Abstract
The impact of non-native species, together with their pervasiveness, necessitates a means of identifying which species are most likely to pose an elevated risk of becoming invasive. This is amongst the first applications of the Aquatic Species Invasiveness Screening Kit (AS-ISK) decision support tool in Southeast Asia, and specifically for Vietnam. In total, 30 extant and horizon non-native aquatic species were screened for their potential invasiveness in Vietnam. A threshold score of 6.75 was identified for distinguishing between species likely to pose a high and low-to-medium risk of becoming invasive in Vietnam for both the basic risk assessment (BRA) and the climate change assessment (BRA + CCA) components of the screening process. However, the absence of nationally-consistent predictions on climate change impacts in Vietnam restricted the applicability of the climate change assessment component. Based on the BRA threshold, of the 30 species screened, 25 were classified as high risk, four as medium risk, and one as low risk. For the BRA, the highest-scoring species were Hypostomus plecostomus, Pomacea canaliculata and Lithobates catesbeianus. This study reliably identified and discriminated between non-invasive and potentially invasive aquatic species in Vietnam, thereby providing appropriate AS-ISK score thresholds with which to guide policy and decision-making. This suggests that the AS-ISK could be successfully employed to screen non-native aquatic species in other parts of Southeast Asia.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Change history
10 April 2021
A Correction to this paper has been published: https://doi.org/10.1007/s10530-021-02498-4
References
Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA for PRIMER: guide to software and statistical methods. PRIMER-E, Plymouth
Armbruster JW (2004) Phylogenetic relationships of the suckermouth armoured catfishes (Loricariidae) with emphasis on the Hypostominae and the Ancistrinae. Zool J Linn Soc 141:1–80. https://doi.org/10.1111/j.1096-3642.2004.00109.x
Barlow J, França F, Gardner TA, Hicks CC, Lennox GD, Berenguer E, Castello L, Economo EP, Ferreira J, Guénard B, Gontijo Leal C, Isaac V, Lees AC, Parr CL, Wilson SK, Young PJ, Graham NAJ (2018) The future of hyperdiverse tropical ecosystems. Nature 559:517–526. https://doi.org/10.1038/s41586-018-0301-1
Bewick V, Cheek L, Ball J (2004) Statistics review 13: receiver operating characteristic curves. Crit Care 8:508–512. https://doi.org/10.1186/cc3000
Bilge G, Filiz H, Yapıcı S, Tarkan AS, Vilizzi L (2019) A risk screening study on the potential invasiveness of Lessepsian fishes in the south-western coasts of Anatolia. Acta Ichthyol Piscatry 49:23–31. https://doi.org/10.3750/AIEP/02422
Branquart E (2009) Guidelines for environmental impact assessment and list classification of non-native organisms in Belgium. Version 2.6. http://ias.biodiversity.be/documents/ISEIA_protocol.pdf. Accessed 19 May 2020
Buckley YM, Catford J (2015) Does the biogeographic origin of species matter? Ecological effects of native and non-native species and the use of origin to guide management. J Ecol 104:4–17. https://doi.org/10.1111/1365-2745.12501
Cacot P, Lazard J (2009) La domestication des poissons du Mékong: les enjeux et le potentiel aquacole. Cah Agric 18:125–135. https://doi.org/10.1684/agr.2009.0304
Carlsson NOL, Brönmark C, Hansson L-A (2004) Invading herbivory: the golden apple snail alters ecosystem functioning in Asian wetlands. Ecology 85:1575–1580. https://doi.org/10.1890/03-3146
Clarke SA, Vilizzi L, Lee L, Wood LE, Cowie WJ, Burt JA, Mamiit RJ, Hassina A, Davison PI, Fenwick GV, Harmer R, Skóra ME, Kozic S, Aislabie LR, Kennerley A, Le Quesne WJF, Copp GH, Stebbing PD (2020) Identifying potentially invasive non-native marine and brackish water species for the Arabian Gulf and Sea of Oman. Glob Change Biol 26:2081–2092. https://doi.org/10.1111/GCB.14964
Copp GH, Vilizzi L, Mumford J, Fenwick GV, Godard MJ, Gozlan RE (2009) Calibration of FISK, an invasiveness screening tool for non-native freshwater fishes. Risk Anal 29:457–467. https://doi.org/10.1111/j.1539-6924.2008.01159.x
Copp GH, Vilizzi L, Tidbury H, Stebbing PD, Tarkan AS, Moissec L, Goulletquer Ph (2016a) Development of a generic decision-support tool for identifying potentially invasive aquatic taxa: AS-ISK. Manag Biol Invasions 7:343–350. https://doi.org/10.3391/mbi.2016.7.4.04
Copp GH, Godard MJ, Russell IC, Peeler EJ, Gherardi F, Tricarico E, Miossec L, Goulletquer P, Almeida D, Britton JR, Vilizzi L, Mumford J, Williams C, Reading A, Rees EMA, Merino-Aguirre R (2016b) A preliminary evaluation of the European Non-native Species in Aquaculture Risk Assessment Scheme applied to species listed on Annex IV of the EU Alien Species Regulation. Fish Manag Ecol 23:12–20. https://doi.org/10.1111/fme.12076
Copp GH, Vilizzi L, Wei H, Li S, Piria M, Al-Faisal AJ, Almeida D, Atique U, Al-Wazzan Z, Bakiu R, Bašić T, Bui TD, Canning-Clode J, Castro N, Chaichana R, Çoker T, Dashinov D, Ekmekçi FG, Erős T, Ferincz Á, Ferreira T, Giannetto D, Gilles AS, Głowacki Ł, Goulletquer Ph, Interesova E, Iqbal S, Jakubčinová K, Kanongdate K, Kim J-E, Kopecký O, Kostov V, Koutsikos N, Kozic S, Kristan P, Kurita Y, Lee H-G, Leuven RSEW, Lipinskaya T, Lukas J, Marchini A, González Martínez AI, Masson L, Memedemin D, Moghaddas SD, Monteiro J, Mumladze L, Naddafi R, Năvodaru I, Olsson KH, Onikura N, Paganelli D, Pavia RT, Perdikaris C, Pickholtz R, Pietraszewski D, Povž M, Preda C, Ristovska M, Rosíková K, Santos JM, Semenchenko V, Senanan W, Simonović P, Smeti E, Števove B, Švolíková K, Ta KAT, Tarkan AS, Top N, Tricarico E, Uzunova E, Vardakas L, Verreycken H, Zięba G, Mendoza R (2021) Speaking their language – Development of amultilingual decision-support tool for communicating invasive species risks to decision makers and stakeholders. Environ Model Softw 135:104900. https://doi.org/10.1016/j.envsoft.2020.104900
Dao HT, Beattie GAC, Watson GW, Pham VL, Nguyen VL, Le DK, Nguyen TH, Nguyen DV, Holford P (2018) Citrus diaspidids in Viet Nam: new, and confirmation of previous, records based on morphological and molecular identification of taxa. J Asia-Pac Entomol 21:81–96. https://doi.org/10.1016/j.aspen.2017.09.010
Di Marco M, Chapman S, Althor G, Kearney S, Besancon C, Butt N, Maina JM, Possingham HP, Rogalla von Bieberstein K, Venter O, Watson JEM (2017) Changing trends and persisting biases in three decades of conservation science. Glob Ecol Conserv 10:32–42. https://doi.org/10.1016/j.gecco.2017.01.008
Dodd JA, Vilizzi L, Bean CW, Davison PI, Copp GH (2019) At what spatial scale should risk screenings of translocated freshwater fishes be undertaken—river basin district or climo-geographic designation? Biol Conserv 230:122–130. https://doi.org/10.1016/j.biocon.2018.12.002
Drolet D, DiBacco C, Locke A, McKenzie CH, McKindsey CW, Moore AM, Webb JL, Therriault TW (2016) Evaluation of a new screening-level risk assessment tool applied to non-indigenous marine invertebrates in Canadian coastal waters. Biol Invasions 18:279–294. https://doi.org/10.1007/s10530-015-1008-y
Drury R (2009) Reducing urban demand for wild animals in Vietnam: examining the potential of wildlife farming as a conservation tool. Conserv Lett 2:263–270. https://doi.org/10.1111/j.1755-263X.2009.00078.x
Early R, Bradley BA, Dukes JS, Lawler JJ, Olden JD, Blumenthal DM, Gonzalez P, Grosholz ED, Ibañez I, Miller LP, Sorte CJB, Tatem AJ (2016) Global threats from invasive alien species in the twenty-first century and national response capacities. Nat Commun 7:12485. https://doi.org/10.1038/ncomms12485
Eaton JA, Nguyen MDT, Willemsen M, Lee J, Chng SCL (2017) Caged in the city: an inventory of birds for sale in Ha Noi and Ho Chi Minh City, Viet Nam. TRAFFIC, Southeast Asia Regional Office, Petaling Jaya, Selangor, Malaysia. www.traffic.org/site/assets/files/1580/caged-in-the-city.pdf. Accessed 16 May 2020
Ellender BR, Weyl OL (2014) A review of current knowledge, risk and ecological impacts associated with non-native freshwater fish introductions in South Africa. Aquat Invasions 9:117–132. https://doi.org/10.3391/ai.2014.9.2.01
Fausch KD, Power ME, Murakami M (2002) Linkages between stream and forest food webs: Shigeru Nakano’s legacy for ecology in Japan. Trends Ecol Evol 17:429–434. https://doi.org/10.1016/S0169-5347(02)02572-7
Glamuzina B, Tutman P, Nikolić V, Vidović Z, Pavličević J, Vilizzi L, Copp GH, Simonović P (2017) Comparison of taxon-specific and taxon-generic risk screening tools to identify potentially invasive non-native fishes in the River Neretva catchment (Bosnia and Herzegovina and Croatia). River Res Appl 33:670–679. https://doi.org/10.1002/rra.3124
Haubrock PJ, Copp GH, Johovic I, Balzani P, Inghilesi AF, Nocita A, Tricarico E (2021) North American channel catfish, Ictalurus punctatus: a neglected but potentially invasive freshwater fish species. Biol Invas. https://doi.org/10.1007/s10530-021-02459-x
Hoover JJ, Killgore KJ, Cofranceso AF (2004) Suckermouth catfishes: threats to aquatic ecosystems of the United States? Aquat Nuisance Species Res Program Bull 4:1–13
Hosmer DW Jr, Lemeshow S, Sturdivant RX (2013) Applied logistic regression, 3rd edn. Wiley, NJ, USA
Interesova E, Vilizzi L, Copp GH (2020) Risk screening of the potential invasiveness of non-native freshwater fishes in the River Ob basin (West Siberian Plain, Russia). Reg Environ Change. https://doi.org/10.1007/s10113-020-01644-3
IPBES (2019) Global assessment report on biodiversity and ecosystem services of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services. In: Brondizio ES, Settele J, Díaz S, Ngo HT (eds) IPBES Secretariat, Bonn, Germany
IPCC (2005) Guidance notes for lead authors of the IPCC fourth assessment report on addressing uncertainties. Intergovernmental Panel on Climate Change, WMO & UNEP. https://www.ipcc.ch/site/assets/uploads/2018/02/ar4-uncertaintyguidancenote-1.pdf. Accessed 16 May 2020
Joshi RC, Cowie RH, Sebastian LS (eds) (2017) Biology and management of invasive apple snails. Philippine Rice Research Institute (PhilRice), Maligaya, Science City of Muñoz, Nueva Ecija
Killi N, Tarkan AS, Kozic S, Copp GH, Davison PI, Vilizzi L (2020) Risk screening of the potential invasiveness of non native jellyfishes in the Mediterranean Sea. Mar Poll Bull 150:110728. https://doi.org/10.1016/j.marpolbul.2019.110728
Law on Biodiversity (2008) https://portal.gms-eoc.org/uploads/resources/953/attachment/Vietname_Law_on_Boidiversity_28_Nov_2008_En.pdf. Accessed 16 May 2020
Law on Environmental Protection (2014) https://www.elaw.org/vietnam-environmental-impact-assessment-eia-laws. Accessed 16 May 2020
Lawson LL Jr, Hill JE, Vilizzi L, Hardin S, Copp GH (2013) Revisions of the Fish Invasiveness Screening Kit (FISK) for its application in warmer climatic zones, with particular reference to peninsular Florida. Risk Anal 33:1414–1431. https://doi.org/10.1111/j.1539-6924.2012.01896.x
Le TB, Truong QB (2016) Quick assessment of the invasiveness of non-native plant species by using eco-physiological parameters in Tram Chim National Park, Vietnam. Weed Biol Manag 16:177–185. https://doi.org/10.1111/wbm.12108
Li S, Chen J, Wang X, Copp GH (2017) Invasiveness screening of non-native fishes for the middle reach of the Yarlung Zangbo River, Tibetan Plateau, China. River Res Appl 33:1439–1444. https://doi.org/10.1002/rra.3196
Lu D (2019) Peirce’s philosophy of communication and language communication. Semiotica 230:407–423. https://doi.org/10.1515/sem-2017-0164
Matsuzaki SS, Kadoya T (2015) Trends and stability of inland fishery resources in Japanese lakes: introduction of exotic piscivores as a driver. Ecol Appl 25:1420–1432. https://doi.org/10.1890/13-2182.1
McElwee P (2010) The social dimensions of adaptation to climate change in Vietnam. Discussion Paper Number 17, The World Bank. http://documents.worldbank.org/curated/en/955101468326176513/pdf/589030NWP0EACC10Box353823B01public1.pdf. Accessed 16 May 2020
McGeoch MA, Spear D, Kleynhans EJ, Marais E (2012) Uncertainty in invasive alien species listing. Ecol Appl 22:959–971. https://doi.org/10.1890/11-1252.1
Ministry of Natural Resources and Environment (2009) Climate change, sea level rise scenarios for Vietnam. Socialist Republic of Viet Nam, Hanoi, Viet Nam. www.preventionweb.net/files/11348_ClimateChangeSeaLevelScenariosforVi.pdf. Accessed 16 May 2020
Ministry of Natural Resources and Environment (2010) Viet Nam’s second national communication to the United Nations Framework Convention on Climate Change. Socialist Republic of Viet Nam, Hanoi, Viet Nam. https://unfccc.int/resource/docs/natc/vnmnc02.pdf. Accessed 16 May 2020
Nghiem LTP, Soliman Y, Yeo DCJ, Tan HTW, Evans TA, Mumford JD et al (2013) Economic and environmental impacts of harmful non-indigenous species in Southeast Asia. PLoS ONE 8:71255. https://doi.org/10.1371%2Fjournal.pone.0071255
Nguyen SV (2008) Wildlife trading in Vietnam: situation, causes and solutions. J Environ Dev 17:145–165. https://doi.org/10.1177%2F1070496508316220
Onikura N, Nakajima J, Inui R, Mizutani H, Kobayakawa M, Fukuda S, Mukai T (2011) Evaluating the potential of invasion by non-native freshwater fishes in northern Kyushu Island, Japan, using the Fish Invasiveness Scoring Kit. Ichthyol Res 58:382–387. https://doi.org/10.1007/s10228-011-0235-1
Peh K (2010) Invasive species in Southeast Asia: the knowledge so far. Biodivers Conserv 19:1083–1099. https://doi.org/10.1007/s10531-009-9755-7
Pyšek P, Richardson DM, Jarošík V (2006) Who cites who in the invasion zoo: insights from an analysis of the most highly cited papers in invasion ecology. Preslia 78:437–468
Pyšek P, Richardson DM, Pergl J, Jarošík V, Sixtová Z, Weber E (2008) Geographical and taxonomic biases in invasion ecology. Trends Ecol Evol 23:237–244. https://doi.org/10.1016/j.tree.2008.02.002
R Development Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. www.R-project.org/
Rejmánek M (1996) Species richness and resistance to invasions. In: Orians GH, Dirzo R, Cushman JH (eds) Diversity and process in tropical forests. Springer, Berlin, pp 153–172. https://doi.org/10.1007/978-3-642-79755-2_8
Rejmánek M, Simberloff D (2017) Origin matters. Environ Conserv 44:97–99. https://doi.org/10.1017/S0376892916000333
Robin X, Turck N, Hainard A, Tiberti N, Lisacek F, Sanchez JC, Müller M (2011) PROC: an open-source package for R and S + to analyze and compare ROC curves. BMC Bioinform 12:e77. https://doi.org/10.1186/1471-2105-12-77
Roy HE, Rabitsch W, Scalera R, Stewart A, Gallardo B, Genovesi P, Essl F, Adriaens T, Booy O, Branquart E, Brunel S, Copp GH, Dean H, D'hondt B, Josefsson M, Kenis M, Kettunen M, Linnamagi M, Lucy F, Martinou A, Moore N, Nieto A, Pergl J, Peyton J, Schindler S, Solarz W, Stebbing PD, Trichkova T, Vanderhoeven S, Van Valkenburg J, Zenetos A (2018) Developing a framework of minimum standards for the risk assessment of alien species. J Appl Ecol 55:526–538. https://doi.org/10.1111/1365-2664.13025
Roy HE, Bacher S, Essl F, Adriaens T, Aldridge DC, Bishop JD, Blackburn TM, Branquart E, Brodie J, Carboneras C, Cottier-Cook EJ, Copp GH, Dean HJ, Eilenberg J, Gallardo B, Garcia M, García-Berthou E, Genovesi P, Hulme PE, Kenis M, Kerckhof F, Kettunen M, Minchin D, Nentwig W, Nieto A, Pergl J, Pescott OL, Peyton J, Preda C, Rabitsch W, Roques A, Rorke SL, Scalera R, Schindler S, Schönrogge K, Sewell J, Solarz W, Stewart AJA, Tricarico E, Vanderhoeven S, Van der Velde G, Vilà M, Wood CA, Zenetos A (2019) Developing a list of invasive alien species likely to threaten biodiversity and ecosystems in the European Union. Glob Change Biol 25:1032–1048. https://doi.org/10.1111/gcb.14527)
Semenchenko V, Lipinskaya T, Vilizzi L (2018) Risk screening of non-native macroinvertebrates in the major rivers and associated basins of Belarus using the Aquatic Species Invasiveness Screening Kit. Manag Biol Invasions 9:127–136. https://doi.org/10.3391/mbi.2018.9.2.06
Shan Lv, Guo Y-H, Nguyen HM, Sinuon M, Sayasone S, Lo NC, Zhou X-N, Andrews JR (2018) Invasive Pomacea snails as important intermediate hosts of Angiostrongylus cantonensis in Laos, Cambodia and Vietnam: implications for outbreaks of eosinophilic meningitis. Acta Trop 183:32–35. https://doi.org/10.1016/j.actatropica.2018.03.021
Sodhi NJ, Pin Koh L, Brook BW, Ng PKL (2004) Southeast Asian biodiversity: an impending disaster. Trends Ecol Evol 19:654–660. https://doi.org/10.1016/j.tree.2004.09.006
Sodhi NJ, Posa MRC, Lee TM, Bickford D, Koh LP, Brook BW (2010) The state and conservation of Southeast Asian biodiversity. Biodiv Conserv 19:317–328. https://doi.org/10.1007/s10531-009-9607-5
Tan DT, Thu PQ, Dell B (2012) Invasive plant species in the national parks of Vietnam. Forests 3:997–1016. https://doi.org/10.3390/f3040997
Tarkan AS, Sari HM, İlhan A, Kurtul I, Vilizzi L (2017a) Risk screening of non-native and translocated freshwater fish species in a Mediterranean-type shallow lake: Lake Marmara (West Anatolia). Zool Middle East 63:48–57. https://doi.org/10.1080/09397140.2017.1269398
Tarkan AS, Vilizzi L, Nildeniz T, Ekmekçi FG, Stebbing PD, Copp GH (2017b) Identification of potentially invasive freshwater fishes, including translocated species, in Turkey using the Aquatic Species Invasiveness Screening Kit (AS-ISK). Int Rev Hydrobiol 102:47–56. https://doi.org/10.1002/iroh.201601877
Triet T, Thi LTL, Nga NP (2008) Survey and assessment of the impacts of alien plant species in some national parks of Vietnam. University of Natural Science, National University of Ho Chi Minh City (in Vietnamese), Ho Chi Minh City
Uyan U, Oh C-W, Tarkan AS, Top N, Copp GH, Vilizzi L (2020) Risk screening of the potential invasiveness of non-native marine fishes in South Korea. Mar Pollut Bull 153:111018. https://doi.org/10.1016/j.marpolbul.2020.111018
Venkataraman B (2007) A matter of attitude: The consumption of wild animal products in Ha Noi, Viet Nam. TRAFFIC Southeast Asia, Greater Mekong Programme, Ha Noi, Viet Nam. https://www.traffic.org/site/assets/files/3374/matter-of-attitude-viet-nam.pdf. Accessed 16 May 2020
Vilizzi L, Copp GH, Adamovich B, Almeida D, Chan J, Davison PI, Dembski S, Ekmekçi FG, Ferincz Á, Forneck SC, Hill JE, Kim J-E, Koutsikos N, Leuven RSEW, Luna SA, Magalhães F, Marr SM, Mendoza R, Mourão CF, Neal JW (2019) A global review and meta-analysis of applications of the freshwater Fish Invasiveness Screening Kit. Rev Fish Biol Fish 29:529–568. https://doi.org/10.1007/s11160-019-09562-2
Wan F, Jiang, M, Zhan A (eds) (2017) Biological invasions and its management in China. Invading nature—Springer series in invasion ecology, vol 13. Springer, Dordrecht. https://doi.org/10.1007/978-94-024-0948-2
Welcomme RL, Vidthayanom C (2003) The impacts of introductions and stocking of exotic species in the Mekong Basin and policies for their control. MRC Technical Paper No. 9. Mekong River Commission, Phnom Penh, Cambodia. http://www.mrcmekong.org/assets/Publications/technical/tech-No9-the-impacts-of-intro-n-stocking.pdf. Accessed 16 May 2020
Weyl OLF, Daga VS, Ellender BR, Vitule JRS (2016) A review of Clarias gariepinus invasions in Brazil and South Africa. J Fish Biol 89:386–402. https://doi.org/10.1111/jfb.12958
Whitehead PG, Jin L, Bussi G, Voepel HE, Darby SE, Vasilopoulos G, Manley R, Rodda H, Hutton C, Hackney C, Tri VPD (2019) Water quality modelling of the Mekong River basin: climate change and socioeconomics drive flow and nutrient flux changes to the Mekong Delta. Sci Tot Environ 673:218–229. https://doi.org/10.1016/j.scitotenv.2019.03.315
Wong PK, Kwong KL, Qiu J-W (2009) Complex interactions among fish, snails and macrophytes: implications for biological control of an invasive snail. Biol Invasions 11:2223–2232. https://doi.org/10.1007/s10530-008-9378-z
World Bank Group (2019) World development indicators—country profile, Vietnam. https://databank.worldbank.org/views/reports/reportwidget.aspx?Report_Name=CountryProfile&Id=b450fd57&tbar=y&dd=y&inf=n&zm=n&country=VNM. Accessed 16 May 2020
Wyckhuys KAG, Hughes AC, Buamas C, Johnson AC, Vasseur L, Reymondin L, Deguine J-P, Sheil D (2019) Biological control of an agricultural pest protects tropical forests. Commun Biol 2:10. https://doi.org/10.1038/s42003-018-0257-6
Zworykin D, Budaev SV (2013) Non-indigenous armoured catfish in Vietnam: invasion and systematics. Ichthyol Res 60:327–333. https://doi.org/10.1007/s10228-013-0356-9
Acknowledgements
The participation of L. Ruykys in this study was facilitated through an assignment with the Australian Volunteers Program, which is an initiative of the Australian Government. The participation of G.H. Copp was supported by Cefas’ Science Excellence Fund.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
The original online version of this article was revised due to the pdf version of the article has been published with errors in punctuation, diacritics and symbols throughout the entire article and they have been corrected in the pdf version.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ruykys, L., Ta, K.A.T., Bui, T.D. et al. Risk screening of the potential invasiveness of non-native aquatic species in Vietnam. Biol Invasions 23, 2047–2060 (2021). https://doi.org/10.1007/s10530-020-02430-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-020-02430-2