Pristimantis relictus, Roberto & Loebmann & Lyra & Ávila, 2022

Roberto, Igor Joventino, Loebmann, Daniel, Lyra, Mariana L. & Ávila, Robson Waldemar, 2022, A new species of Pristimantis Jiménez de la Espada, 1870 (Anura: Strabomantidae) from the “ Brejos de Altitude ” in Northeast Brazil, Zootaxa 5100 (4), pp. 521-540 : 524-532

Pristimantis relictus sp. nov.

Hylodes ramagii Rocha, 1948

Eleutherodactylus sp Lima-Verde & Cascon (1990)

Eleutherodactylus cf. ramagii Borges-Nojosa & Lima (2001)

Ischnocnema gr. ramagii Carnaval & Bates (2007)

Pristimantis sp Loebmann & Haddad (2010)

Pristimantis sp 2 . Canedo & Haddad (2012)

Pristimantis sp Roberto & Loebmann (2016)

Pristimantis sp ( cf. ramagii )— Castro et al. (2019)

Pristimantis sp (Northern Ceará clade)— Trevisan et al. (2020)

Holotype. URCA-H 13344 (adult male) collected at Parque Nacional de Ubajara , municipality of Ubajara, state of Ceará, Brazil (03°50’18.5”S, 40°54’37.9” W; 833 m above sea level), on April 10, 2013 by Igor J. Roberto ( Figure 2 ).

Paratypes. 17 males, 33 females and 3 juveniles of undetermined sex: URCA-H 13343 (adult male) and 13342 (adult female) collected with the holotype. CFBH 20304 (adult male), CFBH 20306–08 , 20310–11 , 20313 (adult females), collected at Parque Nacional de Ubajara, municipality of Ubajara, state of Ceará , Brazil (03°50’31.57” S, 40°53’56” W, 850 m a.s.l.), on June 29, 2008 by Daniel Loebmann. CFBH 15899 –00, 15904 (adult males), collected at Mata das Bromélias , Parque Nacional de Ubajara , municipality of Ubajara, state of Ceará, Brazil (03°51’16” S, 40°55’16” W, 820 m a.s.l), on March 24, 2007 by Daniel Loebmann. URCA-H 1546 (adult male), 1543–45, 1547 (adult females) collected at municipality of Guaramiranga, state of Ceará, Brazil (04°15’21”S, 38°58’17” W, 830 m a.s.l), on February 12, 2012 by Robson W. Ávila. CFBH 20316–17 , 25415–16 , 25419 (adult females), CFBH 25417–18 , 25420–21 (adult males), collected at Parque das Trilhas, municipality of Guaramiranga, state of Ceará, Brazil (04°15’48”S, 38°55’59” W, 853 m asl), on January 23, 2009 by Daniel Loebmann. URCA-H 6988 (adult male), 6979–80, 6984, 6987 (adult females) collected on February 3–5, 2013. URCA-H 9214 (adult male) collected on April 7, 2014 at Área de Proteção Ambiental Bica do Ipu , municipality of Ipu, state of Ceará, Brazil (41°7’21.78”S, 40°42’47.69”W), by Robson W. Ávila. URCA-H 2373 (adult female) collected on March 23, 2011 by Igor J. Roberto, 9828–30 (adult females) and 9633, 9837–38 (juveniles) collected by Herivelto F. Oliveira on August 14–20, 2014 at Serra de Maranguape , municipality of Maranguape, state of Ceará, Brazil (35°3’59.23”S, 38°43’0.32”W, 800 m a.s.l). CFBH 24531 (adult female), collected at Serra de Maranguape , municipality of Maranguape, state of Ceará, Brazil (35°3’59.23”S, 38°43’0.32”W, 770 m a.s.l), on December 11, 2008 by Daniel Loebmann. CFBH 25887 (adult female), CFBH 25888 (adult male) collected at Serra da Aratanha , municipality of Pacatuba, state of Ceará, Brazil (03°58’60”S, 38°38’00” W, 700 m a.s.l), on March 29, 2010 by Daniel Loebmann. CFBH 25406–12 (adult females) collected at Fazenda Gameleira, municipality of Tianguá, state of Ceará, Brazil (03°43’16”S, 40°55’46” W 800 m a.s.l), on October 28, 2008 by Daniel Loebmann. CFBH 25413–14 (adult males) collected at Estrada do Retiro , municipality of Uruburetama, state of Ceará, Brazil (03°35’53.4”S, 39°34’50” W), on January 23, 2009 by Daniel Loebmann. URCA-H 16276–77 (adult males) collected at Serra da Meruoca , municipality of Meruoca, state of Ceará, Brazil (03°37’03.3”S, 40°21’46.7” W, 700 m a.s.l), on February 20, 2019 by Kassio C. Araújo .

Referred specimens: URCA-H 9835-9836 (juveniles) collected at Serra de Maranguape , municipality of Maranguape, state of Ceará, Brazil ; URCA-H 6981-6983 , 12287 collected at municipality of Ipu , state of Ceará ; MNRJ 55882-55883 collected at Serra da Aratanha , municipality of Pacatuba, state of Ceará, Brazil ; MNRJ 55884 collected at Serra da Ubatuba , municipality of Granja, state of Ceará, Brazil ; CHFURG 2119-23 collected at Sítio São José, municipality of Guaramiranga , state of Ceará, Brazil .

Definition. Pristimantis relictus sp. nov. is diagnosed by the following combination of characters: (1) dorsal skin shagreen with small scattered tubercles; (2) ventral skin areolate; (3) dorsolateral fold absent; (4) discoidal fold present; (5) tarsal fold present; (6) lateral fringes absent on fingers, narrow on toes; (7) vocal slits present in males; (8) advertisement call composed of 1–8 pulsed notes (2–5 pulses per note), note rate of 0.5–2.2 notes per second, call duration 20–660 ms, fundamental frequency located at the first energy band between 1895–2153 Hz and dominant frequency located at the second energy band between 3617–4220 Hz; (9) in life dorsum coloration dark brown to yellowish-brown, with presence of dark brown chevrons and black spots in some individuals, transversal brown bars on legs and arms; (10) immaculate cream-colored pattern of concealed surfaces of thighs; (11) presence of a dark brown stripe from tip of snout to eye, including inter-nostril area, and a dark brown interorbital bar; (12) supratympanic fold bold, black; (13) gular region yellowish; (14) iris color cooper with brown reticulations.

Morphological comparisons with other species within the Pristimantis conspicillatus species group. The shagreen texture of the dorsal skin differentiates Pristimantis relictus sp. nov. from P. avicuporum ( Duellman & Pramuk, 1999) , P. metabates ( Duellman & Pramuk, 1999) , P. johannesdei ( Rivero & Serna, 1988) , P. phalaroinguinis ( Duellman & Lehr, 2007) , and P. pictus (all have smooth dorsal skin). Nineteen species have smooth ventral skin, differing from the areolate ventral skin of P. relictus sp. nov.: P. achatinus ( Boulenger, 1898) , P. buccinator ( Rodriguez, 1994) , P. charlottevillensis ( Kaiser, Dwyer, Feichtinger & Schmid, 1995) , P. chiastonotus ( Lynch & Hoogmoed 1977) , P. citriogaster ( Duellman, 1992) , P. condor ( Lynch & Duellman, 1980) , P. conspicillatus ( Günther, 1858) , P. fenestratus ( Steindachner 1864) , P. gaigei , P. gutturalis , P. johannesdei P. latro , P. lymani ( Barbour & Noble, 1920) , P. malkini (Lynch, 1980) , P. metabates , P. peruvianus ( Melin, 1941) , P. phalaroinguinis , P. samaipatae ( Köhler & Jungfer 1995) , and P. vilarsi ( Melin, 1941) . The areolate ventral skin also distinguishes P. relictus sp. nov. from P. dundeei ( Heyer & Muñoz, 1999) , P. giorgii , P. iiap Padial, Gagliardi-Urrutia, Chaparro & Gutiérrez, 2016 , P. incertus , and P. ventrigranulosus Maciel, Vaz-Silva, Oliveira & Padial, 2012 (ventral skin granular or slightly granular). The absence of dorsolateral folds distinguishes P. relictus sp. nov from Pristimantis adiastolus ( Duellman & Hedges, 2007) , P. ardilae , P. avicuporum , P. bipunctatus ( Duellman & Hedges, 2005) , P. buccinator , P. chiastonotus , P. conspicillatus , P. iiap , P. latro , P. malkini , P. meridionalis ( Lehr & Duellman, 2007) , P. peruvianus , P. pluvian , P. skydmainos , and P. zeuctotylus (presence of dorsolateral folds) The subovoid snout in dorsal view of P. relictus sp. nov. distinguishes it from P. carranguerorum ( Lynch, 1994) (obtuse) and P. medemi ( Lynch, 1994) , P. latro , and P. zeuctotylus (subacuminate). The immaculate cream-colored pattern of concealed surfaces of thighs differentiates P. relictus sp. nov. from P. pluvian (red), P. bipunctatus , P. condor , P. conspicillatus , P. malkini , P. peruvianus , and P. pictus (with well-defined spots).

In addition to the new species, five other species of Pristimantis are distributed in Northeast Brazil: P. moa , P. paulodutrai , P. ramagii , P. rupicola and P. vinhai (see Table 1 ). While Pristimantis relictus sp. nov. is distributed in highland marshes of Ceará, P. moa is known from transition areas between the Cerrado and Amazon Forest ( Oliveira et al. 2020), P. rupicola occurs in Campos Rupestres of Chapada Diamantina ( Taucce et al. 2020), and the remaining three species inhabit the Atlantic Forest domain ( Trevisan et al. 2020). Besides geographic distribution, P. relictus sp. nov. can be distinguished from P. moa by areolate ventral skin (smooth in P. moa ), snout subovoid in dorsal view (truncate in P. moa ), immaculate cream-colored pattern of concealed surfaces of thighs (strongly stained yellow on a dark background in P. moa ), finger fringes absent (present in P. moa ), and webbing on toes absent (present in P. moa ) ( Oliveira et al. 2020). The new species differs from P. rupicola by possessing shagreen dorsal skin (granular in P. rupicola ), and snout subovoid in dorsal view (rounded or truncate in P. rupicola ) ( Taucce et al. 2020). The new species can be distinguished from the Atlantic Forest species as follows: from P. paulodutrai by the presence of nuptial pads (absent in P. paulodutrai ), ventral skin areolate (granular in P. paulodutrai ), and immaculate creamcolored pattern of concealed surfaces of thighs (with red blotches in P. paulodutrai ) ( Bokermann, 1975); from P. ramagii by snout subovoid in dorsal view (subacuminate in P. ramagii ), presence of nuptial pads and toe fringes (absent in P. ramagii ) ( Boulenger, 1888); and from P. vinhai by ventral skin areolate (slightly granular in P. vinhai ), snout subovoid in dorsal view (acuminate in P. vinhai ) ( Bokermann, 1975).

Bioacustical comparisons with other species within the Pristimantis conspicillatus species group. The shorter note duration (20–50 ms) differentiates P. relictus sp. nov. from P. samaipatae (59–141 ms) and P. fenestratus (50–91 ms) ( Padial & De La Riva 2009). The lower note rate (0.5–2.2 notes/s) distinguishes P. relictus from P. fenestratus (7.7–12.7), P. koehleri (11.8–17.3), P. samaipatae (2.7–14.9), P. dundeei (13.7–20.7) ( Heyer & Muñoz 1999; Giaretta et al. 2018), and P. vilarsi (14) ( Heyer & Barrio-Amorós 2009). The lower number of pulses per note of P. relictus sp. nov. (2–5) also differentiates the new species from P. fenestratus (9–17), P. samaipatae (11–23), P. latro (6–9), and P. pluvian (8–16). The higher fundamental frequency of P. relictus sp. nov. (1894.9–2153.3 Hz) distinguishes the new species from P. samaipatae (1535–1834 Hz), P. latro (1342–1448.6 Hz), P. moa (1320.8–1660.2 Hz), and P. giorgii (663.2–1872.3 Hz). The higher peak frequency of P. relictus sp. nov. (3617.6–4220.5 Hz) differentiates the new species from P. fenestratus (1710–3591 Hz), P. latro (2635.9–3272 Hz), P. moa (2657.1–3400 Hz), and P. pictus (2487.4–3272.2 Hz) ( Padial & De La Riva 2009; Oliveira et al. 2017, 2020). Also, advertisement call differentiates P. relictus from P. rupicola . The new species has a higher peak of frequency (3617.6–4220.5 Hz), located in the second band of energy, [peak frequency (2410–3490 Hz) in the first band of energy of the call; Taucce et al. (2020)]. The advertisement call of P. relictus is very similar to that of P. ramagii but the species can be distinguished by the number of pulses per note of 2–5 (7–53 in P. ramagii ; Octaven et al. 2017).

Description of the holotype. Adult male (URCA-H 13344; Figure 2 ). Head longer than wide; head width 37% of SVL; head length 40% of SVL; snout subovoid in dorsal view, rounded in lateral view; nostrils not protuberant, directed anterolaterally; internarial distance less than eye-nostril distance; canthus rostralis angular, weakly concave, loreal region slightly concave; eye large, with horizontally elliptical pupil; eye diameter slightly larger than interorbital distance; cranial crests absent; upper eyelid smooth, 74% of eye diameter; tympanum large, with distinct rounded tympanic annulus; tympanic membrane present, visible; supratympanic fold present; labial bars absent; vocal sac subgular, small; tongue ovoid covering the entire floor of mouth, free and notched behind; vocal slits present, lateral to tongue; choana small, rounded; odontophores oblique and widely separated posterior to the choanae, each one bearing six teeth; skin on dorsum shagreen with scattered low tubercles; dorsolateral fold absent; skin on venter areolate, weakly spotted, discoidal fold present; hands large, 29% of SVL; relative lengths of fingers II <IV <I <III; finger fringes absent; finger discs expanded, truncate; disc of Finger III wider than the others, discs of fingers II and IV wider than disc of Finger I; nuptial pad present, single; outer metacarpal tubercle divided inner metacarpal tubercle large, in contact with nuptial pad; subarticular tubercles large, rounded; one subarticular tubercle on fingers I and II, and two on fingers II and IV; supernumerary tubercles present; three horizontal bars present on thigh and tibia; tibia length greater than thigh length, tibia length 51% of SVL; tarsal fold present; inner metatarsal tubercle present, larger than outer metatarsal tubercle, both rounded; toes bearing narrow lateral fringes; webbing absent; relative lengths of toes I <II <III <V <IV; toe discs expanded, smaller on Toe I; subarticular tubercles rounded, one on toes I and II; two on toes III and V, and three on Toe IV; supernumerary tubercles present, barely distinct.

Measurements of the holotype (mm). SVL 24.4, HL 9.7, HW 8.9, ED 3.4, SL 4.4, IND 2.0, END 2.8, IOD 3.3, UEW 2.5, TD 2.0, FAL 5.4, HAL 7.0, FIII 1.4, FIV 1.3, THL 12.4, TL 13.1, TAL 7.1, FL 10.7, and TIV 1.4.

Color in preservative. Dorsal and lateral surfaces pale cream, snout light brown, brown interocular band in dorsal view, distinct dark brown stripe from tip of snout to posterior region of supratympanic fold. Irregular brown marks in lower orbital region. Two brown chevrons on dorsum with irregular brown dots in inguinal region, light brown stripes on dorsal surfaces of limbs. Ventral surface background pale cream in color.

Advertisement call. The call of Pristimantis relictus sp. nov. is described based on three individuals (MNRJ 55582 and two unvouchered individuals) (see Table 2 ;). The vocalization is composed of 1–8 multi pulsed notes (2–5 pulses per note), with an ascendant amplitude modulation. The call duration ranges 0.02– 0.66 s (0.06 ± 0.08; n = 181), with intercall interval of 0.8– 9.6 s (2.12 ± 1.5; n = 74), note duration ranges 0.02– 0.05 s (0.03 ± 0.01; n = 150), with a note rate of 0.52–2.20 notes per second ( Figure 3 . The call has three visible bands. The fundamental frequency is in the first band, ranging 1894.9–2153.3 Hz, followed by a second band located in the dominant frequency, ranging 3617.6–4220.5 Hz, and a third weak band with a higher frequency, ranging 4565–6287.7 Hz.

Variation among paratypes. Adult females (SVL 26.8–32.8 mm) are slightly larger than adult males (SVL 23.1–29.7 mm) ( Table 3 ). Variation in coloration of fixed specimens is mostly related to the presence of chevrons on the dorsum (URCA-H 6980, 2373, 1544, 13342, 6988, and 9828). In life, the dorsal coloration is highly polymorphic: dark brown, reddish to yellowish-brown, or grey ( Figure 4 ), with the presence of dark brown chevrons and black spots in some individuals. Other variations in coloration among paratypes are: brown bars on the leg and arm; dark brown stripe from the tip of the nose to the eye, including the internarial area; dark brown bar in the interorbital region; labial region yellowish to white; supratympanic fold bold black; gular region yellowish; and iris cooper-colored with brown reticulations.

Geographic distribution. Pristimantis relictus is endemic to the “Brejos de Altitude” of the state of Ceará, Northeast Brazil. This species occurs in the Planalto da Ibiapaba (municipalities of Ipu, Tianguá, Ubajara, Granja, Viçosa do Ceará), Serra de Maranguape (municipality of Maranguape), Serra da Aratanha (municipality of Pacatuba), Serra de Baturité (municipalities of Guaramiranga, Pacoti, Aratuba, Mulungu), Serra da Uruburetama ( Roberto & Loebmann 2016), and Serra da Meruoca (municipality of Meruoca) ( Figure 5 ).

Natural history. Pristimantis relictus occurs in dry forests and humid forests ( Loebmann & Haddad 2010; Roberto & Loebmann 2016; Castro et al. 2019), from 100 to 900 m.a.s.l. The species has a prolonged breeding period throughout the raining season from December to April. Vocalization occurs from 5 pm throughout the night, with a peak of individuals vocalizing during 6–9 pm. Individuals were found vocalizing on leaves, tree trunks and twigs, mostly facing downwards. Amplexus is axillary, and the eggs are deposited on humid surfaces of rock and wooden debris. Mature females range 28–33 mm and 1.45–3.27 g (n = 13), and clutches have 21– 53 eggs (n = 13). We observed territorial behavior involving agonistic combat and the emission of territorial and release calls; unfortunately, these calls were not recorded. At Serra de Baturité mountain range we recorded the following species occurring in sympatry with P. relictus : Boana raniceps , Dendropsophus minusculus , D. minutus , D. tapacuarensis , Pithecopus gonzagai , Scinax tropicalia , Trachycephalus typhonius , Adelophryne baturitensis , Odontophrynus carvalhoi , Rhinella casconi , R. dapsilis , R. diptycha , R. granulosa , Adenomera juikitam , Leptodactylus macrosternum , L. natalensis , L. pustulatus , L. mystaceus and Physalaemus cuvieri . See Loebmann & Haddad (2010), and Castro et al. (2019) for the anuran species that occur in sympatry with Pristimantis relictus at the Planalto da Ibiapaba mountain range.

Etymology. The specific epithet is derived from the Latin noun word relictus , meaning left behind, abandoned, in reference to the isolated geographic distribution of the species between the Amazon and Atlantic Forest, where it only occurs in mountain forests of highland marshes of the state of Ceará, Brazil.

Figures

FIGURE 2. Holotype of Pristimantis relictus sp. nov. (URCA-H 13344): Above—dorsal and ventral views; Below—head in lateral view; right hand and right foot in ventral view. Scale bars = 10mm.

FIGURE 3. Advertisement call of Pristimantis relictus sp. nov: A—individual, MNRJ 55582, recorded on the Serra da Aratanha mountain range, municipality of Pacatuba, state of Ceará, Brazil, on December 26, 2006 by Igor J. Roberto, showing one call composed of two notes, each with two distinct pulses. B–unvouchered individual from the Serra de Baturité mountain range, municipality of Pacoti, state of Ceará, recorded on February 11, 2007, by Igor J. Roberto, showing a call composed of eight pulsed notes. Spectrogram (above) and oscillogram (below).

FIGURE 4. Adult specimens of Pristimantis relictus sp. nov. in life: A—Adult male, B–D adult female, municipality of Ubajara; E–F adult female municipality of Guaramiranga, G—amplectant pair, municipality of Pacatuba; H–I—adult calling males, municipality of Guaramiranga, state of Ceará, Brazil.

FIGURE 5. Geographic distribution map of Pristimantis relictus: yellow triangle, type locality in the Ubajara National Park, Serra da Ibiapaba mountain range; green circles, localities of paratypes: 1-municipality of Tianguá, 2-Serra da Ubatuba mountain range, municipality of Granja, 3-Serra da Meruoca mountain range, 4-municipality of Ipu, 5-Serra da Uruburetama mountain range, 6-Serra de Baturité mountain range, 7-Serra de Maranguape mountain range, 8-Serra da Aratanha mountain range.