Herpetology Notes, volume 9: 291-295 (2016) (published online on 14 November 2016)

Occurrence and reproduction of anurans in brackish water in a coastal windbreak forest in Taiwan

Yuan-Mou Chang1,*, Chi-Shiun Wu2, Yi-Sin Huang1, Shau-Min Sung1 and Wenbe Hwang1

Most do not occur in salinity above The Chengxi windbreaks are in belt-type and from the typical freshwater (salinity < 0.5 ppt) because their skin coastal border of Zengwun estuary to Luermen River and egg membranes are highly permeable and has poor in Taijiang National Park, Tainan,Taiwan (about 200 osmoregulatory ability (Duellman & Trueb, 1994; Wells, hectares) (Figure 1). The windbreaks were planted to 2007). However, at least 144 have reduce wind speed, to reduce damage from salt-laden been reported that they can adapt or tolerate elevated winds in coastal areas, to enhance soil conservation, salinities and inhabit brackish habitats (salinity between to create microclimates in the sheltered zone and to 0.5 and 32 ppt) whether coastal, inland, natural or protect crops and houses. The main cultivated plant anthropogenically altered (Wangersky, 1980; Balinsky, is the Australian pine, but plants of the Indian almond 1981; Wu & Kam, 2009; Hopkins & Brodie Jr, 2015). (Terminalia catappa L.), Linden hibiscus (Hibiscus Among these brackish habitats, the saline coastal tiliaceus L.), Bhendi tree (Thespesia populnea (L.) areas are the major habitat type for these salt-tolerant Solad. ex Correa) are also cultivated in the certain amphibians (Hopkins & Brodie Jr, 2015), including areas of the windbreaks. The understory of the forests beaches (Hardy, 1952; Licht, et al., 1975), lagoons (Pyke, is made up of a variety of woody plants and herbs. et al., 2002; Moreira, et al., 2015), salt marshes (Neill, Woody plants include Macaranga (Macaranga tanarius 1958; Thirion, 2014), mangrove swamps (Gordon, (L.) Muell.-Arg.), screw pine (Pandanus odoratissimus 1961; Gordon & Tucker, 1965; Dunson, 1977; Van L. f.), black mangrove (Lumnitzera racemosa Willd), Beurden & Grigg, 1980; Uchiyama, et al., 1990; Hedges white mangrove (Avicennia marina (Forsk.) Vierh), sea & Thomas, 1992; Alvarez-Leon & De Ayala-Monedero, lettuce (Scaevola sericea (Gaertner) Roxb.) while herbs 2000; Rios-López, 2008; Chan & Goh, 2010; Downie, et al., 2010; Ferreira & Tonini, 2010; Glorioso, et al., 2010; Rahman & Asaduzzaman, 2010; Satheeshkumar, 2011; Andrade, et al., 2012; Jena, et al., 2013), brackish ponds (Annandale, 1907; Samraoui, et al., 2012), tidal pools (Gordon & Tucker, 1965; Wu & Kam, 2009; Jena, et al., 2013), tidal streams (Haramura, 2004; 2007; Downie, et al., 2010), and estuaries (Knoepffler, 1962). However, it has not been reported the presence and reproduction of amphibians in the brackish habitats of the coastal Australian pine (Casuarina equisetifolia L.) windbreak forests.

1 Department of Ecoscience and Ecotechnology, National University of Tainan, Tainan, Taiwan; 2 Department of Life Science, Chinese Culture University, Taipei, Taiwan Figure 1. Map of Chengxi windbreaks in Taijiang National * Corresponding author e-mail: [email protected] Park, Tainan, Taiwan. Red circles are survey sites. 292 Yuan-Mou Chang et al.

Figure 2. Anurans of the Chengxi windbreaks of the Taijiang National Park, Taiwan. A. Duttaphrynus melanostictus; B. limnocharis; C. Hoplobatrachus rugulosus; D. fissipes.

include Spanish needle (Bidens sp.), native bloodleaf hours (Heyer, et al., 1994). observed in the day (Achyranthes aspera L. var. indica L.), black nightshade and outside of survey sessions were also recorded. (Solanum americanum Miller), weed passion flower Each survey was attended by two to five persons. The (Passiflora foetida L. var. hispida), Guinea grass reproduction of the frogs was evidenced by observing (Panicum maximum Jacq.). Due to in low-lying regions eggs or in the water bodies. Adults and tadpoles and seawater intrusion, the windbreaks are a land area of frog species were identified according to the Field with water that is static or flowing, fresh or brackish, Guide to Amphibians and Reptiles in Taiwan (Shang, et either permanently or seasonally. The ecosystem al., 2009) and Tadpoles of Taiwan (Chou & Lin, 1997). type of the windbreaks is the intertidal forested We measured salinity and temperature of water bodies wetlands (intertidal swamp forest) (Dugan, 1990). The with eggs or tadpoles using a Conductivity/TDS meter windbreaks are the home and breeding ground of many (Model 8361, AZ Instrument Corp., Taichung, Taiwan) shellfish, fish, crabs, birds, and insects (Chang Yuan during each survey. Mou, personal observation) (Hwang & Chang, 2015). We observed four species of frogs in the windbreaks: We conducted a total of 15 frog surveys in the Indian rice frog Fejervarya limnocharis (Gravenhorst, windbreaks between July and August 2015, and 1829), Asian toad Duttaphrynus melanostictus between March and July 2016. We surveyed frogs (Schneider, 1799), Chinese bull frog Hoplobatrachus with an acoustic-visual survey from 1900 to 2300 rugulosus (Wiegmann, 1834), and ornate narrow- Occurrence and reproduction of anurans in brackish water in Taiwan 293

Figure 3. Examples of two typical breeding habitats in the Chengxi windbreaks of the Taijiang National Park in Taiwan, and egg mass/tadpoles of Fejervarya limnocharis, Hoplobatrachus rugulosus and Microhyla fissipes in these brackish habitats. A. a brackish pond; B. a ditch with brackish water; C and D. egg masses and the , respectively, of F. limnocharis; E. the H. rugulosus tadpole; F. the M. fissipes tadpole. Photograph F courtesy of Chuan-Bin Cheng.

mouthed frog Microhyla fissipes Boulenger, 1884(Figure and tadpoles of these three frog species can be observed 2). Secondly, our surveys indicated that the windbreaks in the same waterbodies. The breeding habitats were are the breeding habitats of F. limnocharis, H. rugulosus brackish and their salinity varied from 1.05 to 7.25 ppt and M. fissipes. We also heard loud advertisement calls with a median of 2.07 ppt (mean ± se = 2.51 ± 0.28 of these three frog species in the windbreaks. There ppt, n = 24), and water temperature varied from 23.7 to were eggs and/or tadpoles of these three frog species 31.2oC with a median of 25.8oC (mean ± se = 26.5 ± 0.6 in the pools, ponds, and ditches (Figure 3). The eggs oC, n = 24). 294 Yuan-Mou Chang et al.

Among these four reported anurans, F. limnocharis Leptodactylidae) in northeastern, Brazil. Herpetology Notes 5: has been reported to occur in brackish tidal streams in 173-175. (Boulenger, 1912) and coastal rock tidal Annandale, N. (1907): The fauna of brackish ponds at Port Canning, Lower Bengal. Records of the Indian Museum (A Journal of pools on islands off the coast of Taiwan (Wu & Kam, Indian Zoology) 1: 35-43. 2009; Wu, et al., 2012). Wu and Kam (2012) reported Balinsky, J.B. (1981): Adaptation of nitrogen metabolism to the salinity of these tidal pools with F. limnocharis hyperosmotic environment in amphibia. Journal of Experimental tadpoles are between 0-12 ppt, while the maximum Zoology 215: 335-350. salinity of tadpoles’ habitats in our study was 7.25 ppt. Boulenger, G.A. (1912): A vertebrate fauna of the Malay Peninsula As the salinity of habitats are so different between rock from the Isthmus of Kra to Singapore including the adjacent tidal pools and windbreaks, it would be interesting to islands: Reptilia and Batrachia. Oxfordshire, UK, Taylor and understand if there are geographic variations in the Francis. Chan, S.H., Goh, C. (2010): Frogs of Sungei Buloh Wetland tolerance and adaptation to water salinity between Reserve (Amphibia: Anura). Nature in Singapore 3: 103-116. populations (Gomez-Mestre, et al., 2004; Hopkins Chou, W.H., Lin, J. Y. (1997): Tadpoles of Taiwan. Taichung, & Brodie Jr, 2015). Adult H. rugulosus occurs tidal Taiwan, National Museum of Natual Science. irrigation ditches with salinity of 5 ppt in Malaysia Davenport, J., Huat, K.K. (1997): Salinity tolerance and preference (Davenport & Huat, 1997). Duttaphrynus melanostictus in the frog Rana rugulosa Wiegmann. Herpetological Journal was recorded only once during the surveys of our study 7: 114-115. and hence may have been of dispersing individual Downie, J.R., Hancock, E.G., Muir, A.P. (2010): The diet of the that were not necessarily inhabiting the windbreaks. paradoxical frog Pseudis paradoxa in Trinidad, West Indies. Herpetological Journal 20: 111-114. However, D. melanostictus has been reported to inhabit Duellman, W.E., Trueb, L. (1994): Biology of Amphibians. brackish ponds of the estuary in India (Annandale, Maryland, USA, The Johns Hopkins University Press. 1907) and brackish mangrove swamps in Bangladesh Dugan, P.J. (1990): Wetland conservation: A review of current (Rahman & Asaduzzaman, 2010) and Singapore (Chan issues and required action. Gland, Switzerland, IUCN. & Goh, 2010). The other important part of this study Dunson, W.A. (1977): Tolerance to high temperature and salinity is that we provided a new record of amphibian species by tadpoles of Philippine frog, Rana cancrivora. 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Accepted by Kanto Nishikawa