The advertisement call of the phytotelm-breeding Melanophryniscus xanthostomus (Anura: Bufonidae)

Sarah Mângia Diego José Santana Lucas Ribeiro Mariotto About the authors

ABSTRACT

Vocalizations are often useful for understanding taxonomic relationships among anuran species. Despite this usefulness, vocalizations are described in only nine of 29 in Melanophryniscus Gallardo, 1961. Here we describe the advertisement call of Melanophryniscus xanthostomus Baldo, Bornschein, Pie, Ribeiro, Firkowski & Morato, 2015 of a population from Serra Dona Francisca, municipality of Campo Alegre, state of Santa Catarina, Brazil. The advertisement call (of three males, total of 17 calls) comprises two segments (the first with short and single notes, followed by a multi-pulsed note), with a duration of 12.194-20.986 s, and dominant frequency of 3101-3618 Hz (first and second segments combined). The advertisement call of M. xanthostomus differs from its congeners mostly by the higher number of pulses in the second segment (294-1033; from 16 to 321 in the other Melanophryniscus species), except Melanophryniscus krauczuki Baldo & Basso, 2004 (1018-1502 pulses in the second segment). This is the first described call of a phytotelm breeding Melanophryniscus, but it presents the same prototype (a compound call formed by two segments, the first composed of short notes followed by a long trill) of its congeners not-phytotelm breedings. This might indicate the advertisement call of Melanophryniscus as a conserved trait and thus can be considered diagnostic for the genus.

KEY WORDS:
Atlantic Forest; bioacoustic; call description; natural history; vocalization

INTRODUCTION

Vocalizations are imperative to solve major taxonomic problems in many distinct anuran groups (Haddad and Pombal-Jr 1998Haddad CF, Pombal-Jr JP (1998) Redescription of Physalaemus spiniger (Anura: Leptodactylidae) and description of two new reproductive modes. Journal of Herpetology 557-565., Carvalho and Giaretta 2013Carvalho TR, Giaretta AA (2013) Bioacoustics reveals two new syntopic species of Adenomera Steindachner (Anura: Leptodactylidae: Leptodactylinae) in the Cerrado of central Brazil. Zootaxa 3731(3): 533-551., Pansonato et al. 2014Pansonato A, Mudrek JR, Simioni F, Alves Martins I, Strüssmann C (2014) Geographical variation in morphological and bioacoustic traits of Pseudopaludicola mystacalis (Cope, 1887) and a reassessment of the taxonomic status of Pseudopaludicola serrana Toledo, 2010 (Anura: Leptodactylidae: Leiuperinae). Advances in Zoology 2014: 1-13. https://doi.org/10.1155/2014/563165
https://doi.org/10.1155/2014/563165...
). The most common vocalization among anuran repertoire is the advertisement call (Wells 2007Wells KD (2007) The ecology and behavior of amphibians. University of Chicago Press, 1400 pp.), which is species-specific and therefore useful for species identification (Gerhardt and Davis 1988Gerhardt HC, Davis MS (1988) Variation in the coding of species identify in the advertisement calls of Litoria verreauxi (Anura: Hylidae). Evolution 42: 556-563.). The advertisement calls of many species-groups have a prototype pattern, well diffused among species - e.g., Microhylidae, Bufonidae (Heyer 1971Heyer WR (1971) Mating calls of some frogs from Thailand. Fieldiana Zoology 58: 61-82., Martin 1972Martin WF (1972) Evolution of vocalization in the genus Bufo. In: Blair WF (Ed.) Evolution in the genus Bufo. Austin, University of Texas Press, 279-309.) -, and can be the synapomorphic characteristic for lineages.

Melanophryniscus Gallardo, 1961 toads (29 valid species) are distributed in South America (Argentina, Bolivia, Brazil, Paraguay, and Uruguay) (Frost 2018Frost DR (2018) Amphibian Species of the World: an Online Reference. New York, American Museum of Natural History, v. 6.0. http://research.amnh.org/herpetology/amphibia/index.html
http://research.amnh.org/herpetology/amp...
). In phylogenies, the genus has been recovered as the sister taxon of all other bufonids (e.g., Frost et al. 2006Frost DR, Grant T, Faivovich J, Bain RH, Haas A, Haddad CFB, de Sá RO, Channing A, Wilkinson M, Donnellan SC, Raxworthy CJ, Campbell JA, Blotto BL, Moler P, Drewes RC, Nussbaum RA, Lynch JD, Green DM, Wheeler WC (2006) The Amphibian Tree of Life. Bulletin of the American Museum of Natural History 297: 1-291., Van Bocxlaer et al. 2010Van Bocxlaer I, Loader SP, Roelants K, Biju SD, Menegon M, Bossuyt F (2010) Gradual adaptation toward a range-expansion phenotype initiated the global radiation of toads. Science 327: 679-682., Peloso et al. 2012Peloso PLV, Faivovich J, Grant T, Gasparini JL, Haddad CFB (2012) An extraordinary new species of Melanophryniscus (Anura, Bufonidae) from Southeastern Brazil. American Museum Novitates 3762: 1-32.), and its monophyly is supported by morphological, biochemical, behavioral, and molecular evidence for adults (McDiarmid 1971McDiarmid RW (1971) Comparative morphology and evolution of frogs of the neotropical genera Atelopus, Dendrophryniscus, Melanophryniscus and Oreophrynella. Bulletin of the Los Angeles County Museum of Natural History Science 12: 1-66., Daly et al. 2007Daly JW, Wilham JM, Spande TF, Garraffo HM, Gil RR, Silva GL, Vaira M (2007) Alkaloids in bufonid toads (Melanophryniscus): temporal and geographic determinants for two Argentinian species. Journal of Chemical Ecology 33(4): 871-887. https://doi.org/10.1007/s10886-007-9261-x
https://doi.org/10.1007/s10886-007-9261-...
, Peloso et al. 2012Peloso PLV, Faivovich J, Grant T, Gasparini JL, Haddad CFB (2012) An extraordinary new species of Melanophryniscus (Anura, Bufonidae) from Southeastern Brazil. American Museum Novitates 3762: 1-32.) and tadpoles, based in a comparative description of the larvae of 23 Melanophryniscus species (Larson et al. 2003Larson PM, de Sá RO, Arrieta D (2003) Chondrocranial, hyobranchial and internal oral morphology in larvae of the basal bufonid genus Melanophryniscus (Amphibia: Anura). Acta Zoologica 84: 145-154., Baldo et al. 2014Baldo D, Candioti FV, Haad B, Kolenc F, Borteiro C, Pereyra MO, Zank C, Colombo P, Bornschein MR, Sisa FN, Brusquetti F, Conte CE, Nogueira-Costa P, Almeida-Santos P, Pie MR (2014) Comparative morphology of pond, stream and phytotelm-dwelling tadpoles of the South American Redbelly Toads (Anura: Bufonidae: Melanophryniscus). Biological Journal of the Linnean Society 112: 417-441. https://doi.org/10.1111/bij.12296
https://doi.org/10.1111/bij.12296...
). The genus is traditionally grouped into three species groups (M. tumifrons, M. stelzneri, and M. moreirae species groups) based mainly on morphology and coloration patterns (Caramaschi and Cruz 2002Caramaschi U, Cruz CAG (2002) Taxonomic status of Atelopus pachyrhynus Miranda-Ribeiro, 1920, redescription of Melanophryniscus tumifrons (Boulenger, 1905), and descriptions of two new species of Melanophryniscus from the state of Santa Catarina, Brazil (Amphibia, Anura, Bufonidae). Arquivos do Museu Nacional 60(4): 303-314.). Some species of Melanophryniscus described after 2003 have not been assigned to any group.

The toad Melanophryniscus xanthostomus Baldo, Bornschein, Pie, Ribeiro, Firkowski & Morato, 2015Bornschein MR, Firkowski CR, Baldo D, Ribeiro LF, Belmonte-Lopes R, Corrêa L, Morato SAA, Pie MR (2015) Three New Species of Phytotelm-Breeding Melanophryniscus from the Atlantic Rainforest of Southern Brazil (Anura: Bufonidae). PlosOne 10(12): e0142791. https://doi.org/10.1371/journal.pone.0142791
https://doi.org/10.1371/journal.pone.014...
was recently described based on individuals from Serra do Quiriri, Campo Alegre, Condomínio Vale dos Lagos and Reserva Particular do Patrimônio Natural Caetezal, Joinville and Morro do Boi, Corupá, municipalities from the state of Santa Catarina, Brazil, and was not assigned to any species groups. Some information about the natural history of M. xanthostomus is provided in the original description of the species (Bornschein et al. 2015Bornschein MR, Firkowski CR, Baldo D, Ribeiro LF, Belmonte-Lopes R, Corrêa L, Morato SAA, Pie MR (2015) Three New Species of Phytotelm-Breeding Melanophryniscus from the Atlantic Rainforest of Southern Brazil (Anura: Bufonidae). PlosOne 10(12): e0142791. https://doi.org/10.1371/journal.pone.0142791
https://doi.org/10.1371/journal.pone.014...
), including data of vocalization sites, and period that males were found calling (from September to February). However, the advertisement call was not described.

Given the rapid increase of the species description in the genus, the search for useful characteristics, as vocalizations, is crucial important to help resolve their taxonomy and to test evolutionary hypothesis. However, from the 29 species of Melanophryniscus, only nine have the advertisement call described (see Caldart et al. 2013Caldart VM, Santos TG, Maneyro R (2013) The advertisement and release calls of Melanophryniscus pachyrhynus (Miranda-Ribeiro, 1920) from the central region of Rio Grande do Sul, southern Brazil. Acta Herpetologica 8(2): 115-122., Duré et al. 2015Duré MI, Schaefer EF, Kehr AI (2015) Acoustic Repertoire of Melanophryniscus cupreuscapularis (Céspedez and Álvarez 2000) (Anura: Bufonidae): Advertisement, Encounter, and Release Calls. Journal of Herpetology 49(1): 53-59.). Because anuran advertisement calls are species-specific (Gerhardt and Davis 1988Gerhardt HC, Davis MS (1988) Variation in the coding of species identify in the advertisement calls of Litoria verreauxi (Anura: Hylidae). Evolution 42: 556-563.) and therefore, are useful in the distinction of the species and an important character for taxonomy (Duellman and Trueb 1986Duellman WE, Trueb L (1986) Biology of Amphibians. Baltimore, Johns Hopkins University Press, 670 pp.), in the present study, we described the advertisement call of M. xanthostomus for a population from Serra Dona Francisca, Campo Alegre, Santa Catarina, Brazil. We also compared the calls of M. xanthostomus with the nine other species of Melanophryniscus.

MATERIAL AND METHODS

We recorded advertisement calls of three males (FURB 22851 - SVL 18.6 mm, FURB 22822 - SVL 19.7 mm, FURB 22713 - SVL 16.9 mm, total of 17 calls, Figs 1-3) at Serra Dona Francisca (-26°12’52.54”S, 49°13’04.92”W), Campo Alegre, Santa Catarina, on November 3rd, 2013. Calls were recorded with a Marantz PMD661 digital recorder coupled with a YOGA HT-81 directional microphone. Recordings were made around midnight (air temperature 18.8 °C, humidity 65%). We digitalized the recordings at 44.1 kHz, resolution of 16 bits. The three specimens were collected and deposited on the Zoology Collection of Universidade Regional de Blumenau (FURB), Santa Catarina, Brazil, under the numbers above.

Figures 1-3
Specimens of Melanophryniscus xanthostomus: dorsal view (1) and ventral view (2) from FURB 22851 specimen and FURB 22713 specimen in life (3).

We analyzed calls in RAVEN PRO 1.5 for Mac (Bioacoustics Research Program 2012) and constructed audio spectrograms in R using the package seewave (Sueur et al. 2008Sueur J, Aubin T, Simonis C (2008) Equipment review: seewave, a free modular tool for sound analysis and synthesis. Bioacoustics 18: 213-226.) with the following parameters: FFT window width = 256, Frame = 100, Overlap = 75, and flat top filter. We analyzed acoustic parameters normally used for species of Melanophryniscus: dominant frequency (Hz), call duration (sec), call interval (sec), first segment duration (sec), second segment duration (sec), interval between first and second segment (sec), number of short notes, duration of short notes (sec), interval between short notes (sec), note rate of the first segment (the ratio of the absolute number of notes and the absolute duration of the segment), pulse number of the second segment, and pulse rate of the second segment (the ratio of the absolute number of pulses and the absolute duration of the segment). Terminology of call descriptions follows Köhler et al. (2017Köhler J, Jansen M, Rodríguez A, Kok PJR, Toledo LF, Emmrich M, Glaw F, Haddad CFB, Rödel MO, Vences M (2017) The use of bioacoustics in anuran taxonomy: Theory, terminology, methods and recommendations for best practice. Zootaxa 4251: 1-124. https://doi.org/10.11646/zootaxa.4251.1.1
https://doi.org/10.11646/zootaxa.4251.1....
).

We compared the advertisement call of M. xanthostomus with nine congeners, although those descriptions did not include all the call parameters that we analyzed (see references in Table 1).

Table 1
Comparison of temporal and spectral parameters of the advertisement call of Melanophryniscus xanthostomus and nine other congeneric species. Values are means with the range in parentheses. (a) Air temperature; (w) water temperature.

RESULTS

The advertisement call of M. xanthostomus is a compound call formed by two segments (Table 1, Fig. 4-6). The first segment is composed by short and single notes (13 ± 4; range 7-20 notes), with a duration of 0.011-0.057 s (0.027 ± 0.010 s), and interval duration of 0.242-0.774 s (0.325 ± 0.109 s) between the short notes, with a pulse rate of 0.002-0.004 s (0.003 ± 0.001 s). The duration of the first segment is 1.774-6.794 s (4.115 ± 1248.98 s). The second segment consists of a multi-pulsed note (a long trill) of 6.278-18.318 s of duration (14.189 ± 2979.77 s), with 294-1033 pulses (685 ± 179.59 pulses), and pulse rate of 0.04-0.06 pulses per second (0.05 ± 0.01 pulses/s). The advertisement call (first and second segments combined) presents a duration of 12.194-20.986 s (18.577 ± 2443.70 s), and dominant frequency of 3101-3618 Hz (3395 ± 180.32 Hz). The interval duration between the first and the second segments is 9.258-221.673 s (82.949 ± 78878.03 s).

Figures 4-6
Advertisement call of Melanophryniscus xanthostomus (LM380, SLV 18.6 mm): (4) oscillogram and spectogram of one call; (5) oscillogram and spectogram of three notes from the first segment; (6) oscillogram and spectogram of 28 pulses from the second segment.

The advertisement call of M. xanthostomus is emitted with both segments in sequence, not only the first or the second segment separately. In November 2013, we observed six males calling on bromeliads at ground level, in two forest fragments at 1027 m altitude. Most toads can be found in bromeliads closer to the ground, which were usually under 1 m high, as well as inside those that fell in the leaf litter. Also we found one female near an egg clutch at the fence of pitfall trap. In January 2014, we registered only one male calling during the fieldworks. No individuals were capture in pitfall traps in the forest fragment. Other species calling along with M. xanthostomus in the forest were Fritizana sp., Cycloramphus bolitoglossus (Werner, 1897) and Adenomera araucaria Kwet & Angulo, 2002.

DISCUSSION

The natural history of the phytotelma-using Melanophryniscus species is very different from their congeners, because of the reproductive mode and tadpole morphology (Langone et al. 2008Langone JA, Segalla MV, Bornschein M, de Sá RO (2008) A new reproductive mode in the genus Melanophryniscus Gallardo, 1961 (Anura: Bufonidae) with description of a new species from the state of Paraná, Brazil. South American Journal of Herpetololy 3(1): 1-9., Baldo et al. 2014Baldo D, Candioti FV, Haad B, Kolenc F, Borteiro C, Pereyra MO, Zank C, Colombo P, Bornschein MR, Sisa FN, Brusquetti F, Conte CE, Nogueira-Costa P, Almeida-Santos P, Pie MR (2014) Comparative morphology of pond, stream and phytotelm-dwelling tadpoles of the South American Redbelly Toads (Anura: Bufonidae: Melanophryniscus). Biological Journal of the Linnean Society 112: 417-441. https://doi.org/10.1111/bij.12296
https://doi.org/10.1111/bij.12296...
), and the type of habitats they inhabit (other species occurs and lay the eggs in freestanding water) (Kwet et al. 2010Kwet A, Lingnau R, Di-Bernardo M (2010) Pró-Mata: Anfíbios da Serra Gaúcha, sul do Brasil. Tübingen, Brasilien-Zentrum, University of Tübingen, 148 pp., Maneyro et al. 2017Maneyro R, Loebmann D, Tozetti A, Fonte LFM (2017) Anfíbios das planícies costeiras do extreme sul do Brasil e Uruguai. São Paulo, Anolis Books, 176 pp.). Concerning its call parameters, this species showed some temporal and spectral characteristics that suggest some acoustic adaptations for forest environments, such as described in the Acoustic Adaptation Hypothesis (AAH) (Morton 1975Morton ES (1975) Ecological sources of selection on avian sounds. The American Naturalist 109(965): 17-34. https://doi.org/10.1086/282971
https://doi.org/10.1086/282971...
, Erdtmann and Lima 2013Erdtmann LK, Lima AP (2013) Environmental effects on anuran call design: what we know and what we need to know. Ethology Ecology & Evolution 25(1): 1-11. https://doi.org/10.1080/03949370.2012.744356
https://doi.org/10.1080/03949370.2012.74...
). According this hypothesis, calls in forest environments will: (1) be longer in length, (2) have a lower repetition rate, (3) have lower minimal, maximal and dominant frequencies and (4) have a smaller frequency bandwidth (Morton 1975Morton ES (1975) Ecological sources of selection on avian sounds. The American Naturalist 109(965): 17-34. https://doi.org/10.1086/282971
https://doi.org/10.1086/282971...
).

The advertisement call of M. xanthostomus differs from its congeners by the higher number of pulses in the second segment (294-1033; from 16 to 321 in the other Melanophryniscus species), except from Melanophryniscus krauczukiBaldo & Basso, 2004Baldo D, Basso NG (2004) A new species of Melanophryniscus Gallardo, 1961 (Anura: Bufonidae), with comments on the species of the genus reported for Misiones, Northeastern Argentina. Journal of Herpetology 38: 393-403. (1018-1502 pulses in the second segment) and M. pachyrhynus (Miranda-Ribeiro, 1920) (164-1382 pulses in the second segment). The lowest pulse rate of the second segment (40.55-56.70 pulses per second) differs M. xanthostomus from most of its congeners (62 to 95 pulses per second in M. atroluteus (Miranda-Ribeiro, 1920), M. cupreuscapularis Céspedez & Alvarez, 2000, M. dorsalis (Mertens, 1933), M. klappenbachi Prigioni & Langone, 2000, M. montevidensis (Philippi, 1902), M. stelzneri (Weyenbergh, 1875), except from M. krauczuki, M. pachyrhynus, and M. rubriventris (Vellard, 1947) (42.35-44.95, 3020-34.30, 45.00-64.00 pulses per second, respectively). The total call and the second segment durations of M. xanthostomus (12.19-20.99 s, 6.28-18.32 s, respectively) are only shorter than M. krauczuki (25.01-36.65 s, 23.78-33.41 s). Melanophryniscus pachyrhynus reaches higher values of call and second segment durations (6.64-75.20 s, 4.79-45.75 s) than M. xanthostomus, however, the values overlap. The higher number of notes in the first segment (7-20) of the advertisement call of M. xanthostomus differs from M. klappenbachi (3-4) and M. rubriventris (2-7). The dominant frequency is higher (3395 Hz) and the amplitude range is lower (± 500 Hz) than other species of Melanophryniscus, except from M. krauczuki (dominant frequency 3300 Hz), M. cupreuscapularis (amplitude ± 200 Hz) and M. rubriventris (amplitude between 100-300 Hz). The interval between calls is longer in M. xanthostomus (82.949 s) than other species. The other acoustic parameters, such as first segment duration and interval between segments, varies among species of the genus, but all the values overlap. Even with some acoustic traits that corroborate with the AAH, we observed that the advertisement calls are similar among Melanophryniscus species.

Species of Melanophryniscus have an advertisement call composed of short notes followed by a long trill (e.g., Kwet et al. 2005Kwet A, Maneyro R, Zillkens A, Mebs D (2005) Advertisement call of Melanophryniscus dorsalis (Mertens, 1933) and M. montevidensis (Phillipi, 1902), two parapatric species from southern Brazil and Uruguay, with comments on morphological variation in the Melanophryniscus stelzneri group (Anu ra: Bufonidae). Salamandra 41: 3-20., Caldart et al. 2013Caldart VM, Santos TG, Maneyro R (2013) The advertisement and release calls of Melanophryniscus pachyrhynus (Miranda-Ribeiro, 1920) from the central region of Rio Grande do Sul, southern Brazil. Acta Herpetologica 8(2): 115-122., Duré et al. 2015Duré MI, Schaefer EF, Kehr AI (2015) Acoustic Repertoire of Melanophryniscus cupreuscapularis (Céspedez and Álvarez 2000) (Anura: Bufonidae): Advertisement, Encounter, and Release Calls. Journal of Herpetology 49(1): 53-59.), as we observed to M. xanthostomus. Most species, including M. xanthostomus, have the first segment composed by one group of short notes, except M. cupreuscapularis and M. dorsalis (from Laguna, Santa Catarina, Brazil), which have two or more groups of short notes, separated by a higher distance than that among notes (Kwet et al. 2005Kwet A, Maneyro R, Zillkens A, Mebs D (2005) Advertisement call of Melanophryniscus dorsalis (Mertens, 1933) and M. montevidensis (Phillipi, 1902), two parapatric species from southern Brazil and Uruguay, with comments on morphological variation in the Melanophryniscus stelzneri group (Anu ra: Bufonidae). Salamandra 41: 3-20., Duré et al. 2015Duré MI, Schaefer EF, Kehr AI (2015) Acoustic Repertoire of Melanophryniscus cupreuscapularis (Céspedez and Álvarez 2000) (Anura: Bufonidae): Advertisement, Encounter, and Release Calls. Journal of Herpetology 49(1): 53-59.). Melanophryniscus xanthostomus emit the advertisement call with both segments in sequence as described for other species of the genus (see Duré et al. 2015Duré MI, Schaefer EF, Kehr AI (2015) Acoustic Repertoire of Melanophryniscus cupreuscapularis (Céspedez and Álvarez 2000) (Anura: Bufonidae): Advertisement, Encounter, and Release Calls. Journal of Herpetology 49(1): 53-59.), except M. pachyrhynus, that also emit calls with the second segment (the trill) alone (Caldart et al. 2013Caldart VM, Santos TG, Maneyro R (2013) The advertisement and release calls of Melanophryniscus pachyrhynus (Miranda-Ribeiro, 1920) from the central region of Rio Grande do Sul, southern Brazil. Acta Herpetologica 8(2): 115-122.). The functional differences of the two segments of the advertisement call of Melanophryniscus species might be investigate in future bioacoustic and behavior studies of these species.

Thus, it is remarkable that the advertisement call of M. xanthostomus presents the same prototype (a compound call formed by two segments, the first composed of short notes followed by a long trill) of its congeners not-phytotelm breedings. Biological concerns, such as species recognition, sexual selection, physiological traits or body size (Gerhardt 1991Gerhardt HC (1991). Female mate choice in treefrogs: static and dynamic acoustic criteria. Animal Behaviour 42(4): 615-635. https://doi.org/10.1016/S0003-3472(05)80245-3
https://doi.org/10.1016/S0003-3472(05)80...
, Bevier et al. 2008Bevier CR, Gomes FR, Navas CA (2008). Variation in call structure and calling behavior in treefrogs of the genus Scinax. South American Journal of Herpetology 3(3): 196-206. https://doi.org/10.1670/144-03A
https://doi.org/10.1670/144-03A...
), may explain the similarities of advertisement calls among Melanophryniscus species, while some evidences showed contrary pattern expected for AAH. Some amphibians species showed larger body mass and lower call frequencies in open-land environments (Bevier et al. 2008Bevier CR, Gomes FR, Navas CA (2008). Variation in call structure and calling behavior in treefrogs of the genus Scinax. South American Journal of Herpetology 3(3): 196-206. https://doi.org/10.1670/144-03A
https://doi.org/10.1670/144-03A...
), such as we detected for M. xanthostomus (higher dominant frequency associated to forest environment). But the open land and stream inhabitant M. krauczuki (Baldo and Basso 2004Baldo D, Basso NG (2004) A new species of Melanophryniscus Gallardo, 1961 (Anura: Bufonidae), with comments on the species of the genus reported for Misiones, Northeastern Argentina. Journal of Herpetology 38: 393-403.) also showed higher dominant frequency, suggesting other environment variables may be associated, such as stream noise. However, the lack of phylogenetic hypothesis for the genus and other described calls from phytotelm breeding Melanophryniscus, makes it hard to test this hypothesis at this moment. Thus, future phylogenetic comparative studies, testing the AAH, could bring new explanations for the evolutinary acoustic patterns of Melanophryniscus. Once this is the first described call of a phytotelm breeding Melanophryniscus, we highlight the need to know the call of the other species with the same reproductive mode in order to confirm this proposal.

ACKNOWLEDGMENTS

We are thankful to all friends involved directly and indirectly to this work, specially to Carlos E. Conte, Renato C. Nali and Daniel Son for suggestions and the help during the fieldworks. We are thankful to H.L. Doerrier and C.T. Ferriolli for the English editing. To Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq processes 132559/2012-9, 167888/2014-5 and 311492/2017-7), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), and Fundação Boticário for the grants. To the SISBIO (#35005) and FUNDEMA (#013/12-GEMAP) for the research licenses.

LITERATURE CITED

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    » https://doi.org/10.1670/144-03A
  • Bornschein MR, Firkowski CR, Baldo D, Ribeiro LF, Belmonte-Lopes R, Corrêa L, Morato SAA, Pie MR (2015) Three New Species of Phytotelm-Breeding Melanophryniscus from the Atlantic Rainforest of Southern Brazil (Anura: Bufonidae). PlosOne 10(12): e0142791. https://doi.org/10.1371/journal.pone.0142791
    » https://doi.org/10.1371/journal.pone.0142791
  • Caldart VM, Santos TG, Maneyro R (2013) The advertisement and release calls of Melanophryniscus pachyrhynus (Miranda-Ribeiro, 1920) from the central region of Rio Grande do Sul, southern Brazil. Acta Herpetologica 8(2): 115-122.
  • Caramaschi U, Cruz CAG (2002) Taxonomic status of Atelopus pachyrhynus Miranda-Ribeiro, 1920, redescription of Melanophryniscus tumifrons (Boulenger, 1905), and descriptions of two new species of Melanophryniscus from the state of Santa Catarina, Brazil (Amphibia, Anura, Bufonidae). Arquivos do Museu Nacional 60(4): 303-314.
  • Carvalho TR, Giaretta AA (2013) Bioacoustics reveals two new syntopic species of Adenomera Steindachner (Anura: Leptodactylidae: Leptodactylinae) in the Cerrado of central Brazil. Zootaxa 3731(3): 533-551.
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Publication Notes

  • Available online:

    July 31, 2019
  • Zoobank Register:

    http://zoobank.org/1F5BD8E4-DB3D-4ACD-B993-6D318A60EB42
  • Publisher:

    © 2019 Sociedade Brasileira de Zoologia. Published by Pensoft Publishers at https://zoologia.pensoft.net

Publication Dates

  • Publication in this collection
    08 Aug 2019
  • Date of issue
    2019

History

  • Received
    10 Apr 2018
  • Accepted
    11 May 2018
  • Published
    31 July 2019
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