Nyctimystes bivocalis, Kraus, Fred, 2012

Kraus, Fred, 2012, Identity of Nyctimystes cheesmani (Anura: Hylidae), with description of two new related species, Zootaxa 3493, pp. 1-26 : 7-12

Nyctimystes bivocalis sp. nov.

Fig. 1 C, D

Holotype. BPBM 15201 (field tag FK 4978), adult male, collected by F. Kraus along Upaelisafupi Stream, 10.4971° S, 150.2330° E, 715 m elevation, Cloudy Mountains, Milne Bay Province, Papua New Guinea, 8 April 2002.

Paratypes (n = 30). Papua New Guinea: Milne Bay Province: Cloudy Mts., along Upaelisafupi Stream, 10.4971° S, 150.2330° E, 715 m elevation, 8–22 April 2002 ( BPBM 15202–07, 15209–24, 15514, PNGNM 24124–28, 24140); SE slope Mt. Pekopekowana, along Wailahabahaba Creek, 10.2826˚ S, 150.1548˚ E, 615 m, 15 May 2002 ( BPBM 15225).

Diagnosis. Nyctimystes bivocalis is unique in its combination of medium body size (male SV = 38.5–49.2 mm, female SV = 42.2–55.7 mm); presence of a small tubercle on heel; webbing on hand extending up to middle of or slightly past penultimate tubercle on fourth finger; tympanum exposed; palpebral reticulum well-developed, with an obliquely vertical orientation but having a few to many horizontal cross-connections; snout relatively long and narrow (EN/IN = 1.04–1.58); iris dark brown in adults, pale tan in juveniles; rear of thighs barred, blotched, or unicolor brown, caramel, or blue-gray; dorsum sexually dimorphic in color, with males typically being gray, brown, or gray-brown ( Fig. 1 C), and females usually being orange-brown ( Fig. 1 D); males with vocal slits; and call a long train (19 to thousands) of two-note, relatively short (0.436– 0.518 s) unpulsed croaks delivered relatively slowly (1.05-1.44 calls/s), with short note durations (0.076– 0.106 s) and with a dominant frequency of 1.56–1.72 Hz.

Comparisons with other species. Nyctimystes bivocalis differs from N. avocalis , N. disruptus , N. oktediensis , N. papua , N. trachydermis , and N. tyleri in having (vs. lacking) vocal slits and vocal sac in males; from N. foricula , N. granti , N. gularis , N. humeralis , N. kubori , N. kuduki , N. montanus , N. narinosus , N. persimilis , and N. zweifeli in having (vs. lacking) a distinct tubercle on the heel; from N. obsoletus in having an exposed tympanum (hidden in N. obsoletus ); from N. pulcher in its smaller size (female SV to 84 mm, male SV to 65 mm in N. pulcher ) and small tubercle (vs. large lappet) on heel; from N. fluviatilis in lacking (vs. having) a row of pale-colored tubercles on outer edge of tarsus, having a thinner palpebral reticulum, and lacking bright orange on rear of thighs (present in N. fluviatilis ); from N. perimetri in its smaller size (male SV to 61 mm, female SV to 76 mm in N. perimetri ), less prominent heel tubercle, and call consisting of a long train of short, two-note croaks (call one or two drawn-out raspy croaks delivered at long intervals in N. perimetri ); from N. semipalmatus in having rear of thighs barred, mottled, or stippled with brown, tan, or blue gray (rear of thighs uniform bright orange in N. semipalmatus ), a brown dorsum sometimes mottled or freckled with dark brown or black but without distinct black spots (dorsum light tan or gray with rounded black spots in N. semipalmatus ), and call consisting of a long train of short, two-note croaks (call a rapid series of single-note croaks in N. semipalmatus ). From N. cheesmani , N. bivocalis differs in its dark-brown iris in adults (light brown in N. cheesmani ), longer snout (EN/IN = 0.98–1.18 in N. cheesmani ), more extensive hand webbing (reaching no further than base of penultimate tubercle on fourth finger in N. cheesmani ), palpebral reticulum with more horizontal cross-connections, sexually dimorphic dorsal color, and two-note call structure (call a regular train of notes in N. cheesmani ) with shorter (0.289– 0.365 s in N. cheesmani ) unpulsed notes (pulsed in N. cheesmani ) and with a lower dominant frequency (1.84–1.96 Hz in N. cheesmani ). Morphologically, N. bivocalis is most similar to N. daymani , from which it differs in its greater size (male SV to 42 mm, female SV to 48 mm in N. daymani ) and its long train of two-note calls (a train of single notes in N. daymani , cf. Menzies 2006). Judging from the information provided by Zweifel (1958), N. bivocalis would appear to differ from N. daymani as well in having more frequent horizontal cross-connections between the vertical lines of the palpebral reticulum.

Description of holotype. An adult male with right-lateral incision. Vomeropalatines with two patches of teeth (4 on right side, 3 on left) between internal nares. Vocal slits and sac present. Head moderately wide (HW/SV = 0.35), equal to length (HL/SV = 0.35, HL/HW = 1.00); loreal region oblique; canthus rostralis sharp, concave; nostrils closer to tip of snout than to eyes; internarial distance less than distance from external naris to eye (EN/IN = 1.08, IN/SV = 0.086, EN/SV = 0.093); snout slightly rounded when viewed from the side, acutely rounded when viewed from above; eyes of moderate size (EY/SV = 0.12), not especially protuberant, eyelid slightly less than width of interorbital distance; tympanic ring distinct but top margin covered by supratympanic skin fold, horizontal diameter less than half width of eye (TY/EY = 0.37). Skin of dorsal surfaces finely granular; ventral surfaces of body and thighs coarsely granular, smooth under arms and tibiae. Fingers less than one-half webbed, I 2.5–2.7 II 1.8–2.8 III 2.5– 2 IV; webbing less extensive between F2 and F3 but reaching top of penultimate tubercle of F2; only basal webbing present between F1 and F2; relative lengths 3>4>2>1; tips flattened into discs bearing circummarginal grooves; discs approximately twice width of penultimate phalanges on F2–F4 but only approximately 1.5 times width of penultimate phalanx on F1; single subarticular tubercle present at base of each phalanx; metacarpals without clear tubercles; low outer metacarpal tubercle present, inner a long, low oval. First finger with nuptial pad of fine, light-brown dermal asperities in approximately an L shape, with main body of pad lying between and dorsal to penultimate phalangeal tubercle and inner metacarpal tubercle, and with a short ventral tail extending posteriorly along the dorsal margin of inner metacarpal tubercle. Toes well webbed, I 1– 2 II 1– 2 III 1– 2 IV 2– 1 V; relative lengths 4>5>3>2>1; tips flattened into discs with circum-marginal grooves; discs only slightly wider than penultimate phalanges; inner metatarsal tubercle a low, short oval; outer absent. Hind legs moderately long (TL/ SV = 0.51), with a small tubercle at the heel.

In preservative, dorsal ground color gray brown with network of darker gray-brown markings and a few tan flecks. Sides dark brown freckled with light gray tan; face light gray tan with many tiny dark-brown flecks. Rear of thighs dark brown with orange cast, vaguely barred or stippled with dark brown and pale tan. Venter cream with tiny brown flecks, these densest from chin to chest, sparse on abdomen; under legs same, with sparsest flecking under thighs. Series of low white tubercles along outer margin of forearm. Hands and feet, including webbing, dark brown. Iris dark brown. Lower eyelid with thick black upper margin; palpebral reticulum with several obliquely vertical lines, these silver and brown and joined by several horizontal cross-connections anteriorly and posteriorly, especially on right side; lower half of lower eyelid dark gray flecked with light gray.

Measurements (in mm). —SV = 45.1, TL = 23.0, HW = 15.7, HL = 15.6, IN = 3.9, EN = 4.2, SN = 7.0, EY = 5.4, TY = 2.0.

Variation. Snout-vent length varies from 38.5–49.2 mm; otherwise, mensural variation is rather minor except for EN/IN, with SD = 0.024 ( Table 3 ). This last represents a wide range of values for snout shape, spanning 1.04–1.58 ( Table 3 ). Sexual mensural dimorphism in the sample is not obvious for any feature, except for SV, with females the larger sex ( Table 3 ).

Males (n = 16) Females (n = 14)

Character

mean SD range mean SD range The heel tubercle is small but usually obvious and often tipped with white. In five specimens, it is so reduced as to not be clearly distinguished from heel skin. In these specimens, its apparent absence is likely a preservation artifact, as it is sometimes obvious on one leg of a specimen but not on the other. Hand webbing reaches to middle of or to beyond penultimate tubercle of F4 and to beyond penultimate tubercle of F2. Series of tubercles along the metacarpals are evident in some specimens but not all, the variation seeming to be a preservation artifact. The third and fifth toes are generally subequal in length, but some specimens have one clearly slightly longer than the other. The palpebral reticulum almost always has some horizontal cross-connections, and often quite a number of them. These are usually concentrated anteriorly, but they can occur anywhere. Nuptial pads are uniformly like those of the holotype.

Males are typically light gray, medium brown, or gray brown and freckled or mottled with darker brown. One is dark brown with a few orange-brown spots; one has a few beige spots; another is orange tan mottled with medium brown. In contrast, females are generally orange brown in color and vaguely mottled with darker brown. One is uniformly gray brown, looking similar to the males; another is dark brown with a dark-orange cast on the sides. Darker mottling can vary from sparse ( Fig. 1 D) to prominent; one female has a few small enamel-cream markings. Venters are cream and usually stippled with dark brown. This stippling is typical for the males and is generally concentrated anteriorly or on the sides; females are usually sparsely stippled, with a little along the jaw margin or on the throat. The two darker females are more generally stippled ventrally. The pattern on the rear of the thighs varies considerably. Some specimens are uniformly dark brown, but most of them have some form of “tiger-striped” pattern consisting of a blue-gray or dark salmon or orange-brown ground with caramel-brown bars and maculations, or the reverse, depending on which color field predominates in areal size. All adults have darkbrown irises, but one newly metamorphosed frog (BPBM 15208) has a pale-tan iris, which is clearly observable in preservative.

Color in life. From field notes for BPBM 15201 (male): Dorsum tan with obscure brown reticulum; ground color and barring on legs more or less same colors as dorsum; venter white with heavy maroon suffusion on chin, throat, chest, sides, and undersides of legs; palpebral reticulum gold on a black background; iris brown. BPBM 15204 (female) was tan with lavender bars on the back of the thighs, and BPBM 15213 (female) had an orangebrown dorsum with darker orange-brown reticulum across the center, yellow-orange in the groin and on the hidden surfaces of the thighs, and a purple-brown palpebral reticulum. Color images illustrate additional variants that are tan with numerous light purple-gray flecks (male, Fig. 1 C) or beige with a pale-lavender reticulum and numerous brick-red dots (female, Fig. 1 D).

Call. The call of Nyctimystes bivocalis consists of a pair of rapid, unpulsed, well-tuned croaks ( Fig. 3 B, 4A, C), each pair delivered as part of a series that can extend interminably: series recorded by me lasted for 21–68 s, but I heard one uncaptured animal call without pause for more than two hours. To the human ear, the impression of these calls is similar to that of a pile driver, but without the musical quality. The two-note call is delivered at a rate of 0.69–0.95 calls/s, calls average 0.476– 0.487 s (range 0.436– 0.508 s) in length for three call series recorded by me, with intervals between calls averaging 0.596– 0.962 s and ranging from 0.507– 1.528 s ( Table 4 ). Calling rate appears to decrease with ambient temperature ( Table 4 ). Each call note is short, averaging 0.080–0.092 for the first note and 0.089–0.095 for the second; intervals between notes within a call average 0.294– 0.311 s across three call series and range from 0.261– 0.335 s ( Table 4 ). For BPBM 15202, the dominant frequency of the first note was usually lower than that for the second note, being of higher pitch in only three of 49 calls. In BPBM 15303 the situation was reversed, with 10 of 14 first notes being of higher pitch than the second note. Notes begin abruptly and increase and decrease in amplitude rather gradually; however, the end of each note tends to decrease more gradually, producing a teardrop-shaped wave function ( Fig. 3 B). This is often more prominently developed in the second note of each call. Notes lack frequency modulation ( Fig. 4 C), have a dominant frequency ranging from 1560–1720 Hz ( Fig. 4 B, Table 4 ), and have harmonics present at around 4800 Hz ( Fig. 4 C) and 8000 Hz (faintly developed and not apparent in Fig. 4 C but apparent in Fig. 3 B).

Etymology. The name is a masculine Latin adjective meaning “having a doubled voice”, and is named for the species’ distinctive two-note call.

Range. Known only from the Cloudy Mts. and the southernmost extent of the Owen Stanley Range west of Alotau, Milne Bay Province, Papua New Guinea ( Fig. 5 , circles).

Ecological notes. Animals were common near small (1–3 m wide) forested streams at elevations of 600– 720 m. One of these streams was shallow, rocky, and with several rapidly flowing riffles; the second was deeper, silty, and with many deeper pools but few riffles. Forest in both elevations was small-crowned lowland hill forest ( Paijmans, 1975, 1976) with canopies of ca. 30–40 m height.

Remarks. Morphological differences between Nyctimystes bivocalis and N. daymani are minor, with body size being the most distinctive feature. Consequently, if not for the call differences, it might be thought that the two are conspecific. That they represent distinct populations is, however, also confirmed by discriminant-function analysis of morphometric features ( Table 5), which mis-assigns only one specimen of N. bivocalis to N. daymani . Discrimination is greatest in EN, IN, and SN, with N. daymani having the greater values for the first two characters and N. bivocalis the greater values for the last. Discrimination among these species is further supported by canonical-variates analysis, which clearly distinguishes N. bivocalis from both N. daymani and N. cheesmani ( Fig. 6 , Table 6 ).

So far as is presently known, the sexually dimorphic color pattern of Nyctimystes bivocalis (males predominantly brown, gray, or gray brown; females predominantly orange brown) is unique within the N. cheesmani complex, including among additional populations not treated in the present study.

n 39 Hotelling’s t2 95.18 F 8.289 p 5.461 e -6 # misassigned 1 Coefficients

SV -0.514 TL 1.379 EN -3.856 IN -4.109 SN 4.859 TY -0.064 EY 7.495 HW 2.578 HL -2.061

Figures

FIGURE 1. Portraits in life of (A) Nyctimystes cheesmani, BPBM 18293, Fane, Central Province; (B) N. cheesmani, BPBM 18294, Fane, Central Province; (C) male N. bivocalis, BPBM 15206, Cloudy Mts., Milne Bay Province; (D) female N. bivocalis, BPBM 15209, Cloudy Mts., Milne Bay Province; (E) N. intercastellus, BPBM 16481, Fergusson Is., Milne Bay Province; (F) N. intercastellus, BPBM 37765, Normanby Is., Milne Bay Province.

FIGURE 3. Expanded waveforms and spectrograms showing note structure for (A) Nyctimystes cheesmani from Fane, Central Province (uncaptured), (B) N. bivocalis (BPBM 15202) from Cloudy Mts., Milne Bay Province, and (C) N. intercastellus (BPBM 17938) from Normanby Island, Milne Bay Province.

FIGURE 4. (A) Waveform, (B) power spectrum, and (C) spectrogram of ten two-note calls of Nyctimystes bivocalis, BPBM 15202, recorded in Cloudy Mts., Milne Bay Province, 9 April 2002, air temperature 24.4 C.

FIGURE 5. Map of the Southeastern Peninsula of New Guinea showing localities for Nyctimystes cheesmani (star), N. bivocalis (circles), and N. intercastellus (triangles). Type localities are solid symbols; additional localities are open symbols.

FIGURE 6. Bivariate plot of canonical variate axes 1 and 2 showing a posteriori multivariate discrimination among Nyctimystes cheesmani (open squares), N. bivocalis (open circles), and N. daymani (diamonds).

Tables

TABLE 3. Mensural variation among adults of Nyctimystes bivocalis.

SV (mm)	45.5	0.7417	38.5–49.2	49.7	1.1183	42.2–55.7
TL/SV	0.52	0.0029	0.50–0.54	0.53	0.0077	0.50–0.62
EN/SV	0.099	0.0016	0.088–0.112	0.102	0.0016	0.092–0.114
IN/SV	0.083	0.0012	0.073–0.094	0.079	0.0014	0.069–0.088
SN/SV	0.16	0.0017	0.14–0.17	0.15	0.0028	0.14–0.17
TY/SV	0.043	0.0013	0.033–0.052	0.047	0.0014	0.038–0.055
EY/SV	0.12	0.0031	0.10–0.14	0.11	0.0015	0.10–0.12
HW/SV	0.35	0.0029	0.34–0.37	0.35	0.0038	0.34–0.39
HL/SV	0.34	0.0028	0.32–0.36	0.34	0.0034	0.32–0.36
EN/IN	1.20	0.0267	1.05–1.40	1.30	0.0369	1.04–1.58
HL/HW	0.97	0.0087	0.91–1.03	0.96	0.0080	0.89–0.99

TABLE 4. Call data for two specimens of Nyctimystes bivocalis from the type locality. Numbers for call parameters are mean ± SD (range).

Character	BPBM 15202 call 1	BPBM 15202 call 2	BPBM 15203
Temperature (C)	24.4	24.4	22.2
Number of calls	19	30	47