Herpetology Notes, volume 4: 011-016 (2011) (published online on 18 January 2011) Monitoring of breeding in Nasikabatrachus sahyadrensis (Anura: Nasikabatrachidae) in the southern Western Ghats, India Prudhvi Raj1, Deepak V.1 and Karthikeyan Vasudevan1* Abstract. The breeding of Nasikabatrachus sahyadrensis was monitored for three consecutive years (2007-2009) in an evergreen forest patch in the Anamalai tiger reserve, Western Ghats. The relationship between climatic variables and pattern of breeding was studied. Few anurans from this region have a reproductive mode analogous to the one observed in N. sahyadrensis. The phenology of calling activity and reproduction of N. sahyadrensis is probably correlated with the onset of south west monsoonal rainfall. Keywords. Explosive breeding, frogs, vocalization, rainfall, egg masses, subterranean. Introduction The taxonomy and phylogeny of anurans of the Western Ghats have gained interest among biologists in recent times, but aspects of their breeding biology, ecology and life history have long been neglected. Faced with 1 Wildlife Institute Of India, Post Box 18, Chandrabani, Dehradun, Uttarakhand -248001, India. e-mail: karthik@wii.gov.in * corresponding author multiple threats that drive them towards extinction, there is an urgent need to document aspects of the biology of the species that will rescue them in the event of extinction (Wilson, 2000). The majority of the Western Ghats anurans merely have a species description based on a few specimens while often nothing is known about their population, diet or breeding behaviour. The recent spate of discoveries in the Western Ghats has increased the already large gap in information that is crucial for rescuing species. We monitored the breeding of the critically endangered Figure 1. Geographical location and physical characteristics of the study area.
12 Prudhvi Raj et al. A Figure 2. A. Mean monthly rainfall in mm of the study area recorded from 2007 to 2009; B. Mean monthly temperature in Celsius of the study area for the years 2008 and 2009. B frog, Nasikabatrachus sahyadrensis Biju and Bossuyt, 2003, found in the Western Ghats at an elevation of 600-1000 m asl (Dutta et al., 2004; Radhakrishnan, Gopi and Palot, 2007). This species is known so far from a few localities in the Western Ghats. The type locality is from Kattappana, Idukki District in Kerela (Biju and Bossuyt, 2003), after which it was later reported from Sankaran Kudi in the Anamalai, Tamil Nadu, Kothamangalam in Ernakulam District and Erumely in Kottayam District, Kerala (Dutta et al., 2004), from Silent valley National park (Das, 2006) and Karuvarakunda, Malappuram District by Radhakrishnan, Gopi and Palot (2007) in Kerala. It is listed as Endangered as of the recent IUCN Redlist 2008. It is a fossorial species with a very brief terrestrial activity period during the breeding season (Dutta et al., 2004) and has a torrent dwelling, exotrophic tadpole (Annandale, 1918; Das, 2007; Dutta et al., 2004). Dutta et al. (2004) reported briefly on the subterranean calling of the species from a location situated about 20 km (straight line distance) from the location where the present study was carried out. Biju and Bossuyt (2003) and Dutta et al. (2004) reported inguinal amplexus in the species. Beyond anecdotal observations not much is known about the biology of the species. We report on the breeding activity of N. sahyadrensis from 2007 to 2009 in an evergreen forest patch in the Anamalai hills, southern Western Ghats. Methods The study was carried out in the Karian shola of Anamalai Tiger Reserve, located in the Southern Western Ghats of India. The study area of 110 ha (Fig. 1) has a southern tropical wet evergreen forest (Champion and Seth, 1968) with a dominant tree community composed of Dipterocarpus indicus, Dipterocarpus bourdilloni and Strombosia ceylanica (Pascal, Ramesh and De Franceschi, 2004). The elevation in the study area varied from 725-785 m a.s.l. (Fig. 1). Rainfall in the study area was measured to the nearest mm using a rain gauge located 800 m away from the centre of the study area. Data on temperature was collected using four stowaway tidbit temperature loggers (BoxCar Pro 4.3 Onset Computer Corporation, Bourne, MA) placed 150 mm above the ground under shade, that recorded temperature every hour. Observations on the breeding of N. sahyadrensis were recorded during day and night surveys along the sides of seasonal streams. Visits to the study area were made twice daily between 0800-1100 h (day survey) and 1700-1900 h (night survey) by one observer during the wet season from May to November each year for three consecutive years (2007, 2008 and 2009). Identification of the species calls were made by locating calling males and verifying the identity of the species. Calls were recorded using a microphone with a parabola attached to a portable stereo recorder (TASCAM HDP2) and unidirectional microphone (Senheiser ME-66). The date when the first call was made and the date when the first egg mass or egg laying was observed in the study area were recorded during the three years. The forest floor near the streams was also surveyed to record breeding of the species. Results The species was found to occur throughout the wet evergreen forest of the protected area. These forests are crisscrossed with many seasonal torrential streams during the monsoon season. Precipitation in the study area typically has two peaks in a year, one during the southwest monsoon (June-August) and the other during the northeast monsoon (September-November). The southwest monsoon brings more rainfall to this region than the northeast monsoon. Sporadic rainfall occurs between December and May every year (Fig. 2a). Annual precipitation for the years 2007, 2008, and 2009 was 2158, 1276 and 2000 mm, respectively.
Breeding behaviour of Nasikabatrachus sahyadrensis 13 Figure 3. Daily rainfall in mm at the study site between May to August for the years 2007 to 2009. Narrow pointer indicates the date on which calling initiated in Nasikabatrachus sahyadrensis for that year. Wide pointer indicates the date on which breeding initiated in N. sahyadrensis for that year. The mean temperature ranged from 19-25 C (Fig. 2b). First calling was recorded on the 10 th, 29 th, and 25 th of May, in 2007, 2008, and 2009, respectively (Fig. 3). This coincided with the first pre-monsoonal showers. Breeding calls persisted for about a month after which amplexus and egg laying was observed. During the total effort of 185 days (925 man hours) spent each year for three consecutive years (2007-2009), calling was heard for 53 days in 2007; 37 days in 2008 and 45 days in 2009. Males called from beneath the soil from the edge of the water to 50 m up slope (away from the water) along the seasonal and perennial streams. There were no calls heard from inside the evergreen forest, 100-150 m away from the stream. A few individuals were found calling from inside small burrows on the ground, but none were observed calling on the soil surface during the observation period. During surveys, we noticed that calling individuals stopped calling when an observer approached the caller by foot. A chorus in N. sahyadrensis involves a series of synchronized calling bouts by males, before the onset of the monsoon. Calling males were recorded in the evening and occasionally a day after heavy monsoonal showers. Usually two to five males were heard calling within a 5 m radius on the forest floor with the observer at the centre, and this was deemed as a chorus. It was difficult to limit the chorus within the confines of the area described, because it was spread over a large area of the forest floor where several males were involved in calling. One or two days before the first amplexus or egg laying, the calling became loud and frequent. Soon after the date of egg laying the calls diminished dramatically. The call of N. sahyadrensis recorded is provided for identification of the species (Audio file: Macaulay Library cat. no. 163897). In the study area we also detected the chorus of Pedostibes tuberculatus. The stream we monitored also had breeding populations of Fejervarya keralensis, Indirana brachytarsus, Indirana beddomi, Euphlyctis cyanophlyctis, Microhyla ornata, M. rubra, Hylarana temporalis, Nyctibatrachus sp and H. auranatiaca. The description of amplexus and egg laying was based on observations of two amplectant pairs in 2007 and 2009. Amplexus took place on the ground and it was inguinal. On 24 th June 2007 at 1815 h, we observed an amplectant pair laying eggs in strings inside a rock crevice in a small rivulet. It was cloudy, but no rainfall was recorded on this day. Egg strings were recorded on 27 th June 2008 at 1400 h, that day received 33 mm rainfall. On 1 st July 2009 at 1030 h, an amplectant pair was observed 10 m away from a torrential stream in a 150 x 150 mm depression on the ground. Eggs of the species were found in the stream on 3 rd July 2009 at 1500 h, and 37 mm of rainfall was recorded on that day. The eggs laid in these water bodies are further washed down to the main stream by the flooding waters. The number of eggs deposited per clutch was not counted during the present study. During amplexus and egg laying, the daily temperature range (difference between the maximum and the minimum temperature) was the least compared to other months of the year (Fig. 2b).
14 Prudhvi Raj et al. Figure 4. View of the stream where amplecting pairs of N.sahyadrensis were found depositing eggs in Anamalai Tiger Reserve. Discussion Breeding patterns of anurans are influenced by abiotic factors such as rainfall, temperature (Saenz et al., 2006), food availability, interspecific competition, predators (Wilbur, 1972; Wilbur 1980) and factors influencing the life history (Wilbur, 1987). In the case of explosive breeders that use ephemeral water bodies, calling in males is clearly associated with rainfall (Saenz et al., 2006). Our observations suggest that N. sahyadrensis is an explosive breeder, i.e. the frog reproduces within a very short favourable time period, and it recedes soon after. Further, among explosive breeders, females are attracted to breeding sites by male vocalizations (Duellman, 1985). Torrential streams (Fig. 4) are the breeding sites of N. sahyadrensis where males aggregate and call. The timing of the initiation of the underground calling in this species could be related to the humidity in the soil that would promote transmission of sound waves. Among anurans the White-lipped frog, Leptodactylus albilabris male calls have seismic signals or thumps, and they call from beneath the soil (Lewis and Narins, 1985; Narins, 1990). The response of calling individuals to an approaching observer suggests that the calling frogs probably sense the approach through vibrations in the ground. Studies have shown that subterranean anurans are sensitive to ground vibrations and receive impulses through the tympanum and the pectoral girdle (Lewis and Narins, 1985). A detailed investigation on the call broadcast, structure, transmission and response is required to understand the breeding vocalization in this species. The consistency in call initiation and amplexus, and egg laying during the years 2007, 2008 and 2009, prompted us to infer that the breeding activity in this species is closely related to monsoonal rainfall in the study area. Amplexus and egg laying was observed only on days with heavy rainfall (range: 30-80 mm) or the subsequent day during the south west monsoon. Rainfall controls circum-annual activity in anurans in the tropical regions (Duellman, 1978; Aichinger, 1987; Bertoluci, 1998). Because parental care or nest building was not observed in N. sahyadrensis, it is hypothesized that all its reproductive effort is used for vocalization and sperm production in the males and egg production in the females. Calling is energetically expensive and exposes the caller to predators (Pough et al., 1992). The adaptation of calling displayed by N. sahyadrensis from below the ground, coupled by the short above ground breeding period, probably minimizes mortality due to predators.
Breeding behaviour of Nasikabatrachus sahyadrensis 15 Figure 5. Adult female of N. sahyadrensis (photo: S. Harikrishnan). Our attempt in this study has been to characterize the breeding period of the species and provide a natural history account of the breeding activity of the species. The information presented here could serve as a baseline for investigators to make detailed observations and monitor the population of the species in the Western Ghats. The details could be readily used to formulate a monitoring program to measure occupancy of the species by detecting calls during their narrow breeding period. Acknowledgements. The Tamil Nadu and Kerala Forest Departments are thanked for supporting the study. We thank the National Bioresource Development Board of the Department of Biotechnology, Government of India (grant no. BT/PR82354/ NDB/51/141/2006) and the WII Grant-in-aid for funding. We thank Silamban for his sustained help during our field work. The anonymous reviewers of the manuscript are thanked for their inputs in improving it. Harikrishnan, Ganeshan and Rajamani are thanked for their assistance in the field. References Aichinger, M. (1987): Annual activity patterns of anurans in the seasonal Neotropical environment. Oecologia 71: 583-592. Annandale, N. (1918): Some undescribed tadpoles from the hills of Southern India. Rec. Ind. Mus. 15: 19-23. Biju, S.D., Bossuyt, F. (2003): New frog family from India reveals an ancient biogeographical link with the Seychelles. Nature 425: 711 714. Bertoluci, J. (1998): Annual patterns of breeding activity in Atlantic rainforest anurans. J. Herptol. 32: 607-611. Champion G. H., Seth,S. K. (1968): A revised survey of the forest types of India. Natraj publishers. Dehradun. Das, A. K. S. (2006): Record of Nasikabatrachus from the Northern Western Ghats. Zoos Print J. 21: 2410. Das, I. (2007): Some forgotten descriptions of Nasikabatrachus (Anura - Sooglossidae). Herp. Review 38: 291-292. Duellman, W. E. (1978): The biology of equatorial herpetofauna in Amazonian Ecuador. Univ. Kans. Mus. Nat. Hist. Misc. Pub. No. 65: 352 pp. Duellman, W.E., Trueb, L. (1985): In Biology of Amphibians. New York, McGraw- Hill. 670pp. Dutta, S.K., Vasudevan, K., Chaitra, M.S., Shankar. K., Aggarwal, R.K. (2004): Jurassic frogs and the evolution of amphibian endemism in the Western Ghats. Curr. Sci. 86: 211 216. [IUCN] International Union for Conservation of Nature. 2008. Nasikabatrachus sahyadrensis. In: IUCN Red List of threatened Species. <www.iucnredlist.org>. Lewis, E.R., Narins, P.M. (1985): Do frogs communicate with seismic signals? Science 227: 187-189. Narins, P.M. (1990): Seismic communication in anuran amphibians. BioScience 40: 268 274. Pascal, J. P., Ramesh, B.R, De Franceschi. D. (2004): Wet evergreen forest types of the Southern Western Ghats, India. Trop Ecol. 45: 281-292. Pough, F.H., Magnusoon, W.E., Ryan, M.J., Wells, K.D. (1992): Behavioural energetics. In Environmental physiology of the amphibians. p. 395-436. Feder M.E., and W.W. Burggren (Eds). University of Chicago press, Chicago. Radhakrishnan, C., Gopi, K.C., Palot, M.J. (2007): Extension of range of distribution of Nasikabatrachus sahyadrensis Biju & Bossuyt (Amphibia: Anura: Nasikabatrachidae) along Western Ghats, with some insights into its bionomics. Curr. Sci. 92: 213-216.
16 Saenz, D., Fitzgerald, L.A., Baum, K. A., Conner, R. N. (2006): Abiotic correlates of anuran calling phenology: The importance of rain, temperature, and season. Herp. Monogr. 20: 64-82. Wilbur, H. M. (1972): Competition, predation, and the structure of the Ambystoma-Rana sylvatica community. Ecology 53: 3-21. Wilbur, H. M. (1980): Complex life cycles. Annu. Rev. Ecol. Syst. 11: 67-93. Prudhvi Raj et al. Wilbur, H. M. (1987): Regulation of structure in complex systems: experimental temporary pond communities. Ecology 68: 1437-1452. Wilson, E.O. (2000): On the future of conservation biology. Cons. Biol. 14: 1-4. Accepted by Angelica Crottini