Vocal Behavior of the Elusive Purple Frog of India (<i>Nasikabatrachus sahyadrensis</i>), a Fossorial Species Endemic to the Western Ghats

<div><p>Quantitative descriptions of animal vocalizations can inform an understanding of their evolutionary functions, the mechanisms for their production and perception, and their potential utility in taxonomy, population monitoring, and conservation. The goal of this study was to provide the first acoustical and statistical analysis of the advertisement calls of <i>Nasikabatrachus sahyadrensis</i>. Commonly known as the Indian purple frog, <i>N. sahyadrensis</i> is an endangered species endemic to the Western Ghats of India. As the only known species in its family (Nasikabatrachidae), it has ancient evolutionary ties to frogs restricted to the Seychelles archipelago (Sooglossidae). The role of vocalizations in the behavior of this unique species poses interesting questions, as the animal is fossorial and potentially earless and it breeds explosively above the soil for only about two weeks a year. In this study, we quantified 19 acoustic properties of 208 calls recorded from 10 males. Vocalizations were organized into distinct call groups typically composed of two to six short (59 ms), pulsatile calls, each consisting of about five to seven pulses produced at a rate of about 106 pulses/s. The frequency content of the call consisted of a single dominant peak between 1200–1300 Hz and there was no frequency modulation. The patterns of variation within and among individuals were typical of those seen in other frogs. Few of the properties we measured were related to temperature, body size, or condition, though there was little variation in temperature. Field observations and recordings of captive individuals indicated that males engaged in both antiphonal calling and call overlap with nearby calling neighbors. We discuss our findings in relation to previous work on vocal behavior in other fossorial frogs and in sooglossid frogs.</p></div

Vocal interaction in <i>Nasikabatrachus sahyadrensis</i>.

<p>Shown are two 23-s segments of a vocal interaction that occurred between two males (A and B) while held in close proximity in captivity. The letter above each series of calls corresponds to the male that produced the call. In instances of call overlap, the first letter indicates the male that called first and was subsequently overlapped by the male indicated by the second letter. Times correspond to the time between the onset of the overlapped male's call and the onset of the subsequent overlapping call. <i>Inset</i>: Shown here are details of the two shaded regions with the calls of male A and male B illustrated in different colors. The first and second 23-s segments of this interaction are included as audio files in the Supporting Information for this article (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0084809#pone.0084809.s002" target="_blank">Audio S2</a> and <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0084809#pone.0084809.s003" target="_blank">Audio S3</a>, respectively).</p

<i>Nasikabatrachus sahyadrensis</i> calling.

<p>Dorsolateral (a) and frontal (b) views of a calling male that was removed from under the soil at the entrance of the tunnel from which it had been calling. The male was induced to call above ground after brief exposure to a female.</p

Advertisement calls of a male <i>Nasikabatrachus sahyadrensis</i>.

<p>(a) 30-s segment of continuous, spontaneous calling by a single male. (b) 5-s segment showing the three consecutive call groups underlined in (a). (c) 0.5-s segment showing the three calls of the call group underlined in (b). (d) 0.1 s segment showing the call underlined in (c). (e) Spectrogram of the call illustrated in (d); <i>Inset</i>: power spectrum averaged over the duration of the call depicted in (d). The entire 30-s segment depicted in this figure is included as an audio file in the Supporting Information for this article (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0084809#pone.0084809.s001" target="_blank">Audio S1</a>).</p

Descriptions of the acoustic properties measured for call groups, calls, and pulses.

†<p>Values for pulses were determined for the middle pulse (k/2+1), where <i>k</i> is the total number of pulses). Because there was no silent interval between pulses, pulse duration is equivalent to the period of the middle pulse.</p

Descriptive statistics for call groups, calls, and pulses, including means (<i>X¯</i>), standard deviations (SDs), ranges, and coefficients of variation.

†<p>For calls per call group and pulses per call, the values reported in the columns headed <i>X¯</i> and SD, respectively, are the median and interquartile range. Note, however, that coefficients of variation for these two properties are computed from the <i>X¯</i> and SD.</p

Results of Spearman rank correlations between acoustic properties and temperature, body size, and condition (<i>N</i> = 10).

†<p>Scatterplots depicting correlations with <i>P</i>-values below the conventional (uncorrected) α level of 0.05 are included in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0084809#pone.0084809.s004" target="_blank">Figure S1</a>.</p

Close-ups of <i>N</i>. <i>sahyadrensis</i>, stage 46.

<p>(A) Lateral oblique view of the skull. (B) Ventral view of the anterior skull. (C) Attachment of the pectoral girdle to the axial skeleton. (D) Articulation of the humeral head with the glenoid fossa. (E) Fusion of ilia. (F) Long cylindrical femur. (G) Tibiafibulare. Abbreviations: ANP, anterior ramus of pterygoid; APM, anterior maxillary process; ARP, articular process; CL, clavicle; CR, coracoid; CSN, crista subnasalis; EPK, epidermal knob; EPY, cartilaginous epiphysis; EX, exoccipital; FC, femoral crest; FNL, fenestra nasolateralis; FP, frontoparietal; HU, humerus; HUC, humeral crest; ILC, ilial crest; IPC, inferior prenasal cartilage; LPI, lateral process of ilium; NSL, nasal; OBC, oblique cartilage; OSQ, otic process of squamosal; PAO, planum antorbitale; PAP, pars alaris of premaxilla; PDM, pars dentalis of maxilla; PDP, pars dentalis of premaxilla; PFM, pars facialis of maxilla; PL, degenerating palatoquadrate; PPM, posterior maxillary process; PPP, pars palatina premaxilla; PU, pubis; SP, scapula; SPC, superior prenasal cartilage; SS, suprascapula. Scale bars: 1 mm.</p

Presence/absence (1/-) of cranial and postcranial bones in <i>N</i>. <i>sahyadrensis</i> between Gosner stages 25 and 46.

<p>Presence/absence (1/-) of cranial and postcranial bones in <i>N</i>. <i>sahyadrensis</i> between Gosner stages 25 and 46.</p

Development of the appendicular skeleton in <i>N</i>. <i>sahyadrensis</i>.

<p>(A) Right side of the pectoral girdle at stage 38. (B) Right side of the pectoral girdle at stage 41. (C) Right side of the pectoral girdle at stage 42. Note the cartilaginous epicoracoid, bridging clavicle and coracoid. (D) Forelimbs attached to the pectoral girdle via proximal end of humeri, stage 45. (E) Manus at stage 46. (F) Lateral view of the pelvis at stage 42. (G) Dorsal view of the pelvis at stage 42. (H) Dorsolateral view of the pelvic girdle at stage 45. (I) Dorsal view of tarsals at stage 45. (J) Dorsal view of hind limb at stage 45. (K) Lateral view of prehallux at stage 45. Abbreviations: AC, acetabulum; CL, clavicle; CP2, carpal 2; CP (3–5), fused carpals 3–5; CR, coracoid; CT, cleithrum; DPP, distal prepollex; EC, epicoracoid cartilage; EY, element Y; FB, fibulare; FM, femur; HU, humerus; IL, ilium; IS, ischium; MC, metacarpals; MT, metatarsals; PC, procoracoid cartilage; PD, phalange digits; PH, prehallux; PH1, distal prehallux 1; PH2, distal prehallux 2; PH3, distal prehallux 3; PP, prepollex; PU, pubis; RD, radiale; RU, radioulna; SP, scapula; SS, suprascapula; TB, tibiale; TF, tibiafibulare; T3, tarsal 3; UL, ulnare. Scale bars: 1 mm.</p