Two new frog species from the Foja Mountains in north western New Guinea ( Amphibia , Anura , Micro hylidae )

Two new microhylid frogs in the genera Choerophryne and Oreophryne are described from the Foja Mountains in Papua Province of Indonesia. Both are small species (males 15.9 – 18.5 mm snout-urostyle length [SUL] and 21.3 – 22.9 mm SUL respectively) that call from elevated positions on foliage in primary lower montane rainforest. The new Choerophryne species can be distinguished from all congeners by, among other characters, a unique advertisement call consisting of an unpulsed (or very finely pulsed) peeping note lasting 0.29 – 0.37 seconds. The new Oreophryne species belongs to a group that has a cartilaginous connection between the procoracoid and scapula and rattling advertisement calls. Its advertisement call is a loud rattle lasting 1.2 – 1.5 s with a note repetition rate of 11.3 – 11.7 notes per second.


Introduction
The Foja Mountains are an isolated mountain range located in northern Papua Province, Indonesian New Guinea.The biodiversity of the the Fojas remained poorly documented (Diamond 1982) until November 2005 when a Rapid Assessment Program biological survey by Conservation International and the Indonesian Institute of Sciences (LIPI) revealed numerous undescribed taxa there, including a new species of bird (Beehler et al. 2007).Amongst the new taxa discovered during that survey and the preliminary reconnaissance conducted during planning activities for it, were a number of frog species, three of which (Litoria gasconi, Callulops fojaensis and Pseu docallulops foja) have since been described (RichaRds et al. 2009;OliveR et al. 2012;GüntheR et al. 2016).Here we describe and illustrate two additional new species of frogs collected during the 2005 Foja Mountains expedition, each of which is currently known only from this isolated mountain range.

Material and methods
Most frogs were collected at night after they were located by their advertisement calls.Representative specimens were photographed in life, and specimens were euthanised in an aqueous chlorobutanol solution and subsequently fixed in 5 % formalin.Liver samples were taken from some specimens before fixation, and stored in 95 % ethanol to enable later DNA sequencing.All specimens were transferred to 70 % ethanol within two days of fixation.The following measurements were taken with a digital calliper ( > 10 mm) or with a binocular dissecting microscope fitted with an ocular micrometer (< 10 mm) to the nearest 0.1 mm from preserved specimens only: SUL snout-urostyle length from tip of snout to pos terior tip of urostyle bone; SUL is generally slightly shorter than snout-vent length (SVL).As the measurement error is higher in the latter, we prefer to use the former.Both measurements are sufficiently similar (unpublished data) that, where relevant, we compare our SUL measurements with SVLs presented for members of the genus in some papers; TL tibia length: external distance between knee and tibio-tarsal articulation; TaL length of tarsus: external distance between tibiotarsal and tarsal-metatarsal joints held at right angles; T4L length of 4th toe: from tip of toe to proximal end of inner metatarsal tubercle; T4D transversal diameter of disc of 4th toe; T1D transversal diameter of disc of first toe; F3L length of 3rd finger; F3D transversal diameter of disc of 3rd finger; F1D transversal diameter of disc of first finger; HL head length: from tip of snout to posterior margin of tympanum; HW head width: taken in the region of the tympana; SL snout length, from an imaginary line connecting the centres of the eyes to tip of the snout; EST distance from anterior corner of orbital opening to tip of snout; END distance from anterior corner of orbital opening to centre of naris; IND internarial distance between centres of nares; ED eye diameter: from anterior to posterior corner of orbital opening; TyD horizontal diameter of tympanum.
Advertisement calls were recorded under natural conditions with a Sony TCM 5000EV tape recorder and a Sennheiser ME66 Microphone with K6 power module, and analysed with Avisoft-SAS Lab Pro software.Air temperatures adjacent to calling males were recorded using a rapid-reading digital thermometer.We measured temporal and spectral parameters of calls using the definitions of cOcROft & Ryan (1995) and these are presented as "mean ± SD (range)".Kampen, 1914 examined for this study, including species previously included in Albericus BuRtOn & Zweifel, 1995, is listed in GüntheR & RichaRds (2011) and in ianella et al. (2014, 2015).Additional comparisons with other "short-nosed" Choerophryne relied on the papers by KRaus & allisOn (2005a, 2005b, 2009) and KRaus (2010).Comparative material from the genus Oreophryne BOettGeR, 1895 is listed in GüntheR et al. (2012) andGüntheR (2015).Moreover, we referred to most of the original species descriptions and recompiled treatises to make our comparisons.an indistinct off-white stripe from posterior edge of eye along flanks to inguinal region; mid-dorsum varies from off-white or light brown to dark brown; discs of fingers and toes predominantly light yellowish and only inconspicuously speckled with darker pigment.Most diagnostic is the advertisement call, an unpulsed (or very finely pulsed) peeping note, as a rule longer than 300 ms, which is unique among Choerophryne species.

Abbreviations of collections:
Description of the holotype (Fig. 1a -1d).Adult male with an SUL of 18.1 mm.Additional measurements and ratios listed in Table 1.Head broader than long (HL/HW 0.83); tip of snout acuminate in dorsal view and truncate in lateral view, bearing a small lobe on the tip; nostrils near tip of snout, directed laterally and not visible from above or below, distance between nares less than distance between eye and naris (END/IND 1.38); canthus rostralis rounded; loreal region slightly sloped; tongue very long, broadening strongly posteriorly, posterior margin with only a slight indentation; anterior prepharyngeal ridge well developed and smooth, posterior "ridge" a plaque with many longitudinal furrows; moderately long vocal slits on both sides of mouth floor near corner of mouth; tympanum medium-sized (about one-half of eye diam- eter), no supratympanic fold in preservative.Fingers unwebbed with broad, grooved terminal discs, their relative lengths 3 > 4 > 2 > 1 (Fig. 1c); disc of third finger more than twice width of penultimate phalanx, no prominent metacarpal or subarticular tubercles.Shanks rather short (TL/SUL 0.41).All toes with wide, grooved terminal discs, those of fourth toe narrower than those of third finger; no webs between toes, no metatarsal tubercles, no prominent subarticular tubercles; relative lengths of toes 4 > 5 > 3 > 2 > 1 (Fig. 1d).All dorsal and ventral surfaces in life densely covered with conspicuous smaller and larger tubercles, in preservative many tubercles disappeared, others became poorly visible; only one tubercle in the shoulder region and another one posterior to the eye are more expressed in preservative than in life.
Colour in life.Ground colour of dorsal and lateral surfaces light yellowish-brown, with dark brown flecks on sides of head, on forelegs and hind legs, as an indistinct ")(" in the neck region and as a crossband mid-dorsally; tips of fingers and toes predominantly yellowish, dorsal and ventral part of iris silvery, its anterior and posterior part red-orange (Fig. 1a).Ground colour of abdomen reddish covered by a mixture of irregular light grey and dark grey-brown spots; throat, chest and ventral surfaces of legs covered by a mixture of different tones of grey.Ventral surfaces of finger tips and toe tips yellowish.A prominent white capped tubercle on anterior and posterior lower jaw (Fig. 1b).

Colour in preservative.
Ground colour of dorsal and lateral surfaces light grey-brownish with irregularly shaped dark brown and blackish flecks and spots mainly on head and dorsum.Conspicuous are an indistinct ")("-shaped fleck in the shoulder-nape region, a crossband on middorsum and in the middle of shanks and forearms.Also conspicuous are whitish heels and whitish finger and toe tips.Abdomen light grey with irregular brown spots partly connected with each other, these brown spots becoming very dense anteriorly covering ground colour on throat and most of ground colour of ventral surfaces of legs.Conspicuous are unpigmented ventral surfaces of fingers and toes and sparsely pigmented palm and sole.

Morphological variation of the types in preservative.
Measurements and body ratios of the type specimens are presented in Table 1.SUL of seven adult males ranges from 15.9 to 18.5 mm (mean 17.2 ± 0.92 mm); one adult female has an SUL of 18.4 mm.Their dorsal surfaces are shown in Fig. 2. Most specimens have an acute snout tip while in several the snout tip is narrowly rounded, and most have a broad dark brown longitudinal mid-dorsal stripe from eyes to posterior back; its lateral margins are as a rule darker than its centre and it forms an X-like figure between shoulders and eyes.This dark stripe is dorsolaterally confined by an irregular yellowish longitudinal stripe.One specimen (MZB Amph.12003) has dark flanks and another (MZB Amph.11975) has a completely whitish dorsum, except a brown "X" between shoulders and eyes (Fig. 3).A whitish postocular fleck that includes the tympanum is present in all specimens.Four specimens exhibit a fairly distinct whitish lumbar spot, in three specimens this spot is rather indistinct, in one it is not present and in another specimen (MZB Amph.11971) it is interspersed with tiny white spots.Discs of fingers and toes in all specimens are conspicuously pale.As in many other short nosed members of the genus Choero phryne, the region around the tibio-tarsal articulation or at least on distal shanks is striking yellowish-white.Ventral surfaces from completely dark reddish-brown (MZB Amph.12003), through more or less mottled, to uniform yellowish with only a few brownish spots on chin and ventral legs.
Distribution and ecological notes.This species was found perched on leaves in extremely wet, mossy lowermontane forest where males called at heights between ~1.0 and 2.5 m above the ground on both wet and dry nights.An adult female (MZB Amph.11971) contained just four apparently mature eggs of about 2 mm diameter, two in each ovary.This species is known only from  Vocalisation.The advertisement call of the new species, recorded at an air temperature of 17°C, consists of a long "peeping" note that is uttered singly or in shorter or longer series and time between single calls or between call series varies considerably (Fig. 4).We recorded calls from three males, two of them bearing field numbers SJR 9835 and 9860 and deposited in the Museum Zoologicum Bogoriense but not available for inclusion in the type series.One male produced three calls at long intervals, the second produced 22 calls at variable intervals, and the third produced 19 calls also at variable intervals.We arbitrarily consider calls to be part of the same 'series' if intercall intervals are < 7 s.Length of calls (in ms) from the first male (n = 3) was 296 ± 10.1 (285 -305), and the two intervals between calls were 37 and 20 s.
Length of calls produced by the second male (n = 22) was 357 ± 11.5 (333 -374) and of 16 intercall intervals shorter than 7 s was 4.4 ± 1.5 (2.9 -6.9) s, while intervals between call series (separated by intervals > 7 s) were 9 s, 12 s, 13 s, 20 s and 38 s.Mean length of calls produced by the third male (n = 19) was 303 ± 7.4 (290 -317) ms; length of 13 intercall intervals shorter than 7 s was 4.3 ± 0.6 (3.0 -5.2) s; intervals greater than 7 s were 15 s, 36 s, 37 s, 38 s and 68 s.Oscillograms of the calls have a spindle-like appearance (Fig. 5, top).In optimal recordings about 600 pulses/s are discernible.Because pulses in many recordings are so fine that they are not discernible, calls could also be considered unpulsed.A finely pulsed (or unpulsed) structure predominates during the greatest part of the call; only at its beginning and its end are some pulses longer and therefore better discernable.Calls are finely tuned with many harmonic bands but are not frequency modulated (Fig. 5, lower).Lowermost visible harmonic band is at 2.6 kHz, dominant frequency centres  1999) is smaller (13.6 -15.4 mm), has longer shanks (TL/SVL 0.43 -0.48 vs. 0.38 -0.43), narrower finger discs (F3D/SVL 0.055 -0.061 vs. 0.061 -0.076 in Ch. pipiens sp.nov.) and advertisement call notes less than 100 ms long at 15 -16.5°C.Choerophryne tubercula is smaller than the new species (15.0 -15.1 mm vs. 15.9 -18.5 mm), shows more and stronger tubercles on dorsal and lateral surfaces and its call resembles a harsh "ank" with about 160 pulses/s (RichaRds et al. 1992).The call of Ch. variegata is unknown but it has longer hind legs than Ch.pipiens sp.nov.(TL/SVL 0.47 vs. 0.38 -0.43), shorter head (HL/SVL 0.27 vs. 0.31 -0.34) and larger eyes (ED/SVL 0.133 vs. 0.112 -0.127).
The new species is morphologically and bioacoustically most similar to Ch. brunhildae (menZies, 1999) and Ch.murrita (KRaus & allisOn, 2009).Our analyses of 22 calls from the holotype and two paratypes of Ch.brunhildae recorded at 18.8 -23°C revealed a call length of 541 ± 49.6 (404 -615) ms and a pulse repetition rate of 224 ± 32.6 (175 -274) pulses/s; these values differ significantly from those of the new species.Ch. brunhildae utters squeaking calls, not peeping ones like Ch. pipiens sp.nov.The calls of Ch. bruhildae are clearly pulsed and harmonics appear in spectrograms as short vertical stripes and not as long horizontal stripes as in Ch. pipiens.The course of a note is also characterized by a strong rise and a strong descent of the amplitude in Ch. brunhildae vs. a slow rise and slow descent in Ch. pipiens sp.nov.Choerophryne brunhildae has a smaller tympanum than Ch.pipiens sp.nov.(TyD/ SVL 0.051 -0.057 vs. 0.059 -0.071), all other body ratios are more or less overlapping.
There is broad overlap with Ch. murrita in most morphological traits, but snout shape and some bioacoustic traits clearly differ.When seen from above, the snout of Ch. murrita is bluntly rounded, while the snout of most Ch.pipiens sp.nov. is distinctly acute (Fig. 2

Diagnosis.
A species of the genus Oreophryne based on the presence of eleutherognathine maxillae, procoracoids and clavicles that do not extend to the scapulae.Snouturostyle length in males (n = 7) of 21.3 -22.9 mm and in females (n = 2) 24.9 -26.1 mm.Cartilaginous connection between procoracoid and scapula; no webs between fingers, basal webs between toes 3 and 4 as well as between 4 and 5; fifth toe longer than third; finger discs clearly wider than toe discs (ratio T4D/F3D 0.64 -0.91); further body ratios are TL/SUL 0.40 -0.46, HL/HW 0.82 -0.90, ED/SUL 0.129 -0.147, TyD/ED 0.32 -0.44, and END/ IND 0.78 -0.95.In preservative, a conspicuous whitish postocular fleck including most of the tympanum; most specimens with a whitish mid-dorsal line.Dorsal surfaces in preservative yellowish with irregular lighter and darker brown mottling, ventral surfaces also yellowish with dense or scarce brown dotting.Advertisement call a loud rattle of 1.2 -1.5 s with a note repetition rate of 11.3 -11.7 notes per second (s).Note length 32 -45 milliseconds (ms) and internote length 37 -69 ms.Dominant frequency at 4.2 kHz.
Description of the holotype (Fig. 7).Adult male with an SUL of 21.8 mm.Additional measurements and ratios are listed in Table 2. Head broader than long (HL/ HW 0.88), tip of snout rounded in dorsal view, truncate and hardly protruding in lateral view; nostrils directed laterally and visible from above, distance between nares larger than distance between eye and naris (END/IND 0.86); canthus rostralis clearly defined and slightly con-cave in dorsal view; loreal region slightly skewed and slightly concave; pupil horizontally oval; tongue long, wide and with posterior indentation, only its most anterior region adhered to mouth floor; middle part of anterior prepharyngeal ridge smooth and well expressed, its lateral parts scarcely visible; posterior prepharyngeal ridge clearly denticulate; long vocal slits on both sides of mouth floor near corner of the mouth; tympanum small (TyD/ED 0.34), its annulus partly covered by skin; short and nearly horizontally directed supratympanic fold.Forelegs and hind legs moderately long; fingers unwebbed and with broad and grooved terminal discs (disc of third finger 2.5 times width of penultimate phalanx), their relative lengths 3 > 2~4 > 1 (Fig. 7c); no prominent metacarpal or subarticular tubercles.All toes with wide and grooved terminal discs, discs of toes less than twice as wide as penultimate phalanges; basal webs between toes 3, 4 and 5, no webs between toes 1, 2 and 3; subarticular tubercles on toes scarcely developed, inner metatarsal tubercle elongate and better developed; relative lengths of toes 4 > 5 > 3 > 2 > 1 (Fig. 7d).Few distinct tubercles sparsely scattered on all dorsal surfaces of body and extremities; a conspicuous glandular fold starting as a prominent supratympanal tubercle and extending, after an emargination on the anterior dorsum, to a whitish lumbar spot; all lower surfaces smooth.

Colour in life.
Ground colour of dorsal and lateral surfaces lighter or darker yellowish with reddish dots and streaks and irregular brown spots (compare Fig. 7a).Iris silvery with dark grey-brown venation and orange inner margin; mid-dorsal line off-white and reaching from snout tip to end of urostyl; ventral surfaces off-white with light-yellowish flecks and numerous brownish dots (Fig. 7b), ventral sides of hands and feet also with dense brown punctuations and light flecks (Fig. 7c and 7d).

Colour in preservative.
Ground colour of flanks offwhite, of dorsum yellowish and of dorsal limbs light brown; the dorsolateral glandular ridges are bordered inferiorly by irregularly shaped brown spots and superiorly by a nearly unspotted yellowish area; due to the emarginated course of these ridges, this yellowish area shows the form of an hourglass; this hourglass mark is confined anteriorly by a triangular brown spot; an interocular light yellowish bar is confined posteriorly by a more solid brown stripe and anteriorly by a more diffuse brown stripe; both stripes as well as the triangle spot in the nape region are medially interrupted by the yellowish mid-dorsal line; dorsal hind legs are almost unspotted, dorsum of forearm exhibits a conspicuous brown spot distally.Conspicuous are also a crescent-shaped dark brown supratympanal spot, whitish ear region, spotted head sides and whitish lumbar spots.Ventral surfaces uniformly straw yellow to the naked eye but with numerous dark brown dots when enlarged.

Morphological variation of the types in preservative.
For body measurements and ratios of all types see Ta-ble 2. Snout-urostyle length in males (n = 7) from 21.3 -22.9 mm and in females (n = 2) from 24.9 -26.1 mm.Ground colour of dorsal surfaces may be off-white, yellowish or light brownish, only one specimen (MZB Amph.12013) is completely dark brown on dorsum.Characteristic for almost all specimens is a short straight or gently curved postocular glandular ridge that is inferiorly demarcated by a dark brown fleck, )(-shaped dorsolateral glandular ridges (that are more or less interrupted in most specimens and extend maximally from eye to the lumbar region); a prominent tubercle between tympanum and insertion of forelimb; a whitish interocular bar that may include parts of the upper eye lid; more or less demarcated whitish lumbar spots; a narrow or wide light mid-dorsal line from snout tip to end of body; a whitish area from eye through tympanum to the above mentioned tubercle; a dark brown fleck or band on distal forearm; ventral surfaces evenly stippled with brown dots or covered by brown flecks or a brownish network.
In life MZB Amph.11990 (Fig. 8) shows a paler dorsal colouration than the holotype without a reddish component, has a wider mid-dorsal line extending to hind legs, and a less expressed ")(" mark on anterior dorsum (more distinct in preservative).
Distribution and ecological notes.Oreophryne albitym panum sp.nov.was found in moss-covered trees in extremely wet, lower-montane forest where males called at heights of between ~2.0 and 4.0 m above the ground on both wet and dry nights.This species is known only from the type locality near the summit of the Foja Mountains in Papua Province, Indonesian New Guinea (Figs. 9 and 10).
Etymology.The specific epithet albitympanum is a compound of the Latin adjective albus, -a,-um meaning white and the Latin substantive tympanum meaning eardrum.It refers to the whitish fleck posterior to the eye, that also includes most of the tympanum, that is exhibited by most specimens.This whitish fleck is more pronounced in preserved specimens than in living ones.The epithet is treated as an invariable noun in apposition.
Comparison with other species.About 30 Oreophryne species have a cartilaginous connection between procoracoid and scapula.Among this group of Oreophryne are species having a peeping call and those with a rattling call.We compare Oreophryne albitympanum sp.nov. to all Ore ophryne of similar size, with a rattling advertisement call and a cartilaginous procoracoid-scapula connection; and to those species for which these characters are unknown.Further, its advertisement calls are shorter (0.83 -0.96 s vs. 1.2 -1.5 s), note and internote length are also shorter (9 -14 ms and 22 -31 ms vs. 32 -45 and 37 -69 ms) and note repetition rate is much faster (26.0 -27.7 notes/s vs. 11.3 -11.7 notes/s).Oreophryne waira GüntheR, 2003 is smaller (SUL of males 17.8 -18.9 mm vs. 21.3-22.9 mm) than the new species and has a different ratio END/IND (0.94 -1.05 vs. 0.79 -0.95) and TyD/ED (0.21 -0.28 vs. 0.32 -0.44).Moreover, its call is considerably shorter (0.34 -0.62 s vs. 1.2 -1.5 s) and note repetition rate is higher (about 14 notes/s at temperatures of 19 -21 °C) than in the new species.Oreophryne wolter storffi (weRneR, 1901) has more extensive webs between toes, web between toe 4 and 5 reaches up to penultimate subarticular tubercle of toe 5, vs. basal webs only between toes 3 and 4 and 4 and 5 in O. albitympanum sp.nov.and web between toe 4 and 5 does not reach to penultimate subarticular tubercle of toe 5.

Discussion
The descriptions of these two frog species brings to five the number of frogs described on the basis of collections made during the 2004 -2005 Foja Mountains RAP expeditions.Two of these, Litoria gasconi and Pseudocallu lops foja, occur at low-to mid-altitudes (RichaRds et al. 2009;GüntheR et al. 2016)  Choerophryne pipiens was included in a phylogenetic assessment of the genus (as Choerophryne sp.A4) by OliveR et al. (2017), who demonstrated that it belongs to a clade inferred to have diversified primarily in montane habitats of New Guinea's central cordillera and that subsequently independently colonised the North Coast Ranges.The two species most morphologically and bioacoustically similar to C. pipiens, C. brunhildae from the isolated Adelbert and Torricelli Ranges in northern Papua New Guinea (menZies 1999; KRaus 2013) and C. murrita from montane habitats in the central cordillera (KRaus & allisOn 2009) were not included in that study and a bet-ter understanding of these species' relationships to congeners must await a more comprehensive phylogenetic assessment.
KRaus (2013) described two new Oreophryne species from the isolated Adelbert and Torricelli mountains in northern Papua New Guinea that have a cartilaginous connection between the procoracoid and scapula.He noted that O. cameroni and O. parkopanorum are the only members of the genus occurring in the mainland North Coast Ranges (excluding the geologically independent 'Birds-head Region') to exhibit this feature.The discovery of O. albitympanum sp.nov. in the Foja Mountains, a range isolated by extensive and presumably unsuitable lowland habitats from the Adelbert and Torricelli Ranges, suggests that more species exhibiting this character may occur on other isolated ranges in the region.KRaus (2013) also noted that all Oreophryne species known to date from these ranges have one of two call types; a series of unpulsed peeping notes or a pulsed rattle; in contrast a range of other call types are exhibited by members of the genus in the central cordillera and in other areas of the mainland.The call of O. albitympanum, a simple 'rattle', conforms to this pattern of limited call types in the North Coast Ranges, reflecting the relatively recent origin and limited colonisation of these accreted island arcs.pRiatna, and Dr yance de fRetes of Conservation International provided support and assistance during the survey and the community of Kwerba generously hosted our field studies.sancOyO lananG facilitated our work in Indonesia, and Ibu mumpuni, hellen KuRniati and iRfan setiK from the Museum Zoologicum Bogoriense allowed examination of specimens in their care, approved export permits, registered specimens and provided various other assistances.maRK hutchinsOn and caROlyn KOvach provided access to specimens at the South Australian Museum and lisa capOn kindly produced Figure 9.Additional funding for this project was provided by grants from the maRK mitchell Foundation, the Australian Pacific Science Foundation, the winifRed viOlet scOtt Trust and the South Australian Museum Board.We are grateful to james menZies (Adelaide) who provided call recordings of Choerophryne brunhildae and fRed KRaus (Ann Arbor) for another relevant call recording.

Fig. 9 .
Fig. 9. Map of New Guinea showing the type locality (arrow) of Oreophryne albitympanum sp.nov.and Choerophryne pipiens sp.nov. in the Foja Mountains, northern Papua Province of Indonesia.

Table 2 .
Body measurements and body ratios of the type series of Oreophryne albitympanum sp.nov.MZB Amph.11996 is the holotype, MZB Amph.12012 and MZB Amph.12013 are adult females, all others are adult males.All measurements are in mm; Reg.No.= registration number, SD = standard deviation.All other abbreviations are explained in "Materials and methods".
whereas three (Callulops fo jaensis, Choerophryne pipiens sp.nov.and Oreophryne albitympanum sp.nov.) are known only from near the summit of the range ( > 1,500 m, OliveR et al. 2012; this study).