Elachistocleis cesarii ( Miranda-Ribeiro, 1920 )

Toledo, Luís Felipe, Loebmann, Daniel & Haddad, Célio F. B., 2010, Revalidation and redescription of Elachistocleis cesarii (Miranda-Ribeiro, 1920) (Anura: Microhylidae), Zootaxa 2418, pp. 50-60 : 52-59

Elachistocleis cesarii ( Miranda-Ribeiro, 1920)

Engystoma ovale cesarii Miranda-Ribeiro, 1920

Engystoma ovale lineatum Miranda-Ribeiro, 1920

Lectotype. MZUSP 529, an adult male, collected at municipality of Piquete, state of São Paulo, southeastern Brazil (approximately 22° 36’ S; 47° 10’ W; 675 m above sea level), on November 1896 by Zech ( Figure 1 ).

Paralectotypes. – MZUSP 33 collected on January 1900 by Hempel, at Ipiranga (Ypiranga), municipality of São Paulo; MZUSP 36 (gravid female) collected on October 1896 by Bicego, at municipality of Perus; MZUSP 37 (gravid female) collected on 1897 by Bicego, at municipality of Cubatão; MZUSP 38 collected on January 1898 by Bicego, at Belém, municipality of São Paulo; MZUSP 42 (gravid female) collected on October 1907 by Ruedervalt and Cheubel at Ipiranga (Ypiranga), municipality of São Paulo; MZUSP 264 (gravid female) collected together with the lectotype; MZUSP 715 collected on 1896 by Bicego, at Alto da Serra; MZUSP 2023 (gravid female) collected on 1897 by Bicego at municipality of Cubatão; MZUSP 2024- 27 (gravid females; except for 2025 which resembles an young male) collected on October 1896 by Bicego at municipality of Perus. All municipalities are in the state of São Paulo, southeastern Brazil.

Diagnosis. Elachistocleis cesarii is recognized by the following combination of characters: 1) ventral coloration is white or yellow with gray marks and reticulations; 2) presence of postcommisural glands behind the corner of mouth; 3) tympanum concealed; 4) advertisement call with the mean dominant frequency of about 3.5 kHz.

Comparison with other species. In life, Elachistocleis cesarii is readily distinguished from E. erythrogaster by the absence of the reddish coloration of the ventral portion of its body (see Figures 2 C, D and 3 C, D), its smallest body size, and the presence of a well defined femoral stripe (not well defined in E.

erythrogaster ). Besides this, the frequency of the advertisement call of E. cesarii is lower than that reported to E. erythrogaster (see Kwet & Di-Bernardo 1998; 1999). E. cesarii is distinguished from E. surinamensis by its smaller size (mean of 32.3 mm in males of E. surinamensis ) and by differences in body coloration (see plate XIII in Kenny 1969, and Figures 3 C, D, and E). E. cesarii is distinguished from E. bicolor and E. ovalis by the absence of the immaculate, yellow, ventral coloration (spotted in E. cesarii ) (see Lavilla et al. 2003 and Figures 2 A, B and 3 C, D). E. cesarii is distinguished from E. skotogaster by presenting postcommisural glands (absent in E. skotogaster ; see Figure 2 E) and by its smaller size (minimum size of 27.5 in males of E. stokogaster ). E. cesarii is distinguished from E. piauiensis by some advertisement call parameters: the call frequency is lower and call duration is shorter in E. cesarii than in E. piauiensis (see Table 2 ). Besides this, E. cesarii has a smaller postcommisural gland (more conspicuous in E. piauiensis ) and the blotches of the inguinal region are less conspicuous in E. piauiensis than in E. cesarii . In figures 2 and 3 it is possible to observe dorsal and ventral color patterns of some species of Elachistocleis in life.

Description of the lectotype. Body robust and ovoid. Texture of the dorsal skin and undersurface of the body smooth. Skin on ventrolateral surface of body and area around the cloacal region smooth. Cloacal flap absent; vent opening positioned posterodorsally. Head small and triangular, broader than long. Cranial crests absent. A conspicuous dorsolateral skin fold from the arms to the groin. Another skin fold crossing the chest between axillae. Eyes small, slightly prominent. Snout pointed in dorsal view and protruding in lateral view. Nostrils directed anterolaterally, slightly protuberant. Choanae relatively small and round. A well developed groove in the terminal part of the lower jaw. Internarial distance small. Canthus rostralis distinct, rounded. Loreal region slightly convex. Interorbital space slightly convex. Lips nearly horizontal when belly is touching the ground. Presence of postcommisural glands behind the corner of mouth. Tympanum concealed. Supratympanic fold absent. Upper jaw projects 1.59 mm beyond the lower jaw. Subgular vocal sac not expanded externally. Vocal slits present. Vomerine odontophores absent. Tongue large, oval. Arms and fingers robust and short. Legs extremely robust; almost equal lengths of thigh, tibia, and foot. Finger lengths I<II<IV<III. Toe lengths I<II<V<III<IV. Fingers and toes without webbing, fringes, or ridges. Finger and toe tips rounded, not flattened or expanded in discs; terminal grooves absent. Supernumerary tubercles absent in hands and feet. Large oval inner metatarsal tubercle. Outer metatarsal tubercle absent. Presence of a large oval thenar tubercle and a longitudinally divided palmar tubercle in hand. Nuptial asperities on males' thumb absent.

Color in life of individuals apart from the type series ( Figure 3 C, D). – Dorsum and limbs are dark brownish gray with small white dots. The single, subgular vocal sac is darker than the venter. The chest is yellow with gray marks. Belly white or yellow, with gray marks and reticulations, which reach the flanks. Orange femoral stripe present on the posterior surface of the thigh. Orange inguinal spots present. There is a tiny white vertebral line from the snout to the vent.

Color in preservative of individuals other than the type series (70% ethanol). – Dorsum and limbs are dark grayish blue. Ventral region is gray with white spots. These spots reach up to the lateral portion of the animals. The throat is darker than chest and belly. The inguinal spots and femoral stripes on the posterior surface of the thigh are white. Vertebral line undistinguished.

Variation. Females are larger than males (see Table 1 ). Females present variation in size, with the SVL varying from 19.4 up to 42.7 mm ( Thomé & Brasileiro, 2007). The vertebral stripe may be absent. The ventral spots may not reach the flanks and the groin region of some individuals. The throat of males is darker than that of females.

Call descriptions. Advertisement calls of E. cesarii were recorded in Itapé, municipality of Rio Claro, São Paulo state, Brazil, on 29 January 2002, at air temperature of 23.1 ºC ( Figure 4 ). The call consists of a loud, high pitched, sustained whistle, ranging from 1.49 to 2.66 s of duration, with a mean dominant frequency of 3,515 Hz, with a mean pulse rate of 238.2 per second, and 460.2 pulses per note in average. The frequency ranged from 3.01 to 4.17 kHz. The duration of the pulses did not vary much (mean of 4.23 ± 0.16 ms; n = 50). Further spectral characteristics are presented in Table 2 (see also Figure 4 ).

Advertisement calls of E. piauiensis were recorded in the municipalities of Pacatuba on 13 March 2007 (air temperature 22 ºC), Caucaia on 15 May 2005 (air temperature 27 ºC), and Viçosa do Ceará on 24 April 2007 (air temperature 25 ºC), all of them in the state of Ceará, Northeastern Brazil. The call structure of E. piauiensis is very similar to that of E. cesarii and consist of a loud, high pitched, sustained whistle (ranging from 2.45 to 2.51 s of duration). The duration of the pulses did not vary much (3.00 ± 0.23 ms; n = 50). However, the mean dominant frequency is higher in E. piauiensis (4.53 ± 0.06 Hz) compared to the new species and the frequency ranged from 3.18 to 5.10 kHz ( Table 2 ; Figure 4 ).

Tadpoles. Tadpoles are unknown; however, 10 tadpoles collected in the municipality of Vitória Brasil, state of São Paulo, Brazil, and briefly described under the name Elachistocleis sp. by Rossa-Feres and Nomura (2006), could be E. cesarii .

Natural history notes. Elachistocleis cesarii calls during the wet and hot season of the year (summer) as a prolonged breeder; however, after heavy rains during the hot nights it may behave like an explosive breeder (sensu Wells 1977). Males call with the legs in the water and the body out of water, holding the emergent vegetation with the forelimbs. The amplexus is axillar. We collected two amplected pairs that laid eggs in plastic bags. One female deposited 736 eggs and the second deposited 1126 eggs. In nature, the eggs are laid in the water surface as a gelatinous mass attached to floating or emergent vegetation ( Figure 3 F). Newly metamorphosed specimens have a mean SVL of 11.83 mm ± 0.38 (11.4 – 12.3; N = 6). The ecology of this species has been studied by Thomé and Brasileiro (2007) and a short communication about the defensive posture was published by Toledo (2004), in both articles under the name Elachistocleis cf. ovalis .

Geographical distribution. Besides the localities of the type series, the species is known in the municipalities of Rio Claro, Campinas, Itirapina, São Paulo, Angatuba, and Ubatuba, all in the state of São Paulo. In the state of Minas Gerais it can be found in the municipalities of Jaboticatubas, Santana do Riacho, Munhoz, and Viçosa. In the state of Goiás it can be found in Pontalina ( Figure 5 ).

Etymology. The meaning of the specific name of E. cesarii was not stated in the original description.

Discussion. The taxonomic status of Elachistocleis ovalis remains unclear. This fact limits the recognition of several related still undescribed species in South America. These species are incorrectly being referred to as E. ovalis and even E. bicolor in the past and current literature, as well as in museum collections. The lack of correct identification of all those taxa has direct implication in conservation, as some of them may be endangered or may be endemic to certain localities, countries or biomes. Therefore, a taxonomic review of the genus urges attention and may reveal a great hidden biodiversity.

Additional specimens examined. Elachistocleis bicolor : CFBH 3841; 3859; 4010 São Domingos, state of Santa Catarina, Brazil; CFBH 4225 Tabapuã, state of São Paulo, Brazil; CFBH 13608-10 Três Lagoas, state of Mato Grosso do Sul, Brazil; CFBH 18199 Bom Jesus, state of Rio Grande do Sul, Brazil. E. cesarii : CFHB 4132–37; 4147–48; 4209; 4230–31; 4233–37; 4256–7 Rio Claro, state of São Paulo, Brazil; ZUEC 8054 Campinas, state of São Paulo, Brazil; ZUEC 12031 Itirapina, state of São Paulo, Brazil, CFBH 4997 Itirapina, state of São Paulo, Brazil; CFBH 3768 Pontalina, state of Goiás, Brazil; CFBH 6575-6578 Rio Claro, state of São Paulo, Brazil; CFBH 10907 Ubatuba, state of São Paulo, Brazil; CFBH 23136 Angatuba, state of São Paulo, Brazil; ZUEC 599-600 São Paulo, state of São Paulo, Brazil; ZUEC 4246-48, 4250-51, 4263 Munhoz, state of Minas Gerais, Brazil; ZUEC 1417-18, 2848, 2862-63, 3031-32, 3069, 3072-76 Jaboticatubas, state of Minas Gerais, Brazil; ZUEC 6157 (adult male recorded) Viçosa, state of Minas Gerais, Brazil; ZUEC 4995-97 Santana do Riacho, state of Minas Gerais, Brazil. E. erythrogaster : MNRJ 39098 adult male, Paratype. E. piauiensis : CFBH: 15880; 15902-03; 23465-71 Viçosa do Ceará, state of Ceará, Brazil. E. surinamensis : ZUEC 9422–23 Rapidos de Komoiran, Estado Bolivar, Venezuela.

Figures

FIGURE 1. Lectotype of Elachistocleis cesarii MZUSP 529 in dorsal (A) and ventral views (B).

FIGURE 2 Dorsal and ventral views of: Elachistocleis bicolor from the state of Rio Grande do Sul, Brazil (A and B, respectively); E. erythrogaster from the municipality of São Francisco de Paula, state of Rio Grande do Sul, Brazil (C and D, respectively); E. skotogaster from Aguas Blancas, provincia de Salta, Argentina (E and F, respectively).

FIGURE 3. Dorsal (A) and ventral (B) views of Elachistocleis piauiensis from the municipality of Viçosa do Ceará, state of Ceará, Brazil; dorsal (C) and ventral (D) views of E. cesarii from Itapé, municipality of Rio Claro, state of São Paulo, Brazil (In C an arrow indicates the postcommisural gland); (E) dorsal view of E. surinamensis from Trinidad and Tobago; (F) gelatinous egg mass of Elachistocleis cesarii photographed in nature, where it is possible to visualize the embryos in development inside the egg capsules.

FIGURE 4. Spectrograms (above) and waveforms (below) of the advertisement calls of (A) Elachistocleis cesarii recorded in the district of Itapé, municipality of Rio Claro, São Paulo, Brazil, on 29 January 2002, air temperature of 23.1 ºC and (B) Elachistocleis piauiensis recorded in the municipality of Caucaia, Ceará, Brazil, on 15 May 2005, air temperature of 27 ºC.

FIGURE 5. Geographic distribution map of Elachistocleis cesarii in the states of São Paulo (SP), Minas Gerais (MG), and Goiás (GO), Brazil. Gray triangle represents the type locality (municipality of Piquete, São Paulo) and black circles represent other localities based on specimens deposited in scientific collections.

Tables

TABLE 2. Advertisement call parameters of Elachistocleis cesarii (two males) and E. piauiensis (three males). Values presented as mean ± standard deviation (range). Data on environmental temperatures and places of recordings are in the text.

	E. cesarii	E. piauiensis
Dominant frequency (kHz)	3.52 ± 0.08 (3.60 – 3.45; n = 8)	4.53 ± 0.06 (4.48 – 4.65; n = 18)
Minimum frequency (kHz)	3.13 ± 0.09 (3.01 – 3.23; n = 8)	3.41 ± 0.25 (3.18 – 3.76; n = 18)
Maximum frequency (kHz)	4.03 ± 0.11 (3.90 – 4.17; n = 8)	5.00 ± 0.09 (4.86 – 5.10; n = 18)
Call duration (s)	1.93 ± 0.46 (1.49 – 2.66; n = 8)	2.24 ± 0.00 (2.01 – 2.51; n = 18)
Pulse durantion (ms)	4.23 ± 0.16 (3.82 – 4.60; n = 50)	3,0 0 ± 0.23 (2.89 – 3.55; n = 50)
Air temperature	23.1 °C	22 – 27 °C

TABLE 1. Measurements of the type series and additional specimens recently collected of Elachistocleis cesarii. Abbreviations of the measurements are defined in the Material and Methods. Values presented as mean ± standard deviation (range).

	Lectotype male	Paralectotype Juvenile male	Paralectotype females Other males (n = 8) (n = 16)	Other females (n = 3)
SVL	27.8	23.2	32.24 ± 2.27 24.94 ± 1.05 (29.0 – 36.0) (22.6 – 26.7)	29.15 ± 0.50 (28.6 – 29.6)
AGL	11.6	9.1	15.51 ± 3.08 9.91 ± 0.85 (9.4 – 19.3) (8.3 – 11.3)	11.97 ± 0.89 (11.1 – 12.8)
HL	6.9	5.3	6.66 ± 0.45 5.90 ± 0.48 (6.0 – 7.4) (5.2 –6.8)	6.32 ± 0.34 (6.1 – 6.7)
HW	6.1	5.3	7.34 ± 0.58 6.89 ± 0.50 (6.5 – 8.0) (6.1 – 8.1)	7,33 ± 0.29 (7.1 – 7.7)
ED	1.2	1.0	1.34 ± 0.47 1.21 ± 0.14 (1.0 – 2.4) (1.0 – 1.4)	1.39 ± 0.23 (1.2 – 1.7)
UEW	1.0	0.9	0.98 ± 0.15 1.18 ± 0.15 (1.0 – 1.2) (1.0 – 1.5)	1.10 ± 0.15 (0.9 – 1.2)
IOD	2.9	1.8	3.32 ± 0.21 2.78 ± 0.24 (2.9 – 3.5) (2.4 – 3.2)	3.15 ± 0.09 (3.1 – 3.2)
END	2.1	1.6	2.48 ± 0.37 1.92 ± 0.20 (2.0 – 3.0) (1.5 – 2.3)	2.25 ± 0.30 (1.9 – 2.5)
SED	3.1	2.9	3.22 ± 0.24 2.92 ± 0.24 (3.2 – 3.4) (2.6 – 3.4)	3.27 ± 0.27 (3.0 – 3.5)
IND	1.4	0.8	1.28 ± 0.33 1.54 ± 0.10 (0.8 – 1.8) (1.4 – 1.7)	1.70 ± 0.12 (1.6 – 1.8)
HUL	3.4	2.6	3.22 ± 0.47 3.19 ± 0.35 (2.6 – 4.0) (2.3 – 3.7)	3.30 ± 0.40 (3.0 – 3.8)
RUL	5.2	3.7	5.37 ± 0.90 4.12 ± 0.38 (4.4 – 6.9) (3.2 – 4.8)	4.41 ± 0.16 (4.2 – 4.5)
HNL	6.0	5.3	6.96 ± 0.62 5.92 ± 0.49 (6.3 – 8.3) (5.1 – 6.9)	6.34 ± 0.27 (6.1 – 6.6)
THL	8.9	8.0	11.49 ± 1.10 9.20 ± 0.59 (10.4 – 13.5) (7.9 – 10.2)	10.89 ± 0.12 (10.8 – 11.0)
TBL	10.6	8.2	11.90 ± 0.85 9.32 ± 0.62 (11.0 – 13.5) (7.7 – 10.3)	10.39 ± 0.45 (10.1 – 10.9)
FL	11.1	10.0	12.78 ± 0.72 10.65 ± 0.55 (11.6 – 14.0) (9.6 – 11.7)	12.41 ± 0.57 (11.8 – 12.8)