ISÓTOPOS ESTÁVEIS E OUTRAS FERRAMENTAS EM ESTUDOS TRÓFICOS DE PEIXES EM RIACHOS TROPICAIS

Míriam Pilz Albrecht, Andressa da Silva Reis, Vinícius Neres-Lima, Eugenia Zandonà

Abstract


A análise de isótopos estáveis (AIE) se tornou uma ferramenta essencial na Ecologia, sendo cada vez mais utilizada em estudos de peixes de riachos tropicais. A AIE permite reconstruir a dieta dos animais e suas variações intraespecíficas, traçar as contribuições dos principais recursos basais que sustentam as teias tróficas, calcular a posição trófica e o nicho trófico, incluindo partilha e alterações de nicho, e construir teias tróficas. A AIE é amplamente utilizada também para entender o impacto de alterações ambientais nas comunidades de peixes e de outros organismos aquáticos. O número de estudos é crescente no Brasil, porém ainda há diversas lacunas. Neste artigo, apresentamos conceitos básicos sobre a análise de isótopos estáveis em estudos tróficos de peixes de riacho, especialmente de carbono, nitrogênio e hidrogênio, suas premissas, usos e limitações, permeando com exemplos em riachos tropicais. Exploramos também novas fronteiras para estudos nessa área, ainda não utilizadas para peixes de riacho no Brasil, como análise de ácidos graxos, análise de isótopos estáveis em compostos específicos, geometria nutricional e conceitos da estequiometria ecológica tais como o Limiar de Proporções de Elementos.    

STABLE ISOTOPES AND OTHER TOOLS IN TROPHIC STUDIES OF TROPICAL STREAM FISH: Stable isotope analysis (SIA) has become an essential tool in Ecology, being increasingly used in studies of fish in tropical streams. The SIA allows to reconstruct the animals' diet and its intraspecific variation, to trace the contributions of the main basal resources throughout the food web, to calculate trophic position and trophic niche, including niche overlap and its alterations, and to build food webs. The SIA is also used to understand the impact of environmental changes on fish communities and other aquatic organisms. The number of such studies is increasing in Brazil, but there are still several gaps. In this study, we present the basic concepts on stable isotopes analysis in trophic studies of stream fish - especially those of carbon, nitrogen and hydrogen - their premises, uses and limitations, presenting examples from tropical streams. We also explore new conceptual tools in this area, still not used for stream fish in Brazil, such as fatty acids, stable isotopes in specific compounds, nutritional geometry and ecological stoichiometry concepts such as the Threshold Elemental Ratio.

Keywords


resources assimilation; energy flow; isotopic niche; trophic position; fatty acids

References


Anjos, M. B. 2013. Fontes autotróficas de energia para a ictiofauna de riachos de floresta de terra firme pertencentes à bacia de drenagem do rio Preto da Eva, Amazonas, Brasil. Tese de Doutorado. INPA/PPG-BADPI. p. 87.

Bastos, R. F., Corrêa, F., Winemiller, K. O., & Garcia, A. M. 2017. Are you what you eat? Effects of trophic discrimination factors on estimates of food assimilation and trophic position with a new estimation method. Ecological Indicators, 75, 234–241. DOI:10.1016/j.ecolind.2016.12.007

Bearhop, S., Adams, C. E., Waldron, S., Fuller, R. A., & Macleod, H. 2004. Determining trophic niche width: A novel approach using stable isotope analysis. Journal of Animal Ecology, 73(5), 1007–1012. DOI:10.1111/j.0021-8790.2004.00861.x

Boecklen, W. J. 2011. Use of stable isotopes in foraging ecology and food web analysis. Annual Review of Ecology, Evolution, and Systematics, 42, 411–440. DOI:10.1146/annurev-ecolsys-102209-144726

Boëchat, I.G., Krüger, A., Giani, A., Figueredo, C.C., & Gücker, B. 2011. Agricultural land-use affects the nutritional quality of stream microbial communities. FEMS Microbiology Ecology 77(3), 568–576. DOI:10.1111/j.1574-6941.2011.01137.x

Bonato, K. O., Burress, E. D., Fialho, C. B., & Armbruster, J. W. 2018. Resource partitioning among syntopic Characidae corroborated by gut content and stable isotope analyses. Hydrobiologia, 805, 311–324. DOI:10.1007/s10750-017-3314-0

Brett, M. T., Bunn, S. E., Chandra, S., Galloway, A. W. E., Guo, F., Kainz, M. J., Kankaala, P., Lau, D. C. P., Moulton, T. P., Power, M. E., Rasmussen, J. B., Taipale, S. J., Thorp, J. H., & Wehr, J. D. 2017. How important are terrestrial organic carbon inputs for secondary production in freshwater ecosystems? Freshwater Biology, 62, 833–853. DOI:10.1111/fwb.12909

Brett, M.T., Holtgrieve, G.W., & Schindler, D.E. 2018. An assessment of assumptions and uncertainty in deuterium‐based estimates of terrestrial subsidies to aquatic consumers. Ecology, 99(5), 1073–1088. DOI: 10.1002/ecy.2211

Brett, M.T., & Müller‐Navarra, D. 1997. The role of highly unsaturated fatty acids in aquatic food web processes. Freshwater Biology 38(3), 483–499

Brito, E. F., Moulton, T. P., De Souza, M. L., & Bunn, S. E. 2006. Stable isotope analysis indicates microalgae as the predominant food source of fauna in a coastal forest stream, southeast Brazil. Austral Ecology, 31(5), 623–633. DOI:10.1111/j.1442-9993.2006.01610.x

Bunn, S. E., Davies, P. M., & Mosisch, T. D. 1999. Ecosystem measures of river health and their response to riparian and catchment degradation. Freshwater Biology, 41(2), 333–345. DOI:10.1046/j.1365-2427.1999.00434.x

Cashman, M. J., Wehr, J.D., & Truhn, K. 2013. Elevated light and nutrients alter the nutritional quality of stream periphyton. Freshwater Biology 58(7), 1447–1457. DOI:10.1111/fwb.12142

Carvalho, D. R., Castro, D., Callisto, M., Moreira, M. Z., & Pompeu, P. S. 2015. Isotopic variation in five species of stream fishes under the influence of different land uses. Journal of Fish Biology, 87(3), 559–578. DOI:10.1111/jfb.12734

Carvalho, D. R., Castro, D., Callisto, M., Moreira, M. Z., & Pompeu, P. S. 2017. The trophic structure of fish communities from streams in the Brazilian Cerrado under different land uses: an approach using stable isotopes. Hydrobiologia, 795, 199–217. DOI:10.1007/s10750-017-3130-6

Carvalho, D. R., Castro, D. M. P., Callisto, M., Chaves, A. J. de M., Moreira, M. Z., & Pompeu, P. S. 2019. Stable isotopes and stomach content analyses indicate omnivorous habits and opportunistic feeding behavior of an invasive fish. Aquatic Ecology, 53, 365–381.

Carvalho, D. R., Alves, C. B. M., Flecker, A. S., Sparks, J. P., Zacharias Moreira, M., & Pompeu, P. S. 2020. Using δ15N of periphyton and fish to evaluate spatial and seasonal variation of anthropogenic nitrogen inputs in a polluted Brazilian river basin. Ecological Indicators, 115(2020), 106372, DOI:10.1016/j.ecolind.2020.106372

Collins, S. M., Kohler, T. J., Thomas, S. A., Fetzer, W. W., & Flecker, A. S. 2016a. The importance of terrestrial subsidies in stream food webs varies along a stream size gradient. Oikos, 125(5), 674–685. DOI:10.1111/oik.02713

Collins, S. M., Sparks, J. P., Thomas, S. A., Wheatley, S. A., & Flecker, A. S. 2016b. Increased Light Availability Reduces the Importance of Bacterial Carbon in Headwater Stream Food Webs. Ecosystems, 19(3), 396–410. DOI:10.1007/s10021-015-9940-3

Collins, S. M., Thomas, S. A., Heatherly, T., MacNeill, K. L., Leduc, A. O. H. C., López-Sepulcre, A., Lamphere, B. A., El-Sabaawi, R. W., Reznick, D. N., Pringle, C. M., & Flecker, A. S. 2016c. Fish introductions and light modulate food web fluxes in tropical streams: A whole-ecosystem experimental approach. Ecology, 97(11), 3154–3166. DOI:10.1002/ecy.1530

Dekar, M. P., King, R. S., Back, J. A., Whigham, D. F., & Walker, C. M. 2012. Allochthonous inputs from grass-dominated wetlands support juvenile salmonids in headwater streams: Evidence from stable isotopes of carbon, hydrogen, and nitrogen. Freshwater Science, 31 (11), 121–132. DOI:10.1899/11-016.1

Doucett, R. R., Marks, J. C., Blinn, D. W., Caron, M., & Hungate, B. A. 2007. Measuring terrestrial subsidies to aquatic food webs using stable isotopes of hydrogen. Ecology, 88(6), 1587–1592. DOI:10.1890/06-1184

Ebm, N., Guo, F., Brett, M. T., Bunn, S. E., & Kainz, M. J. 2020. Polyunsaturated fatty acids in fish tissues more closely resemble algal than terrestrial diet sources. Hydrobiologia, 848(2), 371–383. DOI:10.1007/s10750-020-04445-1

El‐Sabaawi, R. W., Zandonà, E., Kohler, T. J., Marshall, M. C., Moslemi, J. M., Travis, J., López‐Sepulcre, A., Ferriere, R., Pringle, C.M., Thomas, S.A., & Reznick, D.N. 2012. Widespread intraspecific organismal stoichiometry among populations of the Trinidadian guppy. Functional Ecology 26 (3), 666–676.

Elser, J. J., Fagan, W. F., Denno, R. F., Dobberfuhl, D. R., Folarin, A., Huberty, A., Interlandi, S., Kilham, S. S., McCauley, E., Schulz, K. L. & Siemann, E. H. 2000. Nutritional constraints in terrestrial and freshwater food webs. Nature 408(6812), 578–580. DOI:10.1038/35046058

Esteves, K. E., Aranha, J. M., & Albrecht, M. P. 2021. Ecologia trófica de peixes de riachos. Oecologia Australis, 25 (02), 266-282. DOI: 10.4257/oeco.2021.2502.04

Frost, P. C., Benstead, J. P., Cross, W. F., Hillebrand, H., Larson, J. H., Xenopoulos, M. A., & Yoshida, T. 2006. Threshold elemental ratios of carbon and phosphorus in aquatic consumers. Ecology Letters, 9(7), 774–779. DOI:10.1111/j.1461-0248.2006.00919.x

Fry, B. 2006. Stable Isotope Ecology. New York: Springer: p. 308. DOI:10.1007/0-387-33745-8

Fujibayashi, M., Miura, Y., Suganuma, R., Takahashi, S., Sakamaki, T., Miyata, N., & Kazama, S. 2019. Origin of carbon and essential fatty acids in higher trophic level fish in headwater stream food webs. Biomolecules, 9(9), 1–13. DOI:10.3390/biom9090487

Gomes, A. D., Tolussi, C. E., Boëchat, I. G., Pompêo, M. L. M., Cortez, M. P. T., Honji, R. M., & Moreira, R. G. 2016. Fatty acid composition of tropical fish depends on reservoir trophic status and fish feeding habit. Lipids, 51(10), 1193–1206. DOI:10.1007/s11745-016-4196-z

Guo, F., Bunn, S. E., Brett, M. T., & Kainz, M. J. 2017. Polyunsaturated fatty acids in stream food webs – high dissimilarity among producers and consumers. Freshwater Biology, 62(8), 1325–1334. DOI:10.1111/fwb.12956

Guo, F., Kainz, M. J., Sheldon, F., & Bunn, S. E. 2016. The importance of high-quality algal food sources in stream food webs - current status and future perspectives. Freshwater Biology, 61, 815–831. DOI:10.1111/fwb.12755

Hamilton, S. K., Sippel, S. J., & Bunn, S. E. 2005. Separation of algae from detritus for stable isotope or ecological stoichiometry studies using density fractionation in colloidal silica. Limnology and Oceanography: Methods, 3, 149–157.

Hayden, B., McWilliam-Hughes, S. M., & Cunjak, R. A. 2016. Evidence for limited trophic transfer of allochthonous energy in temperate river food webs. Freshwater Science, 35(2), 544–558. DOI:10.1086/686001.

Hayden, B., Tongnunui, S., Beamish, F. W. H., Nithirojpakdee, P., Soto, D. X., & Cunjak, R. A. 2021. Functional and trophic diversity of tropical headwater stream communities inferred from carbon, nitrogen and hydrogen stable isotope ratios. Food webs 26(2021), e00181. DOI10.1016/j.fooweb.2020.e00181

Hondula, K. L., Pace, M. L., Cole, J. J., & Batt, R. D. 2014. Hydrogen isotope discrimination in aquatic primary producers: Implications for aquatic food web studies. Aquatic Sciences, 76(2), 217–229. DOI:10.1007/s00027-013-0331-6

Hotchkiss, E. R., & Hall, R. O. 2015. Whole-stream 13C tracer addition reveals distinct fates of newly fixed carbon. Ecology, 96(2), 403–416. DOI:10.1890/14-0631.1

Hutchinson G. E. 1978. An introduction to population biology. New Haven, CT: Yale University Press.

Ishikawa, N., Doi, H., & Finlay, J. 2012. Global meta-analysis for controlling factors on carbon stable isotope ratios of lotic periphyton. Oecologia. 170(2), 541–549.

Ishikawa, N. F., Finlay, J. C., Uno, H., Ogawa, N. O., Ohkouchi, N., Tayasu, I., & Power, M. E. 2020. Combined use of radiocarbon and stable carbon isotopes for the source mixing model in a stream food web. Limnology and Oceanography, 65(11), 2688–2696. DOI:10.1002/lno.11541

Jackson, A. L., Inger, R., Parnell, A. C., & Bearhop, S. 2011. Comparing isotopic niche widths among and within communities: SIBER - Stable Isotope Bayesian Ellipses in R. Journal of Animal Ecology, 80(3), 595–602. DOI:10.1111/j.1365-2656.2011.01806.x

Lau, D.C.P., Leung, K.M.Y., & Dudgeon, D. 2009. Are autochthonous foods more important than allochthonous resources to benthic consumers in tropical headwater streams? Journal of the North American Benthological Society, 28(2), 426–439. DOI:10.1899/07-079.1

Layman, C. A., Araujo, M. S., Boucek, R., Hammerschlag-Peyer, C. M., Harrison, E., Jud, Z. R., Matich, P., Rosenblatt, A. E., Vaudo, J. J., Yeager, L. A., Post, D. M., & Bearhop, S. 2012. Applying stable isotopes to examine food-web structure: An overview of analytical tools. Biological Reviews, 87(3), 545–562. DOI: 10.1111/j.1469-185X.2011.00208.x

Layman, C. A., Arrington, D. A., Mntaña, C. G., & Post, D. M. 2007a. Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology, 88(1), 42–48. DOI:10.1890/0012-9658(2007)88

Layman, C. A., Quattrochi, J. P., Peyer, C. M., & Allgeier, J. E. 2007b. Niche width collapse in a resilient top predator following ecosystem fragmentation. Ecology Letters, 10, 937–944.

Martínez Del Rio, C., Wolf, N., Carleton, S. A., & Gannes, L. Z. 2009. Isotopic ecology ten years after a call for more laboratory experiments. Biological Reviews, 84(1), 91–111. DOI:10.1111/j.1469-185X.2008.00064.x

Moore, J. W., Semmens, B. X. 2008. Incorporating uncertainty and prior information into stable isotope mixing models. Ecology Letters 11(5), 470–480.

Moulton, T. P., Souza, M. L., Walter, T. L., & Krsulovic, F. A. M. 2009. Pattern of periphyton chlorophyll and dry mass in a neotropical stream: a cheap and rapid analysis using a hand-held fluorometer. Marine and Freshwater Research, 60, 224–233.

McCutchan Jr, J. H., Lewis Jr, W. M., Kendall, C., & McGrath, C. C. 2003. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos, 102, 378–390. DOI:10.1034/j.1600-0706.2003.12098.x

Neres-Lima, V., Brito, E. F., Krsulović, F. A. M., Detweiler, A. M., Hershey, A. E., & Moulton, T. P. 2016. High importance of autochthonous basal food source for the food web of a Brazilian tropical stream regardless of shading. International Review of Hydrobiology, 101(3–4), 132–142. DOI:10.1002/iroh.201601851

Neres-Lima, V., Machado-Silva, F., Baptista, D. F., Oliveira, R. B. S., Andrade, P. M., Oliveira, A. F., Sasada-Sato, C. Y., Silva-Junior, E. F., Feijó-Lima, R., Angelini, R., Camargo, P. B., & Moulton, T. P. 2017. Allochthonous and autochthonous carbon flows in food webs of tropical forest streams. Freshwater Biology, 62(6), 1–12. DOI:10.1111/fwb.12921

Newsome, S. D., Martinez del Rio, C., Bearhop, S., & Phillips, D. L. 2007. A niche for isotopic ecology. Frontiers in Ecology and the Environment, 5(8), 429–436. DOI:10.1890/060150.1

Newsome, S. D., Wolf, N., Bradley, C. J., & Fogel, M. L. 2017. Assimilation and isotopic discrimination of hydrogen in tilapia: Implications for studying animal diet with δ2H. Ecosphere, 8(1). DOI:10.1002/ecs2.1616

Nielsen, J. M., Clare, E. L., Hayden, B., Brett, M. T., & Katrina, P. 2018. Diet tracing in ecology: method comparison and selection. Methods in Ecology and Evolution, 9(2), 278–291.

Parnell, A. C., Inger, R., Bearhop, S., & Jackson, A. L. 2010. Source partitioning using stable isotopes: Coping with too much variation. PLoS O, 5(3), e9672.

Parnell, A. C. 2020. simmr: A Stable Isotope Mixing Model. R package version 0.4.2. https://CRAN.R-project.org/package=simmr

Parzanini, C., Colombo, S.M., Kainz, M.J., Wacker, A., Parrish, C.C., & Arts, M.T. 2020. Discrimination between freshwater and marine fish using fatty acids: ecological implications and future perspectives. Environmental Reviews, 28(4), 546–559. DOI:10.1139/er-2020-0031

Post, D. M. 2002. Using stable isotopes to estimate trophic position: model, methods, and assumptions. Ecology, 83(3), 703–718. DOI:10.1890/0012-9658(2002)083[0703:USITET]2.0.CO;2

Raubenheimer, D., & Simpson, S. J. 1993. The geometry of compensatory feeding in the locust. Animal Behavior, 45(5), 953–963.

Reis, A. S., Albrecht, M. P., & Bunn, S. E. 2020. Food web pathways for fish communities in small tropical streams. Freshwater Biology, 65(5), 893–907. DOI:10.1111/fwb.13471

Sacramento, P. A., Manetta, G. I., & Benedito, E. 2016. Diet-tissue discrimination factors (Δ13C and Δ15N) and turnover rate in somatic tissues of a neotropical detritivorous fish on C3 and C4 diets. Journal of Fish Biology, 89(1), 213–219. DOI:10.1111/jfb.12859

Shipley, O. N., & Matich, P. 2020. Studying animal niches using bulk stable isotope ratios: an updated synthesis. Oecologia, 193(1), 27–51. DOI:10.1007/s00442-020-04654-4

Simpson, S. J., & Raubenheimer, D. 2012. The Nature of Nutrition: A Unifying Framework From Animal Adaptation to Human Obesity. Princenton University Press.

Solomon, C. T., Cole, J. J., Doucett, R. R., Pace, M. L., Preston, N. D., Smith, L. E., & Weidel, B. C. 2009. The influence of environmental water on the hydrogen stable isotope ratio in aquatic consumers. Oecologia, 161(2), 313–324. DOI:10.1007/s00442-009-1370-5

Soto, D. X., Wassenaar, L. I., & Hobson, K. A. 2013. Stable hydrogen and oxygen isotopes in aquatic food webs are tracers of diet and provenance. Functional Ecology, 27(2), 535–543. DOI:10.1111/1365-2435.12054

Stock, B. C., Jackson, A. L., Ward, E. J., Parnell, A. C., Phillips, D. L., & Semmens, B. X. 2018. Analyzing mixing systems using a new generation of Bayesian tracer mixing models. PeerJ, 2018(6), 1–27. DOI:10.7717/peerj.5096

Twining, C. W., Taipale, S. J., Ruess, L., Bec, A., Martin-Creuzburg, D., & Kainz, M. J. 2020. Stable isotopes of fatty acids: current and future perspectives for advancing trophic ecology. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 375(1804), 20190641. DOI:10.1098/rstb.2019.0641

Vander Zanden, H. B., Soto, D. X., Bowen, G. J., & Hobson, K. A. 2016. Expanding the isotopic toolbox: Applications of hydrogen and oxygen stable isotope ratios to food web studies. Frontiers in Ecology and Evolution, 4, 1–19. DOI:10.3389/fevo.2016.00020

Vander Zanden, M. J., & Rasmussen, J. B. 1999. Primary Consumer δ13C and δ15N and the Trophic Position of Aquatic Consumers. Ecology, 80(4), 1395–1404. DOI:10.1890/0012-9658(1999)080[1395:PCCANA]2.0.CO;2

Vanderklift, M. A., & Ponsard, S. 2003. Sources of variation in consumer-diet δ15N enrichment: A meta-analysis. Oecologia, 136(2), 169–182. DOI:10.1007/s00442-003-1270-z

Whiteman, J. P., Smith, E. A. E., Besser, A. C., & Newsome, S. D. 2019. A guide to using compound-specific stable isotope analysis to study the fates of molecules in organisms and ecosystems. Diversity, 11(1). DOI:10.3390/d11010008

Wilkinson, G. M., Cole, J. J., & Pace, M. L. 2015. Deuterium as a food source tracer: sensitivity to environmental water, lipid content, and hydrogen exchange. Limnology and Oceanography: Methods, 13 (5), 213–223. DOI: 10.1002/lom3.10019

Zandonà, E., Dalton, C. M., El-Sabaawi, R. W., Howard, J. L., Marshall, M. C., Kilham, S. S., Reznick, D. N., Travis, J., Kohler, T. J., Flecker, A. S., Thomas, S. A., & Pringle, C. M. 2017. Population variation in the trophic niche of the Trinidadian guppy from different predation regimes. Scientific Reports, 7(1), 1–11. DOI:10.1038/s41598-017-06163-6

Zandonà, E., Oliveira-Cunha, P., & Moreira-Ferreira, B. 2021. O papel dos peixes na reciclagem de nutrientes em riachos tropicais. Oecologia Australis, 25 (02), 450-465. DOI: 10.4257/oeco.2021.2502.14

Zeug, S. C., & Hoeinghaus, D. J. 2008. Can Stable Isotope Ratios Provide for Community-Wide Measures of Trophic Structure? Ecology, 89(8), 2353–2357.




DOI: https://doi.org/10.4257/oeco.2021.2502.05

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