Pseudopaludicola coracoralinae, Andrade & Haga & Lyra & Carvalho & Haddad & Giaretta & Toledo, 2020

Andrade, Felipe Silva de, Haga, Isabelle Aquemi, Lyra, Mariana Lúcio, Carvalho, Thiago Ribeiro de, Haddad, Célio Fernando Baptista, Giaretta, Ariovaldo Antonio & Toledo, Luís Felipe, 2020, Reassessment of the taxonomic status of Pseudopaludicola parnaiba (Anura, Leptodactylidae, Leiuperinae), with the description of a new cryptic species from the Brazilian Cerrado, European Journal of Taxonomy 679, pp. 1-36 : 13-20

Pseudopaludicola coracoralinae sp. nov.

urn:lsid:zoobank.org:act:FAB2ABCB-37D5-429C-9628-91BB62B185B6

Figs 4–5 ; Tables 3–4

Pseudopaludicola facureae from Palmeiras de Goiás, GO — Carvalho et al. 2015a: 267, 271, table 4, appendix 1–2.

Diagnosis

Pseudopaludicola coracoralinae sp. nov. is assigned to Pseudopaludicola by having a hypertrophied antebrachial tubercle (see Lynch 1989; Lobo 1995) and by its phylogenetic position within the genus. The new species is characterized by the following combination of characters: (1) upper eyelids smooth, without enlarged palpebral tubercles; (2) heel smooth, without conical tubercle; (3) single, subgular vocal sac, cream-colored with white or off-white warts; (4) terminal phalanges knobbed, without T-shaped terminal phalanges or expanded toe tips; (5) relative short hind limbs (tibio-tarsal articulation just reaching the corner of the mouth); (6) trilled advertisement call pattern, composed of 2–6 welldefined series of tonal notes, having each series of 7–116 notes, emitted at rates of 1485–2077 notes per minute.

Etymology

The specific name honors Anna Lins dos Guimarães Peixoto Bretas, better known by her pseudonym Cora Coralina. She was a simple woman, a Brazilian candy maker, writer and poetess. She was born and raised on the banks of the Vermelho River, in the municipality of Goiás, GO, and lived apart from urban centers. Cora Coralina studied until the third year of elementary school and did a typing course at the age of 70, due to a requirement of the publisher that would publish her first book. She is considered one of the most influential Brazilian writers. Although Cora Coralina wrote her first verses during her adolescence, she had her first book (Poemas dos Becos de Goiás e Estórias Mais) published in June 1965, when she was 75 years old. In 1984, the Brazilian Union of Writers awarded her the “literary personality of the year”. Following that honor, Carlos Drummond de Andrade, another distinguished Brazilian poet, said: “I admire Cora Coralina and her mastery of living in a state of grace with her poetry. Her verse is like running waters, her lyricism has the power and delicacy of the natural world.”

Type material

Holotype

BRAZIL • adult ♂; state of Goiás, municipality of Palmeiras de Goiás; 16°46′59″ S, 49°52′2″ W; 652 m a.s.l. ( Fig. 1 ); 14 Mar. 2019; F.S. Andrade and I.A. Haga leg.; GenBank: MT385245 ; ZUEC 24704 ( Figs 4 , 5A ).

Paratypes

BRAZIL • 6 adult ♂♂; same data as for holotype; GenBank: MT385243 , MT385244 ; ZUEC 24701 to 24703 , 24707 to 24709 • 5 adult ♀♀; same data as for holotype; ZUEC 24705 , 24706 , 24710 to 24712 • 4 adult ♂♂; state of Goiás, municipality of Palmeiras de Goiás; 16°50′48″ S, 49°51′51″ W; 611 m a.s.l.;

18 Dec. 2013; T.R. de Carvalho and L.B. Martins leg; GenBank: MT385241 , MT385242 ; AAG-UFU 3393 to 3396 .

Type locality

Brazil, GO, municipality of Palmeiras de Goiás (16°46′59″ S, 49°52′2″ W; 652 m a.s.l.; Fig. 1 ).

Description of the holotype

Body elliptic and broad ( Fig. 4 A–B; Table 3). Head elliptical, slightly wider than long. Snout subovoid in dorsal view and rounded in profile ( Fig. 4 C–D). Eye not protuberant. Eye diameter almost equal to interorbital distance. Interorbital area flat. Pupil rounded. Upper eyelid without tubercles. Nostril not protuberant and closer to snout tip than to eye. Canthus rostralis rounded, smooth. Loreal region slightly concave. Single subgular vocal sac, externally expanded with warty texture. Choanae rounded, well separated from each other. Vocal slits present. Tympanum membrane and annulus absent. Discrete tympanic ridge from behind eye to proximal portion of arm insertion. Mouth opening ventral. Vomerine teeth absent. Tongue ovoid, longer than wide, free posteriorly, without pigmentation at its base. Lateral of head and flanks with discrete granules. One ovoid antebrachial tubercle presents in first quarter of forearm. Finger and toe tips not expanded. Outer and inner metacarpal tubercles welldefined; outer metacarpal tubercle rounded and inner metacarpal tubercle ovoid. Fingers with single and rounded subarticular tubercles. Supernumerary tubercles absent on palm of hand. Thumb with discrete, keratinized, light brown nuptial pad, extending from base of hand to proximal limit of terminal phalanx, covering almost entire external portion of finger. Webbing absent between fingers. Relative finger lengths, when adpressed one to another: I<II<IV<III ( Fig. 4E ). Outer metatarsal tubercle well defined, conical, smaller than ovoid inner metatarsal tubercle. Toes with well-defined, single, enlarged, rounded subarticular tubercles. Supernumerary tubercles absent on sole of foot. Toes webbed basally and fringed along their sides to almost their tips. Fringes developed on all toes (mainly on II, III, IV and V). External fringe on Toe V continues almost to outer metatarsal tubercle. Well-developed fold from internal metatarsal tubercle to mid-ventral tarsus, ending in protuberant tarsal tubercle. Relative toe lengths, when adpressed one to another: I<II<V<III <IV ( Fig. 4F ). Hind limb robust with tibiotarsal articulation just reaching posterior margins of eye. Thigh shorter than tibia. Foot longer than thigh. Foot longer than tibia. Heel without tubercles. Belly skin smooth. Abdominal fold present and complete. Well-defined vertebral stripe from snout tip to vent. Dorsal surfaces of head, body and limbs smooth. Paravertebral chevron-shaped dermal ridge from behind eye to scapular region. Cloacal region smooth ( Fig. 4B ). Measurements of the holotype showed in Table 3.

Color pattern of the holotype in preservative

Dorsum brown with dark brown and black gray blotches. Belly whitish (unpigmented). Vocal sac creamcolored with white or off-white warts. Dorsum darker than dorsal surfaces of limbs. Region between upper lip and eye with several rounded white blotches with alternating vertical grey and light beige stripes. Ventral faces of arm and leg unpigmented. Palm of hand brown, pigmented. Sole of foot brown, pigmented and darker than hand, arm and hind limb. Color of sole of foot similar to that of dorsal region of hind limb. Dorsal face of arm light beige with several dark brown blotches. Dorsal face of limb light brown with dark brown transversal discontinuous stripes and with scattered brown blotches. Dark brown transverse stripes on arm (2–3), thigh (2–3), shank (2–3), foot (3–4). Light brown nuptial pads ( Fig. 4 ).

Variation in the type series

Dorsal surface of body varies from brown to dark brown, with black or dark brown irregular blotches ( Fig. 5 ). The specimen ZUEC 24705 does not have well-defined light vertebral line. The specimens ZUEC 24705–06, 24708–10 and AAG-UFU 3396 have no paravertebral chevron-shaped dermal ridges from behind the eyes to the scapular region. The specimens ZUEC 24702–03, 24706, 24710–12 and AAG-UFU 3393–96 have the region between upper lip and eye without alternating vertical stripes. The specimen ZUEC 24705 has no rounded white blotches on the region between upper lip and eye. The specimens ZUEC 24702, 24707–10, 24712 and AAG-UFU 3394 have dorsolateral stains on body, from posterior corner of eyes to almost the region of insertion of legs. The specimens ZUEC 24706, 24708–11 and AAG-UFU 3393 have no transverse stripes on arm.

Advertisement call

The advertisement call of the new species (total duration: 1.3– 25.8 s) consists of 2–6 series of stereotyped tonal notes (non-pulsed) that last 0.2– 4.1 s, separated by intervals of 0.4– 6.7 s. Before the emission of the series of stereotyped tonal notes, 12–40 (mean = 22.1, SD = 9.8) isolated notes with irregular structure, duration and interval are emitted, herein referred to as introductory notes ( Fig. 6A ). Introductory notes last 4–24 ms (mean 12, SD = 3), separated by intervals of 49–477 ms (mean = 146, SD = 27), and their dominant frequency peaks between 3.62–5.16 kHz (mean = 4.39, SD = 0.24). In contrast, within the series of stereotyped tonal notes, the notes have regular structure, duration and interval. These notes last 11–21 ms, separated by intervals of 12–61 ms, and are released at a rate of 1484.7–2076.6 notes per minute; notes have a slight increase in amplitude until the end of the first quartile of their durations, in the last quartile of their durations the notes suffer a decrease in amplitude ( Fig. 6B ). Dominant frequency peaks are between 4.18 and 5.06 kHz; the minimum frequency ranges between 3.84 and 4.59 kHz and the maximum frequency ranges between 4.41 and 5.44 kHz. The notes have a slight increase in frequency along their durations; on average, the notes have an increase of 275 Hz from the first to the third quartiles of frequencies ( Table 4). The dominant frequency coincides with the fundamental harmonic, and the second harmonic ranges between 8.34 and 10.50 kHz ( Fig. 6B ). Air temperature of recorded calls varied from 22.2 to 26.0°C. Traits that were classified as static (between-male CV<11%) to P. coracoralinae sp. nov. were note duration, notes per minute and all spectral traits. The other traits were classified as dynamic. Call quantitative traits and CV values are summarized in Table 4.

Differential diagnosis

Pseudopaludicola coracoralinae sp. nov. is promptly diagnosed from the P. pusilla species group (sensu Lynch 1989), which includes P. boliviana , P. ceratophyes Rivero & Serna, 1985 , P. llanera , P. pusilla and P. motorzinho , by the absence of either T-shaped terminal phalanges or expanded toe tips (discs or pads). The new species has terminal phalanges knobbed, similar in shape to those of P. falcipes ( Cardozo & Suárez 2012: fig. 2B). The new species is also distinguished from P. ceratophyes by having upper eyelids smooth; P. ceratophyes has upper eyelids with an enlarged palpebral tubercle ( Lynch 1989). The new species also differs from P. boliviana , P. ceratophyes , P. llanera and P. motorzinho by having a smooth heel, without enlarged, conical tubercle ( Lynch 1989; Pansonato et al. 2016).

Pseudopaludicola coracoralinae sp. nov. is promptly distinguished from the P. saltica species group that includes P. saltica , P. murundu and P. jaredi , by having short hind limbs (tibiotarsal articulation reaching near the corner of the mouth), whereas all three above-mentioned species have long hind limbs (tibiotarsal articulation extending beyond the tip of snout; Andrade et al. 2016).

The color and skin texture of the vocal sac of the P. coracoralinae sp. nov. is whitish cream with white or off-white warts ( Fig. 4B ), thereby distinguishing it from all congeners, except from P. facureae . Pseudopaludicola ameghini , P. ternetzi , P. falcipes , P. giarettai , P. hyleaustralis Pansonato, Morais, Ávila, Kawashita-Ribeiro, Strussmann & Martins, 2012 , P. canga , P. florencei , P. pocoto , P. mineira , P. restinga , P. matuta , P. mystacalis , P. ceratophyes , P. llanera , P. boliviana , P. motorzinho , P. ibisoroca Pansonato, Veiga-Menoncello, Mudrek, Jansen, Recco-Pimentel, Martins & Str ̹ssmann, 2016 and P. saltica have vocal sacs that are whitish, yellowish, or light cream with no warty texture (combined characters of the vocal sac of all above-mentioned species: Miranda-Ribeiro 1937; Ruthven 1916; Rivero & Serna 1985; Haddad & Cardoso 1987; Lynch 1989; Lobo 1994; Giaretta & Kokubum 2003; Carvalho 2012; Pansonato et al. 2012, 2013, 2016; Roberto et al. 2013; Magalhṳes et al. 2014; Carvalho et al. 2015b, Andrade et al. 2017a, 2018a, 2018b; Cardozo et al. 2018); P. jazmynmcdonaldae has a dark and smooth vocal sac with no warty texture ( Andrade et al. 2019); and P. atragula has a white vocal sac with warty texture and dark-colored reticulations ( Pansonato et al. 2014a).

The trilled pattern of its advertisement call (presence of non-pulsed notes) promptly distinguishes the new species from all species of Pseudopaludicola that have notes with pulsatile structure (pulses separated by silence intervals or not): P. ameghini , P. atragula , P. boliviana , P. falcipes , P. florencei , P. ibisoroca , P. jaredi , P. jazmynmcdonaldae , P. matuta , P. mineira , P. motorzinho , P. murundu , P. mystacalis , P. pocoto , P. restinga , P. saltica and P. ternetzi ( Haddad & Cardoso 1987; Duré et al. 2004; Pereira & Nascimento 2004; Pansonato et al. 2013, 2014 a, 2014b, 2016; Magalhṳes et al. 2014; Andrade et al. 2016, 2017a, 2017b, 2018a, 2018b, 2019; Cardozo et al. 2018).

Acoustic comparison with its sister species

Pseudopaludicola coracoralinae sp. nov. and P. facureae are indistinguishable in external morphology, but the new species was recovered as a sister species of P. facureae + P. atragula ( Fig. 3 ). Furthermore, the RF multivariate approach applied to morphometric data indicated a broad overlap between the two partitions ( Fig. 7 A–B), with a considerable classification error ( Table 5 ). In relation to three species of Pseudopaludicola that share the trilled advertisement call pattern ( P. hyleaustralis , P. facureae and P. canga ), P. facureae is the one with the most similar call to that of P. coracoralinae sp. nov. The trait of notes per minute distinguishes the new species (1485–2077 notes per minute) from P. canga and P. hyleaustralis (368–1286 notes per minute; combined values, Table 1 ; see Carvalho et al. 2015a). The RF multivariate analysis on acoustic data indicated a complete segregation between P. coracoralinae sp. nov. and P. facureae , without any classification error ( Table 5 ; Fig. 7C ). Notes per minute ( P. coracoralinae sp. nov. 1796 ± 123 (1485–2077) vs P. facureae 1383 ± 192 (512–1843)), number of series per call ( P. coracoralinae sp. nov. 3 ± 1 (2–6) vs P. facureae 10 ± 6 (4–20)) and number of notes per series ( P. coracoralinae sp. nov. 29 ± 16 (7–116) vs P. facureae 17 ± 18 (2–93)) were the main sources of variation in both variable importance measurements ( Fig. 7D ). In addition to these abovementioned traits, we found differences (P Ĕ0.01) between these two species in note duration, internote interval, series of notes duration, interseries interval and dominant frequency.

Phylogenetic inference and genetic distances of the new species

Pseudopaludicola coracoralinae sp. nov. was recovered as a sister species of the P. atragula + P. facureae clade ( Fig. 3 ). Uncorrected genetic distance between the P. coracoralinae sp. nov. and P. atragula was 4.5% (mean value), and from P. facureae , it was 4.9% (mean value). The maximum intraspecific distance was 0.4% (Supplementary file 2). No molecular data are available for P. ceratophyes , P. hyleaustralis and P. ibisoroca ; however, the new species is easily diagnosed from these species by morphology and acoustics (see further details in Differential diagnosis section).

Natural history notes

Males of the new species were found calling in a partially flooded open area surrounded by a newly planted cornfield (corn stalk <40 cm tall). We collected the holotype and ZUEC’s paratypes at this site. The AAG-UFU’s paratypes were collected in another partially flooded open area near to a permanent lagoon at the margins of the GO-156 highway. We observed three couples in axillary amplexus in the field. In our field recordings of vocalizations, the males were vocalizing well-spaced from each other, without any close-range encounters. The new species was observed syntopically with Leptodactylus fuscus (Schneider, 1799) and Physalaemus marmoratus (Reinhardt & L̹tken, 1862) at its type locality. Curiously, the congener Pseudopaludicola mystacalis was observed about 50 meters in a similar partially flooded open area surrounded by the same cornfield. We heard and observed only P. mystacalis at this site, not P. coracoralinae sp. nov.

Distribution

Pseudopaludicola coracoralinae sp. nov. is known only from the type locality ( Fig. 1 ). However, we are aware of other populations that have trilled advertisement calls similar to those of P. coracoralinae sp. nov. and P. facureae . These populations occur in Limeira do Oeste, MG ( Andrade & Carvalho 2013); Goianésia, Piracanjuba and in the Altamiro de Moura Pacheco State Park, all in GO, Brazil ( Guimarṳes et al. 2001; Carvalho et al. 2015a; Ramalho et al. 2018). Goianésia is about 180 km northeast from the type locality of P. coracoralinae sp. nov., Piracanjuba is about 100 km southeast and the Altamiro de Moura Pacheco State Park is about 80 km northeast. Limeira do Oeste is closer to the type locality of P. facureae , about 250 km east. However, the specific identities of these populations will only be confirmed when their genetic information is available because they are morphologically and acoustically cryptic.

Figures

Fig. 4. Pseudopaludicola coracoralinae sp. nov., holotype (ZUEC 24704, SVL = 13.1 mm), an adult ♂ from Palmeiras de Goiás, GO, Brazil. A. Dorsal view. B. Ventral view. C. Head, lateral view. D. Head, dorsal view. E. Right hand, ventral view. F. Right foot, ventral view. Scale bar (only for C, D, E, F) = 5 mm.

Fig. 5. Holotype and five paratypes of Pseudopaludicola coracoralinae sp. nov. in life. A. ZUEC 24704 (holotype, adult ♂ and call voucher), SVL = 13.1 mm. B. ZUEC 24703 (adult ♂ and call voucher), SVL = 13.2 mm. C. ZUEC 24707 (adult ♂), SVL = 12.5 mm. D. ZUEC 24712 (adult ♀), SVL = 16.0 mm. E. ZUEC 24705 (adult ♀), SVL = 16.8 mm. F. ZUEC 24706 (adult ♀), SVL = 17.0 mm.

Fig. 1. Partial map of South America showing the Brazilian domains and samples of the species included in our molecular, morphological and acoustic comparisons. The type localities of the species are indicated with stars: Pseudopaludicola coracoralinae sp. nov. in Palmeiras de Goiás, GO (red star), P. facureae Andrade & Carvalho, 2013 in Uberlândia, MG (blue star), P. canga Giaretta & Kokubum, 2003 in Marabá, PA (yellow star) and P. parnaiba Roberto, Cardozo & Ávila, 2013 in Ribeiro Gonçalves, PI (green star). Municipalities:1 = Barreirinhas (MA); 2 = SantoAmaro do Maranhão (MA); 3 =Aragominas (TO); 4 = Palmas (TO); 5 = Mateiros (TO); 6 = São Desidério (BA). Veiga-Menoncello et al. (2014) first noticed a taxonomic unit which they called as Pseudopaludicola sp. 3 from Barreirinhas, MA. Since then it has been treated as a species not yet formally described. It is represented here as P. canga from the localities 1 and 2.

Fig. 6. A. Oscillogram of the entire advertisement call of Pseudopaludicola coracoralinae sp. nov. with the introductory notes followed by three series of tonal notes. B. Audiospectrogram (top) and corresponding oscillogram (bottom) detailing three notes. The male was recorded on 8 November 2016 at 18:08 h; air temperature 26°C, water temperature 29°C; recording_label: Pseudop_ coracoralinaePalmeirasGoiasGO5cFSA_AAGmt.

Fig. 3. Maximum likelihood tree recovered for the phylogenetic relationships of Pseudopaludicola Miranda-Ribeiro, 1926 based on the 12S rRNA, tRNA-val and 16S rRNA mitochondrial genes. Numbers near the nodes are bootstrap values and black dots represent bootstrap = 100; support below species level is not shown.

Fig. 7. A, C. First and second dimensions of the Multidimensional scaling on the proximity scores from the randomForest analysis of adult males of Pseudopaludicola coracoralinae sp. nov. from the type locality (red dots) and P. facureae Andrade & Carvalho, 2013 from the type locality (blue dots). A. Morphometric traits. C. Acoustic traits. Each dot represents an adult male. The circles around the dots represent how males were classified. B, D. Dotcharts of variable importance score as indicated by the randomForest analysis. B. Morphometric traits. D. Acoustic traits.