Augmentation of French grunt diet description using combined visual and DNA-based analyses

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doi:10.1071/MF12099

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Augmentation of French grunt diet description using combined visual and DNA-based analyses

John S. Hargrove ^A ^D, Daryl C. Parkyn ^A, Debra J. Murie ^A, Amanda W. J. Demopoulos ^B and James D. Austin ^A ^C

^A University of Florida, School of Forest Resources and Conservation, Program of Fisheries and Aquatic Sciences, Institute of Food and Agricultural Sciences, PO Box 110600, Gainesville, FL 32611, USA.
^B Southeast Ecological Science Center, US Geological Survey, 7920 NW 71st Street, Gainesville, FL 32653, USA.
^C University of Florida, Department of Wildlife Ecology and Conservation, Institute of Food and Agricultural Sciences, PO Box 110430, Gainesville, FL 32611, USA.
^D Corresponding author. Email: tractor@ufl.edu

Marine and Freshwater Research 63(8) 740-750 http://dx.doi.org/10.1071/MF12099
Submitted: 12 April 2012 Accepted: 13 July 2012 Published: 20 August 2012





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Abstract

Trophic linkages within a coral-reef ecosystem may be difficult to discern in fish species that reside on, but do not forage on, coral reefs. Furthermore, dietary analysis of fish can be difficult in situations where prey is thoroughly macerated, resulting in many visually unrecognisable food items. The present study examined whether the inclusion of a DNA-based method could improve the identification of prey consumed by French grunt, Haemulon flavolineatum, a reef fish that possesses pharyngeal teeth and forages on soft-bodied prey items. Visual analysis indicated that crustaceans were most abundant numerically (38.9%), followed by sipunculans (31.0%) and polychaete worms (5.2%), with a substantial number of unidentified prey (12.7%). For the subset of prey with both visual and molecular data, there was a marked reduction in the number of unidentified sipunculans (visual – 31.1%, combined – 4.4%), unidentified crustaceans (visual – 15.6%, combined – 6.7%), and unidentified taxa (visual – 11.1%, combined – 0.0%). Utilising results from both methodologies resulted in an increased number of prey placed at the family level (visual – 6, combined – 33) and species level (visual – 0, combined – 4). Although more costly than visual analysis alone, our study demonstrated the feasibility of DNA-based identification of visually unidentifiable prey in the stomach contents of fish.

Additional keywords: molecular, morphological, PCR, stomach contents, US Virgin Islands.

References

Abele, L. G., and Kim, W. (1989). ‘An Illustrated Guide to the Marine Decapod Crustaceans of Florida.’ (State of Florida Department of Environmental Regulation: Tallahassee, FL.)

Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, Z., Miller, W., and Lipman, D. J. (1997). Gapped BLAST and PSI–BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 3389–3402.
| CrossRef | CAS |

Berens, E. J., and Murie, D. J. (2008). Differential digestion and evacuation rates of prey in a warm-temperate grouper, gag Mycteroperca microlepis (Goode & Bean). Journal of Fish Biology 72, 1406–1426.
| CrossRef |

Blankenship, L. E., and Yayanos, A. A. (2005). Universal primers and PCR of gut contents to study marine invertebrate diets. Molecular Ecology 14, 891–899.
| CrossRef | CAS |

Böhlke, J. E., and Chaplin, C. C. G. (1993). ‘Fishes of the Bahamas and Adjacent Tropical Waters.’ 2nd edn. (University of Texas Press: Austin, TX.)

Braley, M., Goldsworthy, S. D., Page, B., Steer, M., and Austin, J. J. (2010). Assessing morphological and DNA-based diet analysis techniques in a generalist predator, the arrow squid Nototodarus gouldi. Molecular Ecology Resources 10, 466–474.
| CrossRef | CAS |

Bucklin, A., Steinke, D., and Blanco-Bercial, L. (2011). DNA barcoding of marine metazoa. Annual Review of Marine Science 3, 471–508.
| CrossRef |

Buhay, J. E. (2009). ’COI-like‘ sequences are becoming problematic in molecular systematic and DNA barcoding studies. Journal of Crustacean Biology 29, 96–110.
| CrossRef |

Carreon-Martinez, L., Johnson, T. B., Ludsin, S. A., and Heath, D. D. (2011). Utilization of stomach content DNA to determine diet diversity in piscivorous fishes. Journal of Fish Biology 78, 1170–1182.
| CrossRef | CAS |

Casper, R., Jarman, S., Gales, N., and Hindell, M. (2007). Combining DNA and morphological analyses of faecal samples improves insight into trophic interactions: a case study using a generalist predator. Marine Biology 152, 815–825.
| CrossRef |

Chen, Y., Giles, K. L., Payton, M. E., and Greenstone, M. H. (2000). Identifying key cereal aphid predators by molecular gut analysis. Molecular Ecology 9, 1887–1898.
| CrossRef | CAS |

Clare, E. L., Barber, B. R., Sweeney, B. W., Hebert, P. D., and Fenton, M. B. (2011). Eating local: influences of habitat on the diet of little brown bats (Myotis lucifugus). Molecular Ecology 20, 1772–1780.
| CrossRef | CAS |

Cocheret de la Morinière, E., Pollux, B. J. A., Nagelkerken, I., Hemminga, M. A., Huiskes, A. H. L., and van der Velde, G. (2003a). Ontogenetic dietary changes of coral reef fishes in the mangrove–seagrass–reef continuum: stable isotopes and gut-content analysis. Marine Ecology Progress Series 246, 279–289.
| CrossRef |

Cocheret de la Morinière, E., Pollux, B. J. A., Nagelkerken, I., and van der Velde, G. (2003b). Diet shifts of Caribbean grunts (Haemulidae) and snappers (Lutjanidae) and the relation with nursery-to-coral reef migrations. Estuarine, Coastal and Shelf Science 57, 1079–1089.
| CrossRef |

Cutler, E. B. (1994). ‘The Sipuncula: Their Systematics, Biology, and Evolution.’ (Cornell University Press: Ithaca, NY.)

Danilowicz, B. S., and Sale, P. F. (1999). Relative intensity of predation on the French grunt, Haemulon flavolineatum, during diurnal, dusk, and nocturnal periods on a coral reef. Marine Biology 133, 337–343.
| CrossRef |

Davis, W. P. (1967). Ecological interactions, comparative biology and evolutionary trends of thirteen pomadasyid fishes of Alligator Reef, Florida Keys. Ph. D. Thesis, University of Miami, FL.

Deagle, B. E. (2006). DNA-based methods for studying the diet of marine predators. Ph. D. Thesis, University of Tasmania, Burnie.

Deagle, B. E., Gales, N. J., Evans, K., Jarman, S. N., Robinson, S., Trevilco, R., and Hindell, M. A. (2007). Studying seabird diet through genetic analysis of faeces: a case study on Macaroni penguins (Eudyptes chrysolophus). PLoS ONE 2, e831.
| CrossRef |

Dennis, G. D. (1992). Resource utilization by members of a guild of benthic feeding coral reef fish. Ph.D. Thesis, University of Puerto Rico, Mayagüez.

DeWoody, J. A., Fletcher, D. E., Wilkins, S. D., and Avise, J. C. (2001). Genetic documentation of filial cannibalism in nature. Proceedings of the National Academy of Sciences, USA 98, 5090–5092.
| CrossRef | CAS |

Drummond, A. J., Ashton, B., Buxton, S., Cheung, M., Cooper, A., Duran, C., Field, M., Heled, J., Kearse, M., Markowitz, S., Moir, R., Stones-Havas, S., Sturrock, S., Thierer, T., and Wilson, A. (2011). Geneious v5.4. Available at http://www.geneious.com/ [accessed June 2010]

Dunn, M. R., Szabo, A., McVeagh, M. S., and Smith, P. J. (2010). The diet of deepwater sharks and the benefits of using DNA identification of prey. Deepsea Research. Part I. Oceanographic Research Papers 57, 923–930.
| CrossRef | CAS |

Dunshea, G., Barros, N. B., Wells, R. S., Gales, N. J., Hindell, M. A., and Jarman, S. N. (2008). Pseudogenes and DNA-based diet analyses: a cautionary tale from a relatively well sampled predator–prey system. Bulletin of Entomological Research 98, 239–248.
| CrossRef | CAS |

Elias, M., Hill, R. I., Willmott, K. R., Dasmahapatra, K. K., Brower, A. V. Z., Mallet, J., and Jiggins, C. D. (2007). Limited performance of DNA barcoding in a diverse community of tropical butterflies. Proceedings. Biological Sciences 274, 2881–2889.
| CrossRef | CAS |

Estrada, R. M. (1986). Feeding habits of fishes of the genus Haemulon (Pisces:Haemulidae) from the reefs of Santa Marta region, Colombia. Anales del Instituto de Investigaciones Marinas de Punta de Betin 15–16, 49–66.

Fauchald, K. (1977). ‘The Polychaete Worms, Definitions and Keys to the Orders, Families and Genera.’ (Natural History Museum of Los Angeles County: Los Angeles, CA.)

Feller, R. J. (1992). Potential applications of immunoassays in studies of flatfish recruitment. Netherlands Journal of Sea Research 29, 1–5.
| CrossRef |

Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.
| CAS |

Gannon, J. E. (1976). The effects of differential digestion rates of zooplankton by alewife, Alosa pseudoharengus, on determinations of selective feeding. Transactions of the American Fisheries Society 105, 89–95.
| CrossRef |

Gariepy, T. D., Kuhlmann, U., Gillott, C., and Erlandson, M. (2007). Parasitoids, predators and PCR: the use of diagnostic molecular markers in biological control of arthropods. Journal of Applied Entomology 131, 225–240.
| CrossRef | CAS |

Hajibabaei, M., deWaard, J. R., Ivanova, N. V., Ratnasingham, S., Dooh, R. T., Kirk, S. L., Mackie, P. M., and Hebert, P. D. (2005). Critical factors for assembling a high volume of DNA barcodes. Philosophical Transactions of the Royal Society of London 360, 1959–1967.
| CrossRef | CAS |

Halanych, K. M., and Janosik, A. M. (2006). A review of molecular markers used for Annelid phylogenetics. Integrative and Comparative Biology 46, 533–543.
| CrossRef |

Hammerschlag, N., and Serafy, J. E. (2010). Nocturnal fish utilization of a subtropical mangrove–seagrass ecotone. Marine Ecology Berlin 31, 364–374.
| CrossRef |

Hansson, S. (1998). Methods of studying fish feeding: a comment. Canadian Journal of Fisheries and Aquatic Sciences 55, 2706–2707.
| CrossRef |

Hargrove, J. S. (2010). Visual and molecular analysis of French grunt stomach contents from St John, US Virgin Islands. M.Sc. Thesis, University of Florida, Gainesville, FL.

Hebert, P., Cywinsha, A., Ball, S., and deWaard, J. (2003). Biological identifications through DNA barcodes. Proceedings of the Royal Society of London Biological Sciences 270, 313–321.
| CrossRef | CAS |

Hein, R. G. (1999). Age, growth and factors controlling post settlement habitat of juvenile French grunts (Haemulon flavolineatum) near Tobacco Caye, Belize, Central America. Ph.D. Thesis, University of Rhode Island, Kingston, RI.

Helfman, G. S., and Schultz, E. T. (1984). Social transmission of behavioral traditions in a coral reef fish. Animal Behaviour 32, 379–384.
| CrossRef |

Helfman, G. S., Meyer, J. L., and McFarland, W. N. (1982). The ontogeny of twilight migration patterns in grunts – Haemulidae. Animal Behaviour 30, 317–326.
| CrossRef |

Hyslop, E. J. (1980). Stomach contents analysis, a review of methods and their application. Journal of Fish Biology 17, 411–429.
| CrossRef |

Iverson, S. J., Field, C., Don Bowen, W., and Blanchard, W. (2004). Quantitative fatty acid signature analysis: a new method for estimating predator diets. Ecological Monographs 74, 211–235.
| CrossRef |

Johnston, I., Clarke, A., and Ward, P. (1991). Temperature and metabolic rate in sedentary fish from the Antarctic, North Sea and Indo-West Pacific Ocean. Marine Biology 109, 191–195.
| CrossRef |

King, R. A., Read, D. S., Traugott, M., and Symondson, W. O. C. (2008). Molecular analysis of predation: a review of best practice for DNA-based approaches. Molecular Ecology 17, 947–963.
| CrossRef | CAS |

Krebs, C. J. (1999). ‘Ecological Methodology.’ (Addison-Wesley Longman: Menlo Park, CA.)

Krebs, C. J., and Kenney, A. J. (1999). ‘Programs for Ecological Methodology. Version 5.1.’ (Exeter Software: Setauket, NY.

Lowenstein, J. H., Amato, G., and Kolokotronis, S. (2009). The real maccoyii: identifying tuna sushi with DNA barcodes – Contrasting characteristic attributes and genetic distances. PLoS ONE 4, e7866.
| CrossRef |

Mayfield, S., Lopata, A. L., and Branch, G. M. (2000). Limitation and failure of immunological technique (ELISA) in resolving the diet of the South African rock lobster Jasus Ialandii. Marine Biology 137, 595–604.
| CrossRef |

Meusnier, I., Singer, G., Landry, J.-F., Hickey, D. A., Hebert, P., and Hajibabaei, M. (2008). A universal mini-barcode for biodiversity analysis. BMC Genomics 9, 214.
| CrossRef |

Meyer, C. P. (2004). Toward comprehensiveness: increased molecular sampling within Cypraeidae and its phylogenetic implications. Malacologia 46, 127–156.

Meyer, C. P., and Paulay, G. (2005). DNA barcoding: error rates based on comprehensive sampling. PLoS Biology 3, e422.
| CrossRef |

Meyer, J. L., and Schultz, E. T. (1985). Migrating Haemulid fishes as a source of nutrient and organic matter on coral reefs. Limnology and Oceanography 30, 146–156.
| CrossRef |

Muller, E., Rogers, C., Spitzack, A., and van Woesik, R. (2008). Bleaching increases likelihood of disease on Acropora palmata (Lamarck) in Hawksnest Bay, St John, US Virgin Islands. Coral Reefs 27, 191–195.
| CrossRef |

Murie, D. J., and Lavigne, D. M. (1991). Food consumption of wintering harp seals, Phoca groenlandica, in the St Lawrence Estuary, Canada. Canadian Journal of Zoology 69, 1289–1296.
| CrossRef |

Murie, D. J., and Parkyn, D. C. (2001). Development and implementation of a non-lethal method for collection of stomach contents in relation to diel feeding periodicity: Phase II. Consumption of brachiopods as a model food source for Gulf of Mexico sturgeon. Report to the Florida Fish and Wildlife Conservation Commission. Florida Marine Research Institute, St Petersburg, FL.

Nagelkerken, I., Dorenbosch, M., Verberk, W. C. E. P., Cocheret de la Morinière, E., and van der Velde, G. (2000). Day-night shifts of fishes between shallow-water biotopes of a Caribbean bay, with emphasis on the nocturnal feeding of Haemulidae and Lutjanidae. Marine Ecology Progress Series 194, 55–64.
| CrossRef |

Nagelkerken, I., van der Velde, G., Verberk, W. C. E. P., and Dorenbosch, M. (2006). Segregation along multiple resource axes in a tropical seagrass fish community. Marine Ecology Progress Series 308, 79–89.
| CrossRef |

Ogden, J. C., and Ehrlich, P. R. (1977). The behavior of heterotypic resting schools of juvenile grunts Pomadasyidae. Marine Biology Berlin 42, 273–280.
| CrossRef |

Ohman, M. D., Theilacker, G. H., and Kaupp, S. E. (1991). Immunochemical detection of predation on ciliate protists by larvae of the northern anchovy (Engraulis mordax). The Biological Bulletin 181, 500–504.
| CrossRef |

Pawlowski, J. (2000). Introduction to the molecular systematics of Foraminifera. Micropaleontology 46, 1–12.

Pertsemlidis, A., and Fondon, J. W. (2001). Having a BLAST with bioinformatics (and avoiding BLASTphemy). Genome Biology 2, .
| CAS |

R Development Core Team (2010). ‘R: a Language and Environment for Statistical Computing, Reference Index Version 2.1.4.1.’ (R Foundation for Statistical Computing: Vienna.) Available at http://www.R-project.org [accessed July 2010]

Randall, J. E. (1967). Food habits of reef fishes of the West Indies. Studies in Tropical Oceanography 5, 665–847.

Ratnasingham, S., and Hebert, P. N. (2007). BOLD: the barcode of life data system (http://www.barcodinglife.org). Molecular Ecology Notes 7, 355–364.
| CrossRef | CAS | http://www.barcodinglife.org).&title=Molecular Ecology Notes&date=2007&volume=7&spage=355&epage=364&sid=csiro&aulast=Ratnasingham&aufirst=S." target="_blank" >

Rosel, P. E., and Kocher, T. D. (2002). DNA-based identification of larval cod in stomach contents of predatory fishes. Journal of Experimental Marine Biology and Ecology 267, 75–88.
| CrossRef |

Ross, H. A., Murugan, S., and Sibon Li, W. L. (2008). Testing the reliability of genetic methods of species identification via simulation. Systematic Biology 57, 216–230.
| CrossRef |

Saitoh, K., Takagaki, M., and Yamashita, Y. (2003). Detection of Japanese flounder-specific DNA from gut contents of potential predators in the field. Fisheries Science 69, 473–477.
| CrossRef | CAS |

Sheffield, G., Fay, F. H., Feder, H., and Kelly, B. P. (2001). Laboratory digestion of prey and interpretation of walrus stomach contents. Marine Mammal Science 17, 310–330.
| CrossRef |

Smith, P. J., McVeagh, S. M., Allain, V., and Sanchez, C. (2005). DNA identification of gut contents of large pelagic fishes. Journal of Fish Biology 67, 1178–1183.
| CrossRef |

Symondson, W. O. C. (2002). Molecular identification of prey in predator diets. Molecular Ecology 11, 627–641.
| CrossRef | CAS |

Tollit, D. J., Schulze, A. D., Trites, A. W., Olesiuk, P. F., Crockford, S. J., Ream, R. R., and Killer, K. M. (2009). Development and application of DNA techniques for validating and improving pinniped diet estimates. Ecological Applications 19, 889–905.
| CrossRef |

Ward, R. D., Zemlak, T. S., Innes, B. H., Last, P. R., and Hebert, P. D. (2005). DNA barcoding Australia’s fish species. Philosophical Transactions of the Royal Society B. Biological Sciences 360, 1847–1857.
| CrossRef | CAS |

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