Biol Invasions https://doi.org/10.1007/s10530-018-1720-5 ORIGINAL PAPER Feeding ecology of invasive lionfish (Pterois volitans and Pterois miles) in the temperate and tropical western Atlantic Jonathan Peake . Alex K. Bogdanoff . Craig A. Layman . Bernard Castillo . Kynoch Reale-Munroe . Jennifer Chapman . Kristen Dahl . William F. Patterson III . Corey Eddy . Robert D. Ellis . Meaghan Faletti . Nicholas Higgs . Michelle A. Johnston . Roldan C. Mun˜oz . Vera Sandel . Juan Carlos Villasenor-Derbez . James A. Morris Jr. Received: 11 September 2017 / Accepted: 28 March 2018 Ó This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply 2018 Abstract Numerous location-based diet studies locations. Our regional data indicate lionfish in the have been published describing different aspects of western Atlantic are opportunistic generalist carni- invasive lionfish (Pterois volitans and Pterois miles) vores that consume at least 167 vertebrate and feeding ecology, but there has been no synthesis of invertebrate prey species across multiple trophic their diet composition and feeding patterns across guilds, and carnivorous fish and shrimp prey that are regional gradients. 8125 lionfish stomachs collected not managed fishery species and not considered at risk from 10 locations were analyzed to provide a gener- of extinction by the International Union for Conser- alized description of their feeding ecology at a vation of Nature disproportionately dominate their regional scale and to compare their diet among diet. Correlations between lionfish size and their diet composition indicate lionfish in the western Atlantic J. Peake College of Marine Science, University of South Florida, K. Dahl Á W. F. Patterson III 830 1st St SE, St. Petersburg, FL 33701, USA University of Florida, 7922 NW 71st Street, Gainesville, FL 32653, USA A. K. Bogdanoff Á J. A. Morris Jr. NOAA, National Centers for Coastal Ocean Science, 101 C. Eddy Pivers Island Rd, Beaufort, NC 28584, USA Department of Biology, University of Massachusetts Dartmouth, 285 Old Westport Road, North Dartmouth, A. K. Bogdanoff (&) Á C. A. Layman MA 02747, USA Department of Applied Ecology, North Carolina State University, 127 David Clark Labs, Raleigh, NC 27695, R. D. Ellis USA Fish and Wildlife Research Institute, Florida Fish and e-mail: [email protected] Wildlife Conservation Commission, 100 8th Ave Southeast, St. Petersburg, FL 33701, USA B. Castillo Á K. Reale-Munroe College of Science and Mathematics, University of the M. Faletti Virgin Islands, RR1 Box 10000 Kingshill, St. Croix, Department of Biological Science, Florida State VI 00850, USA University, Tallahassee, FL 32306, USA J. Chapman N. Higgs Level 2 Annex, Omnibus Business Centre, Blue Ventures Marine Institute, Plymouth University, Conservation, 39-41 North Road, London N7 9DP, UK Plymouth PL4 8AA, UK 123 J. Peake et al. transition from a shrimp-dominated diet to a fish- Introduction dominated diet through ontogeny. Lionfish total length (TL) (mm) was found to predict mean prey mass per Indo-Pacific lionfish (Pterois volitans and Pterois stomach (g) by the following equation mean prey miles, Linnaeus, 1758) have become an abundant and mass =0.0002*TL1.6391, which can be used to estimate ubiquitous mesopredator throughout the temperate prey biomass consumption from lionfish length- and tropical western Atlantic (hereafter western frequency data. Our locational comparisons indicate Atlantic) (Morris Jr. 2012). Their range expansion lionfish diet varies considerably among locations, and proliferation is attributed to a variety of biological even at the group (e.g., crab) and trophic guild levels. characteristics including their environmental toler- The Modified Index of Relative Importance developed ances, reproductive output, defense from predation, specifically for this study, calculated as the frequency diet composition, and feeding behavior (Coˆte´ et al. of prey a 9 the number of prey a, can be used in other 2013). Several small-scale studies suggest invasive diet studies to assess prey importance when prey mass lionfish have the potential to negatively affect local data are not available. Researchers and managers can reef communities through predation on native species use the diet data presented in this study to make (e.g., Albins and Hixon 2008; Green et al. 2012; inference about lionfish feeding ecology in areas Albins 2015), and may possibly affect native fish where their diet has yet to be described. These data can populations at regional scales (Ballew et al. 2016). be used to guide research and monitoring efforts, and Understanding lionfish feeding ecology is therefore can be used in modeling exercises to simulate the important for understanding their ecological role and potential effects of lionfish on marine food webs. potential effects on marine food webs in the invaded Given the large variability in lionfish diet composition range (Meister et al. 2005; Ruiz-Carus et al. 2006). among locations, this study highlights the importance Morris and Akins (2009) first described lionfish diet of continued location-based diet assessments to better in The Bahamas in 2009. Since then, over 15 inform local management activities. additional location-based studies have been published describing different aspects of their feeding ecology Keywords Cumulative prey curves Á Feeding (e.g., Dahl and Patterson 2014; Eddy et al. 2016) and ecology Á Food webs Á Indices of prey importance Á foraging behavior (e.g., Green et al. 2011; Green and Invasive species Á Pterois volitans Á Pterois miles Á Coˆte´ 2014). Lionfish diet composition and feeding Regional diet trends patterns are, however, likely to differ among locations due to differences in local environmental factors including habitats and prey assemblages (Mun˜oz et al. 2011). Using the stomach contents of over 8000 lionfish collected from 10 locations throughout the western Atlantic, the goals of this study were to M. A. Johnston provide a generalized description of lionfish feeding NOAA, Flower Garden Banks National Marine Sanctuary, ecology at a regional scale and to compare lionfish diet 4700 Avenue U, Bldg. 216, Galveston, TX 77551, USA composition among locations. Our specific objectives R. C. Mun˜oz were to produce a centralized list of the prey consumed Southeast Fishery Science Center, NOAA, National and the relative contributions and importance of each Marine Fishery Service, 101 Pivers Island Rd, Beaufort, to lionfish diet, assess the diversity of their diet NC 28584, USA composition, describe general diet trends, identify V. Sandel potential ontogenetic diet shifts, and describe key Programa de Maestrı´aen Ciencias Marinas y Costerasde dietary differences among locations. The diet compo- la, Universidad Nacional de Costa Rica, Avenida 2, sitions and patterns described in this study can be used Puntarenas, Costa Rica to make inference about lionfish feeding ecology in J. C. Villasenor-Derbez areas where their diet has yet to be described, inform Bren School of Environmental Science and Management, research and monitoring efforts, and to model and University of California, Santa Barbara, Santa Barbara, predict the effects of lionfish on invaded reefs (e.g., CA 93106, USA Chagaris et al. 2017). 123 Feeding ecology of invasive lionfish (Pterois volitans and Pterois miles) Methods Red List of Threatened Species in December 2016 (http://www.iucnredlist.org/). Trophic guild cate- Data description gories were based on the best available information in the literature detailed in Appendix 2. Only species Lionfish diet data were collated from eight published managed by the National Marine Fisheries Service and seven unpublished datasets (Appendix 1). In total, (NMFS) and the South Atlantic, Gulf, and Caribbean data were obtained on 8125 lionfish collected from Fishery Management Councils (FMCs) were consid- Bermuda, North Carolina, The Bahamas, southeastern ered as fishery species in this study. Although the Florida (Florida), the northeastern Gulf of Mexico species managed by NMFS and the FMCs do not (neGoM), the northwestern Gulf of Mexico (nwGoM), encompass all managed species within the invaded the Yucatan Peninsula (Mexico), Belize, Costa Rica, range, this approach provided a standardized way to and the United States Virgin Islands (USVI) (Ap- categorize prey using the fishery importance [e.g., pendix 1). Samples collected within each location species incorporated into NMFS Fishery Stock Sus- were pooled across environmental gradients (e.g., tainability Index (FSSI)] and fishery status (e.g., depths and habitats) to represent the general area. Data stocks/complexes considered ‘‘overfished’’) designa- collected for each sample included lionfish length tions used by NMFS. The importance levels and sta- (mm) and mass (g) and the mass/volume and length tuses were derived from the December 2016 NMFS (mm) of each prey. Lionfish standard length was Stock Status Update (NMFS 2016). Additional detail converted to total length (TL) as needed using the on prey categorization is available in Appendix 2. conversion equation in Fogg et al. (2013). Prey volume was converted to mass (g) as needed using Prey metrics and indices of importance the 1:1 conversion ratio in Swedberg and Walburg (1970). The relative contribution of each prey category to The number of samples per location ranged from lionfish diet was calculated using three relative metrics 299 to 1481 with an average of 812 ± 405 (mean ± of prey quantity including percent frequency of SD). The lionfish used in this