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Density-dependent colonization and natural disturbance limit the effectiveness of invasive lionfish culling efforts

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Abstract

Culling can be an effective management tool for reducing populations of invasive species to levels that minimize ecological effects. However, culling is labour-intensive, costly, and may have unintended ecological consequences. In the Caribbean, culling is widely used to control invasive Indo-Pacific lionfish, Pterois volitans and P. miles, but the effectiveness of infrequent culling in terms of reducing lionfish abundance and halting native prey decline is unclear. In a 21-month-long field experiment on natural reefs, we found that culling effectiveness changed after the passage of a hurricane part-way through the experiment. Before the hurricane, infrequent culling resulted in substantial reductions in lionfish density (60–79%, on average, albeit with large uncertainty) and slight increases in native prey species richness, but was insufficient to stem the decline in native prey biomass. Culling every 3 months (i.e., quarterly) and every 6 months (i.e., biannually) had similar effects on lionfish density and native prey fishes because of high rates of lionfish colonization among reefs. After the hurricane, lionfish densities were greater on all culled reefs compared to non-culled reefs, and prey biomass declined by 92%, and species richness by 71%, on biannually culled reefs. The two culling frequencies we examined therefore seem to offer a poor trade-off between the demonstrated conservation gains that can be achieved with frequent culling and the economy of time and money realized by infrequent culling. Moreover, stochastic events such as hurricanes can drastically limit the effectiveness of culling efforts.

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References

  • Abrams PA, Quince C (2005) The impact of mortality on predator population size and stability in systems with stage-structured prey. Theor Popul Biol 68:253–266. doi:10.1016/j.tpb.2005.05.004

    Article  PubMed  Google Scholar 

  • Adams AJ, Ebersole JP (2004) Resistance of coral reef fishes in back reef and lagoon habitats to a hurricane. Bull Mar Sci 75:101–113

    Google Scholar 

  • Akins JL (2012) Control strategies: tools and techniques for local control. In Morris JA (ed.) Invasive lionfish: a guide to control and management, pp. 24–50. Gulf and Caribbean Fisheries Institute Special Publication Series Number 1, Marathon, 133 pp

  • Albins MA (2013) Effects of invasive Pacific red lionfish Pterois volitans versus a native predator on Bahamian coral-reef fish communities. Biol Invasions 15:29–43

    Article  Google Scholar 

  • Albins MA (2015) Invasive Pacific lionfish Pterois volitans reduce abundance and species richness of native Bahamian coral-reef fishes. Mar Ecol Prog Ser 522:231–243. doi:10.3354/meps11159

    Article  Google Scholar 

  • Albins MA, Hixon MA (2008) Invasive Indo-Pacific lionfish Pterois volitans reduce recruitment of Atlantic coral-reef fishes. Mar Ecol Prog Ser 367:233–238

    Article  Google Scholar 

  • Andradi-Brown DA, Vermeij MJA, Slattery M et al (2017) Large-scale invasion of western Atlantic mesophotic reefs by lionfish potentially undermines culling-based management. Biol Invasions 19:939–954

    Article  Google Scholar 

  • Arias-González JE, González-Gándara C, Cabrera JL, Christensen V (2011) Predicted impact of the invasive lionfish Pterois volitans on the food web of a Caribbean coral reef. Environ Research 111:917–925

    Article  Google Scholar 

  • Barbour AB, Allen MS, Frazer TK, Sherman KD (2011) Evaluating the potential efficacy of invasive lionfish (Pterois volitans) removals. PLoS ONE 6(5):e19666. doi:10.1371/journal.pone.0019666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bartoń K (2016) MuMIn: multi-model inference. R package version 1.15.6. https://CRAN.Rproject.org/package=MuMIn

  • Beecher H (1973) Effects of a hurricane on a shallow-water population of damselfish, Pomacentrus variabilis. Copeia 1973:613–615

    Article  Google Scholar 

  • Benkwitt CE (2015) Non-linear effects of invasive lionfish density on native coral-reef fish communities. Biol Invasions 17:1383–1395

    Article  Google Scholar 

  • Benkwitt CE (2016a) Central-place foraging and ecological effects of an invasive predator across multiple habitats. Ecology 97:2729–2739

    Article  PubMed  Google Scholar 

  • Benkwitt CE (2016b) Invasive lionfish increase activity and foraging movements at greater local densities. Mar Ecol Prog Ser 558:255–266

    Article  Google Scholar 

  • Benton TG, Cameron TC, Grant A (2004) Population responses to perturbations: predictions and responses from laboratory mite populations. J Animal Ecol 73:983–995

    Article  Google Scholar 

  • Bolker B, Su YS (2011) Coefplot2: coefficient plots, R package version 0.1.3.2. http://CRAN.Rproject.org/package=coefplot2

  • Borski RJ, Hodson RG (2003) Fish research and the institutional animal care and use committee. ILAR J 44:286–294. doi:10.1093/ilar.44.4.286

    Article  CAS  PubMed  Google Scholar 

  • Brook LA, Johnson CN, Ritchie EG (2012) Effects of predator control on behaviour of an apex predator and indirect consequences for mesopredator suppression. J Appl Ecol 49:1278–1286. doi:10.1111/j.1365-2664.2012.02207.x

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  • Cameron TC, Benton TG (2004) Stage-structured harvesting and its effects: an empirical investigation using soil mites. J Anim Ecol 73:996–1006

    Article  Google Scholar 

  • Campbell K, Donlan CJ (2005) Feral goat eradications on islands. Conserv Biol 19:1362–1374. doi:10.1111/j.1523-1739.2005.00228.x

    Article  Google Scholar 

  • Caselle JE, Warner RR (1996) Variability in recruitment of coral reef fishes: the importance of habitat at two spatial scales. Ecology 77:2488–2504

    Article  Google Scholar 

  • Cheal AJ, Coleman G, Delean S et al (2002) Responses of coral and fish assemblages to a severe but short-lived tropical cyclone on the Great Barrier Reef, Australia. Coral Reefs 21:131–142

    Google Scholar 

  • Costantino R, Desharnais R, Cushing J, Dennis B (1997) Chaotic dynamics in an insect population. Science 275:389–391. doi:10.1126/science.275.5298.389

    Article  CAS  PubMed  Google Scholar 

  • Côté IM, Green SJ, Hixon M (2013) Predatory fish invaders: insights from Indo-Pacific lionfish in the western Atlantic and Caribbean. Biol Conserv 164:50–61. doi:10.1016/j.biocon.2013.04.014

    Article  Google Scholar 

  • Côté IM, Darling ES, Malpica-Cruz L et al (2014) What doesn’t kill you makes you wary? Effect of repeated culling on the behaviour of an invasive predator. PLoS ONE 9:e94248. doi:10.1371/journal.pone.0094248

    Article  PubMed  PubMed Central  Google Scholar 

  • Cruz F, Josh Donlan C, Campbell K, Carrion V (2005) Conservation action in the Galapagos: Feral pig (Sus scrofa) eradication from Santiago Island. Biol Conserv 121:473–478. doi:10.1016/j.biocon.2004.05.018

    Article  Google Scholar 

  • Cure K, Benkwitt CE, Kindinger TL et al (2012) Comparative behavior of red lionfish Pterois volitans on native Pacific versus invaded Atlantic coral reefs. Mar Ecol Prog Ser 467:181–192

    Article  Google Scholar 

  • Dahl KA, Patterson WF (2014) Habitat-specific density and diet of rapidly expanding invasive red lionfish, Pterois volitans, populations in the northern Gulf of Mexico. PLoS ONE 9(8):e105852. doi:10.1371/journal.pone.0105852

    Article  PubMed  PubMed Central  Google Scholar 

  • Dahl KA, Patterson WF, Snyder RA (2016) Experimental assessment of lionfish removals to mitigate reef fish community shifts on northern Gulf of Mexico artificial reefs. Mar Ecol Prog Ser 558:207–221. doi:10.3354/meps11898

    Article  Google Scholar 

  • de León R, Vane K, Bertuol P et al (2013) Effectiveness of lionfish removal efforts in the southern Caribbean. Endanger Species Res 22:175–182

    Article  Google Scholar 

  • De Roos AM, Schellekens T, van Kooten T et al (2007) Food-dependent growth leads to overcompensation in stage-specific biomass when mortality increases: the influence of maturation versus reproduction regulation. Am Nat 170:E59–E76. doi:10.1086/520119

    Article  PubMed  Google Scholar 

  • Doherty TS, Ritchie EG (2016) Stop jumping the gun: a call for evidence-based invasive predator management. Conserv Lett 10(1):1–8. doi:10.1111/conl.12251

    Google Scholar 

  • Frazer TK, Jacoby C, Edwards M et al (2012) Coping with the lionfish invasion: can targeted removals yield beneficial effects? Rev Fish Sci 20:185–191. doi:10.1080/10641262.2012.700655

    Article  Google Scholar 

  • Froese R, Pauly D (eds) (2016) FishBase. World Wide Web electronic publication. www.fishbase.org, version (10/2016)

  • Green SJ, Akins JL, Côté IM (2011) Foraging behaviour and prey consumption in the Indo-Pacific lionfish on Bahamian coral reefs. Mar Ecol Prog Ser 433:159–167. doi:10.3354/meps09208

    Article  Google Scholar 

  • Green SJ, Akins JL, Maljković A, Côté IM (2012) Invasive lionfish drive Atlantic coral reef fish declines. PLoS ONE 7:e32596. doi:10.1371/journal.pone.0032596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Green SJ, Tamburello N, Miller SE et al (2013) Habitat complexity and fish size affect the detection of Indo-Pacific lionfish on invaded coral reefs. Coral Reefs 32:413–421. doi:10.1007/s00338-012-0987-8

    Article  Google Scholar 

  • Green SJ, Dulvy NK, Brooks ALM et al (2014) Linking removal targets to the ecological effects of invaders: a predictive model and field test. Ecol Appl 24:1311–1322

    Article  Google Scholar 

  • Harmelin-Vivien ML (1994) The effects of storms and cyclones on coral reefs: a review. J Coast Res 12:211–231

    Google Scholar 

  • Ingeman KE (2016) Lionfish cause increased mortality rates and drive local extirpation of native prey. Mar Ecol Prog Ser 558:235–245. doi:10.3354/meps11821

    Article  Google Scholar 

  • Johnston MW, Purkis SJ (2015a) A coordinated and sustained international strategy is required to turn the tide on the Atlantic lionfish invasion. Mar Ecol Prog Ser 533:219–235. doi:10.3354/meps11399

    Article  Google Scholar 

  • Johnston MW, Purkis SJ (2015b) Hurricanes accelerated the Florida–Bahamas lionfish invasion. Glob Chang Biol 21:2249–2260. doi:10.1111/gcb.12874

    Article  PubMed  Google Scholar 

  • Kaufman SL (1983) Coral reefs effects of Hurricane Allen on reef fish assemblages. Coral Reefs 2:43–47

    Article  Google Scholar 

  • Lieury N, Ruette S, Devillard S et al (2015) Compensatory immigration challenges predator control: an experimental evidence-based approach improves management. J Wildl Manag 79:425–434

    Article  Google Scholar 

  • Mazerolle MJ (2016) AICcmodavg: model selection and multimodel inference based on (Q)AIC(c). R package version 2.0-4. https://cran.r-project.org/package=AICcmodavg

  • Morris J Jr (ed) (2012) Invasive lionfish: a guide to control and management. Gulf and Caribbean Fisheries Instituute, Marathon

    Google Scholar 

  • Morris J, Akins JL (2009) Feeding ecology of invasive lionfish (Pterois volitans) in the Bahamian archipelago. Environ Biol Fishes 86:389–398. doi:10.1007/s10641-009-9538-8

    Article  Google Scholar 

  • Morris JA, Shertzer KW, Rice JA (2011) A stage-based matrix population model of invasive lionfish with implications for control. Biol Invasions 13:7–12. doi:10.1007/s10530-010-9786-8

    Article  Google Scholar 

  • Muñoz RC, Currin CA, Whitfield PE (2011) Diet of invasive lionfish on hard bottom reefs of the Southeast USA: insights from stomach contents and stable isotopes. Mar Ecol Prog Ser 432:181–193. doi:10.3354/meps09154

    Article  Google Scholar 

  • Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142. doi:10.1111/j.2041-210x.2012.00261.x

    Article  Google Scholar 

  • Nogales M, Martín A, Tershy BR et al (2004) A review of feral cat eradication on islands. Conserv Biol 18:310–319

    Article  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D and R Core Team (2016) nlme: linear and nonlinear mixed effects models. R package version 3.1-127. https://CRAN.R-project.org/package=nlme

  • Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists, first. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. http://www.R-project.org

  • Sale PF, Sharp BJ (1983) Correction for bias in visual transect censuses of coral reef fishes. Coral Reefs 2:37–42. doi:10.1007/BF00304730

    Article  Google Scholar 

  • Smith RK, Pullin AS, Stewart GB, Sutherland WJ (2010) Effectiveness of predator removal for enhancing bird populations. Conserv Biol 24:820–829. doi:10.1111/j.1523-1739.2009.01421.x

    Article  PubMed  Google Scholar 

  • Tamburello N, Côté LM (2015) Movement ecology of Indo-Pacific lionfish on Caribbean coral reefs and its implications for invasion dynamics. Biol Invasions 17:1639–1653

    Article  Google Scholar 

  • Tracey SR, Baulch T, Hartmann K et al (2015) Systematic culling controls a climate driven, habitat modifying invader. Biol Invasions 17:1885–1896. doi:10.1007/s10530-015-0845-z

    Article  Google Scholar 

  • Walsh WJ (1983) Stability of a coral reef fish community following a catastrophic storm. Coral Reefs 2:49–63

    Article  Google Scholar 

  • Wantiez L, Chateau O, Le Mouellic S (2006) Initial and mid-term impacts of cyclone Erica on coral reef fish communities and habitat in the South Lagoon Marine Park of New Caledonia. J Mar Biol Assoc U K 86:1229–1236

    Article  Google Scholar 

  • Weidel BC, Josephson DC, Kraft CE (2007) Littoral fish community response to smallmouth bass removal from an adirondack lake. Trans Am Fish Soc 136:778–789. doi:10.1577/T06-091.1

    Article  Google Scholar 

  • Whitlock M, Schulter D (2008) The analysis of biological data, first. Roberts and Company Publishers, Greenwood Village

    Google Scholar 

  • Wickham H (2007) Reshaping data with the reshape package. J Stat Software 21:1–20

    Article  Google Scholar 

  • Woodley JD, Chornesky EA, Cliffo PA, Sid EM (1981) Hurricane Allen’s impact on Jamaican coral reefs. Science 214(80):749–755

    Article  CAS  PubMed  Google Scholar 

  • Zipkin EF, Sullivan PJ, Cooch EG et al (2008) Overcompensatory response of a smallmouth bass (Micropterus dolomieu) population to harvest: release from competition? Can J Fish Aquat Sci 65:2279–2292. doi:10.1139/F08-133

    Article  Google Scholar 

  • Zipkin EF, Kraft CE, Cooch EG, Sullivan PJ (2009) When can nuisance and invasive species control efforts backfire? Ecol Appl 19:1585–1595

    Article  PubMed  Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Book  Google Scholar 

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Acknowledgements

We are grateful to Jocelyn Curtis-Quick and interns at the Cape Eleuthera Institute for assistance in the field, and to the Earth to Ocean Research Group and Stats-Beerz study group for discussions on statistical analyses. Administrative and logistical support was provided by The Bahamas Department of Marine Resources, The Centre for Agriculture and Bioscience International, and the Cape Eleuthera Institute. Funding was provided by a Global Environment Facility-United Nations Environment Program grant to The Bahamas Department of Marine Resources, an Organization of American States Academic Graduate Scholarship to NSS, a Canada Graduate Fellowship from the Natural Sciences and Engineering Research Council (NSERC) of Canada to SG, and an NSERC Discovery grant to IMC.

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  1. Stephanie J. Green

    Present address: Center for Ocean Solutions, Stanford University, Monterey, CA, 93940, USA

Authors and Affiliations

  1. Earth to Ocean Research Group, Department of Biological Sciences, Simon Fraser University, Burnaby, BC, V5A 1S6, Canada

    Nicola S. Smith, Stephanie J. Green & Isabelle M. Côté

  2. Reef Environmental Education Foundation, 98300 Overseas Highway, Key Largo, FL, 33037, USA

    John L. Akins

  3. Cape Eleuthera Institute, Rock Sound, Eleuthera, Bahamas

    Skylar Miller

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  1. Nicola S. Smith
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Correspondence to Nicola S. Smith.

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Smith, N.S., Green, S.J., Akins, J.L. et al. Density-dependent colonization and natural disturbance limit the effectiveness of invasive lionfish culling efforts. Biol Invasions 19, 2385–2399 (2017). https://doi.org/10.1007/s10530-017-1449-6

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