Physalaemus carrizorum, Cardozo & Pereyra, 2018

Cardozo, Dario E. & Pereyra, Martin O., 2018, A new species of Physalaemus (Anura, Leptodactylidae) from the Atlantic Forest of Misiones, northeastern Argentina, Zootaxa 4387 (3), pp. 580-590 : 582-587

Physalaemus carrizorum , new species

Synonyms

Paludicola gracilis Boulenger, 1883 : Berg, 1896 (partim); Nieden, 1923 (partim); Miranda-Ribeiro, 1926 (partim).

Physalaemus gracilis ( Boulenger, 1883) : Parker, 1927 (partim); Freiberg, 1942 (partim); Cochran, 1955 (partim); Cei, 1956 (partim); Cei and Roig, 1961; Gallardo, 1961; Barrio, 1965 (partim); Gallardo, 1966; Cei, 1980 (partim); Frost, 1985 (partim); Cei, 1987 (partim); Langone, 1989 (partim); Gallardo and Varela, 1992 (partim); Klappenbach and Langone, 1992 (partim); Duellman, 1993 (partim); Langone, 1994 (partim); Achaval and Olmos, 1997 (partim); Lavilla et al., 2000 (partim); Lavilla and Cei, 2001 (partim); Nascimento et al., 2005 (partim).

Physalaemus aff. gracilis: Vaira et al., 2012 .

Physalaemus sp . ( aff. gracilis ): Kwet, 2001.

Physalaemus sp.: Lourenço et al., 2015.

Holotype (fig. 2, table 2). MACN 35081 (adult male) collected on 10–18 February 1994 by J.C. Baciluk, J. Faivovich and M. López at “ INTA, campo anexo cuartel Río Victoria ” (26°58’S, 54°29’W, datum WGS 84; 550 m above sea level [asl]), San Vicente , National Route 14 km. 1025, Departamento Guaraní, Misiones province, Argentina .

Paratopotypes (table 2). MACN 35082–4 (adult males) with the same data as holotype . MACN 49611–2 (adult males) collected on 5–18 January 1995 by J.C. Baciluk and J. Faivovich . MACN 50747 (adult male) collected on 12 December 2001 by J. Faivovich, S. Nenda, and A. Sehinkman. Paratypes (table 2). All the paratypes collected in Misiones province, Argentina at Departamento Cainguás: MACN 50755 (male) collected on October 1972 by A. Barrio and J. Poirot at Arroyo Moncholito and Arroyo Central, General Belgrano . MACN 50757 (female) collected on 14 September 1971 by J. Foerster at 2 de Mayo (27°2’23”S, 54°40’30”W; 505 m asl) . LGE 15330 (female) collected on 22 June 2004 at Private Reserve Tangára (27°00’S, 54°7’W; 300 m asl), by D. Cardozo and M. Giménez. Departamento General Manuel Belgrano: MACN 30156 (male) collected on 10 August 1972 by C. and M. Stiebel , MACN 50748 (female) collected on 11 March 1969 by A. Barrio , and MACN 50749 (male) collected on 25 January 1971 by J. Enriquez, at Bernardo de Irigoyen (26°15’16”S, 53°38’50”W, 815 m asl) , MACN 50750 (male) collected on 17 October 1971 by A. Barrio, MACN 50751 (male) collected on October 1972 by A. Barrio and J. Poirot , MACN 50752–4 (males) and 50756 (female) collected on 17 October 1971 by “ Comisión Vertebrados FCEN ”, and MACN50758–75 (females, males) collected on 12 October 1971 by “ Comisión Vertebrados FCEN ”, at Arroyo Moncholito (26°3’06”S, 53°49’56”W; 497 m asl. Departamento San Pedro: MACN 34103 (male) collected on 5 August 1985 by T. Waller, and MACN 40763 (male) collected on 26 September 2010 by B.L. Blotto, L. Nicoli, M.O. Pereyra, and A. Sehinkman, at Parque Provincial Cruce Caballero (26°31’S, 53°59’W; 590 m asl) . MACN 37030 (subadult) collected on 9 February 1996 at Colonia La Flor, El Soberbio, (27°9’S, 54°8’W; 375 m asl) by E. Krauczuk. LGE 8877 (male) , LGE 15314–5 (female, male), and LGE 15317–23 (seven males) collected on 27–30 August 2005 at Parque Provincial Moconá (27°10’S, 53°54’W; 250 m asl), El Soberbio by E. Krauczuk . LGE 15316 (male) collected on 21 June 2009 by E. Krauczuk , LGE 15324 (male) collected on 28 April 2007 by D. Baldo , E. Castillo , and M.O. Pereyra, and LGE 15656 and 15659 (juveniles) collected on 12 February 2001 by D. Baldo and E. Krauczuk, at Parque Provincial El Piñalito, San Pedro (26°25’33”S, 53°50’21”W; 760 m asl) . Departamento 25 de Mayo: LGE 15325–328 (two males, two females) collected on 22 September 2007 at Puerto Londero, intersection Arroyo Los Muertos and Provincial Route 2 (27°22’12”S, 54°24’30”W; 130 m asl), 25 de Mayo, by D. Baldo, L. Cotichelli, J.M. Ferro, M. Giombini, and M.O. Pereyra.

Diagnosis. Physalaemus carrizorum sp. nov. is diagnosed by a combination of morphological and acoustic characters: 1) large size (mean SVL (mm) = 32.0 males; 34.0 females); 2) slender body aspect; 3) head longer than wide; 4) supratympanic fold developed, curved toward the arm insertion; 5) A light median stripe on throat, chest, and/or abdomen; 6) medium sized inguinal glands; 7) tarsal tubercle present; 8) supernumerary tubercles on hands and feet; 9) advertisement call non-pulsed, with descendant frequency modulation;10) call duration 2.40 s (2.246– 2.513 s); 11) fundamental frequency 2270.33 Hz (2179–2361 Hz).

Comparison with other species. The new species could be differentiated from all the species of Physalaemus not belonging to the P. gracilis group (see Lourenço et al., 2015) by having a median stripe defined by the absence of melanocytes on throat, chest, and/or abdomen which is a putative synapomorphy of the P. gracilis group. The only exception is P. riograndensis , of the P. biligonigerus group, that have a similar pattern ( Milstead, 1960) with an independent phylogenetic origin (see Lourenço et al., 2015: fig. 4–5). However, the new species clearly differs from P. riograndensis in having inguinal glands, larger adult size (> 25 mm vs. <20.5 mm), and a dorsal skin texture near smooth (vs. tuberculate in P. riograndensis ). Physalaemus carrizorum sp. nov. could be differentiated from the remaining species of the P. gracilis group by the presence of a supratympanic fold developed, curved towards the arm insertion (supratympanic fold poorly developed in P. barrioi, Provete et al., 2012 ; supratympanic fold not evident in P. evangelistai , P. gracilis , P. lisei , and P. jordanensis ). In addition, the largest SVL (mm) (27.4–36.7 males; 31.5–35.1 females, table 2) separates P. carrizorum sp. nov. from P. evangelistai : 21.5–23.0 mm in males ( Bokermann, 1967); P. lisei : 23.1–25.0 mm in males, 24.2–29.0 mm in females ( Braun & Braun, 1977), P. jordanensis 24.0 mm in holotype (male), 27.0 mm in allotype (female) ( Bokermann, 1967).

Physalaemus carrizorum sp. nov. presents longer call duration (2.148– 2.880 s.) than P. barrioi (1.030– 1.720 s., Provete et al., 2012), P. evangelistai (1.0– 1.2 s.; Bokermann, 1967), P. jordanensis (0.62– 1.204 s; Giaretta et al., 2009), and P. gracilis (0.707– 1.123 s.; this work). The new species can be distinguished from P. jordanensis by the absence of pulsed notes (pulsed advertisement call in P. jordanensis ; Bokermann, 1967; Giaretta et al., 2009), and from P. lisei by having descendant modulation of the call (ascendant modulation in P. lisei, Morais & Kwet, 2012 ).

Description of holotype (fig. 2). Slender body aspect. Narrow head, longer than wide (HL/HW= 1.1). Snout long, subacuminate in dorsal view, protruding from the jaw in lateral view. Eyes slightly protuberant. Pupil horizontal. Tongue piriform and free. Vomerine teeth absent, maxillary teeth present. Canthus rostralis rounded. Loreal region concave. Tympanic annulus visible under skin, tympanic membrane poorly evident. Supratympanic fold pronounced, curved towards arm insertion. Dorsum with small glands arranged in longitudinal irregular folds, with some isolated rounded glands in the head, eyelids and the sacral region. Inguinal glands, medium sized, rounded not prominent. A thin urostilar vertebral line is evident. Ventral surface smooth, with flat granules in thighs. Vocal sac well-developed, with lateral folds. Arms short, fingers without fringes or webbing. Length of the fingers II = V <III <IV. Prominent metacarpal tubercles: external rounded, internal ovoid. Evident subarticular tubercles on hands, with numerous and prominent supernumerary tubercles. Nuptial pad on thumbs, covering the inner region of the internal metacarpal tubercle. Tibia longer than femur. Finger and toe tips not expanded. Toes formula I<II<V<III<IV. External metatarsal tubercle small, internal metatarsal tubercle ovoid. Tarsal tubercle, small and rounded. Tarsal fold poorly developed. Subarticular tubercles developed, multiple and prominent plantar supernumerary tubercles.

Measurements of holotype (in mm). SVL 31.5; HL 10.1; HW 9.5; ED 3.1; TD 2.0; IOD 2.6; IND 2.3; TL 14.9; THL 14.3; FL 17.0.

Color in preservative. The holotype and the rest of the specimens examined vary in the dorsum coloration from brown pale to grayish, with the anterior region of the head lighter (dorsal view). Urostilar vertebral line thin and whitish. Inguinal gland black, delimited by a white border. Anterior limbs with similar pattern than dorsum, with a dark irregular spot at the inner portion in the middle of the forearms. Dorsum of posterior limbs with dark bars crossing the femur and tibia. In lateral view, the head is light with a thin dark stripe at the tip of the snout and a dark stripe extending from postorbital region to groin, bordered by small white spots. In addition, the dorsal pattern could be with irregular shapes, tending to form a dorsal ovoid spot in the middle of the pectoral girdle, or homogenous without a defined pattern.

As in living specimens, the belly presents the gular region, chest, and posterior region of the abdomen densely spotted (marbled) dark brown on a whitish background, with the posterior region of the abdomen less spotted. An irregular stripe in the ventral region could be extended from the mental region to the middle of abdomen in some specimens (fig. 3B), whereas in others, this stripe is minimally discernible or not evident in the abdominal region (fig. 2B) or throat. This line is not evident in specimens MACN 50751, and 50770. In some males, the lateral region of the vocal sac is light brown, and the withe spot bordering the mandibular are less evident. In addition, the reddish coloration present in thighs, inguinal region and tibia disappear in preservative. All males have beige to light brown colored nuptial pads.

Variation. Scant variation is observed between the holotype and the rest of the specimens examined. The lateral and ventral pattern is constant. However, the dorsal skin is nearly smooth in some paratypes (LGE 15315, 15319), while in others could be observed some isolated granules in eyelids and head (LGE 15314, 15321), dispersed through the dorsum (LGE 15320), or flanking the urostilar vertebral line (LGE 8877, 15326). Most of specimens have uniformly brownish dorsum, with the antero dorsal region of the head lighter brown or green (fig. 3A). All specimens have a thin urostilar vertebral line, from the cloacal to the pelvic region. This urostilar vertebral line is white in most of specimens, but green in those specimens that have the dorsal region of the head green. The inguinal region, outer portion of thigh and inner of tibia are reddish (ventral view, fig. 3B). The black inguinal spots are bordered with yellow. An irregular dark brown interorbital spot is present in some specimens. In ventral view, the gular region, chest, and posterior region of the abdomen are always densely spotted on a white background, with the posterior region of the abdomen less spotted. An irregular stripe in the ventral region is defined by the absence of melanocytes in the medial line. In some males, the lateral region of the vocal sac is brown, and the border of the mandibular is densely spotted with white dots (fig. 3B). All males have beige to light brown nuptial pads.

Advertisement call (fig. 4). The advertisement call of Physalaemus carrizorum sp. nov. (n = 20) is composed by a single, long, and non-pulsed note, with a slightly descendant modulation. With the equipment used, we detected between 7–12 S-shaped harmonics, with decreasing frequency modulation. The mean call duration is 2.40 s (2.246– 2.513 s); fundamental frequency 432.67 Hz (409–455), and dominant frequency 2270.33 Hz (2179– 2361). Calls are given at a rate of 7.21 calls/minute (4.83–10.11).

Geographic distribution. Physalaemus gracilis ( Boulenger, 1883) , was first cited for Argentina (Misiones and Buenos Aires provinces, as Paludicola gracilis ) by Berg (1896) without reference specimens. In subsequent lists of amphibians of Argentina, some authors continued using Berg´s reference ( Freiberg, 1942; Cei, 1956). Cei and Roig (1961) and Barrio (1965) presented new data and reported specimens from Misiones province as Physalaemus gracilis . Subsequent works (e.g., Cei, 1980, 1987; Gallardo, 1966; Gallardo & Varela, 1992; Lavilla et al., 2000; Lavilla & Cei, 2001) cited P. gracilis for Argentina based on those reports. Barrio (1965) also cited this species for Corrientes province, but provided no reference specimens. No voucher specimens from Corrientes are currently deposited in Barrio´s herpetological collection (Ex CENAI, now in MACN). Gallardo (1966) and Contreras and Contreras (1982) also mentioned this species for some localities in Corrientes province but they did not provide voucher information. Contreras (1982) reported P. gracilis for Chaco Province, but all the reported specimens correspond to P. biligonigerus . Based on the specimens examined by us, we found that Physalaemus carrizorum sp. nov. is present in Argentina only in some localities of Misiones province (fig. 5). The species is likely to occur in neighboring Brazil. For instance, the advertisement call assigned to P. aff. gracilis from Pró- Mata, Rio Grande do Sul state ( Kwet, 2001) match the call duration length of P. carrizorum sp. nov. However, the quality of the advertisement call is poor, and the taxonomic status of this population should be reassessed. In the same way, the voucher specimen USMN 103684 cited as P. gracilis for Nova Teutônia, Santa Catarina, Brazil, by Cochran (1955) have similar morphological traits than P. carrizorum sp. nov. being tentatively assigned to the new species.

Etymology. The new species is dedicated to Gustavo R. Carrizo and his sons, Rodrigo and Ramiro Carrizo.

Remarks. Barrio (1965) described the advertisement call of Physalaemus gracilis from Oberá, Misiones, Argentina, presenting a spectrogram ( Barrio, 1965; Lam. V. 6), but in the Specimens Examined Section, only one voucher from Argentina (Tobuna, Misiones province) is referred (MACN 2967). However, the characteristics of this advertisement call, for example call duration (0.9– 1.0 s) and dominant frequency (4000–5000 Hz), diverge remarkably from those of P. carrizorum sp. nov. (2.246– 2.513 s and 2179–2361 Hz respectively). The analyzed advertisement call from Montevideo, Uruguay (this work) shares with Barrio’s spectrogram the length of the advertisement call. However, the dominant and fundamental frequencies are not in concordance with those of P. gracilis , or with any species of Physalaemus present in Argentina, although this could be consequence of the equipment used to record the advertisement call and the methodology employed in the analysis. Since Barrio (1965) reported having heard the call of P. gracilis in Uruguay and Rio Grande do Sul ( Brazil), we believe that the recording used for his call description may belong to a specimen of this species from those places, and does not belong to P. carrizorum sp. nov.