Adelophryne glandulata, Lourenço-De-Moraes, Ricardo, Ferreira, Rodrigo Barbosa, Fouquet, Antoine & Bastos, Rogério Pereira, 2014

Lourenço-De-Moraes, Ricardo, Ferreira, Rodrigo Barbosa, Fouquet, Antoine & Bastos, Rogério Pereira, 2014, A new diminutive frog species of Adelophryne (Amphibia: Anura: Eleutherodactylidae) from the Atlantic Forest, southeastern Brazil, Zootaxa 3846 (3), pp. 348-360 : 348-360

Adelophryne glandulata sp. nov.

Figs. 2 A, B; 4A, B; 5

Holotype. Adult male ( MNRJ 87077; Fig. 2 ) collected on 28 August 2012 in a primary forest (Trilha Roda d’água) at REBIO Augusto Ruschi in the municipality of Santa Teresa, state of Espírito Santo, Brazil (19º 54’ 35.55’’ S, 40º 32’ 31.76’’ W, 806 m asl).

Paratypes. Six adult males ( MBML 7636–7, MNRJ 87081, MZUESC 12178, and ZUFG 7961–2), and eleven adult females ( MBML 7638–9, MNRJ 87078–80, MZUESC 12179–81, and ZUFG 7963–5). These specimens were collected from August to December 2012 and June to July 2013.

Diagnosis. The new species inhabits the leaf litter of forest floor; none exceeds 20 mm in SVL; the terminal digits are either barely or not expanded; the digits are pointed apically. These features are included in the subfamily Phyzelaphryninae (see Hedges et al. 2008). These specimens are distinguished from the genus Phyzelaphryne because they possess: subdigital pads rather than subarticular tubercles (subarticular tubercles in Phyzelaphryne ), reduction of the phalanges in the finger IV (no reduction in Phyzelaphryne ), and indistinct tympanum (distinct in Phyzelaphryne ). For more details see Hoogmoed & Lescure (1984), Hogmoed et al. (1994) and Hedges et al. (2008).

The generic assignment of Adelophryne glandulata sp. nov. is based on the possession of a head narrower than body, small size, cranial crests absent, finger IV with single subdigital pad and tip slightly mucronate, toes III and IV with discs and mucronate tips, and terminal phalanges of toes and fingers T-shaped.

The new taxon is diagnosed by the following combination of character states: (1) male SVL smaller than 11 mm (males 10.5±0.3; females 12.2±0.6); (2) tympanum indistinct without visible membrane; (3) tympanic annulus absent; (4) dentigerous processes of vomers absent; (5) fingers without terminal discs, tips of fingers slightly mucronate and terminal phalanges T-shaped; (6) toes with circumferential grooves and either terminal or vestigial discs, terminal tips mucronate; (7) terminal phalanges of toes T-shaped; (8) finger I shorter than finger II; (9) phalangeal formula to fingers 2–2–3–2; (10) phalangeal formula to toes 2–2–3–4–3; (11) subarticular tubercles absent (subdigital pads present); (12) belly skin smooth; (13) dorsum skin shagreened; (14) anal flap absent; (15) a glandular ridge line that runs from the posterior part of eye to the insertion of the forelimb.

Comparison with other species. Adelophryne glandulata sp. nov. is distinguished from several congeners by its smaller size (maximum SVL 16.3 mm in A. baturitensis , 16.0 mm in A. gutturosa , 17.4 mm in A. maranguapensis , 14.9 mm in A. mucronatus , and 23.0 mm in A. patamona , and 13.1 mm in A. glandulata sp. nov.). The new species can be distinguished from A. baturitensis and A. maranguapensis by lacking discs or circumferential grooves on fingers. It can also be distinguished from A. baturitensis by the absence of subarticular tubercles (subdigital pads present in A. glandulata sp. nov.). From all other congeners by subdigital pad formula (2–3–4– 2 in A. pachydactyla , 1–1–2–2, A. maranguapensis , 1–1–2– 1 in A. adiastola , A. gutturosa , A. meridionalis , and A. patamona , 1–2–3– 1 in A. mucronatus , and 1–2–2– 1 in A. glandulata sp. nov.). It can also be distinguished from all other congeners but A. gutturosa by the presence of a distinct glandular ridge line that runs from the posterior part of the eye to the insertion of the forelimb. It is further distinguished from A. baturitensis , A. gutturosa , A. maranguapensis , A. mucronatus , and A. patamona by having two phalanges in finger IV (three in A. baturitensis , A. gutturosa , A. maranguapensis , A. mucronatus , and A. patamona ). It is distinguished from A. adiastola , A. baturitensis , A. meridionalis , A.mucronatus , A. pachydactyla , and A. patamona by skin texture of dorsum (smooth in A. baturitensis , A. meridionalis , and A. pachydactyla , smooth with scattered small granules in A. mucronatus , shagreened to granular in A. adiastola , and tuberculated in A. patamona , shagreened with small and rounded tubercles in A.glandulata sp. nov.). It is distinguished from A. baturitensis , A. adiastola , A. gutturosa , A. maranguapensis , A. mucronatus , A. pachydactyla , and A. patamona by having a indistinct tympanum (distinct in A. baturitensis , A. adiastola , A. gutturosa , A. maranguapensis , A. mucronatus , A. pachydactyla , and A. patamona ). It is distinguished from A. meridionalis by having toes II, III, IV and V with circumferencial grooves or disc ( A. meridionalis has only toe IV with circumferencial grooves).

Description of the holotype. Adult male, SVL 10.5 mm ( Fig. 2 ). Snout rounded in ventral, lateral and dorsal views ( Fig. 2 ). ETSD slightly smaller than ED with approximately 6.2%. END smaller than IND with approximately 53.8%. Nostrils not protruding and rounded. IND smaller than IOD with approximately 72.2%. Canthus rostralis indistinct, concave in lateral view. Loreal region concave. Choanae small, round, located laterally. Dentigerous processes absent. Tongue ovoid, free except its anterior margin. Vocal sac single, subgular. Pupil horizontally oval. Upper eyelid slightly convex. Temporal region vertical, tympanum indistinct, tympanic annulus absent, and a distinct glandular ridge line that runs from the posterior part of eye to the insertion of the forelimb and two smaller-rounded glandular posterior to the eye with to 0.3 mm diameter. Skin texture of venter smooth, dorsum and limbs shagreened, rough to the touch with small and rounded tubercles, approximate equal size and very close to one another, relatively flat; flanks and ventral region of thighs areolate. Anal flap absent, cloacal opening positioned at slightly below the level of the dorsal surface of the thigh. Fingers without discs and mucronate tips; fingers thin, depressed and short, without webbing. Finger formula: I=IV<II<III ( Fig. 2 C). Phalangeal formula for fingers 2–2–3–2 ( Fig. 3 A). Fingers and palm appear to be surrounded by a narrow strip of transparent skin. Subarticular tubercles absent with subdigital pads (1–2–2–1); no pads under ultimate phalanges. Inner metacarpal tubercle ovoid, outer metacarpal tubercle round, slightly larger than inner. Toes without webbing, cylindrical but slightly flattened. Toes formula: I<V<II<III<IV; tips of toes II and V with circumferential groove and slightly mucronate, III and IV with discs and mucronate tips; tip of toe I without disc or circumferential groove, slightly mucronate ( Fig. 2 D). Phalangeal formula for toes 2–2–3–4–3 ( Fig. 3 B). Skin transparent only on the distal portion of toes. Subarticular tubercles absent with round subdigital pads present (1–1–2–3–1); no pads under ultimate phalanges and no supernumerary tubercles. Inner metatarsal tubercle oval; outer metatarsal tubercle smaller and rounded. For measurements see Table 1.

Color. Venter dark with numerous small white dots. Throat and underside of thighs and shanks black. Dorsum golden brown, dark brown or reddish brown with two dark brown lines of variable width in mid-dorsum. Loreal region dark brown; a dark brown stripe extending along the flanks and reaching the groin. Thigh and tibia with one or two dark brown bands. Numerous tiny white dots on dorsum, flanks, and dorsal surfaces of limbs. Iris reddish brown or dark brown with black reticulations ( Fig. 4 A). The color pattern does not change in preservative, although colors become darker than in life.

Variation. The individuals vary greatly in dorsal coloration (not sexually dimorphic), from golden to dark brown and reddish brown. Females are larger than males (mean SVL in females 12.2± 0.6 mm, males 10.5± 0.3mm); males vary in THL more than females (mean in females 4.9–5.7 mm, in males 4.9–5.9 mm), TL (mean in females 5.1–5.7, in males 4.5–5.6) and FL (mean in females 8.2–10.0 mm, in males 7.0– 9.2 mm); females vary more than males in HL (mean in females 3.9–4.6 mm, in males 3.5–3.9 mm) and IOD (mean females 1.6–2.6 mm, males 1.7–1.9 mm). The rounded glandular series posterior to the eye vary in size among individuals or may be absent. For morphometric variation see Table 1.

Holotype Paratypes

Measurement Male Males (n=6) Females (n=6) SVL 10.5 10.5±0.3 12.2±0.6 (10.9–10.1) (13.1–11.5)

HL 3.6 3.8±0.2 4.2±0.3

(3.9–3.5) (4.6–3.9)

HW 3.7 3.8±0.2 4.1±0.1

(4.0–3.6) (4.2–3.9)

ED 1.5 1.7±0.1 1.8±0.1

(1.9–1.6) (2.0–1.7)

UEW 1.0 1.2±0.0 1.3±0.1

(1.2–1.1) (1.4–1.1)

IOD 1.8 1.8±0.1 2.0±0.3

(1.9–1.7) (2.6–1.6)

IND 1.3 1.5±0.1 1.7±0.1

(1.6–1.3) (1.9–1.5)

END 0.7 0.9±0.0 1.0±0.1

(1.0–0.9) (1.2–0.8)

NSD 0.8 0.9±0.1 0.9±0.1

(1.0–0.7) (1.0–0.7)

THL 5.0 5.2±0.3 5.2±0.3

(5.9–4.9) (5.7–4.9)

TL 5.0 4.9±0.4 5.4±0.3

(5.6–4.5) (5.7–5.1)

FL 8.3 8.3±0.8 9.0±0.8

(9.2–7.0) (10.0–8.2)

ETSD 1.4 1.6±0.1 1.8±0.1

(1.8–1.5) (1.9–1.7) Geographic Distribution. Adelophryne glandulata sp. nov. is only known from the type locality, in forested areas of the municipality of Santa Teresa, Espírito Santo state, southeastern Brazil, from 675 m to 922 m elevation.

Natural History and Ecology. A total of 109 individuals of A. glandulata sp. nov. were captured inside the forest across 252 plots of 5 m x 5 m. If we consider detection probability = 1, the species density is 1.73/ 100 m 2. This represents the third greatest density among all frog species collected along our samplings. The most abundant species were Haddadus binotatus (Spix, 1824) and Ischnocnema sp. 1 aff. parva (C.A. Cruz, In Prep.).

Fourteen individuals were found in plots at forest edge, 47 were in plots at 50 m inside the forest, and 44 at 200 m inside the forest. Abundance was significantly higher in plots at 50 and 200 m inside primary forest compared to plots at the forest edge (Chi-Square (χ2) = 18.38, P <0.005). Only three individuals were found in a secondarygrowth forest, although 28 plots were placed in each of the three matrix-habitat types sampled across the studied landscape (coffee plantation, Eucalyptus plantation, and secondary-growth forest).

We found 13 species co-occurring with A. glandulata sp. nov. in the same 5 m x 5 m plots ( Chiasmocleis schubarti Bokermann, 1952 ; Euparkerella tridactyla Izecksohn, 1988 ; Haddadus binotatus [Spix,1824]; Ischnocnema abdita Canedo & Pimenta, 2010 ; I. guentheri [Steindachner, 1864]; I. oea [Heyer, 1984]; I. verrucosa Reinhardt & Lutken, 1862 ; Ischnocnema sp1. aff. parva; Ischnocnema sp. 2 aff. parva; Physalaemus crombiei Heyer & Wolf,1989 ; Proceratophrys boiei [Wied-Neuwied,1824]; P. paviotii Cruz, Prado & Izecksohn, 2005 ; and Zachaenus carvalhoi Izecksohn,1983 ). We did not observe any interspecific aggression.

We found A. glandulata sp. nov. throughout all sampling months (September to December 2012 and June to July 2013). Despite the presence of vocal sac, no calling males were observed neither were amplectant couples. Eggs are visible through the female skin ( Fig. 4 B). A female containing three eggs (2.0 mm diameter) was collected on 0 6 November 2012, suggesting this species reproduces during the rainy season. Adelophryne maranguapensis also reproduces in the rainy season and has clutches with three to eight eggs ( Cassiano-Lima et al. 2011). Due to the low number of eggs and their relatively large size, we suspect A. glandulata sp. nov. exhibits direct development with embryos metamorphosing directly as fully formed froglets as observed in A. maranguapensis as well as in other terraranas ( Hedges et al. 2008).

Adelophryne glandulata sp. nov. is a leaf-litter inhabitant. It forages on and under the leaf-litter and commonly uses fleeing (active escaping) as defensive strategy. Because their dorsal coloration is similar to a decomposing leaf, it may act as camouflage. In laboratory, four types of defensive behaviors were exhibited by A. glandulata : fleeing (N= 7), immobility (N= 3), mouth-gaping (N= 3; Fig. 5 ), and puffing-up the body (N= 2) (see Toledo et al. 2011 for further description of these behaviors). Mouth-gaping behavior was also observed for A. mucronatus (Lourenço-de-Moraes et al. 2012).

We dissected seven specimens of A. glandulata for stomach content analysis. One specimen had two ants. The other five specimens had one beetle per stomach and one specimen had one beetle and one ant. Ants were also found in A. gutturosa ( MacCulloch et al. 2008) and in A. mucronatus (Lourenço-de-Moraes et al. 2012).

Etymology. The latin epithet “ glandulata ”, meaning “glandular”, is used in refers to the glandular ridge line that runs from the posterior part of the eye to the insertion of the forelimb ( Fig. 2 B).

Common name. Teresensis Flea Frog or Rãzinha-Pulga Teresensis (in Portuguese).

Figures

FIGURE 2. Adult male holotype of Adelophryne glandulata sp. nov. (MNRJ 87077). Lateral (A) and dorsal (B) views of head, ventral

FIGURE 3. Views of hand (A) and foot (B) of a cleared and stained paratype Adelophryne glandulata sp. nov. (MZUESC 12181).

FIGURE 4. Adult individuals of Adelophryne glandulata sp. nov. in life: (A) male paratype (MZUESC 12180 — 10.2 mm), and (B) female paratype with eggs visible through flank skin (MNRJ 87080 — 12.8 mm).

FIGURE 5. Mouth-gaping exhibited as defensive behavior (specimen no vouched).