Abstract
Large pelagic predators occupy high positions in food webs and could control lower trophic level species by direct and indirect ecological interactions. In this study we aimed to test the hypotheses: (1) pelagic predators are keystone species, and their removals could trigger impacts on the food chain; (2) higher landings of pelagic predators could trigger fishing impacts with time leading to a drop in the mean trophic level of catches; and (3) recovery in the pelagic predators populations, especially for sharks, could be achieved with fishing effort reduction. We performed a food web approach using an Ecopath with Ecosim model to represent the Southeastern and Southern Brazil, a subtropical marine ecosystem, in 2001. We then calibrated the baseline model using catch and fishing effort time series from 2001 to 2012. Afterwards, we simulated the impact of fishing effort changes on species and assessed the ecological impacts on the pelagic community from 2012 to 2025. Results showed that the model was well fitted to landing data for the majority of groups. The pelagic predators species were classified as keystone species impacting mainly on pelagic community. The ecosystem was resilient and fisheries seem sustainable at that time. However, the temporal simulation, from 2001 to 2012, revealed declines in the biomass of three sharks, tuna and billfish groups. It was possible observe declines in the mean trophic level of the catch and in the mean total length of landings. Longline fisheries particularly affected the sharks, billfish and swordfish, while hammerhead sharks were mostly impacted by gillnet fishery. Model simulations showed that large sharks’ biomasses could be recovered or maintained only after strong fishing effort reduction.
Similar content being viewed by others
References
Ahrens R, Walters C, Christensen V (2011) Foraging arena theory. Fish Fish 13:41–49
Allen RR (1971) Relation between production and biomass. J Fish Res Board Can 28:1573–1581
Amaral ACZ, Rossi-Wongtschowski CLDB (2004) Biodiversidade bentônica da região Sudeste-Sul do Brasil—plataforma externa e talude superior. Série documentos REVIZEE, Instituto Oceanográfico da Univ. de São Paulo, São Paulo
Amorim AF, Arfelli CA, Fagundes L (1998) Pelagic elasmobranchs caught by long liners off southern Brazil during 1974–97: an overview. Mar Fresh Res 49:621–632
Angelini R, Morais RJ, Catella AC, Resende EK, Libralato S (2013) Aquatic food webs of the oxbow lakes in the Pantanal: A new site for fisheries guaranteed by alternated control? Ecol Model 253:82–96
Arancibia H, Neira S (2005) Long-term changes in the mean trophic level of Central Chile fishery landings. Sci Mar 69:295–300
Baeta F, Costa MJ, Cabral H (2009) Changes in the trophic level of Portuguese landings and fish market price variation in the last decades. Fish Res 97:216–222
Barreto RP (2015) Historia de Vida e Vulnerabilidade dos Tubarões Oceânicos do Atlantico Sul. PhD Thesis, Universidade Federal Rural de Pernambuco, Brazil
Barreto R, Ferretti F, Mills J, Amorim A, Andrade H, Worm B, Lessa R (2016) Trends in the exploitation of South Atlantic shark populations. Conserv Biol 30:792–804
Baum JK, Worm B (2009) Cascading top-down effects of changing oceanic predator abundances. J Anim Ecol 78:699–714
Bornatowski H, Braga RR, Vitule JRS (2013) Shark mislabeling threatens biodiversity. Science 340(6135):923
Bornatowski H, Braga RR, Vitule JRS (2014a) Threats to sharks in a developing country: the need for effective simple conservation measures. Nat Conserv 12(1):11–18
Bornatowski H, Navia AF, Braga RR, Abilhoa V, Corrêa MFM (2014b) Ecological importance of sharks and rays in a structural foodweb analysis in southern Brazil. ICES J Mar Sci 71(7):1586–1592
Bornatowski H, Barreto RP, Navia AF, Amorim AF (2016) Topological redundancy and “small-world” patterns in a food web in a subtropical ecosystem of Brazil. Mar Ecol. doi:10.1111/maec.12407
Bornatowski H, Braga RR, Barreto RP (2017 in press) Elasmobranchs consumption in Brazil: impacts and consequences. In: Rossi-Santos MR, Finkl CW (eds) Advances in marine vertebrate research in Latin America. Springer, Berlin. ISBN: 978-3-319-56984-0. doi:10.1007/978-3-319-56985-7_10
Britten GL, Dowd M, Minto C, Ferretti F, Boero F, Lotze HK (2014) Predator decline leads to decreased stability in a coastal fish community. Ecol Lett 17:1518–1525
Burrows MT, Schoeman DS, Buckley LB, Moore P, Poloczanska ES et al (2011) The pace of shifting climate in marine and terrestrial ecosystems. Science 334:652–655
Camhi M, Fowler S, Musick J, Bräutigam A, Fordham S (1998) Sharks and their relatives: ecology and conservation. Occas Pap IUCN Species Surv Comm 20:63
Carvalho F, Ahrens R, Murie D, Bigelow K, Aires-Silva A, Maunder MN, Hazin F (2015) Using pop-up satellite archival tags to inform selectivity in fisheries stock assessment models: a case study for the blue shark in the South Atlantic Ocean. ICES J Mar Sci Journal du Conseil 72(6):1715–1730
Christensen V, Walters CJ (2004) Trade-offs in ecosystem-scale optimization of fisheries management policies. Bull Mar Sci 74(3):549–562
Christensen V, Walters C, Pauly D, Forrest R (2008) Ecopath with Ecosim version 6. User Guide. Lenfest Ocean Futures Project
Coll M, Shannon LJ, Moloney CL, Palomera I, Tudela S (2006) Comparing trophic flows and fishing impacts of a NW Mediterranean ecosystem with coastal upwelling systems by means of standardized models and indicators. Ecol Model 198:53–70
Coll M, Santojanni A, Palomera I, Arneri E (2010) Ecosystem assessment of the North-Central Adriatic Sea: towards a multivariate reference framework. Mar Ecol Prog Ser 417:193–210
Coll M, Navarro J, Palomera I (2013a) Ecological role, fishing impact, and management options for the recovery of a Mediterranean endemic skate by means of food web models. Biol Conserv 157:108–120
Coll M, Navarro J, Olson R, Christensen V (2013b) Assessing the trophic position and ecological role of squids in marine ecosystems by means of food-web models. Deep Sea Res II Top Stud Oceanogr 95:21–36
Coll M, Shannon LJ, Kleisner K et al (2016) Ecological indicators to capture the effects of fishing on biodiversity and conservation status of marine ecosystems. Ecol Indic 60:947–962
Collette B, Carpenter K, Polidoro B, Juan-Jordai M, Boustany A et al (2011) High value and long life—double jeopardy for tunas and billfishes. Science 333:291–292
Corrales X, Coll M, Tecchio S, Bellido JM, Fernández ÁM, Palomera I (2015) Ecosystem structure and fishing impacts in the northwestern Mediterranean Sea using a food web model within a comparative approach. J Mar Syst 148:183–199
Cox SP, Essington TE, Kitchell JF, Martell SJD, Walters CJ, Boggs C, Kaplan I (2002) Reconstructing ecosystem dynamics in the central Pacific Ocean, 1952–1998. II. A preliminary assessment of the trophic impacts of fishing and effects on tuna dynamics. Can J Aquat Sci 59:1736–1747
Darimont CT, Fox CH, Bryan HM, Reimchen TE (2015) The unique ecology of human predators. Science 349:858–860
Dario F, Alves CBM, Boos H et al (2015) A better way forward for Brazil’s fisheries. Science 347:1079
Dent F, Clarke S (2015) State of the global market for shark products. FAO fisheries and aquaculture technical paper no. 590. Rome, FAO
Domingo A, Forselledo R, Miller P, Jiménez S, Mas F, Pons M (2014) General description of longline fisheries. ICCAT manual, 3.1.2. http://www.iccat.es/Documents/SCRS/Manual/CH3/CHAP_3_1_2_LL_ENG.pdf. Assessed 05 Oct 2016
Dulvy NK, Baum JK, Clarke S et al (2008) You can swim but you can’t hide: the global status and conservation of oceanic pelagic sharks. Aquat Conserv 18:459–482
Dulvy NK, Harisson LR, Carlson JK et al (2014) Extinction risk and conservation of the world’s sharks and rays. eLife 3: e00590
Fahrbach E, Meincke J (1979) Some observations on the variability of the Cabo Frio upwelling. CUEA Newsl 8(3):13–18
Ferretti F, Worm B, Britten GL, Heithaus MR, Lotze HK (2010) Patterns and ecosystem consequences of shark declines in the ocean. Ecol Lett 13:1055–1071
Freire KMF, Pauly D (2010) Fishing down Brazilian marine food webs, with emphasis on the east Brazil large marine ecosystem. Fish Res 105(1):57–62
Freire KMF, Christensen V, Pauly D (2008) Description of the East Brazil Large Marine Ecosystem using a trophic model. Sci Mar 72: 477-491
Freire KMF, Aragão JAN, Araújo ARR et al (2014) Revisiting Brazilian catch data for Brazilian marine waters (1950–2010). Fisheries Centre, University of British Columbia. Working paper series. Working paper pp 23–41
Froese R, Pauly D (2015) FishBase. http://www.fishbase.org. Accessed 20 Nov 2015
Gasalla MA, Rossi-Wongtschowski CLDB (2004) Contribution of ecosystem analysis to investigating the effects of changes in fishing strategies in the South Brazil Bight coastal ecosystem. Ecol Model 172:283–306
Gasalla MA, Velasco G, Rossi-Wongtschowski CLDB, Haimovici M, Madureira LSP (2007). Modelo de equilíbrio de biomassas do ecossistema marinho da Região Sudeste-Sul do Brasil entre 100–1000 m de profundidade. Série documentos Revizee: Score Sul
Griffiths SP, Young JW, Lansdell MJ et al (2010) Ecological effects of longline fishing and climate change on the pelagic ecosystem off eastern Australia. Rev Fish Biol Fisher 20:239–272
Haimovici M, Rossi-Wongtschowski CLDB, Ávila-Bernardes R, Fischer LG, Vooren CV, Santos RA, Rodrigues AR, Santos S (2008). Prospecção pesqueira de espécies demersais com rede de arrasto-de-fundo na Região Sudeste-Sul do Brasil. Série documentos REVIZEE, Instituto Oceanográfico da Univ. de São Paulo, São Paulo
Haimovici M, Fischer LG, Rossi-Wongtschowski CLDB, Bernardes RA, Santos RAS (2009) Biomass and fishing potential yield of demersal resources from the outer shelf and slope of southern Brazil. Lat Am J Aquat Res 37(3):395–408
Hall SJ (1999) Fish biology and aquatic resources series 1. Blackwell, Oxford
Harnik PG, Lotze HK, Anderson SC et al (2012) Extinctions in ancient and modern seas. Trends Ecol Evol 27(11):608–617
Hayes CG, Jiao Y, Cortés E (2009) Stock assessment of scalloped hammerheads in the Western North Atlantic Ocean and Gulf of Mexico. N Am J Fish Manage 29(5):1406–1417
Hazin FHV, Broadhurst MK, Amorim AF, Arfelli CA, Domingo A (2008) Catches of pelagic sharks by subsurface longline fisheries in the South Atlantic Ocean during the last century: a review of available data with emphasis on Uruguay and Brazil. In: Camhi MD, Pickitch EA (eds) Sharks of the open ocean: biology, fisheries and conservation. Blackwell, Oxford, pp 213–227
Heithaus MR, Frid A, Wirsing AJ, Worm B (2008) Predicting ecological consequences of marine top predator declines. Trends Ecol Evol 23(4):202–210
Heithaus MR, Frid A, Vaudo JJ, Worm B, Wirsing AJ (2010) Unraveling the ecological importance of elasmobranchs. In: Carrier JC, Musick J, Heithaus MR (eds) Biology of Sharks and their relatives II. CRC Press, Boca Raton, pp 611–637
Heymans JJ, Coll M, Link JS, Mackinson S, Steenbeek J, Walters C, Christensen V (2016) Best practice in Ecopath with Ecosim food-web models for ecosystem-based management. Ecol Model 331:173–184
Hussey NE, MacNeil MA, McMeans BC, Olin JA, Dudley SFJ, Cliff G, Wintner SP, Fennessy ST, Fisk AT (2014) Rescaling the trophic structure of marine food webs. Ecol Lett 17:239–250
Hussey NE, MacNeil MA, Siple MC, Popp BN, Dudley SFJ, Fisk AT (2015) Expanded trophic complexity among large sharks. Food Webs 4:1–7
IUCN (2016) Red list of threatened species. http://www.iucnredlist.org. Accessed on 27 Jan 2017
Jackson JBC, Kirby MX, Berger WH et al (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–638
Kell LT, Urbina JO, Bruyn P (2014) Stock assessment diagnostics for north Atlantic Swordfish. Collect Vol Sci Pap ICCAT 70(4):1954–1963
Kitchell JF, Essington TE, Boggs CH, Schindler DE, Walters CJ (2002) The role of sharks and long-line fisheries in a pelagic ecosystem of central pacific. Ecosystems 5:202–216
Kitchell JF, Martell SJD, Walters CJ, Jensen OP, Kaplan IC, Watters J, Essington TE, Boggs CH (2006) Billfishes in an ecosystem context. Bull Mar Sci 79:669–682
Kotas JE, Petrere M Jr, Fiedler F, Mastrochirico V, Sales G (2008) A pesca de emalhe-de-superfície de Santa Catarina direcionada à captura dos tubarões-martelo, Sphyrna lewini (Griffith & Smith 1834) e Sphyrna zygaena (Linnaeus 1758). Atlântica 30(2):113–128
Leontief WW (1951) The structure of American economy, 1919-1939: an empirical application of equilibrium analysis (No. HC106. 3 L3945 1951)
Libralato S, Christensen V, Pauly D (2006) A method for identifying keystone species in food web models. Ecol Model 195:153–171
Link JS (2010) Adding rigor to ecological network models by evaluating a set of pre-balance diagnostics: a plea for PREBAL. Ecol Model 221:1580–1591
Lucifora LO, García VB, Worm B (2011) Global diversity hotspots an conservation priorities for sharks. PLoS ONE 6:e0019356
Madureira LSP, Rossi-Wongtschowski CLDB (2005) Pros-pecção de recursos pesqueiros pelágicos na Zona Econômica Exclusiva da Região Sudeste-Sul do Brasil: hidroacústica e bio-massas. Série documentos REVIZEE, Instituto Oceanográfico da Univ. de São Paulo, São Paulo
McClenachan L, Cooper AB, Dulvy NK (2016) Rethinking trade-driven extinction risk in marine and terrestrial megafauna. Curr Biol 26:1–7
Mills LS, Soule ME, Doak DF (1993) The keystone-species concept in ecology and conservation. Bioscience 43:219–224
Myers RA, Worm B (2003) Rapid worldwide depletion of predatory fish communities. Nature 423:280–283
Myers RA, Baum JK, Shepherd TD, Powers SP, Peterson CH (2007) Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315:1846–1850
Naem S (1998) Species redundancy and ecosystem reliability. Conserv Biol 12:39–45
Nascimento MC, Velasco G, Okey TA, Christensen V, Amaral C (2010) Trophic model of the outer continental shelf and upper slope demersal community of the southeastern Brazilian Bight. Sci Mar 76:763–779
Navia AF, Cortés E, Mejía-Falla PA (2010) Topological analysis of the ecological importance of elasmobranch fishes: a food web study on the Gulf of Tortugas, Colombia. Ecol Model 221:2918–2926
Navia AF, Cruz-Escalona VH, Giraldo A, Barausse A (2016) The structure of a marine tropical food web, and its implications for ecosystem-based fisheries management. Ecol Model 328:23–33
Odum EP (1969) The strategy of ecosystem development. Science 164:262–270
Okey T, Griffiths S, Pascoe S et al (2007) The effect of illegal foreign fishing on the ecosystem in the Gulf of Carpentaria: management options and downstream effects on other fisheries. Final report to the Australian Fisheries Management Authority for Project 2006/825
Paine RT (1995) A conversation on refining the concept of keystone species. Conserv Biol 9(4):962–964
Palomares MLD, Pauly D (1998) Predicting food consumption of fish populations as functions of mortality, food type, morphometrics, temperature and salinity. Mar Fresh Res 49(5):447–453
Pauly D (1980) On the interrelationships between natural mortality, growth parameters and mean environmental temperature in 175 fish stocks. J Conserv Int Explor Mer 39(3):175–192
Pauly D, Watson R (2005) Background and interpretation of the ‘Marine Trophic Index’ as a measure of biodiversity. Phil Trans R Soc B 360:415–423
Pauly D, Christensen V, Dalsgaard J, Froese R, Torres F (1998) Fishing down marine food webs. Science 279:860–863
Pauly D, Palomares ML, Froese R, Sa-a P, Vakily M, Preikshot D, Wallace S (2001) Fishing down Canadian aquatic food webs. Can J Fish Aquat Sci 58:51–62
Perez JAA, Wahrlich R (2005) A bycatch assessment of the gillnet monkfish Lophius gastrophysus fishery off southern Brazil. Fish Res 72:81–95
Pimm SL, Jenkins CN, Abell R, Brooks TM, Gittleman JL, Joppa LN, Raven PH, Roberts CM, Sexton JO (2014) The biodiversity of species and their rates of extinction, distribution, and protection. Science 344:987
Power ME, Tilman D, Estes JA et al (1996) Challenges in the quest for keystones. Bioscience 46(8):609–620
Ritchie EG, Johnson CN (2009) Predator interactions, mesopredator release and biodiversity conservation. Ecol Lett 12:982–998
Rossi-Wongtschowski CLDB, Ávila-da-Silva AO, Cergole MC (2006) Análise das principais pescarias comerciais do Sudeste-Sul do Brasil: dinâmica populacional das espécies em explotação–Vol. II. Série documentos REVIZEE, Instituto Oceanográfico da Univ. de São Paulo, São Paulo
Scott E, Serpetti N, Steenbeek J, Heymans J (2016) A Stepwise Fitting Procedure for automated fitting of Ecopath with Ecosim models. SoftwareX. doi:10.1016/j.softx.2016.02.002
Shannon L, Coll M, Bundy A et al (2014) Trophic level-based indicators to track fishing impacts across marine ecosystems. Mar Ecol Prog Ser 512:115–140
Shin Y-J, Rochet M-J, Jennings S, Field JG, Gislason H (2005) Using size-based indicators to evaluate the ecosystem effects of fishing. ICES J Mar Sci 62:384–396
Sibert J, Hampton J, Kleiber P, Maunder M (2006) Biomass, size, and trophic status of top predators in the Pacific Ocean. Science 314:1773–1776
Steenbeek J, Buszowski J, Christensen V et al (2016) Ecopath with Ecosim as a model-building toolbox: source code capabilities, extensions, and variations. Ecol Model 319:178–189
Stevens JD, Bonfil R, Dulvy NK, Walker PA (2000) The effects of fishing on sharks, rays, and chimeras (chondrichthyans), and the implications for marine ecosystems. ICES J Mar Sci 57:476–494
Tsagarakis K, Coll M, Giannoulaki M, Somarakis S, Papaconstantinou C, Machias A (2010) Food-web traits of the North Aegean Sea ecosystem (Eastern Mediterranean) and comparison with other Mediterranean ecosystems. Estuar Coast Shelf Sci 88:233–248
Ulanowicz RE, Puccia CJ (1990) Mixed trophic impacts in ecosystems. Coenoses 5:7–16
Valls A, Coll M, Christensen V (2015) Keystone species: toward an operational concept for marine biodiversity conservation. Ecol Monogr 85(1):29–47
Velasco G, Castello JP (2005) An ecotrophic model of southern Brazil continental shelf and fisheries scenarios for Engraulis anchoita (Pisces, Engraulididae). Atlântica 27(1):59–68
Walker BH (1991) Biodiversity and ecological redundancy. Conserv Biol 6:18–23
Walters C, Christensen V (2007) Adding realism to foraging arena predictions of trophic flow rates in Ecosim ecosystem models: shared foraging arenas and about feeding. Ecol Model 209:34–350
Walters C, Christensen V, Pauly D (1997) Structuring dynamic models of exploited ecosystems from trophic mass-balance assessments. Rev Fish Biol Fisher 7:139–172
Walters C, Pauly D, Christensen V, Kitchell JF (2000) Representing density dependent consequences of life history strategies in aquatic ecosystems: Ecosim II. Ecosystems 3:70–83
Worm (2015) A most unusual (super) predator. Science 349:784–785
Worm B, Hilborn R, Baum JK et al (2009) Rebuilding global fisheries. Science 325:578–585
Worm B, Davis B, Kettemer L, Ward-Paige CA, Chapman D, Heithaus MR, Kessel ST, Gruber SH (2013) Global catches, exploitation rates, and rebuilding options for sharks. Mar Policy 40:194–204
Yeakel JD, Dunne JA (2015) Modern lessons from ancient food webs. Am Sci 103:188–195
Zerbini AN, Kotas JE (1998) A note on cetacean bycatch in pelagic driftnetting off southern Brazil. Rep Int Whal Comm 48(1):519–524
Acknowledgements
We thank Dr. Jeffrey Muehlbauer for English reviewing, the São Paulo Research Foundation (FAPESP—2013/25930-0) and the Coordination for the Improvement of Higher Education Personnel (CAPES) for scholarships to HB, and the National Counsel of Technological and Scientific Development (CNPq) for a research grant to RB. CAPES supported M. Coll (Proc. PVE A063/2013, Ed.71/2013). Thanks also to Ministry of Agriculture (Brazilian Government) and University of Vale do Itajaí (UNIVALI) for organizing the dataset of the Landing Statistics Program. Two anonymous reviewers contributed to increase quality of this paper.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
11160_2017_9492_MOESM1_ESM.docx
Online Resource 1 List of input data and references used to build the Ecopath model of the southeastern and southern Brazil (SSB) ecosystem. (DOCX 32 kb)
11160_2017_9492_MOESM3_ESM.xlsx
Online Resource 3 Sections 1 to 3—Section 1: references used to construct the diet composition (DC) matrix; Section 2: original diet composition matrix for the SSB model; Section 3: diet composition matrix adjusted to balance the SSB model. (XLSX 32 kb)
11160_2017_9492_MOESM4_ESM.xlsx
Online Resource 4 Landing data (value in tons); Trophic Level and Maximum Length (cm) used to calculate the Marine Trophic Level Index (MTLI) and the Maximum Total Length (MaxT) for the SSB ecosystem. (XLSX 17 kb)
Rights and permissions
About this article
Cite this article
Bornatowski, H., Angelini, R., Coll, M. et al. Ecological role and historical trends of large pelagic predators in a subtropical marine ecosystem of the South Atlantic. Rev Fish Biol Fisheries 28, 241–259 (2018). https://doi.org/10.1007/s11160-017-9492-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11160-017-9492-z