Referred specimens: Four adult specimens (all males), all from the state of Amazonas. Two males INPA-H 041289 and INPA-H 041290 (field number 02ZF2 and 03ZF2) collected by R.F. Jorge and S.S. Sales on 19th January 2017 on the banks of a stream in the middle course of the Cuieiras River near LBA/ZF2 scientific station (2°33’32.40″ S, 60°13’48.36″ W), municipality of Manaus; two males INPA-H 041291 and INPA-H 041292 (field number 16FU and 17FU) collected by R.F. Jorge and S.S. Sales on 26th January 2017 on the margins of a stream in the headwaters of the Taruma-Açu River at Fazenda Experimental da Universidade Federal do Amazonas (2°38’31.20″ S, 60°5’45.6″ W), municipality of Manaus. These specimens were used for genetic analyses. Two males INPA-H 041372 and INPA-H 041373 (field number: PTAP03-1 and 55DI) were used to record the type 2 and type 3 calls.
Diagnosis: A small species of
Atelopus; adult males SVL 19.1–26.4 mm (
n = 11), adult females 27.9–28.8 mm (
n = 2); interdigital webbing covering all of Finger I and a phalange of Finger II and rudimentary between other fingers; absence of serrated fringe on the sides of Finger III (
Figure 4A,B); first phalange of Toe I atrophied, completely hidden in skin of the foot (similar to a callus), with no visible phalanges (
Figure 5A,B); subarticular tubercles absent from hand and foot; palmar tubercles round and visible and plantar tubercles oval and poorly defined; the interdigital webbing reaches half of the third phalange of Toe IV and half of the first phalange of Toe V; in life, dorsum light brown to reddish brown with light yellow or light green reticulation network (
Figure 6A–D); ventral surface of feet, hands, half of the posteroventral portion of thighs and half or all of the posteroventral portion of the cloacal region red (
Figure 6E–H); throat, chest, and central portion of belly white or whitish cream without spots in males, spotted in females; advertisement call consisting of a single multipulsed note with a call duration of 689–840 ms consisting of 15–26 pulses, with a dominant frequency of 3088–3610 Hz and bandwidth of 633–915 Hz (
Figure 7A,B). Morphometric measurements of the holotype and type series are shown in
Table 4.
3.3.1. Taxonomic Comparisons
Interspecific morphological and bioacoustic comparisons were made between Atelopus manauensis sp. nov. and the geographically and phylogenetically closest species. Characteristics of the compared species are presented in parentheses, unless specified.
Atelopus manauensis sp. nov. differs from the population of
A.
hoogmoedi of REBIO Uatumã and Pitinga River by lacking basal and subarticular tubercles on the hands [
A.
hoogmoedi basal tubercles present on hands (
Figure 8A) and feet and two subarticular tubercles on Toe IV (
Figure 8B)].
Atelopus manauensis sp. nov. is smaller than any individual from the populations of
A.
hoogmoedi of REBIO Uatumã and Pitinga River and is differentiated by a maximum SVL of 26.4 mm for adult males (minimum SVL for
A.
hoogmoedi of REBIO Uatumã and Pitinga River 32.9 mm); dorsum light brown to reddish brown with a light yellow or light green reticulation network (dorsum dark brown to black with yellow reticulation network); ventral surface of hand and feet red in life, cream or brown in preservative, without spots (cream-colored with dark brown spots in life and in preservative); venter all white or white with a cream-colored gular region and head (bright yellow); red spot restricted to half of the posteroventral portion of thighs and all or half of the posteroventral portion of cloacal region red (black spot limited to the cloacal region); advertisement call with a maximum duration of 840 ms (1071 ms) consisting of up to 26 pulses (37 pulses) and a dominant frequency of 3088–3610 Hz (2498–3058 Hz) (
Figure 7F,G).
It differs from
Atelopus hoogmoedi of Amapá (Brazil) by having a light brown to reddish brown dorsum with a light yellow or light green reticulation network (dark brown to black dorsum with yellow, orange, or pink reticulation network); venter all white or white with cream-colored gular region and head (bright yellow); red spot restricted to half of the posteroventral region of thighs and half or all of the posteroventral portion of the cloacal region red (red spot covering the entire posteroventral portion of the cloacal region extending to near the knee and to the initial portion of the belly; photos C.E. Costa-Campos at AmphibiaWeb/
Atelopus hoogmoedi); advertisement call duration of 689–840 ms (873–1710 ms; [
50]) consisting of up to 26 pulses (35 pulses; [
50]), dominant frequency of 3088–3610 Hz (2812–2838 Hz; [
50]), and a bandwidth of 633–915 Hz (280–568 Hz; [
50]) (
Figure 7D,E).
Atelopus manauensis sp. nov. can be differentiated from
A.
hoogmoedi SS of French Guiana by a maximum SVL of 28.8 mm for females (minimum SVL 31.2 mm for females; [
9]), tibia 47% of SVL (tibia varying from 43% to 45% of SVL among populations; [
9]); dorsum light brown to reddish brown with light yellow or light green reticulation network (dorsum dark brown to black with yellow, orange, or pink reticulation network; [
52,
53]); and advertisement call duration of 689–840 ms (1190–1200 ms; [
7]) consisting of 15–26 pulses (40–42 pulses; [
7]).
It differs from
Atelopus hoogmoedi of Guyana by having a light brown to reddish brown dorsum with a light yellow or light green reticulation network (dark brown to black dorsum with yellow dorsolateral bands and marks with black spots; [
54]); venter all white or white with a cream-colored gular region and head (venter, throat, and head yellow, pink, or orange with irregular black marks; [
54]); interdigital webbing covering all of Finger I and a phalange of Finger II and rudimentary between other fingers (fingers unwebbed; [
54]); longer interdigital webbing between toes IV and V (toes moderately webbed; [
54]); and Toe I reduced (Toe I and Toe II much reduced; [
54]).
The new species is distinguished from
Atelopus franciscus by the larger size of females, a minimum SVL of 27.9 mm (maximum SVL of 26.5 mm; [
9]); venter all white or white with a cream-colored gular region and head (venter and thighs red; [
9]); and advertisement call duration of 689–840 ms (1340–1640 ms; [
7]) consisting of 15–26 pulses (31–39 pulses; [
7]).
Atelopus manauensis sp. nov. differs from
A.
flavescens by the smaller size of females, maximum SVL of 28.8 mm (minimum SVL of 31.5 mm; [
9]), and of males, maximum SVL of 26.4 mm (minimum SVL of 27 mm; [
9]); shorter tibia in females of 12.1–12.9 mm (minimum tibia length 13.0–16.0 mm; [
9]); dorsum light brown to reddish brown with light yellow or light green reticulation network (dorsum varies in light yellow tones with small brown or light red vermiculation; [
9]); venter all white or white with cream-colored gular region and head in males and white with rounded spots in females (venter pink-salmon in females and pink in males; [
8]); and advertisement call duration of 689–840 ms (1340–1820 ms; [
7]) consisting of 15–26 pulses (45–58 pulses; [
7]).
The new species is distinguished from
A.
barbotini by having on average a longer tibia in males (TL/SVL = 0.47 in
A.
manauensis sp. nov.; TL/SVL = 0.44–0.45 in
A.
barbotini; [
7]); dorsum light brown to reddish brown with light yellow or light green reticulation network (dorsum black with scattered sinuous lines of opaque red colors; Lescure [
7]); and advertisement call duration of 689–840 ms (1300–1680 ms; [
7]) consisting of 15–26 pulses (41–53 pulses; [
7]).
Atelopus manauensis sp. nov. differs from
A.
spumarius SS by possessing a longer tibia, 47% of SVL (43% of SVL; [
7]), although female sizes are similar; absence of small warts behind the eyes (warts present; [
55]); and advertisement call consisting of up to 26 pulses (37 pulses; [
7]).
The new species differs from
A.
pulcher by its smaller size, with a maximum SVL for females of 28.8 mm (minimum SVL of 32.0 mm; [
4]); longer interdigital webbing between toes IV and V (shorter interdigital webbing; [
4]); no subarticular tubercles on the hand or foot (ill-defined subarticular tubercles on fingers II, III, and IV and toes II, III, IV, and V; [
4]); venter all white or white with a cream-colored gular region and head in males and white with dark brown rounded spots in females (light red venter; [
4]); red spot restricted to half of the posteroventral region of thighs and all or half of the posteroventral portion of the cloacal region red in males and females (red spot covering the entire ventral region of the thighs and all of the posteroventral portion of the cloacal region extending to the belly in males, and all of the venter, thighs, and head red with black spots in females; [
4]); advertisement call duration 689–840 ms (1100–1300 ms; [
4]) consisting of up to 26 pulses (47 pulses; [
4]) and a dominant frequency of 3088–3610 Hz (2034–2824 Hz; [
4]).
Finally,
Atelopus manauensis sp. nov. differs from
A.
seminiferus by the smaller size of males and females: SVL 19.1–26.4 mm in males, 27.9–28.8 mm in females (SVL 33.8–35.2 mm in males, 40 mm in females; [
56]); interdigital webbing covers two phalanges of Toe IV (interdigital webbing covers all of Toe IV; [
57]); dorsum light brown to reddish brown with light yellow or light green reticulation network (dorsum uniformly dark brown or black with small yellow spots; [
56,
57]); venter all white or white with a cream-colored gular region and head (venter dark brown streaked with white and orange; [
56]); and smooth sides (sides with tubercles; [
57]).
Description of the Holotype: Body slender; neural spines not evident externally; head slightly longer than wide (HW/HL = 0.97); snout acuminate, with oval tip, dorsally concave; head length 30% of SVL; maxilla projected slightly over mandible; nostrils lateral and not visible from above; canthus rostralis concave between nostril and tip of snout and moderately straight between eye and nostril; loreal region concave; nostril closer to tip of snout than to eye; distance between nostrils and eye equal to eye diameter; distance between nostrils greater than eye diameter; tibia 51% of SVL; foot shorter than tibia (FOOT/TL = 0.74); relative sizes of fingers I < II < IV < III and toes I < II < III < V < IV, with first phalange of Toe I being atrophied and the toe hidden in the skin, similar to a callus; hand webbing rudimentary, present only between Finger I and Finger II; foot webbing, disregarding the Toe I in the form of a callus: II 0−2
−, III 1
1/2–2
−1/2, IV 2
−1/3−1
+ V; palmar tubercle well defined and rounded (
Figure 4A) and plantar tubercle poorly defined and oval (
Figure 5A); subarticular tubercles absent; thumb 44% of hand length (THBL/HAND = 0.44), covered by tiny brown keratinized spikes (nuptial pads); dorsal skin smooth; belly with tiny black keratinized dots; gular region smooth. In life, dorsal and lateral surfaces of the body with a lime-green reticulated network spread irregularly on a chocolate brown background. Ventral region white with a cream-colored gular region and head; lower part of limbs with brown bands on the sides. Red spot restricted to half of the posteroventral region of thighs and half of the posteroventral portion of the cloacal region (
Figure 6E). In preservative, the dorsal surface was brown and the reticulated network was pale yellow. Ventral region colored similar as in life, only the red spots on the hands, feet, posteroventral region of thighs, and posteroventral portion of the cloacal region turn reddish brown (
Figure 3A–D).
Vocalization: The advertisement call of
Atelopus manauensis sp. nov. consists of a single multi-pulsed note issued at regular time intervals (
Figure 7A). The mean call duration is 744 ± 84 ms (689–840 ms) and consists of 19 ± 6 pulses (15–26 pulses) (
Figure 7B). Based on the inter-pulse interval, the song can be temporally divided into two portions, with the pulses being emitted more widely during the first two-thirds of the call than during the last third. The first pulse and central pulse have similar average pulse durations of 7 ± 1 ms (6–8 ms) and 6 ± 1 ms (5–7 ms), respectively. On the other hand, the last pulse is on average longer than all the other pulses in the song with a pulse duration of 14 ± 6 ms (8–19 ms), with downward frequency modulation (
Figure 7C). The inter-pulse interval at the beginning and center of the song lasts for 54 ± 16 ms (36–67 ms) and 50 ± 13 ms (40–65 ms), respectively, while the inter-pulse interval between the last two pulses lasts for 7 ± 3 ms (4–9 ms). The total pulse period duration of the first three pulses [132 ± 40 ms (92–172 ms)] is approximately three times longer than the pulse period duration of the last three pulses of the call [43 ± 6 ms (38–49 ms)]. The call has a dominant frequency of 3334 ± 263 Hz (3088–3610 Hz) and a bandwidth of 743 ± 151 Hz (633–915 Hz). The temporal and spectral parameters of the advertisement call of
A.
manauensis sp. nov.,
A.
hoogmoedi of REBIO Uatumã, of Pitinga River, and of Amapá are provided in
Table 5.
Type 2 call (pure tone call) of
Atelopus manauensis sp. nov. consists of an unpulsed short note (
Figure 9A–C) with a call duration of 137–217 ms (174 ± 24 ms,
n = 15) and shows an upward frequency modulation from the onset until the central portion of the call, and a downward frequency modulation from the central until the final portion (
Figure 9C). Calls are commonly emitted singly (
n = 12) and in a series of two (
n = 5) or three (
n = 2) calls. The average inter-call interval within a series is 499 ± 39 ms (434–541 ms,
n = 6) while the inter-call interval between single calls is 2793 ± 1441 ms (963–4766 ms,
n = 10). Type 2 calls have a dominant frequency of 2928–3143 Hz (3059 ± 75 Hz,
n = 15), a low frequency of 2630–2692 Hz (2676 ± 19 Hz,
n = 15), and a high frequency of 3052–3252 Hz (3171 ± 72 Hz,
n = 15). The average bandwidth is 303 ± 55 Hz (215–388 Hz,
n = 15).
The type 3 call (short pure tone call) of
Atelopus manauensis sp. nov. is characterized by an unpulsed short note (
Figure 9D–F) with a call duration of 57–165 ms (129 ± 31 ms,
n = 15). The frequency modulation of type 3 calls rapidly descends during the first fifth portion, after which it declines slowly until the end of the call (
Figure 9F). Type 3 calls are irregularly emitted and have an inter-call interval of 493–9264 ms (2295 ± 2812 ms,
n = 10). Type 3 calls are characterized by having a dominant frequency of 2907–3100 Hz (3020 ± 66 Hz,
n = 15), a low frequency of 2722–2907 Hz (2800 ± 69 Hz,
n = 15), and a high frequency of 3031–3304 Hz (3174 ± 78 Hz,
n = 15). Bandwidth ranges from 129 to 366 Hz (182 ± 75 Hz,
n = 15).
Different from type 2 and type 3 calls, the type 4 call (short pulsed call) of
Atelopus manauensis sp. nov. (
Figure 9G–I) consists of a short-pulsed note with a downward frequency modulation. Type 4 calls have a call duration of 53–93 ms (77 ± 10 ms,
n = 15), 4–8 pulses (6 ± 1 pulses,
n = 15), and inter-call interval of 285–1394 ms (437 ± 285 ms,
n = 15). The last pulse is always longer than the others (
Figure 9I); the first pulse has a pulse duration of 4–10 ms (5 ± 2 ms,
n = 15), while the last pulse has a pulse duration of 13–25 ms (17 ± 4 ms,
n = 15). Type 4 calls are emitted with a dominant frequency of 2585–2842 Hz (2721 ± 80 Hz,
n = 15), a low frequency of 2358–2482 Hz (2421 ± 46 Hz,
n = 15), and a high frequency of 3181–3421 Hz (3319 ± 77 Hz,
n = 15). The bandwidth of the type 4 call is 409–538 Hz (476 ± 42 Hz,
n = 15).