Skip to main content
SpringerLink
Log in

Biotic resistance on coral reefs? Direct and indirect effects of native predators and competitors on invasive lionfish

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

Biotic resistance is the ability of an ecological community to prevent or limit the establishment or success of non-indigenous species. Native species can confer resistance by outcompeting or directly consuming non-native invaders. The fear of being eaten could also limit invader success, but non-consumptive effects of native predators have rarely been documented as a source of biotic resistance. Here, we test whether native groupers on Caribbean coral reefs can promote biotic resistance to invasive Indo-Pacific lionfish through competition, consumption, and/or through non-consumptive effects. Stomach content analysis of more than 200 groupers, comprising five species, revealed no instances of predation on lionfish. To test for competitive and non-consumptive effects of groupers, we released tagged juvenile lionfish onto reef patches that varied in grouper densities and monitored lionfish behaviours over five weeks. At dawn, during peak grouper and lionfish hunting times, juvenile lionfish hid more on reefs with more grouper predators. Juvenile lionfish were also less active during the day on reefs with high grouper densities. Hiding and inactivity are incompatible with foraging and thus should result in lionfish eating fewer prey and having reduced somatic growth rates. Although there was no substantial effect of interspecific competition on lionfish behaviours, we found that lionfish swam greater distances with increasing densities of intraspecific competitors at dawn. We did not detect a cascading effect of grouper predators on smaller fishes, perhaps because the seasonal peak in prey fish recruitment masked the effects of lower lionfish predation. Fear of native predators by lionfish has the potential to reduce invader foraging success, although it might not fully mitigate the negative effects on native prey communities. Efforts to rebuild grouper populations throughout the Caribbean may still aid in controlling the lionfish invasion despite weak evidence of interspecific competition and lack of direct predation on lionfish, but further research is needed. At broader scales, our findings highlight that the global depletion of large predators can have implications beyond demographic effects on prey.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alofs KM, Jackson DA (2014) Meta-analysis suggests biotic resistance in freshwater environments is driven by consumption rather than competition. Ecology 95:3259–3270

  • Alvarez-Filip L, Côté IM, Gill JA, Watkinson AR, Dulvy NK (2011) Region-wide temporal and spatial variation in Caribbean reef architecture: is coral cover the whole story? Glob Chang Biol 17:2470–2477

  • Beckstead J, Parker IM (2003) Invasiveness of Ammophila arenaria: release from soil-borne pathogens? Ecol 84:2824–2831

  • Benkwitt CE (2013) Density-dependent growth in invasive lionfish (Pterois volitans). PLoS ONE 8:e066995

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

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

  • Böhlke JE, Chaplin CC (1993) Fishes of The Bahamas and adjacent tropical waters. Second edition. University of Texas Press, Austin

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

  • Cade BS (2015) Model averaging and muddled multimodel inferences. Ecol 96:2370–2382

  • Cohen AN, Carlton JT (1998) Accelerating invasion rate in a highly invaded estuary. Science 279:555–557

  • Côté IM, Darling ES, Malpica-Cruz L, Smith NS, Green SJ, Curtis-Quick J, Layman C. (2014) What doesn’t kill you makes you wary? Effect of repeated culling on the behaviour of an invasive predator. PLoS ONE 9:e94248

  • Côté IM, Smith NS (2018) The lionfish Pterois sp. invasion: Has the worst-case scenario come to pass? J Fish Biol 92:660–689

  • Cure K, Benkwitt CE, Kindinger TL, Pickering EA, Pusack TJ, McIIwain JL, Hixon MA (2012) Comparative behavior of red lionfish Pterois volitans on native Pacific versus invaded Atlantic coral reef fishes. Mar Ecol Prog Ser 467:18–192

  • Curtis JS, Wall KR, Albins MA, Stallings CD (2017) Diet shifts in a native mesopredator across a range of invasive lionfish biomass. Mar Ecol Progr Ser 573:215–228

  • Curtis JS, Albins MA, Peebles EB, Stallings CD (2020) Stable isotope analysis of eye lenses from invasive lionfish yields record of resource use. Mar Ecol Prog Ser 637:181–194

  • Davis K, Carlson PM, Bradley D, Warner RR, Caselle JE (2017) Predation risk influences feeding rates but competition structures space use for a common Pacific parrotfish. Oecologia 184:139–149

  • Ellis RD, Faletti ME (2016) Native grouper indirectly ameliorates the negative effects of invasive lionfish, Mar Ecol Progr Ser 558:267–279

  • Ferreira CEL, Luiz OJ, Floeter SR, Lucena MB, Barbosa MC, Rocha CR, Rocha LA (2015) First record of invasive lionfish (Pterois volitans) for the Brazilian Coast. PLoS ONE 10:e0123002

  • Frederick JL (1997) Evaluation of fluorescent elastomer injection as a method for marking small fish. Bull Mar Sci 61, 399–408

  • Froese R, Pauly D (editors). 2018. FishBase. www.fishbase.org

  • Green PT, Lake PS, O’Dowd DJ (2004) Resistance of island rainforest to invasion by alien plants: influence of microhabitat and herbivory on seedling performance. Biol Invasions 6:1–9

  • 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

  • Green SJ, Akins JL, Maljković A, Côté IM (2012) Invasive lionfish drive Atlantic coral reef fish declines. PLoS ONE:e0032596

  • Green SJ, Tamburello N, Miller SE, Akins JL, Côté IM (2013) Habitat complexity and fish size affect the detection of Indo-Pacific lionfish on invaded coral reefs. Coral Reefs 32:413–421

  • Green SJ, Dulvy NK, Brooks ALM, Akins JL, Cooper AB, Miller S, Côté IM (2014) Linking removal targets to the ecological effects of invaders: a predictive model and field test. Ecol Appl 24:1311–1322

  • Grueber CE, Nakagawa S, Laws RJ, Jamieson IG (2011) Multimodel inference in ecology and evolution: challenges and solutions. J Evol Biol 24:699–711

  • Hackerott S, Valdivia A, Green SJ, Côté IM, Cox CE, Akins L, Layman CA, Precht WF, Bruno JF (2013) Native predators do not influence invasion success of Pacific lionfish on Caribbean reefs. PLoS ONE 8:e0068259

  • Harrison XA, Donaldson L, Correa-Cano ME, Evans J, Fisher DN, Goodwin CED, Robinson BS, Hodgsoon DJ, Inger R (2018) A brief introduction to mixed effects modelling and multi-model inference in ecology. PeerJ 6:e4794

  • Heithaus M, Frid A, Wirsing AJ, Worm B (2008) Predicting ecological consequences of marine top predator declines. Trends Ecol Evol 23:202–210

  • Helfman GS (1986) Fish behaviour by day, night and twilight. Pp 366–387 in: Pitcher T, editor. The behaviour of teleost fishes. Croom-Helm, London

  • Hixon MA (1991) Predation as a process structuring coral reef fish communities. Pp 475–507 in Sale PF, editor. The ecology of fishes on coral reefs. Academic Press, New York

  • Hobson ES (1972) Activity of Hawaiian reef fishes during the evening and morning transitions between daylight and darkness. Fishery Bull 70:715–740

  • Humann P, Deloach N (2002) Reef fish identification: Florida, Caribbean, Bahamas. Third edition. New World Publications, Jacksonville

  • Keene JL, Noakes DL, Moccia RD, Soto CG (1998) The efficacy of clove oil as an anaesthetic for rainbow trout, Oncorhynchus mykiss (Walbaum). Aquac Res 29:89–101

  • Kelley JL, Magurran AE (2003) Learned predator recognition and antipredator responses in fishes. Fish Fisher 4:216–226

  • Kimbro DL. Cheng BS, Brosholz ED (2013) Biotic resistance in marine environments. Ecol Lett 16:821–833

  • Layman CA, Allgeier JE (2012) Characterizing trophic ecology of generalist consumers: a case study of the invasive lionfish in The Bahamas. Mar Ecol Progr Ser 448:131–141

  • Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7:975–989

  • Lima SL (1998) Nonlethal effects in the ecology of predator-prey interactions. What are the ecological effects of anti-predator decision-making? BioSci 48:25–34

  • Luckhurst BE, Luckhurst K (1978) Analysis of the influence of substrate variables on coral reef fish communities. Mar Biol 49:317–323

  • Maljković A, Leeuwen TEV, Cove SN (2008) Predation on the invasive red lionfish, Pterois volitans (Pisces: Scorpaenidae), by native groupers in the Bahamas. Coral Reefs 27:501

  • Mumby PJ, Harborne AR, Brumbaugh DR (2011) Grouper as a natural biocontrol of invasive lionfish. PLoS ONE 6:e0021510

  • Nyström P (2005) Non-lethal predator effects on the performance of a native and an exotic crayfish species. Freshw Biol 50:1938–1949

  • O’Farrell S, Bearhop S, McGill RA, Dahlgren CP, Brumbaugh DR, Mumby PJ (2014) Habitat and body size effects on the isotopic niche space of invasive lionfish and endangered Nassau grouper. Ecosphere 5:123

  • Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288

  • Raymond WW, Albins MA, Pusack TJ (2015) Competitive interactions for shelter between invasive Pacific red lionfish and native Nassau grouper. Environ Biol Fishes 98:57−65

  • Sala OE, et al (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774

  • Sale P (1978) Coexistence of coral reef fishes – a lottery for living space. Environ Biol Fish 3:85–102

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

  • Salomon AK, Gaichas SK, Shears NT, Smith JE, Madin EMP, Gaines SD (2010) Key features and context-dependence of fishery-induced trophic cascades. Conserv Biol 24:382–394

  • Schielzeth H (2010) Simple means to improve the interpretability of regression coefficients. Methods Ecol Evol 1:103–113

  • Schofield P (2009) Geographic extent and chronology of the invasion of non-native lionfish (Pterois volitans [Linnaeus 1758] and P. miles [Bennett 1828]) in the western North Atlantic and Caribbean Sea. Aquat Invasions 4:473–479

  • Semmens BX, Buhle ER, Salomon AK, Pattengill-Semmens CV (2004) A hotspot of non-native marine fishes: evidence for the aquarium trade as an invasion pathway. Mar Ecol Prog Ser 266:239–244

  • Sherman KD, Dahlgren CP, Stevens JR, Tyler CR (2016) Integrating population biology into conservation management for endangered Nassau grouper Epinephelus striatus. Mar Ecol Prog Ser 554:263–280

  • Sih A, Bolnick DI, Luttbeg B, Orrock JL, Peacor SD, Pintor LM, Preisser E, Rehage JS, Vonesh JR (2010) Predator-prey naïveté, antipredator behavior and the ecology of predator invasions. Oikos 119:610–621

  • Sluka R, Chiappone M, Sullivan KM (1994) Comparison of juvenile grouper populations in Southern Florida and the Central Bahamas. Bull Mar Sci 54:871–880

  • Smith NS, Green SJ, Akins JL, Miller S, Côté (2017) Density-dependent colonization and natural disturbance limit the effectiveness of invasive lionfish culling efforts. Biol Invasions 19:2385–2399

  • Stallings CD (2008) Indirect effects of an exploited predator on recruitment of coral-reef fishes. Ecol 89:2090–2095

  • Suraci JP, Clinchy M, Dill LM, Roberts D, Zanette LY (2016) Fear of large carnivores causes a trophic cascade. Nat Commun 7:10698

  • Symonds MRE, Moussalli A (2011) A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behav Ecol Sociobiol 65:13–21

  • Tamburello N, Côté IM (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 

  • Trehern RH, Raguse C, Bigelow WF, GargA., Hauptman H, Brooks A, Van Leeuwen TE, Hawkes LA (2020) The effect of salinity on behavioural interactions between native Schoolmaster snapper (Lutjanus apodus) and invasive lionfish (Pterois spp). J Exp Mar Biol Ecol 530–531:151414

  • Valdivia A, Bruno JF, Cox CE, Hackerott S, Green SJ (2014) Re-examining the relationship between invasive lionfish and native grouper in the Caribbean. PeerJ 2:e348

  • Vaudo JJ, Heithaus MR (2013) Microhabitat selection by marine mesoconsumers in a thermally heterogeneous habitat: behavioural thermoregulation or avoiding predation risk? PLoS ONE 8:e0061907

  • Yamanishi Y, Yoshida K, Fujimori N, Yusa Y (2012) Predator-driven biotic resistance and propagule pressure regulate the invasive apple snail Pomacea canaliculata in Japan. Biol Invasions 14:1343–1352

Download references

Acknowledgements

We thank Jocelyn Curtis-Quick, Fiona Francis, Kyla Jeffrey, Helen Yan, Emma Atkinson, and Adrienne Berchtold for assistance collecting data in the field. We also thank the Cape Eleuthera Institute for facilitating this work. We thank Simon Brandl for fruitful discussion on data analysis. NSS was supported by an Organization of American States Graduate Scholarship and a Bullitt Foundation Environmental Fellowship. Fieldwork was supported by a Natural Sciences and Engineering Research Council of Canada Discovery grant to IMC.

Author information

Authors and Affiliations

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

    Nicola S. Smith & Isabelle M. Côté

Authors
  1. Nicola S. Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Isabelle M. Côté
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nicola S. Smith.

Ethics declarations

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Topic Editor Alastair Harborne

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 24947 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Smith, N.S., Côté, I.M. Biotic resistance on coral reefs? Direct and indirect effects of native predators and competitors on invasive lionfish. Coral Reefs 40, 1127–1136 (2021). https://doi.org/10.1007/s00338-021-02117-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-021-02117-7

Keywords

Search

Navigation