Rhinella bernardoi, Sanabria, Eduardo, Quiroga, Lorena, Arias, Federico & Cortez, Ricardo, 2010

Sanabria, Eduardo, Quiroga, Lorena, Arias, Federico & Cortez, Ricardo, 2010, A new species of Rhinella (Anura: Bufonidae) from Ischigualasto Provincial Park, San Juan, Argentina, Zootaxa 2396, pp. 50-60 : 51-56

Rhinella bernardoi sp. nov.

Holotype. FML 18400, adult male. Ischigualasto Provincial Park, Valle Fértil Department, San Juan Province, Argentina (30º 10' 9" S; 67º 48' 37" W; 1400 m). 24 January 2006. Collectors; Florencia Cano, Lorena Quiroga, Viviana Orozco, Rodrigo López, and Eduardo Sanabria.

Paratypes. IMCN-UNSJ 5043–5046. Four adult males with same locality data as holotype.

Etymology. Dedicated to Bernardo de la Iglesia Sanabria, a man of exceptional reputation and a great friend, to whom we are greatly thankful for his wholehearted trust and patience.

Diagnosis and comparisons. Rhinella bernardoi sp. nov. is assigned to the granulosa group in the genus Rhinella because it shares synapomorphies of the group ( Pramuk 2002) including dorsally oriented nostrils and prenasal bones located anterior to the premaxillary bone.

Rhinella bernardoi sp. nov. (male SVL = 57.3 mm, n = 5) differs from all members of the “ granulosa ” group by combination of the following characters: Rhinella granulosa average SVL of males is 53.8 mm (n = 21); very large conical keratinized tubercles covering its skin; granulose cephalic crests, an expanded maxillary crest visible both dorsally and ventrally; snout with angular edges and square-shaped in ventral and lateral views; large, divided subarticular tubercle on Finger III, covered with keratinized conical tubercles; subtriangular parotoid gland; short hind legs, with end of Toe IV reaching the nostril when the legs is adpressed anteriorly along the body. In contrast, R. bernardoi sp. nov. has a low density of dorsal granulations, continuous cephalic crests, lacking a maxillary extension, prominent snout, square-shaped from a ventral view but round from a lateral view, long hind legs, with end of toe IV surpassing the snout when adpressed anteriorly along the body. Thirteen morphometric variables show significant differences ( Table 1 ) between R. granulosa and R. bernardoi sp. nov.

The average SVL of males of Rhinella fernandezae is 51.9± 1.4 mm (n = 20). This species has a midvertebral line, continuous cephalic crests, a parietal crest, infraorbital crest surpasses postorbital and maxillary crests; and the body is completely covered by very conspicuous conical keratinized tubercles. In contrast, R. bernardoi lacks a midvertebral line, continuous cephalic crests but the parietal crest is absent, and infraorbital crests do not surpass postorbital and maxillary crests. In addition, there are fourteen statistically significant morpholometric differences ( Table 2 ).

The average SVL of males of Rhinella beebei is 51 mm and a very short parietal crest. Subnasal crests indistinct. Vertebral midline just visible. The ventral region may be light with small dark spots ( Gallardo, 1965). In contrast, R. bernardoi does not have a visible vertebral midline; continuous cephalic crests but the parietal crest is absent, and subnasal crests are present. The average SVL of males of Rhinella dorbignyi is 48.2 mm and 55.6 mm for females ( Narvaez 2003); reduced postorbital crest, infraorbital crest absent; tympanum barely visible, midvertebral line present ( Narváez 2003). The average SVL size of Rhinella bergi males is 35.8 ± 0.95 mm (n =15); parietal crest present and infraorbital crest extends posteriorly over the postorbital crest, the dorsum has a appreciable vertebral line and small black points over abdominal skin; the infraorbital crest extends caudally over the postorbital crest; the parietal crest is present and the posterior end of the supraorbital crest extends over the postorbital crest ( Narváez 2003). The average SVL of males of Rhinella pygmaea is 31.4 mm ( Narvaez 2003); parietal crest present and infraorbital crest extends posteriorly over the postorbital crest ( Narváez 2003). Rhinella bernardoi sp. nov. is larger than R. dorbignyi , R. bergi , and R. pygmaea these species has an average snout–vent length (SVL) of less than 40 mm. Also, in Rhinella bernardoi sp. nov. the infraorbital crest never surpasses the postorbital crest and the new species lacks a midvertebral line.

Holotype description. Adult male, snout–vent length (63.9 mm.). Head wider (33.8% SVL) than long (28.9% SVL) or tall (14.8% SVL), subtriangular in dorsal view. Snout truncated from dorsal view, rounded in profile. Upper jaw extends past margin of lower jaw. Eyes positioned laterally, not very prominent. Eye diameter 1.13 times eye–snout distance. Nostrils subelliptical and dorsally positioned, nearer to tip of snout than to eye. Prominent and continuous cranial crests. Supraorbital crests strongly curved, following line of eye. Canthal crest long and continuous but not extending over nostrils. Infraorbital crests straight, ending at postorbital crest forming a 90º angle. Preorbital crests straight, forming curve at juncture with infraorbital crests. Postorbital crests straight, continue with infraorbital crests. Supratympanic folds very short, joining postorbital crests and parotoid gland. No parietal crests, subnasal crests greatly reduced, similar size as nostrils. Maxillary crest located over the lip and continuing over length of maxillary, without visible lateral or dorsal expansion and appearing more like a well-defined line in the shape of a moustache. Oval-shaped tympanum, diameter 59.7% of eye diameter; green tympanic membrane between parotoid gland and postorbital crest, separated from latter by tympanic annulus. Parotoid gland oval shaped, longer (14% SVL) than wide (6.8% SVL), with poorly defined edges and covered by small, scarce, flat tubercles with a small keratinized spicule each.

Dorsum covered by scarce flattened tubercles with a keratinized spicule each; tubercles on flanks large, conical, keratinized. Interorbital area, area surrounding the nostrils, and region between parotoid gland and tympanum smooth. Dorsally light buff with long black blotches with green and yellow margins; markings joined from tympanum to vent forming an irregular line; dorsum markings scarce, lacking a regular pattern. Ventral region with small, flat, non-keratinized granules. Throat region yellow; otherwise ventrally cream with small black dots and a red patch on the lower abdomen and thighs.

Forelegs relatively long (forearm 23.1% of SVL; arm 21.4% of SVL), hands (23.7% of SVL). Fingers free with a relative length of 3>1<4>2. Hands with a round outer metacarpal tubercle larger than inner ovoid metacarpal tubercle. Subarticular tubercles fingers I and II divided. Nuptial pads on fingers I and II; Hind legs long (122.8% SVL), with webbed feet (57.5% SVL) except on toe 4 where webbing reaches middle toe and continues as a noticeable skin flap. Relative length of toes 1<2<3<4>5. Inner and outer metatarsal tubercles similar, oval, and spade-shaped. Subarticular tubercles on toes III and IV divided.

Holotype measurements. SVL= 63.9 mm. HW= 21.6 mm. HL= 18.5 mm. IND = 3.8 mm. SW= 6.8 mm. END = 4.6 mm. ESD= 7.6 mm. IOD= 1 8.3 mm, IOD2= 7.7 mm, IOD3= 9.4 mm. ED= 6.7 mm. TD1= 4.4 mm. TD2= 4.0 mm. ELW= 4.7 mm. PGL = 9 mm. PGW= 4.4 mm. AbL= 14.8 mm. AL= 13.7 mm. HndL= 15.2 mm. FL= 22.2 mm. TL= 19.5 mm. FtL= 36.8 mm. HH= 9.5 mm. 4TL= 11.8 mm. OMCTD = 4.2 mm. IMCTD = 2.5 mm. BW= 29.3 mm.

Color in life. The dorsum is light buff with long black blotches surrounded by green and yellow edges; the pattern of blotches on the flanks is similar in the specimens examined. Lateral markings are joined from the tympanum to the vent, forming an irregular line; dorsum markings are scarce and lack a regular pattern ( Fig. 1 ). Ventrally, males are cream with a reddish-red patch covering part of the abdomen, thighs, and pelvic patch. The throat is yellow. The ventral area has round black blotches small distributed randomly.

Color in ethanol. Buff background color remains, but the green blotches on the dorsum fade, becoming a pattern of dark blotches that are noticeable from the background. The throat remains yellow, but the red patch on the abdomen and thighs fades.

Variation. One paratype has black round blotches randomly located on the ventral area, other two paratypes are similar to the holotype. Variation in morphometric variables is summarized in Appendix II.

Osteology. Based on one adult male paratype (IMCN-UNSJ-5045). The skull of Rhinella bernardoi sp. nov. is wider than long with the greatest width at the level of the quadratojugals. It is heavily ossified with prominent dermal ornamentation on the dorsal surface of the nasals and frontoparietals. In dorsal view, the nasal is posterolaterally expanded and articulates with the frontoparietal covering the sphenethmoid completely ( Fig. 2 ). Prenasal bones are anterior to the premaxillary bone in the dorsal region of the skull ( Pramuk 2000). These are dermal, paired, and ovoid and lie posterior to the nares, which is unique among members of the granulosa group. In lateral view, the orbit appears closed with the margin of the orbit being formed by the articulation of the zygomatic ramus of the squamosal, the dorsal surface of maxilla, and the confluence of preorbital and suborbital crests. The quadratojugals are poorly developed and located between the maxilla and the zygomatic ramus of the squamosal. The maxilla has a dorsal expansion in the facial region, which is in contact with the ventrolateral surface of the nasal. In ventral view, the prenasals lie at the anterior margin of the skull. The maxilla and premaxilla are thin. The vomers are slender with poorly developed postchoanal processes. The sphenethmoid covers the anterior region of the base of the skull. The anterior edge of the cultriform process of the parasphenoid is acuminate and the suture between parasphenoid and pterygoid is not visible.

The vertebral column ( Fig. 3 ) of Rhinella bernardoi sp. nov. is formed by eight presacral vertebrae. The transverse process of vertebrae II, III, IV, V, VI, and VII are posterolaterally oriented in relation to the vertebral column, whereas the transverse process of vertebra VIII is oriented perpendicular to the axis of the column. The sacral diapophyses are broadly dilated and flat, and are wider than long.

Distribution. The granulosa group has a wide geographic distribution in almost all South American countries except Ecuador and Chile ( Gallardo 1965, 1969). In Argentina, the group is distributed primarily in the northeast, with species occurring in the provinces of Buenos Aires, Santa Fé, Chaco, Córdoba, Corrientes, Entre Ríos, Formosa, Jujuy, La Pampa, Misiones, Río Negro, Salta, and Santiago del Estero ( Narváez 2003). Rhinella bernardoi sp. nov. is only known from Ischigualasto Provincial Park in San Juan province ( Fig. 4 ). Here, the new species is syntopic with three other frogs: Pleurodema nebulosum , P. tucumanum , and Rhinella arenarum , whereas R. spinulosa uses permanent bodies of water to breed ( Sanabria & Quiroga 2009).

Natural history. The new species occurs in habitat known as the Monte phytogeographic region, which has an arid climate with a mean annual temperature of 20 ºC, a mean annual maximum temperature of 40 ºC, a mean annual minimum temperature of 16 ºC, and a mean annual rainfall of 84 mm concentrated in summer ( Cabrera 1994). The most common shrubs are Larrea sp. (“jarillas”) and Prosopis sp. (“algarrobos”) and riparian species such as Baccharis salicifolia (mulefat) and Grabowskia obtusa ( Márquez et al. 2005) ( Fig. 5 ). Specimens were found in temporary pools following summer rains, which were used by the new species, R. arenarum , and Pleurodema nebulosum for reproduction. There are no data regarding other aspects of the biology of R. bernardoi sp. nov., but other species in this group have an explosive, but brief (1–2 d) reproductive period following strong summer rains ( Gallardo 1972; Yanosky et al. 1997; Langone 1999).

Figures

FIGURE 1. Rhinella bernardoi sp. nov. (a) Dorsal, (b) lateral, and ventral (c) views of paratype IMCN-UNSJ 5044. Photo: Eduardo Sanabria.

FIGURE 2. Dorsal view of the skull of Rhinella bernardoi sp. nov. (IMCN-UNSJ- 5045), illustrating prenasal bone located anterior to the premaxillary bone, a synapomorphy of the granulosa group. Scale bar = 1 cm. Drawing: Federico Arias.

FIGURE 3. Vertebral column of the Rhinella bernardoi sp. nov. (IMCN-UNSJ- 5045). Note that the sacral diapophysis is broadly dilated and flat, a character of the granulosa group. Scale bar = 1 cm. Drawing: Federico Arias.

FIGURE 4. (a) Type locality of Rhinella bernardoi sp. nov. at Ischigualasto Provincial Park. (b) Distribution of the granulosa group: R. bergi (blue), R. granulosa (black), R. fernandezae (white dots), R. dorbignyi (orange), R. bernardoi sp. nov. (green). Modified from Narváez (2003).

FIGURE 5. Habitat of Rhinella bernardoi sp. nov. at the type locality, Ischigualasto Provincial Park, San Juan, Argentina. Photo: Eduardo Sanabria.

Tables

TABLE 1. Comparison of Rhinella bernardoi sp. nov (Rsp. nov.; N = 5) with the similar R. granulosa (Rg; N = 20). Morphometric variables and ratios (obtained dividing original measurements by SVL) of morphometric variables shown as mean ± standard error (only variables showing significant differences shown). Significance values refer to Mann Whitney U – tests.

Morphometric variable	Mean±SE R sp. nov.	R a t io s Mean±SE R sp. nov.	Mean±SE Rg	R a ti o s Mean±SE Rg	P<
Head length	16.5±0.8	0.29±0.002	15.8±0.2	0.26±0.002	0.0001
Internostril distance	3.1±0.2	0.05±0.001	2.7±0.2	0.06±0.001	0.001
Eye-nostril distance	4.08±0.4	0.07±0.003	3.6±0.08	0.06±0.001	0.009
Eye snout distance	6.6±0.5	0.12±0.003	5.9±0.1	0.10±0.001	0.00003
Inter orbital distance 1	7.32±0.3	0.13±0.003	6.9±0.1	0.12±0.001	0.004
Inter orbital distance 2	6.8±0.5	0.12±0.003	6.3±0.1	0.11±0.002	0.007
Maximum tympanum diameter	4.1±0.2	0.10±0.002	3.7±0.09	0.12±0.001	0.002
Parotid gland width	4.4±0.2	0.14±0.002	8.2±0.2	0.17±0.01	0.01
Arm length	13.6±0.9	0.24±0.01	10.5±0.2	0.18±0.04	0.001
Radioulna length	12.2±0.8	0.47±0.01	11.2±0.4	0.56±0.01	0.00007
Femur length	20.5±0.8	0.24±0.002	21.1±0.5	0.23±0.002	0.01
Head height	8.5±0.6	0.57±0.01	7.3±0.09	0.47±0.01	0.00003
Fourth toe length	11.7±0.3	0.15±0.004	10.3±0.2	0.12±0.013	0.0003

TABLE 2. Comparison of Rhinella bernardoi sp. nov (Rsp. nov.; N = 5) with the similar R. fernandezae (Rf; N = 20). Morphometric variables and ratios (obtained dividing original measurements by SVL) of morphometric variables shown as mean ± standard error (only variables showing significant differences shown). Significance values refer to Mann Whitney U – tests.

Morphometric variable	Mean±SE R sp. nov.	R a ti o s Mean±SE R sp. nov	Mean±SE Rf	R a t io s Mean±SE Rf	P<
Head length	16.5±0.8	0.29±0.002	13.7±0.3	0.26±0.003	0.001
Eye-nostril distance	4.08±0.4	0.07±0.003	3.04±0.06	0.06±0.001	0.003
Eye-snout distance	6.6±0.5	0.12±0.003	5±0.1	0.10±0.001	0.00007
Inter orbital distance 1	7.3±0.3	0.13±0.003	5.6±0.1	0.11±0.002	0.0001
Inter orbital distance 2	6.8±0.5	0.12±0.003	5.5±0.2	0.11±0.002	0.03
Minimum tympanum diameter	3.1±0.2	0.07±0.002	2.1±0.06	0.06±0.001	0.001
Eyelid width	4.4±0.1	0.06±0.002	3.8±0.1	0.04±0.008	0.00003
Arm length	13.6±0.9	0.24±0.01	8.2±0.2	0.16±0.003	0.03
Radioulna length	12.2±0.8	0.47±0.01	6.1±0.4	0.52±0.01	0.00003
Hand length	13.9±0.6	0.21±0.003	12.4±0.4	0.12±0.01	0.00003
Tibia length	17.4±1.1	0.36±0.01	14.8±0.5	0.3±0.01	0.0001
Head height	8.5±0.6	0.57±0.01	7.1±0.2	0.49±0.01	0.0002
Fourth toe length	11.7±0.3	0.15±0.004	9.3±0.3	0.14±0.002	0.02
Inner metacarpal tubercle diameter	2.1±0.1	0.06±0.003	1.7±0.3	0.05±0.004	0.01