DOI: https://doi.org/10.3354/meps15012
copiedGeographic variation in the nutritional ecology of nominally herbivorous fishes in the southwestern Atlantic Ocean
- G. C. Cardozo-Ferreira
- K. D. Clements
- J. H. Choat
- T. C. Mendes
- R. M. Macieira
- C. E. Rezende
- J.-C. Joyeux
- C. E. L. Ferreira
Spatial and temporal niche partitioning are the basis for the coexistence of species. Determining niche partitioning among species over broad geographical scales requires multiple approaches, as local environmental features may vary spatially. We analysed the trophic ecology of 3 nominally herbivorous fishes—the doctorfish Acanthurus chirurgus, the grey parrotfish Sparisoma axillare, and the brassy chub Kyphosus vaigiensis—to identify the drivers of variation in resource use at different locations along the Brazilian coast: Natal, Abrolhos Archipelago, and Arraial do Cabo. We used 2 complementary approaches—dietary (at 2 scales of magnification) and stable isotope analyses (SIA)—to investigate variation in the nutritional ecology of the study species. We observed interspecific dietary variation at each location. Doctorfish showed the highest dietary variability, with significant contributions from diatoms and cyanobacteria; grey parrotfish mainly ingested detritus, cyanobacteria, and green filamentous algae, while brassy chub mainly ingested brown algae but with some supplementation from red and green macroalgae. Interspecific isotopic niche overlap varied among locations following variation in the isotopic niche width of species. Trophic positions (TP) varied unexpectedly, with grey parrotfish displaying a relatively higher TP in one location and the lowest in the others. The use of complementary approaches, providing short- and comparatively long-term information (diet and SIA, respectively), and a detailed description of dietary items are essential to understand niche and resource partitioning when studying the nutritional ecology of nominally herbivorous fishes.
KEYWORDS
Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: Guide to software and statistical methods. PRIMER-E, Plymouth
Andrades R, Jackson AL, Macieira RM, Reis-Filho JA, Bernardino AF, Joyeux J, Giarrizzo T (2019) Niche-related processes in island intertidal communities inferred from stable isotopes data. Ecol Indic 104:648-658 Crossref
Andrades R, Joyeux J, Macieira RM, Godoy BS, Reis-Filho JA, Jackson AL, Giarrizzo T (2021) Niche-relationships within and among intertidal reef fish species. Front Mar Sci 8:659579 Crossref
Aued AW, Smith F, Quimbayo JP, Cândido DV and others (2018) Large-scale patterns of benthic marine communities in the Brazilian Province. PLOS ONE 13:e0198452 Crossref
Behrens MD, Lafferty KD (2012) Geographic variation in the diet of opaleye (Girella nigricans) with respect to temperature and habitat. PLOS ONE 7:e45901 Crossref
Bellwood DR, Tebbett SB (2024) Habitat trumps biogeography in structuring coral reef fishes. Coral Reefs 43:1599-1609 Crossref
Bode A, Lamas AF, Mompeán C (2020) Effects of upwelling intensity on nitrogen and carbon fluxes through the planktonic food web off A Coruña (Galicia, NW Spain) assessed with stable isotopes. Diversity 12:121 Crossref
Bouillon S, Koedam N, Raman AV, Dehairs F (2002) Primary producers sustaining macro-invertebrate communities in intertidal mangrove forests. Oecologia 130:441-448 Crossref
Bringloe TT, Starko S, Wade RM, Vieira C and others (2020) Phylogeny and evolution of the brown algae. Crit Rev Plant Sci 39:281-321 Crossref
Burkepile DE, Adam TC, Roycroft M, Ladd MC, Munsterman KS, Ruttenberg BI (2019) Species-specific patterns in corallivory and spongivory among Caribbean parrotfishes. Coral Reefs 38:417-423 Crossref
Carassou L, Léopold M, Guillemot N, Wantiez L, Kulbicki M (2013) Does herbivorous fish protection really improve coral reef resilience? A case study from New Caledonia (South Pacific). PLOS ONE 8:e60564 Crossref
Cardozo-Ferreira GC, Macieira RM, Francini-Filho RB, Joyeux JC (2018) Inferring labrid functional roles through morphological and ecological traits. Mar Ecol Prog Ser 588:135-145 Crossref
Cardozo-Ferreira GC, Calazans TL, Benevides LJ, Luiz OJ, Ferreira CEL, Joyeux JC (2021) Ecological traits influencing anthropogenic debris ingestion by herbivorous reef fishes. Front Mar Sci 8:717435 Crossref
Cardozo-Ferreira GC, Ferreira CEL, Choat JH, Mendes TC and others (2023) Seasonal variation in diet and isotopic niche of nominally herbivorous fishes in subtropical rocky reefs. Mar Ecol Prog Ser 722:125-143 Crossref
Caut S, Angulo E, Courchamp F (2009) Variation in discrimination factors (D15N and D13C): the effect of diet isotopic values and applications for diet reconstruction. J Appl Ecol 46:443-453 Crossref
Choat JH, Clements KD (1992) Diet in odacid and aplodactylid fishes from Australia and New Zealand. Aust J Mar Freshwater Res 43:1451-1459 Crossref
Choat JH, Clements KD (1998) Vertebrate herbivores in marine and terrestrial environments: a nutritional ecology perspective. Annu Rev Ecol Evol Syst 29:375-403 Crossref
Choat JH, Clements KD, Robbins WD (2002) The trophic status of herbivorous fishes on coral reefs. 1: Dietary analyses. Mar Biol 140:613-623 Crossref
Choat JH, Robbins WD, Clements KD (2004) The trophic status of herbivorous fishes on coral reefs: II. Food processing modes and trophodynamics. Mar Biol 145:445-454 Crossref
Choi SW, Graf L, Choi JW, Jo J and others (2024) Ordovician origin and subsequent diversification of the brown algae. Curr Biol 34:740-754.e4 Crossref
Clarke KR, Warwick RM (1994) Similarity-based testing for community pattern: the two-way layout with no replication. Mar Biol 118:167-176 Crossref
Clements KD, Choat JH (1995) Fermentation in tropical marine herbivorous fishes. Physiol Zool 68:355-378 Crossref
Clements KD, Choat JH (1997) Comparison of herbivory in the closely-related marine fish genera Girella and Kyphosus. Mar Biol 127:579-586 Crossref
Clements KD, Choat JH (2018) Nutritional ecology of parrotfishes (Scarinae, Labridae). In: Hoey AS, Bonaldo RM (eds) Biology of Parrotfishes. CRC Press, Boca Raton, FL, p 42-68
Clements KD, Raubenheimer D, Choat JH (2009) Nutritional ecology of marine herbivorous fishes: ten years on. Funct Ecol 23:79-92 Crossref
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 120:729-751
Crossman DJ, Choat JH, Clements KD, Hardy T, McConochie J (2001) Detritus as food for grazing fishes on coral reefs. Limnol Oceanogr 46:1596-1605 Crossref
Cvitanovic C, Hoey AS (2010) Benthic community composition influences within-habitat variation in macroalgal browsing on the Great Barrier Reef. Mar Freshw Res 61:999-1005 Crossref
de Goeij JM, van Oevelen D, Vermeij MJA, Osinga R, Middelburg JJ, de Goeij AFPM, Admiraal W (2013) Surviving in a marine desert: the sponge loop retains resources within coral reefs. Science 342:108-110 Crossref
Docmac F, Araya M, Hinojosa IA, Dorador C, Harrod C (2017) Habitat coupling writ large: pelagic-derived materials fuel benthivorous macroalgal reef fishes in an upwelling zone. Ecology 98:2267-2272 Crossref
Dromard CR, Bouchon-Navaro Y, Harmelin-Vivien ML, 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 Crossref
Eurich JG, Matley JK, Baker R, McCormick MI, Jones GP (2019) Stable isotope analysis reveals trophic diversity and partitioning in territorial damselfishes on a low-latitude coral reef. Mar Biol 166:17 Crossref
Ferreira CEL, Peret AC, Coutinho R (1998) Seasonal grazing rates and food processing by tropical herbivorous fishes. J Fish Biol 53:222-235
Ferreira CEL, Floeter SR, Gasparini JL, Ferreira BP, Joyeux J (2004) Trophic structure patterns of Brazilian reef fishes: a latitudinal comparison. J Biogeogr 31:1093-1106 Crossref
Floeter SR, Ferreira CEL, Dominici-Arosemena A, Zalmon IR (2004) Latitudinal gradients in Atlantic reef fish communities: trophic structure and spatial use patterns. J Fish Biol 64:1680-1699 Crossref
Floeter SR, Behrens MD, Ferreira CEL, Paddack MJ, Horn MH (2005) Geographical gradients of marine herbivorous fishes: patterns and processes. Mar Biol 147:1435-1447 Crossref
Francini-Filho RB, Ferreira CM, Coni EOC, De Moura RLL, 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 Biol Assoc UK 90:481-492 Crossref
Francini-Filho RB, Coni EOC, Meirelles PM, Amado-Filho GM and others (2013) Dynamics of coral reef benthic assemblages of the Abrolhos Bank, eastern Brazil: inferences on natural and anthropogenic drivers. PLOS ONE 8:e54260 Crossref
Fry BG (2002) Stable isotopic indicators of habitat use by Mississippi River fish. J N Am Benthol Soc 21:676-685 Crossref
Fry BG (2006) Stable isotope ecology. Springer, New York, NY
Gaines SD, Lubchenco J (1982) A unified approach to marine plant-herbivore interactions. II. Biogeography. Annu Rev Ecol Evol Syst 13:111-138 Crossref
Goecker ME, Heck KL Jr, Valentine JF (2005) Effects of nitrogen concentrations in turtlegrass Thalassia testudinum on consumption by the bucktooth parrotfish Sparisoma radians. Mar Ecol Prog Ser 286:239-248 Crossref
Gu Z, Gu L, Eils R, Schlesner M, Brors B (2014) circlize implements and enhances circular visualization in R. Bioinformatics 30:2811-2812 Crossref
Hardison EA, Eliason EJ (2024) Diet effects on ectotherm thermal performance. Biol Rev Camb Philos Soc 99:1537-1555 Crossref
Horn MH (1989) Biology of marine herbivorous fishes. Oceanogr Mar Biol Annu Rev 27:167-272
Hudspith M, de Goeij JM, Streekstra M, Kornder NA and others (2022) Harnessing solar power: photoautotrophy supplements the diet of a low-light dwelling sponge. ISME J 16:2076-2086 Crossref
Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER—Stable Isotope Bayesian Ellipses in R. J Anim Ecol 80:595-602 Crossref
Johnson JS, Raubenheimer D, Bury SJ, Clements KD (2020) Does temperature constrain diet choice in a marine herbivorous fish? Mar Biol 167:99 Crossref
Kartzinel TR, Chen PA, Coverdale TC, Erickson DL and others (2015) DNA metabarcoding illuminates dietary niche partitioning by African large herbivores. Proc Natl Acad Sci USA 112:8019-8024 Crossref
Knudsen SW, Choat JH, Clements KD (2019) The herbivorous fish family Kyphosidae (Teleostei: Perciformes) represents a recent radiation from higher latitudes. J Biogeogr 46:2067-2080 Crossref
Kroon D, Ganssen G (1989) Northern Indian Ocean upwelling cells and the stable isotope composition of living planktonic foraminifers. Deep-Sea Res A, Oceanogr Res Pap 36:1219-1236 Crossref
Lapointe BE, Barile PJ, Littler MM, Littler DS (2005) Macroalgal blooms on southeast Florida coral reefs: II. Cross-shelf discrimination of nitrogen sources indicates widespread assimilation of sewage nitrogen. Harmful Algae 4:1106-1122 Crossref
Longo GO, Hay ME, Ferreira CEL, Floeter SR (2019) Trophic interactions across 61 degrees of latitude in the Western Atlantic. Glob Ecol Biogeogr 28:107-117 Crossref
Lorrain A, Graham BS, Popp BN, Allain V and others (2015) Nitrogen isotopic baselines and implications for estimating foraging habitat and trophic position of yellowfin tuna in the Indian and Pacific Oceans. Deep See Res II 113:188-198 Crossref
Madigan DJ, Litvin SY, Popp BN, Carlisle AB, Farwell CJ, Block BA (2012) Tissue turnover rates and isotopic trophic discrimination factors in the endothermic Teleost, Pacific bluefin tuna (Thunnus orientalis). PLOS ONE 7:e49220 Crossref
Magaña-Gallegos E, Villegas-Muñoz E, Salas-Acosta ER, Barba-Santos MG, Silva R, van Tussenbroek BI (2023) The effect of temperature on the growth of holopelagic Sargassum species. Phycology 3:138-146 Crossref
McMurray SE, Stubler AD, Erwin PM, Finelli CM, Pawlik JR (2018) A test of the sponge-loop hypothesis for emergent Caribbean reef sponges. Mar Ecol Prog Ser 588:1-14 Crossref
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 165:180 Link
Mountfort DO, Campbell J, Clements KD (2002) Hindgut fermentation in three species of marine herbivorous fish. Appl Environ Microbiol 68:1374-1380 Crossref
Ng JSS, Wai TC, Williams GA (2007) The effects of acidification on the stable isotope signatures of marine algae and molluscs. Mar Chem 103:97-102 Crossref
Nicholson GM, Clements KD (2020) Resolving resource partitioning in parrotfishes (Scarini) using microhistology of feeding substrata. Coral Reefs 39:1313-1327 Crossref
Nicholson GM, Clements KD (2023) Fine-scale analysis of substrata grazed by parrotfishes (Labridae: Scarini) on the outer-shelf of the Great Barrier Reef, Australia. Mar Biol 170:121 Link
Nicholson GM, Clements KD (2023) Micro-photoautotroph predation as a driver for trophic niche specialization in 12 syntopic Indo-Pacific parrotfish species. Biol J Linn Soc 139:91-114 Crossref
Nicholson GM, Clements KD (2024) A role for encrusting, endolithic sponges in the feeding of the parrotfish Scarus rubroviolaceus? Evidence of further trophic diversification in Indo-Pacific Scarini. Coral Reefs 43:541-556 Crossref
Ogle DH, Wheeler P, Dinno A (2019) FSA: fisheries stock analysis. R package version 0.8.26. Link
Pereira PHC, Santos M, Lippi DL, Silva P (2016) Ontogenetic foraging activity and feeding selectivity of the Brazilian endemic parrotfish Scarus zelindae. PeerJ 4:e2536 Crossref
Pires-Teixeira LM, Neres-Lima V, Creed JC (2021) Is acidification of samples for isotopic analysis of carbon and nitrogen necessary for shoreline marine species? Mar Freshw Res 72:256-262 Crossref
Pisaniello A, Bojarski LD, Handley KM, White WL, Angert ER, Clements KD (2022) Sources of variation in community composition of the hindgut microbiota in two tropical Kyphosus species. Coral Reefs 41:1523-1535 Crossref
Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montaña CG (2007) Getting to the fat of the matter: Models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179-189 Crossref
Quezada-Romegialli C, Jackson AL, Hayden B, Kahilainen KK, Lopes C, Harrod C (2018) tRophicPosition, an R package for the Bayesian estimation of trophic position from consumer stable isotope ratios. Methods Ecol Evol 9:1592-1599 Crossref
R Core Team (2024) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Radice VZ, Hoegh-Guldberg O, Fry BG, Fox MD, Dove SG (2019) Upwelling as the major source of nitrogen for shallow and deep reef-building corals across an oceanic atoll system. Funct Ecol 33:1120-1134 Crossref
Sammarco PW, Risk MJ, Schwarcz HP, Heikoop JM (1999) Cross-continental shelf trends in coral d15N on the Great Barrier Reef: further consideration of the reef nutrient paradox. Mar Ecol Prog Ser 180:131-138 Crossref
Solomon CT, Carpenter SR, Rusak JA, Vander Zanden MJ (2008) Long-term variation in isotopic baselines and implications for estimating consumer trophic niches. Can J Fish Aquat Sci 65:2191-2200 Crossref
Stevenson SJR, Lee KC, Handley KM, Angert ER, White WL, Clements KD (2022) Substrate degradation pathways, conserved functions and community composition of the hindgut microbiota in the herbivorous marine fish Kyphosus sydneyanus. Comp Biochem Physiol A Mol Integr Physiol 272:111283 Crossref
Thompson C, Silva R, Gibran FZ, Bacha L and others (2024) The Abrolhos nominally herbivorous coral reef fish Acanthurus chirurgus, Kyphosus sp., Scarus trispinosus, and Sparisoma axillare have similarities in feeding but species-specific microbiomes. Microb Ecol 87:110 Crossref
Underwood GJC (2001) Microphytobenthos. In: Steele JH, Thorpe SA, Turekian KK (eds) Encyclopedia of ocean sciences. Elsevier, Amsterdam, p 1770-1777
Vuorio K, Meili M, Sarvala J (2006) Taxon-specific variation in the stable isotopic signatures (d13C and d15N) of lake phytoplankton. Freshw Biol 51:807-822 Crossref
Wickham H (2016) Ggplot2: elegant graphics for data analysis. Springer-Verlag, New York, NY
Wilkinson CR, Fay P (1979) Nitrogen fixation in coral reef sponges with symbiotic cyanobacteria. Nature 279:527-529 Crossref
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 Annu Rev 41:279-309
Wulff JL (2021) Targeted predator defenses of sponges shape community organization and tropical marine ecosystem function. Ecol Monogr 91:e01438 Crossref
Zhu Y, Newman SP, Reid WDK, Polunin NVC (2019) Fish stable isotope community structure of a Bahamian coral reef. Mar Biol 166:160 Crossref
G. C. Cardozo-Ferreira (Corresponding Author)
- Reef Systems Ecology and Conservation Lab, Department of Marine Biology, Universidade Federal Fluminense,Niterói, RJ 24220-900, Brazil
- Laboratory of Ichthyology, Department of Oceanography, Universidade Federal do Espírito Santo, Vitória, ES 29075-910, Brazil
K. D. Clements (Co-author)
- School of Biological Sciences, University of Auckland, Auckland 09-373 79, New Zealand
J. H. Choat (Co-author)
- College of Science and Engineering, James Cook University, Townsville, QLD 4814, Australia
- Reef Systems Ecology and Conservation Lab, Department of Marine Biology, Universidade Federal Fluminense,Niterói, RJ 24220-900, Brazil
- Laboratory of Ichthyology, Department of Oceanography, Universidade Federal do Espírito Santo, Vitória, ES 29075-910, Brazil
C. E. Rezende (Co-author)
- Research Group on Biogeochemistry of Aquatic Ecosystems, Centre for Bioscience and Biotechnology, Environmental Sciences Laboratory, Universidade Estadual do Norte Fluminense Darcy Ribeiro,Campos dos Goytacazes, RJ 28.015-622, Brazil
J.-C. Joyeux (Co-author)
- Laboratory of Ichthyology, Department of Oceanography, Universidade Federal do Espírito Santo, Vitória, ES 29075-910, Brazil
- Reef Systems Ecology and Conservation Lab, Department of Marine Biology, Universidade Federal Fluminense,Niterói, RJ 24220-900, Brazil
Handling Editor:
Antonio Bode, A Coruña, Spain
Reviewers:
3 anonymous referees
Acknowledgements:
We thank L. Benevides, R. Andrades, A. Bernardino, V. Giglio, and R. Francini-Filho for their valuable comments on the manuscript, and to L. Benevides, L. Eggertsen, R. Bonaldo, R. Freitas, T. Calazans, N. Roos, C. Pimentel, J. Gonçalves, J. Gasparini, and G. Longo for their help with field and lab work. This project was funded by the Brazilian National Council for Scientific and Technological Development (CNPq 401908/2013-5) and Rio de Janeiro State Foundation for Support to Research (FAPERJ E-26/111.168/2014 and E-26/200.638/2016) grants to C.E.L.F., and to T.C.M. (E-26/202.372/2021). G.C.C.-F. had financial support from FAPERJ (E-26/201.026/2022), FAPES (Foundation for Research and Innovation Support of Espírito Santo) (292/2015-70223165/15), and CNPq (208399/2017-8). This research was conducted under the Brazilian Environmental Agency collection permit (SISBIO #48112). C.E.L.F. is supported by CNPq (310219/2023-0) and FAPERJ (E-26/201.026/2022) productivity research grants.
