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Precipitous Declines in Northern Gulf of Mexico Invasive Lionfish Populations Following the Emergence of an Ulcerative Skin Disease

  • 1.

    Lockwood, J. L., Hoopes, M. F. & Marchetti, M. P. Invasion Ecology, https://doi.org/10.1111/aec.12295 (Wiley‐Blackwell, 2013).

    • Article
    • Google Scholar
  • 2.

    Blackburn, T. M. et al. A unified classification of alien species based on the magnitude of their environmental impacts. PLoS Biol. 12 (2014).

  • 3.

    Kolar, C. S. & Lodge, D. M. Progress in invasion biology: predicting invaders. Trends Ecol. Evol. 16, 199–204 (2001).

  • 4.

    Simberloff, D. & Gibbons, L. Now you see them, now you don’t! – Population crashes of established introduced species. Biol. Invasions 6, 161–172 (2004).

    • Article
    • Google Scholar
  • 5.

    Strayer, D. L. et al. Boom-bust dynamics in biological invasions: towards an improved application of the concept. Ecol. Lett. 20, 1337–1350 (2017).

  • 6.

    Nei, M., Maruyama, T. & Chakraborty, R. The genetic bottleneck effect and genetic variability in populations. Evolution (N. Y). 29, 1–10 (1975).

    • Google Scholar
  • 7.

    Zhan, A. et al. Complex genetic patterns in closely related colonizing invasive species. Ecol. Evol. 2, 1331–1346 (2012).

  • 8.

    Lee, K. A. & Klasing, K. C. A role for immunology in invasion biology. Trends Ecol. Evol. 19, 523–529 (2004).

  • 9.

    Lambrinos, J. G. How interactions between ecology and evolution influence contemporary invasion dynamics. Ecology 85, 2061–2070 (2004).

    • Article
    • Google Scholar
  • 10.

    Lee, C. E. Evolutionary genetics of invasive species. Trends Ecol. Evol. 17, 386–391 (2002).

    • Article
    • Google Scholar
  • 11.

    Peake, J. et al. Feeding ecology of invasive lionfish (Pterois volitans and Pterois miles) in the temperate and tropical western Atlantic. Biol. Invasions 20, 2567–2597 (2018).

    • Article
    • Google Scholar
  • 12.

    Rojas-Vélez, S., Tavera, J. & Acero, A. Unraveling lionfish invasion: is Pterois volitans truly a morphologically novel predator in the Caribbean? Biol. Invasions 21, 1921–1931 (2019).

    • Article
    • Google Scholar
  • 13.

    Barker, B. D., Horodysky, A. Z. & Kerstetter, D. W. Hot or not? Comparative behavioral thermoregulation, critical temperature regimes, and thermal tolerances of the invasive lionfish Pterois sp. versus native western North Atlantic reef fishes. Biol. Invasions 20, 45–58 (2018).

    • Article
    • Google Scholar
  • 14.

    Jud, Z. R., Nichols, P. K. & Layman, C. A. Broad salinity tolerance in the invasive lionfish Pterois spp. may facilitate estuarine colonization. Environ. Biol. Fishes 98, 135–143 (2015).

    • Article
    • Google Scholar
  • 15.

    Fogg, A. Q. et al. Comparison of age and growth parameters of invasive red lionfish (Pterois volitans) across the northern Gulf of Mexico. Fish. Bull. 117, 1–15 (2019).

    • Article
    • Google Scholar
  • 16.

    Gardner, P. G., Frazer, T. K., Jacoby, C. A. & Yanong, R. P. E. Reproductive biology of invasive lionfish (Pterois spp.). Front. Mar. Sci. 2, 7 (2015).

    • Article
    • Google Scholar
  • 17.

    Fogg, A., Brown-Peterson, N. & Peterson, M. Reproductive life history characteristics of invasive red lionfish (Pterois volitans) in the northern Gulf of Mexico. Bull. Mar. Sci. 93, 791–813 (2017).

    • Article
    • Google Scholar
  • 18.

    Green, S. J. & Côté, I. M. Record densities of Indo-Pacific lionfish on Bahamian coral reefs. Coral Reefs 28, 107–107 (2009).

  • 19.

    Dahl, K., Edwards, M. & Patterson, W. F. III Density-dependent condition and growth of invasive lionfish in the northern Gulf of Mexico. Mar. Ecol. Prog. Ser. 623, 145–159 (2019).

  • 20.

    Côté, I. M. & Smith, N. S. The lionfish Pterois sp. invasion: has the worst-case scenario come to pass? J. Fish Biol. 92, 660–689 (2018).

  • 21.

    Hixon, M., Green, S., Albins, M., Akins, J. & Morris, J. Lionfish: a major marine invasion. Mar. Ecol. Prog. Ser. 558, 161–165 (2016).

  • 22.

    Dahl, K. A., Patterson, W. F. III. & Snyder, R. A. 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 (2016).

  • 23.

    Albins, M. Invasive Pacific lionfish Pterois volitans reduce abundance and species richness of native Bahamian coral-reef fishes. Mar. Ecol. Prog. Ser. 522, 231–243 (2015).

  • 24.

    Green, S. J., Akins, J. L., Maljković, A. & Côté, I. M. Invasive lionfish drive Atlantic coral reef fish declines. PLoS One 7, e32596 (2012).

  • 25.

    Lesser, M. P. & Slattery, M. Phase shift to algal dominated communities at mesophotic depths associated with lionfish (Pterois volitans) invasion on a Bahamian coral reef. Biol. Invasions 13, 1855–1868 (2011).

    • Article
    • Google Scholar
  • 26.

    Kindinger, T. L. & Albins, M. A. Consumptive and non-consumptive effects of an invasive marine predator on native coral-reef herbivores. Biol. Invasions 19, (2017).

  • 27.

    Chagaris, D. et al. An ecosystem-based approach to evaluating impacts and management of invasive lionfish. Fisheries 42, 421–431 (2017).

    • Article
    • Google Scholar
  • 28.

    Kulbicki, M. et al. Distributions of Indo-Pacific lionfishes Pterois spp. in their native ranges: implications for the Atlantic invasion. Mar. Ecol. Prog. Ser. 446, 189–205 (2012).

  • 29.

    Darling, E. S., Green, S. J., O’Leary, J. K. & Côté, I. M. Indo-Pacific lionfish are larger and more abundant on invaded reefs: A comparison of Kenyan and Bahamian lionfish populations. Biol. Invasions 13, 2045–2051 (2011).

    • Article
    • Google Scholar
  • 30.

    Benkwitt, C. E. et al. Is the lionfish invasion waning? Evidence from The Bahamas. Coral Reefs 36, 1255–1261 (2017).

  • 31.

    Hackerott, S. et al. Native predators do not influence invasion success of Pacific lionfish on Caribbean reefs. PLoS One 8, e68259 (2013).

  • 32.

    Bejarano, S., Lohr, K., Hamilton, S. & Manfrino, C. Relationships of invasive lionfish with topographic complexity, groupers, and native prey fishes in Little Cayman. Mar. Biol. 162, 253–266 (2015).

    • Article
    • Google Scholar
  • 33.

    Valdivia, A., Bruno, J. F., Cox, C. E., Hackerott, S. & Green, S. J. Re-examining the relationship between invasive lionfish and native grouper in the Caribbean. PeerJ 2, e348 (2014).

  • 34.

    Anton, A., Simpson, M. S. & Vu, I. Environmental and biotic correlates to lionfish invasion success in Bahamian coral reefs. PLoS One 9, e106229 (2014).

  • 35.

    Fogg, A. Q., Ruiz, C. F., Curran, S. S. & Bullard, S. A. Parasites from the red lionfish, Pterois volitans from the Gulf of Mexico. Gulf Caribb. Res. 27, SC 1-5 (2016).

  • 36.

    Sellers, A. J., Ruiz, G. M., Leung, B. & Torchin, M. E. Regional variation in parasite species richness and abundance in the introduced range of the invasive lionfish, Pterois volitans. PLoS One 10, e0131075 (2015).

  • 37.

    Tuttle, L. J., Sikkel, P. C., Cure, K. & Hixon, M. A. Parasite-mediated enemy release and low biotic resistance may facilitate invasion of Atlantic coral reefs by Pacific red lionfish (Pterois volitans). Biol. Invasions 19, 563–575 (2017).

    • Article
    • Google Scholar
  • 38.

    Sikkel, P. C., Tuttle, L. J., Cure, K., Coile, A. M. & Hixon, M. A. Low susceptibility of invasive red lionfish (Pterois volitans) to a generalist ectoparasite in both its introduced and native ranges. PLoS One 9, e95854 (2014).

  • 39.

    Loerch, S. M., McCammon, A. M. & Sikkel, P. C. Low susceptibility of invasive Indo-Pacific lionfish Pterois volitans to ectoparasitic Neobenedenia in the eastern Caribbean. Environ. Biol. Fishes 98, 1979–1985 (2015).

    • Article
    • Google Scholar
  • 40.

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

    • Article
    • Google Scholar
  • 41.

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

  • 42.

    Ingeman, K. E. Lionfish cause increased mortality rates and drive local extirpation of native prey. Mar. Ecol. Prog. Ser. 558, (2016).

  • 43.

    Dahl, K. A. et al. Genotyping confirms significant cannibalism in northern Gulf of Mexico invasive red lionfish, Pterois volitans. Biol. Invasions 20, 3513–3526 (2018).

    • Article
    • Google Scholar
  • 44.

    Benkwitt, C. E. Density-dependent growth in invasive lionfish (Pterois volitans). PLoS One 8, e66995 (2013).

  • 45.

    Pérez-Portela, R. et al. Genetic homogeneity of the invasive lionfish across the Northwestern Atlantic and the Gulf of Mexico based on single nucleotide polymorphisms. Sci. Rep. 8, 5062 (2018).

  • 46.

    Burford Reiskind, M. O. et al. The genomics of invasion: characterization of red lionfish (Pterois volitans) populations from the native and introduced ranges. Biol. Invasions 1–13, https://doi.org/10.1007/s10530-019-01992-0 (2019).

    • Article
    • Google Scholar
  • 47.

    Johnson, J., Bird, C. E., Johnston, M. A., Fogg, A. Q. & Hogan, J. D. Regional genetic structure and genetic founder effects in the invasive lionfish: comparing the Gulf of Mexico, Caribbean and North Atlantic. Mar. Biol. 163, 216 (2016).

    • Article
    • Google Scholar
  • 48.

    White, T. A. & Perkins, S. E. The ecoimmunology of invasive species. Funct. Ecol. 26, 1313–1323 (2012).

    • Article
    • Google Scholar
  • 49.

    Harris, H. E. et al. First report of an emerging ulcerative skin disease in invasive lionfish. UF/IFAS Ext. Electron. Data Inf. Source FA209, 1–7 (2018).

    • Google Scholar
  • 50.

    Ahasan, M. S. et al. Determining the etiology of an emerging ulcerative disease in invasive lionfish. In 8th International Symposium on Aquatic Animal Health, https://doi.org/10.13140/RG.2.2.26050.63680 (2018).

  • 51.

    Harris, H. E., Patterson, W. F. III., Ahrens, R. N. M. & Allen, M. S. Detection and removal efficiency of invasive lionfish in the northern Gulf of Mexico. Fish. Res. 213, 22–32 (2019).

    • Article
    • Google Scholar
  • 52.

    Dahl, K. A. & Patterson, W. F. Habitat-specific density and diet of rapidly expanding invasive red lionfish, Pterois volitans, populations in the northern Gulf of Mexico. PLoS One 9, e105852 (2014).

  • 53.

    Karnauskas, M. et al. Red snapper distribution on natural habitats and artificial structures in the northern Gulf of Mexico. Mar. Coast. Fish. 9, 50–67 (2017).

    • Article
    • Google Scholar
  • 54.

    Johnson, E. G. & Swenarton, M. K. Age, growth and population structure of invasive lionfish (Pterois volitans/miles) in northeast Florida using a length-based, age-structured population model. PeerJ 4, e2730 (2016).

  • 55.

    Barbour, A. B., Allen, M. S., Frazer, T. K. & Sherman, K. D. Evaluating the potential efficacy of invasive lionfish (Pterois volitans) removals. PLoS One 6, (2011).

  • 56.

    Morris, J. A., Shertzer, K. W. & Rice, J. A. A stage-based matrix population model of invasive lionfish with implications for control. Biol. Invasions 13, 7–12 (2011).

    • Article
    • Google Scholar
  • 57.

    Ramsay, J. M., Watral, V., Schreck, C. B. & Kent, M. L. Pseudoloma neurophilia infections in zebrafish (Danio rerio): effects of stress on survival, growth, and reproduction. Dis. Aquat. Organ. 88, 69–84 (2009).

  • 58.

    Ellis, R. & Faletti, M. Native grouper indirectly ameliorates the negative effects of invasive lionfish. Mar. Ecol. Prog. Ser. 558, 267–279 (2016).

  • 59.

    Diller, J. L., Frazer, T. K. & Jacoby, C. A. Coping with the lionfish invasion: evidence that naïve, native predators can learn to help. J. Exp. Mar. Bio. Ecol. 455, 45–49 (2014).

    • Article
    • Google Scholar
  • 60.

    Maljković, A., Van Leeuwen, T. E. & Cove, S. N. Predation on the invasive red lionfish, Pterois volitans (Pisces: Scorpaenidae), by native groupers in the Bahamas. Coral Reefs 27, 501–501 (2008).

  • 61.

    Mumby, P. J., Harborne, A. R. & Brumbaugh, D. R. Grouper as a natural biocontrol of invasive lionfish. PLoS One 6, 2–5 (2011).

  • 62.

    Green, S. J. et al. Linking removal targets to the ecological effects of invaders: a predictive model and field test. Ecol. Appl. 24, 1311–1322 (2014).

  • 63.

    Harms-Tuohy, C., Appeldoorn, R. & Craig, M. The effectiveness of small-scale lionfish removals as a management strategy: effort, impacts and the response of native prey and piscivores. Manag. Biol. Invasions 9, 149–162 (2018).

    • Article
    • Google Scholar
  • 64.

    Morris, J. A., Shertzer, K. W. & Rice, J. A. A stage-based matrix population model of invasive lionfish with implications for control. Biol. Invasions 13, 7–12 (2010).

    • Article
    • Google Scholar
  • 65.

    Smith, N. S., Green, S. J., Akins, J. L., Miller, S. & Côté, I. M. Density-dependent colonization and natural disturbance limit the effectiveness of invasive lionfish culling efforts. Biol. Invasions 19, 2385–2399 (2017).

    • Article
    • Google Scholar
  • 66.

    Johnston, M. W. & Purkis, S. J. Hurricanes accelerated the Florida-Bahamas lionfish invasion. Glob. Chang. Biol. 21, 2249–2260 (2015).

  • 67.

    Johnston, M. & Purkis, S. A coordinated and sustained international strategy is required to turn the tide on the Atlantic lionfish invasion. Mar. Ecol. Prog. Ser. 533, 219–235 (2015).

  • 68.

    Johnston, M. W., Bernard, A. M. & Shivji, M. S. Forecasting lionfish sources and sinks in the Atlantic: are Gulf of Mexico reef fisheries at risk? Coral Reefs 36, 169–181 (2017).

  • 69.

    Stevens, J. L. & Olson, J. B. Invasive lionfish harbor a different external bacterial community than native Bahamian fishes. Coral Reefs 32, 1113–1121 (2013).

  • 70.

    Stevens, J., Jackson, R. & Olson, J. Bacteria associated with lionfish (Pterois volitans/miles complex) exhibit antibacterial activity against known fish pathogens. Mar. Ecol. Prog. Ser. 558, 167–180 (2016).

  • 71.

    Torchin, M. E., Lafferty, K. D., Dobson, A. P., McKenzie, V. J. & Kuris, A. M. Introduced species and their missing parasites. Nature 421, 628–630 (2003).

  • 72.

    Torchin, M. E., Lafferty, K. D. & Kuris, A. M. Parasites and marine invasions. Parasitology 124, 137–151 (2002).

    • Article
    • Google Scholar
  • 73.

    Blakeslee, A. M. H., Fowler, A. E. & Keogh, C. L. Marine invasions and parasite escape: updates and new perspectives. Adv. Mar. Biol. 66, 87–169 (2013).

  • 74.

    Gendron, A. D., Marcogliese, D. J. & Thomas, M. Invasive species are less parasitized than native competitors, but for how long? The case of the round goby in the Great Lakes-St. Lawrence Basin. Biol. Invasions 14, 367–384 (2012).

    • Article
    • Google Scholar
  • 75.

    Peiffer, F., Bejarano, S., Palavicini de Witte, G. & Wild, C. Ongoing removals of invasive lionfish in Honduras and their effect on native Caribbean prey fishes. PeerJ 5, e3818 (2017).

  • 76.

    Klein, D. R. The introduction, increase, and crash of reindeer on St. Matthew Island. J. Wildl. Manage. 32, 350 (1968).

    • Article
    • Google Scholar
  • 77.

    Kelly, D. W., Paterson, R. A., Townsend, C. R., Poulin, R. & Tompkins, D. M. Parasite spillback: a neglected concept in invasion ecology? Ecology 90, 2047–2056 (2009).

  • 78.

    Ziskowski, J. J. et al. Disease in commercially valuable fish stocks in the Northwest Atlantic. Mar. Pollut. Bull. 18, 496–504 (1987).

    • Article
    • Google Scholar
  • 79.

    Murawski, S. A., Hogarth, W. T., Peebles, E. B. & Barbeiri, L. Prevalence of external skin lesions and polycyclic aromatic hydrocarbon concentrations in Gulf of Mexico fishes, post-Deepwater. Horizon. Trans. Am. Fish. Soc. 143, 1084–1097 (2014).

  • 80.

    Pace, M. L., Strayer, D. L., Fischer, D. & Malcom, H. M. Recovery of native zooplankton associated with increased mortality of an invasive mussel. Ecosphere 1 (2010).

  • 81.

    Ratcliffe, F. N., Myers, K., Fennessy, B. V. & Calaby, J. H. Myxomatosis in Australia: a step towards the biological control of the rabbit. Nature 170, 7–11 (1952).

  • 82.

    Mutze, G., Cooke, B. & Alexander, P. The initial impact of rabbit hemorrhagic disease on European rabbit populations in South Australia. J. Wildl. Dis. 34, 221–227 (1998).

  • 83.

    Kerr, P. J. Myxomatosis in Australia and Europe: a model for emerging infectious diseases. Antiviral Res. 93, 387–415 (2012).

  • 84.

    Mutze, G. et al. Recovery of South Australian rabbit populations from the impact of rabbit haemorrhagic disease. Wildl. Res. 41, 552 (2014).

    • Article
    • Google Scholar
  • 85.

    Mutze, G., Bird, P., Cooke, B. & Henzell, R. Geographic and seasonal variation in the impact of rabbit haemorrhagic disease on European rabbits, Oryctolagus cuniculus, and rabbit damage in Australia. in Lagomorph Biology 279–293, https://doi.org/10.1007/978-3-540-72446-9_19 (Springer Berlin Heidelberg, 2008).

    • Google Scholar
  • 86.

    Kitchens, L. L. et al. Occurrence of invasive lionfish (Pterois volitans) larvae in the northern Gulf of Mexico: characterization of dispersal pathways and spawning areas. Biol. Invasions 19, 1971–1979 (2017).

    • Article
    • Google Scholar
  • 87.

    Frazer, T. K., Jacoby, C. A., Edwards, M. A., Barry, S. C. & Manfrino, C. M. Coping with the lionfish invasion: can targeted removals yield beneficial effects? Rev. Fish. Sci. 20, 185–191 (2012).

    • Article
    • Google Scholar
  • 88.

    Ogle, D. H. Weight-Length Relationships. in Introductory Fisheries Analyses with R 131–152 (Chapman and Hall/CRC, 2019). doi:10.1201/9781315371986-7.

    • Google Scholar
  • 89.

    Le Cren, E. D. The length-weight relationship and seasonal cycle in gonad weight and condition in the Perch (Perca fluviatilis). J. Anim. Ecol. 20, 201 (1951).

    • Article
    • Google Scholar
  • 90.

    Froese, R. Cube law, condition factor and weight-length relationships: history, meta-analysis and recommendations. J. Appl. Ichthyol. 22, 241–253 (2006).

    • Article
    • Google Scholar
  • 91.

    Neumann, R. M. & Allen, M. S. Size Structure. In Analysis and Interpretation of Freshwater Fisheries Data (eds. Guy, C. S. & Brown, M. L.) (American Fisheries Society, 2007).

  • 92.

    Bolker, B. M. et al. Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol. Evol. 24, 127–135 (2009).

    • Article
    • Google Scholar
  • 93.

    Patterson, W. F. III., Dance, M. A. & Addis, D. T. Development of a remotely operated vehicle based methodology to estimate fish community structure at artificial reef sites in the northern Gulf of Mexico. Proc. 61st Gulf Caibb. Fish. Inst. 263–270 (2009).

  • 94.

    Patterson, W. F. III., Tarnecki, J. H., Addis, D. T. & Barbieri, L. R. Reef fish community structure at natural versus artificial reefs in the northern Gulf of Mexico. Proc. 66th Gulf Caribb. Fish. Inst. 4–8 (2013).

  • 95.

    Florida Fish and Wildlife Conservation Commission. 2010–2018 commercial fishery landings data through batch 1402, https://myfwc.com/research/saltwater/fishstats/commercial-fisheries/landings-in-florida/ (2019).


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