Acta Herpetologica 15(2): 87-94, 2020 ISSN 1827-9635 (print) © Firenze University Press ISSN 1827-9643 (online) www.fupress.com/ah DOI: 10.13128/a_h-9670 Potential effects of climate change on the distribution of invasive bullfrogs Lithobates catesbeianus in China Li Qing Peng1, Min Tang1, Jia Hong Liao1, Hai Fen Qing1, Zhen Kun Zhao1, David A. Pike2, Wei Chen1,* 1 Ecological Security and Protection Key Laboratory of Sichuan Province, Mianyang Normal University, Mianyang 621000, China 2 Department of Biology, Rhodes College, Memphis Tennessee 38111, USA *Corresponding author. E-mail: wchen1949@163.com Submitted on 2020, 4th September; revised on 2020, 10th October; accepted on 2020, 26th October Editor: Rocco Tiberti Abstract. Climate plays important roles in determining the geographical distribution of species, including the inva- sion area of alien species. Little is known, however, about the influence of climate change on the distribution area of invasive amphibian species in China. We adopted a maximum entropy model to predict the potential suitable invasive range of invasive bullfrogs Lithobates catesbeianus in China under two future climate scenarios in 2050 and 2070. Our results reveal that bullfrogs were mainly distributed in East and Central China at present, and the suitable area for the species may decrease in future. This suggests that climate change may negatively impact this alien-invasive species. Keywords. Bullfrog, climate change, environmental limitations, invasive species, potential distribution, species dis- tribution model. INTRODUCTION Biological invasion of alien invasive species is consid- ered to be the second leading cause of global biodiversity loss and habitat degradation (Pimentel et al., 2000; Bel- lard et al., 2012; Runyon et al., 2012), seriously threat- ening the health of ecosystems (Hobbs and Huenneke, 1992; D’Antonio et al., 2004; Vilà et al., 2011; Espíndola et al., 2012; Sorte et al., 2013) and causing significant economic losses (Pimentel et al., 2000). The proliferation and outbreak of invasive species are becoming more and more serious (Pyšek and Hulme, 2010). The accelera- tion of globalization has affected the distribution of inva- sive species and almost no ecosystem is immune to the impact of alien species (Weber and Li, 2008; Catford et al., 2012). China is a large country encompassing many different climatic regions, where many invasive species can find suitable habitats where to establish. Investigating the potential distribution of invasive species could help to address the conservation efforts to eliminate or reduce the negative effects of biological invasions on local wild- life and ecosystems (Xie et al., 2001). As in the rest of the world, climate change is affect- ing also China’s ecosystems (Hu et al., 2012). Climate change has shown enormous influence on species distri- bution (Erasmus et al., 2002; Walther et al., 2002; Root et al., 2003; Hari et al., 2006; Guralnick, 2007). For exam- ple, climate change in the 20th century has changed the distribution of butterflies (Parmesan et al., 1999), birds (Thoms and Lennon, 1999), amphibians (Araújo et al., 2006) and mammals (Hersteinsson and Macdonald, 1992). Climate change has attracted wide attention of governments and scientists because of its enormous influ- ences on ecosystem functions and global environmental quality (Thomas et al., 2004; Kiritani, 2011). The bullfrog Lithobates catesbeianus is native to east- ern North America, but has been introduced throughout the world during the past two centuries (Lever, 2003). 88 Li Qing Peng et alii The species is considered as one of the most harm- ful and threatening invasive species, since it is relatively large and negatively affects native amphibians through competition (Zhou et al., 2005), predation (Kieseck- er and Blaustein, 1998; Lowe et al., 2000) and disease transmission (Hanselmann et al., 2004). Knowledge of the patterns of bullfrog invasion is, therefore, extremely important for planning conservation strategies aim- ing to understand and reduce the impacts of their inva- sion. Bullfrogs were introduced into China in 1959 via the aquaculture and aquarium trades (Han, 1991). The species successfully established wild populations, and it is spreading locally (Li and Xie, 2004; Wu et al., 2004). Once established it is extremely difficult to eradicate (Li and Xie, 2004). Although the distribution of the species has been simulated at a global scale (Ficetola et al., 2007) to predict areas susceptible to invasion, little is known about its potential distribution in China and how future climate scenarios will influence its distribution. We there- fore modeled the potential distribution of bullfrog based on current climatic models and projected the results onto future climate scenarios (2050 and 2070) under two emis- sions scenarios, RCP4.5 (a radiative forcing of 4.5 W/ m2 at the end of 2100) and RCP8.5 (a radiative forcing of 8.5 W/m2 at the end of 2100). Our main aims were to describe the current potential distribution of the bullfrogs in China and to model its distribution under future cli- mate change scenarios. MATERIALS AND METHODS We collected individual records of bullfrogs in China from: 1) the relevant literature (n = 83 records); 2) the Global Bio- diversity Information Facility database (GBIF, http://data.gbif. org, n = 6 records); and 3) our own field investigations (n = 6 records). We used Arcgis 10.2, combined with Google Earth, to extract the longitude and latitude coordinates and discard duplicate records (Warren and Seifert, 2011). All the distribu- tion points with a spatial resolution of 30 arc-sec are buffered in GIS to ensure that only one point exists within the range of 30 arc-seconds (approximately 1 km × 1 km). Totally, we achieved 95 individual records of bullfrogs in China. We downloaded climate data with a spatial resolution of 30 arc-sec from the Worldclim database (http//www.worldclim.org/ bioclim). We used Arcgis 10.2 to unify all the factors into the same coordinate system and extent (Tang and Yang, 2006). As our base map, we used a 1: 4,000,000 map of China as origi- nal map from the national basic geographic information system (http://nfgis.nsdi.gov.cn). We prepared a total of 22 layers of variables (19 environ- mental variables and 3 topography variables), that mainly reflect seasonal variation in temperature and precipitation (Hijmans et al., 2005), and topography factors (elevation, aspect and slope). We extracted their values at each distribution point and we cal- culated the pairwise Pearson product-moment correlation coef- ficients. In the cases where two variables were inter-correlated to a high degree (r > 0.75, Nori et al., 2011a, b), we selected the most important biologically factors (Bourke et al., 2018). We selected 6 final bioclimatic variables and 3 topography vari- ables that did not show high correlation with other variables (r < 0.75) (Nori et al., 2011a, b). The final variable set included “Annual Mean Temperature” (bio1), “Mean diurnal range of temperature” (bio2; the mean of monthly maximum tempera- tures minus the monthly minimum temperatures), “Isothermal- ity” (bio3, Mean Diurnal Range/(Max Temperature of Warm- est Month-Min Temperature of Coldest Month)×100), “Mean Temperature of Wettest Quarter” (bio8), “Annual Precipitation” (bio12), and “Precipitation Seasonality” (bio15, Coefficient of Variation), elevation, aspect and slope. To estimate the influ- ence of global climate change on the potential distribution of the species, we modeled the distribution for three different time slices: present, 2050 and 2070. The climate data was available from the Worldclim data (http//www.worldclim.org/bioclim). Due to the large effect of different Atmosphere Global Circula- tion Models (AGCMs) in species range projections (Diniz-Filho et al., 2009), we selected three different AGCMs (BCC-CSM1-1, ACCESS1-0 and IPSL_CM4) for each time slice with each cli- mate models involving two future emissions scenarios devel- oped by IPCC’s Fifth Assessment Report (RCP4.5 and RCP8.5) (http//www.worldclim.org/bioclim). The selected AGCMs have different equilibrium climate sensitivity values ranging from 0.9 °C to 4.8 °C. Maximum Entropy Modeling (Maxent) is a useful method to simulate the potential habitat redistribution under climate change, due to high predictive accuracy and strong stability (Phillips et al., 2006; Steven et al., 2006; Wisz et al., 2008). We used a maximum entropy approach to model climatically suit- able areas of bullfrogs in China using Maxent 3.3.3e (www. cs.princeton.edu/~shapire/maxent), and we validated the mod- el using a cross-fold approach (Hijmans, 2012). We randomly selected 75% of bullfrog records for model training (Bourke et al., 2017) and the remaining 25% for model testing, with a logistic output format ranging from 0 (unsuitable environmen- tal conditions) to 1 (optimal) (values near 0.5 representative of average habitat quality; Phillips and Dudík, 2008). Jackknife tests were run to measure variable importance (Phillips et al., 2006). In addition, a bias file was included in the run to repre- sent sampling effort to reduce the sampling bias and increasing speed (Young et al., 2011). The accuracy of the model was evaluated by using the area under the receiver operating characteristic curve called AUC (Swets, 1988), commonly recognized as the optimal model pre- diction since it is unaffected by the threshold value and insen- sitive to incidence of species (Fielding and Bell, 1997). AUC scores quantify the SDM’s ability to differentiate between ran- dom prediction (AUC = 0.5) and perfect identification of suit- able grid cells (AUC = 1.0) (Hanley and McNeil, 1982; Phillips et al., 2006; Wang et al., 2007). After converting the Maxent output avg.asc into raster format, we reclassified the results of Maxent with thresholds in ArcGIS (Lu et al., 2012) and divided the suit bal environmental conditions into 4 levels based on the fitness index size (Wang et al., 2007; Zhai and Li, 2012) with 89Potential effects of climate change on the distribution of invasive bullfrogs Lithobates catesbeianus in China low potential (< 0.2), moderate potential (0.2-0.4), good poten- tial (0.4-0.6), high potential (> 0.6) (Yang et al., 2013). To test for possible differences of the predicted distribution under different climate scenarios, each out of the twelve maps was compared to the current distribution map using Map Com- parison Kit software (version 3.2.3; MCK, 2017) and an overall similarity index was computed between a map pair. We applied the “fuzzy numerical” algorithm as these maps were numerical (Visser and de Nijs, 2006; Falaschi et al., 2018). RESULTS We obtained a good SDM performance with an aver- age test AUC value of 0.867, which indicated that the pre- diction has high credibility. Analysis of variable contri- butions revealed that the “Annual Precipitation” had the highest explanative power, explaining 34.7% of the vari- ation, followed by “Mean Diurnal Range” (33.9%), “Ele- vation” (20.4%) and “Annual Mean Temperature” (3.1%), suggesting that the geographical distribution of bullfrog was most affected by these four factors. The results from Maxent analysis showed at present there were many areas unsuitable for habitation by bull- frogs: Inner Mongolia, Gansu, Qinghai and Tibet. Over- all, mainly the center, east, southeast and the southwest of China were suitable area of bullfrog survival, with a small number of suitable areas in Xinjiang, Ningxia, Jilin, Liaoning and Heilongjiang (Fig. 1). The AUC values were above 0.8 in all of the models, indicating that the prediction results have high credibil- ity. Generally, climatically suitable areas may become nar- rower as the invasion begins to retract in the southeast coastal the north of the north China plain, Sichuan basin and the middle and lower reaches of the Yangtze River (Fig. 2; Table 1). Only minor differences were observed in model projection onto climate change scenarios derived from BCC-CSM1-1, ACCESS1-0 and IPSL_CM4 (Fig. 3; Table 1), and these differences and similarities were also confirmed by the fuzzy numerical comparison performed in MCK: similarity maps (Fig. 4) showed only slight dif- ferences between current distribution map and these future distribution maps with the similarity index rose from 0.552 to 0.773. DISCUSSION We investigated the current potential and future distri- bution for bullfrogs under different climate change scenari- os. The results show that under the current climatic condi- tions, bullfrogs have a wide range of potential distribution in China, located in the center, east, southeast and south- west China, with only a small number of suitable areas in north China including Xinjiang, Ningxia, Liaoning, Jilin and Helongjiang. Generally, our models also revealed that global climate change is likely to shrink slightly the extent of suitable habitat under future scenarios. Compared to Ficetola et al. (2007), who found that bullfrogs are mainly distributed in eastern China, our study results extend its distribution area to central Chi- na, with a few locations in the west and northeast Chi- na, which may represent new invasion areas. This can be explained by the facts that some new invasion sites have been found in China recently (Fei et al., 2012). The current distribution pattern of bull frogs in China can mainly be explained by precipitation and tem- peratures. Previous study also showed that bullfrog pres- ence seems to be positively related to precipitation (Fice- tola et al., 2007). The availability of water (including the presence of permanent wetlands) for breeding are com- monly recorded important environmental features need- ed for the presence of bullfrogs (Maret et al., 2006) and their tadpoles’ growth, development and metamorphosis (Govindarajulu et al., 2006). In addition, Mean Diurnal Range also influences the distribution of bullfrogs. This is also similar to the results from Ficetola et al. (2007) and, indeed, Bullfrog is a ‘warm-adapted species’ (Bachmann, 1969; Harding, 1997). Besides, previous studies showed that the current distribution of bullfrogs in China is also explained by 1) the proximity to the frogfarms, from where bullfrogs can escape: most of the bullfrog farm- ing in China is surrounded by highly suitable habitats, and the frogs can establish wild population there (Wu et al., 2004; Li and Xie, 2004); 2) the abandonment/release of bullfrogs mainly by religious groups, which also led to the establishment of new wild population, e.g., in Yunnan Fig. 1. Map of the suitable distribution of bullfrog in China (Pre- sent). 90 Li Qing Peng et alii and Sichuan (Wu et al., 2004; Li and Xie, 2004). As shown by the fuzzy numerical comparison per- formed in MCK, slight differences between current and future distribution maps have been observed. Also, pro- jecting bullfrogs’ climatically suitable areas on future cli- mate change scenarios (RCP4.5 and RCP8.0) indicated that climatically suitable areas will become narrower in China. The potential habitats of bullfrogs in China will retreat to the most suitable area including the north of the north China plain, Sichuan basin and the middle and lower reaches of the Yangtze River (Fig. 2), where bull- frog farming is particularly common (Fei et al., 2012). Biological invasions are complex and the potential habitat distribution is determined by a variety of fac- tors (Li et al., 2009). In this study, we only considered the effect of the climate and terrain, but we did not con- sider the effect of the other factors including the vegeta- tion cover, biotic interactions with other species, species Fig. 2. Maps of the potential suitable distribution of bullfrog in China in 2050 and 2070. 91Potential effects of climate change on the distribution of invasive bullfrogs Lithobates catesbeianus in China migration capacity, species evolutionary adaptations, and human exploitation of wild populations, on the poten- tial distribution of the bullfrog. If these factors were fully considered, the predicted results could have been more closely related to the current distribution of species (Gra- ham and Hijmans, 2006). To effectively prevent further invasions of bullfrogs in China, management policies should be more prag- matic, preventing new introductions within suitable habi- tats and eradicating populations when possible. Based on the predictions on bullfrog potential habitats from SDMs, the authorities should consider the model results to focus the management strategies on these potentially sensitive regions. In addition, authorities should tighten control of bullfrog farming to prevent their escape. In addition, frog factories could be moved to areas which are surrounded by unsuitable habitats of bullfrogs, which would reduce a lot the possibility of survival of escaped captive individuals. ACKNOWLEDGMENTS We thank Litao Gan, Kejun Hua and Xuli Ren for assistance in the field, and Rocco Tiberti, Marco Man- giacotti and anonymous reviewers for their kind sug- gestion. This study was funded by the Natural Sciences Foundation for Distinguished Young Scholar of Sichuan (grant number 2016JQ0038), Key Foundation of Sichuan Provincial Department of Education (grant number 18ZA0255) and the National Sciences Foundation of Chi- na (grant number 31670392). REFERENCES Araújo, M.B., Thuiller, W., Pearson, R.G. (2006): Climate warming and the decline of amphibians and reptiles in Europe. J. Biogeogr. 33: 1712-1728. Bachmann, K. (1969): Temperature adaptations of amphibian embryos. Am. Nat. 103: 115-130. Bellard, C., Bertelsmeier, C., Leadley, P., Thuiller, W., Courchamp, F. (2012): Impacts of climate change on the future of biodiversity. Ecol. Lett. 15: 365-377. Bourke, J., Busse, K., Böhme, W. (2018): Potential effects of climate change on the distribution of the endan- gered Darwin’s frog. North-West. J. Zool. 14: 165-170. Catford, J.A., Vesk, P.A., Richardson, D.M., Pyšek, P. (2012): Quantifying levels of biological invasion: towards the objective classification of invaded and invasible ecosystems. Global Change Biol. 18: 44-62. D’Antonio, C.M., Jackson, N.E., Horvitz, C.C., Hedberg, R. (2004): Invasive plants in wild land ecosystems: merging the study of invasion processes with manage- ment needs. Front. Ecol. Environ. 2: 513-521. Diniz - Filho, J.A.F., Bini, L.M., Range, T.F., Loyola, R.D., Hof, C., Nogués-Bravo, D., Araújo, M.B. (2009): Par- titioning and mapping uncertainties in ensembles of forecasts of species turnover under climate change. Ecography 32: 897-906. Erasmus, B.F., Jaarsveld, A.S., Chown, S.L., Chown, S.L., Kshatriya, M., Wessels, K.J. (2002): Vulnerability of South African animal taxa to climate change. Global Change Biol. 8: 679-693. Espíndola, A., Pellissier, L., Maiorano, L., Hordijk, W., Guisan, A., Alvarez, N. (2012): Predicting present and future intra-specific genetic structure through niche hind casting across 24 millennia. Ecol. Lett. 15: 649-657. Table 1. Changes in the potential distribution area under climate change in 2050 and 2070. Climate scenarios Atmosphere Global Circulation Models (AGCMs) Area of the most suitable zone (the red part of the map)/ Million square kilometers Percentage (%) Present 82.27201 9.19% 2050RCP4.5 ACCESS1-0 BCC-CSML-1 IPSL-CM$ 66.06528 68.44306 80.92153 6.88% 7.12% 8.42% 2050RCP8.0 ACCESS1-0 BCC-CSML-1 IPSL-CM$ 59.2675 69.33708 89.20736 6.18% 7.22% 9.28% 2070RCP4.5 ACCESS1-0 BCC-CSML-1 IPSL-CM$ 67.75792 72.75847 78.15097 7.05% 7.57% 8.13% 2070RCP8.0 ACCESS1-0 BCC-CSML-1 IPSL-CM$ 55.53778 60.97194 78.69361 5.78% 6.35% 8.19% Fig. 3. Comparison of potential suitable distribution of bullfrog at present, in 2050 and in 2070 under future climatic conditions with low potential (< 0.2), moderate potential (0.2-0.4), good potential (0.4 – 0.6), high potential (> 0.6). 92 Li Qing Peng et alii Falaschi, M., Mangiacotti, M., Sacchi, R., Scali, S., Razzetti, E. (2018): Electric circuit theory applied to alien inva- sions: a connectivity model predicting the Balkan frog expansion in Northern Italy. Acta Herpetol. 13: 33-42. Fei, L., Ye, C.Y., Jiang, J.P. (2012): Colored atlas of Chi- nese amphibians and their distributions. Chengdu, Sichuan publishing group, Sichuan Publishing House of Science and Technology. Ficetola, G.F., Thuiller, W., Miaud, C. (2007): Prediction and validation of the potential global distribution of a problematic alien invasive species-the American bull- frog. Divers. Distrib. 13: 476-485. Fielding, A.H., Bell, J.F. (1997): A review of models for the assessment of prediction errors in conserva- tion presence/absence models. Environ. Conserv. 24: 38-49. Fig. 4. Similarity maps of the fuzzy numerical comparison between current distribution map and future potential distribution maps under future climatic conditions performed in MCK with similarity index of each map 93Potential effects of climate change on the distribution of invasive bullfrogs Lithobates catesbeianus in China Govindarajulu, P., Price, S., Anholt, B.R. (2006): Intro- duced bullfrogs (Rana catesbeiana) in western Can- ada: has their ecology diverged? J. Herpetol. 40: 249- 260. Graham, C.H., Hijmans, R.J. (2006): A comparison of methods for mapping species range and species rich- ness. Global Ecol. Biogeogr. 15: 578-587. Guralnick, R. (2007): Differential effects of past climate warming on mountain and flatland species distribu- tions: a multispecies North American mammal assess- ment. Global Ecol. Biogeogr. 16: 14-23. Han, D.B., Lu, Y., Wang, D.R., Zhang, Z.Z. (1991): Assay of the common nutritional compositions on the bull- frog. Zoology 12: 161-162. Hanley, J., McNeil, B. (1982): The meaning of use of the area under a receiver operating characteristic (ROC) curve. Radiology 143: 29-36. Hanselmann, R., Rodriguez, A., Lampo, M., Fajardo- Ramos, L., Aguirre, A.A., Kilpatrick, A.M., Rodriguez, J.P., Daszak, P. (2004): Presence of an emerging patho- gen of amphibians in recently introduced Rana cates- beiana in Venezuela. Biol. Conserv. 120: 115-119. Harding, J.H. (1997): Amphibians and reptiles of the great lakes region. The University of Michigan Press, Ann Arbor, Michigan. Hari, R., Livingstone, D.M., Siber, R., Burkhardt-holm, P., Güttinger, H. (2006): Consequences of climate change for water temperature and brown trout populations in alpine rivers and streams. Global Change Biol. 12: 10-26. Hersteinsson, P., Macdonald, D.W. (1992). Interspecific competition and the geographical distribution of red and arctic foxes Vulpes vulpes and Alopex lagopus. Oikos 64: 505-515. Hijmans, R.J. (2012): Cross‐validation of species distribu- tion models: removing spatial sorting bias and cali- bration with a null model. Ecology 93: 679-688. Hijmans, R.J., Cameron, S.E., Parra, J.L., Jones, P.G., Jarvis, A. (2005): Very high-resolution interpolated climate surfaces for global land areas. Internat. J. Cli- matol. 25: 1965-1978. Hobbs, R.J., Huenneke, L.F. (1992): Disturbance, diversity and invasion: implication for conversation. Conver. Biol. 6: 324-337. Hu, L.L., Zhang, H.Y., Qin, L., Yan, B.Q. (2012): Cur- rent distribution of Schisandra chinensi in China and its predicted responses to climate change. Chinese J. Appl. Ecol. 23: 2445-2450. Kiesecker, J.M., Blaustein, A.R. (1998): Effects of intro- duced bullfrogs and small mouth bass on micro- habitat use, growth, and survival of native red-legged frogs (Rana aurora). Conser. Biol. 12: 776-787. Kiritani, K. (2011): Impacts of global warming on Nezara viridula and its native congeneric species. J. Asia-Pac. Entomol. 14: 221-226. Lever, C. (2003): Naturalized amphibians and reptiles of the world. Oxford University Press, New York. Li, B., Liao, C.H., Zhang, X.D., Chen, H.L., Wang, Q., Chen, Z.Y., Gan, X.J., Wu, J.H., Zhao, B., Ma, Z.J., Cheng, X.L., Jiang, L.F., Chen, J.K. (2009): Spartina alterniflora invasions in the Yangtze River estuary, China: An overview of current status and ecosystem effects. Ecol. Eng. 35: 511-520 Li, C., Xie, F. (2004): Analysis of new cases and management counter measures of bullfrog invasion. Journal of applied and environmental biology. Biodiversity 10: 95-98. Lowe, S., Browne, M., Boudjelas, S., de Poorter, M. (2000): 100 of the world’s worst invasive alien species: a selection from the global invasive species database (Vol. 12). Auckland: Invasive Species Specialist Group. Lu, C.Y., Gu, W., Dai, A.H., Wei, H.Y. (2012): Assessing habitat suitability based on geographic information system (GIS) and fuzzy: a case study of Schisandra sphenanthera Rehd. et Wils. in Qinling Mountains, China. Ecol. Model. 242: 105-115. Maret, T.J., Snyder, J.D., Collins, J.P. (2006): Altered dry- ing regime controls distribution of endangered sala- manders and introduced predators. Biol. Conserv. 127: 129-138. MCK (2017): Map Comparison Kit. Available at: http:// mck.riks.nl/software. Nori, J., Akmentins, M., Ghirardi, R., Frutos, N., Ley- naud, G.C. (2011a): American Bullfrog invasion in Argentina: where should we take urgent measures? Biodivers. Conserv. 20: 1125-1132. Nori, J., Urbina-Cardona, J.N., Loyola, R.D., Lescano, J.N., Leynaud, G.C. (2011b): Climate change and American bullfrog invasion: what could we expect in South America? Plos One e25718 Parmesan, C., Ryholm, N., Stefanescu, C., Hill, J.K., Thomas, C.D., Descimon, H., Huntley, B., Kaila, L., Kullberg, J., Tammaru, T., Tennent, W.J., Thomas, J., Warren, M. (1999): Poleward shifts in geographi- cal range of butterfly species associated with regional warming. Nature 399: 579-583. Phillips, S. J., Dudík, M. (2008): Modeling of species dis- tributions with Maxent: new extensions and a com- prehensive evaluation. Ecography 31: 161-175. Phillips, S.J., Anderson, R.P., Schapire, R.E. (2006): Maxi- mum entropy modeling of species geographic distri- bution. Ecol. Model. 190: 231-259. Pimentel, D., Lach, L., Zuniga, R., Morrison, D. (2000): Environmental and economic costs of non-indigenous species in the United States. Bioscience 50: 53-65. 94 Li Qing Peng et alii Pyšek, P., Hulme, P.E. (2010): Biological invasions in Europe 50 years after Elton: time to sound the alarm // Richardson D M. Fifty Years of Invasion Ecol- ogy: the Legacy of Charles Elton. Oxford, UK: Wiley Blackwell. Root, T.L., Price, J.T., Hall, K.R., Schneider, S.H., Rosen- zweig, C., Pounds, J.A. (2003): Fingerprints of global warming on wild animals and plants. Nature 421: 57-40. Runyon, J.B., Butler, J.L., Friggens, M.M., Meyer, S.E., Sing, S.E. (2012): Invasive species and climate change / / Finch D.M. Climate Change in Grasslands, Shrub lands and Deserts of the Interior American West: A Review and Needs Assessment. USDA Forest Ser- vice RMRS-GTR-285, Fort Collins, CO.: U.S. Depart- ment of Agriculture, Forest Service, Rocky Mountain research Station. 97-115. Sorte, C.J.B., Ibanze, I., Blumantal, D.M. (2013): Poised to prosper across system comparison of climate change effects on native and non-native species performance. Ecol. Lett. 16: 261-270. Steven, J.P., Robert, P.A., Robert, E.S. (2006): Maximum entropy modeling of species geographic distributions. Ecol. Model. 190: 231-259. Swets, K. (1988): Measuring the accuracy of diagnostic systems. Science 240: 1285-1293. Tang, G.A., Yang, X. (2006): ArcGIS Geographic informa- tion systems spatial analysis experiments tutorial. Sci- ence Press, Beijing. Thomas, C.D., Cameron, A., Green, R.E., Bakkenes, M., Beaumont, L.J., Collingham, Y.C., Erasmus, B.F.N., de Siqueira, M.F., Grainger, A., Hannah, L., Hughes, L., Huntley, B., van Jaarsveld, A., Midgley, G.F., Miles, L., Ortega-Huerta, M.A., Peterson, A.T., Phillips, O.L., Williams, S.E. (2004): Extinction risk from climate change. Nature 427: 145-148. Thoms, C.D., Lennon, J.J. (1999): Birds extend their range northwards. Nature 399: 213. Vilà, M., Espinar, J.L., Hejda, M., Hulme, P.E., Jarošík, V., Maron, J.L., Pergl, J., Schaffner, U., Sun, Y., Pyšek, P. (2011): Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol. Lett. 14: 702-708. Visser, H., de Nijs, T. (2006): The Map Comparison Kit. Environ. Model. Softw. 21: 346-358. Walther, G.R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T.J., Fromentin, J.M., Hoegh-Guldberg, O., Bairlein, F. (2002): Ecological responses to recent cli- mate change. Nature 416: 389-395. Wang, Y.S., Xie, B.Y., Wan, F.G., Xiao, Q.M., Dai, L.Y. (2007): Application of ROC curve analysis in evaluat- ing the performance of alien species’ potential distri- bution models. Biodivers. Sci. 15: 365-372. Warren, D.L., Seifert, S.N. (2011): Ecological niche mod- eling in Maxent: the importance of model complexity and the performance of model selection criteria. Ecol. Appl. 21: 335-342. Weber, E., Li, B. (2008): Plant invasions in China: what is to be expected in the wake of economic development? Bioscience 58: 437-444. Wisz, M.S., Hijmans, R.J., Peterson, A.T., Graham, C.H., Guisan, A. (2008): Effects of sample size on the per- formance of species distribution models. Divers. Dis- trib. 14: 763-773. Wu, Z.J., Wang, Y.P., Li, Y.M. (2004): Natural population and potential hazards of bullfrog in eastern Zhejiang province, Biodiversity Science 12: 441-446. Xie, Y., Li, Z.Y., Gregg, W.P., Dianmo, L. (2001): Invasive species in China—an overview. Biodivers. Conserv. 10: 1317-1341. Yang, X.Q., Kushwaha, S.P.S., Saran, S., Xu, J., Roy, P.S. (2013): Maxent modeling for predicting the potential distribution of medicinal plant, Justicia adhatoda L. in Lesser Himalayan foothills. Ecol. Eng. 51: 83-87. Young, N., Carter, L., Evangelista, P., Jarnevich C. (2011): A MaxEnt Model v3.3.3e Tutorial (ArcGIS v10). Fort Collins, Colorado. Zhai, T.Q., Li, X.H. (2012): Climate change induced potential range shift of the Crested Ibis based on ensemble models. Acta Ecol. Sin. 32:168-177. Zhou, W., Li, M.H., Zhang, X.Y., He, J.F. (2005): Food Comparison between tadpoles of Rana catebeiana and R. chaochiaoensis from the same habitat. Zool. Res. 26: 89-95. Acta Herpetologica Vol. 15, n. 2 - December 2020 Firenze University Press Estimating abundance and habitat suitability in a micro-endemic snake: the Walser viper Gentile Francesco Ficetola1,2,*, Mauro Fanelli3, Lorenzo Garizio3, Mattia Falaschi1, Simone Tenan4, Samuele Ghielmi5, Lorenzo Laddaga6, Michele Menegon7,8, Massimo Delfino3,9. Potential effects of climate change on the distribution of invasive bullfrogs Lithobates catesbeianus in China Li Qing Peng1, Min Tang1, Jia Hong Liao1, Hai Fen Qing1, Zhen Kun Zhao1, David A. Pike2, Wei Chen1,* A bibliometric-mapping approach to identifying patterns and trends in amphibian decline research Claudio Angelini1,*, Jon Bielby2, Corrado Costa3 Food composition of a breeding population the endemic Anatolia newt, Neurergus strauchii (Steindachner, 1887) (Caudata: Salamandridae), from Bingöl, Eastern Turkey Kerim Çiçek1,*, Mustafa Koyun2, Ahmet Mermer1, Cemal Varol Tok3 Stomach histology of Crocodylus siamensis and Gavialis gangeticus reveals analogy of archosaur “gizzards”, with implication on crocodylian gastroliths function Ryuji Takasaki1,2,*, Yoshitsugu Kobayashi3 Does chronic exposure to ammonium during the pre-metamorphic stages promote hindlimb abnormality in anuran metamorphs? A comparison between natural-habitat and agrosystem frogs Sonia Zambrano-Fernández1, Francisco Javier Zamora-Camacho2,3,*, Pedro Aragón2,4 Confirming Lessona’s brown frogs distribution sketch: Rana temporaria is present on Turin Hills (Piedmont, NW Italy) Davide Marino1, Angelica Crottini2, Franco Andreone3,* Phylogenetic relationships of the Italian populations of Horseshoe Whip Snake Hemorrhois hippocrepis (Serpentes, Colubridae) Francesco Paolo Faraone1, Raffaella Melfi2, Matteo Riccardo Di Nicola3, Gabriele Giacalone4, Mario Lo Valvo5* First karyological analysis of the endemic Malagasy phantom gecko Matoatoa brevipes (Squamata: Gekkonidae) Marcello Mezzasalma1,2,*, Fabio M. Guarino3, Simon P. Loader1, Gaetano Odierna3, Jeffrey W. Streicher1, Natalie Cooper1 Notes on sexual dimorphism, diet and reproduction of the false coral snake Oxyrhopus rhombifer Duméril, Bibron & Duméril, 1854 (Dipsadidae: Pseudoboini) from coastal plains of Subtropical Brazil Fernando M. Quintela1,*, Felipe Caseiro¹, Daniel Loebmann¹