Policy Recommendation for the Conservation of the Suweon Treefrog (Dryophytes suweonensis) in the Republic of Korea
Amaël Borzée* 
Yikweon Jang- Division of EcoScience and Department of Life Science, Ewha Womans University, Seoul, South Korea
The Suweon treefrog (Dryophytes suweonensis) is an endangered species with an important evolutionary significance. However, the current rate of decline projects the extinction of the species within a few decades in the Republic of Korea. The species is presently exclusively inhabiting rice paddies and is not present in any protected area, although it would be relatively easy to designate protected area under the RAMSAR convention and correct the current negative population dynamics. Through three policy recommendations, we present the points of importance for the conservation of the Suweon Treefrog, list the site of importance for its conservation, and introduce an agricultural model allowing for the conservation of the species as well as continued rice production and economic income.
Actionable recommendations:
- Establishment of protected areas within the range of D. suweonensis
- Pesticide and herbicide ban in rice-paddy complexes where D. suweonensis occurs
- Vegetation mowing limit for surroundings of rice paddies where D. suweonensis occurs.
Introduction
The Suweon Treefrog (Dryophytes [Hyla] suweonensis; Duellman et al., 2016) is an endangered species in the Republic of Korea (IUCN, 2018) due to a low extent of occurrence (Borzée et al., 2017a), fragmented population (Borzée, 2018) and continuing decline in area of occurrence (Borzée et al., 2018a). About 2,500 calling males are estimated to be present in the Republic of Korea (Borzée et al., 2018a), segregated into 14 disconnected areas (Borzée, 2018). The species is also known to occur at a minimum of three sites in the Democratic People's Republic of Korea, with at least one seemingly healthy sub-population (Chun et al., 2012; Borzée and Seliger, 2018); although population sizes are not available for the country. Under the current threat levels, the species could become extinct within decades (Borzée, 2018).
In the Republic of Korea the species ranges from the Mangyeong River in the south to the Imjin River in the north (Kim et al., 2012; Borzée et al., 2016c, 2017a). Population sizes are generally decreasing because of habitat loss through encroachment and urbanization (Lee and Miller-Rushing, 2014), although some rare populations displayed low increases between 2015 and 2017 (Borzée et al., 2018a). Despite landscape modifications being the first reason for the endangered status of D. suweonensis (Borzée and Jang, 2015; Borzée, 2018), the species is under multiple threats including hybridization (Kuramoto, 1984; Borzée and Jang, 2018b), competition with D. japonicus (Borzée et al., 2016a,b, 2018e; Borzée and Jang, 2018a), environmental pollution (Borzée et al., 2018d), crop management and harvest (Borzée and Jang, 2017; Borzée et al., 2018b), emergent diseases such as the Chytrid fundus (Borzée et al., 2017b), and invasive species (Kim, 2016; Borzée et al., 2017b), among the main and defined threats.
It is important to protect the species due to its clear evolutionary potential, differentiated from other Hylid species by a switch in heterogamety resulting in a ZW system (Dufresnes et al., 2015), and in regard to the international conservation crisis involving amphibians worldwide (Stuart et al., 2004; Beebee and Griffiths, 2005; Bishop et al., 2012; Wake, 2012; Howard and Bickford, 2014; Pimm et al., 2014). Despite the current situation, D. suweonensis is not present in any protected area (Borzée et al., 2017a) and is only known to breed in rice paddies (Borzée and Jang, 2015), while original potential habitats might have included wetlands with low vegetation including Alopecurus sp. and Typha spp. (Borzée and Jang, 2015). The only conservation project to reintroduce the species was unsuccessful (Borzée et al., 2018c) and despite plans for ex-situ breeding facilities having been drafted (Noh, 2017), conservation of populations in the wild would simplify the protection of the species (Snyder et al., 1996). Additionally, the species (Borzée et al., 2018b) and other anuran species can adequately take advantage of the artificial flooding of rice paddies for agricultural purposes (Fujioka and Lane, 1997; Machado and Maltchik, 2010; Naito et al., 2013; Holzer, 2014; Orchard et al., 2019).
Amphibian conservation plans benefit from articulating local policies around the prioritized actions of the Amphibian Conservation Action Plan (Wren et al., 2015). Out of the 12 chapters of the ACAP, some sections on habitat protection and ecotoxicology are relevant to the policy recommendations recommended here. Regarding habitat protection, the ACAP recommends first to refine the definition of “Critical Habitat” for the target species and develop a list of standards for the identification of important sites. In the long term, the ACAP recommends developing “Amphibian Critical Habitat” keys to identify priority sites. Regarding ecotoxicology, short term recommendations include identifying organic agriculture movements to explore potential development and working with authorities to change legislation. They also include developing outreach material on the effects of locally applied pollutants on amphibian and human health at the stakeholder level, here rice farmers. Long term recommendations include long-term partnerships with organic agriculture organizations and the social marketing of the issue through the establishment of links with grassroots organizations. The policy recommendations made here are in-line with these global recommendations.
Policy and Practice
Consequently, we recommend three policies for the in-situ conservation of the Suweon Treefrog (D. suweonensis). These policies are independent of each other and need not be implemented in the order presented here.
Designation of Protected Areas Within the Range of the Species
We strongly urge the preservation of the current rice paddy system and the continued agricultural practices by farmers such as current timing of flooding, tilling and planting (Borzée et al., 2018b). However, avoiding burning straws left-over from the harvest before the fallow phase would avoid lethal consequences to individuals brumating in the vicinity of the rice paddies (Borzée et al., 2019). The designation of agricultural wetlands as protected area and their continued harvest may be conducted under the guidelines stipulated in the RAMSAR convention (see Classification of Wetland Type, §4.3.4; Ramsar Convention Secretariat, 2013) and governmental funding following those provided for “agri-environment” support programmes in the UK, where funding is matched to a score based on defined environmental benefits (Baker et al., 2011). This recommendation is based on the fact that the breeding activity of D. suweonensis is synchronized with the regulated hydroperiod resulting from the flooding of rice paddies for rice cultivation (Borzée et al., 2018b), which has so far resulted in adequate population recruitment. The transformation of rice paddies into natural wetlands is not recommended at the moment as the data available on the natural requirements of the species are still limited and transformations may result in the local extirpation of the species if conducted inadequately. The knowledge currently available only includes partial vegetation data, habitat size, and distribution models (Borzée and Jang, 2015; Song, 2015; Borzée et al., 2017a). In this regard, we recommend the implementation of protected area at the sites of Sihung, Iksan, Paju, Asan, and Chungju based on genetic variability (Borzée et al., 2018c; Figure 1), large source populations, buffer populations and important populations for connectivity (Borzée, 2018).
Figure 1. Distribution of Dryophytes suweonensis in the Republic of Korea. Each black patch represents an area within which sites where the species is present are connected (Borzée et al., 2018a), but disconnected from the nearest rice-paddy complex (Borzée, 2018). The species range is extracted from Borzée et al. (2017a). Map generated through ArcMap 10.5 (Environmental Systems Resource Institute, Redlands, California, USA).
Habitat Protection
We recommend the ban of pesticides and herbicides in the rice-paddy complexes where D. suweonensis is known to occur (Borzée et al., 2017a; Figure 1), as these are related to lower population sizes (Borzée et al., 2018d). The chemicals to be avoided are the ones resulting in high levels of phosphates and nitrates in the environment, and their application should be avoided during the breeding season (May and June) and tadpole development (June and July). We recommend a shift to ecological agriculture, a demonstrated way to maintain sustainability (Bellon and Penvern, 2014), including for rice harvest (Mendoza, 2008; Lestari and Suryana, 2013), as recommended by the government of the Republic of Korea (Jeong and Moon, 2013; Ministry of Agriculture Food and Rural Affairs, 2013) and already locally demonstrated (Lee et al., 2016). This would enable the conservation of the D. suweonensis in rice agricultural landscapes. We recommend the policy shift to be acknowledged by a special “Suweon Treefrog friendly” label, which would be economically sustainable (Jaďuďová et al., 2018) and in line with the rising environment and conservation awareness worldwide (Sutherland et al., 2018). This is the case of “Gangwha Maewha-malleum rice,” set up to protect the endangered Ranunculus kazusensis makino in a Ramsar site composed of rice paddies only and managed by the Korea National Trust Foundation (Ramsar Convention, 2018).
Microhabitat Management
Finally, we recommend a limit in the cutting of grass surrounding rice paddies at all sites where D. suweonensis occurs. Mowing grass present on ditches and delimitation banks between rice paddies is negatively impacting the species, as this environment is the preferred diurnal resting habitat (Borzée et al., 2016a; Groffen et al., 2018) and is also used for feeding, microhabitat segregation with D. japonicus and overwintering (Borzée et al., 2016a, 2019). We acknowledge the need for weed control and shade prevention for rice growth, and when the vegetation needs to be cut, it should not be done below 30 cm as frogs diurnal activity is below this height (Borzée et al., 2016a), and as this is unlikely to impact rice production due to a lower height than the rice itself. When possible, vegetation including Korean willows (Salix koreensis), and occasionally high grasses such as Elymus repens and Phragmites communis should be maintained in the vicinity of rice paddies to allow for population connectivity (Driscoll et al., 2013; Schneider-Maunoury et al., 2016), as well as foraging and overwintering by D. suweonensis (Borzée et al., 2016a, 2019).
The implementation of these policies will enable the survival of the Suweon treefrog (D. suweonensis) and the continued production of rice, highlighting the importance of the Republic of Korea in biological conservation and organic sustainable development. Moreover, our recommendations are based on a review of the literature presenting such cases and can be adapted to protect any species relying on rice paddies during their life cycle.
Author Contributions
All authors listed have made a substantial, direct and intellectual contribution to the work, and approved it for publication.
Funding
This policy results from the research supported by numerous Small Grants for Science and Conservation from The Biodiversity Foundation, with special thanks to Sanha Kim and Jaeha Ahn, and a grant from the National Geographic Society Asia (Young Explorer #17-15) to AB; and Research Grants from the National Research Foundation of Korea (#2017R1A2B2003579) and the Rural Development Administration (PJ012285) to YJ. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Conflict of Interest Statement
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
References
Baker, J., Beebee, T., Buckley, J., Gent, T., and Orchard, D. (2011). Amphibian Habitat Management Handbook. Bournemouth: Amphibian and Reptile Conservation.
Beebee, T. J. C., and Griffiths, R. A. (2005). The amphibian decline crisis: a watershed for conservation biology? Biol. Cons. 125, 271–285. doi: 10.1016/j.biocon.2005.04.009
Bellon, S., and Penvern, S. (2014). “Organic food and farming as a prototype for sustainable agricultures,” in Organic Farming, Prototype for Sustainable Agricultures, eds S. Bellon and S Penvern (Dordrecht: Springer), 1–19.
Bishop, P. J., Angulo, A., Lewis, J. P., Moore, R. D., Rabb, G. B., and Garcia Moreno, J. (2012). The amphibian extinction crisis-what will it take to put the action into the Amphibian Conservation Action Plan? Surveys Perspect. Integr. Environ. Soc. 5, 97–111.
Borzée, A. (2018). Why are Anurans Threatened? The case of Dryophytes suweonensis. Ph.D. Seoul National University, Seoul, Republic of Korea.
Borzée, A., Andersen, D., and Jang, Y. (2018a). Population trend inferred from aural surveys for calling anurans in Korea. PeerJ. 6:e5568. doi: 10.7717/peerj.5568
Borzée, A., Choi, Y., Kim, Y. E., Jablonski, P. G., and Jang, Y. (2019). Interspecific variation in seasonal migration and brumation behavior in two closely related species of treefrogs. Front. Ecol. Evol. 7:55. doi: 10.3389/fevo.2019.00055
Borzée, A., Heo, K., and Jang, Y. (2018b). Relationship between agroenvironmental variables and breeding Hylids in rice paddies. Sci. Rep. 8:8049. doi: 10.1038/s41598-018-26222-w
Borzée, A., and Jang, Y. (2015). Description of a seminatural habitat of the endangered Suweon treefrog, Hyla suweonensis. Anim Cells Syst. 19, 1–5. doi: 10.1080/19768354.2015.1028442
Borzée, A., and Jang, Y. (2017). Impact of rice and bean harvests on the Suweon Treefrog (Dryophytes suweonensis). Int. J. Curr. Res. 9, 59620–59623.
Borzée, A., and Jang, Y. (2018a). Interference competition driven by hydric stress in Korean Hylids. Nat. Conserv. Res. 3,120–124. doi: 10.24189/ncr.2018.008
Borzée, A., and Jang, Y. (2018b). “Large-scale hybridisation as an extinction threat to the Suweon treefrog (Dryophytes suweonensis),” in Conservation Asia 2018, vol. 1, (Bishkek: Society for Conservation Biology – Asia section).
Borzée, A., Kim, J. Y., Cunha, M. A. M., Lee, D., Sin, E., Oh, S., et al. (2016a). Temporal and spatial differentiation in microhabitat use: Implications for reproductive isolation and ecological niche specification. Integr. Zool. 11, 375–387. doi: 10.1111/1749-4877.12200
Borzée, A., Kim, J. Y., and Jang, Y. (2016b). Asymmetric competition over calling sites in two closely related treefrog species. Sci. Rep. 6:32569. doi: 10.1038/srep32569
Borzée, A., Kim, K., Heo, K., Jablonski, P. G., and Jang, Y. (2017a). Impact of land reclamation and agricultural water regime on the distribution and conservation status of the endangered Dryophytes suweonensis. PeerJ. 5:e3872. doi: 10.7717/peerj.3872
Borzée, A., Kim, Y. I., Kim, Y. E., and Jang, Y. (2018c). Translocation of the endangered and endemic Korean treefrog Dryophytes suweonensis. Conserv. Evid. 15, 6–11.
Borzée, A., Kosch, T. A., Kim, M., and Jang, Y. (2017b). Introduced bullfrogs are associated with increased Batrachochytrium dendrobatidis prevalence and reduced occurrence of Korean treefrogs. PLoS ONE. 12:e0177860. doi: 10.1371/journal.pone.0177860
Borzée, A., Kyong, C. N., Kil, H. K., and Jang, Y. (2018d). Impact of water quality on the occurrence of two endangered Korean anurans: Dryophytes suweonensis and Pelophylax chosenicus. Herpetologica. 74, 1–7. doi: 10.1655/Herpetologica-D-17-00011
Borzée, A., and Seliger, B. (2018). Dryophytes suweonensis (Suweon Treefrog). Herpetol. Rev. 49:707.
Borzée, A., Yu, A.-Y., and Jang, Y. (2018e). Variations in boldness, behavioural and physiological traits of an endangered and a common hylid species from Korea. Ethol. Ecol. Evol. 30, 515–533. doi: 10.1080/03949370.2018.1441192
Borzée, A., Yu, S. H., and Jang, Y. (2016c). Dryophytes suweonensis (Suweon Treefrog). Herpetol. Rev. 47:418.
Chun, S., Chung, E., Voloshina, I., Chong, J. R., Lee, H., and Min, M.-S. (2012). Genetic diversity of korean tree frogs (Hyla suweonensis and Hyla japonica): assessed by mitochondrial cytochrome b gene and cytochrome oxidase subunit I gene. Kor. J. Herpetol. 4, 31–41. doi: 10.1080/23802359.2017.1292475
Driscoll, D. A., Banks, S. C., Barton, P. S., Lindenmayer, D. B., and Smith, A. L. (2013). Conceptual domain of the matrix in fragmented landscapes. Trends Ecol. Evol. 28, 605–613. doi: 10.1016/j.tree.2013.06.010
Duellman, W. E., Marion, A. B., and Hedges, S. B. (2016). Phylogenetics, classification, and biogeography of the treefrogs (Amphibia: Anura: Arboranae). Zootaxa. 4104, 1–109. doi: 10.11646/zootaxa.4104.1.1
Dufresnes, C., Borzée, A., Horn, A., Stöck, M., Ostini, M., Sermier, R., et al. (2015). Sex-chromosome homomorphy in Palearctic tree frogs proceeds from both turnovers and X-Y recombination. Mol. Biol. Evol. 32, 2328–2337. doi: 10.1093/molbev/msv113
Fujioka, M., and Lane, S. J. (1997). The impact of changing irrigation practices in rice fields on frog populations of the Kanto Plain, central Japan. Ecol. Res. 12, 101–108. doi: 10.1007/BF02523615
Groffen, J., Borzée, A., and Jang, Y. (2018). Positioning of two treefrog species within rice paddies in relation to different habitat borders. Anim. Cells Syst. 22, 205–211. doi: 10.1080/19768354.2018.1475301
Holzer, K. A. (2014). Amphibian-Human Coexistence in Urban Areas. San Diego, CA: University of California Davis.
Howard, S. D., and Bickford, D. P. (2014). Amphibians over the edge: silent extinction risk of Data Deficient species. Divers Distrib. 20, 837–846. doi: 10.1111/ddi.12218
Jaďuďová, J., Marková, I., Hroncová, E., and Vicianová, J. H. (2018). An assessment of regional sustainability through quality labels for small farmers' products: a Slovak case study. Sustainability 10:1273. doi: 10.3390/su10041273
Jeong, H.-K., and Moon, D.-H. (2013). Response Atrategy to the Abolishment of Low-Pesticide Agricultural Product Certification. Seoul: Korea Rural Economic Institute.
Kim, I.-H., Son, S.-H., Kang, S.-W., and Kim, J.-B. (2012). Distribution and habitat characteristics of the endangered Suweon-Tree Frog (Hyla suweonensis). Kor. J. Herpetol. 4, 15–22.
Kim, Y. E. (2016). Differential Antipredator Behavior Between Hyla Japonica and H. suweonensis Suggests Separate Evolution. Ms.C. Ewha Womans University, Seoul.
Kuramoto, M. (1984). Systematic implications of hybridization experiments with some eurasian treefrogs (genus Hyla). Copeia 3, 609–616. doi: 10.2307/1445141
Lee, S., Nguyen, T. T., Poppenborg, P., Shin, H.-J., and Koellner, T. (2016). Conventional, partially converted and environmentally friendly farming in South Korea: Profitability and factors affecting farmers' choice. Sustainability 8:704. doi: 10.3390/su8080704
Lee, S.-D., and Miller-Rushing, A. J. (2014). Degradation, urbanization, and restoration: a review of the challenges and future of conservation on the Korean Peninsula. Biol Cons. 176, 262–276. doi: 10.1016/j.biocon.2014.05.010
Lestari, Y. K., and Suryana, A. T. (2013). “Sustainability of organic rice farming in indonesia,” in The 10th Hokkaido Indonesia Student Association Scientific Meeting (HISAS 10). (Hokkaido).
Machado, I. F., and Maltchik, L. (2010). Can management practices in rice fields contribute to amphibian conservation in southern Brazilian wetlands? Aquatic Conserv. 20, 39–46. doi: 10.1002/aqc.1070
Mendoza, T. C. (2008). Evaluating the benefits of organic farming in rice agroecosystems in the Philippines. J. Sustain. Agric. 2, 93–115. doi: 10.1300/J064v24n02_09
Ministry of Agriculture Food and Rural Affairs (2013). The 3rd Environment-Friendly Agriculture Promotion 5-year Plan. Sejong: MAFRA - Environment-friendly agriculture division.
Naito, R., Sakai, M., Natuhara, Y., Morimoto, Y., and Shibata, S. (2013). Microhabitat use by Hyla japonica and Pelophylax porosa brevipoda at levees in rice paddy areas of Japan. Zool. Sci. 30, 386–391. doi: 10.2108/zsj.30.386
Noh, H. K. (2017). “Endangered wildlife restoration road map (2017-2021),” in Focus on Medium and Large Mammal Species. vol. 1, ed S.O.R.O.E. Wildlife (Wonju: Korea National Park Services & Ministry of Environment), 11.
Orchard, D., Tessa, G., and Jehle, R. (2019). Age and growth in a European flagship amphibian: equal performance at agricultural ponds and favourably managed aquatic sites. Aquat. Ecol. 53:37–48. doi: 10.1007/s10452-018-09671-3
Pimm, S. L., Jenkins, C. N., Abell, R., Brooks, T. M., Gittleman, J. L., Joppa, L. N., et al. (2014). The biodiversity of species and their rates of extinction, distribution, and protection. Science 344, 987–997. doi: 10.1126/science.1246752
Ramsar Convention (2018). “Annotated list of wetlands of international importance - republic of korea. ganghwa maehwamareum habitat,” in Ganghwa Maehwamareum Habitat, vol. 1. ed R. S. I. Service (Gland: Ramsar Convention), 3.
Ramsar Convention Secretariat (2013). The Ramsar Convention Manual: a Guide to the Convention on Wetlands (Ramsar, Iran, 1971), 6th edn. Gland: Ramsar Convention Secretariat.
Schneider-Maunoury, L., Lefebvre, V., Ewers, R. M., Medina-Rangel, G. F., Peres, C. A., Somarriba, E., et al. (2016). Abundance signals of amphibians and reptiles indicate strong edge effects in Neotropical fragmented forest landscapes. Biol. Cons. 200, 207–215. doi: 10.1016/j.biocon.2016.06.011
Snyder, N. F., Derrickson, S. R., Beissinger, S. R., Wiley, J. W., Smith, T. B., Toone, W. D., et al. (1996). Limitations of captive breeding in endangered species recovery. Conserv. Biol. 10, 338–348. doi: 10.1046/j.1523-1739.1996.10020338.x
Song, W. (2015). Habitat analysis of Hyla suweonensis in the breeding season using species distribution modeling. J. Kor. Soc. Environ. Restor. Technol. 18, 71–82. doi: 10.13087/kosert.2015.18.1.71
Stuart, S. N., Chanson, J. S., Cox, N. A., Young, B. E., Rodrigues, A. S., Fischman, D. L., et al. (2004). Status and trends of amphibian declines and extinctions worldwide. Science 306, 1783–1786. doi: 10.1126/science.1103538
Sutherland, W. J., Dicks, L. V., Ockendon, N., Petrovan, S. O., and Smith, R. K. (2018). WhatWorks in Conservation: 2018. Cambridge, UK: Open Book Publishers.
Wake, D. B. (2012). Facing extinction in real time. Science 335, 1052–1053. doi: 10.1126/science.1218364
Wren, S., Angulo, A., Meredith, H., Kielgast, J., Santos, M. D., and Bishop, P. (2015). Amphibian Conservation Action Plan. IUCN SSC Amphibian Specialist Group. Available online at: http://www.amphibians.org/acap/ (accessed March 24, 2019).
Keywords: conservation, policy, Suweon Treefrog, Republic of Korea, Dryophytes suweonensis
Citation: Borzée A and Jang Y (2019) Policy Recommendation for the Conservation of the Suweon Treefrog (Dryophytes suweonensis) in the Republic of Korea. Front. Environ. Sci. 7:39. doi: 10.3389/fenvs.2019.00039
Received: 27 September 2018; Accepted: 13 March 2019;
Published: 04 April 2019.
Edited by:
Franco Andreone, Museo Regionale di Scienze Naturali, ItalyReviewed by:
Nicolas Urbina-Cardona, Pontificia Universidad Javeriana, ColombiaAttila D. Sándor, University of Agricultural Sciences and Veterinary Medicine of Cluj-Napoca, Romania
Copyright © 2019 Borzée and Jang. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Amaël Borzée, amaelborzee@gmail.com