Bioacoustics of Hylidae

The population previously identified as Boana multifasciata (Günther, 1859) from the Guiana Shield is currently known to be an unnamed candidate species, inhabiting the Guianas and the Brazilian states of Roraima , Pará and Amapá ( Fouquet et al. 2021c ) based only on molecular data. We added the molecularbased records from Vacher et al. (2020) and Fouquet et al. (2021c) corresponding to this taxon, as well as the literature records with overall morphology more similar to B. multifasciata . We decided to keep using this name for Amapá populations until more studies clarify their taxonomic status. In the species group of B. semilineata , two species are known to occur in Amapá , Boana diabolica Fouquet, Martinez, Zeidler, Courtois, Gaucher, Blanc, Lima, Souza, Rodrigues & Kok, 2016 and an unnamed species, B. aff. semilineata ( Fouquet et al. 2016 ) . Besides these two names, records in Amapá have also been identified as Boana geographica (Spix, 1824) ( Lima 2008 ; Pereira-Júnior et al. 2013; Benício & Lima 2017 ; Ferreira-Lima et al. 2017 ) and B. aff. geographica ( Lima 2006b ) . These records could belong either to B. diabolica or B. aff. semilineata , so we chose to consider in our list only the molecular confirmed records ( Fouquet et al. 2016 ; Vacher et al. 2020 ). Dendropsophus counani Fouquet, Orrico, Ernst, Blanc, Martinez, Vacher, Rodrigues, Ouboter, Jairam & Ron, 2015 has long been confused with Dendropsophus brevifrons (Duellman & Crump, 1974) (Fouquet et al. 2015) , and we consider the record of D. brevifrons ( Benício & Lima 2017 ) to be D. counani . Dendropsophus minusculus (Rivero, 1971) is morphologically similar to Dendropsophus branneri (Cochran, 1948) , with which D. minusculus has been historically confused ( Zina et al. 2014 ). Dendropsophus minusculus is distributed in northern Brazil and the Guiana Shield, mainly within Amazonia, with some sparse records in northeastern Brazil in the states of Maranhão , Piauí , Ceará , and an isolated record from Bahia , whereas D. branneri inhabits the Atlantic Forest of southeastern and northeastern Brazil ( Zina et al. 2014 ; Frost 2022 ). Both species seem to have a contact zone in northeastern Brazil , but the state of Amapá is within the distribution range of D. minusculus . Thus, we consider the records of D. branneri ( Lima 2006a , 2006b ) to be D. minusculus . Orrico et al. (2021) has recently defined the populations with the overall morphology like D. minutus (Peters, 1872) in the Guiana Shield as D. amicorum , and we agreed with them regarding the records of Amapá . It is important to note that, even though the IUCN status of the species is Critically Endangered (CR, IUCN 2022 ), it was evaluated when it was known only from the type localiy, and the conservation status of D. amicorum is likely to change during next evaluations. Dendropsophus walfordi (Bokermann, 1962) and Dendropsophus nanus (Boulenger, 1889) are also very similar to each other, being even considered as representing a single species ( Lutz 1973 ). Despite being currently considered as separate species ( Langone & Basso 1987 ), these are morphologically and genetically closely related to each other, with D. walfordi being frequently recovered within D. nanus , leaving it paraphyletic ( Fouquet et al. 2011 ; Medeiros et al. 2013 ; Orrico et al. 2021 ). Recently, Seger et al . (2021) evaluated the D. nanus - D. walfordi complex with a broad molecular study and defined that D. nanus is the lineage inhabiting Paraguay , northeastern Argentina , and southern Brazil , whereas D. walfordi is the single lineage inhabiting Amazonia. Thus, we decided to adopt the name D. walfordi to records from both species within the state of Amapá . Benício & Lima (2017) recorded Dendropsophus microcephalus (Cope, 1886) and Dendropsophus parviceps (Boulanger, 1882) in the Amapá National Forest. The first species is distributed from southern Mexico to northern South America ( Frost 2022 ) but, although the specimens east of Venezuela have been called D. microcephalus due to morphological similarities, they probably correspond to other species, such as D. minusculus or even Dendropsophus gaucheri ( Lescure & Marty, 2000 ) (V.G.D. Orrico, pers. comm.). Although Benício & Lima (2017) cited both D. minusculus and D. microcephalus , there are no voucher specimens cited in their study. Thus, we decided to remove the record of D. microcephalus from the list until more data from the Amapá National Forest is available to help clarifying the taxonomic status of this population. Moreover, we considered the record of D. microcephalus from Queiroz et al. (2011) as D. minusculus . Dendropsophus parviceps is currently known from Ecuador , Colombia , and the Brazilian state of Amazonas, with related populations from Brazilian states of Acre and Rondônia being recently described as Dendropsophus kamagarini Rivadeneira, Venegas & Ron, 2018 ( Rivadeneira et al. 2018 ). Besides D. parviceps, Benício & Lima (2017) found another species from the group of D. parviceps (sensu Orrico et al. 2021 ) in the Amapá National Forest, D. brevifrons (that we consider D. counani , see above). As in the previous case concerning D. microcephalus and D. minusculus , we also decided to remove D. parviceps from our list and consider the record as D. counani until additional data is available. The record of Lysapsus laevis (Parker, 1935) from Araújo & Costa-Campos (2015) (as Pseudis laevis ) is actually Lysapsus bolivianus (Gallardo, 1961) (Costa-Campos, pers. comm.). There are two species of the group of Osteocephalus buckleyi (sensu Jüngfer et al. 2013 ) cited for Amapá , O. buckleyi (Boulenger, 1882) ( Lima 2008 ; Queiroz et al. 2011 ) and O. cabrerai (Cochran & Goin, 1970) ( Lima 2006b , 2008 ; Pedroso-Santos et al. 2019 ). Dewynter et al. (2019) also found two species of the group of O. buckleyi in French Guiana , both reaching the border with Amapá : O. cabrerai and Osteocephalus helenae (Ruthven, 1919) . Vacher et al. (2020) also adopted these two species names in their molecular survey for populations of Osteocephalus from Amapá and French Guiana . Even though the two species were recovered as a single taxonomic entity in their species delimitation analysis, they applied both names to the clade formed by two lineages of Osteocephalus that appear to be morphologically diagnosable to each other and coexist in the Eastern Guiana Shield (see Dewynter et al. 2016 ). Thus, we consider both O. cabrerai and O. helenae in our list. We did not have access to the voucher specimens of most studies and most of the known previous records do not provide photographs of species of Osteocephalus . As such, we could not be precise about the locations where each of the two species occurs in Amapá . One exception is at Reserva Extrativista Municipal Beija-Flor-Brilho-deFogo, central part of Amapá , from where Pedroso-Santos et al. provided a picture of what they identified as O. cabrerai ( Pedroso-Santos et al. 2019: 801 , fig. 1.11) and it corresponds to the same morphotype Dewynter et al. (2016) consider O. cabrerai . Scinax garbei (Miranda-Ribeiro, 1926) is a widespread species of the group of S. rostratus distributed throughout the middle and upper Amazon Basin in Venezuela , Ecuador , Colombia , Peru , Bolivia and Brazil ( Faivovich et al. 2005 ; Frost 2022 ). Although there are records of S. garbei from Amapá (FerreiraLima et al. 2017; Lima 2018 ; Silva e Silva & Costa-Campos 2018 ), there is molecular evidence of only Scinax jolyi Lescure & Marty, 2000 inhabiting Amapá ( Vacher et al. 2020 ). Due to the taxonomic complexity of S. garbei ( Ron et al. 2018 ) and the overall morphological similarity between the two species, we consider more plausible that the records of S. garbei in Amapá are indeed S. jolyi . Scinax cruentomma (Duelmann, 1972) is mainly distributed in western Amazonia, but there are a few additional records in other Amazonian regions ( Carvalho et al. 2015 : fig. 3). Those authors conducted acoustic comparisons between populations from the type locality (Santa Cecilia, Ecuador ), the upper Negro River (Amazonas, Brazil ), and French Guiana (data derived from Lescure & Marty 2000 ) and found that the high variation in some of the analyzed call traits indicate that the French Guiana population could represent another, potentially unnamed, species. Therefore, we provisionally assign the Amapá population to S. cf. cruentomma until the taxonomic status of the populations of Scinax bearing a horizontal red streak on the iris from the Eastern Guiana Shield is addressed.

Boana caiapo ( Fig. 3F ).This species was described based on morphological, acoustic, and osteological characteristics ( Pinheiro et al . 2018 ). The authors identified two types of notes, A and B, which can be emitted separately or together. Although both types are very similar in structure and frequency, note A has a shorter duration and fewer pulses. Additionally, note A is emitted more frequently and sometimes in combination with note B, whereas note B is rarely emitted alone ( Pinheiro et al . 2018 ). We observed only the note A in the advertisement call of B. caiapo from Caseara, which reached a higher number of pulses per call (78–195 pulses; 69–122 pulses in the original description) (n = 169; Table S3 ). There are no female individuals in the type series of B. caiapo , and we provide here the measurements of four females , which are generally bigger than males (SVL 47.63–53.78 mm in females, n = 4; 39.88–49.51 mm in males, n = 39, present work; 42.2–51.2 mm in males, Pinheiro et al . 2018 ) ( Table S2 ). Boana sp. ( aff. semilineata ) ( Fig. 4B ). The Boana semilineata species group is mainly characterized by the presence of a reticulated lower eyelid membrane and is known to present several cryptic lineages ( Fouquet et al . 2016 ; Peloso et al . 2018 ). The lineage of the B. semilineata group collected in Caseara municipality presents dark brown irregular bands on the dorsal surface of tibia and thighs, flanks black with white and yellowish spots, iris reddish surrounded by a black circle, and pupils black. Fouquet et al . (2016) identified an unnamed lineage with occurrence in Altamira municipality, Pará state , and Guaraí municipality, Tocantins state , called as Boana aff. semilineata 2. Silva et al . (2020) also recorded individuals that belong to this lineage in the municipalities of Ananás, Aragominas, Araguaína, Babaçulândia, Colinas do Tocantins , Muricilândia, Nazaré, and Santa Fé do Araguaia, all in the state of Tocantins . Our record may also represent this cryptic lineage, but we do not have acoustic and molecular data to confirm the identity of this population. Taxa SJF CF GF RPPN LJ GD Env. IUCN Data Amphibia Aromobatidae Allobates crombiei (Morales, 2002 “2000”) - X - X AM FF LC MM, ML, BA Bufonidae Rhaebo guttatus (Schneider, 1799) - - - X AM FF LC MM, ML Rhinella diptycha (Cope, 1862) - X - X WD AT LC MM, ML Rhinella mirandaribeiroi (Gallardo, 1965) - X X X EN AT LC MM, ML Rhinella ocellata (Günther, 1859 “1858”) - - - X EN AT, OE LC MM, ML, BA Hylidae Boana caiapo Pinheiro, Cintra, Valdujo, Silva, Martins, Silva & Garcia, 2018 X X X - AM AT, FF, OE LC MM, ML, BA, GN Boana multifasciata (Günther, 1859 “1858”) X X X X WD AT, FF, OE LC MM, ML Boana punctata (Schneider, 1799) X X X - WD AT, FF LC MM, ML Boana raniceps (Cope, 1862) - X X - WD AT, OE LC MM, ML, BA Boana sp. (gr. semilineata ) X - - - AM AT - MM, ML Dendropsophus anataliasiasi (Bokermann, 1972) - X - X EN AT, OE LC MM, ML Dendropsophus cruzi (Pombal & Bastos, 1998) X X - X EN AT LC MM, ML, BA Dendropsophus melanargyreus (Cope, 1887) - X - X AM AT, FF LC MM, ML, BA Dendropsophus minutus - X - X WD AT, FF LC MM, ML ......continued on the next page Taxa SJF CF GF RPPN LJ GD Env. IUCN Data Dendropsophus nanus (Boulenger, 1889) X X - - WD AT LC MM, ML Lysapsus caraya Gallardo, 1964 X X X - EN AT LC MM , ML , BA Pithecopus hypochondrialis (Daudin, 1800) - X - X AM AT, FF, OA LC MM , ML Osteocephalus taurinus Steindachner , 1862 - X X X AM FF LC MM, ML Scinax constrictus Lima, Bastos & Giaretta, 2004 X X X X EN AT, OE LC MM, ML, BA, GN Scinax fuscomarginatus (A. Lutz, 1925) - X X X WD AT LC MM, ML, BA, GN Scinax similis (Cochran, 1952) - - - X - FF LC MM, ML, BA, GN Trachycephalus typhonius (Linnaeus, 1758) X X - - WD AT, FF LC MM, ML Leptodactylidae Adenomera cotuba Carvalho & Giaretta, 2013 X X - X EN AT, OE NT MM, ML, BA Adenomera juikitam Carvalho & Giaretta, 2013 - X - X EN AT, OE LC MM, ML, BA Adenomera saci Carvalho & Giaretta, 2013 - X - X EN AT, OE LC MM, ML, BA Adenomera sp. (aff. hylaedactyla ) - X - - - AT - MM, ML Leptodactylus fuscus (Schneider, 1799) X X - X WD AT LC MM, ML, BA Leptodactylus labyrinthicus (Spix, 1824) X X X X WD AT, FF LC MM, ML Leptodactylus macrosternum Miranda-Ribeiro, 1926 X X X X X DA AT, FF LC MM, ML Leptodactylus mystaceus (Spix, 1824) - X - X WD AT, FF LC MM, ML, BA Leptodactylus podicipinus (Cope, 1862) X X X X WD AT, FF, OE LC MM, ML Leptodactylus pustulatus (Peters, 1870) X X X - EN AT LC MM, ML ......continued on the next page Taxa SJF CF GF RPPN LJ GD Env. IUCN Data Leptodactylus natalensis Lutz, 1930 - Lithodytes lineatus (Schneider, 1799) - Physalaemus centralis Bokermann, 1962 X Physalaemus sp. (gr. cuvieri ) - Pseudopaludicola canga Giaretta & X Kokubum, 2003 Pseudopaludicola jazmynmcdonaldae Andrade, Silva, Koroiva, Fadel, and X Santana, 2019 - - X X X X - - X - - - X X X X X X X - AM EN - AM EN AT, FF FF AT, FF AT, FF AT, OE AT, OE LC LC LC - LC EN ML, NA MM, ML MM , ML , BA, GN MM, ML, BA, GN MM, ML, BA MM, ML Microhylidae Chiasmocleis centralis Bokermann, 1952 - Elachistocleis magna Toledo, 2010 X - X - - X X EN - FF, OE AT, FF, OE DD LC MM, ML MM, ML, BA, GN Odontophrynidae Proceratophrys sp. ( cf. ararype ) - - - X - FF, OE - MM, ML, BA, GN Strabomantidae Barycholos ternetzi (Miranda Ribeiro, 1937) X X X X EN FF LC MM, ML Total 21 35 16 34 3 - - - Dendropsophus melanargyreus ( Fig. 4E ). We identified individuals of Dendropsophus melanargyreus in the study area according to morphological characteristics described by Caramaschi and Jim (1983) . This species occurs in the states of Goiás and Mato Grosso states to São Paulo , Minas Gerais , and northeastern Brazil ; Surinam and French Guiana , Bolivia , and the Pantanal of northeastern Paraguay ( Neves et al . 2020 ; Frost 2024 ). Despite this reported distribution, there is few information available about geographic variation of this species. The advertisement call of D. melanargyreus is currently described for two localities, Puerto Almacén, Bolivia and Belém municipality, Pará state, Brazil , both in the Amazon biome (Duelmann & Pyles 1983; Marquéz et al . 1993 ). Here we update the description of the advertisement call of this species, providing data for a new location at the CAT. The call of the species from the study area is composed of one pulsed note emitted sporadically, with duration ranging from 0.32 to 0.48 s (0.38 ± 0.04). The calls present 36 to 48 pulses (40 ± 2.5), with pulse rate ranging from 98 to 119 pulses per second (106.2 ± 7.7). The dominant frequency varies from 3359.2 to 3876.0 Hz (3566.7 ± 146) ( Fig. 9A , Table S3 ). The advertisement call from Caseara is more similar to the calls provided for Bolivia (0.37– 0.46 s , 34–39 pulses/call, 83–97 pulses/s, and 3036–3661 Hz), and differs significantly in all parameters from the Belém population (0.25– 0.33 s , 127–140 pulses/s, 2093–2399 Hz). These call differences and the gap of knowledge about D. melanargyreus suggest that more than one species may be hidden under this name ( Faivovich et al . 2005 ; Pyron & Wiens 2011 ; Fouquet et al . 2011 ; Medeiros et al . 2013 ). Dendropsophus minutus ( Fig. 4F ). This is a small hylid frog, thought to be widely distributed in South America. However, Gehara et al . (2014) recovered a high genetic diversity within Dendropsophus minutus suggesting the existence of numerous distinct species. The authors recovered 43 lineages, including the population from Caseara municipality, designated as lineage 36, which is widely distributed across several Brazilian states. Lysapsus caraya ( Fig. 4H ). The advertisement call of this species was first described to Araguapaz municipality, Goiás state , characterized by a pulsed call, composed of three notes with different note durations and pulse numbers ( Bastos et al . 2011 ). Santana et al . (2013) described the advertisement call of four species of Lysapsus and found two types of call (A and B) for each species, except for L. caraya (only type A). According to the authors, the call A is emitted more frequently and may be classified as an advertisement call composed of several pulses, which may be concatenated or not; and call B, subdivided in notes x and y, it may be the result of choruses with intense social interactions among individuals. In the present study, we recorded the two types of calls for L. caraya ( Fig. 9B , Table S3 ). The call A presents duration of 0.082 to 0.205 s (0.141 ± 0.035), with the number of pulses ranging from 8 to 17 (12.5 ± 24) and dominant frequency ranging from 4312.5 to 4781.2 Hz (4593.8 ± 119.9) ( Fig. 9B ). The duration of call B ranges from 0.111 to 0.211 s (0.171 ± 0.024) and dominant frequency from 4406.2 to 4875.0 Hz (4651.8 ± 127.4) ( Fig. 9B ). The first note (x) of call B presents a duration of 0.018 to 0.060 s (0.043 ± 0.013), with 5 to 16 pulses per note (10.5 ± 3.2), and dominant frequency ranging from 2718.8 to 4593.8 Hz (3850.4 ± 801.8). The duration of the second note (y) ranges from 0.026 to 0.088 s (0.064 ± 0.021), 4 to 8 number of pulses per note (6.0 ± 1.0), and dominant frequency ranging from 4406.2 to 4875.0 Hz (4654 ± 149.8). The values of call A overlap with those described by Santana et al . (2013) , and both calls can be emitted alone or together, with several arrangements (e.g. A, B, A+B, A+B+B, B+A, A+A, B+B, B+B+B). We compared the call B of L. caraya with the same call of L. bolivianus and L. laevis , that present structure similarities. The entire call B duration of L. caraya overlaps with both species, and there are similarities between the parameters analyzed in the two types of notes (x and y). The number of pulses of the note x of L. caraya overlaps with L. bolivianus (5–16 and 6–22 pulses, respectively), and the duration of the note y of L. caraya overlaps with L. laevis (0.03– 0.09 s and 0.03– 0.13 s , respectively). Scinax fuscomarginatus ( Fig. 5C ). This species presents a rich genetic structure and extensive geographical distribution, showing variation in morphological and call parameters throughout its distribution ( Toledo & Haddad 2005 ; Brusquetti et al . 2014 ). The advertisement call from Caseara is composed of multipulsed note, with a duration of 0.27 to 0.33 s (0.30 ± 0.02), 53 to 65 pulses per call (58.6 ± 3.5), a pulse rate ranging from 187.3 to 205.9 (196.2 ± 3.6), and a dominant frequency ranging from 4134.4 to 4306.6 Hz (4300 ± 33.8) ( Fig. 9C , Table S3 ). We focused our comparisons with two other localities of Cerrado and Amazon biomes, close to the studied area: Formoso do Araguaia municipality, Tocantins state , and Altamira municipality, Pará state (~ 300 km and ~ 700 km from Caseara, respectively). The call is consistent with both populations, but its duration is more similar to that of Tocantins population (0.27– 0.36 s , 183.1–195.3 pulses/s, 3444.4–3888.9 Hz) than to the Altamira population (0.74– 0.94 s , 165.2–201.2 pulses/s, 2888.9–4222.2 Hz). Scinax similis . This species was mainly found in open and anthropized areas. Its SVL ranged from 32.8–39.1 mm in males and 27.1–37.7 mm in females ( Table S2 ). In life, lineage presents gray to yellowish dorsum, with a light cream belly. The Scinax similis reported here is conspecific regard to the population misidentified by Silva et al . (2020) as S. x-signatus (figure 4J in the mentioned study). The advertisement call of this population presents a duration range from 0.15 to 0.29 s , with 6 to 11 pulses per call, pulse rate from 35.2 to 40.9 pulses/s, and dominant frequency ranging from 1033.6 to 4048 Hz ( Table S3 ).