Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-10T08:07:31.939Z Has data issue: false hasContentIssue false

Investigating food assimilation in a carnivorous teleost by stable isotopes analysis: the case of ribbonfish off south-east Brazil

Published online by Cambridge University Press:  20 April 2020

Ana Paula Madeira Di Beneditto*
Affiliation:
Laboratório de Ciências Ambientais, Centro de Biociências e Biotecnologia, Universidade Estadual do Norte Fluminense Darcy Ribeiro – UENF, Av. Alberto Lamego, 2000, Campos dos Goytacazes, RJ, 28013-602, Brazil
Pedro Viana Gatts
Affiliation:
Laboratório de Ciências Ambientais, Centro de Biociências e Biotecnologia, Universidade Estadual do Norte Fluminense Darcy Ribeiro – UENF, Av. Alberto Lamego, 2000, Campos dos Goytacazes, RJ, 28013-602, Brazil
Vanessa Trindade Bittar
Affiliation:
Laboratório de Ciências Ambientais, Centro de Biociências e Biotecnologia, Universidade Estadual do Norte Fluminense Darcy Ribeiro – UENF, Av. Alberto Lamego, 2000, Campos dos Goytacazes, RJ, 28013-602, Brazil
*
Author for correspondence: Ana Paula Madeira Di Beneditto, E-mail: anapaula@uenf.br, anadibeneditto@gmail.com

Abstract

This study verifies the food assimilation of a carnivorous teleost in different timescales (weeks vs months) and evaluates how it uses the food sources. The target species is the adult ribbonfish, Trichiurus lepturus, a voracious teleost caught in commercial fisheries off south-east Brazil (21°S–22°S). The isotope models indicated Chirocentrodon bleekerianus as the main food in the ribbonfish diet in the last weeks (liver: 38.5%; 95% credible intervals: 3.4–73.9%) and last months (muscle: 36.2%; 95% credible intervals: 3.4–68.7%). The contribution of other food sources ranges from 10–16% (liver) and from 10–20% (muscle). Food assimilation remains similar at different timescales. The isotope models suggested a strong and long-lasting association of the adult females of ribbonfish with coastal waters along the study area.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alt, KG, Kuhn, T, Münster, J, Klapper, R, Kochmann, J and Klimpel, S (2018) Mesopredatory fishes from the subtropical upwelling region off NW-Africa characterized by their parasite fauna. PeerJ 6, e5339.10.7717/peerj.5339CrossRefGoogle Scholar
Baumgartner, LJ (2007) Diet and feeding habits of predatory fishes upstream and downstream a low-level weir. Journal of Fish Biology 70, 879894.10.1111/j.1095-8649.2007.01352.xCrossRefGoogle Scholar
Bearzi, G, Politi, E, Agazzi, S and Azzellino, A (2006) Prey depletion caused by overfishing and the decline of marine megafauna in the eastern Ionian Sea coastal waters (central Mediterranean). Biological Conservation 127, 373382.10.1016/j.biocon.2005.08.017CrossRefGoogle Scholar
Bittar, VT and Di Beneditto, APM (2009) Diet and potential feeding overlap between Trichiurus lepturus (Osteichthyes: Perciformes) and Pontoporia blainvillei (Mammalia: Cetacea) in northern Rio de Janeiro, Brazil. Zoologia 26, 374378.CrossRefGoogle Scholar
Bittar, VT, Castello, BFL and Di Beneditto, APM (2008) Hábito alimentar do peixe-espada adulto, Trichiurus lepturus, na costa norte do Rio de Janeiro, sudeste do Brasil. Biotemas 21, 8390.CrossRefGoogle Scholar
Bittar, VT, Awabdi, DR, Tonini, WCT, Vidal Júnior, MV and Di Beneditto, APM (2012) Feeding preference of adult females of ribbonfish Trichiurus lepturus L. 1758 through prey proximate-composition and caloric values. Neotropical Ichthyology 10, 93203.CrossRefGoogle Scholar
Bonfim, BC, Santos, AFGN and Di Beneditto, APM (2017) A pesca extrativa marinha no porto de Atafona, São Joção da Barra – RJ: passado e presente. Brazilian Journal of Aquatic Science and Technology 21, http://dx.doi.org/10.14210/bjast.v21n1.10346.Google Scholar
Caut, S, Angulo, E and Courchamp, F (2009) Variation in discrimination factors (d15N and d13C): the effect of diet isotopic values and applications for diet reconstruction. Journal of Applied Ecology 46, 443453.CrossRefGoogle Scholar
Chiou, WD, Chen, CY, Wang, CM and Chen, CT (2006) Food and feeding habits of ribbonfish Trichiurus lepturus in coastal waters of south-western Taiwan. Fisheries Science 72, 373381.10.1111/j.1444-2906.2006.01159.xCrossRefGoogle Scholar
Collette, BB, Smith-Vaniz, WF, Hartmann, S, Bishop, J, Almukhtar, M, Al-Husaini, M, Alghawzi, Q, Kaymaram, F, Abdulqader, E and Alam, S (2015) Trichiurus lepturus. The IUCN Red List of Threatened Species. Cambridge: IUCN, e.T190090A57283875 (Accessed 20 January 2020).Google Scholar
Costalago, D, Navarro, J, Álvarez-Calleja, I and Palomera, I (2012) Ontogenetic and seasonal change in the feeding habits and trophic levels of two small pelagic fish species. Marine Ecology Progress Series 460, 169181.CrossRefGoogle Scholar
Cruz-Torres, J, Martínez-Pérez, JA, Franco-Ló, J and Ramírez-Villalobos, AJ (2014) Biological and ecological aspects of Trichiurus lepturus Linnaeus, 1758 (Perciformes: Trichiuridae) in Boca Del Rio, Veracruz, Mexico. American-Eurasian Journal of Agriculture & Environmental Science 14, 10581066.Google Scholar
Di Beneditto, APM and Tavares, MTM (2019) Notes on the diet of adult yellow catfish Aspistor luniscutis (Pisces: Siluriformes) in northern Rio de Janeiro State, southeastern Brazil. Journal of Threatened Taxa 11, 1392013924.CrossRefGoogle Scholar
Di Beneditto, APM, Ramos, RMA and Lima, NRW (2001) Os Golfinhos: Origem, classificação, captura acidental, hábito alimentar, 1st Edn. Porto Alegre: Editora Cinco Continentes.Google Scholar
Di Beneditto, APM, Bittar, VT, Camargo, PB, Rezende, CE and Kehrig, HA (2012) Mercury and nitrogen isotope in a marine species from a tropical coastal food web. Archives of Environmental Contamination and Toxicology 62, 264271.CrossRefGoogle Scholar
Di Beneditto, APM, Santos, RA, Rosa, KR and Siciliano, S (2015) Magellanic penguins: stomach contents and isotopic profiles to assess the feeding demands of juveniles in a wintering area off Brazil. Journal of the Marine Biological Association of the United Kingdom 95, 423430.10.1017/S0025315414001532CrossRefGoogle Scholar
Di Beneditto, APM, Tavares, MTM and Monteiro, LR (2018) Isotopic niche of the catfishes Bagre bagre and Genidens barbus in a coastal area of south-eastern Brazil. Biota Neotropica 18, e20180527.CrossRefGoogle Scholar
Elston, C, von Brandis, RG and Cowley, PD (2015) Gastric lavage as a non-lethal method for stingray (Myliobatiformes) diet sampling. African Journal of Marine Science 37, 415419.CrossRefGoogle Scholar
Estes, JA, Terborgh, J, Brashares, JS, Power, ME, Berger, J, Bond, WJ, Carpenter, SR, Essington, TE, Holt, RD, Jackson, JBC, Marquis, RJ, Oksanen, L, Oksanen, T, Paine, RT, Pikitch, EK, Ripple, WJ, Sandin, AS, Csheffer, M, Schoener, TW, Shurin, JB, Sinclair, ARE, Sulé, mE, Virtanen, R and Wardle, DA (2011) Trophic downgrading of planet earth. Science (New York, N.Y.) 333, 301306.10.1126/science.1205106CrossRefGoogle ScholarPubMed
FAO – Food and Agriculture Organization of the United Nations (2014) FAO Fisheries and Aquaculture Department. Summary tables of fishery statistics. http://www.fao.org/fishery/docs/STAT/summary/default.htm (Accessed 10 November 2019).Google Scholar
FAO – Food and Agriculture Organization of the United Nations (2019) FAO Yearbook. Fishery and Aquaculture Statistics 2017. http://www.fao.org/fishery/static/Yearbook/YB2017_USBcard/booklet/CA5495T_web.pdf (Accessed 20 January 2020).Google Scholar
Fernandes, LP, Keunecke, KA and Di Beneditto, APM (2014) Produção e socio economia da pesca do camarão sete-barbas no norte do Estado do Rio de Janeiro. Boletim do Instituto de Pesca 40, 541555.Google Scholar
Froese, R and Pauly, D (2019) FishBase. http://www.fishbase.org (Accessed 15 September 2019).Google Scholar
Fry, B (2008) Stable Isotope Ecology, 3rd Edn. New York, NY: Springer-Verlag.Google Scholar
Greenwell, CN, Coulson, PG, Tweedley, JR and Loneragan, NR (2018) Regional differences in the feeding of the ambush predator Neosebastes pandus and comparisons of diets in the Scorpaenidae, Triglidae and Platycephalidae. Journal of Fish Biology 93, 95109.10.1111/jfb.13677CrossRefGoogle ScholarPubMed
Jackson, AL, Inger, R, Parnell, AC and Bearhop, S (2011) Comparing isotopic niche widths among and within communities: SIBER – Stable Isotope Bayesian Ellipses in R. Journal of Animal Ecology 80, 595602.CrossRefGoogle ScholarPubMed
Jansen, T, Post, S, Olafsdottir, AH, Reynisson, P, Oskarsson, GJ and Arendt, KE (2019) Diel vertical feeding behaviour of Atlantic mackerel (Scomber scombrus) in the Irminger current. Fisheries Research 214, 2534.10.1016/j.fishres.2019.01.020CrossRefGoogle Scholar
Kohlbach, D, Schaafsma, FL, Graeve, M, Lebreton, B, Lange, BA, David, C, Vortkamp, M and Flores, H (2017) Strong linkage of polar cod (Boreogadus saida) to sea ice algae-produced carbon: evidence from stomach content, fatty acid and stable isotope analyses. Progress in Oceanography 152, 6274.CrossRefGoogle Scholar
Landry, JJ, Fisk, AT, Yurkowski, DJ, Hussey, NE, Dick, T, Crawford, RE and Kessel, ST (2018) Feeding ecology of a common benthic fish, shorthorn sculpin (Myoxocephalus scorpius) in the high arctic. Polar Biology 41, 20192102.CrossRefGoogle Scholar
Liu, Y, Cheng, J and Chen, Y (2009) A spatial analysis of trophic composition: a case study of hairtail (Trichiurus japonicus) in the East China Sea. Hydrobiologia 632, 7990.CrossRefGoogle Scholar
Logan, JM, Jardine, TD, Miller, TJ, Bunn, SE, Cunjak, RA and Lutcavage, ME (2008) Lipid corrections in carbon and nitrogen stable isotope analyzes: comparison of chemical extraction and modelling methods. Journal of Animal Ecology 77, 838846.CrossRefGoogle Scholar
Martins, AS and Haimovici, M (1997) Distribution, abundance and biological interactions of the cutlassfish Trichiurus lepturus in the Southern Brazil subtropical convergence ecosystem. Fisheries Research 30, 217227.CrossRefGoogle Scholar
Martins, AS, Haimovici, M and Palacios, R (2005) Diet and feeding of the cutlassfish Trichiurus lepturus in the Subtropical Convergence ecosystem of southern Brazil. Journal of the Marine Biological Association of the United Kingdom 85, 12231229.10.1017/S002531540501235XCrossRefGoogle Scholar
Matley, JK, Fisk, AT, Tobin, AJ, Heupel, MR and Simpfendorfer, CA (2016) Diet-tissue discrimination factors and turnover of carbon and nitrogen stable isotopes in tissues of an adult predatory coral reef fish, Plectropomus leopardus. Rapid Communications in Mass Spectrometry 30, 2944.10.1002/rcm.7406CrossRefGoogle ScholarPubMed
Nakamura, I and Parin, NV (1993) FAO Species Catalogue (Vol. 15). Snake mackerels and cutlassfishes of the world (families Gempylidae and Trichiuridae). An annotated and illustrated catalogue of the snake mackerels, snoeks, escolars, gemfishes, sackfishes, domine, oilfish, cutlassfishes, scabbardfishes, hairtails and frostfishes known to date. FAO Fisheries Synopsis 125, 136 pp.Google Scholar
Newsome, SD, Del Rio, CM, Bearhop, S and Phillips, DL (2007) A niche for isotopic ecology. Frontiers in Ecology and Environment 5, 429436.10.1890/1540-9295(2007)5[429:ANFIE]2.0.CO;2CrossRefGoogle Scholar
Newsome, SD, Bentall, GB, Tinker, MT, Oftedal, OT, Ralls, K, Estes, JA and Fogel, ML (2010) Variation in δ13C and δ15N diet-vibrissae trophic discrimination factors in a wild population of California sea otters. Ecological Applications 20, 17441752.CrossRefGoogle Scholar
Parnell, AC, Inger, R, Bearhop, S and Jackson, AL (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS ONE 5, e9672.CrossRefGoogle ScholarPubMed
Pereira, LS, Agostinho, AA and Winemiller, KO (2017) Revisiting cannibalism in fishes. Review of Fish Biology and Fisheries 27, 499513.10.1007/s11160-017-9469-yCrossRefGoogle Scholar
Phillips, DL, Inger, R, Bearhop, S, Jackson, AL, Moore, JW, Parnell, AC, Semmens, BX and Ward, EJ (2014) Best practices for use of stable isotope mixing models in food-web studies. Canadian Journal of Zoology 92, 823835.CrossRefGoogle Scholar
Pierce, GJ and Boyle, PR (1991) A review of methods for diet analysis in piscivorous marine mammals. Oceanography and Marine Biology: an Annual Review 29, 409486.Google Scholar
Polito, MJ, Trivelpiece, WZ, Karnovsky, NJ, Ng, E, Patterson, WP and Emslie, SD (2011) Integrating stomach content and stable isotope analyses to quantify the diets of Pygoscelid penguins. PLoS ONE 6, e26642.CrossRefGoogle ScholarPubMed
Post, DM, Layman, CA, Arrington, DA, Takimoto, G, Quattrochi, J and Montaña, CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152, 179189.CrossRefGoogle ScholarPubMed
Prikryl, T and Novosad, B (2009) Direct evidence of cannibalism in the Oligocene cutlassfish Anenchelum glarisianum Blainvillei, 1818 (Perciformes: Trichiuridae). Bulletin of Geosciences 84, 569572.10.3140/bull.geosci.1114CrossRefGoogle Scholar
R Core Team (2019) R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. Available at https://www.R-project.org/.Google Scholar
Roper, CFE, Sweeney, MJ and Nauen, CE (1984) FAO Species Catalogue (Vol. 3) – Cephalopods of the World, 1st Edn. Rome: FAO. Available at http://www.fao.org/3/ac479e/ac479e00.htm.Google Scholar
Shelton, AO and Mangel, M (2011) Fluctuations of fish populations and the magnifying effects of fishing. Proceedings of the National Academy of Sciences USA 108, 70757080.10.1073/pnas.1100334108CrossRefGoogle ScholarPubMed
Silveira, EL, Semmar, N, Cartes, JE, Tuset, VM, Lombarte, A, Ballester, ELC and Vaz-dos-Santos, AM (2020) Methods for trophic ecology assessment in fishes: a critical review of stomach analyses. Reviews in Fisheries Science & Aquaculture 28, 71106.CrossRefGoogle Scholar
Stock, BC and Semmens, BX (2016) MixSIAR GUI User Manual. Version 3.1. Vienna: The R Foundation. Available at https://github.com/brianstock/MixSIAR/.Google Scholar
Tavares, MTM and Di Beneditto, APM (2017) Feeding habits and behaviour of Bagre bagre and Genidens barbus, two ariid catfishes (Pisces: Siluriformes) from Southeastern Brazil. Journal of Threatened Taxa 9, 1077110775.CrossRefGoogle Scholar
Venables, WN and Ripley, BD (2002) Modern Applied Statistics with S, 4th Edn. New York, NY: Springer-Verlag.CrossRefGoogle Scholar
Wallach, AD, Izhaki, I, Toms, JD, Ripple, WJ and Shanas, U (2015) What is an apex predator? Oikos 124, 14531461.CrossRefGoogle Scholar
Willems, T, De Backer, A, Kerkhove, T, Dakriet, NN, De Troch, M, Vincx, M and Hostens, K (2016) Trophic ecology of Atlantic sea-bob shrimp Xiphopenaeus kroyeri: intertidal benthic microalgae support the subtidal food web off Suriname. Estuarine Coastal and Shelf Science 182, 146157.CrossRefGoogle Scholar
Yan, Y, Hou, G, Chen, J, Lu, H and Jin, X (2011) Feeding ecology of hairtail Trichiurus margarites and largehead hairtail Trichiurus lepturus in the Beibu Gulf, the South China Sea. Chinese Journal of Oceanology and Limnology 29, 174183.10.1007/s00343-011-0004-zCrossRefGoogle Scholar