhance the understanding about the role of repertoire calls on species-specific re cognition and interbreeding isolation processes (assortative mating), and provide a way to overcome the problem of field i dentification of female capuchinos at the species level. KEY-WORDS: acoustic communication, assortative mating, bioacoustic, songbirds, Sporophila, vocal repertory. INTRODUCTION visual observation (Sick 1963 & 1967, Short-Jr. 1969, Ouellet 1992, Areta 2008, Repenning et al. 2010b, Areta Females of the Neotropical genus Sporophila are very et al. 2011, Areta & Repenning 2011). cryptic, which has limited field resear ch in this group. The Despite improvements in our knowledge of the absence of morphological divergence and a uniform dull taxonomy and ecology of Sporophila species in the last brownish plumage, which is common among females in decade, the diagnosis of females remains uncertain. A this genus, make the study of this group very challenging single attempt to find a differentiation among females of (Meyer de Schauensee 1952, Ridgely & Tudor 1989, capuchino species was based on the wavelength reflected Ouellet 1992, Sick 1997, Areta et al. 2011, Rising et al. from their plumage, which did not refute the hypothesis 2011). of simply the limitation of human vision (Benites et al. Currently, there are ten Sporophila (i.e., capuchino) 2010). However, researcher has yet to resolve the subject seedeater species, all derived from a common ancestor of species-level diagnosis of female capuchino. As a result, (Campagna et al. 2015, Di Giacomo & Kopuchian there is still no detailed analysis to objectively determine 2016). Species within this clade vary little in morphology female capuchino, perhaps because of our sensorial and size and are notably sexually dimorphic in the limitations in detecting and assimilating the slight coloration of their plumage, with males typically being differences in their voices. Conversely, based on previous colorful while females are brownish (Ridgely & Tudor experience, we suspect that female call types differ among 1989). Despite inter-specific differences based on adult species. We believe that the ability to successfully identify male plumage and song, genomic variation between capuchino female's voice would open a new window capuchino seedeaters is minimal (Campagna et al. 2017), into research on the behavioral ecology, evolution and exemplifying the recent radiation of this Neotropical taxonomy of Neotropical seedeaters (Odom & Benedict passerines (e.g., Campagna et al. 2010, Burns et al. 2014). 2018). Additionally, it could have positive implications As incipient species, some inconsistencies exist in the for the conservation of threatened species of capuchinos, identification of the capuchinos: hybridization, aberrant helping authorities identify specimens in female plumage plumages, color morphs, individual and seasonal variation that are confiscated from the illegal pet trade (e.g., females, of plumage color, and lack of diagnosis of the female by first year males and males in complete “eclipse” plumage). Revista Brasileira de Ornitologia 27(2): 2019 Species-level diagnosis of capuchino seedeater females Repenning & Fontana METHODS Besides the importance of making the correct diagnosis of Sporophila females at the species level in the field, mapping their sex-specific voi ce repertoires Study species and site would provide a new approach to study species-specific recognition and assortative mating (Paterson 1985, We studied two long-distance migratory species of the capuchino group: Tawny-bellied Seedeater Sporophila Slabbekoorn & Smith 2002). Sexual selection that operates on traits used to transmit information to rivals hypoxantha, and Black-bellied Seedeater Sporophila and potential mates is an important driver in the evolution melanogaster. These species segregate spatially from each of passerines (Irwin et al. 2000). Sporophila capuchinos, other throughout an environmental gradient (altitude besides using visual signals, may use simple vocal signals as and habitat) in the inner Planalto Meridional Brasileiro (Repenning et al. 2010a; Fig. 1). Sporophila melanogaster premating barriers, thus maintaining differences between incipient species (Price 2008). is common in the highest eastern grasslands (average Here, we present a new way to diagnose visually 1000 m a.s.l.) and S. hypoxantha occurs in western valleys indistinguishable capuchino females. We studied two or at lower altitudes. They are the smallest among the migratory capuchino species, Tawny-bellied Seedeater and Sporophila seedeaters species with total length of ~98.0 mm and a body mass of ~8.8 g (Franz & Fontana 2013, Black-bellied Seedeater, which breed mostly in allopatry and also in narrow contact zones in southern Brazilian Fontana & Repenning 2014). The distinguishable grasslands (Repenning et al. 2010a). Our main aim was plumage color of the adult male in breeding season was to evaluate whether capuchino females that are members the primary criteria for the selection of these two species, of closely-related species differ vocally when breeding in because the unequivocal diagnosis of males was an assumption for this study. contact zones. To address that question, we aimed to (1) provide an objective method for species-level diagnosis Current knowledge about the pattern of the of Sporophila females, testing for differences in the breeding ranges of both species was secondarily relevant. repertories of calls; and (2) tested whether there is intra- We carried out 10 years (2008–2018) of fieldwork in specific, sex-based variation in contact call repertoires. broad upland grassland localities in southern Brazil, including breeding areas of complete allopatry and areas Finally, we discuss the role of calls in assortative mating in the genus Sporophila. of syntopy of both species, across five c ontact zone areas (Fig. 1, Table S1). Figure 1. Breeding range of Sporophila melanogaster (solid black line) and S. hypoxantha (grey polygons) in the southern Brazilian highlands. Hachured polygons are five areas identified in situ as contact (hybrid) zones. Distributional limits were inferred based on a potential distribution estimates model, using the author's bird nesting records (Fig. S1 & S2). Revista Brasileira de Ornitologia 27(2): 2019 Species-level diagnosis of capuchino seedeater females Repenning & Fontana Definitions is an efficient way to measure similarities between short vocal elements over time and recorded sound quality with Allopatric areas are the localities where only males of regard to signal-to-noise contrast (Bioacoustic Research pure phenotype (plumage and song) of each species Program 2004). We assumed that pairs of call types had were recorded breeding. The contact (hybridization or the same sound element or note correlation when they introgression) zones are the areas in which we recorded had values higher than 0.7. Definition of sound units nesting activity of coupled males of both species with may be difficult due to the characteristic of continuity a breeding territory in contiguous areas, and breeding or discontinuity of each typical vocal element in oscine simultaneously, i.e., in syntopy. Males with a non-pure passerines (Lynch 1996). Therefore, we used analytical phenotype were also documented in these syntopic tools in a complementary way, aiming to reduce subjectivity areas, suggesting some level of introgression of plumage regarding the discrete limits of each vocal element (Horn characteristics. We recorded some of these males, but we & Falls 1996). Classic experiments have shown that the did not include them in the sound analysis. shape note or syllable within the repertoire in passerines can be a functional signal, with a more important role in Field recording and alarm call behavior species-specific re cognition than syntax or the structural characteristics of the voices (Bremond 1976, Catchpole The recor ding of capuchino female songs occurred after a & Slater 2008). Hence, understanding the extension of rigorous identification of the social mate of each female, the similarity of call repertoires would allow us to assess by observing mate-guarding behavior. Only recordings of the role of acoustic communication on assortative mating females that were associated with evidence of breeding among closely-related capuchino species. (e.g., incubating, taking care of nestlings or newly An evaluation of the scanned recordings was based fledglings) were considered. We recor ded vocalizations on an analysis of the spectrogram, using a frequency under a standardized close range to the focal bird (~10– resolution of 172 Hz and a time resolution of 2.3 ms, 15 m) using Sony TC-D5M recorder and Nagra LB, generated with RAVEN Pro 1.5 software. We selected Tascam DR-680 or Sony PCM-D50 digital recorders, individual call types automatically (Band Limiter Energy with Sennheiser ME66 or ME62 external microphones Detector - BLED) using the following configuration: associated with a Telinga parabola (21.5in/6.1in). All minimum frequency of 1076 Hz, maximum of 6696 Hz, sounds recorded will be archived at the Macaulay Library minimum duration of 0.0243 s, maximum of 0.855 s of Natural Sounds (e.g., ML111751281), Cornell Lab. of and a minimum separation of 0.0087 s in Target Signal Ornithology (Ithaca, NY). Territorial males and females Parameters. Other parameters followed the default were captured with an Ecotone mist net (16/20 mm) for configuration. After the detector interaction, another color and metal banding. We banded all birds caught visual review was carried out to certify that heterospecific for individual identification and to prevent sample notes were not selected. This procedure was applied for replication (Roos 2010). each recorded individual. Lastly, each call type was labeled directly in a BLEDs interaction result table. Sound processing and call definitions Statistical analysis We consider a call type the unity of sounds that can be constituted by a single long note, a short note or syllables, The recor ding sample available for analyses comprised i.e. a building block of songs or a regularly grouped a total of 1021 and 527 selected call types recorded in combination of multiple whistled notes produced as a allopatry and syntopy, respectively, for S. hypoxantha (n common unit (Baptista 1996, Hagemeyer et al. 2012). = 32 females, n = 24 males), and 946 and 481 selected The very fast (shorter) calls we named chirps. We first call types recorded in allopatry and syntopy, respectively, classified each call type based on visual inspection of of S. melanogaster (n = 25 females, n = 16 males). discrete categories under the temporal-spectral shape of Frequency contour measurements were designed through the spectrogram. Calls were assumed as the same type spectrogram pitch tracking, which uses the dominant when they were consistently equivalent in duration and frequency value of a sound over time. The chosen tool frequency range, in their starting and ending frequencies, to do this was the Frequency Contour Percentile 50% and in their frequencies at inflection points (Hagemeyer (Hz) which selects the frequency values (Y axis) through et al. 2012). Secondly, we built a reference collection time (X axis), and amplitude (Z axis = grayscale in the with labeled sequential call types. For calls that were spectrogram). more difficult to discriminate, the Cross-Correlation A distance matrix was built using aligned call types, analysis was also used, and slow-speed playback was used in which each column represents a set of calls from a to help solving specific doubts. Such an analytical tool unique specimen. Each call type represents a sequential Revista Brasileira de Ornitologia 27(2): 2019 Species-level diagnosis of capuchino seedeater females Repenning & Fontana pitch frequency (shape note) set of values, i.e., frequency S. hypoxantha having an average of 6 (4–9) and 7 (3–8) contour measurements (Hz). We ran Bray-Curtis Cluster call types, respectively. Also, females of S. melanogaster Analysis (Single Link) in BioDiversity Pro (McAleece and S. hypoxantha often issued fast calls, with two and 1997). Only specimens with a bias to stabilize the three chirps, respectively. Some calls were produced by repertoire were analyzed. For each individual we used almost every female (e.g., calls 4, 6 and 8 of S. hypoxantha, an average of three calls of each call type, aiming to and calls 14 and 16 of S. melanogaster). Some call types understand the extent of intra-individual variation in (e.g., 1 and 18; Fig. 3) were rarely produced by females calls. After assessing this variation in calls and realizing of either species. Female call types corresponded to male that it was smaller than that of the inter-individual calls, call type repertoire in both species. Nevertheless, male S. we selected only one call type to describe the individual melanogaster calls have two notes that are absent in the repertoire that was used in the final similarity analysis. repertoires of co-specific females (e.g., call types 19 and 20) (Fig. 3). RESULTS Intra and inter-specific repertoire variation Repertoire accumulation The cluster analysis of male and female S. melanogaster and S. hypoxantha repertoires revealed a dichotomy of The time over which t he call types were revealed in species-level call repertoires (Fig. 4). We did not find any successive voice recordings for each female is illustrated shared calls in the repertories of either species, even in the in Fig. 2. Female call type accumulation curves reached syntopic population. Additionally, no female coupled with an asymptote in approximately 12 to 25 of the recorded a S. melanogaster male presented a repertoire of pure call calls. There was also variation in the rate in which females types exhibited by S. hypoxantha, or vice versa. We found produced different call types, with some females exhibiting no intersexual divergence in call types because males and the full repertoire within the first eight recor ded calls, females did not present a clear intra-specific sub-cluster whereas others required more than 30 calls to present and within the two larger clusters observed for S. melanogaster equivalent-sized call type repertoire (Fig. 2). and S. hypoxantha (Fig. 4). Finally, we found that note types used by males in advertising songs were also used Female call type repertoire as contact/alarm calls by their co-specific females (S. melanogaster males [songs] and females [call repertory] The size of call type repertoires was similar between shared 50% of note types and S. hypoxantha males [songs] both species, with each female of S. melanogaster and and females [call repertory] shared 43%; Fig. 3). Figure 2. Call type repertoire size and accumulation functions for each individual in the sample of female Sporophila hypoxantha (n = 35, A) and S. melanogaster (n = 26, B) from allopatric and syntopic breeding areas in the southern Brazilian highlands. Each line represents a different female. Revista Brasileira de Ornitologia 27(2): 2019 Species-level diagnosis of capuchino seedeater females Repenning & Fontana Figure 3. Call type repertoires for Sporophila melanogaster and S. hypoxantha in breeding areas in the southern Brazilian highlands. Call types are labeled by ordinal numerals and chirps with a “C” associated with a numeral (see mp3 files in supporting information). (A) Breeding females of S. hypoxantha in formative plumage and (B) definitive plumage; (C) S. melanogaster in formative plumage and (D) definitive plumage. Definitive plumage: typical adult male S. hypoxantha (left) and S. melanogaster (right). Revista Brasileira de Ornitologia 27(2): 2019 Species-level diagnosis of capuchino seedeater females Repenning & Fontana Figure 4. Similarities between the call type repertoires of Sporophila melanogaster and S. hypoxantha females and males of breeding populations in southern Brazil, based on Bray-Curtis Cluster Analysis. DISCUSSION We observed few changes in the shape of notes, but found no cogent cluster that suggest sexual differentiation. The sound degradation hypothesis can explain the subtle We provide the first substantial evidence that voices are variations in calls between the sexes in passerines (Searcy useful for species-level determination of female capuchino seedeaters in the field, as supported by several lines of & Brenowitz 1988, Ratcliffe & Otter 1996, Collins evidence. First, we found no sharing (introgression) in 1999). This phenomenon has been reported for songs call type repertoires of females of S. melanogaster and S. of S. melanogaster and S. hypoxantha when temporal variation was documented in note types (Repenning et hypoxantha. Second, males and females of both species al. 2010b, Areta & Repenning 2011). Conservatively, it use the same call type repertoire as contact voices. Finally, call type repertoires seem to be a more stable signal than makes sense that sound degradation in capuchino calls color plumage patterns in females and males of these two should occur in parallel in both sexes, especially because species (pers. obs.). of the preserved homology in their note shapes over time. Revista Brasileira de Ornitologia 27(2): 2019 Species-level diagnosis of capuchino seedeater females Repenning & Fontana We highlight that results presented in this study (Baptista 1996). Capuchino call types could be innate are a more reliable and less complex way to discriminate elements (begging calls that develop into social calls) between species of capuchino females than previous of their vocalization or inherently learnt from their co- attempts, which involved visually modeling UV- specific calls (Groth 1993, Hughes et al. 1998, Riebel wavelength separation (Benites et al. 2010), and which 2003). In addition, a considerable number of female is operationally complex. Additionally, we observed call types (half) are composed of advertising male song. evidence of variation in the extent of female plumage These traits may be favorable to transmit species-specific coloration (primarily by age) within these capuchino sound signals long distances, when the breeding season species. When comparing first-year females (formative starts (Riebel 2003, Catchpole & Slater 2008). These plumage) of S. melanogaster and S. hypoxantha, they vocal systems seem to contribute to a favorable co-specific look more similar to each other than when comparing acoustic environment in the process of assortative mating a first-year female with a co-specific female in a different (Béguin et al. 1998, Baptista & Kroodsma 2001). This plumage cycle (e.g., formative vs. definitive plumage) (Fig. scenario would induce birds to breed near their natal 3). This observation illustrates the complexity of relying areas because oscine female sexual imprinting occurs on on the use of plumage parameters for identification of familiar songs of her natal population (Irwin & Price capuchino females. Concerning plumage similarities, 1999, Nelson 2000, MacDougall-Shackleton et al. 2001). we also highlight that there is evidence showing that Which signals would be more important in isolating the measurement of plumage color reflectance in the populations or species? This is a recurrent question in laboratory/museum may be less reliable as compared to studies on the evolution of prezygotic isolation (Brelsford that on live birds captured in the field (Doucet & Hill & Irwin 2009). For capuchino seedeaters, contact calls 2009, Hubbard et al. 2017). are likely to play a key role in the isolation process, In comparison, with some experience (i.e., an since they are more concordant and stable signals for ability to distinguish between capuchino calls), one can communication between them. Vocal communication widely improve their ability to detect and identify visually appears to be the first signal during the species-specific identical females in the field. However, un like the relatively mate recognition process among capuchino seedeaters, pure, long and very distinctive capuchino male songs, since concordance in voice might influence females to female contact calls across species are very short and may select males that sing dialects of the female's birthplace. sound extremely similar to the human ear. Hence, the Moreover, the quality or differences of male plumage sonogram is a valuable tool for seeing and, in turn, hearing coloration could be a secondary visual signal, more the complexities of these short vocalizations. In addition, associated with male-male competition (Searcy & using slow-speed playback appeared effec tive to learn how Nowicki 2000, Byers & Kroodsma 2009) in the process to listen to the very fast pitch changes of the vocalizations. of intra-specific sexual selection. Paradoxi cally, we By following such steps in the process of sound analysis, highlight that vocal and male plumage divergences did we will enhance our understanding of the extension of co- not completely prevent interbreeding between these two specific communication of the studied species, and even species, because putative hybrid males have been recorded that of other capuchino species that are diffic ult to identify. in contact zones. Nevertheless, we attribute rape behavior We found that females of each species have fully as the primary cause of interbreeding between these two distinct contact call types, and as do males, females of species, which has been occasionally observed in areas of different species sing different songs (Repenning et al. syntopy (pers. obs.). 2010b). Although we initially suspected there was a Finally, based on strong evidence of differentiation certain degree of introgression in the S. hypoxantha and among closely-related capuchino females, we suggest S. melanogaster voice elements, it was not confirmed rigorous field song-c all recording followed by spectrogram even in syntopic populations. Additionally, we did not analyses of the call type repertoires for species-level find females with a repertoire of S. melanogaster coupled diagnosis and to solve the cryptic female discrimination with S. hypoxantha males or vice versa, revealing there is problem. Our analysis, in addition to visual modeling for nonrandom mating (Servedio 2004). This observation reflec tance quantific ation of female plumage (Benites et al. suggests that capuchinos present positive assortative 2010), reinforces the human sensorial limitation bias for mating with concordant intra-specific, sex-based call type accurately distinguishing capuchino females. We encourage repertoires and no mixed pairing (Randler 2002). In this a similar evaluation for other species or populations scenario, social calls should play an important role in of capuchino seedeaters with independent trajectories specific mate recognition between recently diverged taxa and ongoing speciation across a wide geographic area as (Searby & Jouventin 2004). possible. Populations also  can be identified by their call The relationships between songs and calls and notes, as in other oscine passerines (Groth 1993), even how song is derived from calls varies among songbirds when they are in their wintering areas (Areta 2012). Revista Brasileira de Ornitologia 27(2): 2019 Species-level diagnosis of capuchino seedeater females Repenning & Fontana Bremond J.C. 1976. Specific re cognition in the song of Bonelli's The improvement of this kind of resear ch would Warbler (Phylloscopus bonelli). Behaviour 58: 99–116. have positive implications for taxonomy, evolutionary Burns K.J., Shultz A.J., Title P.O., Mason N.A., Barker F.K., and behavioral ecology studies in Neotropical seedeaters. Klicka J., Lanyon S.M. & Lovette I.J. 2014. Phylogenetics and From a conservation perspective, the identification of diversification of tanagers (Passeriformes: Thraupidae), the largest species-specific calls and songs can be a useful tool for radiation of Neotropical songbirds. Molecular Phylogenetics and Evolution 75: 41–77. conservation of threatened capuchino species, since it can Byers B.E. & Kroodsma D.E. 2009. Female mate choice and songbird help in the identification of specimens illegally captured song repertoires. Animal Behaviour 77: 13–22. in nature and in female-like plumage. Campagna L., Lijtmaer D.A., Kerr K.C.R., Barreira A.S., Hebert P.D.N., Lougheed S.C. & Tubaro P.L. 2010. DNA barcodes provide new evidence of a recent radiation in the genus Sporophila (Aves: Passeriformes). Molecular Ecology Resources 10: 449–458. ACKNOWLEDGEMENTS Campagna L., Gronau I., Silveira L.F., Siepel A. & Lovette I.J. 2015. Distinguishing noise from signal in patterns of genomic We thank the Brazilian Federal Agencies (CNPq and divergence in a highly polymorphic avian radiation. Molecular CAPES) for a scholarship to M.R. and funds to CSF, and Ecology 24: 4238–4251. Campagna L., Repenning M., Silveira L.F., Fontana C.S., Tubaro P.L. Fundação Grupo Boticário de Proteção à Natureza (FBPN- & Lovette I.J. 2017. Repeated divergent selection on pigmentation project No. 0795-20082) and Neotropical Grassland genes in a rapid finch radiation. Science A dvances 3: e1602404. 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Rio de Janeiro: Nova Fronteira. morph of  Sporophila Seedeater from capuchinos group (Aves, Slabbekoorn H. & Smith T.B. 2002. Bird song, ecology and Emberizidae). Iheringia: Série Zoologia 100: 369–378. speciation. Philosophical Transactions of the Royal Society of London Ridgely R.S. & Tudor G. 1989. The bir ds of South America, v. 1. B: Biological Sciences 357: 493–503. Austin: University of Texas Press. Riebel K. 2003. The “mute” sex revisited: vocal production and Associate Editor: Gustavo S. Cabanne. Revista Brasileira de Ornitologia 27(2): 2019 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Ornithology Research Springer Journals

Distinguishing females of capuchino seedeaters: call repertoires provide evidence for species-level diagnosis

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Revista Brasileira de Ornitologia 27(2): 70–78. ARTICLE June 2019 Distinguishing females of capuchino seedeaters: call repertoires provide evidence for species-level diagnosis 1,2 1 Márcio Repenning & Carla Suertegaray Fontana Laboratório de Ornitologia, Museu de Ciências e Tecnologia, Programa de Pós-graduação em Ecologia e Evolução da Biodiversidade, Pontifícia Universidade Católica do Rio Grande do Sul, PUCRS, Porto Alegre, RS, Brazil. Corresponding author: mrepenning@gmail.com Received on 17 September 2018. Accepted on 03 May 2019. ABSTRACT: Reliable identification of cryptic Neotropical capuchino seedeater females remains as a recurrent and non-trivial issue in field ornithology. Even in the hand, capuchino females cannot be accurately diagnosed to the species level based solely on visual plumage examination, which may present a problem for future research on this group. During 10 years of field resear ch on this group, we observed subtle vocal differences. We studied females of two parapatric species that may bree d in syntopic upland grassland areas in southern Brazil: Tawny-bellied Seedeater Sporophila hypoxantha and Black-bellied Seedeater Sporophila melanogaster. Our main aim was to measure dissimilarities between inter-specific and intersexual repertory calls. We found unequivocal inter-specific divergences in call type repertoires revealed by cluster analysis, and no intersexual differences in the co-specific repertoire calls. These combined results enhance the understanding about the role of repertoire calls on species-specific re cognition and interbreeding isolation processes (assortative mating), and provide a way to overcome the problem of field i dentification of female capuchinos at the species level. KEY-WORDS: acoustic communication, assortative mating, bioacoustic, songbirds, Sporophila, vocal repertory. INTRODUCTION visual observation (Sick 1963 & 1967, Short-Jr. 1969, Ouellet 1992, Areta 2008, Repenning et al. 2010b, Areta Females of the Neotropical genus Sporophila are very et al. 2011, Areta & Repenning 2011). cryptic, which has limited field resear ch in this group. The Despite improvements in our knowledge of the absence of morphological divergence and a uniform dull taxonomy and ecology of Sporophila species in the last brownish plumage, which is common among females in decade, the diagnosis of females remains uncertain. A this genus, make the study of this group very challenging single attempt to find a differentiation among females of (Meyer de Schauensee 1952, Ridgely & Tudor 1989, capuchino species was based on the wavelength reflected Ouellet 1992, Sick 1997, Areta et al. 2011, Rising et al. from their plumage, which did not refute the hypothesis 2011). of simply the limitation of human vision (Benites et al. Currently, there are ten Sporophila (i.e., capuchino) 2010). However, researcher has yet to resolve the subject seedeater species, all derived from a common ancestor of species-level diagnosis of female capuchino. As a result, (Campagna et al. 2015, Di Giacomo & Kopuchian there is still no detailed analysis to objectively determine 2016). Species within this clade vary little in morphology female capuchino, perhaps because of our sensorial and size and are notably sexually dimorphic in the limitations in detecting and assimilating the slight coloration of their plumage, with males typically being differences in their voices. Conversely, based on previous colorful while females are brownish (Ridgely & Tudor experience, we suspect that female call types differ among 1989). Despite inter-specific differences based on adult species. We believe that the ability to successfully identify male plumage and song, genomic variation between capuchino female's voice would open a new window capuchino seedeaters is minimal (Campagna et al. 2017), into research on the behavioral ecology, evolution and exemplifying the recent radiation of this Neotropical taxonomy of Neotropical seedeaters (Odom & Benedict passerines (e.g., Campagna et al. 2010, Burns et al. 2014). 2018). Additionally, it could have positive implications As incipient species, some inconsistencies exist in the for the conservation of threatened species of capuchinos, identification of the capuchinos: hybridization, aberrant helping authorities identify specimens in female plumage plumages, color morphs, individual and seasonal variation that are confiscated from the illegal pet trade (e.g., females, of plumage color, and lack of diagnosis of the female by first year males and males in complete “eclipse” plumage). Revista Brasileira de Ornitologia 27(2): 2019 Species-level diagnosis of capuchino seedeater females Repenning & Fontana METHODS Besides the importance of making the correct diagnosis of Sporophila females at the species level in the field, mapping their sex-specific voi ce repertoires Study species and site would provide a new approach to study species-specific recognition and assortative mating (Paterson 1985, We studied two long-distance migratory species of the capuchino group: Tawny-bellied Seedeater Sporophila Slabbekoorn & Smith 2002). Sexual selection that operates on traits used to transmit information to rivals hypoxantha, and Black-bellied Seedeater Sporophila and potential mates is an important driver in the evolution melanogaster. These species segregate spatially from each of passerines (Irwin et al. 2000). Sporophila capuchinos, other throughout an environmental gradient (altitude besides using visual signals, may use simple vocal signals as and habitat) in the inner Planalto Meridional Brasileiro (Repenning et al. 2010a; Fig. 1). Sporophila melanogaster premating barriers, thus maintaining differences between incipient species (Price 2008). is common in the highest eastern grasslands (average Here, we present a new way to diagnose visually 1000 m a.s.l.) and S. hypoxantha occurs in western valleys indistinguishable capuchino females. We studied two or at lower altitudes. They are the smallest among the migratory capuchino species, Tawny-bellied Seedeater and Sporophila seedeaters species with total length of ~98.0 mm and a body mass of ~8.8 g (Franz & Fontana 2013, Black-bellied Seedeater, which breed mostly in allopatry and also in narrow contact zones in southern Brazilian Fontana & Repenning 2014). The distinguishable grasslands (Repenning et al. 2010a). Our main aim was plumage color of the adult male in breeding season was to evaluate whether capuchino females that are members the primary criteria for the selection of these two species, of closely-related species differ vocally when breeding in because the unequivocal diagnosis of males was an assumption for this study. contact zones. To address that question, we aimed to (1) provide an objective method for species-level diagnosis Current knowledge about the pattern of the of Sporophila females, testing for differences in the breeding ranges of both species was secondarily relevant. repertories of calls; and (2) tested whether there is intra- We carried out 10 years (2008–2018) of fieldwork in specific, sex-based variation in contact call repertoires. broad upland grassland localities in southern Brazil, including breeding areas of complete allopatry and areas Finally, we discuss the role of calls in assortative mating in the genus Sporophila. of syntopy of both species, across five c ontact zone areas (Fig. 1, Table S1). Figure 1. Breeding range of Sporophila melanogaster (solid black line) and S. hypoxantha (grey polygons) in the southern Brazilian highlands. Hachured polygons are five areas identified in situ as contact (hybrid) zones. Distributional limits were inferred based on a potential distribution estimates model, using the author's bird nesting records (Fig. S1 & S2). Revista Brasileira de Ornitologia 27(2): 2019 Species-level diagnosis of capuchino seedeater females Repenning & Fontana Definitions is an efficient way to measure similarities between short vocal elements over time and recorded sound quality with Allopatric areas are the localities where only males of regard to signal-to-noise contrast (Bioacoustic Research pure phenotype (plumage and song) of each species Program 2004). We assumed that pairs of call types had were recorded breeding. The contact (hybridization or the same sound element or note correlation when they introgression) zones are the areas in which we recorded had values higher than 0.7. Definition of sound units nesting activity of coupled males of both species with may be difficult due to the characteristic of continuity a breeding territory in contiguous areas, and breeding or discontinuity of each typical vocal element in oscine simultaneously, i.e., in syntopy. Males with a non-pure passerines (Lynch 1996). Therefore, we used analytical phenotype were also documented in these syntopic tools in a complementary way, aiming to reduce subjectivity areas, suggesting some level of introgression of plumage regarding the discrete limits of each vocal element (Horn characteristics. We recorded some of these males, but we & Falls 1996). Classic experiments have shown that the did not include them in the sound analysis. shape note or syllable within the repertoire in passerines can be a functional signal, with a more important role in Field recording and alarm call behavior species-specific re cognition than syntax or the structural characteristics of the voices (Bremond 1976, Catchpole The recor ding of capuchino female songs occurred after a & Slater 2008). Hence, understanding the extension of rigorous identification of the social mate of each female, the similarity of call repertoires would allow us to assess by observing mate-guarding behavior. Only recordings of the role of acoustic communication on assortative mating females that were associated with evidence of breeding among closely-related capuchino species. (e.g., incubating, taking care of nestlings or newly An evaluation of the scanned recordings was based fledglings) were considered. We recor ded vocalizations on an analysis of the spectrogram, using a frequency under a standardized close range to the focal bird (~10– resolution of 172 Hz and a time resolution of 2.3 ms, 15 m) using Sony TC-D5M recorder and Nagra LB, generated with RAVEN Pro 1.5 software. We selected Tascam DR-680 or Sony PCM-D50 digital recorders, individual call types automatically (Band Limiter Energy with Sennheiser ME66 or ME62 external microphones Detector - BLED) using the following configuration: associated with a Telinga parabola (21.5in/6.1in). All minimum frequency of 1076 Hz, maximum of 6696 Hz, sounds recorded will be archived at the Macaulay Library minimum duration of 0.0243 s, maximum of 0.855 s of Natural Sounds (e.g., ML111751281), Cornell Lab. of and a minimum separation of 0.0087 s in Target Signal Ornithology (Ithaca, NY). Territorial males and females Parameters. Other parameters followed the default were captured with an Ecotone mist net (16/20 mm) for configuration. After the detector interaction, another color and metal banding. We banded all birds caught visual review was carried out to certify that heterospecific for individual identification and to prevent sample notes were not selected. This procedure was applied for replication (Roos 2010). each recorded individual. Lastly, each call type was labeled directly in a BLEDs interaction result table. Sound processing and call definitions Statistical analysis We consider a call type the unity of sounds that can be constituted by a single long note, a short note or syllables, The recor ding sample available for analyses comprised i.e. a building block of songs or a regularly grouped a total of 1021 and 527 selected call types recorded in combination of multiple whistled notes produced as a allopatry and syntopy, respectively, for S. hypoxantha (n common unit (Baptista 1996, Hagemeyer et al. 2012). = 32 females, n = 24 males), and 946 and 481 selected The very fast (shorter) calls we named chirps. We first call types recorded in allopatry and syntopy, respectively, classified each call type based on visual inspection of of S. melanogaster (n = 25 females, n = 16 males). discrete categories under the temporal-spectral shape of Frequency contour measurements were designed through the spectrogram. Calls were assumed as the same type spectrogram pitch tracking, which uses the dominant when they were consistently equivalent in duration and frequency value of a sound over time. The chosen tool frequency range, in their starting and ending frequencies, to do this was the Frequency Contour Percentile 50% and in their frequencies at inflection points (Hagemeyer (Hz) which selects the frequency values (Y axis) through et al. 2012). Secondly, we built a reference collection time (X axis), and amplitude (Z axis = grayscale in the with labeled sequential call types. For calls that were spectrogram). more difficult to discriminate, the Cross-Correlation A distance matrix was built using aligned call types, analysis was also used, and slow-speed playback was used in which each column represents a set of calls from a to help solving specific doubts. Such an analytical tool unique specimen. Each call type represents a sequential Revista Brasileira de Ornitologia 27(2): 2019 Species-level diagnosis of capuchino seedeater females Repenning & Fontana pitch frequency (shape note) set of values, i.e., frequency S. hypoxantha having an average of 6 (4–9) and 7 (3–8) contour measurements (Hz). We ran Bray-Curtis Cluster call types, respectively. Also, females of S. melanogaster Analysis (Single Link) in BioDiversity Pro (McAleece and S. hypoxantha often issued fast calls, with two and 1997). Only specimens with a bias to stabilize the three chirps, respectively. Some calls were produced by repertoire were analyzed. For each individual we used almost every female (e.g., calls 4, 6 and 8 of S. hypoxantha, an average of three calls of each call type, aiming to and calls 14 and 16 of S. melanogaster). Some call types understand the extent of intra-individual variation in (e.g., 1 and 18; Fig. 3) were rarely produced by females calls. After assessing this variation in calls and realizing of either species. Female call types corresponded to male that it was smaller than that of the inter-individual calls, call type repertoire in both species. Nevertheless, male S. we selected only one call type to describe the individual melanogaster calls have two notes that are absent in the repertoire that was used in the final similarity analysis. repertoires of co-specific females (e.g., call types 19 and 20) (Fig. 3). RESULTS Intra and inter-specific repertoire variation Repertoire accumulation The cluster analysis of male and female S. melanogaster and S. hypoxantha repertoires revealed a dichotomy of The time over which t he call types were revealed in species-level call repertoires (Fig. 4). We did not find any successive voice recordings for each female is illustrated shared calls in the repertories of either species, even in the in Fig. 2. Female call type accumulation curves reached syntopic population. Additionally, no female coupled with an asymptote in approximately 12 to 25 of the recorded a S. melanogaster male presented a repertoire of pure call calls. There was also variation in the rate in which females types exhibited by S. hypoxantha, or vice versa. We found produced different call types, with some females exhibiting no intersexual divergence in call types because males and the full repertoire within the first eight recor ded calls, females did not present a clear intra-specific sub-cluster whereas others required more than 30 calls to present and within the two larger clusters observed for S. melanogaster equivalent-sized call type repertoire (Fig. 2). and S. hypoxantha (Fig. 4). Finally, we found that note types used by males in advertising songs were also used Female call type repertoire as contact/alarm calls by their co-specific females (S. melanogaster males [songs] and females [call repertory] The size of call type repertoires was similar between shared 50% of note types and S. hypoxantha males [songs] both species, with each female of S. melanogaster and and females [call repertory] shared 43%; Fig. 3). Figure 2. Call type repertoire size and accumulation functions for each individual in the sample of female Sporophila hypoxantha (n = 35, A) and S. melanogaster (n = 26, B) from allopatric and syntopic breeding areas in the southern Brazilian highlands. Each line represents a different female. Revista Brasileira de Ornitologia 27(2): 2019 Species-level diagnosis of capuchino seedeater females Repenning & Fontana Figure 3. Call type repertoires for Sporophila melanogaster and S. hypoxantha in breeding areas in the southern Brazilian highlands. Call types are labeled by ordinal numerals and chirps with a “C” associated with a numeral (see mp3 files in supporting information). (A) Breeding females of S. hypoxantha in formative plumage and (B) definitive plumage; (C) S. melanogaster in formative plumage and (D) definitive plumage. Definitive plumage: typical adult male S. hypoxantha (left) and S. melanogaster (right). Revista Brasileira de Ornitologia 27(2): 2019 Species-level diagnosis of capuchino seedeater females Repenning & Fontana Figure 4. Similarities between the call type repertoires of Sporophila melanogaster and S. hypoxantha females and males of breeding populations in southern Brazil, based on Bray-Curtis Cluster Analysis. DISCUSSION We observed few changes in the shape of notes, but found no cogent cluster that suggest sexual differentiation. The sound degradation hypothesis can explain the subtle We provide the first substantial evidence that voices are variations in calls between the sexes in passerines (Searcy useful for species-level determination of female capuchino seedeaters in the field, as supported by several lines of & Brenowitz 1988, Ratcliffe & Otter 1996, Collins evidence. First, we found no sharing (introgression) in 1999). This phenomenon has been reported for songs call type repertoires of females of S. melanogaster and S. of S. melanogaster and S. hypoxantha when temporal variation was documented in note types (Repenning et hypoxantha. Second, males and females of both species al. 2010b, Areta & Repenning 2011). Conservatively, it use the same call type repertoire as contact voices. Finally, call type repertoires seem to be a more stable signal than makes sense that sound degradation in capuchino calls color plumage patterns in females and males of these two should occur in parallel in both sexes, especially because species (pers. obs.). of the preserved homology in their note shapes over time. Revista Brasileira de Ornitologia 27(2): 2019 Species-level diagnosis of capuchino seedeater females Repenning & Fontana We highlight that results presented in this study (Baptista 1996). Capuchino call types could be innate are a more reliable and less complex way to discriminate elements (begging calls that develop into social calls) between species of capuchino females than previous of their vocalization or inherently learnt from their co- attempts, which involved visually modeling UV- specific calls (Groth 1993, Hughes et al. 1998, Riebel wavelength separation (Benites et al. 2010), and which 2003). In addition, a considerable number of female is operationally complex. Additionally, we observed call types (half) are composed of advertising male song. evidence of variation in the extent of female plumage These traits may be favorable to transmit species-specific coloration (primarily by age) within these capuchino sound signals long distances, when the breeding season species. When comparing first-year females (formative starts (Riebel 2003, Catchpole & Slater 2008). These plumage) of S. melanogaster and S. hypoxantha, they vocal systems seem to contribute to a favorable co-specific look more similar to each other than when comparing acoustic environment in the process of assortative mating a first-year female with a co-specific female in a different (Béguin et al. 1998, Baptista & Kroodsma 2001). This plumage cycle (e.g., formative vs. definitive plumage) (Fig. scenario would induce birds to breed near their natal 3). This observation illustrates the complexity of relying areas because oscine female sexual imprinting occurs on on the use of plumage parameters for identification of familiar songs of her natal population (Irwin & Price capuchino females. Concerning plumage similarities, 1999, Nelson 2000, MacDougall-Shackleton et al. 2001). we also highlight that there is evidence showing that Which signals would be more important in isolating the measurement of plumage color reflectance in the populations or species? This is a recurrent question in laboratory/museum may be less reliable as compared to studies on the evolution of prezygotic isolation (Brelsford that on live birds captured in the field (Doucet & Hill & Irwin 2009). For capuchino seedeaters, contact calls 2009, Hubbard et al. 2017). are likely to play a key role in the isolation process, In comparison, with some experience (i.e., an since they are more concordant and stable signals for ability to distinguish between capuchino calls), one can communication between them. Vocal communication widely improve their ability to detect and identify visually appears to be the first signal during the species-specific identical females in the field. However, un like the relatively mate recognition process among capuchino seedeaters, pure, long and very distinctive capuchino male songs, since concordance in voice might influence females to female contact calls across species are very short and may select males that sing dialects of the female's birthplace. sound extremely similar to the human ear. Hence, the Moreover, the quality or differences of male plumage sonogram is a valuable tool for seeing and, in turn, hearing coloration could be a secondary visual signal, more the complexities of these short vocalizations. In addition, associated with male-male competition (Searcy & using slow-speed playback appeared effec tive to learn how Nowicki 2000, Byers & Kroodsma 2009) in the process to listen to the very fast pitch changes of the vocalizations. of intra-specific sexual selection. Paradoxi cally, we By following such steps in the process of sound analysis, highlight that vocal and male plumage divergences did we will enhance our understanding of the extension of co- not completely prevent interbreeding between these two specific communication of the studied species, and even species, because putative hybrid males have been recorded that of other capuchino species that are diffic ult to identify. in contact zones. Nevertheless, we attribute rape behavior We found that females of each species have fully as the primary cause of interbreeding between these two distinct contact call types, and as do males, females of species, which has been occasionally observed in areas of different species sing different songs (Repenning et al. syntopy (pers. obs.). 2010b). Although we initially suspected there was a Finally, based on strong evidence of differentiation certain degree of introgression in the S. hypoxantha and among closely-related capuchino females, we suggest S. melanogaster voice elements, it was not confirmed rigorous field song-c all recording followed by spectrogram even in syntopic populations. Additionally, we did not analyses of the call type repertoires for species-level find females with a repertoire of S. melanogaster coupled diagnosis and to solve the cryptic female discrimination with S. hypoxantha males or vice versa, revealing there is problem. Our analysis, in addition to visual modeling for nonrandom mating (Servedio 2004). This observation reflec tance quantific ation of female plumage (Benites et al. suggests that capuchinos present positive assortative 2010), reinforces the human sensorial limitation bias for mating with concordant intra-specific, sex-based call type accurately distinguishing capuchino females. We encourage repertoires and no mixed pairing (Randler 2002). In this a similar evaluation for other species or populations scenario, social calls should play an important role in of capuchino seedeaters with independent trajectories specific mate recognition between recently diverged taxa and ongoing speciation across a wide geographic area as (Searby & Jouventin 2004). possible. Populations also  can be identified by their call The relationships between songs and calls and notes, as in other oscine passerines (Groth 1993), even how song is derived from calls varies among songbirds when they are in their wintering areas (Areta 2012). Revista Brasileira de Ornitologia 27(2): 2019 Species-level diagnosis of capuchino seedeater females Repenning & Fontana Bremond J.C. 1976. Specific re cognition in the song of Bonelli's The improvement of this kind of resear ch would Warbler (Phylloscopus bonelli). Behaviour 58: 99–116. have positive implications for taxonomy, evolutionary Burns K.J., Shultz A.J., Title P.O., Mason N.A., Barker F.K., and behavioral ecology studies in Neotropical seedeaters. Klicka J., Lanyon S.M. & Lovette I.J. 2014. Phylogenetics and From a conservation perspective, the identification of diversification of tanagers (Passeriformes: Thraupidae), the largest species-specific calls and songs can be a useful tool for radiation of Neotropical songbirds. Molecular Phylogenetics and Evolution 75: 41–77. conservation of threatened capuchino species, since it can Byers B.E. & Kroodsma D.E. 2009. Female mate choice and songbird help in the identification of specimens illegally captured song repertoires. 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Journal

Ornithology Research – Springer Journals

Published: Jun 1, 2019

Keywords: acoustic communication; assortative mating; bioacoustic; songbirds; Sporophila; vocal repertory

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