Pets or predators? climate change and invasion risk of red-eared slider (Trachemys scripta elgans)

Authors

  • SM Sehgal Foundation Centre for Biodiversity and Conservation, Ashoka Trust for Research in Ecology and the Environment (ATREE), Royal Enclave, Srirampura, Jakkur PO, Bangalore – 560064, Karnataka
  • Zoological Survey of India, Reptilia Section, Indian Museum Campus, Kolkata, West Bengal – 700016
  • SM Sehgal Foundation Centre for Biodiversity and Conservation, Ashoka Trust for Research in Ecology and the Environment (ATREE), Royal Enclave, Srirampura, Jakkur PO, Bangalore – 560064, Karnataka
  • SM Sehgal Foundation Centre for Biodiversity and Conservation, Ashoka Trust for Research in Ecology and the Environment (ATREE), Royal Enclave, Srirampura, Jakkur PO, Bangalore – 560064, Karnataka

DOI:

https://doi.org/10.26515/rzsi/v123/i2/2023/172493

Keywords:

Climate Change, IAS, Native Biodiversity, Niche Shift, Policy

Abstract

Red-eared slider (Trachemys scripta elegans) is one of the popular turtles in the pet trade worldwide and is known to be the worst invasive species in several countries. Several records of T. s. elegans exist from India, indicating its possible expansion in the natural habitat but lack a comprehensive investigation. Using the ecological niche modelling tools, we here predict the possible expansion with changing climatic scenarios and test the hypothesis of niche conservatism. Our study indicates a significant increase in the suitable areas of RES that also correlates with the high diversity regions of Indian chelonians. We also discuss the gaps in existing laws and policies in India handling exotic/invasive species and recommend policy and management suggestions.

Downloads

Download data is not yet available.

Downloads

Published

2023-11-03

How to Cite

N. A. Aravind, Mohopatra, P. P., Bhat, H. N. P., & Narayanan, S. (2023). Pets or predators? climate change and invasion risk of red-eared slider (<I>Trachemys scripta elgans</I>). Records of the Zoological Survey of India, 123(2), 185–197. https://doi.org/10.26515/rzsi/v123/i2/2023/172493

Issue

Section

Articles

References

Ahmad, R., Khuroo, A.A. and Hamid, M. 2019. Predicting invasion potential and niche dynamics of Parthenium hysterophorus (Congress grass) in India under projected climate change. Biodiversity and Conservation, 28: 2319-2344. https://doi.org/10.1007/ s10531-019-01775-y

Aiello-Lammens, M.E., Boria, R.A., Radosavljevic, A., Vilela, B. and Anderson, R.P. 2015. spThin: An R package for spatial thinning of species occurrence records for use in ecological niche models. Ecography, 38: 541-545. https://doi.org/10.1111/ecog.01132

Allouche, O., Tsoar, A., and Kadmon, R. 2006. Assessing the accuracy of species distribution models: prevalence, kappa and the True Skill Statistic (TSS). Journal of Applied Ecology, 43(6): 1223-1232. https://doi.org/10.1111/j.1365-2664.2006.01214.x

Anonymous. 2009. Animal Pest Alert, Red-eared Slider, No 6/2009, Department of Agriculture and Food, Government of Australia.

Barhadiya, G., Ghosh, C., and Singh, S. 2021. Invasive red-eared sliders, Trachemys scripta elegans (Weid, 1838), in urban wetlands of Delhi, India. Reptiles and Amphibians, 28(1): 15-17. https://doi.org/10.17161/randa.v28i1.15277

Beaumont, L.J., Graham, E., Duursma, D.E., Wilson, P.D., Cabrelli, A., Baumgartner, J.B., Hallgren, W., Esperón-Rodríguez, M., Nipperess, D.A., Warren, D.L. and Laffan, S.W. 2016. Which species distribution models are more (or less) likely to project broadscale, climate-induced shifts in species ranges? Ecological Modelling, 42: 135-146. https://doi.org/10.1016/j.ecolmodel.2016.10.004

Bomford, M. 2008. Risk assessment models for establishment of exotic vertebrates in Australia and New Zealand. Invasive Animals Cooperative Research Centre, Canberra.

Born, W., Rauschmayer, F., and Bräuer, I. 2005. Economic evaluation of biological invasions—A survey. Ecological Economics, 55: 321- 336. https://doi.org/10.1016/j.ecolecon.2005.08.014

Bosch, S., Tauxe, R.V., and Behravesh, C.B. 2016. Turtle-associated Salmonellosis, United States, 2006-2014. Emerging Infectious Diseases, 22(7): 1149-1155. https://doi.org/10.3201/eid2207.150685

Breiman, L. 2001. Random forests. Machine Learning, 45(1): 5-32. https://doi.org/10.1023/A:1010933404324

Breiman, L., Friedman, J.H., Olshen, R.A., and Stone, C.J. 1984. Classification and regression trees (The Wadsworth Statistics/Probability Series) Chapman and Hall. New York ( pp. 1-358).

Bringsøe, H. 2006. NOBANIS – Invasive Alien Species Fact Sheet – Trachemys scripta. http://www.nobanis.org/files/factsheets/ Trachemys_scripta.pdf

Broennimann, O., Treier, U.A., Müller-Schärer, H., Thuiller, W., Peterson, A.T. and Guisan, A. 2007. Evidence of climatic niche shift during biological invasion. Ecological Letters, 10: 701-709. https://doi.org/10.1111/j.1466-8238.2011.00698.x

Broennimann, O., Fitzpatrick, M.C., Pearman, P.B., Petitpierre, B., Pellissier, L., Yoccoz, N.G., Thuiller, W., Fortin, M.J., Randin, C., Zimmermann, N.E. and Graham, C.H. 2012. Measuring ecological niche overlap from occurrence and spatial environmental data. Global Ecology and Biogeography, 21(4): 481-497. https://doi.org/10.1111/j.1461-0248.2007.01060.x

Buhlmann, K.A., Akre, T.S.B., Iverson, J.B., Karapatakis, D., Mittermeier, R.A., Georges, A., Rhodin, A.G.J., Van Dijk, P.P., and Gibbons, J.W. 2009. A global analysis of tortoise and freshwater turtle distributions with identification of priority conservation areas. Chelonian Conservation and Biology, 8 (2): 116-149. https://doi.org/10.2744/CCB-0774.1

Cadi, A. and Joly, P. 2003. Competition for basking places between the endangered European pond turtle (Emys orbicularis galloitalica) and the introduced red-eared slider (Trachemys scripta elegans). Canadian Journal of Zoology, 81: 1392-1398. https://doi. org/10.1139/z03-108

Cadi, A. and Joly, P. 2004. Impact of the introduction of the red-eared slider (Trachemys scripta elegans) on survival rates of the European pond turtle (Emys orbicularis).Biodiversity and Conservation,13: 2511-2518.https://doi.org/10.1023/B:BIOC.0000048451.07820.9c

Cann, J. 1998. Australian Freshwater Turtles. Beaumont Publishing, Singapore, 292pp.

Chaudhuri, A., Banerjee, A., Chowdhury, S. and Deuti, K. 2019. Report of red-eared slider turtle (Trachemys scripta elegans) from a wetland near Kolkata, West Bengal, India. Herpetological Bulletin, 146: 41-42.

Cohen, M.L, Potter, M., Pollard, R. and Feldman, R.A. 1980. Turtle-associated salmonellosis in the United States: Effect of public health action, 1970 to 1976. Journal of the American Medical Association, 243: 1247-1249. https://doi.org/10.1001/ jama.1980.03300380027016

Cowie, R.H. 2000. Non-indigenous land and freshwater molluscs in the islands of the Pacific: conservation impacts and threats (G. Sherley ed.). Invasive species in the Pacific: A technical review and draft regional Strategy. South Pacific Regional Environment Programme, Australia (pp. 143-166)

da Mata, R.A., Tidon, R., Côrtes, L.G., De Marco, J.R. and Diniz-Filho, J.A.F. 2010. Invasive and flexible: niche shift in the drosophilid Zaprionus indianus (Insecta, Diptera). Biological Invasions, 12: 1231-1241. https://doi.org/10.1007/s10530-009-9542-0

Datta, A., Schweiger, O. and Kühn, I. 2019. Niche expansion of the invasive plant species Ageratina adenophora despite evolutionary constraints. Journal of Biogeography, 46(7): 1306-1315. https://doi.org/10.1111/jbi.13579

Di Cola, V., Broennimann, O., Petitpierre, B., Breiner, F.T., D’amen, M., Randin, C., Engler, R., Pottier, J., Pio, D., Dubuis, A. and Pellissier, L. 2017. Ecospat: An R package to support spatial analyses and modeling of species niches and distributions. Ecography, 40(6): 774-787. https://doi.org/10.1111/ecog.02671

Doherty T.S., Glen, A.S., Nimmo, D.G., Ritchie, E.G. and Dickman, C.R. 2016. Invasive predators and global biodiversity loss. Proceedings of National Academy of Sciences, 113(40): 11261-11265. https://doi.org/10.1073/pnas.1602480113

Fielding, A.H. and Bell, J.F. 1997. A review of methods for the assessment of prediction errors in conservation presence/absence models. Environmental Conservation, 24(1): 38-49. https://doi.org/10.1017/S0376892997000088

Fitzpatrick, M.C., Weltzin, J.F., Sanders, N.J. and Dunn, R.R. 2007. The biogeography of prediction error: why does the introduced range of the fire ant over-predict its native range. Global Ecology and Biogeography, 16: 24-33. https://doi.org/10.1111/j.1466- 8238.2006.00258.x

Friedman, J.H. 1991. Multivariate adaptive regression splines. The Annals of Statistics, 19(1): 1-67. https://doi.org/10.1214/ aos/1176347963

Friedman, J.H. 2001. Greedy function approximation: a gradient boosting machine. The Annals of Statistics, 29(5): 1189-1232. https:// doi.org/10.1214/aos/1013203451

González-Moreno, P., Jeff. D., Richardson, D. and Vilà, M. 2014. Beyond climate: Disturbance niche shifts in invasive species. Global Ecology and Biogeography, 24 (3): 360-370. https://doi.org/10.1111/geb.12271

Goode J. and Russell J. 1968. Incubation of eggs of three species of chelid tortoises, and notes on their embryological development. Aust. J. Zool. 16: 749-761.

Guisan, A., Petitpierre, B., Broennimann, O., Daehler, C. and Kueffer, C. 2014. Unifying niche shift studies: Insights from biological invasions. Trends in Ecology and Evolution, 29: 260-269. https://doi.org/10.1016/j.tree.2014.02.009

Hays, D.W., Mcallister, K.R., Richardson, S.A. and Stinson, D.W. 1999. Washington State recovery plan for the western pond turtle. Washington Department of Fish and Wildlife. Olympia (pp. 66).

HerpMapper. 2023. HerpMapper - A Global Herp Atlas and Data Hub. Iowa, U.S.A. Available http://www.herpmapper.org. (Accessed: 21-03-2023).

Hijmans, R., Cruz, M., Rojas, E. and Guarino, L. 2001. DIVA-GIS version 1.4: A geographic information system for the analysis of biodiversity data, manual. DIVA-GIS. https://www.diva-gis.org/docs/DIVA-GIS_manual_7.pdf

Hmar, G.Z., Lalbiakzuala, Lalmuansanga, Zote, D., Vanlalhruaia, Ramengmawii, H.B., Decemson, H., Das, K. and Lalremsanga, H.T. 2021. First record of the exotic Red-eared Slider, Trachemys scripta elegans (Wied 1838) (Emydidae), from Mizoram, India. Reptiles and Amphibians, 28 (1): 52-53. https://doi.org/10.17161/randa.v28i1.15310

iNaturalist. 2022. Red-eared slider (Trachemys scripta elgans). Available at https://www. inaturalist.org. Accessed on 8 February.

ISSG. 2011. Global Invasive Species Database (GISD). Invasive Species Specialist Group of the IUCN Species Survival Commission. http://www.issg.org/database

Jadhav, T., Sawant, N.S. and Shyama, S.K. 2018. First report on presence and status of introduced invasive species Red-eared Slider, Trachemys scripta elegans in Goa, India. NeBIO, 9 (2): 177-179.

Lauzeral, C., Leprieur, F., Beauchard, O., Duron, Q., Oberdorff, T. and Brosse, S. 2011. Identifying climatic niche shifts using coarsegrained occurrence data: A test with non-native freshwater fish. Global Ecology and Biogeography, 20: 407-414. https://doi. org/10.1111/j.1466-8238.2010.00611.x

Lever, C. 2003. Naturalised Reptiles and Amphibians of the World. Oxford University Press, New York.

Li, Y., Liu, X., Li, X., Petitpierre, B. and Guisan, A. 2014. Residence time, expansion toward the equator in the invaded range and native range size matter to climatic niche shifts in non-native species. Global Ecology and Biogeography, 23: 1094-1104. https://doi. org/10.1111/geb.12191

Lindeman, P.V. 1999. Aggressive interactions during basking among four species of emydid turtles. Journal of Herpetology, 33: 214–219.

Liu, C., Wolter, C., Xian, W. and Jeschke, J.M. 2020. Most invasive species largely conserve their climatic niche. Proceedings of National Academy of Sciences, 117 (38): 23643-23651. https://doi.org/10.1073/pnas.2004289117

Lockwood, J.L., Welbourne, D.J., Romagosa, C.M., Cassey, P., Mandrak, N.E., Strecker, A., Leung, B., Stringham, O.C., Udell, B., Episcopio-Sturgeon, D.J., Tlusty, M.F., Sinclair, J., Springborn, M.R., Pienaar, E.F., Rhyne, A.L. and Keller, R. 2019. When pets become pests: The role of the exotic pet trade in producing invasive vertebrate animals. Frontiers in Ecology and Environment, 17: 323-330. https://doi.org/10.1002/fee.2059

López, J.L.B., Estrada, C.E.E., Méndez, U.R., Rodríguez, J.J.S., Goyenechea, I.G.M., Cerón, J.M.C. 2017. Evidence of niche shift and invasion potential of Lithobates catesbeianus in the habitat of Mexican endemic frogs. PLoS ONE, 12:1–15. https://doi. org/10.1371/journal.pone.0185086

Lososová, Z., Chytrý, M., Tichý, L., Danihelka, J., Fajmon, K., Hájek, O., Kintrová, K., Láníková, D., Otýpková, Z. and Rehoˇrek, V. 2021. Biotic homogenization of Central European urban floras depends on residence time of alien species and habitat types. Biological Conservation, 145: 179-184. https://doi.org/10.1016/j.biocon.2011.11.003

Lowe S., Browne, M., Boudjelas, S. and De Poorter, M. 2000. 100 of the World’s worst invasive alien species. Global Invasive Species database. (pp. 12).

Manzoor, S.A., Griffiths, G., Obiakara, M.C., Esparza‐Estrada, C.E. and Lukac, M. 2020. Evidence of ecological niche shift in Rhododendron ponticum (L.) in Britain: Hybridisation as a possible cause of rapid niche expansion. Ecology and Evolution, 10 (4): 2040-2050. https://doi.org/10.1002/ece3.6036

Mccullagh, P. and Nelder, J.A. 1989. Generalized linear models. 2nd Edition. Chapman and Hall, London. https://doi.org/10.1007/978- 1-4899-3242-6

Medley, K.A. 2010. Niche shifts during the global invasion of the Asian tiger mosquito, Aedes albopictus Skuse (Culicidae), revealed by reciprocal distribution models. Global Ecology and Biogeography, 19: 122-133. https://doi.org/10.1111/j.1466-8238.2009.00497.x

Mohanty, N.P. and Measey, J. 2019. The global pet trade in amphibians: species traits, taxonomic bias, and future directions. Biodiversity and Conservation, 28: 3915-3923. https://doi.org/10.1007/s10531-019-01857-x

Mugo, R. and Saitoh, S.I. 2020. Ensemble modelling of skipjack tuna (Katsuwonus pelamis) habitats in the western north pacific using satellite remotely sensed data; a comparative analysis using machine-learning models. Remote Sensing, 12 (16): 2591. https://doi. org/10.3390/rs12162591

Munjpara, S. 2014. Will the exotic red-eared slider turtle Trachemys scripta elegans become invasive in India? Jalaplavit, 5 (2): 47-48.

Naimi, B. and Araújo, M.B. 2016. sdm: a reproducible and extensible R platform for species distribution modelling. Ecography, 39 (4): 368-375. https://doi.org/10.1111/ecog.01881

O’Keefe, S. 2005. Investing in conjecture: eradicating the red-eared slider in Queensland. 13th Australasian Vertebrate Pest Conference, Wellington, New Zealand.

Paini, D.R., Sheppard, A.W., Cook, D.C., De Barro, P.J., Worner, S.P. and Thomas, M.B. 2016. Global threat to agriculture from invasive species. Proceedings of Natural Academy of Science, 113 (27): 7575-7579. https://doi.org/10.1073/pnas.1602205113

Pearson, S.H., Avery, H.W. and Spotilaa, J.R. 2015. Juvenile invasive red-eared slider turtles negatively impact the growth of native turtles: Implications for global freshwater turtle populations. Biodiversity Conservation, 186: 115-121. https://doi.org/10.1016/j. biocon.2015.03.001

Petitpierre, B., Kueffer, C., Broennimann, O., Randin, C., Daehler, C. and Guisan, A. 2012. Climatic niche shifts are rare among terrestrial plant invaders. Science, 335 (6074): 1344-1348. https://doi.org/10.1126/science.1215933

Phillips, S.J., Anderson, R.P. and Schapire, R.E. 2006. Maximum entropy modelling of species geographic distributions. Ecological Modelling, 190 (3-4): 231-259. https://doi.org/10.1016/j.ecolmodel.2005.03.026

Polo-Cavia, N., López, P. and Martín, J. 2010. Competitive interactions during basking between native and invasive freshwater turtle species. Biological Invasions, 12: 2141-2152. https://doi.org/10.1007/s10530-009-9615-0

Powell, R., Conant, R. and J.T. Collins. 2016. Peterson Field Guide to Reptiles and Amphibians of Eastern and Central North America. 4th edition. Houghton Mifflin Harcourt, Boston, Massachusetts. xiii +494 pp.

Pragatheesh, A., Deepak, V., Girisha, H.V. and Tomar, M.S. 2021. A looming exotic reptile pet trade in India: patterns and knowledge gaps. Journal of Threatened Taxa, 13 (6): 18518-18531. https://doi.org/10.11609/jott.6998.13.6.18518-18531

Prevot-Julliard, A., Gousset, E., Archinard, C., Cadi, A. and Girondot, M. 2007. Pets and invasion risks: is the slider turtle strictly carnivorous? Amphibia-Reptilia, 28: 139-143. https://doi.org/10.1163/156853807779799036

Ramsay, N.F., Ng, P.K., O’Riordan, R.M., Chou, L.M. 2007. The red-eared slider (Trachemys scripta elegans) in Asia: a review. In: Gherardi F (Ed.) Biological invaders in inland waters: Profiles, distribution, and threats. Springer Netherlands, Dordrecht: 161– 174. https://doi.org/10.1007/978-1-4020-6029-8_8

Rejmánek, M., Richardson, D.M. and Pyšek, P. 2013. Plant Invasions and Invasibility of plant communities, in vegetation ecology. (E. van der Maarel, and J. Franklin eds.) John Wiley & Sons Ltd (pp. 387-424). https://doi.org/10.1002/9781118452592.ch13

Resasco, J., Tuff, K.T., Cunningham, S.A., Melbourne, B.A., Hicks, A.L., Newsome, S.D. and Davies, K.F. 2018. Generalist predator’s niche shifts reveal ecosystem changes in an experimentally fragmented landscape. Ecography, 41: 1209-1219. https://doi.org/10.1111/ecog.03476

Rodder, D. and Engler, J.O. 2011. Quantitative metrics of overlaps in Grinnellian niches: Advances and possible drawbacks. Global Ecology and Biogeography, 20: 915-927. https://doi.org/10.1111/j.1466-8238.2011.00659.x

Rodder, D., Lotters, S. 2009. Niche shift versus niche conservatism? Climatic characteristics of the native and invasive ranges of the Mediterranean house gecko (Hemidactylus turcicus). Global Ecology and Biogeography, 18: 674-687. https://doi.org/10.1111/ j.1466-8238.2009.00477.x

Rzeżutka, A., Kaupke, A. and Gorzkowski, B. 2020. Detection of Cryptosporidium parvum in a red-eared slider turtle (Trachemys scripta elegans), a noted invasive alien species, captured in a rural aquatic ecosystem in Eastern Poland. Acta Parasitologica, 65: 768-773. https://doi.org/10.2478/s11686-020-00180-8

Salerno, A.P. and van den Burg, M.P. 2021. Predation of a live duckling (Anas platyrhynchos) by Trachemys scripta: concerns for native avifauna in the non-native range of this widely established turtle? Herpetological Notes, 14: 45-48.

Sandilyan, S., Meenakumari, B., Babu, C.R. and Mandal, R. 2018. Invasive alien species of India. National Biodiversity Authority, Chennai.

Sankaran K V, Khuroo A A, Raghavan R, Molur S, Kumar B, Wong L J, Pagad S. 2021. Global Register of Introduced and Invasive Species - India. Version 1.5. Invasive Species Specialist Group ISSG. Checklist dataset. https://doi.org/10.15468/uvnf8m accessed via GBIF.org on 2023-10-17.

Sarma, R.R., Munsi, M. and Aravind, N.A. 2015. Effect of climate change on invasion risk of giant African snail (Achatina fulica Férussac, 1821: Achatinidae) in India. PLoS One, 10 (11): Article e0143724. https://doi.org/10.1371/journal.pone.0143724

Scalera, R. 2006. Trachemys scripta. DAISIE (Delivering Alien Invasive Species Inventories for Europe). Available at: http://www. europe-aliens.org/(23.08.2013).

Schoener, T.W. 1970. Nonsynchronous spatial overlap of lizards in patchy habitats. Ecology, 51 (3): 408-418. https://doi. org/10.2307/1935376

Stam, F., Romkens, T.E., Hekker, T.A. and Smulders, Y.M. 2003. Turtle-associated human salmonellosis.Clinical and Infectious Diseases,37: 167-169. https://doi.org/10.1086/379612

Stanford, C.B., Iverson, J.B., Rhodin, A.G.J., van Dijk, P.P., Mittermeier, R.A., Kuchling, G., Berry, K.H., Bertolero, A., Bjorndal, K.A., Blanck, T.E.G., Buhlmann, K.A., Burke, R.L., Congdon, J.D., Diagne, T., Edwards, T., Eisemberg, C.C., Ennen, J.R., ForeroMedina, G., Frankel, M. and Walde, A.D. 2020. Turtles and tortoises are in trouble. Current Biology, 30 (12): R721-R735. https:// doi.org/10.1016/j.cub.2020.04.088

Stull, J.W., Peregrine, A.S., Sargeant, J.M. and Weese, J.S. 2012. Household knowledge, attitudes and practices related to pet contact and associated zoonoses in Ontario, Canada. BMC Public Health, 12: 553. https://doi.org/10.1186/1471-2458-12-553

Swets, J.A. 1988. Measuring the accuracy of diagnostic systems. Science, 240 (4857): 1285-1293. https://doi.org/10.1126/science.3287615

Vilcinskas, A. 2019. Pathogens associated with invasive or introduced insects threaten the health and diversity of native species. Current Opinion in Insect Science, 33: 43-48, https://doi.org/10.1016/j.cois.2019.03.004

Vyas, R. 2019. Distribution of Invasive Red-eared Sliders, Trachemys scripta (Testudines: Emydidae) in the Wetlands of Gujarat State, India. India. Reptiles and Amphibians, 26: 145-150. https://doi.org/10.17161/randa.v26i2.14389

Vyas, R. 2020. A Captive Study of interactions between the invasive red-eared slider, Trachemys scripta elegans (Wied 1838) and Native Indian Turtles. Reptiles and Amphibians, 27 (2), 318-323. https://doi.org/10.17161/randa.v27i2.14487

Warren, D.L., Glor, R.E. and Turelli, M. 2008. Environmental niche equivalency versus conservatism: quantitative approaches to niche evolution. Evolution, 62 (11): 2868-2883. https://doi.org/10.1111/j.1558-5646.2008.00482.x

Williams, T. 1999. The Terrible Turtle Trade. Audubon, 101 (44): 46–48.