Large-scale invasion of western Atlantic mesophotic reefs by lionfish potentially undermines culling-based management

Abstract

The detrimental effects of invasive lionfishes (Pterois volitans and Pterois miles) on western Atlantic shallow reefs are well documented, including declines in coral cover and native fish populations, with disproportionate predation on critically endangered reef fish in some locations. Yet despite individuals reaching depths >100 m, the role of mesophotic coral ecosystems (MCEs; reefs 30–150 m) in lionfish ecology has not been addressed. With lionfish control programs in most invaded locations limited to 30 m by diving restrictions, understanding the role of MCEs in lionfish distributions remains a critical knowledge gap potentially hindering conservation management. Here we synthesise unpublished and previously published studies of lionfish abundance and body length at paired shallow reef (0–30 m) and MCE sites in 63 locations in seven western Atlantic countries and eight sites in three Indo-Pacific countries where lionfish are native. Lionfish were found at similar abundances across the depth gradient from shallow to adjacent MCEs, with no difference between invaded and native sites. Of the five invaded countries where length data were available three had larger lionfish on mesophotic than shallow reefs, one showed no significant difference, while the fifth represented a recently invaded site. This suggests at least some mesophotic populations may represent extensions of natural ontogenetic migrations. Interestingly, despite their shallow focus, in many cases culling programs did not appear to alter abundance between depths. In general, we identify widespread invasive lionfish populations on MCE that could be responsible for maintaining high densities of lionfish recruits despite local shallow-biased control programs. This study highlights the need for management plans to incorporate lionfish populations below the depth limit of recreational diving in order to address all aspects of the local population and maximise the effectiveness of control efforts.

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References

  1. Ahrenholz DW, Morris JA (2010) Larval duration of the lionfish, Pterois volitans along the Bahamian Archipelago. Environ Biol Fish 88:305–309. doi:10.1007/s10641-010-9647-4

    Article  Google Scholar 

  2. Akins JL, Morris JA Jr, Green SJ (2014) In situ tagging technique for fishes provides insight into growth and movement of invasive lionfish. Ecol Evol 4:3768–3777. doi:10.1002/ece3.1171

    Article  PubMed  PubMed Central  Google Scholar 

  3. 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 

  4. Andradi-Brown D, Laverick J, Bejarano I et al (2016) Threats to mesophotic coral ecosystems and management options. In: Baker EK, Puglise KA, Harris PT (eds) Mesophotic coral ecosystems—a lifeboat for coral reefs?. The United Nations Environment Programme and GRID-Arendal, Nairobi and Arendal

    Google Scholar 

  5. Appeldoorn RS, Friedlander A, Sladek Nowlis J et al (2003) Habitat connectivity in reef fish communities and marine reserve design in Old Providence-Santa Catalina, Colombia. Gulf Caribb Res 14:61–77

    Google Scholar 

  6. Arias-González JE, González-Gándara C, Luis Cabrera J, Christensen V (2011) Predicted impact of the invasive lionfish Pterois volitans on the food web of a Caribbean coral reef. Environ Res 111:917–925. doi:10.1016/j.envres.2011.07.008

    Article  PubMed  Google Scholar 

  7. Bejarano I, Appeldoorn RS, Nemeth M (2014a) Fishes associated with mesophotic coral ecosystems in La Parguera, Puerto Rico. Coral Reefs 33:313–328. doi:10.1007/s00338-014-1125-6

    Article  Google Scholar 

  8. Bejarano S, Lohr K, Hamilton S, Manfrino C (2014b) Relationships of invasive lionfish with topographic complexity, groupers, and native prey fishes in Little Cayman. Mar Biol. doi:10.1007/s00227-014-2595-3

    Google Scholar 

  9. Benkwitt CE (2013) Density-Dependent Growth in Invasive Lionfish (Pterois volitans). PLoS ONE 8:e66995. doi:10.1371/journal.pone.0066995

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. Bogdanoff AK, Akins JL, Morris JA 2013 GCFI Lionfish Workgroup (2014) invasive lionfish in the marketplace: challenges and opportunities. In: Proceedings of the 66th Gulf and Caribbean Fisheries Institute November 4–8, 2013, vol 66. Corpus Christi, Texas USA, pp 140–147

  11. Brokovich E, Einbinder S, Shashar N et al (2008) Descending to the twilight-zone: changes in coral reef fish assemblages along a depth gradient down to 65 m. Mar Ecol Prog Ser 371:253–262. doi:10.3354/meps07591

    Article  Google Scholar 

  12. Claydon J, Calosso MC, Traiger SB (2012) Progression of invasive lionfish in seagrass, mangrove and reef habitats. Mar Ecol Prog Ser 448:119–129. doi:10.3354/meps09534

    Article  Google Scholar 

  13. Coates KA, Fourqurean JW, Kenworthy WJ et al (2013) Introduction to Bermuda: geology, oceanography and climate. In: Sheppard CRC (ed) Coral reefs of the United Kingdom overseas territories, coral reefs of the world 4. Springer, Berlin, pp 115–133

    Google Scholar 

  14. Côté IM, Green SJ, Hixon MA (2013) Predatory fish invaders: insights from Indo-Pacific lionfish in the western Atlantic and Caribbean. Biol Conserv 164:50–61

    Article  Google Scholar 

  15. 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 

  16. Darling ES, Green SJ, O’Leary JK, Côté IM (2011) Indo-Pacific lionfish are larger and more abundant on invaded reefs: a comparison of Kenyan and Bahamian lionfish populations. Biol Invasions 13:2045–2051. doi:10.1007/s10530-011-0020-0

    Article  Google Scholar 

  17. de León R, Vane K, Bertuol P et al (2013) Effectiveness of lionfish removal efforts in the southern Caribbean. Endang Species Res 22:175–182. doi:10.3354/esr00542

    Article  Google Scholar 

  18. Ferreira CEL, Luiz OJ, Floeter SR et al (2015) first record of invasive lionfish (Pterois volitans) for the Brazilian coast. PLoS ONE 10:e0123002. doi:10.1371/journal.pone.0123002.g002

    Article  PubMed  PubMed Central  Google Scholar 

  19. Frazer TK, Jacoby CA, Edwards MA 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 

  20. Freshwater DW, Hamner RM, Parham S, Wilbur AE (2009) Molecular evidence that the lionfishes Pterois miles and Pterois volitans are distinct species. J N C Acad Sci 125:39–46

    CAS  Google Scholar 

  21. Gratwicke B, Speight MR (2005) The relationship between fish species richness, abundance and habitat complexity in a range of shallow tropical marine habitats. J Fish Biol 66:650–667. doi:10.1111/j.0022-1112.2005.00629.x

    Article  Google Scholar 

  22. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. 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 

  24. Green SJ, Dulvy NK, Brooks AML et al (2014) Linking removal targets to the ecological effects of invaders: a predictive model and field test. Ecol Appl 24:1311–1322. doi:10.1890/13-0979.1

    Article  Google Scholar 

  25. Grol MGG, Rypel AL, Nagelkerken I (2014) Growth potential and predation risk drive ontogenetic shifts among nursery habitats in a coral reef fish. Mar Ecol Prog Ser 502:229–244

    Article  Google Scholar 

  26. Hedges LV, Olkin I (1985) Statistical method for meta-analysis. Academic Press, Orlando

    Google Scholar 

  27. Higgins JPT, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558. doi:10.1002/sim.1186

    Article  PubMed  Google Scholar 

  28. Hinderstein LM, Marr JCA, Martinez FA et al (2010) Theme section on “Mesophotic coral ecosystems: characterization, ecology, and management”. Coral Reefs 29:247–251. doi:10.1007/s00338-010-0614-5

    Article  Google Scholar 

  29. Kimball ME, Miller J, Whitfield PE, Hare JA (2004) Thermal tolerance and potential distribution of invasive lionfish (Pterois volitans/miles complex) on the east coast of the United States. Mar Ecol Prog Ser 283:269–278

    Article  Google Scholar 

  30. Kimirei IA, Nagelkerken I, Trommelen M et al (2013) What drives ontogenetic niche shifts of fishes in coral reef ecosystems? Ecosystems 16:783–796. doi:10.1007/s10021-013-9645-4

    Article  Google Scholar 

  31. Koricheva J, Gurevitch J, Mengersen K (2013) Handbook of meta-analysis in ecology and evolution, 1st edn. Princeton University Press, Princeton

    Google Scholar 

  32. Kulbicki M, Beets J, Chabanet P et al (2012) Distributions of Indo-Pacific lionfishes Pterois spp. in their native ranges: implications for the Atlantic invasion. Mar Ecol Prog Ser 446:189–205. doi:10.3354/meps09442

    Article  Google Scholar 

  33. Lee S, Buddo DSA, Aiken KA (2012) Habitat preference in the invasive lionfish (Pterois volitans/miles) in Discovery Bay, Jamaica: use of GIS in management strategies. In: Proceedings of the 64rd Gulf and Caribbean Fisheries Institute October 31 November 5, 2011, vol 64. Puerto Morelos, Mexico, pp 39–48

  34. Lesser MP, Slattery M (2011) 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. doi:10.1007/s10530-011-0005-z

    Article  Google Scholar 

  35. Lindfield SJ, McIlwain JL, Harvey ES (2014) Depth refuge and the impacts of SCUBA spearfishing on coral reef fishes. PLoS ONE 9:e92628. doi:10.1371/journal.pone.0092628

    Article  PubMed  PubMed Central  Google Scholar 

  36. McTee SA, Grubich JR (2014) Native densities, distribution, and diurnal activity of Red Sea lionfishes (Scorpaenidae). Mar Ecol Prog Ser 508:223–232. doi:10.3354/meps10847

    Article  Google Scholar 

  37. Mitchell SJ, Doolette DJ (2013) Recreational technical diving part 1: an introduction to technical diving methods and activities. Diving Hyperb Med 43:86–93

    PubMed  Google Scholar 

  38. Molnar JL, Gamboa RL, Revenga C, Spalding MD (2008) Assessing the global threat of invasive species to marine biodiversity. Front Ecol Environ 6:485–492

    Article  Google Scholar 

  39. Morris JA, Akins JL, Barse A et al (2009) Biology and ecology of the invasive lionfishes, Pterois miles and Pterois volitans. Proc Gulf Caribb Fish Inst 61:409–414

    Google Scholar 

  40. Morris JA, Thomas A, Rhyne AL, Breen N, Akins L, Nash B (2011) Nutritional properties of the invasive lionfish: a delicious and nutritious approach for controlling the invasion. AACL Bioflux 4:21–26

    Google Scholar 

  41. Nuttall MF, Johnston MA, Eckert RJ et al (2014) Lionfish (Pterois volitans [Linnaeus, 1758] and P. miles [Bennett, 1828]) records within mesophotic depth ranges on natural banks in the Northwestern Gulf of Mexico. BioInvasions Rec 3:111–115

    Article  Google Scholar 

  42. Pitt JM, Trott TM (2015) Trapping lionfish in Bermuda, part II: lessons learned to date. In: Proceedings of the 67th Gulf and Caribbean Fisheries Institute November 3–7 2014, vol 67. Christ Church, Barbados, pp 221–224

  43. Pyle RL (1998) Use of advanced mixed-gas diving technology to explore the coral reef “twilight zone”. In: Tanacredi JT, Loret J (eds) Ocean pulse: a critical diagnosis, 1st edn. Springer, New York, pp 71–88

    Google Scholar 

  44. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  45. Raudenbush SW (2008) Analyzing effect sizes: random effects models. In: Cooper H, Hedges LV, Valentine JC (eds) The handbook of research synthesis and meta-analysis, 2nd edn. Russell Sage Foundation, New York, p 632

    Google Scholar 

  46. Rocha LA, Rocha CR, Baldwin CC et al (2015) Invasive lionfish preying on critically endangered reef fish. Coral Reefs 34:803–806. doi:10.1007/s00338-015-1293-z

    Article  Google Scholar 

  47. Schofield PJ (2010) Update on geographic spread of invasive lionfishes (Pterois volitans [Linnaeus, 1758] and P. miles [Bennett, 1828]) in the Western North Atlantic Ocean, Caribbean Sea and Gulf of Mexico. Aquat Invasions 5:S117–S122

    Article  Google Scholar 

  48. Simberloff D, Martin J-L, Genovesi P et al (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28:58–66. doi:10.1016/j.tree.2012.07.013

    Article  PubMed  Google Scholar 

  49. Smith SR, Sarkis S, Murdoch TJ et al (2013) Threats to coral reefs of Bermuda. In: Sheppard CRC (ed) Coral Reefs of the United Kingdom overseas territories, Coral Reefs of the World 4. Springer, Berlin, pp 173–188

    Google Scholar 

  50. Thresher RE, Kuris AM (2004) Options for managing invasive marine species. Biol Invasions 6:295–300. doi:10.1023/B:BINV.0000034598.28718.2e

    Article  Google Scholar 

  51. Travis JMJ, Park KJ (2004) Spatial structure and the control of invasive alien species. Anim Conserv 7:321–330. doi:10.1017/S1367943004001507

    Article  Google Scholar 

  52. Trégarot E, Fumaroli M, Arqué A et al (2015) First records of the red lionfish (Pterois volitans) in Martinique, French West Indies: monitoring invasion status through visual surveys. Mar Biodivers Rec 8:e1. doi:10.1017/S1755267214001341

    Article  Google Scholar 

  53. Tyler E, Speight M, Henderson P, Manica A (2009) Evidence for a depth refuge effect in artisanal coral reef fisheries. Biol Conserv 142:652–667. doi:10.1016/j.biocon.2008.11.017

    Article  Google Scholar 

  54. Viechtbauer W (2010) Conducting meta-analyses in R with the metafor package. J Stat Softw. http://www.jstatsoft.org/v36/i03/. Accessed 30 May 2013

  55. Werner EE, Gilliam JF (1984) The ontogenetic niche and species interactions in size-structured populations. Annu Rev Ecol Syst 15:393–425

    Article  Google Scholar 

  56. Whitfield PE, Muñoz RC, Buckel CA et al (2014) Native fish community structure and Indo-Pacific lionfish Pterois volitans densities along a depth-temperature gradient in Onslow Bay, North Carolina, USA. Mar Ecol Prog Ser 509:241–254. doi:10.3354/meps10882

    Article  Google Scholar 

  57. Williams SL, Grosholz ED (2008) The invasive species challenge in estuarine and coastal environments: marrying management and science. Estuaries Coasts 31:3–20. doi:10.1007/s12237-007-9031-6

    Article  Google Scholar 

  58. Wright DJ (2005) Report of HURL Cruise KOK0510: submersible dives and multibeam mapping to investigate benthic habitats of Tutuila, American Samoa. Technical Report, NOAA’s Office of Undersea Research Submersible Science Program, Hawai’i Undersea Research Lab

Download references

Acknowledgements

We thank Matthew Speight for illustrating Fig. 5. DAAB was jointly funded by a Fisheries Society of the British Isles (FSBI) PhD studentship and Operation Wallacea. IB and RA were supported by the National Oceanic and Atmospheric Administration’s Center for Sponsored Coastal Ocean Research (NOAA/CSCOR) (Grant No. NA06NOS4780190). GGG, ADC, JMP, CE and SRS acknowledge the support of the Darwin Plus Overseas Territories Environment and Climate Fund through the UK Department of Environment Food and Rural Affairs (DEFRA) for data collected in Bermuda. LAR, HTP, BS and EJ acknowledges the logistical support of “Dutch” and his team at the Curaçao Seaquarium. HTP is a recipient of a doctoral fellowship from CNPq (Ciência sem Fronteiras; GDE 202475/2011-5). Financial support for data collection in Bermuda and Curaçao was also provided by the Bermuda Institute of Ocean Sciences and the California Academy of Sciences. We would like to thank the editor and reviewers for comments that improved this manuscript.

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Correspondence to Dominic A. Andradi-Brown.

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Alex D. Rogers and Dan A. Exton have contributed equally to the manuscript and are joint last authors

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Andradi-Brown, D.A., Vermeij, M.J.A., Slattery, M. et al. Large-scale invasion of western Atlantic mesophotic reefs by lionfish potentially undermines culling-based management. Biol Invasions 19, 939–954 (2017). https://doi.org/10.1007/s10530-016-1358-0

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Keywords

  • Pterois volitans
  • Pterois miles
  • Lionfish
  • Mesophotic
  • MCE
  • Invasive species
  • Twilight zone
  • Ontogenetic migration