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Zoologisch-Botanische Datenbank/Zoological-Botanical Database

Digitale Literatur/Digital Literature

Zeitschrift/Journal: Herpetozoa

Jahr/Year: 2017

Band/Volume: 30_1_2

Autor(en)/Author(s): Batista Vinicius G., Oda Fabricio H., Amaral Diogo F. do, Costa Nathane de Q., Macel Natan M., Bastos Rogerio P.

Artikel/Article: Release and distress calls of abei (BALDISSERA, CARAMASCHI & HADDAD, 2004), and Rhinella icteria (SPIX, 1824) 100-105 All_Short_Notes_(Seiten 59-112):SHORT_NOTE.qxd 07.08.2017 19:51 Seite 42

100 SHORT NOTE HERPETOZOA 30 (1/2) Wien, 30. Juli 2017 SHORT NOTE

GRilliTScH , H. & F ARkAS , B. & G ál , J. & S ušić , G . NATAlE et al. 2011 ; TO lEDO et al. 2014). (2006): Herpetofaunal data from cres island, croatia.- loud and explosive notes characterize the Herpetozoa, Wien; 19 (1/2): 27-58. TRAPP , B. (2007): Amphibien und Reptilien des griechischen Festlandes; distress call, which distinguishes it from Münster (Natur und Tier - Verlag), pp. 279. VEiTH , G . other vocalizations ( DuEllMAN & T RuEB (1991): Die Reptilien Bosniens und der Herzegowina, 1994 ). Distress calls can be emitted with Teil ii.- Herpetozoa, Wien; 4 (1/2): 1-96. WiRTH , M. mouth open or closed ( TOlEDO & HADDAD (2009): königinnen der europäischen Schlangen: Vierstreifennatter ( Elaphe quatuorlineata ), Äskulap - 2009). calls are stereotyped and also help natter ( Zamenis longissimus ) und leopardnatter ( Za - to identify differences among menis situla ).- Draco, Münster; 10 (3): 61-74. ŽAGAR , (cARVAlHO et al. 2013). in the present note, A. & c AFuTA , V. & D RAšlER , k. & J AGAR , T. & k RO - the authors describe the release and distress FEl , M. & l uŽNik , M. & O STANEk , E. & P ETkOVSkA , V. & P lANiNc , G. & S OPOTNik , M. & V AMBERGER , M. calls of (BAlDiSSERA , c ARA- (2013): A review of eleven short-term reptile surveys in MAScHi &HADDAD , 2004 ) (of the Rhinella the Western Balkans.- Hyla herpetološki bilten, crucifer group) and (SPix , Zagreb; 2013 (1): 3-18. 1824 ) (of the Rhinella marina group). kEY WORDS: Reptilia: Squamata: Serpentes: Five male individuals of R. abei and colubridae: Elaphe quatuorlineata , Dugi Otok, three of R. icterica were spotted on Sep - croatia, Dalmatia, Balkan Peninsula, Adriatic island, new island record, melanism tember 9, 2014, and September 23, 2015. Specimens were found calling from the edge SuBMiTTED: August 10, 2016 of water bodies, near an Araucaria Forest AuTHOR: Robert MADl < r.madl.agar@gmx. remnant in the Atlantic Rain Forest domain de >, Roßdorfer Straße 28, D-60385 Frankfurt a. M., Germany. in the municipality of campo largo (25°30’ 26.90” S, 49°22’35.88” W, 905 m above sea level), Paraná state, southern . The were caught, positioned sitting on the Release and distress calls of ground, and squeezed in the lateral abdomi - Rhinella abei (BAlDiSSERA , nal region behind the forelimbs, simulating an amplexus. This procedure caused the cARAMAScHi & H ADDAD , 2004), and males to emit release calls. When the males Rhinella icterica (SPix , 1824) were squeezed the same way lifted off the ground, they emitted distress calls. Record - Vocalization is the main form of com - ings were obtained using Marantz ® PMD munication in anurans. These pro - 660 and Tascam ® Dr-40 digital recorders duce many different types of sounds which connected to a Sennheiser ® ME66/k6 di - have specific meanings in the social context rectional microphone. calls were recorded they are used in ( WEllS et al. 2007; TOlEDO at 44.1 kHz with 16-bit resolution. Bio - et al. 2014). The advertisement call is the acoustic traits were analyzed using Raven best known and thus, most frequently Pro 64 1.5 software from the cornell lab of described and used call type in taxonomic Ornithology ( BiOAcOuSTicS RESEARcH PRO- studies ( WEllS et al. 2007; GAMBAlE & GRAM 2014). Spectrograms were produced BASTOS 2014; BATiSTA et al. 2015). How- applying a window size of 256 samples, 75 ever, other calls, such as release calls, play % overlap, a hop size of 64 samples, DFT of important roles in anuran biology. Release 1024 samples, and Hamming window type. calls are emitted by males or females when Oscillogram and spectrogram figures were another , either conspecific or not, produced using TuneR 1.0 ( liGGES et al. attempts to mate with them ( WEllS et al. 2013) and Seewave 1.7.3 ( SuEuR et al. 2008) 2007; TOlEDO et al. 2014). like advertise - packages for R version 3.3.3 ( R D EVElOP - ment calls, release calls may vary between MENT cORE TEAM 2016). Voucher speci - species and help distinguish between close - mens are housed at the zoological collection ly related taxa ( BROWN & l iTTlEJOHN 1972; of universidade Federal de Goiás (ZuFG), GRENAT & M ARTiNO 2013 ). Distress call is Goiás state and the herpetological collection a defensive scream call emitted by males, of Museu Nacional, universidade Federal females, juveniles, newly metamorphosed do Rio de Janeiro (MNRJ), Rio de Janeiro as well as larvae of anurans when grasped state, Brazil ( R. abei : ZuFG 9884; ZuFG by potential predators ( WEllS 2007; 9885; R. icterica : MNRJ 89526; MNRJ All_Short_Notes_(Seiten 59-112):SHORT_NOTE.qxd 07.08.2017 19:51 Seite 43

SHORT NOTE HERPETOZOA 30 (1/2) Wien, 30. Juli 2017 SHORT NOTE 101

89527). The following acoustic parameters consists of a series of pulsed notes (Table 1; were analyzed: call duration, note duration, Fig. 2B). While emitting release calls the note number, internote interval, pulse num - males of R. icterica made small body vibra - ber, pulse duration, inter-pulse interval, tions. The distress call of R. icterica was dominant frequency of the call, and lower emitted by three males and consisted of a and upper frequency of the call (see BATiSTA single note with a harmonic structure (Table et al. 2015; FORTi et al. 2015). Parameters 1; Fig. 2c). were measured from 87 calls of R. abei and Rhinella abei showed a greater release 68 calls of R. icterica . Measurements are call repertoire than R. icterica . Such reper - presented as the mean (or mode) ± standard toire was composed of single and compound deviation (minimum – maximum). call de - calls. There are no release and distress call scription and terminology follow TOlEDO et descriptions for any other species in the al. (2014). Voucher individuals were meas - group. in the Rhinella ured (snout-vent length) using a digital marina group, the release call is only known caliper (to the nearest 0.1 mm) and the tem - for (S TEVAux , 2002) (GARDA perature was taken using a digital thermo - et al. 2010). The release call repertoire of R. hygrometer (to the nearest 0.01 °c). icterica is more extensive than R. jimi and Average snout-vent length (SVl) of R. the pulse number of the notes is higher. abei males recorded was 60.01 ± 2.64 mm However, the dominant frequency is similar (57–64.02 mm; N = 5) and mean air tem - and overlaps in both species. A male of R. perature was 16.7 ± 0.82 °c (15.0 – 17.6 °c, abei and six males of R. icterica were eval - N = 5). Three types of release call and one uated by TOlEDO et al. (2009). However, of distress call were identified. Release call they did not emit distress calls. in the pres - “A” was emitted by five males of R. abei ent work all males that were handled emit - and consists of a single pulsed note (Table ted release and/or distress calls. All individ - 1; Fig. 1A). Release call “B” was emitted uals tested responded to the handling with a by three males and consists of a series of series of vibrations, similar with the muscu - pulsed notes (Table 1; Fig. 1B). in the lar contractions produced by R. mirandari- release call “B” the first (0.366 ± 0.158 s, beiroi (G AllARDO , 1965) (ViEiRA et al. 2014). 0.077–0.531 s, N = 10) and last (0.355 ± Vibrations displayed by some anuran spe- 0.093 s, 0.077–0.208 s, N = 6) notes of the cies may be important to initiate dismount - call have longer duration in relation to the ing of males ( WEllS 2007). Such behavior is middle notes (0.058 ± 0.039 s, 0.031–0.187 com monly found among Rhinella species s, N = 15), which comprise the notes be - (BlAiR 1947; R ENGEl 1948; V iEiRA et al. tween the first and last notes of the call. 2014). The release and distress calls record - Release call “c” was emitted by one male ed by R. abei and R. icterica were emitted and has a harmonic structure. This call pre - with mouths closed as noted in other bufo- sented three well-defined harmonics (Table nids ( WEBER 1978). 1; Fig. 1c). When emitting release calls, all Some of the functions of release calls males of R. abei made small body vibra - are to avoid breeding energy expenditure tions. Distress calls were emitted by four with a misleading amplexus, to warn con - males of R. abei as a loud scream of short specifics of predator presence and/or to duration and harmonic structure (Table 1; frighten (or surprise) auditively oriented Fig. 1D). predators, or even to attract a secondary Rhinella icterica specimens recorded predator capable of interfering in the preda - had an average SVl of 96.73±24.81 mm tory process ( HöDl & G OllMANN 1986; (68.09–111.50 mm, N = 3) and mean air TOlEDO et al. 2014). However, a case of temperature was 18.01±0.70 °c (17.20– amplexus between a male of R. icterica and 18.41 °c, N = 3). The authors identified two a male of the invasive bullfrog Lithobates types of release call and one of distress call. catesbeianus (S HAW , 1802) , indicated that The release call type “A” was emitted by all release calls emitted by the amplected male males of R. icterica and consists of a single of R. icterica were not effective to prevent pulsed note (Table 1; Fig. 2A). The release the interspecific amplexus ( THEiS & c AlD- call type “B” was emitted by two males and ART 2015). Future researches using experi - All_Short_Notes_(Seiten 59-112):SHORT_NOTE.qxd 07.08.2017 19:51 Seite 44

102 SHORT NOTE HERPETOZOA 30 (1/2) Wien, 30. Juli 2017 SHORT NOTE

A B

c D

Fig. 1 : Release and distress calls of Rhinella abei (BAlDiSSERA , c ARAMAScHi & H ADDAD , 2004) from campo largo, Paraná state, southern Brazil. A, B, c ‒ release call types, D ‒ distress call. upper graphs: Audiospectrograms. lower graphs: Oscillograms. Air temperature at time of recording ‒ 17.6 °c. Water temperature ‒ 20.0 °c. Male SVl ‒ 64.2 mm. unvouchered specimen.

A B

c

Fig. 2 : Release and distress calls of Rhinella icterica (SPix , 1824) from campo largo, Paraná state, southern Brazil. A, B ‒ release call types, c ‒ distress call. upper graphs: Audiospectrograms. lower graphs: Oscillograms. Air temperature at time of recording ‒ 17.6 °c. Water temperature ‒ 17.2 °c. Male SVl ‒ 110.6 mm. unvouchered specimen. All_Short_Notes_(Seiten 59-112):SHORT_NOTE.qxd 07.08.2017 19:51 Seite 45

SHORT NOTE HERPETOZOA 30 (1/2) Wien, 30. Juli 2017 SHORT NOTE 103 a a P t h r n D e e d

Taxon Rhinella icterica c p Rhinella ab ei ‒ c a r

c p e l ) l A D A ; c B c B s u T . a

e

d l

a l

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l

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s 7

2 1 5 9 9 0 t

D

9 7 5 6 7 6 2

c

± A = i = m ± = = = ± ± ± ± ± ------a o = = 0

0 1 2

1 0 0 0 c 0 0 0 0 0 0

1

l ( n e 1 3 .

1 2 l o s ...... 0 . . . . 0 9 3 a

; 8 1 1 9 1 6 6 6 7 1 0 2 1 0 6 ) 5 7 ( u

3 n 1 2 4 0 i 1 8 8 D 5 3 5 9 3 7 s n 3

3 2 5 6 5 2 0 0 1 1 8 7 9 t ± ) o 8 i ) ) ) ) ) ) )

. c

t

S

p ‒ R D N N a

h ( ( i

r

N n 3 2 i ( a = = n – – – – – – – – – – – – – – – 5 2 t o - - m N e

7 e 8

r 3 1

r l

) ) e - l 7 0 m

n a t e o

o 0 ( ( r i 0 t 0 d 0 c s . e 2 .

t . e . 2

o 0 e 0 3

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0

s .

. .

a r 7 2 1 1 r 3 . ) p e 3 e l 1 6 6 ; a l l 3

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± ± ± ± – – – ± = = ------

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1 1 0 0 0 0 0 0

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s 0 8 4 3 3 . . . . . s . f y . . . . . a 5 2 0 0 0 0 0 0 ) 0 0 0 0 0

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6 5 1 ± 1 1 1 1 7

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1 3 1 1 4 2 2 0 l 4 0 0 u 9 n 9 8 1 7 H l 2 7 4 4 1 7 8 7 5 5 2 7 0 3 ) 3 3 e s 9 u 9 6 2 . 4 2 3 3 3 5

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a f ; All_Short_Notes_(Seiten 59-112):SHORT_NOTE.qxd 07.08.2017 19:51 Seite 46

104 SHORT NOTE HERPETOZOA 30 (1/2) Wien, 30. Juli 2017 SHORT NOTE

ments could be conducted in order to better kREY , S. & M ERSMANN , O. & S cHNAckENBERG , S. understand the role of release and distress (2013): Tuner: Analysis of music. WWW resource, information and software available at < http://r-forge.r- calls. The taxonomic status of some bufo - project.org/projects/tuner/ >. [last accessed on January nid species is problematic due their similar 10, 2015]. NATAlE , G. S. & A lcAlDE , l. & H ERRERA , external morphology and on account of R. & c AJADE , R. & S cHAEFER , E. F. & M ARANGONi , F. hybridization zones between sympatric & T RuDEAu , V. l. (2011): underwater acoustic com - munication in the macrophagic carnivorous larvae of species such as e.g., (S Pix , Ceratophrys ornata (Anura: ceratophryidae).- Acta 1824), and R. abei (THOMé et al. 2012). Zoologica : Royal Swedish Academy of Sciences etc.; Basic natural history information is funda - Oxford; 92: 46-53. R D EVElOPMENT cORE TEAM mental to evaluate the process shaping the (2016): R: A language and environment for statistical computing. R Foundation for Statistical computing, ecology of the species and to differentiate Vienna, Austria. iSBN 3-900051-07-0. WWW re - the species-specific characters of important source, information and software available at < http:// taxonomic value. www.R-project.org/ >. RENGEl , D. (1948): Sobre la vibración preventiva (“warning vibration“) en los AckNOWlEDGMENTS: The authors thank sapos machos del norte argentino.- Acta Zoológica the Postgraduate Program on Ecology of continental lilloana, Tucumán; 6: 279-282. SuEuR , J. & A uBiN , T. Aquatic Environments (PROEx/ PEA) for the logisti - & S iMO NiS , c. (2008): Seewave: a free modular tool for cal support. Thanks to Priscila c. SilVEiRA for critical sound analysis and synthesis.- Bioacoustics, Abingdon; reading and valuable comments on the manuscript. V. 18: 213-226. THEiS , T. F. & c AlDART , V. M. (2015): G. B ATiSTA and F. H. O DA would like to thank The Multiple interspecific amplexus between a male of the coordination for the improvement of Higher Education invasive Bullfrog Lithobates catesbeianus (Ranidae) Personnel (cAPES) by fellowships. and two males of the cururu Rhinella icterica (Bufonidae).- Herpetology Notes, Braunschweig; 8: REFERENcES: BATiSTA , V. G. & G AMBAlE , P. 448-451. THOMé , M. T. c. & Z AMuDiO , k. R. & G. & l OuRENçO -D E-M ORAES , R. & c AMPOS R. M. & AlExANDRiNO , J. (2012): Delimiting genetic units in BASTOS , R.P. (2015): Vocalizations of two species of Neotropical under incomplete lineage sorting and the Hypsiboas pulchellus group (Anura: Hylidae) with hybridization.- BMc Evolutionary Biology, london comments on this species group.- North-Western etc.; 12: 242. TOlEDO l. F. & c. F. B. H ADDAD (2009): Journal of Zoology, Oradea; 11: 253-261. BiOAcOuS - Defensive vocalizations of Neotropical anurans.- South TicS RESEARcH PROGRAM (2014): Raven Pro: interac- American Journal of Herpetology, São Paulo; 4: 25-42. tive sound analysis software. Version 1.5. The cornell TOlEDO , l. F. & M ARTiNS , i. A. & B RuScHi , D. P. & lab of ornithology, ithaca, New York. WWW resource, PASSOS , M. A. & A lExANDRE , c. & H ADDAD , c.F.B. information and software available at < http://www. (2014): The anuran calling repertoire in the light of birds.cornell.edu/raven >. BlAiR , A. P. (1947): The social context.- Acta Ethologica, Berlin, Heidelberg; male warning vibration in Bufo .- American Museum 18: 87-99. ViEiRA , R. R. S. & B ASTOS , R. P. & G AM- Novitates, New York; 1344: 1-7. BROWN , l. E. & BAlE , P. G. (2014): The release call of Rhinella miran - liTTlE JOHN , M. J. (1972): Male release call in the Bufo daribeiroi (GAllARDO , 1965) (Anura: Bufonidae).- americanus group; pp. 310-323. in: BlAiR , W. F. (Ed.): Herpetology Notes, Braunschweig; 7: 543-545. WE - Evolution in the genus Bufo . Austin (university of BER , E. (1978): Distress calls of Bufo calamita and B. Texas Press). cARVAlHO , T. R. & G iARETTA , A. A. viridis (Amphibia: Anura).- copeia, Washington; 1978: (2013): Taxonomic circumscription of Adenomera 354-356. WEllS , k. D. (1977): The social behavior of martinezi (BOkERMANN , 1956) (Anura: leptodacty- anuran .- Behavior, Amsterdam; 25: lidae: leptodactylinae) with the recognition of a new 666-693. cryptic taxon through a bioacoustic approach.- Zootaxa, Auckland; 3701: 207-237. DuEllMAN , W. E. kEY WORDS: Amphibia: Anura: Bufonidae: & T RuEB , l. (1994): Biology of amphibians. Balti- Rhinella abei , Rhinella icterica , Rhinella crucifer more and london (Johns Hopkins university Press), group, Rhinella marina group; acoustic behavior, pp. 670. FORTi , l. 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Av. colombo, 5790, cEP São Paulo; 5: 151-156. GRENAT , P. R. & M ARTiNO , A. 87020-900, Maringá, PR, Brazil. l. (2013): The release call as a diagnostic character 2) centro universitário cesumar (unicesumar), between cryptic related species Odontophrynus cor - Programa de Pós-Graduação em Promoção da Saúde. dobae and O. americanus (Anura: cycloramphidae).- Avenida Guedner 1610, Jardim Aclimação, cEP Zootaxa, Auckland; 3635: 583-586. HöDl , W. & G Oll - 87050-390, Maringá, PR, Brazil. MANN , G. (1986): Distress calls in Neotropical frogs.- 3) Programa de Pós-Graduação em conservação Amphibia-Reptilia, leiden; 7: 11-21. liGGES , u. & de Recursos Naturais do cerrado. Rodovia Geraldo All_Short_Notes_(Seiten 59-112):SHORT_NOTE.qxd 07.08.2017 19:51 Seite 47

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Silva Nascimento, km 2,5—Zona Rural, cEP 75.790- Tahan Pahang, Gunong Benom Pahang 000, urutaí, GO, Brazil. (BERRY 1975), ulu Muda Forest kedah 4) universidade Federal de Goiás (uFG), in- stituto de ciências Biológicas, Departamento de (JuliANA et al. 2002), Bubu Forest Perak Ecologia, laboratório de Herpetologia e comporta- (iBRAHiM et al. 2011) and Bukit Fraser mento Animal, campus Samambaia, 74001-970, cx. Pahang ( NORHAYATi et al. 2011). Postal 131, Goiânia, GO, Brazil. Building its foam nest in small forest rain pools and puddles, including the beds of intermittent streams ( SukuMARAN et al. Breeding activity of Rhacophorus 2004) is almost everything that was known MiTH about the reproductive behavior of R. pro - prominanus S , 1924 , from minanus . in the present note, the author Peninsular Malaysia reports the first data on oviposition sites, amplexus behavior, foam nest construction, Among the genera and species of the egg clutches and egg diameter of R. promi - tree frog family Rhacophoridae, various de- nanus from Peninsular Malaysia (Figs. 2-4). velopmental and reproductive modes are On 15 November, 2014, between found, including life history traits such as 19:00-19:30 h amplectant individuals of R. larval or direct development and foam nest prominanus were observed at Sungai Sedim production ( DuEllMAN & T RuEB 1986). The Receational Forest, kedah, Malaysia (5° latter is known in the genera Polypedates , 25’N, 100°46’E; elevation about 200 m Rhacophorus , Chiromantis and Chirixa lus a.s.l.). Two males grasping a single gravid (GROSJEAN et al. 2008). Foam nests are usu - female were perched on leaves approxi - ally deposited in or on vegetation above the mately 2.5-3 m above a shallow rock pool, water ( iNGER 1966; B ERRY 1975; i BRA HiM et at the edge of the main river. The size of the al. 2008) to protect the eggs from desicca - shady and clear water rock pool located on tion ( DuEllMAN & T RuEB 1986). The foam a large granite boulder was approximately originates from amplectant pairs who whisk one meter length, 0.5 m width and 3-18 cm their skin secretions during the amplexus depth. it was filled with dead leaves and (GRiSMER 2011). Numerous rhacophorid twigs on top of a sandy-pebbly bottom. species from Malaysia including Polype dates Both males clung to the female in axil - leucomystax (G RAVENHORST , 1829) (BERRY lary amplexus, one from the dorsal side in 1964; S HERiDAN 2008), P. macrotis (B OulEN - almost normal position, the other from lat - GER , 1891) and Rhacophorus ni gropalmatus eral, the first male being posterior to the sec - BOulENGER , 1895 (iNGER & S TuEBiNG 1989) ond. The female individual had flattened, deposit their eggs in foam nests. in P. leu - pressed her body on the leaves, and gripped comystax , multiple males were seen in the fingers on the outer edge of the leaves, amplexus with a single gravid female ( FENG to support her own weight and that of the & N ARiN 1991; G RiS MER 2011). males. Rhacophorus prominanus SMiTH , At about 19:45 h, all three frogs start - 1924, is a medium-sized tree frog of 65-68 ed wiping the posterior area of their backs mm snout-vent-length (Fig.1). For a concise with the hind limbs to produce a secretion, morphological diagnosis see BERRY (1975) . which is used to construct a foam nest. This species is native to indonesia, Malay - Around 22:30 h, the foam nest was com - sia and Thailand where it is recorded be- pleted and the female had deposited eggs tween 250 and 1,100 m a.s.l. ( Suku MARAN inside it. later the two male frogs released et al. (2004). in Peninsular Malay sia, it can the female and leaped to other leaves. The be encountered perched on leaves and exhausted female, rested on top of the foam branches of vegetation in primary rain forest nest for nearly 15 minutes before she leaped and clearing areas near primary forest to another branch. After this, the author took (BERRY 1975). The existence of R. promi - the frogs and the foam nest to the laboratory nanus has been documented in several for measurements and further inspection. forested areas including Jor, Batang Padang Snout-vent-length, head width and Perak, which is the type locality of this body mass of individual 1 (male), individual species, Templer Park Selangor, kuala 2 (male) and individual 3 (female) were 57,