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Anuran acoustic communities in Sabah, Malaysia SALAMANDRA

43

3

129-138

Rheinbach, 20 August 2007

ISSN 0036-3375

Comparison of anuran acoustic communities of two habitat types in the Danum Valley Conservation Area, Sabah, Malaysia Doris Preininger, Markus Böckle & Walter Hödl Abstract. We compared advertisement calls of frog assemblages in two different habitats, (i) an open area along a dirt road with ponds and secondary vegetation; (ii) a fast flowing stream in primary forest. Eleven frog species were recorded and significant differences in the dominant call frequencies between the two observed frog communities were discovered. Stream-breeding species produce higher frequencies than species occurring in the roadside habitat. Noisy habitats have an influence on dominant frequency and demand acoustic adaptations to increase the signal-to-noise ratio. Selective logging represents a major threat to stream-breeding anurans in Sabah. Pollution of clear water threatens the stream-dependent herpetofauna. Keywords. Amphibia, Anura, conservation, vocalisation, Malaysia.

Introduction Selective logging has been the main cause of disturbance to tropical forests in Southeast Asia (Marsh & Greer 992, Willott et al. 2000). Concession-based timber extraction and plantation establishment result in highly fragmented forests (McMorrow & Talip 200, Curran et al. 2004) and increase river sediment yields (Douglas et al. 993). The extent to which biodiversity is altered in selectively logged forest is an important conservation issue. Fragmentation, degradation and conversion of rainforests affect the tropical herpetofauna (Alcala et al. 2004). About half the frog species in Southeast Asia are restricted to riparian habitats and develop in streams (Inger 969, Zimmerman & Simberloff 996). Most anuran stream-side communities in Borneo are known to breed in clear, turbulent water and are absent in streams with silt bottoms and lacking riffles and torrents (Inger & Voris 993). Several anuran community studies have focused on environmental conditions such as vegetation, elevation, rainfall and microhabitat (In-

ger 969, Duellman 978, Inger & Voris 993, Gillespie et al. 2004). Apart from behavioural and morphological adaptations to the environment, frog assemblages also show acoustic differences. A prime factor separating species within anuran assemblages is vocalization (Duellman & Trueb 986). Acoustic partitioning through temporal and spectral features minimizes competition and allows conspecific females to recognize individual signalling males (Hödl 977, GarciaRutledge & Narins 200, Gerhardt & Huber 2002). The dominant frequency of a frog’s call is partially constrained by its body size (Kime et al. 2000). Snout-vent length and dominant frequency are negatively correlated (Littlejohn 977, Duellman & Pyles 983, Ryan & Brenowitz 985). Sounds produced by waterfalls and fast-flowing streams contribute to the ambient noise level. Distinct, acoustic habitat properties (“melotops”) demand different adaptations on animal vocalizations. In this study, species composition was determined for two habitats within the Danum Valley Conservation Area (DVCA), a fast flowing stream in the primary forest

© 2007 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT) http://www.salamandra-journal.com

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and a roadside habitat with secondary vegetation, and spectral and temporal features of the acoustic signals were compared. Material and methods Study area From 0 January to3 March 2006, we studied frog communities in DVCA, Sabah, Malaysia. DVCA has an area of 43,800 ha of lowland tropical rainforest and is located in the upper catchment area of the Segama River. The Danum Valley Field Centre (DVFC) is located on the western edge of the DVCA (4°57´40” N 7°48´00” E; all but 9% of the area is below 760 m above sea level) from where a 2.8 km long trail leads south to the Tembaling waterfall. The rainy season in Sabah extends from December to March (Northeast Monsoon) with rainfall peak during February (monthly mean 788 mm). Annual precipitation is near 3000 mm with year-to-year fluctuation of about 00 mm. Mean annual temperature is 26.7°C with mean maximum 30.9°C and mean minimum 22.5°C. Daily temperature fluctuations are noticeably more pronounced than the year-to-year fluctuations. In the period from January to March the highest recorded temperature was 32.5°C and the lowest was 20.3°C; mean relative humidity at the DVFC was 97.0% at 8:00h and 89.7% at 4:00h. Daily rainfall and temperature data from January to March 2006 derived from the Danum Valley weather station, which is maintained by the staff of the Royal Society SE Asia Rain Forest Research Programme. Sampling methods We focused on two macrohabitat types. One is pristine, the other disturbed. The Tembaling River within the primary dipterocarp forest at about 900 m elevation is a fast flowing freshwater stream with rapids, waterfalls and no siltation. The selected disturbed habitat was along a dirt road in the DVFC with sec-

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ondary vegetation, ephemeral roadside pools filling seasonally with water and varying degrees of human disturbance. In both habitats 000 m long and y-shaped transects were established and marked with coloured tape. We performed visual and acoustic encounter surveys. The search areas also included adjacent riverbanks or vegetation up to a distance of 3 m to the water- or road-edge. Sampling was performed independent of prevailing weather conditions. Each transect was sampled at least 20 times by two observers during the day and during nocturnal censuses. Repeated controls of the same transect on consecutive days were avoided to ensure independence of samples. To determine all calling species, a 24-hour time period was sampled four times during one month along both transects. After locating a vocalizing male, call recordings were made from distances of  to 5 m using directional and surround microphones (Sennheiser Me 66, AKG D 90 E) and DAT- recorders (Sony DAT-Rec. TCDD8). Microhabitat temperature and humidity were measured with a digital thermohygrometer (Testo 60 GM) before each recording. Frogs were located at their resting sites, and if possible, captured and placed in plastic bags. Snout-vent length and snout-urostyle length were measured using a Wiha calliper (± 0.mm). To differentiate between individuals we photographed and compared dorsal colour patterns. All individuals were released after taking their measurements. Data analysis We digitized and analysed the recorded calls with the sound-analysis software Raven .2. at a sampling frequency of 44. Hz and with a mono 6 bit PCM Input and a 0 Hz update rate at normal speed. Power spectra, sonograms and oscillograms of  to 5 advertisement calls were analyzed for each frog and the average dominant frequency, minimum and maximum frequency, call duration, note duration, repetition rate and number

Anuran acoustic communities in Sabah, Malaysia

of notes, when applicable were calculated for each individual. Spectrogram views were produced with a Hann-filter with a sample size of 52 and a 3-dB filter bandwidth of 24 Hz. The correlation between body size (SVL) and dominant frequency was calculated with a Spearman non-parametric correlation (p ≤ 0.05). ANOVA (p ≤ 0.05) was used to test for statistical differences, in SVL (mm) and dominant frequency (Hz) of advertisement calls, among frog assemblages in two habitats. The influence of SVL and habitat on the dominant frequency of the frog species was calculated by an ANCOVA (p ≤ 0.05). Since the sample size for some anuran species tested was N = , the influence of SVL on dominant frequency was calculated twice: once corrected according to number of individuals and once without correction. All statistical tests were produced with SPSS for Mac .0.4.

(Fig. 5), Polypedates otilophus (Fig. 6), and Bufo asper (Fig. 7), Meristogenys orphnocnemis (Fig. 8), Microhyla sp. (Fig. 9), Staurois natator (Fig. 0), Staurois latopalmatus (Fig. ), respectively. No calls could be recorded for species without frequency data (Tab. ). A total of 23 calls were analyzed. The dominant call frequencies of the anuran species are not dependent on the SVL of the vocalizing individuals (N = ; c = -0.555; p ≤ 0.077; r2 = 0.30) (Fig. 3). Meristogenys orphnocnemis, a species found in the stream habitat produced the highest calling frequency (7205.0 Hz). Frog species from the torrent are above the

Results During the sampling period 20 frog species were found. Eleven frog species were recorded, six along the disturbed area and five within the pristine habitat: Fejervarya nicobariensis (Fig. ), Fejervarya limnocharis (Fig. 2), Rhacophorus dulitensis (Fig. 3), Polypedates leucomystax (Fig. 4), Polypedates macrotis

Fig. 2. Spectrogram (frequency [kHz]) and waveform (rel. amplitude [kUnit] = proportional to sound pressure of the recording) of the advertisement call of Fejervarya limnocharis. Temperature during recording 24.6 °C.

Fig. 1. Spectrogram (frequency [kHz]) and waveform (rel. amplitude [kUnit] = proportional to sound pressure of the recording) of the advertisement call and non-collected specimen of Fejervarya nicobariensis. Temperature during recording 25.4 °C.

Fig. 3. Spectrogram (frequency [kHz]) and waveform (rel. amplitude [kUnit] = proportional to sound pressure of the recording) of the advertisement call and non-collected specimen of Rhacophorus dulitensis. Temperature during recording 26.3 °C. 131

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Fig. 4. Spectrogram (frequency [kHz]) and waveform (rel. amplitude [kUnit] = proportional to sound pressure of the recording) of the advertisement call and non-collected specimen of Polypedates leucomystax. Temperature during recording 25.0 °C.

Fig. 6. Spectrogram (frequency [kHz]) and waveform (rel. amplitude [kUnit] = proportional to sound pressure of the recording) of the advertisement call and non-collected specimen of Polypedates otilophus. Temperature during recording 25.4 °C.

Fig. 5. Spectrogram (frequency [kHz]) and waveform (rel. amplitude [kUnit] = proportional to sound pressure of the recording) of the advertisement call and non-collected specimen of Polypedates macrotis. Temperature during recording 24.9 °C.

Fig. 7. Spectrogram (frequency [kHz]) and waveform (rel. amplitude [kUnit] = proportional to sound pressure of the recording) of the advertisement call and non-collected specimen of Bufo asper. Temperature during recording 24.6 °C.

calculated regression except Bufo asper and Microhyla sp. All frog species in the roadside habitat are below the calculated regression. The largest frog species was Polypedates otilophus with a dominant call frequency of ,033.6 Hz. No frog species with a dominant call frequency below ,000 Hz was recorded. Frequencies of advertisement calls of anuran species found in the stream transect are higher than call frequencies recorded of species occurring in the roadside habitat (Fig. 4) (N

= ; df = ; F = 7.35, p = 0.024). Dominant frequency is not dependent on the SVL (N = ; df = ; F = 3.822, p = 0.082) but the influence of the habitat is significant (N = ; df = ; F = 7.03, p = 0.029). If the number of analyzed individuals is included, the dependency of the dominant frequency, the influence of SVL (N = ; df = ; F = 0.59, p = 0.049) and the influence of the habitat (N = ; df = ; F = .435, p = 0.00) become more significant.

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Fig. 8. Spectrogram (frequency [kHz]) and waveform (rel. amplitude [kUnit] = proportional to sound pressure of the recording) of the advertisement call and non-collected specimen of Meristogenys orphnocnemis. Temperature during recording 24.8 °C.

Fig. 10. Spectrogram (frequency [kHz]) and waveform (rel. amplitude [kUnit] = proportional to sound pressure of the recording) of the advertisement call and non-collected specimen of Staurois natator. Temperature during recording 25.3 °C.

Fig. 9. Spectrogram (frequency [kHz]) and waveform (rel. amplitude [kUnit] = proportional to sound pressure of the recording) of the advertisement call and non-collected specimen of Microhyla sp. Temperature during recording 25.3 °C.

Fig. 11. Spectrogram (frequency [kHz]) and waveform (rel. amplitude [kUnit] = proportional to sound pressure of the recording) of the advertisement call and non-collected specimen of Staurois latopalmatus. Temperature during recording 25.2 °C.

Discussion

grams of streams show high sound pressure levels in low frequencies and lower sound pressure levels in frequencies above 3,000 Hz (Hödl & Amézquita 200, Feng et al. 2006, authors’ unpublished data). Environmental constraints should have an effect on the evolution of signals (Narins & Zelick 988). Selection favors signals that minimize the effects of background noise and interfering signals from other species (Endler 993). Riparian frog species are acoustically well adapted to their environment and show

The comparison of two local frog assemblages in different habitats shows that advertisement calls of frog species living in noisy environments constrain higher frequencies. Fast flowing streams and waterfalls produce low-frequency-dominated noise which may present a selective force for stream-breeding species (Hödl & Amézquita 200, Feng et al. 2006). The high-frequency calls exceed the constant ambient noise level. Spectro-

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a

b

c

d

e

f

g

h

Fig. 12. a) Fejervarya nicobariensis, b) Fejervarya limnocharis, c) Rhacophorus dulitensis, d) Polypedates leucomystax, e) Polypedates macrotis, f) Polypedates otilophus, g) Bufo asper, h) Meristogenys orphnocnemis, i) Microhyla sp., j) Staurois natator, k) Staurois latopalmatus. Photos: M. Böckle, W. Hödl, T. Reis.

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i

j

k

strong habitat affiliations. With the exception of Bufo asper the mean dominant frequency was above 3.9 kHz for frogs calling in the undisturbed habitat. A possible explanation for the call frequency in B. asper could be that it prefers stream banks, with small riffles that produced less background noise. Additionally, dominant frequency is determined by SVL. Larger frogs call with lower frequencies than smaller frogs (Littlejohn 977, Kime et al. 2000). The sampling size was probably too small to produce the dependency of SVL on dominant frequency. Only weighted data were able to show the influence. All species found in the disturbed roadside habitat

call with lower frequencies and less constant noise is emitted by the surrounding environment. This gives rise to the question why a high proportion of species breeds close to fast flowing streams (Inger 969). Zimmerman & Simberloff (996) showed that reproductive mode and developmental habitat are strongly associated with phylogeny. The same limited set of ecological and reproductive traits is shared by ranids, pelopatids and rhacophorids. Environmental conditions and interspecific interactions may have led to adaptations, but local selection on species can not be counted independent when closely related species occur in the same community. Phylogeny was not included in our analysis and a certain bias may result from the fact that two species of the genus Staurois are present at the stream habitat. Advertisement calls are important determinants of reproductive success and could have evolved in a common ancestor. However, we were able to record five species of the family of ranids, three at the stream (Staurois latopalmatus, S. natator and Meristogenys orphnocnemis) and two along the roadside (Fejervarya nicobariensis and F. limnocharis). All three ranid species recorded along the stream produce advertisement calls in which the dominant frequencies are above the calculated linear regression line (Fig. 3). Although morphological and phylogenetic limitations constrain frog vocalizations, selective pressures such as environmental factors have resulted in a diversity of advertisement calls (Duellman & Trueb 986). Acoustic partitioning and increasing the signal-to-noise ratio is a prerequisite for frogs living along torrents and streams. The influence of the habitat on advertisement calls should emphasize the importance of microhabitat composition on frog assemblages. Most recorded species are threatened by habitat loss (Tab. ). Deforestation and subsequent siltation of streams and rivers are the major threats to most streambreeding species in Sabah. Out of twelve species found along the stream, three are classified as “near threatened” according to the

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Fig. 13. Influence of SVL on dominant frequency of the species advertisement call (y = -55.49x + 5472.71). Frog species of the stream transect are marked with a square, those from the roadside habitat with a circle.

Fig. 14. Dominant call frequencies of the anuran species from two different habitat types. Species along the stream call with higher frequencies than frog species in the roadside habitat.

IUCN Red List status (Tab. ). Inger & Voris (993) found that a stream with a silt bottom completely lacked all the species known to 136

breed along clear and fast flowing streams. Selective logging changes the water chemistry considerably in nearby streams. Sediment yields of streams are 8 times higher within the next five months in selectively logged areas (Douglas et al. 992, 993). The increase in sedimentation levels has a clear effect on larval anurans and on reproduction of several stream-breeding species. Frog assemblages as those found at the Tembaling River show the importance of conservation areas like Danum Valley. On the other hand more microhabitats are created through reduced impact logging which attracts frog species that are normally not found in primary forests (e.g., Polypedates macrotis, Fejervarya nicobariensis and Rhacophorus pardalis) (Wong in press). We believe that disturbed areas such as those around the Danum Valley Field Center and adjacent roads contain suitable ponds and breeding habitats for disturbancetolerant breeders, but the large destruction and fragmentation of primary forest poses a

Anuran acoustic communities in Sabah, Malaysia Tab. 1. List of anuran species found including weight, snout-vent length (SVL), dominant call frequency (DF) and IUCN Red List status. Habitat: 1 = stream, 2 = road edge (numbers in parentheses are the absolute number of individuals measured); weight [g]; SVL [mm]; dominant frequency, DF [Hz] (number of individuals/number of analyzed calls); major threat: HL = habitat loss, P = pollution of streams and rivers, ID = infrastructure development, N = none; Red List status according to IUCN et al. (2006). species

habitat

SVL

DF

major threat

Bufo asper Meristogenys orphnocnemis Microhyla sp. Staurois natator Staurois latopalmatus Ansonia longidigita Ansonia spinulifer Leptobrachium abbotti Limnonectes leporinus Rana picturata Pedostibes rugosus Chaperina fusca Chaperina fusca Polypedates leucomystax Polypedates macrotis Polypedates otilophus Fejervarya limnocharis Fejervarya nicobariensis Rhacophorus dulitensis Rhacophorus pardalis Occidozyga laevis

1 1 1 1 1 1 1 1 1 1 1 1 2 2 2 2 2 2 2 2 2

76.2 (1) 30.2 (4) 14.9 (5) 33.9 (4) 47.7 (11) 3.2 (1) 56.5 (5) 106.8 (1) 39.8 (2) 18.8 (1) 30.0 (7) 57.0 (5) 81.1 (9) 33.4 (3) 41.2 (6) 46.6 (4) 43.5 (6) 31.0 (10)

1,031.2 (1/9) 7,205.0 (1/6) 3,969.3 (4/25) 4,746.0 (3/19) 5,149.4 (5/20) 2,056.7 (4/35) 1,388.9 (1/3) 1,033.6 (1/2) 1,274.0 (3/3) 3,169.7 (5/44) 1,868.6 (5/47) -

HL/P HL/P HL/ID HL/P HL/P HL/P HL HL HL HL/P HL HL N N HL HL/N HL HL N

major threat to the characteristic herpetofauna of Sabah. Acknowledgements We thank the Danum Valley Management Committee, the Economic Planing Unit, the Sabah Wildlife Department and the Universiti of Malaysia Sabah for giving us the opportunity to work in the Danum Valley Conservation Area. Special thanks go to the Royal Society (RS) and Glen Reynolds for their support and commitment to make this project possible. Julia Felling and Karoline Schmidt assisted during our fieldwork and Markus Gmeiner did the photo editing. We are very thankful for the statistical help of Adolfo Amézquita. Anna Wong acted as our local collaborator. Financial support was given by the University of Vienna (Brief Scientific Stays Abroad) and the DGHT (Wilhelm-Peters-Fonds). The Department of Evolutionary Biology (University of Vienna) provided the necessary field equipment. Last but not least we thank the DVCA and RS staff for keeping our spirits up.

IUCN Red List status least concern least concern least concern least concern near threatened near threatened least concern least concern least concern near threatened least concern least concern least concern least concern least concern least concern least concern near threatened least concern least concern

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Serve. (2006): Global Amphibian Assessment. – Washington. [www.globalamphibians.org, latest accessed 5 December 2006] Kime, N.M., W.R. Turner & M.J. Ryan (2000): The transmission of advertisement calls in Central American frogs. – Behav. Ecol., : 783. Littlejohn, M.J. (977): Long range acoustic communication in anurans. - Pp 263-294 in: Taylor, D. H & S.I. Guttman (eds.), The reproductive biology of amphibians. – Plenum Press, New York. Marsh, C.W. & A.G. Greer (992): Forest landuse in Sabah, Malaysia: An introduction to Danum Valley. – Phil. Trans. R. Soc. Lond. B, 335: 33-339. McMorrow, J. & M.A. Talip (200): Decline of forest area in Sabah, Malaysia: Relationship to state policies, land code and land capability. – Global Environ. Change, : 27-230. Narins, P.M. & R. Zelick (988): The effects of noise on auditory processing and behavior in amphibians. - pp. 5-536 in: Fritzsch, B., M. Ryan, W. Wilczynski, T. Hetherington & W. Walkowiak (eds.), The evolution of the amphibian auditory system. – John Wiley & Sons, New York. Ryan, M.J. & E.A. Brenowitz (985): The role of body size, phylogeny, and ambient noise in the evolution of bird song. – Amer. Nat., 26: 8700. Willott, S.J., D.C. Lim, S.G. Compton & S.L. Sutton (2000): Effects of selective logging on the butterflies of a Bornean rainforest. – Conserv. Biol., 4: 055-065. Wong, A. (in press): The impact of forestry practices on frog communities in Sabah, Malaysia. – PhD Dissertation. Universiti Putra Malaysia, Kota Kinabalu, Malaysia. Zimmerman, B. & D. Simberloff (996): An historical interpretation of habitat use by frogs in a Central Amazonian forest. – J. Biogeogr., 23: 27-46.

Manuscript received: 24 August 2006 Authors’ addresses: Doris Preininger, Markus Böckle, Walter Hödl, Department for Evolutionary Biology, University of Vienna, Althanstrasse 14, A-1090 Vienna, Austria, E-Mails: doris_ [email protected]; [email protected]; [email protected].

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