Abstract
Tributaries greatly influence the supply of organic matter to large rivers. In this study, we used carbon (ẟ13C) and nitrogen (ẟ15N) stable isotopes to assess if organic matter from tributaries with different 15N compositions influenced the food webs of downstream fish assemblages. In addition, we aimed to evaluate if estimates of fish trophic position (TP) are influenced by 15N-depleted and 15N-enriched baselines. We compared the food web of a fish assemblage upstream from tributaries (control site), with food webs downstream from 15N-depleted (site 1) and 15N-enriched tributaries (site 2). Fishes and resources collected from sites 1 and 2 had significant differences in ẟ15N composition (15 N-depleted and 15N-enriched, respectively) relative to their conspecifics from the control site. At the control site, fish species’ TPs were more reliable and realistic based on their known feeding ecology, with TPs ranging between 2 and 3. In contrast, fish TPs at sites 1 and 2 ranged between 2 and 6, and no consistency was observed among trophic guilds. We conclude that tributaries exert a great influence on fish food webs at downstream sites, either by direct assimilation of organic matter by consumers, or by assimilation of the dissolved inorganic nitrogen by primary producers. In addition, fishes under influence of pollution may exhibit an inaccurate representation of their TP, drawing attention to possible source of bias for TP estimates, and consequently, in the food web structure of nitrogen-polluted areas.
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References
Alves CBM, Pompeu PS (2005) Historical changes in the Rio das Velhas fish fauna—Brazil. Am Fish Soc Symp 45:587–602
Alves CBM, Pompeu PS (2010) A fauna de peixes da bacia do rio das Velhas no final do século XX. In: Alves CBM, Pompeu PS (eds) Peixes do rio das Velhas: passado e presente. ARGVMENTVM, Belo Horizonte, pp 167–189
Alves GHZ, Tófoli RM, Ganassin MJM, Hahn NS (2016) Diet of Poecilia reticulata Peters, 1959 in streams from Paraná River basin: influence of the urbanization. Acta Sci Biol Sci 38:313. https://doi.org/10.4025/actascibiolsci.v38i3.29881
Anderson C, Cabana G (2009) Anthropogenic alterations of lotic food web structure: evidence from the use of nitrogen isotopes. Oikos 118:1929–1939. https://doi.org/10.1111/j.1600-0706.2009.17368.x
Aranibar JN, Anderson IC, Epstein HE et al (2008) Nitrogen isotope composition of soils, C3 and C4 plants along land use gradients in southern Africa. J Arid Environ 72:326–337. https://doi.org/10.1016/j.jaridenv.2007.06.007
Barrie A, Prosser SJ (1996) Automated analysis of light-element stable isotopes by isotope ratio mass spectrometry. In: Boutton TW, Yamasaki S-I (eds) Mass spectrometry of soils. Marcel Dekker, Inc., pp 1–46
Bunn SE, Leigh C, Jardine TD (2013) Diet-tissue fractionation of δ15N by consumers from streams and rivers. Limnol Oceanogr 58:765–773. https://doi.org/10.4319/lo.2013.58.3.0765
Busst GMA, Britton JR (2018) Tissue-specific turnover rates of the nitrogen stable isotope as functions of time and growth in a cyprinid fish. Hydrobiologia 805:49–60. https://doi.org/10.1007/s10750-017-3276-2
Cabana G, Rasmussen JB (1996) Comparison of aquatic food chains using nitrogen isotopes. Proc Natl Acad Sci U S A 93:10844–10847
Carvalho DR, Castro D, Callisto M et al (2015) Isotopic variation in five species of stream fishes under the influence of different land uses. J Fish Biol 87:559–578. https://doi.org/10.1111/jfb.12734
CBH Rio das Velhas (2016a) Cartilha Plano Diretor de Recursos Hídricos Unidade Territorial Estratégica Nascentes. https://cdn.agenciapeixevivo.org.br/arquivos/uploads/2016/04/01_cartilha_ute_nascentes_2016_04_13_isuuu.pdf. Accessed 18 Oct 2021
CBH Rio das Velhas (2016b) Cartilha Plano Diretor de Recursos Hídricos Unidade Territorial Estratégica Ribeirão Arrudas. https://cdn.agenciapeixevivo.org.br/arquivos/uploads/2016/04/06_cartilha_arrudas_225x27cm_2016_04_13_issuuu.pdf. Accessed 18 Oct 2021
CBH Rio das Velhas (2016c) Cartilha Plano Diretor de Recursos Hídricos Unidade Territorial Estratégica Ribeirão Onça. http://cbhvelhas.org.br/wp-content/uploads/2016/04/07_cartilha_onca_225x27cm_2016_04_13_issuuu-2.pdf
CBH Rio das Velhas (2016d) Cartilha Plano Diretor de Recursos Hídricos Unidade Territorial Estratégica Ribeirão da Mata. https://cdn.agenciapeixevivo.org.br/arquivos/uploads/2016/04/09_cartilha_ribeiraodamata_225x27cm_2016_04_13_issuuu.pdf. Accessed 18 Oct 2021
CBH Rio das Velhas (2016e) Cartilha Plano Diretor de Recursos Hídricos Unidade Territorial Estratégica Ribeirão Jequitibá. https://cdn.agenciapeixevivo.org.br/arquivos/uploads/2016/04/13_cartilha_ribeiraojequitiba_225x27cm_2016_04_13_issuuu.pdf. Accessed 18 Oct 2021
CBH Velhas (2019) A bacia hidrográfica do Rio das Velhas. In: Com. da bacia hidrográfica do Rio das Velhas. http://cbhvelhas.org.br/a-bacia-hidrografica-do-rio-das-velhas/. Accessed 3 Jun 2019
Ceneviva-Bastos M, Casatti L (2007) Oportunismo alimentar de Knodus moenkhausii (Teleostei, Characidae): uma espécie abundante em riachos do noroeste do Estado de São Paulo, Brasil. Iheringia Série Zool 97:7–15. https://doi.org/10.1590/S0073-47212007000100002
Cohen RA, Fong P (2005) Experimental evidence supports the use of δ15N content of the opportunistic green macroalga Enteromorpha intestinalis (Chlorophyta) to determine nitrogen sources to estuaries. J Phycol 41:287–293. https://doi.org/10.1111/j.1529-8817.2005.04022.x
Cohen RA, Fong P (2004) Nitrogen uptake and assimilation in Enteromorpha intestinalis (L.) Link (Chlorophyta): using 15N to determine preference during simultaneous pulses of nitrate and ammonium. J Exp Mar Bio Ecol 309:67–77. https://doi.org/10.1016/j.jembe.2004.03.009
Coll M, Navarro J, Olson RJ, Christensen V (2013) Assessing the trophic position and ecological role of squids in marine ecosystems by means of food-web models. Deep Sea Res Part II Top Stud Oceanogr 95:21–36. https://doi.org/10.1016/j.dsr2.2012.08.020
Cook GD (2001) Effects of frequent fires and grazing on stable nitrogen isotope ratios of vegetation in northern Australia. Austral Ecol 26:630–636. https://doi.org/10.1046/j.1442-9993.2001.01150.x
Costanzo SD, Udy J, Longstaff B, Jones A (2005) Using nitrogen stable isotope ratios (δ15N) of macroalgae to determine the effectiveness of sewage upgrades: changes in the extent of sewage plumes over four years in Moreton Bay, Australia. Mar Pollut Bull 51:212–217. https://doi.org/10.1016/j.marpolbul.2004.10.018
Dailer ML, Knox RS, Smith JE et al (2010) Using δ15N values in algal tissue to map locations and potential sources of anthropogenic nutrient inputs on the island of Maui, Hawai‘i, USA. Mar Pollut Bull 60:655–671. https://doi.org/10.1016/j.marpolbul.2009.12.021
Dalerum F, Angerbjörn A (2005) Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes. Oecologia 144:647–658. https://doi.org/10.1007/s00442-005-0118-0
de Carvalho D, Alves C, Flecker A et al (2020a) Using δ15N of periphyton and fish to evaluate spatial and seasonal variation of anthropogenic nitrogen inputs in a polluted Brazilian river basin. Ecol Indic 115:106372. https://doi.org/10.1016/j.ecolind.2020.106372
de Carvalho D, Flecker A, Alves C et al (2019a) Trophic responses to aquatic pollution of native and exotic livebearer fishes. Sci Total Environ 681:503–515. https://doi.org/10.1016/j.scitotenv.2019.05.092
de Carvalho DR, Alves CBM, Moreira MZ, Pompeu PS (2020b) Trophic diversity and carbon sources supporting fish communities along a pollution gradient in a tropical river. Sci Total Environ 738:139878. https://doi.org/10.1016/j.scitotenv.2020.139878
de Carvalho DR, de Castro DMP, Callisto M et al (2019b) Stable isotopes and stomach content analyses indicate omnivorous habits and opportunistic feeding behavior of an invasive fish. Aquat Ecol 53:365–381. https://doi.org/10.1007/s10452-019-09695-3
de Carvalho DR, de Castro DMP, Callisto M et al (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. https://doi.org/10.1007/s10750-017-3130-6
de Carvalho DR, Sparks JP, Flecker AS et al (2021) Nitrogen pollution promotes changes in the niche space of fish communities. Oecologia 197:485–500. https://doi.org/10.1007/s00442-021-05029-z
DeNiro M, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351
DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506. https://doi.org/10.1016/0016-7037(78)90199-0
Dethier M, Sosik E, Galloway A et al (2013) Addressing assumptions: variation in stable isotopes and fatty acids of marine macrophytes can confound conclusions of food web studies. Mar Ecol Prog Ser 478:1–14. https://doi.org/10.3354/meps10310
Drenner RW, Hambright RKD (2002) Piscivores, trophic cascades, and lake management. Sci World J 2:284–307. https://doi.org/10.1100/tsw.2002.138
Feio MJ, Ferreira WR, Macedo DR et al (2015) Defining and testing targets for the recovery of tropical streams based on macroinvertebrate communities and abiotic conditions. River Res Appl 31:70–84. https://doi.org/10.1002/rra.2716
Finlay JC, Kendall C (2007) Stable isotope tracing of temporal and spatial variability in organic matter sources to freshwater ecosystems. In: Finlay JC, Kendall C (eds) Stable isotope tracing of organic matter sources and food web interactions in watersheds, Second. pp 283–333
France RL (1995) Carbon-13 enrichment in benthic compared to planktonic algae: foodweb implications. Mar Ecol Prog Ser 124:307–312
Fry B, Sherr EB (1984) δ13C measurements as indicators of carbon flow in marine and freshwater ecosystems. In: Contributions in marine science. pp 13–47
Gaiser EE, Childers DL, Jones RD et al (2006) Periphyton responses to eutrophication in the Florida Everglades: cross-system patterns of structural and compositional change. Limnol Oceanogr 51:617–630. https://doi.org/10.4319/lo.2006.51.1_part_2.0617
Ganassin MJM, Frota A, Muniz CM et al (2020) Urbanisation affects the diet and feeding selectivity of the invasive guppy Poecilia reticulata. Ecol Freshw Fish 29:252–265. https://doi.org/10.1111/eff.12511
Garcia-Domingo JL, Saldaña J (2008) Effects of heterogeneous interaction strengths on food web complexity. Oikos 117:336–343. https://doi.org/10.1111/j.2007.0030-1299.16261.x
Hadwen WL, Arthington AH (2007) Food webs of two intermittently open estuaries receiving 15N-enriched sewage effluent. Estuar Coast Shelf Sci 71:347–358. https://doi.org/10.1016/j.ecss.2006.08.017
Hadwen WL, Bunn SE (2005) Food web responses to low-level nutrient and 15N-tracer additions in the littoral zone of an oligotrophic dune lake. Limnol Oceanogr 50:1096–1105. https://doi.org/10.4319/lo.2005.50.4.1096
Hairston NG, Hairston NG (1993) Cause-effect relationships in energy flow, trophic structure, and interspecific interactions. Am Nat 142:379–411. https://doi.org/10.1086/285546
Hall SJ, Hale RL, Baker MA, et al (2015) Riparian plant isotopes reflect anthropogenic nitrogen perturbations: robust patterns across land use gradients. Ecosphere 6. 10.1890/ES15-00319.1
Hamer KC, Newton RJ, Edwards FA et al (2015) Impacts of selective logging on insectivorous birds in Borneo: the importance of trophic position, body size and foraging height. Biol Conserv 188:82–88. https://doi.org/10.1016/j.biocon.2014.09.026
Hansson S, Hobbie JE, Elmgren R et al (1997) The stable nitrogen isotope ratio as a marker of food-web interactions and fish migration. Ecology 78:2249–2257. https://doi.org/10.1890/0012-9658(1997)078[2249:TSNIRA]2.0.CO;2
Hesslein RH, Hallard KA, Ramlal P (1993) Replacement of sulfur, carbon, and nitrogen in tissue of growing broad whitefish (Coregonus nasus) in response to a change in diet traced by δ34S, δ13C, and δ15N. Can J Fish Aquat Sci 50:2071–2076. https://doi.org/10.1139/f93-230
Hill WR, Fanta SE, Roberts BJ (2008) 13C dynamics in benthic algae: effects of light, phosphorus, and biomass development. Limnol Oceanogr 53:1217–1226. https://doi.org/10.4319/lo.2008.53.4.1217
IBGE (2018) Estimativas de população. In: Inst. Bras. Geogr. e Estatística. https://www.ibge.gov.br/estatisticas-novoportal/sociais/populacao/9103-estimativas-de-populacao.html?=&t=resultados. Accessed 26 Feb 2019
IGAM - Instituto Mineiro de Gestão das águas (2017) Monitoramento de qualidade das águas. In: Monit. Qual. das Águas. http://portalinfohidro.igam.mg.gov.br/monitoramento-de-qualidade-das-aguas. Accessed 16 Jan 2019
Karr JR (1981) Assessment of biotic integrity using fish communities. Fisheries 6:21–27. https://doi.org/10.1577/1548-8446(1981)006%3c0021:AOBIUF%3e2.0.CO;2
Kendall C (1998) Tracing nitrogen sources and cycling in catchments. In: Kendall C, McDonnell JJ (eds) Isotope tracers in catchment hydrology. Elsevier B.V., pp 519–576
Loomer HA, Oakes KD, Schiff SL et al (2015) Use of stable isotopes to trace municipal wastewater effluents into food webs within a highly developed river system. River Res Appl 31:1093–1100. https://doi.org/10.1002/rra.2826
Lopes C, Benedito E, Martinelli L (2009) Trophic position of bottom-feeding fish in the Upper Paraná River floodplain. Brazilian J Biol 69:573–581. https://doi.org/10.1590/S1519-69842009000300012
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 42:930–937. https://doi.org/10.4319/lo.1997.42.5.0930
McCutchan JH, Lewis WM, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378–390. https://doi.org/10.1034/j.1600-0706.2003.12098.x
McCutchan JH Jr, Lewis WM Jr (2001) Seasonal variation in stable isotope ratios of stream algae. Verhandlungen Des Int Verein Limnol 27:3304–3307
McIntyre PB, Flecker AS (2006) Rapid turnover of tissue nitrogen of primary consumers in tropical freshwaters. Oecologia 148:12–21. https://doi.org/10.1007/s00442-005-0354-3
Middelburg JJ (2014) Stable isotopes dissect aquatic food webs from the top to the bottom. Biogeosciences 11:2357–2371. https://doi.org/10.5194/bg-11-2357-2014
Mill AC, Pinnegar JK, Polunin NVC (2007) Explaining isotope trophic-step fractionation: why herbivorous fish are different. Funct Ecol 21:1137–1145. https://doi.org/10.1111/j.1365-2435.2007.01330.x
Nakagawa M, Hyodo F, Nakashizuka T (2007) Effect of forest use on trophic levels of small mammals: an analysis using stable isotopes. Can J Zool 85:472–478. https://doi.org/10.1139/Z07-026
Nikolenko O, Jurado A, Borges AV et al (2018) Isotopic composition of nitrogen species in groundwater under agricultural areas: a review. Sci Total Environ 621:1415–1432. https://doi.org/10.1016/j.scitotenv.2017.10.086
Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703. https://doi.org/10.2307/3071875
Prado do MR, Carvalho DR, de Alves CBM, et al. (2020) Convergent responses of fish belonging to different feeding guilds to sewage pollution. Neotrop Ichthyol 18:e190041. https://doi.org/10.1590/1982-0224-2019-0045
Quezada-Romegialli C, Jackson AL, Hayden B et al (2018) tRophicPosition, an R package for the Bayesian estimation of trophic position from consumer stable isotope ratios. Methods Ecol Evol 9:1592–1599. https://doi.org/10.1111/2041-210X.13009
Sacramento PA, Manetta GI, 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. J Fish Biol 89:213–219. https://doi.org/10.1111/jfb.12859
Sprules WG, Bowerman JE (1988) Omnivory and food chain length in zooplankton food webs. Ecology 69:418–426. https://doi.org/10.2307/1940440
Taylor KG, Owens PN, Batalla RJ, Garcia C (2008) Sediment and contaminant sources and transfers in river basins. In: Owens PN (ed) Sustainable management of sediment resources. pp 83–135
Toda H, Uemura Y, Okino T et al (2002) Use of nitrogen stable isotope ratio of periphyton for monitoring nitrogen sources in a river system. Water Sci Technol 46:431–435. https://doi.org/10.2166/wst.2002.0774
Vander Zanden MJ, Cabana G, Rasmussen JB (1997) Comparing trophic position of freshwater fish calculated using stable nitrogen isotope ratios (δ15N) and literature dietary data. Can J Fish Aquat Sci 54:1142–1158. https://doi.org/10.1139/cjfas-54-5-1142
Vander Zanden MJ, Rasmussen JB (2001) Variation in δ15N and δ13C trophic fractionation: Implications for aquatic food web studies. Limnol Oceanogr 46:2061–2066. https://doi.org/10.4319/lo.2001.46.8.2061
Vander Zanden MJ, Rasmussen JB (1999) Primary consumer δ13C and δ15N and the trophic position of aquatic consumers. Ecology 80:1395–1404. https://doi.org/10.1890/0012-9658(1999)080[1395:pccana]2.0.co;2
Vander Zanden MJ, Shuter BJ, Lester N, Rasmussen JB (1999) Patterns of food chain length in lakes: a stable isotope study. Am Nat 154:406–416. https://doi.org/10.1086/303250
Vanderklift MA, Ponsard S (2003) Sources of variation in consumer-diet 15N enrichment: a meta-analysis. Oecologia 136:169–182. https://doi.org/10.1007/s00442-003-1270-z
Wang Y, Liu D, Richard P, Di B (2016) Selection of effective macroalgal species and tracing nitrogen sources on the different part of Yantai coast, China indicated by macroalgal δ15N values. Sci Total Environ 542:306–314. https://doi.org/10.1016/j.scitotenv.2015.10.059
Winemiller KO, Hoeinghaus DJ, Pease AA et al (2011) Stable isotope analysis reveals food web structure and watershed impacts along the fluvial gradient of a Mesoamerican coastal river. River Res Appl 27:791–803. https://doi.org/10.1002/rra.1396
Won E-J, Choi B, Hong S et al (2018) Importance of accurate trophic level determination by nitrogen isotope of amino acids for trophic magnification studies: a review. Environ Pollut 238:677–690. https://doi.org/10.1016/j.envpol.2018.03.045
Acknowledgements
We thank the Agência Peixe Vivo and the Comitê de Bacia Hidrográfica do Rio das Velhas (CBH—Rio das Velhas) for the project financial support and the Projeto Manuelzão for the logistical support. Thanks to Aline Junqueira Grossi (Federal University of Lavras, UFLA) and Luiza Hoehne (Federal University of Minas Gerais, UFMG) for the support on processing of samples. Thanks also to the Benthos Ecology Laboratory (UFMG) and the Laboratory of Fish Ecology (UFLA) who assisted in the processing of samples and infrastructure, and to the Center for Nuclear Energy in Agriculture (CENA) for their support and partnership in the isotopic analysis.
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This work was supported by the Agência Peixe Vivo and Comitê de Bacia Hidrográfica do Rio das Velhas—CBH Rio das Velhas (grant/contract number 001/2015). Débora Reis de Carvalho has received research support from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (Finance code 32004010017P3 and 88881.190508/2018–01). Paulo Santos Pompeu has received research support from Conselho Nacional de Desenvolvimento Científico e Tecnológico (grant number 303548/2017–7) and Fundação de Amparo à Pesquisa do Estado de Minas Gerais (grant number PPM-00237/13).
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All authors contributed to the study conception and design. Carlos Bernardo Mascarenhas Alves was responsible for funding acquisition. Material preparation and data collection were performed by Débora Reis de Carvalho and Carlos Bernardo Mascarenhas Alves. Analysis was performed by Débora Reis de Carvalho and Paulo Santos Pompeu. The first draft of the manuscript was written by Débora Reis de Carvalho and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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de Carvalho, D.R., Alves, C.B.M. & Pompeu, P.S. Uncertainty in estimating fish trophic positions and food web structure in highly polluted river basins. Environ Biol Fish 105, 119–137 (2022). https://doi.org/10.1007/s10641-021-01199-0
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DOI: https://doi.org/10.1007/s10641-021-01199-0