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Biological Invasions

, Volume 20, Issue 9, pp 2567–2597 | Cite as

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. Muñoz
  • Vera Sandel
  • Juan Carlos Villasenor-Derbez
  • James A. MorrisJr.
Original Paper

Abstract

Numerous location-based diet studies have been published describing different aspects of invasive lionfish (Pterois volitans and Pterois miles) feeding ecology, but there has been no synthesis of their diet composition and feeding patterns across regional gradients. 8125 lionfish stomachs collected from 10 locations were analyzed to provide a generalized description of their feeding ecology at a regional scale and to compare their diet among locations. Our regional data indicate lionfish in the western Atlantic are opportunistic generalist carnivores that consume at least 167 vertebrate and invertebrate prey species across multiple trophic guilds, and carnivorous fish and shrimp prey that are not managed fishery species and not considered at risk of extinction by the International Union for Conservation of Nature disproportionately dominate their diet. Correlations between lionfish size and their diet composition indicate lionfish in the western Atlantic transition from a shrimp-dominated diet to a fish-dominated diet through ontogeny. Lionfish total length (TL) (mm) was found to predict mean prey mass per stomach (g) by the following equation mean prey mass =0.0002*TL1.6391, which can be used to estimate prey biomass consumption from lionfish length-frequency data. Our locational comparisons indicate lionfish diet varies considerably among locations, even at the group (e.g., crab) and trophic guild levels. The Modified Index of Relative Importance developed specifically for this study, calculated as the frequency of prey a × the number of prey a, can be used in other diet studies to assess prey importance when prey mass data are not available. Researchers and managers can use the diet data presented in this study to make inference about lionfish feeding ecology in areas where their diet has yet to be described. These data can be used to guide research and monitoring efforts, and can be used in modeling exercises to simulate the potential effects of lionfish on marine food webs. Given the large variability in lionfish diet composition among locations, this study highlights the importance of continued location-based diet assessments to better inform local management activities.

Keywords

Cumulative prey curves Feeding ecology Food webs Indices of prey importance Invasive species Pterois volitans Pterois miles Regional diet trends 

Notes

Acknowledgements

We appreciate the thoughtful comments provided by K. Shertzer, S. Gittings, T. Kellison, A. Hohn, A. Chester, and two anonymous reviewers. We thank NOAAs National Centers for Coastal Ocean Science, NOAAs Office of Education, and the Earnest F. Hollings Scholarship Program for providing support for this project. We are grateful to all who helped collect the data that were used in this study including N. Van Der Haar, M. Doodey, G. Lotz-Cador, the Caribbean Oceanic Restoration and Education Foundation (CORE), UVI CHE 495 students, New Wave Ltd. fishing co., the Bermuda Lionfish Culling Program, C. Buckel, C. Coy, B. Degan, W. Freshwater, J. Hoyt, D. Kesling, M. Lacroix P. Maddi, T. Potts, C. Shemanski, J. Styron, G. Taylor, L. Akins, NOAA Sanctuaries divers, divers from Texas A&M University Galveston, the MV FLING, the Fish Conservation Lab at Texas A&M University Corpus Christi, staff and volunteers of Blue Ventures Expeditions in Belize, D. Kennedy, C. Retherford, S. Bartel, B. Clark, A. Clark, J. Tarnecki, J. Mostowy, and S. Stockton-Teleske.

Author’s contribution

Statement of authorship: J.A.M. and A.K.B. conceived and designed the study; A.K.B. & J.P. conducted the study and wrote the manuscript; all authors contributed stomach content data and revised the manuscript. Authors after C.A.L are listed alphabetically by institution.

References

  1. Albertoni EF, Palma-Silva C, Esteves FDA (2003) Natural diet of three species of shrimp in a tropical coastal lagoon. Braz Arch Biol Technol 46:395–403Google Scholar
  2. Albins MA (2013) Effects of invasive Pacific red lionfish Pterois volitans versus a native predator on Bahamian coral-reef fish communities. Biol Invasions 15:29–43Google Scholar
  3. Albins MA (2015) Invasive Pacific lionfish Pterois volitans reduce abundance and species richness of native Bahamian coral-reef fishes. Mar Ecol Prog Ser 522:231–243Google Scholar
  4. Albins MA, Hixon MA (2008) Invasive Indo-Pacific lionfish Pterois volitans reduce recruitment of Atlantic coral-reef fishes. Mar Ecol Prog Ser 367:233–238Google Scholar
  5. Ballew NG, Bacheler NM, Kellison GT, Schueller AM (2016) Invasive lionfish reduce native fish abundance on a regional scale. Sci Rep 6:32169.  https://doi.org/10.1038/srep32169 PubMedPubMedCentralGoogle Scholar
  6. Bardach JE (1959) The summer standing crop of fish on a shallow Bermuda reef. Limnol Oceanogr 4(1):77–85Google Scholar
  7. Bizzarro JJ, Robinson HJ, Rinewalt CS, Ebert DA (2007) Comparative feeding ecology of four sympatric skate species off central California, USA. In: Ebert DA, Sulikowski JA (eds) Biology of skates. Springer, Dordrecht, pp 91–114Google Scholar
  8. Böhlke JE, Chaplin CCG (1993) Fishes of the Bahamas and adjacent tropical waters, 2nd edn. University of Texas Press, AustinGoogle Scholar
  9. Bowen SH (1996) Quantitative description of the diet. In: Murphy BR, Willis DW (eds) Fisheries techniques, 2nd edn. American Fisheries Society, Bethesda, pp 513–532Google Scholar
  10. Bullock LH, Smith GB (1991) Seabasses: (Pisces:Serranidae), vol 8. Florida Marine Research Institute, St. PetersburgGoogle Scholar
  11. Burgess WE (2002) Pomacanthidae. Angelfishes. In: Carpenter KE (ed) FAO species identification guide for fishery purposes. The living marine resources of the Western Central Atlantic, vol 3: Bony fishes part 2 (Opistognathidae to Molidae), sea turtles and marine mammals., Rome, pp 1673–1683Google Scholar
  12. Carter J (2002) Pomacentridae: damselfishes. In: Carpenter K (ed) The living marine resources of the Western Central Atlantic, vol 2. FAO, RomeGoogle Scholar
  13. Cartes JE (1993) Diets of two deep-sea decapods: Nematocarcinus exilis (Caridea: Nematocarcinidae) and Munida tenuimana (Anomura: Galatheidae) on the Western Mediterranean slope. Ophelia 37(3):213–229.  https://doi.org/10.1080/00785326.1993.10429919 Google Scholar
  14. Cervigón F (1993) Los peces marinos de Venezuela, vol 2, 2 edn. Fundación Científica Los RoquesGoogle Scholar
  15. Chagaris D, Binion-Rock S, Bogdanoff A, Dahl K, Granneman J, Harris H, Mohan J, Rudd MB, Swenarton MK, Ahrens R, Patterson WF, Morris JA, Allen M (2017) An ecosystem-based approach to evaluating impacts and management of invasive lionfish. Fisheries 42(8):421–431Google Scholar
  16. Chande A, Mgaya Y (2005) Food habits of the blue swimming crab Portunus pelagicus along the coast of Dar es Salaam, Tanzania. West Indian Ocean J Mar Sci 3(1):37–42.  https://doi.org/10.1186/s41200-016-0073-y Google Scholar
  17. Claro R, Lindeman KC (2008) Biología y manejo de los pargos (Lutjanidae) en el Atlántico occidental. Instituto de Oceanología, La HabanaGoogle Scholar
  18. Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. Lawrence Erlbaum, HillsdaleGoogle Scholar
  19. Corredor L (1978) Notes on the behavior and ecology of the new fish cleaner shrimp Brachycarpus biunguiculatus (Lucas) (Decapoda Natantia, Palaemonidae). Crustaceana 35(1):35–40.  https://doi.org/10.1163/156854078X00187 Google Scholar
  20. Côté IM, Green SJ, Hixon MA (2013) Predatory fish invaders: insights from Indo-Pacific lionfish in the western Atlantic and Caribbean. Biol Cons 164:50–61Google Scholar
  21. Dahl KA, Patterson WF III (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.  https://doi.org/10.1371/journal.pone.0105852 PubMedPubMedCentralGoogle Scholar
  22. Darnell RM (1962) Fishes of the Rio Tamesi and related coastal lagoons in east-central Mexico. Institute of Marine ScienceGoogle Scholar
  23. Davenport J (2009) A cleaning association between the oceanic crab Planes minutus and the loggerhead sea turtle Caretta caretta. J Mar Biol Assoc UK 74(3):735–737.  https://doi.org/10.1017/S0025315400047780 Google Scholar
  24. de Boer BA (1980) A causal analysis of the territorial and courtship behaviour of Chromis cyanea (Pomacentridae, Pisces). Behaviour 73(1/2):1–50Google Scholar
  25. Doncel O, Paramo J (2010) Food habits of the lane snapper, Lutjanus synagris (Perciformes: Lutjanidae), in the north zone of the Colombian Caribbean. Lat Am J Aquat Res 38(3):413–426Google Scholar
  26. Eddy C, Pitt J, Morris JA Jr, Smith S, Goodbody-Gringley G, Bernal D (2016) Diet of invasive lionfish (Pterois volitans and P. miles) in Bermuda. Mar Ecol Prog Ser 558:193–206Google Scholar
  27. Efron B (1979) Bootstrap methods: another look at the jack-knife. Ann Stat 7:1–26Google Scholar
  28. Elise S, Urbina-Barreto I, Boadas-Gil H, Galindo-Vivas M, Kulbicki M (2014) No detectable effect of lionfish (Pterois volitans and P. miles) invasion on a healthy reef fish assemblage in Archipelago Los Roques National Park, Venezuela. Mar Biol 162:319–330Google Scholar
  29. Ellis RD, Faletti ME (2016) Native grouper indirectly ameliorates the negative effects of invasive lionfish. Mar Ecol Prog Ser 558:267–279Google Scholar
  30. Emery AR (1978) Pomacentridae. In: Fischer W (ed) FAO species identification sheets for fishery purposes. West Central Atlantic (Fishing Area 31), vol 4. FAO, RomeGoogle Scholar
  31. Floeter SR, Ferreira C, Dominici-Arosemena A, Zalmon I (2004) Latitudinal gradients in Atlantic reef fish communities: trophic structure and spatial use patterns. J Fish Biol 64(6):1680–1699Google Scholar
  32. Fogg AQ, Hoffmayer ER, Driggers WB, Campbell MD, Pellegrin GJ, Stein W (2013) Distribution and length frequency of invasive lionfish (Pterois sp.) in the northern Gulf of Mexico. Gulf Caribb Res 25:111–115Google Scholar
  33. Franks JS, VanderKooy KE (2000) Feeding habits of juvenile lane snapper Lutjanus synagris from Mississippi coastal waters, with comments on the diet of gray snapper Lutjanus griseus. Gulf Caribb Res 12(1):11–17Google Scholar
  34. Frick MG, Williams KL, Bolten AB, Bjorndal KA, Martins HR (2004) Diet and fecundity of Columbus crabs, Planes minutus, associated with oceanic-stage loggerhead sea turtles, Caretta caretta, and inanimate flotsam. J Crustac Biol 24(2):350–355.  https://doi.org/10.1651/C-2440 Google Scholar
  35. Gibran FZ (2007) Activity, habitat use, feeding behavior, and diet of four sympatric species of Serranidae (Actinopterygii: Perciformes) in southeastern Brazil. Neotrop Ichthyol 5:387–398Google Scholar
  36. Gladfelter WB, Johnson WS (1983) Feeding niche separation in a guild of tropical reef fishes (Holocentridae). Ecology 64(3):552–563.  https://doi.org/10.2307/1939975 Google Scholar
  37. Gloeckner DR, Luczkovich JJ (2008) Experimental assessment of trophic impacts from a network model of a seagrass ecosystem: direct and indirect effects of gulf flounder, spot and pinfish on benthic polychaetes. J Exp Mar Biol Ecol 357(2):109–120.  https://doi.org/10.1016/j.jembe.2007.12.031 Google Scholar
  38. Gomon MF (1978) Labridae. In: Fischer W (ed) FAO species identification sheets for fishery purposes. West Central Atlantic (Fishing Area 31), vol 4. FAO, RomeGoogle Scholar
  39. Gray AE, Mulligan TJ, Hannah RW (1997) Food habits, occurrence, and population structure of the bat ray, Myliobatis californica, in Humboldt Bay, California. Environ Biol Fishes 49(2):227–238.  https://doi.org/10.1023/a:1007379606233 Google Scholar
  40. Green SJ, Côté IM (2014) Trait-based diet selection: prey behaviour and morphology predict vulnerability to predation in reef fish communities. J Anim Ecol 83(6):1451–1460.  https://doi.org/10.1111/1365-2656.12250 PubMedGoogle Scholar
  41. Green SJ, Akins JL, Cote IM (2011) Foraging behaviour and prey consumption in the Indo-Pacific lionfish on Bahamian coral reefs. Mar Ecol Prog Ser 433:159–167Google Scholar
  42. Green SJ, Akins JL, Maljkovi A, Côté IM (2012) Invasive lionfish drive Atlantic coral reef fish declines. PLoS ONE 7(3):e32596.  https://doi.org/10.1371/journal.pone.0032596 PubMedPubMedCentralGoogle Scholar
  43. Hackerott S, Valdivia A, Cox CE, Silbiger NJ, Bruno JF (2017) Invasive lionfish had no measurable effect on prey fish community structure across the Belizean Barrier Reef. PeerJ 5:e3270.  https://doi.org/10.7717/peerj.3270 PubMedPubMedCentralGoogle Scholar
  44. Halpern BS, Floeter SR (2008) Functional diversity responses to changing species richness in reef fish communities. Mar Ecol Prog Ser 364:147–156Google Scholar
  45. Harmelin-Vivien ML, Bouchon C (1976) Feeding behaviour of some carnivorous fishes (Serranidae and Scorpaenidae) from Tuléar (Madagascar). Mar Biol 37:329–340Google Scholar
  46. Hazlett BA (1981) The behavioral ecology of hermit crabs. Annu Rev Ecol Syst 12(1):1–22.  https://doi.org/10.1146/annurev.es.12.110181.000245 Google Scholar
  47. Heemstra P, Randall J (1993) An annotated and illustrated catalogue of the grouper, rockcod, hind coarl grouper and lyretail species known to date, FAO species catalogue, vol 16. Groupers of the world (Family Serranidae, Subfamily Epinephelinae), p 382Google Scholar
  48. Heemstra P, Anderson W Jr, Lobel P (2002) Serranidae. In: Carpenter K (ed) The living marine resources of the Western Central Atlantic, vol 2. FAO, RomeGoogle Scholar
  49. Hughes TP (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean reef. Sciecne 265:1547–1551Google Scholar
  50. Hughes RN, Elner RW (1989) Foraging behaviour of a tropical crab: Calappa ocellata Holthuis feeding upon the mussel Brachidontes domingensis (Lamarck). J Exp Mar Biol Ecol 133(1):93–101.  https://doi.org/10.1016/0022-0981(89)90160-3 Google Scholar
  51. Humann P, Deloach N (2004) Reef fish identification: Florida. New World Publications Jacksonville, CaribbeanGoogle Scholar
  52. Hunt SL, Mulligan TJ, Komori K (1999) Oceanic feeding habits of Chinook salmon, Oncorhynchus tshawytscha, off northern California. Fish Bull Natl Ocean Atmos Adm 97:717–721Google Scholar
  53. Hyslop EJ (1980) Stomach contents analysis—a review of methods and their application. J Fish Biol 17(4):411–429.  https://doi.org/10.1111/j.1095-8649.1980.tb02775.x Google Scholar
  54. Ingeman KE (2016) Lionfish cause increased mortality rates and drive local extirpation of native prey. Mar Ecol Prog Ser 558:235–245.  https://doi.org/10.3354/meps11821 Google Scholar
  55. Iversen ES, Jory DE, Bannerot SP (1986) Predation on queen conchs, Strombus gigas, in the Bahamas. Bull Mar Sci 39(1):61–75Google Scholar
  56. Jiang W, Jorgensen T (1996) The diet of haddock (Melanogrammus auglefinus L.) in the Barents Sea in the period 1984 to 1991. ICES J Mar Sci 53:11–21Google Scholar
  57. Johnson WS, Ruben P (1988) Cleaning behavior of Bodianus rufus, Thalassoma bifasciatum, Gobiosoma evelynae, and Periclimenes pedersoni along a depth gradient at Salt River Submarine Canyon, St. Croix. Environ Biol Fishes 23(3):225–232.  https://doi.org/10.1007/bf00004913 Google Scholar
  58. Katsuragawa M, Ekau W (2003) Distribution, growth and mortality of young rough scad, Trachurus lathami, in the south-eastern Brazilian Bight. J Appl Ichthyol 19(1):21–28.  https://doi.org/10.1046/j.1439-0426.2003.00335.x Google Scholar
  59. Kindinger TL, Albins MA (2017) Consumptive and non-consumptive effects of an invasive marine predator on native coral-reef herbivores. Biol Invasions 19(1):131–146Google Scholar
  60. Lavalli KL, Spanier E, Grasso F (2007) Behavior and sensory biology of slipper lobsters. In: Lavalli K, Spanier E (ed) The biology and fisheries of the slipper lobster, vol 7. CRC, Boca Raton, pp 133–181Google Scholar
  61. Layman CA, Allgeier JE (2012) Characterizing trophic ecology of generalist consumers: a case study of the invasive lionfish in The Bahamas. Mar Ecol Prog Ser 448:131–141.  https://doi.org/10.3354/meps09511 Google Scholar
  62. Layman CA, Jud ZR, Nichols P (2014) Lionfish alter benthic invertebrate assemblages in patch habitats of a subtropical estuary. Mar Biol 161:2179–2182Google Scholar
  63. 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 13:1855–1868Google Scholar
  64. Lieske E, Myers R (1994) Collins pocket guide. In: Coral reef fishes. Indo-Pacific & Caribbean including the Red Sea. Haper Collins Publishers, p 400Google Scholar
  65. Link G (1980) Age, growth, reproduction, feeding, and ecological observations on the three species of Centropristis (Pisces: Serranidae) in north Carolina waters. University of North Carolina, Chapel HillGoogle Scholar
  66. Matsuura K (2002) Monacanthidae. In: Carpenter K (ed) The living marine resources of the Western Central Atlantic, vol 2. FAO, RomeGoogle Scholar
  67. McEachran JD (2009) Fishes (Vertebrata: Pisces) of the Gulf of Mexico. In: Felder DL, Camp DK (eds) Gulf of Mexico origins, waters, and biota. Biodiversity. Texas A&M Press, College Station, pp 1223–1316Google Scholar
  68. McEachran JD, Fechhelm JD (2005) Fishes of the Gulf of Mexico, volume 2: Scorpaeniformes to Tetraodontiformes, vol 2. University of Texas Press, AustinGoogle Scholar
  69. Medeiros DV, de Anchieta CC, Nunes J, Reis-Filho JA, Sampaio CLS (2011) Yellowline arrow crab Stenorhynchus seticornis (Brachyura: Majidae) acting as a cleaner of reef fish, eastern Brazil. Mar Biodivers Rec.  https://doi.org/10.1017/S1755267211000637 Google Scholar
  70. Meister HS, Wyanski DM, Loefer JK, Ross SW, Quattrini AM, Sulak KJ (2005) Further evidence for the invasion and establishment of Pterois volitans (Teleostei: Scorpaenidae) along the Atlantic Coast of the United States. Southeast Nat 4(2):193–206Google Scholar
  71. Morris JA, Akins JL (2009) Feeding ecology of invasive lionfish (Pterois volitans) in the Bahamian archipelago. Environ Biol Fishes 86(3):389–398.  https://doi.org/10.1007/s10641-009-9538-8 Google Scholar
  72. Morris JA Jr (ed) (2012) Invasive lionfish: a guide to control and management. Gulf and Caribbean Fisheries Institute Special Publication Series Number 1, Marathon, Florida, USA, 113 ppGoogle Scholar
  73. Mumby PJ (2006) The impact of exploiting grazers (Scaridae) on the dynamics of Caribbean coral reefs. Ecol Appl 16:747–769PubMedGoogle Scholar
  74. 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 432:181–193Google Scholar
  75. Natarajan A, Jhingran V (1961) Index of preponderance: a method of grading food elements in the stomach analysis of fishes. Indian J Fish 8(1):54–59Google Scholar
  76. Pinkas L, Oliphant MS, Iverson IL (1970) Fish bulletin 152. Food habits of albacore, bluefin tuna, and bonito in California Waters. UC San Diego: Library – Scripps Collection. Retrieved from https://escholarship.org/uc/item/7t5868rd
  77. Puccio V, Relini M, Azzurro E, Relini LO (1853) Feeding habits of Percnon gibbesi (H. Milne Edwards, 1853) in the Sicily Strait. Hydrobiologia 557(1):79.  https://doi.org/10.1007/s10750-005-1310-2 Google Scholar
  78. Randall JE (1967) Food habits of reef fishes of the West Indies. Stud Trop Oceanogr 5:665–847Google Scholar
  79. Randall JE (1996) Caribbean reef fishes. T.F.H. Publications, New JerseyGoogle Scholar
  80. Randall JE (2002) Mullidae: goatfishes. In: Carpenter K (ed) The living marine resources of the Western Central Atlantic, vol 2. FAO, RomeGoogle Scholar
  81. Randall JE, Schroeder R, Starck W (1964) Notes on the biology of the echinoid Diadema antillarum. Caribb J Sci 4(2–3):421–433Google Scholar
  82. R Core Team (2017) R: A language and environment for statistical computing. https://www.R-project.org/
  83. Reed EP (1954) Palinuridae. Scientia, Valparaiso 21:131–139Google Scholar
  84. Rilov G (2009) Predator–prey interactions of marine invaders. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems: ecological, management, and geographic perspectives. Springer, Berlin, pp 261–285Google Scholar
  85. Robertson DR (1981) The social and mating systems of two labrid fishes, Halichoeres maculipinna and H. garnoti, off the Caribbean coast of Panama. Mar Biol 64(3):327–340.  https://doi.org/10.1007/bf00393634 Google Scholar
  86. Romero MC, Lovrich GA, Tapella F, Thatje S (2004) Feeding ecology of the crab Munida subrugosa (Decapoda: Anomura: Galatheidae) in the Beagle Channel, Argentina. J Mar Biol Assoc UK 84(2):359–365.  https://doi.org/10.1017/S0025315404009282h Google Scholar
  87. Roux O, Conand F (2000) Feeding habits of the bigeye scad, Selar crumenophthalmus (Carangidae) in La Reunion Island waters (South-Western Indian Ocean). Cybium 24(2):173–179Google Scholar
  88. Ruiz-Carus R, Matheson RE, Roberts DE, Whitfield PE (2006) The western Pacific red lionfish, Pterois volitans (Scorpaenidae), in Florida: evidence for reproduction and parasitism in the first exotic marine fish established in state waters. Biol Cons 128(3):384–390.  https://doi.org/10.1016/j.biocon.2005.10.012 Google Scholar
  89. Ryan EP (1956) Observations on the life histories and the distribution of the Xanthidae (Mud Crabs) of Chesapeake Bay. Am Midl Nat 56(1):138–162.  https://doi.org/10.2307/2422450 Google Scholar
  90. Samson SA, Yokota M, Strüssmann CA, Watanabe S (2007) Natural diet of grapsoid crab Plagusia dentipes de Haan (Decapoda: Brachyura: Plagusiidae) in Tateyama Bay, Japan. Fish Sci 73(1):171–177.  https://doi.org/10.1111/j.1444-2906.2007.01315.x Google Scholar
  91. Sandel V, Martinez-Fernandez D, Wangpraseurt D, Sierra L (2015) Ecology and management of the invasive lionfish Pterois volitans/miles complex (Perciformes: Scorpaenidae) in Southern Costa Rica. Rev Biol Trop 63(1):213–221PubMedGoogle Scholar
  92. Sedberry GR, Cuellar N (1993) Planktonic and benthic feeding by the reef-associated vermilion snapper, Rhomboplites aurorubens (Teleostei, Lutjanidae). Fish Bull 91(4):699–709Google Scholar
  93. Sharp WC, Hunt JH, Teehan WH (2007) Observations on the ecology of Scyllarides aequinoctialis, Scyllarides nodifer, and Parribacus antarcticus and a description of the Florida Scyllarid lobster fishery. In: Lavalli KL, Spanier E (eds) The biology and fisheries of the slipper lobster. CRC, Boca Raton, pp 231–242Google Scholar
  94. Snyderman M, Wiseman C (1996) Guide to marine life: Caribbean. Aqua Quest Publications Inc, BahamasGoogle Scholar
  95. Squatriglia C (2001) Teeny–tiny predator/vicious shrimp gorging on aquarium’s critters. San Francisco Chronicle, San FranciscoGoogle Scholar
  96. Starck I, Walter A, Colin PL (1978) Gramma linki: a new species of grammid fish from the tropical western Atlantic. Bull Mar Sci 28(1):146–152Google Scholar
  97. Sterrer W (1992) Bermuda’s marine life. Bermuda Natural History Museum and Bermuda Zoological SocietyGoogle Scholar
  98. Sterrer W, Schoepfer-Sterrer C (1986) Marine fauna and flora of Bermuda: a systematic guide to the identification of marine organisms. Wiley, HobokenGoogle Scholar
  99. Swedberg DV, Walburg CH (1970) Spawning and early life history of the freshwater drum in Lewis and Clark Lake, Missouri River. Trans Am Fish Soc 99(3):560–570. https://doi.org/10.1577/1548-8659(1970)99<560:SAELHO>2.0.CO;2
  100. Tirasin EM, Jorgensen T (1999) An evaluation of the precision of diet description. Mar Ecol Prog Ser 182:243–252Google Scholar
  101. Villaseñor-Derbez JC, Herrera-Pérez R (2014) Brief description of prey selectivity and ontogenetic changes in the diet of the invasive lionfish Pterois volitans (Actinopterygii, Scorpaenidae) in the Mexican Caribbean. Pan Am J Aquat Sci 9(2):131–135Google Scholar
  102. Whiteman EA, Côté IM (2004) Monogamy in marine fishes. Biol Rev 79(2):351–375.  https://doi.org/10.1017/S1464793103006304 PubMedGoogle Scholar
  103. Whiteman EA, Côté IM, Reynolds JD (2007) Ecological differences between hamlet (Hypoplectrus: Serranidae) colour morphs: between-morph variation in diet. J Fish Biol 71(1):235–244.  https://doi.org/10.1111/j.1095-8649.2007.01485.x Google Scholar
  104. Woods L, Greenfield D (1978) Holocentridae. In: Fischer W (ed) FAO species identification sheets for fishery purposes. West Central Atlantic (Fishing Area 31), vol 4. FAO, RomeGoogle Scholar
  105. Zhang D, Lin J, LeRoy Creswell R (1998) Mating behavior and spawning of the banded coral shrimp Stenopus hispidus in the laboratory. J Crustac Biol 18(3):511–518Google Scholar

Copyright information

© This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply 2018

Authors and Affiliations

  • Jonathan Peake
    • 1
  • Alex K. Bogdanoff
    • 2
    • 3
  • Craig A. Layman
    • 3
  • Bernard Castillo
    • 4
  • Kynoch Reale-Munroe
    • 4
  • Jennifer Chapman
    • 5
  • Kristen Dahl
    • 6
  • William F. Patterson III
    • 6
  • Corey Eddy
    • 7
  • Robert D. Ellis
    • 8
  • Meaghan Faletti
    • 9
  • Nicholas Higgs
    • 10
  • Michelle A. Johnston
    • 11
  • Roldan C. Muñoz
    • 12
  • Vera Sandel
    • 13
  • Juan Carlos Villasenor-Derbez
    • 14
  • James A. MorrisJr.
    • 2
  1. 1.College of Marine ScienceUniversity of South FloridaSt. PetersburgUSA
  2. 2.NOAA, National Centers for Coastal Ocean ScienceBeaufortUSA
  3. 3.Department of Applied EcologyNorth Carolina State UniversityRaleighUSA
  4. 4.College of Science and MathematicsUniversity of the Virgin IslandsSt. CroixUSA
  5. 5.Level 2 Annex, Omnibus Business CentreBlue Ventures ConservationLondonUK
  6. 6.University of FloridaGainesvilleUSA
  7. 7.Department of BiologyUniversity of Massachusetts DartmouthNorth DartmouthUSA
  8. 8.Fish and Wildlife Research InstituteFlorida Fish and Wildlife Conservation CommissionSt. PetersburgUSA
  9. 9.Department of Biological ScienceFlorida State UniversityTallahasseeUSA
  10. 10.Marine InstitutePlymouth UniversityPlymouthUK
  11. 11.NOAA, Flower Garden Banks National Marine SanctuaryGalvestonUSA
  12. 12.Southeast Fishery Science CenterNOAA, National Marine Fishery ServiceBeaufortUSA
  13. 13.Programa de Maestríaen Ciencias Marinas y Costerasde laUniversidad Nacional de Costa RicaPuntarenasCosta Rica
  14. 14.Bren School of Environmental Science and ManagementUniversity of CaliforniaSanta BarbaraUSA

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