Abstract
The lower abundance, biomass, and homogenization of sizes of herbivorous fish caused by overfishing may lead to a disproportionate loss of functions. The present work explores to which extent fishing affects species niche and functions by comparing the isotopic niche breadth and redundancy and resource use in a herbivorous fish community. While the video analysis was not able to discriminate large differences in feeding preferences, all ate preferentially the epilithic algal matrix (EAM), the SIA suggests that within the marine protected area (MPA) fish may be feeding on more diverse sources (greater amplitude of isotopic niche) and have more overlapping niches (greater redundancy). Corroborating with works that claim that the delimitation of MPAs can contribute to the redundancy of functions and resilience of coral reefs. For clarifying if fish are using (preying on or digesting) different resource species or same, the species in different environments with different basal SI values would definitively need to have a better isotopic characterization of resources within the MPA. Our work contributes to new discoveries that have implications for the conservation of coral reefs, as fishing appears not only to affect the biomass and body size of herbivorous fish but also reduces the trophic niche of fish species, compromising many of their ecological functions.
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The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Adam TC, Duran A, Fuchs CE, Roycroft MV, Rojas MC, Ruttenberg BI, Burkepile DE (2018) Comparative analysis of foraging behavior and bit mechanics reveals complex functional diversity among Caribbean parrotfishes. Mar Ecol Prog Ser 597:207–220. https://doi.org/10.3354/meps12600
Barnes C, Sweeting CJ, Jennings S, Barry JT, Polunin NV (2007) Effect of temperature and ration size on carbon and nitrogen stable isotope trophic fractionation. Funct Ecol 21(2):356–362. https://doi.org/10.1111/j.1365-2435.2006.01224.x
Bellwood DR, Choat JH (1990) A functional analysis of grazing in parrotfishes (family Scaridae): the ecological implications. In: Bruton MN (ed) Alternative life-history styles of fishes. Springer, Netherlands, Dordrecht, pp 189–214. https://doi.org/10.1007/978-94-009-2065-1_11
Bellwood DR, Hoey AS, Choat JH (2003) Limited functional redundancy in high diversity systems: resilience and ecosystem function on coral reefs. Ecol Lett 6(4):281–285. https://doi.org/10.1046/j.1461-0248.2003.00432.x
Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429(6994):827–833. https://doi.org/10.1038/nature02691
Bellwood DR, Hughes TP, Hoey AS (2006) Sleeping functional group drives coral-reef recovery. Curr Biol 16(24):2434–2439. https://doi.org/10.1016/j.cub.2006.10.030
Bender D, Diaz-Pulido G, Dove S (2014) The impact of CO2 emission scenarios and nutrient enrichment on a common coral reef macroalga is modified by temporal effects. J Phycol 50(1):203–215. https://doi.org/10.1111/jpy.12153
Bennett S, Bellwood DR (2011) Latitudinal variation in macro - algal consumption by fishes on the Great Barrier Reef. Mar Ecol Prog Ser 426:241–252
Bocher P, Robin F, Kojadinovic J, Delaporte P, Rousseau P, Dupuy C, Bustamante P (2014) Trophic resource partitioning within a shorebird community feeding on intertidal mudflat habitats. J Sea Res 92:115–124. https://doi.org/10.1016/j.seares.2014.02.011
Bonaldo RM, Krajewski JPS, C. et al (2006) Foraging activity and resource use by three parrotfish species at Fernando de Noronha Archipelago, tropical West Atlantic. Mar Biol 149:423–433. https://doi.org/10.1007/s00227-005-0233-9
Bonaldo RM, Hoey AS, Bellwood DR (2014) The ecosystem roles of parrotfishes on tropical reefs. Oceanogr Mar Biol Annu Rev 52:81–132
Box SJ, Mumby PJ (2007) Effect of macroalgal competition on growth and survival of juvenile Caribbean corals. Mar Ecol Prog Ser 342:139–149
Brasil. Decreto n° 88.218, de 6 de abril de 1983 (1983). Parque Nacional Marinho dos Abrolhos, Brasília. http://www.planalto.gov.br/ccivil_03/decreto/1980-1989/D88218.htm
Burkepile DE, Hay ME (2011) Feeding complementarity versus redundancy among herbivorous fishes on a Caribbean reef. Coral Reefs 30(2):351–362. https://doi.org/10.1007/s00338-011-0726-6
Capitani L, Roos N, Longo GO, Angelini R, Schenone L (2021) Resource-to-consumer ratio determines the functional response of an herbivorous fish in a field experiment. Oikos. https://doi.org/10.1111/oik.08784
Carassou L, Kulbicki M, Nicola TJ, Polunin NV (2008) Assessment of fish trophic status and relationships by stable isotope data in the coral reef lagoon of New Caledonia, southwest Pacific. Aquat Living Resour 21(1):1–12. https://doi.org/10.1051/alr:2008017
Carreón-Palau L, Parrish CC, del Angel-Rodríguez JA, Pérez-Espana H, Aguiñiga-García S (2013) Revealing organic carbon sources fueling a coral reef food web in the Gulf of Mexico using stable isotopes and fatty acids. Limnol Oceanogr 58(2):593–612. https://doi.org/10.4319/lo.2013.58.2.0593
Choat J, Clements K, Robbins W (2002) The trophic status of herbivorous fishes on coral reefs. Mar Biol 140(3):613–623. https://doi.org/10.1007/s00227-001-0715-3
Clements KD, German DP, Piché J, Tribollet A, Choat JH (2017) Integrating ecological roles and trophic diversification on coral reefs: multiple lines of evidence identify parrotfishes as microphages. Biol J Linn Soc 120(4):729–751. https://doi.org/10.1111/bij.12914
Clements KD, Choat JH. (2018). Nutritional ecology of parrotfishes (Scarinae, Labridae). In Biology of parrotfish. CRC Press, pp 42-68
Cline TJ, Allgeier JE (2022) Fish community structure and dynamics are insufficient to mediate coral resilience. Nat Ecol Evol 6:1700–1709. https://doi.org/10.1038/s41559-022-01882-0
Cocheret de la Morinière E, Pollux BJA, Nagelkerken I, Hemminga MA, Huiskes AHL, van der Velde G (2003) Ontogenetic dietary changes of coral reef fishes in the mangrove-seagrass-reef continuum: stable isotopes and gut-content analysis. Mar Ecol Prog Ser 246:279–289. https://doi.org/10.3354/meps246279
Colléter M, Gascuel D, Ecoutin JM, de Morais LT (2012) Modelling trophic flows in ecosystems to assess the efficiency of marine protected areas (MPA), a case study on the coast of Sénégal. Ecol Model 232:1–13. https://doi.org/10.1016/j.ecolmodel.2012.01.019
Cortés E (1999) Standardized diet compositions and trophic levels of sharks. ICES J Mar Sci 56(5):707–717. https://doi.org/10.1006/jmsc.1999.0489
Crossman DJ, Choat HJ, Clements KD, Hardy T, McConochie J (2001) Detritus as food for grazing fishes on coral reefs. Limnol Oceanogr 46(7):1596–1605. https://doi.org/10.4319/lo.2001.46.7.1596
Crossman DJ, Choat JH, Clements KD (2005) Nutritional ecology of nominally herbivorous fishes on coral reefs. Mar Ecol Prog Ser 296:129–142. https://doi.org/10.3354/meps296129
Dias T, Rosa IL, Feitoza BM (2001) Food resource and habitat sharing by the three western South Atlantic surgeonfishes (Teleostei: Acanthuridae: Acanthurus) off Paraiba Coast, northeastern Brazil. Aqua J Ichthyol Aquat Biol 5:1–10
Dromard C (2013) Niches trophiques des poissons herbivores des Antilles: apports des isotopes stables. Doctoral dissertation, Antilles-Guyane
Dromard CR, Bouchon-Navaro Y, Harmelin-Vivien M, Bouchon C (2015) Diversity of trophic niches among herbivorous fishes on a Caribbean reef (Guadeloupe, Lesser Antilles), evidenced by stable isotope and gut content analyses. J Sea Res 95:124–131. https://doi.org/10.1016/j.seares.2014.07.014
Dromard CR, Vaslet A, Gautier F, Bouchon-Navaro Y, Harmelin-Vivien M, Bouchon C (2017) Resource use by three juvenile scarids (Cryptotomus roseus, Scarus iseri, Sparisoma radians) in Caribbean seagrass beds. Aquat Bot 136:1–8. https://doi.org/10.1016/j.aquabot.2016.08.003
Dutra GF, Allen GR, Werner T, McKenna SA. (2006) A rapid marine biodiversity assessment of the Albrolhos Bank. Center for Applied Biodiversity Science (CABS), Brazil
Dutra G et al (2012) Abrolhos Bank and Vitória-Trindade Chain. Ecologically or biologically significant marine areas (EBSAs). Wider Carib West mid-Atl Reg 28:72–75
Edgar GJ, Barrett NS (1999) Effects of the declaration of marine reserves on Tasmanian reef fishes, invertebrates and plants. J Exp Mar Biol Ecol 242(1):107–144. https://doi.org/10.1016/S0022-0981(99)00098-2
Ferreira CEL, Gonçalves JEA (2006) Community structure and diet of roving herbivorous reef fishes in the Abrolhos Archipelago, south-western Atlantic. J Fish Biol 69(5):1533–1551. https://doi.org/10.1111/j.1095-8649.2006.01220.x
Ferreira CM, Nagelkerken I, Goldenberg SU, Walden G, Leung JY, Connell SD (2019) Functional loss in herbivores drives runaway expansion of weedy algae in a near-future ocean. Sci Total Environ 695:133829. https://doi.org/10.1016/j.scitotenv.2019.133829
Floeter SR et al (2008) Atlantic reef fish biogeography and evolution. J Biogeogr 35(1):22–47. https://doi.org/10.1111/j.1365-2699.2007.01790.x
Fox RJ, Bellwood DR (2008) Direct versus indirect methods of quantifying herbivore grazing impact on a coral reef. Mar Biol 154:325–334. https://doi.org/10.1007/s00227-008-0927-x
Francini-Filho RB, Moura RL, Thompson FL, Reis RM, Kaufman L, Kikuchi RK, Leão ZM (2008) Diseases leading to accelerated decline of reef corals in the largest South Atlantic reef complex (Abrolhos Bank, eastern Brazil). Mar Pollut Bull 56(5):1008–1014. https://doi.org/10.1016/j.marpolbul.2008.02.013
Francini-Filho RB, Ferreira CM, Coni EOC, De Moura RL, Kaufman L (2010) Foraging activity of roving herbivorous reef fish (Acanthuridae and Scaridae) in eastern Brazil: influence of resource availability and interference competition. J Mar Biolog Assoc U K 90(3):481–492. https://doi.org/10.1017/S0025315409991147
Francini-Filho RB, Coni EOC, Meirelles PM, Amado-Filho GM, Thompson FL, Pereira-Filho GH, Güth AZ (2013) Dynamics of coral reef benthic assemblages of the Abrolhos Bank, eastern Brazil: inferences on natural and anthropogenic drivers. PLoS ONE 8(1):e54260. https://doi.org/10.1371/journal.pone.0054260
Francini-Filho RB, Cordeiro MC, Omachi CY, Rocha AM, Bahiense L, Garcia GD, Thompson FL (2019) Remote sensing, isotopic composition and metagenomics analyses revealed Doce River ore plume reached the southern Abrolhos Bank Reefs. Sc Total Environ 697:134038. https://doi.org/10.1016/j.scitotenv.2019.134038
Frédérich B, Fabri G, Lepoint G, Vandewalle P, Parmentier E (2009) Trophic niches of thirteen damselfishes (Pomacentridae) at the Grand Récif of Toliara Madagascar. Ichthyol Res 56(1):10–17. https://doi.org/10.1007/s10228-008-0053-2
Freitas LM, Oliveira MDDM, Leão ZM, Kikuchi RKP (2019) Effects of turbidity and depth on the bioconstruction of the Abrolhos reefs. Coral Reefs 38(2):241–253. https://doi.org/10.1007/s00338-019-01770-3
Fry B (2006) Stable isotope ecology. Springer, New York, p 318
Giglio VJ, Suhett AC, Zapelini CS, Ramiro AS, Quimbayo JP (2020) Assessing captures of recreational spearfishing in Abrolhos reefs, Brazil, through social media. Reg Stud Mar Sci 34:100995. https://doi.org/10.1016/j.rsma.2019.100995Get
Gorokhova E (2018) Individual growth as a non-dietary determinant of the isotopic niche metrics. Methods Ecol Evol 9(2):269–277. https://doi.org/10.1111/2041-210X.12887
Graham NA, Wilson SK, Carr P, Hoey AS, Jennings S, MacNeil MA (2018) Seabirds enhance coral reef productivity and functioning in the absence of invasive rats. Nature 559(7713):250–253. https://doi.org/10.1038/s41586-018-0202-3
Hackradt CW, García-Charton JA, Harmelin-Vivien M, Perez-Ruzafa A, Le Direach L, Bayle-Sempere J, Valle C (2014) Response of rocky reef top predators (Serranidae: Epinephelinae) in and around marine protected areas in the Western Mediterranean Sea. PLoS ONE 9(6):e98206. https://doi.org/10.1371/journal.pone.0098206
Hackradt CW, Félix-Hackradt FC, Treviño-Otón J, Pérez-Ruzafa Á, García-Charton JA (2020) Density-driven habitat use differences across fishing zones by predator fishes (Serranidae) in south-western Mediterranean rocky reefs. Hydrobiologia 847:757–770. https://doi.org/10.1007/s10750-019-04135-7
Hadwen WL, Arthington AH (2007) Food webs of two intermittently open estuaries receiving 15N-enriched sewage effluent. Estuar Coast Shelf Sci 71(1–2):347–358. https://doi.org/10.1016/j.ecss.2006.08.017
Harris JL, Lewis LS, Smith JE (2015) Quantifying scales of spatial variability in algal turf assemblages on coral reefs. Mar Ecol Prog Ser 532:41–57. https://doi.org/10.3354/meps11344
Hawkins JP, Roberts CM (2004) Effects of artisanal fishing on Caribbean coral reefs. Conserv Biol 18(1):215–226. https://doi.org/10.1111/j.1523-1739.2004.00328.x
Hette-Tronquart N (2019) Isotopic niche is not equal to trophic niche. Ecol Lett 22(11):1987–1989. https://doi.org/10.1111/ele.13218
Ho, CT & Fu, Yi-Cheng & Sun, Chi-Lu & Kao, Shuh-JI & Jan, Rong-Quen. (2009). Plasticity of Feeding Habits of Two Plectroglyphidodon Damselfishes on Coral Reefs in Southern Taiwan: Evidence from Stomach Content and Stable Isotope Analyses. Zoological Studies. 48.
Hooper DU, Vitousek PM (1998) Effects of plant composition and diversity on nutrient cycling. Ecol Monogr 68(1):121–149. https://doi.org/10.1890/0012-9615(1998)068[0121:EOPCAD]2.0.CO;2
Hughes TP et al (2007) Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr Biol 17(4):360–365. https://doi.org/10.1016/j.cub.2006.12.049
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
Ives AR, Carpenter SR (2007) Stability and diversity of ecosystems. Science 317:58–62
Jackson A, Inger R, Parnell A, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER – Stable Isotope Bayesian Ellipses in R. J Anim Ecol 80:595–602
Johansson CL, Van De Leemput IA, Depczynski M, Hoey AS, Bellwood DR (2013) Key herbivores reveal limited functional redundancy on inshore coral reefs. Coral Reefs 32(4):963–972. https://doi.org/10.1007/s00338-013-1044-y
Kelly JR, Scheibling RE (2012) Fatty acids as dietary tracers in benthic food webs. Mar Ecol Prog Ser 446:1–22. https://doi.org/10.3354/meps09559
Kindsvater HK, Palkovacs EP (2017) Predicting eco-evolutionary impacts of fishing on body size and trophic role of Atlantic cod. Copeia 105(3):475–482. https://doi.org/10.1643/OT-16-533
Lamb K, Swart PK, Altabet MA (2012) Nitrogen and carbon isotopic systematics of the Florida reef tract. Bull Mar Sci 88(1):119–146. https://doi.org/10.5343/bms.2010.1105
Lau DC, Leung KM, Dudgeon D (2009) What does stable isotope analysis reveal about trophic relationships and the relative importance of allochthonous and autochthonous resources in tropical streams? A synthetic study from Hong Kong. Freshw Biol 54(1):127–141
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
Layman CA, Arrington DA, Montaña CG, Post DM (2007) Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88(1):42–48. https://doi.org/10.1890/0012-9658(2007)88[42:CSIRPF]2.0.CO;2
Leão ZMAN, Kikuchi RKP (2001) The Abrolhos Reefs of Brazil. In: Seeliger U, Kjerfve B (eds) Coastal Marine Ecosystems of Latin America. Ecological Studies, Springer, Berlin, Heidelberg, pp 83–96. https://doi.org/10.1007/978-3-662-04482-7_7
Lellys NT, De Moura RL, Bonaldo RM, Francini-Filho RB, Gibran FZ (2019) Parrotfish functional morphology and bioerosion on SW Atlantic reefs. Mar Ecol Prog Ser 629:149–163. https://doi.org/10.3354/meps13102
Linhares BDA, Bugoni L (2022) Seabirds subsidize terrestrial food webs and coral reefs in a tropical rat-invaded archipelago. Ecol Appl. https://doi.org/10.1002/eap.2733
Littler MM, Littler DS. (1984). Models of tropical reef biogenesis: the contribution of algae. Progress in phycological research.
Mantyka CS, Bellwood DR (2007) Macroalgal grazing selectivity among herbivorous coral reef fishes. Mar Ecol Prog Ser 352:177–185. https://doi.org/10.3354/meps07055
Matich P, Shipley ON, Weideli OC (2021) Quantifying spatial variation in isotopic baselines reveals size-based feeding in a model estuarine predator: implications for trophic studies in dynamic ecotones. Mar Biol 168:108. https://doi.org/10.1007/s00227-021-03920-0
McClelland JW, Valiela I, Michener RH (1997) Nitrogen-stable isotope signatures in estuarine food webs: A record of increasing urbanization in coastal watersheds. Limnol Oceanogr 42(5):930–937. https://doi.org/10.4319/lo.1997.42.5.0930
McCullagh, P., & Nelder, J. A. (1989). Binary data. In Generalized linear models (pp. 98–148). Springer US.
Mendes TC, Ferreira CEL, Clements KD (2018) Discordance between diet analysis and dietary macronutrient content in four nominally herbivorous fishes from the Southwestern Atlantic. Mar Biol 165(11):180. https://doi.org/10.1007/s00227-018-3438-4
Michael PJ, Hyndes GA, Vanderklift MA, Vergés A (2013) Identity and behaviour of herbivorous fish influence large-scale spatial patterns of macroalgal herbivory in a coral reef. Mar Ecol Prog Ser 482:227–240. https://doi.org/10.3354/meps10262
Minte-Vera CV, De Moura RL, Francini-Filho RB (2008) Nested sampling: an improved visual-census technique for studying reef fish assemblages. Mar Ecol Prog Ser 367:283–293. https://doi.org/10.3354/meps07511
Moura RL, Secchin NA, Amado-Filho GM, Francini-Filho RB, Freitas MO, Minte-Vera CV, Bastos AC (2013) Spatial patterns of benthic mega habitats and conservation planning in the Abrolhos Bank. Cont Shelf Res 70:109–117. https://doi.org/10.1016/j.csr.2013.04.036
Nagelkerken I, Van der Velde G, Wartenbergh SLJ, Nugues MM, Pratchett MS (2009) Cryptic dietary components reduce dietary overlap among sympatric butterflyfishes (Chaetodontidae). J Fish Biol 75(6):1123–1143. https://doi.org/10.1111/j.1095-8649.2009.02303.x
Nicholls AO (1989) How to make biological surveys go further with generalised linear models. Biol Cons 50(1–4):51–75. https://doi.org/10.1016/0006-3207(89)90005-0
Olson AM, Trebilco R, Salomon AK (2019) Expanded consumer niche widths may signal an early response to spatial protection. PLoS ONE 14(10):e0223748. https://doi.org/10.1371/journal.pone.0223748
Petta JC, Shipley ON, Wintner SP et al (2020) Are you really what you eat? Stomach content analysis and stable isotope ratios do not uniformly estimate dietary niche characteristics in three marine predators. Oecologia 192:1111–1126. https://doi.org/10.1007/s00442-020-04628-6
Plass-Johnson JG, McQuaid CD, Hill JM (2013) Stable isotope analysis indicates a lack of inter-and intra-specific dietary redundancy among ecologically important coral reef fishes. Coral Reefs 32(2):429–440. https://doi.org/10.1007/s00338-012-0988-7
Plass-Johnson JG, McQuaid CD, Hill JM (2015) The effects of tissue type and body size on δ13C and δ15N values in parrotfish (Labridae) from Zanzibar. Tanzania J Appl Ichthyol 31(4):633–637. https://doi.org/10.1111/jai.12746
Post DM, Layman CA, Arrington DA et al (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179–189. https://doi.org/10.1007/s00442-006-0630-x
Previeiro M, Gasalla MA (2018) Mapping fishing grounds, resource and fleet patterns to enhance management units in data-poor fisheries: The case of snappers and groupers in the Abrolhos Bank coral-reefs (South Atlantic). Ocean Coast Manag 154:83–95. https://doi.org/10.1016/j.ocecoaman.2018.01.007
Previeiro M. (2014). A pesca do budião-azul (Scarus trispinosus Valenciennes, 1840) no maior complexo coralíneo do Atlântico Sul. Dissertation, State University of Maringá.
R Core Team. (2017). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
Riegl B, Bruckner A, Coles SL, Renaud P, Dodge RE (2009) Coral reefs: threats and conservation in an era of global change. Ann N Y Acad Sci 1162(1):136–186. https://doi.org/10.1111/j.1749-6632.2009.04493.x
Roos NC, Pennino MG, de Macedo Lopes PF, Carvalho AR (2016) Multiple management strategies to control selectivity on parrotfishes harvesting. Ocean Coast Manag 134:20–29. https://doi.org/10.1016/j.ocecoaman.2016.09.029
Ross NC, Longo GO, Pennino MG, Francini-Filho RB, Carvalho AR (2020) Protecting nursery areas without fisheries management is not enough to conserve the most endangered parrotfish of the Atlantic Ocean. Sci Rep 10(1):1–10. https://doi.org/10.1038/s41598-020-76207-x
Russ GR (2003) Grazer biomass correlates more strongly with production than with biomass of algal turfs on a coral reef. Coral Reefs 22(1):63–67. https://doi.org/10.1007/s00338-003-0286-5
Semmler RF, Brandl SJ, Keith SA, Bellwood DR (2021) Fine-scale foraging behavior reveals differences in the functional roles of herbivorous reef fishes. Ecol Evol 11(9):4898–4908. https://doi.org/10.1002/ece3.7398
Seytre C, Francour P (2013) A long-term survey of Posidonia oceanica fish assemblages in a Mediterranean Marine Protected Area: emphasis on stability and no-take area effectiveness. Mar Freshw Res 65(3):244–254. https://doi.org/10.1071/MF13080
Shipley ON et al (2017) Polar compounds preclude mathematical lipid correction of carbon stable isotopes in deep-water sharks. J Exp Mar Biol Ecol 494:69–74. https://doi.org/10.1016/j.jembe.2017.05.002
Sinopoli M, Fanelli E, D’Anna G, Badalamenti F, Pipitone C (2012) Assessing the effects of a trawling ban on diet and trophic level of hake, Merluccius merluccius, in the southern Tyrrhenian Sea. Sci Mar 76:677–690
Smith KM, Quirk-Royal BE, Drake-Lavelle K, Childress MJ (2018) Influences of ontogenetic phase and resource availability on parrotfish foraging preferences in the Florida Keys, FL (USA). Mar Ecol Prog Ser 603:175–187. https://doi.org/10.3354/meps12718
Soler GA, Edgar GJ, Thomson RJ, Kininmonth S, Campbell SJ, Dawson TP, Stuart-Smith RD (2015) Reef fishes at all trophic levels respond positively to effective marine protected areas. PLoS ONE 10(10):e0140270. https://doi.org/10.1371/journal.pone.0140270
Steneck RS, Dethier MN (1994) A functional group approach to the structure of algal-dominated communities. Oikos 69(3):476–498
Steneck RS, Arnold SN, Mumby PJ (2014) Experiment mimics fishing on parrotfish: insights on coral reef recovery and alternative attractors. Mar Ecol Prog Ser 506:115–127. https://doi.org/10.3354/meps10764
Streit RP, Cumming GS, Bellwood DR (2019) Patchy delivery of functions undermines functional redundancy in a high diversity system. Funct Ecol 33(6):1144–1155. https://doi.org/10.1111/1365-2435.13322
Tebbett SB, Siqueira AC, Bellwood DR (2022) The functional roles of surgeonfishes on coral reefs: past, present and future. Rev Fish Biol Fisheries 32:387–439. https://doi.org/10.1007/s11160-021-09692-6
Tietbohl M (2016) Assessing the functional diversity of herbivorous reef fishes using a compound-specific stable isotope approach. KAUST Res Rep. https://doi.org/10.2578/KAUST-9S3HX
Turner TF, Collyer ML, Krabbenhoft TJ (2010) A general hypothesis-testing framework for stable isotope ratios in ecological studies. Ecology 91(8):2227–2233. https://doi.org/10.1890/09-1454.1
Vanderklift MA (2003) Ponsard, S. Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136:169–182. https://doi.org/10.1007/s00442-003-1270-z
Vergés A, Bennett S, Bellwood DR. (2012). Diversity among macroalgae-consuming fishes in coral reefs: a transcontinental comparison. PLoS ONE 7: e45543 https://doi.org/10.1371/journal.pone.0045543
Veron JE et al (2009) The coral reef crisis: The critical importance of< 350 ppm CO2. Mar Pollut Bull 58(10):1428–1436. https://doi.org/10.1016/j.marpolbul.2009.09.009
Whiteman JP, Elliott Smith EA, Besser AC, Newsome SD (2019) A Guide to Using Compound-Specific Stable Isotope Analysis to Study the Fates of Molecules in Organisms and Ecosystems. Diversity 11(1):8. https://doi.org/10.3390/d11010008
Wilson SK, Bellwood DR, Choat JH, Furnas MJ (2003) Detritus in the epilithic algal matrix and its use by coral reef fishes. Oceanogr Mar Biol 41:279–310
Wolfe K, Anthony K, Babcock RC, Bay L, Bourne DG, Burrows D, Mumby PJ (2020) Priority species to support the functional integrity of coral reefs. In: Oceanography and marine biology. Taylor & Francis. https://doi.org/10.1201/9780429351495-5
Wyatt AS, Waite AM, Humphries S (2012) Stable isotope analysis reveals community-level variation in fish trophodynamics across a fringing coral reef. Coral Reefs 31(4):1029–1044. https://doi.org/10.1007/s00338-012-0923-y
Yoneshigue-Valentin Y, Valentin JL. (1992). Macroalgae of the Cabo Frio upwelling region, Brazil: ordination of communities. In Coastal plant communities of Latin America. Academic Press, pp 31–50.
Acknowledgements
We would like to thank Budiões Project and its sponsor Petrobras. We also tanks R. Herández-Andreu and J.A. Nunes for field assistance in sample collection. We thank the reviewers for their contributions.
Funding
This work was supported in part by the Projeto Budiões, funded by Petrobras (Programa Petrobras Socioambiental).
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MLCL, CWH, JCB and FCFH conceived the original idea and were involved in supervised the project. MLCL and JCB contributed to sample preparation. CWH, JCB and FCFH verified the analytical methods. MLCL processed the experimental data, performed the analysis, drafted the manuscript and designed the figures with support from ILS, JCB and FCFH. All authors discussed the results and contributed to the final manuscript.
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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. Field protocols were approved by Brazilian legislation (ICMBio-MMA—Ministry of the Environment) and the sampling was carried out using observational and non-destructive techniques, under license SISBIO-11709–1.
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Leitão, M., Hackradt, C.W., Silva, Í.L.e. et al. Effect of human impact on coral reef herbivorous fish niche. Mar Biol 170, 59 (2023). https://doi.org/10.1007/s00227-023-04199-z
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DOI: https://doi.org/10.1007/s00227-023-04199-z