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Identifying risk factors for persistent versus casual establishment to prioritize rapid response to non-indigenous aquarium fish

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Abstract

Rapid response strategies are necessary to effectively manage non-indigenous species. After detection, only few species persist and potentially cause harm. To help prioritize resources, we employed a multispecies, geographically explicit approach, focusing on non-indigenous aquarium fish establishment in the USA. We modeled casual (i.e. temporary) establishment and persistence separately, to identify which species should be prioritized after detection. To facilitate the usability of quantitative models, we converted our results into simple “rules of thumb”, wherein each factor’s contribution represents a multiplier. Finally, from a fundamental perspective, separating casual and persistent establishment improved our understanding of the earlier stages of invasions. We identified five species ranking highest for rapid response, if detected in California, New Mexico and Texas. These states, along with Florida and Hawaii, should take precedence in management funding, being those that currently host more persistent species and where more new establishments are forecasted. Expectedly, the important factors differed considerably between sub-stages, with species traits and propagule pressure being most relevant for casual establishment, and the environment being more predictive of persistence. Notably, propagule pressure had no effect on persistence, suggesting that it would not help target eradication for aquarium fish. Our model allows comparisons for > 1000 species across locations to target rapid responses after detection, and can provide guidance for species not currently traded. Our analysis re-evaluates “risky” species in terms of persistence, suggesting that many species which were flagged in the literature actually pose low risk. Conversely, we identify species that, if detected, warrant rapid response.

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References

  • Abellán P, Carrete M, Anadón JD, Cardador L, Tella JL (2016) Non-random patterns and temporal trends (1912–2012) in the transport, introduction and establishment of exotic birds in Spain and Portugal. Divers Distrib 22:263–273

    Google Scholar 

  • Aho K, Derryberry D, Peterson T (2017) A graphical framework for model selection criteria and significance tests: refutation, confirmation and ecology. Methods Ecol Evol 8:47–56

    Google Scholar 

  • Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723

    Google Scholar 

  • Albert A, Anderson JA (1984) On the existence of maximum likelihood estimates in logistic regression models. Biometrika 71:1–10

    Google Scholar 

  • Alvarez S, Solis D (2019) Rapid response lowers eradication costs of invasive species: evidence from Florida. Choices 33(4):1–9

    Google Scholar 

  • Anderson DR, Burnham KP (2002) Avoiding pitfalls when using information-theoretic methods. J Wildl Manag 66:912–918

    Google Scholar 

  • Bennett WA, Currie RJ, Wagner PF, Beitinger TL (1997) Cold tolerance and potential overwintering of the red-bellied piranha Pygocentrus nattereri in the United States. Trans Am Fish Soc 126:841–849

    Google Scholar 

  • Blackburn TM, Cassey P, Lockwood JL (2009) The role of species traits in the establishment success of exotic birds. Glob Change Biol 15:2852–2860

    Google Scholar 

  • Blackburn TM, Pyšek P, Bacher S, Carlton JT, Duncan RP, Jarošík V, Wilson JR, Richardson DM (2011) A proposed unified framework for biological invasions. Trends Ecol Evol 26:333–339

    PubMed  Google Scholar 

  • Bland JM, Altman DG (2000) The odds ratio. BMJ 320:1468

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bomford M, Barry SC, Lawrence E (2010) Predicting establishment success for introduced freshwater fishes: a role for climate matching. Biol Invasions 12:2559–2571

    Google Scholar 

  • Bradie J, Leung B (2017) A quantitative synthesis of the importance of variables used in MaxEnt species distribution models. J Biogeogr 44:1344–1361

    Google Scholar 

  • Bradie J, Chivers C, Leung B (2013) Importing risk: quantifying the propagule pressure–establishment relationship at the pathway level. Divers Distrib 19:1020–1030

    Google Scholar 

  • Britton JR, Gozlan RE, Copp GH (2011) Managing non-native fish in the environment. Fish Fish 12:256–274

    Google Scholar 

  • Buckley YM (2008) The role of research for integrated management of invasive species, invaded landscapes and communities. J Appl Ecol 45:397–402

    Google Scholar 

  • Cassey P, Delean S, Lockwood JL, Sadowski J, Blackburn TM (2018a) Dissecting the null model for biological invasions: a meta-analysis of the propagule pressure effect. PLoS Biol 16:e2005987

    PubMed  PubMed Central  Google Scholar 

  • Cassey P, García-Díaz P, Lockwood JL, Blackburn TM (2018b) Invasion biology: searching for predictions and prevention, and avoiding lost causes. Invasion Biol Hypotheses Evid 9:1

    Google Scholar 

  • Chadès I, Martin TG, Nicol S, Burgman MA, Possingham HP, Buckley YM (2011) General rules for managing and surveying networks of pests, diseases, and endangered species. Proc Natl Acad Sci 108:8323–8328

    PubMed  PubMed Central  Google Scholar 

  • Chapman FA, Fitz-Coy SA, Thunberg EM, Adams CM (1997) United States of America trade in ornamental fish. J World Aquac Soc 28:1–10

    Google Scholar 

  • Cook CN, Hockings M, Carter RB (2010) Conservation in the dark? The information used to support management decisions. Front Ecol Environ 8:181–186

    Google Scholar 

  • Cummings P (2009) The relative merits of risk ratios and odds ratios. Arch Pediatr Adolesc Med 163:438–445

    PubMed  Google Scholar 

  • Dawson W, Burslem DF, Hulme PE (2009) Factors explaining alien plant invasion success in a tropical ecosystem differ at each stage of invasion. J Ecol 97:657–665

    Google Scholar 

  • Della Venezia L, Samson J, Leung B (2018) The rich get richer: invasion risk across North America from the aquarium pathway under climate change. Divers Distrib 24:285–296

    Google Scholar 

  • Dogliotti A, Gossn J, Vanhellemont Q, Ruddick K (2018) Detecting and quantifying a massive invasion of floating aquatic plants in the río de la plata turbid waters using high spatial resolution ocean color imagery. Remote Sens 10:1140

    Google Scholar 

  • Drake JM, Lodge DM (2004) Effects of environmental variation on extinction and establishment. Ecol Lett 7:26–30

    Google Scholar 

  • Duggan IC, Rixon CA, MacIsaac HJ (2006) Popularity and propagule pressure: determinants of introduction and establishment of aquarium fish. Biol Invasions 8:377–382

    Google Scholar 

  • Duncan RP, Bomford M, Forsyth DM, Conibear L (2001) High predictability in introduction outcomes and the geographical range size of introduced Australian birds: a role for climate. J Anim Ecol 70:621–632

    Google Scholar 

  • Duncan RP, Blackburn TM, Rossinelli S, Bacher S (2014) Quantifying invasion risk: the relationship between establishment probability and founding population size. Methods Ecol Evol 5:1255–1263

    Google Scholar 

  • Ehrenfeld JG (2010) Ecosystem consequences of biological invasions. Annu Rev Ecol Evol Syst 41:59–80

    Google Scholar 

  • Essl F, Dullinger S, Moser D, Steinbauer K, Mang T (2015) Macroecology of global bryophyte invasions at different invasion stages. Ecography 38:488–498

    Google Scholar 

  • Ficetola GF, Thuiller W, Padoa-Schioppa E (2009) From introduction to the establishment of alien species: bioclimatic differences between presence and reproduction localities in the slider turtle. Divers Distrib 15:108–116

    Google Scholar 

  • Finnoff D, Shogren JF, Leung B, Lodge D (2007) Take a risk: preferring prevention over control of biological invaders. Ecol Econ 62:216–222

    Google Scholar 

  • Forsyth DM, Duncan RP, Bomford M, Moore G (2004) Climatic suitability, life-history traits, introduction effort, and the establishment and spread of introduced mammals in Australia. Conserv Biol 18:557–569

    Google Scholar 

  • Froese R, Pauly D (eds) (2018) FishBase. World Wide Web electronic publication. www.fishbase.org, version (02/2018)

  • Hanley JA, McNeil BJ (1982) The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology 143:29–36

    CAS  PubMed  Google Scholar 

  • Hayes KR, Barry SC (2008) Are there any consistent predictors of invasion success? Biol Invasions 10:483–506

    Google Scholar 

  • Herrel A, van der Meijden A (2014) An analysis of the live reptile and amphibian trade in the USA compared to the global trade in endangered species. Herpetol J 24:103–110

    Google Scholar 

  • Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978

    Google Scholar 

  • Howeth JG, Gantz CA, Angermeier PL, Frimpong EA, Hoff MH, Keller RP, Mandrak NE, Marchetti MP, Olden JD, Romagosa CM, Lodge DM (2016) Predicting invasiveness of species in trade: climate match, trophic guild and fecundity influence establishment and impact of non-native freshwater fishes. Divers Distrib 22:148–160

    Google Scholar 

  • Jenkins PT (2013) Invasive animals and wildlife pathogens in the United States: the economic case for more risk assessments and regulation. Biol Invasions 15:243–248

    Google Scholar 

  • Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19:101–108

    PubMed  Google Scholar 

  • Keller RP, Perrings C (2011) International policy options for reducing the environmental impacts of invasive species. Bioscience 61:1005–1012

    Google Scholar 

  • Kerr NZ, Baxter PW, Salguero-Gómez R, Wardle GM, Buckley YM (2016) Prioritizing management actions for invasive populations using cost, efficacy, demography and expert opinion for 14 plant species world-wide. J Appl Ecol 53:305–316

    PubMed  PubMed Central  Google Scholar 

  • Kolar CS, Lodge DM (2002) Ecological predictions and risk assessment for alien fishes in North America. Science 298:1233–1236

    CAS  PubMed  Google Scholar 

  • Leung B, Lodge DM, Finnoff D, Shogren JF, Lewis MA, Lamberti G (2002) An ounce of prevention or a pound of cure: bioeconomic risk analysis of invasive species. Proc R Soc Lond B Biol Sci 269:2407–2413

    Google Scholar 

  • Leung B, Finnoff D, Shogren JF, Lodge D (2005) Managing invasive species: rules of thumb for rapid assessment. Ecol Econ 55:24–36

    Google Scholar 

  • Leung B, Roura-Pascual N, Bacher S, Heikkilä J, Brotons L, Burgman MA, Dehnen‐Schmutz K, Essl F, Hulme PE, Richardson DM, Sol D (2012) TEASIng apart alien species risk assessments: a framework for best practices. Ecol Lett 15:1475–1493

    PubMed  Google Scholar 

  • Lockwood JL, Hoopes MF, Marchetti MP (2013) Invasion ecology. Wiley, London

    Google Scholar 

  • Lohr CA, Hone J, Bode M, Dickman CR, Wenger A, Pressey RL (2017) Modeling dynamics of native and invasive species to guide prioritization of management actions. Ecosphere 8:e01822

    Google Scholar 

  • Mahoney PJ, Beard KH, Durso AM, Tallian AG, Long AL, Kindermann RJ, Nolan NE, Kinka D, Mohn HE (2015) Introduction effort, climate matching and species traits as predictors of global establishment success in non-native reptiles. Divers Distrib 21:64–74

    Google Scholar 

  • Marchetti MP, Moyle PB, Levine R (2004) Invasive species profiling? Exploring the characteristics of non-native fishes across invasion stages in California. Freshw Biol 49:646–661

    Google Scholar 

  • Mehta SV, Haight RG, Homans FR, Polasky S, Venette RC (2007) Optimal detection and control strategies for invasive species management. Ecol Econ 61:237–245

    Google Scholar 

  • Milbau A, Stout JC (2008) Factors associated with alien plants transitioning from casual, to naturalized, to invasive. Conserv Biol 22:308–317

    PubMed  Google Scholar 

  • Mumbare SS, Maindarkar G, Darade R, Yenge S, Tolani MK, Patole K (2012) Maternal risk factors associated with term low birth weight neonates: a matched-pair case control study. Indian Pediatr 49:25–28

    PubMed  Google Scholar 

  • Peoples BK, Midway SR (2018) Fishing pressure and species traits affect stream fish invasions both directly and indirectly. Divers Distrib 24:1158–1168

    Google Scholar 

  • Peterson DP, Rieman BE, Dunham JB, Fausch KD, Young MK (2008) Analysis of trade-offs between threats of invasion by nonnative brook trout (Salvelinus fontinalis) and intentional isolation for native westslope cutthroat trout (Oncorhynchus clarkii lewisi). Can J Fish Aquat Sci 65:557–573

    Google Scholar 

  • Pyšek P, Jarošík V, Pergl J, Randall R, Chytrý M, Kühn I, Tichý L, Danihelka J, Chrtek Jun J, Sádlo J (2009) The global invasion success of Central European plants is related to distribution characteristics in their native range and species traits. Divers Distrib 15:891–903

    Google Scholar 

  • Pyšek P, Jarošík V, Hulme PE, Pergl J, Hejda M, Schaffner U, Vilà M (2012) A global assessment of invasive plant impacts on resident species, communities and ecosystems: the interaction of impact measures, invading species’ traits and environment. Glob Change Biol 18:1725–1737

    Google Scholar 

  • R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Ribeiro F, Elvira B, Collares-Pereira MJ, Moyle PB (2008) Life-history traits of non-native fishes in Iberian watersheds across several invasion stages: a first approach. Biol Invasions 10:89–102

    Google Scholar 

  • Rixon CA, Duggan IC, Bergeron NM, Ricciardi A, Macisaac HJ (2005) Invasion risks posed by the aquarium trade and live fish markets on the Laurentian Great Lakes. Biodivers Conserv 14:1365–1381

    Google Scholar 

  • Robinson JE, Griffiths RA, John FAS, Roberts DL (2015) Dynamics of the global trade in live reptiles: shifting trends in production and consequences for sustainability. Biol Cons 184:42–50

    Google Scholar 

  • Ruesink JL (2005) Global analysis of factors affecting the outcome of freshwater fish introductions. Conserv Biol 19:1883–1893

    Google Scholar 

  • Saul WC, Roy HE, Booy O, Carnevali L, Chen HJ, Genovesi P, Harrower CA, Hulme PE, Pagad S, Pergl J, Jeschke JM (2017) Assessing patterns in introduction pathways of alien species by linking major invasion data bases. J Appl Ecol 54:657–669

    Google Scholar 

  • Simberloff D (2003) How much information on population biology is needed to manage introduced species? Conserv Biol 17:83–92

    Google Scholar 

  • Simberloff D, Martin JL, Genovesi P, Maris V, Wardle DA, Aronson J, Courchamp F, Galil B, García-Berthou E, Pascal M, Pyšek P (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28:58–66

    PubMed  Google Scholar 

  • Sol D, Maspons J, Vall-Llosera M, Bartomeus I, García-Peña GE, Piñol J, Freckleton RP (2012) Unraveling the life history of successful invaders. Science 337:580–583

    CAS  PubMed  Google Scholar 

  • Stewart-Koster B, Olden JD, Johnson PT (2015) Integrating landscape connectivity and habitat suitability to guide offensive and defensive invasive species management. J Appl Ecol 52:366–378

    Google Scholar 

  • U.S. Geological Survey (2017) Nonindigenous aquatic species database. http://nas.er.usgs.gov Gainesville, FL

  • Vander Zanden MJ, Olden JD (2008) A management framework for preventing the secondary spread of aquatic invasive species. Can J Fish Aquat Sci 65:1512–1522

    Google Scholar 

  • Vander Zanden MJ, Hansen GJ, Higgins SN, Kornis MS (2010) A pound of prevention, plus a pound of cure: early detection and eradication of invasive species in the Laurentian Great Lakes. J Great Lakes Res 36:199–205

    Google Scholar 

  • Westbrooks RG (2004) New approaches for early detection and rapid response to invasive plants in the United States. Weed Technol 18:1468–1471

    Google Scholar 

  • Wittenberg R, Cock MJ (eds) (2001) Invasive alien species: a toolkit of best prevention and management practices. CABI, Abingdon

    Google Scholar 

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Acknowledgements

The authors would like to thank E. Hudgins, D. Nguyen, N. Richards and S. Varadarajan for insightful discussions. This research was supported by Natural Sciences and Engineering Research Council of Canada—Canadian Aquatic Invasive Species Network and Natural Sciences and Engineering Research Council of Canada—Discovery Grants to BL.

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Both LDV and BL conceived the project. LDV built and analysed the models, and derived the multiplicative risk factors for rapid response. LDV led the preparation of the manuscript, and both LDV and BL contributed to the final version.

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Correspondence to Lidia Della Venezia.

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Della Venezia, L., Leung, B. Identifying risk factors for persistent versus casual establishment to prioritize rapid response to non-indigenous aquarium fish. Biol Invasions 22, 1397–1410 (2020). https://doi.org/10.1007/s10530-019-02191-7

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