a detailed account of the reproductive strategy and developmental stages of nasikabatrachus...

7/30/2019 A Detailed Account of the Reproductive Strategy and Developmental Stages of Nasikabatrachus Sahyadrensis (An

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Accepted by M. Vences: 10 Sep. 2012; published: 9 Oct. 2012

ZOOTAXA

ISSN 1175-5326 (print edition)

ISSN1175-5334(online edition)Copyright 2012 Magnolia Press

Zootaxa 3510: 5364 (2012)www.mapress.com/zootaxa/

Article

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urn:lsid:zoobank.org:pub:1D2C3790-E2E0-4D80-8D7B-144884AFDD50

A detailed account of the reproductive strategy and developmental stages ofNasikabatrachus sahyadrensis (Anura: Nasikabatrachidae),

the only extant member of an archaic frog lineage

ANIL ZACHARIAH1, ROBIN KURIAN ABRAHAM2, 3, SANDEEP DAS4, K. C. JAYAN5 & RONALD ALTIG6

1Beagle, Chandakunnu, Wayanad 673 121, Kerala, India2Parolikal, YMR Jn., Nanthencode, Thiruvananthapuram 695 003, Kerala, India4Santhi Nivas, Chembukkavu, Thrissur 680 020, Kerala, India5Souparnika, Periyappuram, Muvattupuzha, Ernakulam 686 667, Kerala, India6Department of Biological Sciences, Mississippi State University, Mississippi State, MS 39762 USA.

E-mail: [email protected]

3Corresponding author. E-mail: [email protected]

Abstract

Novel and significant data on the breeding biology and tadpole morphology ofNasikabatrachus sahyadrensisexpands our

understanding of this unusual frog and clarifies some data in other reports. Nonpigmented eggs are laid in arrays or clumps

in small shaded rocky pools in the bedrock of torrential streams, as they are charged by early monsoon rains. The suctorial

tadpole adapted to rheophilic habitats, has a strongly depressed body, dorsal eyes, complete marginal papillae, a labial

tooth row formula of 2/3 or 2/3(1), and a medial vent with unusual flaps subtending the vent and limb buds. Tadpoles meta-

morphose in about 100 days. Additional site records and issues relating to the conservation of this frog and its habitat in

the southern Western Ghats of India are discussed.

Key words:Nasikabatrachus, tadpole, breeding, development, morphology, India

Introduction

Nasikabatrachus sahyadrensis, the sole member of the Nasikabatrachidae, is a rotund, fossorial frog endemic to the

mountains and foothills of southwest India. The presence of a fossorial adult that breeds explosively in streams

after episodic monsoon rains, adds to the oddity of this frog. After the description of this taxon (Biju & Bossuyt

2003), and the identification of the tadpole (Dutta et al. 2004), I. Das (2007) realized that the unusual tadpole had

been described almost 100 years earlier (e.g., Annandale 1918; Annandale & Rao 1916 1917; Fig. 5AB) with

various interpretations of its relationships (Annandale & Hora 1922; Ramaswami 1944; Rao 1938). The longeraccess to the tadpoles in streams and the short-term access to the secretive breeding adults surely accounts for this

discrepancy. Observation of the large metatarsal tubercle on the tadpoles hind limb indicated that the species had a

fossorial adult, and Rao (1938) suggested that the frog might belong to a novel subfamily.

Studying the biology of an explosive breeder demands that one accommodate for sporadic weather patterns.

After intensive surveys, we present new information that is vital for understanding the conservation issues of this

endemic amphibian. We discuss and illustrate data on the call, amplexus, eggs, embryos, and tadpole ofN.

sahyadrensis that enhances our understanding of this cryptic species and of its strange tadpole beyond the old

description by Annandale (1918) and the character list by Dutta et al. (2004).
http://zoobank.org/urn:lsid:zoobank.org:pub:1D2C3790-E2E0-4D80-8D7B-144884AFDD50http://zoobank.org/urn:lsid:zoobank.org:pub:1D2C3790-E2E0-4D80-8D7B-144884AFDD50


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ZACHARIAH ET AL.54 Zootaxa 3510 2012 Magnolia Press

Material and methods

This study was made from 20082012 in a stretch of the Munthirithodu stream (550700 m ASL), near Melukavu,

Kerala, India. Thirty-four specimens in Stages 146 from field collections were staged (Gosner 1960), measured,

and photographed, and some were fixed in 10% formalin for morphological measurements. Specimens [TNHM

(H) 12.6.22/71, 72] were deposited in the Natural History Museum, Trivandrum, India.

A tadpole in Stage 38 at 78 days of age was measured and described in detail with the terminology of Altig and

McDiarmid (1999). Measurements (rounded to 0.1 mm) were made with a Mitutoyo Digimatic caliper.

Reproductive behavior was observedduring early phases of the monsoons in AprilMay. Tadpoles were followed

and recorded till metamorphosis in AugustSeptember. Calls recorded with a TASCAM HDP2 portable stereo

recorder were analyzed with Raven 2.1, and behavioral photographs were made in the field.

Results

The habitat inhabited by Nasikabatrachus, comprising of a matrix of deciduous forests and grasslands (Fig. 1A),

includes seasonally flowing streams that are nourished by monsoon rains. Apart from the month long breeding

period, when they come out very briefly for the exclusive purpose of reproduction, adult Nasikabatrachus

sahyadrensis spend the rest of the year in the soil, often in proximity to a breeding site. Animals that have been dug

up from burrows appear healthy and alert and are not encased in any aestivation cocoon. Local people digging a

well found a female 200 m from a probable breeding site and 7.9 m below ground in December 2009. A gravid

female encountered 1.5 m below ground was found about 80 m from a breeding site by a farmer in April 2010.

FIGURE 1. (A) General habitat ofNasikabatrachus sahyadrensis, (B) a rocky crevice adjoining the stream, which is the

typical oviposition site, showing the opening through which the amplectic pair enters and arrow = watercourse through which

developed tadpoles exit the crevice, and (C) a fast-flowing reach of stream where the rheophilic tadpoles occur.

Male vocalization. The males have a single, pale, subgular vocal sac (Fig. 2AB) and produce a loud,

multinote call (Fig. 2DE) that is emitted in irregular series from inside shallow burrows adjacent to the streams.The fundamental frequency of the mating call is about 1200 Hz along with several harmonics; there are 56 pulses


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Zootaxa 3510 2012 Magnolia Press 55BIOLOGY OFNASIKABATRACHUS

per note. We were not able to get a recording of a softer sounding call that may have been an encounter call when a

female approached a male. Choruses were heard during the day and night, on rainy days from late April into middle

May. Twenty-two vocalizing males located along a 270 m stretch, on 25 April 2011 were all close to the stream in

individual burrows. Each burrow is spaced at an average of 3 m from each other, and is covered by leaf litter and

other vegetative debris. The weather was sunny with an ambient temperature of 25C and humidity of 96% at 1030

h. Call intensity remained high at 1200 h (overcast, 25C, 97%), but by 1530 h, twelve individuals were calling at

much lower intensities (rain, 23.8C, 97%). By 1800 h, only seven individuals were vocalizing (rain, 23.3C,

99%), and by 2100 h a single individual was calling with call intervals of 10 min (rain, 22.8C, 99%). Four other

males were heard calling from rocky seepage areas 25 m from the stream. This observation was made during the

earliest showers of the season, when conditions were overcast, but typically male calling activity begins on rainy

evenings, going on till early dawn and declining with decreasing rains as the pre-monsoon progresses.

FIGURE 2. (A) A male showing the single, subgular vocal sac while calling above ground, (B) a male calling at the opening of

a burrow, (C) a male retreating into its burrow after being disturbed by the researchers, (D) a spectrogram (24.7C, 28 April

2011; fundamental frequency about 1200 Hz with several harmonics; time in seconds versus kilohertz) of two notes of a call,

and (E) a plot of sound pressure in kilounits showing 56 pulses/note.

Courtship and oviposition. Adult males are about one-third of the size of females and vary in color from a

ruddy brown to purple. Females are mostly purplish-grey, and ovarian eggs could be seen through the ventrolateral

abdominal wall (Fig. 3BC). The behavior of a single pair, out of 14 amplectic pairs that were observed, is

described in detail. A female was spotted at 1920 h as she emerged from the soil and homed in on a male calling

from a burrow near the stream at 640 m ASL. The male exited his burrow, continuing to call. He clambered ontothe females back in a position typical of pectoral amplexus, but because of the rotund body shapes and short limbs

of these frogs, the small male presses his fists into each side of the large females vertebral column, clasping tightly

(Fig. 3AB). There are no adhesive glands on the males chest or belly. The females used a combination of walking

and hopping, to move the typically short distances to suitable oviposition sites that primarily included small,

hidden cavities and crevices in the rocky substrate of second-order streambeds (Fig. 1B). The amplectic pair

entered a shaded crevice, which opened at the bottom into a shallow, rock pool, which would become part of the

stream flow with additional rains. Once inside the crevice, the female rotated forward and backward inside the

cavity, in various directions, up to 80 times over an hour, between the exit opening and bottom of the crevice,

probably to ensure optimality of the selected oviposition site. The pair then moved to the base of the crevice with a

pool of water at the bottom and rested with their vents touching the water. The male positioned his vent nearer to

that of the female without changing his clasping position, to her inguinal area. The male pushed at the eggs in thefemales abdomen with his hind limbs, without changing his clasping position from the pectoral position. The


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fertilized, nonpigmented eggs (Fig. 4A) with one jelly layer, fell onto the submerged rock surfaces in the pool as an

array or unorganized clumps (terminology of Altig and McDiarmid 2007; Figs. 3D). A large part of the clutch of

about 1100 eggs, of a total of 3600 eggs was deposited in several bouts, and while still in amplexus, the pair moved

out of the crevice and deposited several small arrays of 1136 eggs on rocks and leaf litter along the streambed.

Other rock pools were also visited for depositing remaining eggs, and eggs from the final bout had traces of blood

(Fig. 3E). Females that entered amplexus further from the stream sometimes carried males for longer distances to

the oviposition sites (Fig. 3A). Most clutches in open pools were exposed to the air when the water receded.

Females appeared emaciated with loose folds of skin, after oviposition.

FIGURE 3. (A) A femaleNasikabatrachus sahyadrensis carrying a male to an oviposition site while in a generally pectoral

amplexus position, but with the male gripping her tightly near her vertebral column, (B) amplectic pair entering a pool inside a

rocky crevice, before oviposition, (C) a male realigning his vent over that of the female without changing forelimb position

appreciably; eggs are visible through the females abdominal wall and arrow = single extruded egg suggest beginning of

ovulation, (D) a freshly oviposited clutch in a pool at the bottom of a crevice in the rocky substrate, (E) final bout of eggs

deposited as disorganized clumps, exposed on rocks and dead leaves outside crevice; arrow = blood from the many small

hemorrhages caused by the rupture of follicle cells during ovulation.

Larval development. As with other large, yolky eggs, the embryos develop on top of the yolk instead of

within it (Fig. 4BC), and pigmentation does not appear on the dorsal surfaces until at least Stage 22. Gills appear

at about Stage 20 (Fig. 4E), and the snout, influenced by the development of the large oral disc, is truncate. By

Stage 23, the tadpole can use the oral disc for adherence to the substrate even as gills remain (Fig. 4G), and a fullyformed, pigmented suctorial tadpole occurs by Stage 25 (Fig. 4H) on Day 5, even though a large yolk reserve is

present. By the later phases of this stage (Fig. 4I), heavy rains help flush the young tadpoles out of their nursery

crevices (Fig. 4J), and they are subsequently found attached to rocks in flowing parts of the stream (Fig. 1C). By

Stage 27, the rectus abdominus development is complete and it covers the coiled gut. Now, the tadpole is capable of

amphibious ventures outside of the water flow into the spray zone. The hind limb buds remain concealed beneath

the triangular flap until Day 56 (Stage 38), and the large metatarsal tubercle is obvious. At Day 60 (Stage 39), the

tadpole has attained its maximum growth with noticeable hind limbs. By Day 72 (Stage 41), the left forelimb has

erupted, and by Day 90 (Stage 42), the vent flap starts to atrophy and tail resorption commences. The ventral body

surface is flat and transparent until about Stage 42 when white iridophores cover the viscera. At Day 98 (Stage 43),

metamorphic atrophy of the oral disc has started. The massive rectus abdominus (Fig. 5G:inset 4), with closed

myosepta and six myotomic bundles, covers most of the abdominal area, and various hyobranchial muscles visiblethrough the transparent belly are also quite large.


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FIGURE 4. (A) An egg with one jelly layer, embryos and tadpoles at the approximate stages of (B) 17, (C) 18, (D) 19, (E) 20,

(F) 22, (G) 23 (note that tadpole is adhered to the substrate with the oral disc even as gills remain), free-living tadpoles at stages

(H) 25 (note large yolk reserves that remain in early free-swimming stages) and (I) 26, and (J) a group of recent hatchlings

clustered inside the nursery pool before dispersing into stream. Bar represents 1 mm.

Metamorphic atrophy of the oral apparatus follows the typical sequence outlined by Thibaudeau and Altig

(1988). Labial tooth row P-3 starts to atrophy first at Stage 40, and at Stage 4243, a metamorph was seen walking

across the surface of a rock while using its oral apparatus in typical tadpole feeding movements. As in lentic

tadpoles, the jaw sheaths can open 180 (Fig.6: Stage 39). The entire tadpole ontogeny is summarized in Fig. 6.


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FIGURE 5. (A) Lateral view of the tadpole and (B) tadpole mouthparts ofNasikabatrachus sahyadrensis edited from

Annandale (1918; collected by F. H. Gravely from Parambikulam, September 1914), (C) a living tadpole at Stage 39 feeding on

a wet rock, (D) the oral apparatus of a living tadpole, and a (E) dorsal, (F) lateral, and (G) ventral view of the tadpole (Stage 38,

69.8 mm TL). Notations: 1 = groove on sides of head and snout, 2 = epidermal keratinization areas lateral to lower jaw sheath,

3 = musculus interhyoideus, 4 = rectus abdominus, 5 = flap subtending the vent tube, and 6 = triangular flap subtending the

limb buds (6 digitally darkened differentially for better visibility).


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FIGURE 6. Overview of the general developmental pattern of the oral apparatus and the tadpole ofNasikabatrachus

sahyadrensis during Stages 2646 and a graph showing the growth trajectories of (TL) total length and (BL) body length versus

days (note: open/closed jaws of oral apparatus, an artifact of preservation).

Tadpole morphology. The suctorial tadpole [TNHM (H) 12.6.22/72] in Stage 38 (Figs.56; Table 1) has a

labial tooth row formula of 2/3 or 2/3(1) composed of small, closely spaced labial teeth on a large, ventral oral disc

(12.3 mm diameter; about 95% of body width). The robust, compact jaw sheaths are finely serrated, and areas of

thin, epidermal keratinization (Fig. 5G: 3) occur lateral to the lower sheath and other areas adjacent to the jaw

sheaths. Irregular rows of submarginal papillae occur between the last posterior labial tooth row and the disc

margin and distal to the first anterior row. Marginal papillae are complete, and a slight emargination occurslaterally. The elongate, depressed snout is broadly rounded in dorsal and lateral views. A narrow groove extending


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along the dorsolateral margin of the head is constricted through the internarial region (Fig. 5E: 1). The spiracle is

sinistral. The medial vent tube is underlain by a fleshy flap (Fig. 5G: 5), and a larger, long, triangular flap subtends

the limb buds (Fig. 5G: 6). The tail, at about 61% of total length, has an acute tip and a dorsal fin only slightly taller

than the ventral fin. The dorsal tail fin originates at about one-half of the tail length and the lower tail fin originates

at the base of the tail muscle. Both fins reach maximum height posterior to the midlength of the tail. Measurements

(mm) of the representative tadpole were as follows: 69.8 total length from tip of snout to tip of tail, 27.1 body

length as the distance from the tip of the snout to the junction of the body and tail, 42.7 tail length from the body-

tail junction to the tip of the tail, 14.6 body width at the plane of the spiracle, 8.9 body height at the plane of the

eyes, 7.4 tail muscle height at the base of the tail, 5.6 tail muscle width at the base of the tail, 2.1 maximum upper

fin height, 1.7 maximum lower fin height, 8.2 maximum tail height including the fins, 4.0 eye-naris distance

between the centers of the nares to the anterior edge of the eyes, 9.8 naris-snout distance between the centers of the

narial apertures to tip of snout, 22.1 snout-spiracle distance from the tip of the snout and the terminal end of the

spiracle, 2.0 internarial distance between the centers of the narial apertures, 4.8 interorbital distance between the

medial borders of the eyes, 1.7 eye diameter, and 12.3 transverse oral disc width.

TABLE 1. Means of representative measurements (mm) of tadpoles ofNasikabatrachus sahyadrensis at seven stages: TL =

total length, BL = body length, TAL = tail length, BW = body width, NSD = naris-snout distance, and END = eye-naris

distance. The standard deviations were 0.08 or smaller in all cases. Stage (Sample Size).

Discussion

Nasikabatrachus sahyadrensis has been previously reported in the Western Ghats, from the southwestern slopes of

the Nilgiri Hill Range in the north, to Mundakayam in the western foothills of the Cardamom Hill Range in the

south (Biju and Bossuyt 2003; Dutta et al. 2004; A. K. S. Das 2006; Radhakrishnan et al. 2007). Most sites are in

the state of Kerala with some populations occurring in adjacent areas of Tamil Nadu. We report the species from

the following new sites: Edavanna of the Chaliyar river basin, Dhoni Hill of the Siruvani Hill Range and Kaikatti in

the Nelliyampathy Hills of the Bharathapuzha river basin, Pattathipara of the Keecheripuzha river basin,

Malakkapara in the Chalakudy river basin, Idamalakkudi, Mankulam and Thattekkad of the Periyar river basin,

Melukavu of the Muvattupuzha river basin, Vagamon of the Meenachil river basin, and streams of the Ambanad

Hills draining into the Kallada river basin (Fig. 7; see Appendix for GPS coordinates). These sites from Kerala

expand the known elevational range of the species, from 601100 m ASL and the latitudinal range of the speciesnorthward to the Camels Hump Hill Range (1118N) and southward to the northernmost portions of the

Agasthyamalai Hill Range (0900N).

The northern Muvattupuzha and the southern Meenachil rivers drain westward from the Melukavu Hills in

Kottayam and Idukki districts, Kerala, India. This area receives an average of 3680 mm of annual rainfall

(20062010), and a network of first- and second-order, swift flowing, seasonal streams fed by the monsoons drain

these hills. The streams flow for 79 months each year from the onset of premonsoon showers in AprilMay and an

average annual rainfall of 3937 mm (Krishnakumar et al. 2009). With the first showers, seepages from the riparian

vegetation and grasses along the dry streams charge the drainage that stimulates algal growth on the rocks. Along

with rejuvenation of the stream, pools form in the rocky crevices as a result of these early showers. The streams

first become torrential as the southwest monsoon advances in June and July and then reduce as the monsoons wane

at the beginning of August. The Melukavu Hills are dominated by Charnokite rocks, interspersed with surfacelayers of laterite. A deep, well-drained, gravelly loam of the Ustic Humitropept formation occurs on the steep

Stage 26 (2) 34 (2) 38 (3) 40 (3) 41 (2) 42 (3) 44 (2)

TL 19.7 43.8 72.4 75.8 69.8 44.8 33.2

BL 7.7 19.4 29.7 27.1 28.3 27.9 24.7

TAL 12.0 24.4 42.7 42.7 47.5 17.9 8.5

BW 3.3 8.1 15.8 13.0 14.0 14.7 12.0

NSD 3.1 6.2 11.0 9.8 9.4 10.7 8.7

END 0.9 1.9 4.0 4.0 3.2 3.1 2.7


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slopes, and well-drained clayey soils of the Ustic Palehumult formation occur on moderate slopes (Anon 1996).

The study area is heavily cultivated because it lies outside any protected area, but the higher areas still support

remnants of moist deciduous forests and grasslands (Fig. 1A).

FIGURE 7. Distribution map ofNasikabatrachus sahyadrensis; Current records (2011) and primary study site: 1. Edavanna, 2.

Dhoni Hill, 3. Pattathipara, 4. Kaikkati, 5. Malakkappara, 6. Idamalakkudi, 7. Thattekkad, 8. Mankulam, 9. Melukavu, 10.

Vagamon, 11. Ambanad.

The upper reaches of streams preferred by Nasikabatrachus for breeding, mostly have a bed of sheet rock,

which have several recesses and crevices. Because the upper reaches of the streams do not support much aquatic

life during the dry period, at least at the surface, probable competitors and predators are largely absent during the


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early periods of stream flow when the frogs breed. Eggs deposited in exposed pools and rocks were predated by

terrestrial insects and aquatic larvae of mayflies and caddisflies, which were observed in low densities soon after

the initial breeding phase. By the time most populations of other organisms become established, the tadpoles are

well developed, and settle into high velocity torrents on sheet rocks, where few competitors and predators affect

them. However, rheophilic fishes of the balitorid genera Bhavania and Travancoria and the sisorid Glyptothorax

that occur in the lower reaches of the same habitat with the tadpoles (e.g., Annandale & Hora 1922) may be

competitors.

In Southern India, many anuran species co-breeding following the southwest monsoons are subjected to severe

competition (intra- and interspecific). The dominant way to avoid such competition is to select exclusive

microhabitats vis--vis adaptation to specific breeding periods and appropriate breeding zones within a given

aquatic habitat (Saidapur, 2001). Having adapted to exploit the early showers of the pre-monsoon along with

exclusive zones in torrential streams, the large, rheophilic Nasikabatrachus tadpoles have effectively no

competition from any other anuran larvae within its range.

The biology ofNasikabatrachus is unique in a number of ways. Other species with adults of comparable

morphology, a fossorial adult, and explosive breeding with episodic rains all have lentic and mostly suspension

feeding tadpoles (e.g., the hemisotidHemisus, the microhylids Glyphoglossus and Uperodon and the rhinophrynid

Rhinophrynus), even though the Australian Myobatrachus gouldii is a direct developer. The proposed relatives

(Pyron & Wiens 2011) ofNasikabatrachus have either direct development (Sooglossidae) or suctorial tadpoles in

streams (Heleophrynidae). The climatic and hydrological features of the region, including its paleohistorical past

discussed by Dutta et al. (2004) surely have influenced the range and biology of this species.

Of the various modes of amplexus, variations of pectoral (i.e., hands of the male placed somewhere near the

pectoral girdle of the female) and inguinal (hands of the male placed somewhere near the insertion of the hind legs

of the female) are the most common. Changes in amplectic position during breeding are known (Duellman & Trueb

1994), and the absolute position of the vents of the two frogs is not used in such designations; the vents of the two

frogs do not need to be close together. Biju and Bossuyt (2003), Dutta et al. (2004) and Raj et al. (2011) reported

inguinal amplexus without descriptions or illustrations, and our observations show a type of pectoral amplexus. In

our observations, the small male firmly clasps the large female on each side of her vertebral column. Almost all

members of the Archaeobatrachia, Mesobatrachia and the basal families of Neobatrachia, such as Heleophrynidae,

Sooglossidae and Myobatrachidae exhibit inguinal amplexus. Nasikabatrachidae, though nested amongst these

basal families (Pyron & Wiens 2011), has deviated from the typical inguinal mode of amplexus. Also, our images

show that the eggs are deposited as arrays or clumps and not a string as reported by Raj et al. (2011); perhaps they

saw a line of single eggs and assumed they formed a string.

Some lotic hylid (Snchez 2010) and ranid tadpoles have the hind limb buds enclosed in a sac until at least

half-way through larval ontogeny, and the vent tube ofAscaphus is underlain by a vent flap. Both of these features

are assumed to reduce turbulence at the tail-body junction of lotic tadpoles. The large pair of flaps associated with

the vent and limb buds ofNasikabatrachus and the function of the groove on the snout will have to wait for further

examinations. We have seen numerous tadpoles gregariously feeding and moving upwards and downwards over

rock surfaces that have just a skim of water flowing over them at night. The particularly large rectus abdominus and

hyobranchial muscles likely reflect the common nocturnal feeding habits of these large tadpoles outside of the

water. A four-legged metamorph seen walking across a rock while feeding with typical extension-retraction cycles

of the oral disc, verifies that feeding occurs well into metamorphosis even though the suctorial function of the disc

is likely compromised by metamorphic atrophy at this stage. Lentic tadpoles have atrophied mouthparts by these

stages, but various suctorial tadpoles retain their mouthparts much later into ontogeny than lentic forms (Nodzenski

& Inger 1990). Other suctorial tadpoles feed on surfaces out of the water (e.g.,Bokermannohyla claresignata, Lutz

& Orton 1946,Ascaphus truei, RA, personal observation and Ghatophryne ornata, AZ, personal observation) but

not to the extent that tadpoles ofNasikabatrachus seem to do.

The mountains of southwestern India are a biological hotspot (Aggarwal 2004) and have recently been

designated as a UNESCO World Heritage Site, and the several protected areas in Kerala include about 35% of the

known range ofNasikabatrachus. Many other species of frogs with various reproductive habits inhabit the general

area, and some breed in the lower reaches of the streams. Water abstraction, forestry and agricultural practices

(Myers et al. 2000), unchecked tourism development and pollution threaten the fauna of the unprotected areas

(Daniels et al. 1995). We have found several roadkills of gravid femaleNasikabatrachus near oviposition sites, and


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the local people eat the gravid frogs in the belief that they possess medicinal properties. Irregularities in monsoon

rainfall in recent years also impact survival of early-stage tadpoles, as low rainfall in the early monsoon months can

affect stream flow, thus preventing the flushing out of tadpoles from nursery pools out into the main stream.

Reduction in optimal tadpole habitat, along with accidental and deliberate mortality of tadpoles and breeding adults

likely impose limitations to recruitment that impact the population. Understanding the biology and phenology of

Nasikabatrachus, and other species of amphibians that occur in the general region and use these habitats, is

paramount to ensuring the survival of these populations from the Western Ghats complex.

Acknowledgments

We are most grateful to Shri. V. Gopinathan IFS, Principal Chief Conservator of Forests & Chief Wildlife Warden,

Kerala, for kindly providing access and collection permits to the first two authors. We thank K. Sethumadhavan,

Gijimon Joseph and Winni Joseph for offering us logistic support and encouragement, Sunil, Rajeev, Sabu, P. K.

Umesh, N. Babu and Jobin Mathew for valuable assistance in field, Indraneil Das, Dharamveer Shetty, Tarun Nair,

Zhang Lu and Robert Alexander Pyron for generously sharing important literature, V. Srinivas for helping to

generate the map template and W. R. Heyer for assistance with the call analysis.

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APPENDIX

Sl. No. Site Hill Range River Basin Latitude Longitude

1 Edavanna Camel's Hump Hills Chaliyar 11.259469 N 76.12145 E

2 Dhoni Hill Siruvani Hills Bharathapuzha 10.872033 N 76.612164 E

3 Pattathipara Machad Hills Keecheripuzha 10.572378 N 76.309264 E

4 Kaikatti Nelliyampathy Hills Bharathapuzha 10.500428 N 76.704947 E

5 Malakkappara Anamalai Hills Chalakudi 10.288997 N 76.849336 E

6 Idamalakkudi High Ranges Periyar 10.226694 N 76.951739 E

7 Thattekkad High Ranges Periyar 10.105672 N 76.73795 E

8 Mankulam High Ranges Periyar 10.124578 N 76.912456 E

9 Melukavu Cardamom Hills Muvatupuzha 9.803764 N 76.767678 E

10 Wagamon Cardamom Hills Meenachil 9.692175 N 76.897003 E

11 Ambanad Ambanad Hills Kallada 9.038978 N 77.082231 E

a detailed account of the reproductive strategy and developmental stages of nasikabatrachus...

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