Observation of the Eggs of Parachute Gecko, Genus Ptychozoon (Squamata: Gekkonidae), on an Epiphytic Fern Growing in the Forest Canopy

Herpetology Notes, volume 12: 1077-1081 (2019) (published online on 30 October 2019)

Observation of the eggs of parachute gecko, genus Ptychozoon (Squamata: Gekkonidae), on an epiphytic fern growing in the forest canopy

Takaki Kurita1,*, Akira Nakanishi2,3, Natsuki Komada2, Satoshi Shimano4, Rijal Satria5, Usun Shimizu–kaya6,7, Mizuki Shinoda8, Asano Iku8, Takao Itioka8, Mohamad Yazid Hossman9, and Kanto Nishikawa8

Among various environments occurring in tropical birds, mammals, and even anurans (Kays and Allison, rainforests, the tree canopy, which is the uppermost 2001; Nadkarni et al., 2011), although a significant layer of forest, sustains the large portion of biodiversity portion of squamates are arboreal species (Kays and (Basset, 2001; Kays and Allison, 2001; Floren et al., Allison, 2001; Das, 2012). Recently, various methods 2014). Methodological developments for accessing for surveying herpetofauna in arboreal habitat were tree crowns and collecting plants and animals on the proposed and reviewed (Das, 2012), and some exciting treacherous footing have partly solved the difficulties in works have attempted to evaluate the communities by surveying forest canopies (Lowman, 2009). However, qualitative and quantitative ways (e.g., McCracken and recent studies on reptiles in these habitats have been Fostner, 2008, 2014; Scheffers et al., 2014a, b; Donald et relatively limited when compared with arthropods, al., 2017). Nonetheless, the accumulation of individual observations provides additional information, revealing how arboreal reptiles and amphibians are living in the upper layers of the tropical rainforest. Here we report an observation of egg oviposition sites for a rainforest 1 Chiba Biodiversity Center. Aoba-cho 955-2, Chuo-ku, Chiba canopy gecko. 260-8682, Japan. The second to ninth authors conducted surveys on 2 Graduate School of Agriculture, Kyoto University. epiphytic ferns in the Lambir Hills National Park, Kitashirakawa Oiwake-cho, Sakyo-ku, Kyoto 606-8502, Sarawak, Malaysian Borneo (4.1983°N, 114.0428°E, Japan. 100–200 m above sea level; Inoue et al., 1995) in 3 Current address: Subtropical Field Science Center, Faculty of August and September 2016. Annual mean temperature Agriculture, University of the Ryukyus. 685 Yona, Kunigami, Okinawa 905-1427, Japan. in this area is ca. 27°C with little seasonal fluctuation 4 Science Research Center, Hosei University. Fujimi 2-17-1, (Kumagai et al., 2009). Monthly precipitation is rarely Chiyoda-ku, Tokyo 102-8160, Japan. less than 100 mm all year round, and relatively high from 5 Graduate School of Science and Engineering, Tokyo October to December and low in February and March Metropolitan University. Minami-Osawa 1-1, Hachioji, (Kato et al., 1995). The national park is mostly covered Tokyo 192-0397, Japan. with multi-layered, primary lowland mixed-dipterocarp 6 Research Core for Interdisciplinary Sciences, Okayama forest (Ashton and Hall, 1992), whose canopy reaches University. Tsushimanaka 3-1-1, Kita-ku, Okayama 700- 8530, Japan. 35–40 m in height, with emergent trees attaining over 7 Current address: Faculty of Life and Environmental Science, 70 m (Kato et al., 1995). Shimane University. Nishikawatsu 1060, Matsue, Shimane On 4 September, AN and NK (the second and third 690-8504, Japan. authors, respectively) collected an epiphytic bird’s nest 8 Graduate School of Human and Environmental Studies, Kyoto fern, Aspelnium sp., from the trunk of a host tree (Fig. University. Yoshida Nihonmatsu-cho, Sakyo-ku, Kyoto 606- 1-A) by tree climbing using the single- and doubled- 8501, Japan. rope techniques, and found a pair of unidentified eggs 9 Research Development and Innovation Division, Forest Department Sarawak. 93250 Kuching, Sarawak, Malaysia. attached to the fern. The fern was rooted on the base of a * Corresponding author. E-mail: main branch at 32.3 m above ground. The host tree was [email protected] Shorea confusa (Dipterocarpaceae), whose diameter at 1078 Takaki Kurita et al. breast height (130 cm above ground) was 129.8 cm. The to the frond basally (Fig. 1-C). The diameter of base, length of the longest frond (leaf-like portion of fern) of the widest part of the eggs, were 16.4–18.5 mm and the the bird’s nest fern was 137 cm, 40 cm in root length, 60 maximum height of eggs (including thin frond height) cm in diameter at base of root, and the fern had 19 live were 10.5 and 10.6 mm. matured fronds. The eggs were attached to the surface The eggs were kept in a laboratory of the park, and on of a dead frond of the fern (Fig. 1-B, C). The side of the 18 October 2016, two neonates of geckos hatched from frond (adaxial or abaxial) and direction of the surface the eggs, whose snout–vent length were 34.9 and 36.0 (outer or inner) that the eggs were attached were not mm (Fig. 1-D). The individuals were euthanatized by recorded because the eggs were found after the frond overdose of anaesthetic (6.5% w/v pentobarbital sodium; was cut from the fern body. Nacalai Tesque) via intra-abdominal injection, fixed in The eggs were hemispherical in shape with round base, formalin, and deposited in the Research, Development widest at the base, immaculate white in colour, having and Innovation Division, Forest Department Sarawak as well-calcified shell, and cemented together laterally and SRC00504 and 00505. The neonates had dermal flaps

Figure 1. In situ condition of an Asplenium fern that the eggs of Ptychozoon were attached to (A). Dead frond used as egg-laying substrate hanged under body of live plant (B). Hemispherical-shaped Ptychozoon eggs were attached the dead frond (C). Hatched neonates from the eggs (D). Observation of the eggs of parachute gecko on an epiphytic fern 1079 on head, flanks, and limbs laterally, saw-like tail lappets, consider this merely due to the difficulty in accessing to and inter-digital webbing, appearing to be geckos of canopy layer. genus Ptychozoon. Boulenger (1903) mentioned that pairs of calcareous Characteristics of the neonates were as follows: 12–13 eggs were laid adhering to leaves and trunks of trees, supralabials; 9–12 infralabials; two postmentals; head sometimes near the ground. Barbour (1912) noted that uniformly covered with granular scales; trunk dorsum the eggs were usually found on the wood under the bark covered with uniform granular scales in one individual, of the trees. Tweedie (1954) found hemispherical eggs of but granular scales obviously interspersed with enlarged P. kuhli attached on an epiphyte’s leaf growing on more tubercles in another; 26–27 contiguous enlarged femoral than 3 m above ground. Tiwari (1961) found that two and precloacal scales (putative pore-bearing scales) eggs, which were dirty white in colour, hemispherical arranged in a chevron shape; 14–16 undivided, weakly- in shape, and 15 mm and 11 mm in diameter and height wavy subdigital lamellae on fourth toe, of which the respectively, vertically adhered to bark of trees at 45–60 eighth to 10th distal lamellae broadest; tail lappets cm above ground. The eggs of P. rhacophorus, have elongate right angle on tail; tail terminates in broad been found attached to a dried leaf, were found from the flap; ground colour of head, trunk, and limbs grey, with forest floor (Min and Das, 2012). four or five wavy, transverse, black bands on dorsum As far as we know, our observation is the first formal between limb insertions; six transverse black bands, report on the use of the forest canopy as an egg-laying with the last one more than twice as wide as those on site by P. kuhli. Compared with the forest floor, the anterior, encircling tail. Three species of Ptychozoon are environmental conditions in the canopy layer is less confirmed to be distributed in Borneo (Min and Das, homogenous, i.e., hot, dry, and frequent extreme events 2012), i.e., P. horsfieldii (Gray, 1827), P. rhacophorus like squall (Freiberg, 1997). In the tropical rainforest (Boulenger, 1899), and P. kuhli (Stejneger, 1902). canopy, epiphytes are a frequently used microhabitat The specimens reported here have 26–27 contiguous by herpetofauna (McCracken and Forstner, 2014), putative pore-bearing femoral and precloacal scales as especially by frogs (Scheffers et al., 2014b). Although P. kuhli. On the other hand, P. horsfieldii has separated observations on the use of epiphytes by geckos are 8–11 enlarged pore-baring femoral scales and 10–11 still very limited (e.g., McCracken and Forstner, 2008; precloacal pores, and P. rhacophorus has no enlarged Henwood et al., 2014; Donald et al., 2017; also in Brown femoral scales and 12–18 precloacal pores (Table 4 in and Diesmos, 2000), the occurrence of epiphytes would Grismer et al., 2018). The specimens have fused tail lobes likely benefit survival of eggs of geckos in canopy. forming tail flap but P. horsfieldii and P. rhacophorus Epiphytes are considered to have various ecological have no tail flaps or no fused tail lobes. The specimens functions and are known to increase species diversity also differed from P. horsfieldii in having dorsal and biomass of organisms, such as structural complexity, tubercles (obvious in one but not in another specimen nutrients source, and water retention (Stuntz et al., 1999; vs. no dorsal tubercles), and from P. rhacophorus in Tobón et al., 2010; Díaz et al., 2012). As an egg-laying site, epiphytes could provide buffered microclimate that having 4–5 wavy transverse bands on dorsum (vs. no is lower in temperature, higher in humidity, and less clear bands) and more developed dermal folds on the fluctuated than ambient air where living organisms are lateral sides of trunk (vs. less developed). Although ten�� exposed to severe physical stress (Angelini and Silliman, species of Ptychozoon have been described, this species 2014). Asplenium bird’s nest ferns effectively reduce also differed from other seven species by the above the occurrence of fatally overheating of canopy animals characters (Wang et al. 2016; Grismer et al. 2018). We�� by up to 32-fold (Scheffers et al., 2014a). As Donald thus identified these specimens as P. kuhli. et al. (2017) mentioned, it would provide a refuge in Parachute geckos or flying geckos, genus Ptychozoon, the canopy layer. Stability and mildness of environment are adapted for arboreal habitats (Tweedie, 1950, 1954; are considered to be a primary aspect of epiphytes in Young et al., 2002), and are known to occur least 35 selecting egg-laying site for Ptychozoon geckos. m above ground (Das, 2010). Thus, our observation of eggs of P. kuhli at 32.3 m above ground is not Acknowledgements. The State Government of Sarawak surprising. On the other hand, eggs of Ptychozoon kindly permitted us to conduct the project (Permit Nos. have been usually reported from the lowest strata of NCCD.907.4.4(Jld.12)-149, NCCD.907.4.4(Jld.12)-186, and rainforest in the previous studies (Boulenger, 1903; NCCD.907.4.4(Jld.14)-61, and Park Permit Nos. 358/2015, Tweedie, 1954; Tiwari, 1961; Min and Das, 2012). We 436/2015, and 66/2017), and the Research, Development and 1080 Takaki Kurita et al.

Innovation Division, Sarawak Forest Department provided all variation in Ptychozoon lionotum (Squamata: Gekkonidae) and facilities for conducting research. We are grateful to Paulus Meleng a new species from an isolated volcano in Myanmar. Zootaxa for his support and guidance and to Engkamat Anak Lading for 4514(2): 202–214, granting permission to conduct research and export specimens. Henwood, O.R., Kirby, C.L., Cutting, B.T. (2014): An exploratory We deeply thank Januarie Anak Kulis for allowing us to conduct faunal survey of New Zealand temperate rainforest epiphytes. survey in Lambir Hills National Park. We are grateful to Tsutomu New Zealand Natural Science 39: 10–24. Hikida for pre peer-reviewing our manuscript and verifying Inoue, T., Yumoto, T., Hamid, A.A., Lee, H.S., Ogino, K. (1995): species identification. This work was supported by Grant-in-Aid Construction of a canopy observation system in a tropical forest from the Monbukagakusho through the Japan Society for the of Sarawak. Selbyana 16: 100–111. Promotion of Science (JSPS KAKENHI Grant Nos. 24255007 Kato, M., Inoue, T., Hamid, A.A., Nagamitsu, T., Merdek, M.B., to Mamoru Kanzaki, JP15K07201 to SS, and 16J06038 to US), Nova, A.R., Itino, T., Yamane, S., Yumoto, T. (1995): Seasonality and a grant from JSPS Core-to-Core programme B Asia-Africa and vertical structure of light-attracted insect communities Science Platforms (2017-2019) to Masaharu Motokawa. in a dipterocarp forest in Sarawak. Researches on Population Ecology 37: 59–79. References Kays, R., Allison, A. (2001): Arboreal tropical forest vertebrates: current knowledge and research trends. Plant Ecology 153: Angelini, C., Shilliman, B.R. (2014): Secondary foundation species 109–120. as drivers of trophic and functional diversity: evidence from a Kumagai, T., Yoshifuji, N., Tanaka, N., Suzuki, M., Kume, T. tree–epiphyte system. Ecology 95: 185–196. (2009): Comparison of soil moisture dynamics between a Ashton, P.S., Hall, P. (1992): Comparisons of structure among tropical rain forest and a tropical seasonal forest in Southeast mixed dipterocarp forests of north-western Borneo. Journal of Asia: impact of seasonal and year-to-year variations in rainfall. Ecology 80: 459–481. Water Resources Research 45: w04413. Barbour, T. (1912): A contribution to the zoogeography of the Lowman, M.D. (2009): Canopy research in the twenty-first century: East Indian Islands. Memoirs of the Museum of Comparative a review of arboreal ecology. Tropical Ecology 50: 125–136. Zoölogy at Harvard College 44: 1–203. McCracken, S.F., Forstner, M.R.J. (2008): Bromeliad patch Basset, Y. (2001): Invertebrates in the canopy of tropical rain sampling technique for canopy herpetofauna in neotropical forests: how much do we really know? Plant Ecology 153: forests. Herpetological Review 39: 170–174. 87–107. McCracken, S.F., Forstner, M.R.J. (2014): Herpetofaunal Boulenger, G.A. (1903): Report on the batrachians and reptiles. community of a high canopy tank bromeliad (Aechmea zebrina) Fasciculi Malayensis, Zoology 1: 130–176. in the Yasuní Biosphere Reserve of Amazonian Ecuador, Brown, R.M., Diesmos, A.C. (2000): The lizard genus with comments on the use of “arboreal” in the herpetological Luperosaurus: taxonomy, history, and conservation prospects literature. Amphibian & Reptile Conservation 8: 65–75. for some of the world’s rarest lizards. Sylvatrop: The Technical Journal of Philippine Ecosystems and Natural Resources 10: Min, P.Y., Das, I. (2012): A significant range extension for the 107–124. Kinabalu parachute gecko, Ptychozoon rhacophorus (Boulenger, Das, I. (2010): A Field Guide to the Reptiles of South-East Asia. 1899) (Squamata: Gekkonidae) and a new state record from London, UK, New Holland Publishers. Sarawak, northwestern Borneo. Herpetology Notes 5: 177–179. Das, I. (2012): Arboreal reptiles: tree-trunk and canopy-dwelling Nadkarni, N.M., Parker, G.G., Lowman, M.D. (2011): Forest species. In: Reptile Biodiversity: Standard Methods for Inventory canopy studies as an emerging field of science. Annals of Forest and Monitoring, p. 175–179. McDiarmid, R.W., Foster, M.S., Science 68: 217–224. Guyer, C., Gibbons, J. W., Chernoff, N., Eds., California, USA, Scheffers, B.R., Edwards, D.P., Diesmos, A., Williams, S.E., Evans, University of California Press. T.A. (2014a): Microhabitats reduce animal’s exposure to climate Díaz, I.A., Sieving, K.E., Peña–Foxon, M., Armesto, J.J. (2012): extremes. Global Change Biology 20: 495–503. A field experiment links forest structure and biodiversity: Scheffers, B.R., Phillips, B.L., Shoo, L.P. (2014b): Asplenium bird’s epiphytes enhance canopy invertebrates in Chilean forests. nest ferns in rainforest canopies are climate-contingent refuges Ecosphere 3: 5 for frogs. Global Ecology and Conservation 2: 37–46. Donald, J.D., Clegg, J.R., Ellwood, M.D.F. (2017): Colonisation Stuntz, S., Simon, U., Zotz, G. (1999): Assessing the potential of epiphytic ferns by skinks and geckos in the high canopy of a influence of vascular epiphytes on arthropod diversity in Bornean rainforest. The Herpetological Bulletin 141: 32�34. tropical tree crowns: hypotheses, approaches and preliminary Floren, A., Wetzel, W., Staab, M. (2014): The contribution of canopy data. Selbyana 20: 276–283. species to overall ant diversity (Hymenoptera: Formicidae) in Tiwari, K.K. (1961): The eggs and flight of the gecko Ptychozoon temperate and tropical ecosystems. Myrmecological News 19: kuhli Stejneger from Car Nicobar. Journal of the Bombay 65–74. Natural History Society 58: 523–527. Freiberg, M. (1997): Spatial and temporal pattern of temperature Tobón, C., Köhler, L., Frumau, K.F.A., Bruijnzeel, L.A., Burkard, and humidity of a tropical premontane rain forest tree in Costa R., Shmid, S. (2010): Water dynamics of epiphytic vegetation Rica. Selbyana 18: 77–84. in a lower montane cloud forest: fog interception, storage, Grismer, L.L., Wood Jr., P.L. Thura, M.K., Grismer, M.S., Brown, and evaporation. In: Tropical Montane Cloud Forests: Science R.M., Stuart, B.L. (2018): Geographically structured genetic for Conservation and Management, p. 261–267. Bruijnzeel, Observation of the eggs of parachute gecko on an epiphytic fern 1081

L.A., Scatena, F.N., Hamilton, L.S., Eds., New York, USA, Cambridge University Press. Tweedie, M.W.F. (1950): The flying gecko, Ptychozoon kuhli Stejn. Proceedings of the Zoological Society of London 120: 13. Tweedie, M.W.F. (1954): Notes on Malayan reptiles, No. 3. The Bulletin of the Raffles Museum 25: 107–117. Young, B.A., Lee, C.E., Daley, K.M. (2002): On a flap and a foot: aerial locomotion in the “Flying” gecko, Ptychozoon kuhli. Journal of Herpetology 36: 412–418.

Accepted by Benjamin Tapley