Integrating an individual-based model with approximate Bayesian computation to predict the invasion of a freshwater fish provides insights into dispersal and range expansion dynamics

Alford RA, Brown GP, Schwarzkopf L, Phillips BL, Shine R (2009) Comparisons through time and space suggest rapid evolution of dispersal behaviour in an invasive species. Wildl Res 36:23–28. https://doi.org/10.1071/WR08021

Allouche O, Tsoar A, Kadmon R (2006) Assessing the accuracy of species distribution models: prevalence, kappa and the true skill statistic (TSS). J Appl Ecol 43:1223–1232

Antognazza CM, Andreou D, Zaccara S, Britton RJ (2016) Loss of genetic integrity and biological invasions result from stocking and introductions of Barbus barbus: insights from rivers in England. Ecol Evol 6:1280–1292. https://doi.org/10.1002/ece3.1906

Barros C, Palmer SCF, Bocedi G, Travis JMJ (2016) Spread rates on fragmented landscapes: the interacting roles of demography, dispersal and habitat availability. Divers Distrib 22:1266–1275. https://doi.org/10.1111/ddi.12487

Bayley PB, Herendeen RA (2000) The efficiency of a seine net. Trans Am Fish Soc 129:901–923. https://doi.org/10.1577/1548-8659(2000)129%3c0901:TEOASN%3e2.3.CO;2

Beardsley H, Britton JR (2012) Contribution of temperature and nutrient loading to growth rate variation of three cyprinid fishes in a lowland river. Aquat Ecol 46:143–152. https://doi.org/10.1007/s10452-011-9387-3

Berry O, England P, Marriott RJ, Burridge CP, Newman SJ (2012) Understanding age-specific dispersal in fishes through hydrodynamic modelling, genetic simulations and microsatellite DNA analysis. Mol Ecol 21:2145–2159. https://doi.org/10.1111/j.1365-294X.2012.05520.x

Bocedi G, Palmer SCF, Pe’er G, Heikkinen RK, Matsinos YG, Watts K, Travis JMJ (2014) Range Shifter: a platform for modelling spatial eco-evolutionary dynamics and species’ responses to environmental changes. Methods Ecol Evol 5:388–396. https://doi.org/10.1111/2041-210X.12162

Boyd R, Roy S, Sibly R, Thorpe R, Hyder K (2018) A general approach to incorporating spatial and temporal variation in individual-based models of fish populations with application to Atlantic mackerel. Ecol Model 382:9–17. https://doi.org/10.1016/j.ecolmodel.2018.04.015

Brandner J, Cerwenka AF, Schliewen UK, Geist J (2013) Bigger is better: characteristics of round gobies forming an invasion front in the Danube River. PLoS ONE 8:e73036. https://doi.org/10.1371/journal.pone.0073036

Britton JR, Gozlan RE (2013) How many founders for a biological invasion? predicting introduction outcomes from propagule pressure. Ecology 94:2558–2566. https://doi.org/10.1890/13-0527.1

Britton JR, Davies GD, Brazier M, Pinder AC (2007) A case study on the population ecology of a topmouth gudgeon (Pseudorasbora parva) population in the UK and the implications for native fish communities. Aquat Conserv 17:749–759. https://doi.org/10.1002/aqc.809

Britton JR, Davies GD, Brazier M (2008) Contrasting life history traits of invasive topmouth gudgeon (Pseudorasbora parva) in adjacent ponds in England. J Appl Ichthyol 24:694–698. https://doi.org/10.1111/j.1439-0426.2008.01163.x

Britton JR, Davies GD, Harrod C (2010) Trophic interactions and consequent impacts of the invasive fish Pseudorasbora parva in a native aquatic foodweb: a field investigation in the UK. Biol Invasions 12:1533–1542. https://doi.org/10.1007/s10530-009-9566-5

Britton JR, Gozlan RE, Copp GH (2011) Managing non-native fish in the environment. Fish Fish 12:256–274. https://doi.org/10.1111/j.1467-2979.2010.00390.x

Byers JE, Pringle JM (2006) Going against the flow: retention, range limits and invasions in advective environments. Mar Ecol Prog Ser 313:27–41. https://doi.org/10.3354/meps313027

Caswell H (2001) Matrix population models: construction, analysis, and interpretation. Sinauer Associates

Copp GH, Vilizzi L, Mumford J, Fenwick GV, Godard MJ, Gozlan RE (2009) Calibration of FISK, an invasiveness screening tool for nonnative freshwater fishes. Risk Anal 29:457–467. https://doi.org/10.1111/j.1539-6924.2008.01159.x

Core Team R (2018) R: a language and environment for statistical computing. Austria, Vienna

Cote J, Fogarty S, Weinersmith K, Brodin T, Sih A (2010) Personality traits and dispersal tendency in the invasive mosquitofish (Gambusia affinis). Proc R Soc B 277:1571–1579. https://doi.org/10.1098/rspb.2009.2128

Coulon A, Aben J, Palmer SCF, Stevens VM, Callens T, Strubbe D, Lens L, Matthysen E, Baguette M, Travis JMJ (2015) A stochastic movement simulator improves estimates of landscape connectivity. Ecology 96:2203–2213. https://doi.org/10.1890/14-1690.1

Csillery K, Blum MG, Gaggiotti OE, Francois O (2010) Approximate Bayesian Computation (ABC) in practice. Trends Ecol Evol 25:410–418. https://doi.org/10.1016/j.tree.2010.04.001

Damme DV, Bogutskaya N, Hoffmann RC, Smith C (2007) The introduction of the European bitterling (Rhodeus amarus) to west and central Europe. Fish Fish 8:79–106. https://doi.org/10.1111/j.1467-2679.2007.00239.x

Davies GD, Britton JR (2015) Assessing the efficacy and ecology of biocontrol and biomanipulation for managing invasive pest fish. J Appl Ecol 52:1264–1273. https://doi.org/10.1111/1365-2664.12488

Davies GD, Britton JR (2016) Assessment of non-native fish dispersal from a freshwater aquaculture site. Fish Manag Ecol 23:428–430. https://doi.org/10.1111/fme.12176

Davies CE, Shelley J, Harding P, McLean I, Gardiner R, Peirson G (2004) Freshwater fishes in Britain: the species and their distribution. Harley Books, Colchester

Davies GD, Gozlan RE, Britton RJ (2013) Can accidental introductions of non-native species be prevented by fish stocking audits? Aquat Conserv 23:366–373. https://doi.org/10.1002/aqc.2341

Day CC, Landguth EL, Bearlin A, Holden ZA, Whiteley AR (2018) Using simulation modeling to inform management of invasive species: a case study of eastern brook trout suppression and eradication. Biol Conserv 221:10–22. https://doi.org/10.1016/j.biocon.2018.01.017

DeAngelis DL, Grimm V (2014) Individual-based models in ecology after four decades. F1000Prime Rep. 6:39. https://doi.org/10.12703/P6-39

DiCiccio TJ, Efron B (1996) Bootstrap confidence intervals. Stat Sci 11:189–228. https://doi.org/10.1214/ss/1032280214

Early R, Bradley BA, Dukes JS, Lawler JJ, Olden JD, Blumenthal DM, Gonzalez P, Grosholz ED, Ibañez I, Miller LP, Sorte CJ, 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

Environment-Agency (2018) National Fish Populations Database (NFPD): Freshwater Fish Counts for all Species, all Areas and all Years. https://data.gov.uk/dataset/f49b8e4b-8673-498e-bead-98e6847831c6/freshwater-fish-counts-for-all-species-all-areas-and-all-years. Accessed 20 Jan 2019

Frank KT (1992) Demographic consequences of age-specific dispersal in marine fish populations. Can J Fish Aquat Sci 49:2222–2231. https://doi.org/10.1139/f92-243

Fraser EJ, Lambin X, Travis JMJ, Harrington LA, Palmer SCF, Bocedi G, Macdonald DW (2015) Range expansion of an invasive species through a heterogeneous landscape—the case of American mink in Scotland. Divers Distrib 21:888–900. https://doi.org/10.1111/ddi.12303

Gámez-Virués S, Perović DJ, Gossner MM, Börschig C, Blüthgen N, De Jong H, Simons NK, Klein AM, Krauss J, Maier G, Scherber C, Steckel J, Rothenwohrer C, Steffan-Dewenter I, Weiner CN, Weisser W, Werner M, Tscharntke T, Westphal C (2015) Landscape simplification filters species traits and drives biotic homogenization. Nat Commun 6:8568. https://doi.org/10.1038/ncomms9568

Gilbert MA, Gaffney EA, Bullock JM, White SM (2014) Spreading speeds for plant populations in landscapes with low environmental variation. J Theor Biol 363:436–452. https://doi.org/10.1016/j.jtbi.2014.08.022

Gilbert MA, White SM, Bullock JM, Gaffney EA (2017) Speeding up the simulation of population spread models. Methods Ecol Evol 8:501–510. https://doi.org/10.1111/2041-210X.12684

Gozlan RE, Britton JR, Cowx I, Copp GH (2010a) Current knowledge on non-native freshwater fish introductions. J Fish Biol 76:751–786. https://doi.org/10.1111/j.1095-8649.2010.02566.x

Gozlan RE, Andreou D, Asaeda T, Beyer K, Bouhadad R, Burnard D, Caiola N et al (2010b) Pan-continental invasion of Pseudorasbora parva: towards a better understanding of freshwater fish invasions. Fish Fish 11:315–340. https://doi.org/10.1111/j.1467-2979.2010.00361.x

Grimm V, Berger U, Bastiansen F, Eliassen S, Ginot V, Giske J, Goss-Custard J, Grand T, Heinz SK, Huse G, Huth A, Jepsen JU, Jørgensen C, Mooij WM, Müller B, Pe’er G, Piou C, Railsback SF, Robbins AM, Robbins MM, Rossmanith E, Rüger N, Strand E, Souissi S, Stillman RA, Vabø R, Visser U, DeAngelis DL (2006) A standard protocol for describing individual-based and agent-based models. Ecol Model 198:115–126. https://doi.org/10.1016/j.ecolmodel.2006.04.023

Hastings A, Cuddington K, Davies KF, Dugaw CJ, Elmendorf S, Freestone A, Harrison S, Holland M, Lambrinos J, Malvadkar U, Melbourne BA, Moore K, Taylor C, Thomson D (2005) The spatial spread of invasions: new developments in theory and evidence. Ecol Lett 8:91–101. https://doi.org/10.1111/j.1461-0248.2004.00687.x

Havel JE, Kovalenko KE, Thomaz SM, Amalfitano S, Kats LB (2015) Aquatic invasive species: challenges for the future. Hydrobiologia 750:147–170. https://doi.org/10.1007/s10750-014-2166-0

Hedger RD, Sundt-Hansen LE, Forseth T, Diserud OH, Ugedal O, Finstad AG (2013a) Modelling the complete life-cycle of Atlantic salmon (Salmo salar L.) using a spatially explicit individual-based approach. Ecol Model 248:119–129. https://doi.org/10.1016/j.ecolmodel.2012.10.003

Hedger RD, Sundt-Hansen LE, Forseth T, Ugedal O, Diserud OH, Kvambekk ÅS, Finstad AG (2013b) Predicting climate change effects on subarctic–Arctic populations of Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 70:159–168. https://doi.org/10.1139/cjfas-2012-0205

Heikkinen RK, Bocedi G, Kuussaari M, Heliölä J, Leikola N, Pöyry J, Travis JMJ (2014) Impacts of land cover data selection and trait parameterisation on dynamic modelling of species’ range expansion. PLoS ONE 9:e108436. https://doi.org/10.1371/journal.pone.0108436

Karakuş U, Top N, Tepeköy EG, Britton JR, Tarkan AS (2018) Life history characteristics of the potentially invasive Ponto–Caspian goby Neogobius fluviatilis in natural lakes from its native range (Black Sea region of Turkey). Mar Freshw Res 69:1544–1556. https://doi.org/10.1071/MF17350

Klinard NV, Halfyard EA, Fisk AT, Stewart TJ, Johnson TB (2018) Effects of surgically implanted acoustic tags on body condition, growth, and survival in a small, laterally compressed forage fish. Trans Am Fish Soc 147:749–757. https://doi.org/10.1002/tafs.10064

Madenjian CP, Cochran PA, Bergstedt RA (2003) Seasonal patterns in growth, blood consumption, and effects on hosts by parasitic-phase sea lampreys in the great lakes: an individual-based model approach. J Great Lakes Res 29:332–346. https://doi.org/10.1016/S0380-1330(03)70498-5

Mills SC, Reynolds JD (2002) Mussel ventilation rates as a proximate cue for host selection by bitterling, Rhodeus sericeus. Oecologia 131:473–478. https://doi.org/10.1007/s00442-002-0895-7

Mills SC, Reynolds JD (2003) Operational sex ratio and alternative reproductive behaviours in the European bitterling, Rhodeus sericeus. Behav Ecol Sociobiol 54:98–104. https://doi.org/10.1007/s00265-003-0616-1

Mills SC, Taylor MI, Reynolds JD (2005) Benefits and costs to mussels from ejecting bitterling embryos: a test of the evolutionary equilibrium hypothesis. Anim Behav 70:31–37. https://doi.org/10.1016/j.anbehav.2004.09.016

Mooney C, Duval R (1993) Quantitative applications in the social sciences: bootstrapping. SAGE Publications, Inc., pp 1–26

Mostert E (2017) River basin management and community: the Great Ouse Basin, 1850–present. Int J River Basin Manag 16:51–59. https://doi.org/10.1080/15715124.2017.1339355

Neeson TM, Wiley MJ, Adlerstein SA, Riolo RL (2012) How river network structure and habitat availability shape the spatial dynamics of larval sea lampreys. Ecol Model 226:62–70. https://doi.org/10.1016/j.ecolmodel.2011.11.031

Neubert MG, Caswell H (2000) Density-dependent vital rates and their population dynamic consequences. J Math Biol 41:103–121. https://doi.org/10.1007/s002850070001

Nilsson PA, Brönmark C (2000) Prey vulnerability to a gape-size limited predator: behavioural and morphological impacts on northern pike piscivory. Oikos 88:539–546. https://doi.org/10.1034/j.1600-0706.2000.880310.x

Nunn AD, Harvey JP, Britton JR, Frear PA, Cowx IG (2007) Fish, climate and the Gulf Stream: the influence of abiotic factors on the recruitment success of cyprinid fishes in lowland rivers. Freshw Biol 52:1576–1586. https://doi.org/10.1111/j.1365-2427.2007.01789.x

O’Hagana A, Stevens JW (2003) Assessing and comparing costs: how robust are the bootstrapand methods based on asymptotic normality? Health Econ 12:33–49. https://doi.org/10.1002/hec.699

Ordnance Survey, OS MasterMap Water Network, Scale 1:2,500 [GML3 geospatial data]. Updated Jan 2018 © Crown copyright and database rights 2018 Ordnance Survey (100025252). Using: EDINA Digimap Ordnance Survey Service, http://edina.ac.uk/digimap, Created: November 2018

Palmer SCF, Coulon A, Travis JMJ (2011) Introducing a ‘stochastic movement simulator’ for estimating habitat connectivity. Methods Ecol Evol 2:258–268. https://doi.org/10.1111/j.2041-210X.2010.00073.x

Parry H, Sadler R, Kriticos D (2013) Practical guidelines for modelling post-entry spread in invasion ecology. NeoBiota 18:41–66. https://doi.org/10.3897/neobiota.18.4305

Phang SC, Stillman RA, Cucherousset J, Britton JR, Roberts D, Beaumont WR, Gozlan RE (2016) FishMORPH—an agent-based model to predict salmonid growth and distribution responses under natural and low flows. Sci Rep 6:29414. https://doi.org/10.1038/srep29414

Pyke CR, Thomas R, Porter RD, Hellmann JJ, Dukes JS, Lodge DM, Chavarria G (2008) Current practices and future opportunities for policy on climate change and invasive species. Conserv Biol 22:585–592. https://doi.org/10.1111/j.1523-1739.2008.00956.x

Reichard M, Ondrackova M, Przybylski M, Liu H, Smith C (2006) The costs and benefits in an unusual symbiosis: experimental evidence that bitterling fish (Rhodeus sericeus) are parasites of unionid mussels in Europe. J Evol Biol 19:788–796. https://doi.org/10.1111/j.1420-9101.2005.01051.x

Reichard M, Liu H, Smith C (2007) The co-evolutionary relationship between bitterling fishes and freshwater mussels: insights from interspecific comparisons. Evol Ecol Res 9:239–259

Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332. https://doi.org/10.1146/annurev.ecolsys.32.081501.114037

Samson E, Hirsch PE, Palmer SCF, Behrens JW, Brodin T, Travis JMJ (2017) Early engagement of stakeholders with individual-based modeling can inform research for improving invasive species management: the round goby as a case study. Front Ecol Evol 5:149. https://doi.org/10.3389/fevo.2017.00149

Simberloff D, Martin JL, Genovesi P, Maris V, Wardle DA, Aronson J, Courchamp F, Galil B, García-Berthou E, Pascal M, Pyšek P, Sousa R, Tabacchi E, Vila M (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28:58–66. https://doi.org/10.1016/j.tree.2012.07.013

Skellam JG (1951) Random dispersal in theoretical populations. Biometrika 38:196–218. https://doi.org/10.1093/biomet/38.1-2.196

Smith C (2017) Bayesian inference supports the host selection hypothesis in explaining adaptive host specificity by European bitterling. Oecologia 183:379–389. https://doi.org/10.1007/s00442-016-3780-5

Stiver KA, Desjardins JK, Fitzpatrick JL, Neff B, Quinn JS, Balshine S (2007) Evidence for size and sex-specific dispersal in a cooperatively breeding cichlid fish. Mol Ecol 16:2974–2984. https://doi.org/10.1111/j.1365-294X.2007.03350.x

Tarkan AS, Karakuş U, Tepeköy EG, Top N, Yalçın-Özdilek S, Partal N, Britton JR (2018) Trophic interactions of two Ponto–Caspian gobies in the Turkish part of their native range. Turk J Fish Aquat Sci 18:1279–1286. https://doi.org/10.4194/1303-2712-v18_11_04

Top N, Karakuş U, Tepeköy EG, Britton JR, Tarkan AS (2018) Plasticity in life history traits of the native Proterorhinus semilunaris suggests high adaptive capacity in its invasive range. Knowl Manag Aquat Ecosyst 419:48. https://doi.org/10.1051/kmae/201803

Urban MC, Bocedi G, Hendry AP, Mihoub JB, Pe’er G, Singer A, Bridle JR, Crozier LG, De Meester L, Godsoe W, Gonzalez A, Hellmann JJ, Holt RD, Huth A, Johst K, Krug CB, Leadley PW, Palmer SCF, Pantel JH, Schmitz A, Zollner PA, Travis JMJ (2016) Improving the forecast for biodiversity under climate change. Science 353:6304. https://doi.org/10.1126/science.aad8466

van der Vaart E, Beaumont MA, Johnston ASA, Sibly RM (2015) Calibration and evaluation of individual-based models using approximate Bayesian computation. Ecol Model 312:182–190. https://doi.org/10.1016/j.ecolmodel.2015.05.020

van der Vaart E, Johnston ASA, Sibly RM (2016) Predicting how many animals will be where: how to build, calibrate and evaluate individual-based models. Ecol Model 326:113–123. https://doi.org/10.1016/j.ecolmodel.2015.08.012

van der Vaart E, Prangle D, Sibly R (2018) Taking error into account when fitting models using approximate Bayesian computation. Ecol Appl 28:267–274. https://doi.org/10.1002/eap.1656

Vitule JRS, Skóra F, Abilhoa V (2012) Homogenization of freshwater fish faunas after the elimination of a natural barrier by a dam in Neotropics. Divers Distrib 18:111–120. https://doi.org/10.1111/j.1472-4642.2011.00821.x

Wilson JR, Dormontt EE, Prentis PJ, Lowe AJ, Richardson DM (2009) Something in the way you move: dispersal pathways affect invasion success. Trends Ecol Evol 24:136–144. https://doi.org/10.1016/j.tree.2008.10.007