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Advances in the aquatic sciences
RESEARCH ARTICLE

Comparison of microbial processing of Brachiaria brizantha, a C4 invasive species and a rainforest species in tropical streams of the Atlantic Forest of south-eastern Brazil

A. F. Figueiredo A C , F. G. Augusto A , L. D. Coletta A , P. J. Duarte-Neto B , E. A. Mazzi A and L. A. Martinelli A
+ Author Affiliations
- Author Affiliations

A Universidade de São Paulo, Centro de Energia Nuclear na Agricultura, Laboratório de Ecologia Isotópica, Avenida Centenário, 303 – São Dimas, 13400-970, Piracicaba, São Paulo, Brazil.

B Departamento de Estatística e Informática, Universidade Federal Rural de Pernambuco, Rua Dom Manoel de Medeiros, s/n – Dois Irmãos, 52171-900, Recife, Pernambuco, Brazil.

C Corresponding author. Email: alinefigueiredo89@gmail.com

Marine and Freshwater Research 69(9) 1397-1407 https://doi.org/10.1071/MF17080
Submitted: 3 June 2016  Accepted: 6 February 2018   Published: 28 May 2018

Abstract

The breakdown of allochthonous organic matter is considered to be the main source of energy and nutrients for the majority of first-order streams. Thus, land-use change and riparian vegetation, such as deforestation and conversion of native forest to pasture lands, will lead to unwanted changes of the structure and function of aquatic ecosystems due to the disturbance of organic-matter supply. The C4 grasses, extensively used as forage in tropical regions, are poorly studied as important sources of allochthonous material because they are usually considered as a poor source of nutrients. Because the effects of land-use change on ecosystem functions are not fully known, we aimed to evaluate how such changes in riparian vegetation can affect nutrient cycling by means of measuring the decomposition rate of an abundant native C3 species and an exotic C4 grass species in first-order streams of the Atlantic Forest. Our results showed that C4 detritus decomposed faster than did C3 detritus, despite its lower nutrient concentration. This was likely to be due to the lower lignin concentration of the C4 species than the native C3 species. Lignin also influenced nutrient-loss dynamics of the C3 species, because it can interact with other cellular constituents and prevent the decomposition of most labile compounds. Our results supported the observation that the replacement of riparian vegetation alters breakdown rates and nutrient distributions, which may disrupt aquatic food webs.

Additional keywords: litter decomposition, nutrient cycling, pasture.


References

Alvim, E. A., Medeiros, A. O., Rezende, R. S., and Junior, J. F. G. (2014). Leaf breakdown in a natural open tropical stream. Journal of Limnology 74, 248–260.

Andrade, T. M. B., Camargo, P. B., Silva, D. M. L., Piccolo, M. C., Vieira, S. A., Alves, L. F., Joly, C. A., and Martinelli, L. A. (2011). Dynamics of dissolved forms of carbon and inorganic nitrogen in small watersheds of the coastal Atlantic forest in southeast Brazil. Water, Air, and Soil Pollution 214, 393–408.
Dynamics of dissolved forms of carbon and inorganic nitrogen in small watersheds of the coastal Atlantic forest in southeast Brazil.Crossref | GoogleScholarGoogle Scholar |

Antonio, J. (2016). O efeito da transposição na decomposição de folhas de diferentes espécies arbóreas entre a Floresta Ombrófila Densa de Terras Baixas e Montana do litoral norte do Estado de São Paulo. Ph.D. Dissertation, Universidade de São Paulo, Brazil.

Arato, H. D. (2006). Caracterização química e decomposição de folhas de espécies arbóreas nativas da Mata Atlântica. M.Sc. Dissertation, Federal University of Viçosa, Viçosa, Brazil.

Augusto, F. G., Tassoni Filho, M., Ferreira, A., Pereira, A. L., Camargo, P. B. D., and Martinelli, L. A. (2015). Land use change in the Atlantic Forest affects carbon and nitrogen sources of streams as revealed by the isotopic composition of terrestrial invertebrates. Biota Neotropica 15, e20140188.
Land use change in the Atlantic Forest affects carbon and nitrogen sources of streams as revealed by the isotopic composition of terrestrial invertebrates.Crossref | GoogleScholarGoogle Scholar |

Baldy, V., Gessner, M. O., and Chauvet, E. (1995). Bacteria, fungi and the breakdown of leaf litter in a large river. Oikos 74, 93–102.
Bacteria, fungi and the breakdown of leaf litter in a large river.Crossref | GoogleScholarGoogle Scholar |

Barbehenn, R. V., Chen, Z., Karowe, D. N., and Spickard, A. (2004a). C3 grasses have higher nutritional quality than C4 grasses under ambient and elevated atmospheric CO2. Global Change Biology 10, 1565–1575.
C3 grasses have higher nutritional quality than C4 grasses under ambient and elevated atmospheric CO2.Crossref | GoogleScholarGoogle Scholar |

Barbehenn, R. V., Karowe, D. N., and Chen, Z. (2004b). Performance of a generalist grasshopper on a C3 and a C4 grass: compensation for the effects of elevated CO2 on plant nutritional quality. Oecologia 140, 96–103.
Performance of a generalist grasshopper on a C3 and a C4 grass: compensation for the effects of elevated CO2 on plant nutritional quality.Crossref | GoogleScholarGoogle Scholar |

Bärlocher, F. (1992). Research on aquatic hyphomycetes: historical background and overview. In ‘The Ecology of Aquatic Hyphomycetes’. (Eds F. Bärlocher.) pp 1–15. (Springer: Berlin, Germany.)

Bärlocher, F. (2005). Leaf mass loss estimated by litter bag technique. In ‘Methods to Study Litter Decomposition: a Practical Guide’. (Eds M. A. S. Graça, F. Barlocher, and M. Gessner.) pp. 37–42. (Springer: Dordrecht, Netherlands.)

Berg, B., and McClaugherty, C. (2008). ‘Plant Litter. Decomposition, Humus Formation, Carbon Sequestration’, 2nd edn. (Springer-Verlag: Berlin, Germany.)

Boddey, R. M., Jantalia, C. P., Macedo, M. O., de Oliveira, O. C., Resende, A. S., Alves, B. J. R., and Urquiaga, S. (2006). Potential of carbon sequestration in soils of the Atlantic Forest region of Brazil. In ‘Carbon Sequestration in Soil of Latin America’. (Eds R. Lal, C. C. Cerri, M. Bernoux, J. Etchevers, and E. Cerri.) pp. 305–348. (Howarth: New York, NY, USA.)

Boulton, A. J., and Boon, P. I. (1991). A review of methodology used to measure leaf litter decomposition in lotic environments: time to turn over an old leaf? Marine and Freshwater Research 42, 1–43.
A review of methodology used to measure leaf litter decomposition in lotic environments: time to turn over an old leaf?Crossref | GoogleScholarGoogle Scholar |

Boyero, L., Pearson, R. G., Gessner, M. O., Barmuta, L. A., Ferreira, V., Graca, M. A. S., Dudgeon, D., Boulton, A. J., Callisto, M., Chauvet, E., Helson, J. E., Bruder, A., Albarino, R. J., Yule, C. M., Arunachalam, M., Davies, J. N., Figueroa, R., Flecker, A. S., Rarnirez, A., Death, R. G., Iwata, T., Mathooko, J. M., Mathuriau, C., Goncalves, J. F., Moretti, M. S., Jinggut, T., Lamothe, S., M’Erimba, C., Ratnarajah, L., Schindler, M. H., Castela, J., Buria, L. M., Cornejo, A., Villanueva, V. D., and West, D. C. (2011). A global experiment suggests climate warming will not accelerate litter decomposition in streams but might reduce carbon sequestration Ecology Letters 14, 289–294.
A global experiment suggests climate warming will not accelerate litter decomposition in streams but might reduce carbon sequestrationCrossref | GoogleScholarGoogle Scholar |

Boyero, L., Pearson, R. G., Gessner, M. O., Dudgeon, D., Ramírez, A., Yule, C. M., Callisto, M., Pringle, C. M., Encalada, A. C., Arunachalam, M., Mathooko, J., Helson, J. E., Rincón, J., Bruder, A., Cornejo, A., Flocker, A. S., Mathuriau, C., M’érimbau, C., Gonçalves, J. F., Moretti, M., and Jinggut, T. (2015). Leaf-litter breakdown in tropical streams: is variability the norm? Freshwater Science 34, 759–769.
Leaf-litter breakdown in tropical streams: is variability the norm?Crossref | GoogleScholarGoogle Scholar |

Bruder, A., Chauvet, E., and Gessner, M. O. (2011). Litter diversity, fungal decomposers and litter decomposition under simulated stream intermittency. Functional Ecology 25, 1269–1277.
Litter diversity, fungal decomposers and litter decomposition under simulated stream intermittency.Crossref | GoogleScholarGoogle Scholar |

Callisto, M., Melo, A. S., Baptista, D. F., Gonçalves, J. F., Graça, M. A. S., and Augusto, F. G. (2012). Future ecological studies of Brazilian headwater streams under global-changes. Acta Limnologica Brasiliensia 24, 293–302.
Future ecological studies of Brazilian headwater streams under global-changes.Crossref | GoogleScholarGoogle Scholar |

Campbell, M. M., and Sederoff, R. R. (1996). Variation in lignin content and composition (mechanisms of control and implications for the genetic improvement of plants). Plant Physiology 110, 3–13.
Variation in lignin content and composition (mechanisms of control and implications for the genetic improvement of plants).Crossref | GoogleScholarGoogle Scholar |

Chizzotti, F. H. M., Pereira, O. G., Valadares Filho, S. C., Garcia, R., Chizzotti, M. L., Leão, M. I., and Pereira, D. H. (2005). Consumo, digestibilidade total e desempenho de novilhos Nelore recebendo dietas contendo diferentes proporções de silagens de Brachiaria brizantha cv. Marandu e de sorgo. Revista Brasileira de Zootecnia 34, 2427–2436.
Consumo, digestibilidade total e desempenho de novilhos Nelore recebendo dietas contendo diferentes proporções de silagens de Brachiaria brizantha cv. Marandu e de sorgo.Crossref | GoogleScholarGoogle Scholar |

Clapcott, J. E., and Bunn, S. E. (2003). Can C4 plants contribute to the aquatic food webs of subtropical streams? Freshwater Biology 48, 1105–1116.
Can C4 plants contribute to the aquatic food webs of subtropical streams?Crossref | GoogleScholarGoogle Scholar |

Coelho, J. S., Araújo, S. D. C., Viana, M. C. M., Villela, S. D. J., Freire, F. M., and Braz, T. D. S. (2014). Morphophysiology and nutritive value of signalgrass in silvipastoral system with different tree arrangements. Semina Ciencias Agrarias 35, 1487–1499.
Morphophysiology and nutritive value of signalgrass in silvipastoral system with different tree arrangements.Crossref | GoogleScholarGoogle Scholar |

Coletta, L. D. (2015). Decomposição foliar na Floresta Ombrófila Densa em diferentes altitudes e condições climáticas. Ph.D. Dissertation, University of São Paulo, Brazil.

Coûteaux, M. M., Bottner, P., and Berg, B. (1995). Litter decomposition, climate and litter quality. Trends in Ecology & Evolution 10, 63–66.
Litter decomposition, climate and litter quality.Crossref | GoogleScholarGoogle Scholar |

Craine, J. M., Morrow, C., and Fierer, N. (2007). Microbial nitrogen limitation increases decomposition. Ecology 88, 2105–2113.
Microbial nitrogen limitation increases decomposition.Crossref | GoogleScholarGoogle Scholar |

Crowther, T. W., Boddy, L., and Jones, T. H. (2011). Species-specific effects of soil fauna on fungal foraging and decomposition. Oecologia 167, 535–545.
Species-specific effects of soil fauna on fungal foraging and decomposition.Crossref | GoogleScholarGoogle Scholar |

Dang, C. K., Schindler, M., Chauvet, E., and Gessner, M. O. (2009). Temperature oscillation coupled with fungal community shifts can modulate warming effects on litter decomposition. Ecology 90, 122–131.
Temperature oscillation coupled with fungal community shifts can modulate warming effects on litter decomposition.Crossref | GoogleScholarGoogle Scholar |

de Souza Rezende, R., Gonçalves, J. F., and Petrucio, M. M. (2010). Leaf breakdown and invertebrate colonization of Eucalyptus grandis (Myrtaceae) and Hirtella glandulosa (Chrysobalanaceae) in two Neotropical lakes. Acta Limnologica Brasiliensia 22, 23–34.
Leaf breakdown and invertebrate colonization of Eucalyptus grandis (Myrtaceae) and Hirtella glandulosa (Chrysobalanaceae) in two Neotropical lakes.Crossref | GoogleScholarGoogle Scholar |

de Toledo Castanho, C., and de Oliveira, A. A. (2008). Relative effect of litter quality, forest type and their interaction on leaf decomposition in south-east Brazilian forests. Journal of Tropical Ecology 24, 149–156.
Relative effect of litter quality, forest type and their interaction on leaf decomposition in south-east Brazilian forests.Crossref | GoogleScholarGoogle Scholar |

Fernandes, I., Uzun, B., Pascoal, C., and Cássio, F. (2009). Responses of aquatic fungal communities on leaf litter to temperature change events. International Review of Hydrobiology 94, 410–418.
Responses of aquatic fungal communities on leaf litter to temperature change events.Crossref | GoogleScholarGoogle Scholar |

Ferreira, V., and Chauvet, E. (2011). Synergistic effects of water temperature and dissolved nutrients on litter decomposition and associated fungi. Global Change Biology 17, 551–564.
Synergistic effects of water temperature and dissolved nutrients on litter decomposition and associated fungi.Crossref | GoogleScholarGoogle Scholar |

Ferreira, A., De Paula, F. R., De Barros Ferraz, S. F., Gerhard, P., Kashiwaqui, E. A., Cyrino, J. E., and Martinelli, L. A. (2012). Riparian coverage affects diets of characids in neotropical streams. Ecology Freshwater Fish 21, 12–22.
Riparian coverage affects diets of characids in neotropical streams.Crossref | GoogleScholarGoogle Scholar |

Follstad Shah, J. J., Kominoski, J. S., Ardón, M., Dodds, W. K., Gessner, M. O., Griffiths, N. A., Hawkins, C. P., Johnson, S. L., Lecerf, A., Leroy, C. J., Manning, D. W. P., Rosemond, A. D., Sinsabaugh, R. L., Swan, C. M., Webster, J. R., and Zeglin, Y. H. (2017). Global synthesis of the temperature sensitivity of leaf litter breakdown in streams and rivers. Global Change Biology 23, 3064–3075.
Global synthesis of the temperature sensitivity of leaf litter breakdown in streams and rivers.Crossref | GoogleScholarGoogle Scholar |

Frainer, A., Jabiol, J., Gessner, M. O., Bruder, A., Chauvet, E., and McKie, B. G. (2016). Stoichiometric imbalances between detritus and detritivores are related to shifts in ecosystem functioning. Oikos 125, 861–871.
Stoichiometric imbalances between detritus and detritivores are related to shifts in ecosystem functioning.Crossref | GoogleScholarGoogle Scholar |

Gessner, M. O., and Chauvet, E. (1994). Importance of stream microfungi in controlling breakdown rates of leaf litter. Ecology 75, 1807–1817.
Importance of stream microfungi in controlling breakdown rates of leaf litter.Crossref | GoogleScholarGoogle Scholar |

Gessner, M. O., Swan, C. M., Dang, C. K., Mckie, B. G., Bardgett, R. D., Wall, D. H., and Häettenschwiler, S. (2010). Diversity meets decomposition. Trends in Ecology & Evolution 25, 372–380.
Diversity meets decomposition.Crossref | GoogleScholarGoogle Scholar |

Giné-Rosias, M. F. G. (1979). Determinação espectrofotométrica simultânea de nitrato e nitrito em águas e solos por injeção de fluxo contínuo. M.Sc. Dissertation, University of São Paulo, Piracicaba, Brazil.

Gingerich, R. T., and Anderson, J. T. (2011). Litter decomposition in created and reference wetlands in West Virginia, USA. Wetlands Ecology and Management 19, 449–458.
Litter decomposition in created and reference wetlands in West Virginia, USA.Crossref | GoogleScholarGoogle Scholar |

Goering, H. K., and Van Soest, P. J. (1970). ‘Forage Fiber Analyses (Apparatus, Reagent, Procedures and some Applications). USDA Agriculture Handbook.’ (US Agricultural Research Service: Washington, DC, USA.)

Goma-Tchimbakala, J., and Bernhard-Reversat, F. (2006). Comparison of litter dynamics in three plantations of an indigenous timber-tree species (Terminalia superba) and a natural tropical forest in Mayombe, Congo. Forest Ecology and Management 229, 304–313.
Comparison of litter dynamics in three plantations of an indigenous timber-tree species (Terminalia superba) and a natural tropical forest in Mayombe, Congo.Crossref | GoogleScholarGoogle Scholar |

Gonçalves, J. F., de Souza Rezende, R., França, J., and Callisto, M. (2012). Invertebrate colonisation during leaf processing of native, exotic and artificial detritus in a tropical stream. Marine and Freshwater Research 63, 428–439.
Invertebrate colonisation during leaf processing of native, exotic and artificial detritus in a tropical stream.Crossref | GoogleScholarGoogle Scholar |

Gonçalves, A. L., Graça, M. A., and Canhoto, C. (2013a). The effect of temperature on leaf decomposition and diversity of associated aquatic hyphomycetes depends on the substrate. Fungal Ecology 6, 546–553.
The effect of temperature on leaf decomposition and diversity of associated aquatic hyphomycetes depends on the substrate.Crossref | GoogleScholarGoogle Scholar |

Gonçalves, J. F., Martins, R. T., de Paiva Ottoni, B. M., and Couceiro, S. R. M. (2013b). Uma visão sobre a decomposição foliar em sistemas aquáticos brasileiros. In ‘Insetos Aquáticos na Amazônia Brasileira: Taxonomia, Biologia e Ecologia’. (Eds N. Hamada, J. L. Nessimian, and R. B. Querino.) pp. 89–116. (INPA: Manaus, Brazil.)

Graça, M. A. S., and Zimmer, M. (2005). Leaf toughness. In ‘Methods to Study Litter Decomposition: a Practical Guide’. (Eds M. A. S. Graça, F. Bärlocher, and M. O. Gessner.) pp. 109–113. (Springer: Dordrecht, Netherlands.)

Griffiths, N. A., Tank, J. L., Royer, T. V., Rosi-Marshall, E. J., Whiles, M. R., Chambers, C. P., Frauendorf, T. C., and Evans-White, M. A. (2009). Rapid decomposition of maize detritus in agricultural headwater streams. Ecological Applications 19, 133–142.
Rapid decomposition of maize detritus in agricultural headwater streams.Crossref | GoogleScholarGoogle Scholar |

Hättenschwiler, S., and Gasser, P. (2005). Soil animals alter plant litter diversity effects on decomposition. Proceedings of the National Academy of Sciences of the United States of America 102, 1519–1524.
Soil animals alter plant litter diversity effects on decomposition.Crossref | GoogleScholarGoogle Scholar |

Hättenschwiler, S., and Jørgensen, H. B. (2010). Carbon quality rather than stoichiometry controls litter decomposition in a tropical rain forest. Journal of Ecology 98, 754–763.
Carbon quality rather than stoichiometry controls litter decomposition in a tropical rain forest.Crossref | GoogleScholarGoogle Scholar |

Hossain, M. Z., Okubo, A., and Sugiyama, S. I. (2010). Effects of grassland species on decomposition of litter and soil microbial communities. Ecological Research 25, 255–261.
Effects of grassland species on decomposition of litter and soil microbial communities.Crossref | GoogleScholarGoogle Scholar |

Ihnen, K., and Zimmer, M. (2008). Selective consumption and digestion of litter microbes by Porcellio scaber (Isopoda: Oniscidea). Pedobiologia 51, 335–342.
Selective consumption and digestion of litter microbes by Porcellio scaber (Isopoda: Oniscidea).Crossref | GoogleScholarGoogle Scholar |

Kennedy, K., and El‐Sabaawi, R. W. (2017). A global meta‐analysis of exotic versus native leaf decay in stream ecosystems. Freshwater Biology 62, 977–989.
A global meta‐analysis of exotic versus native leaf decay in stream ecosystems.Crossref | GoogleScholarGoogle Scholar |

Lapola, D. M., Martinelli, L. A., Peres, C. A., Ometto, J. P. H. B., Ferreira, M. E., Nobre, C. A., Aguiar, A. P. D., Bustamante, M. M. C., Cardoso, M. F., Costa, M. H., Joly, C. A., Leite, C. C., Moutinho, P., Sampaio, G., Strassburg, B. B. N., and Vieira, I. C. G. (2014). Pervasive transition of the Brazilian land-use system Nature Climate Change 4, 27–35.
Pervasive transition of the Brazilian land-use systemCrossref | GoogleScholarGoogle Scholar |

Larsen, S., Muehlbauer, J. D., and Marti, E. (2016). Resource subsidies between stream and terrestrial ecosystems under global change. Global Change Biology 22, 2489–2504.
Resource subsidies between stream and terrestrial ecosystems under global change.Crossref | GoogleScholarGoogle Scholar |

Lima, M. A., Gomez, L. D., Steele-King, C. G., Simister, R., Bernardinelli, O. D., Carvalho, M. A., Rezende, C. A., Labate, C. A., Azevedo, E. R., Mcqueen-Mason, S. J., and Polikarpov, I. (2014). Evaluating the composition and processing potential of novel sources of Brazilian biomass for sustainable biorenewables production. Biotechnology for Biofuels 7, 10.
Evaluating the composition and processing potential of novel sources of Brazilian biomass for sustainable biorenewables production.Crossref | GoogleScholarGoogle Scholar |

Loranger, G., Ponge, J. F., Imbert, D., and Lavelle, P. (2002). Leaf decomposition in two semi-evergreen tropical forests: influence of litter quality. Biology and Fertility of Soil 35, 247–252.
Leaf decomposition in two semi-evergreen tropical forests: influence of litter quality.Crossref | GoogleScholarGoogle Scholar |

Manzoni, S., Jackson, R. B., Trofymow, J. A., and Porporato, A. (2008). The global stoichiometry of litter nitrogen mineralization. Science 321, 684–686.
The global stoichiometry of litter nitrogen mineralization.Crossref | GoogleScholarGoogle Scholar |

Maranhão, C. M. A., Silva, C. C. F., Bonomo, P., and Pires, A. J. V. (2009). Produção e composição químico-bromatológica de duas cultivares de braquiária adubadas com nitrogênio e sua relação com o índice SPAD. Acta Scientiarum. Animal Sciences 31, 117–122.
Produção e composição químico-bromatológica de duas cultivares de braquiária adubadas com nitrogênio e sua relação com o índice SPAD.Crossref | GoogleScholarGoogle Scholar |

Masese, F. O., Abrantes, K. G., Gettel, G. M., Bouillon, S., Irvine, K., and McClain, M. E. (2015). Are large herbivores vectors of terrestrial subsidies for riverine food webs? Ecosystems 18, 686.
Are large herbivores vectors of terrestrial subsidies for riverine food webs?Crossref | GoogleScholarGoogle Scholar |

Medeiros, G. G. (2016). Efeito da exclusão experimental de vertebrados na decomposição de três tipos de plantas sob diferentes coberturas de solo no parque estadual da serra do mar-núcleo Santa Virgínia. Ph.D. Dissertation, Universidade de São Paulo, Brazil.

Menninger, H. L., and Palmer, M. A. (2007). Herbs and grasses as an allochthonous resource in open-canopy headwater streams. Freshwater Biology 52, 1689–1699.
Herbs and grasses as an allochthonous resource in open-canopy headwater streams.Crossref | GoogleScholarGoogle Scholar |

Meschede, D. K., Carbonari, C. A., Velini, E. D., Trindade, M. L. B., and Gomes, G. L. G. C. (2011). Efeitos do glyphosate nos teores de lignina, celulose e fibra em Brachiaria decumbens. Revista Brasileira de Herbicidas 10, 57–63.
Efeitos do glyphosate nos teores de lignina, celulose e fibra em Brachiaria decumbens.Crossref | GoogleScholarGoogle Scholar |

Moraes, E. H. B. K., Paulino, M. F., Zervoudakis, J. T., Valadares Filho, S. D. C., and Moraes, K. D. (2005). Avaliação qualitativa da pastagem diferida de Brachiaria decumbens Stapf., sob pastejo, no período da seca, por intermédio de três métodos de amostragem. Revista Brasileira de Zootecnia 34, 30–35.
Avaliação qualitativa da pastagem diferida de Brachiaria decumbens Stapf., sob pastejo, no período da seca, por intermédio de três métodos de amostragem.Crossref | GoogleScholarGoogle Scholar |

Moulton, T. P., Magalhaes-Fraga, S. A., Brito, E. F., and Barbosa, F. A. (2010). Macroconsumers are more important than specialist macroinvertebrate shredders in leaf processing in urban forest streams of Rio de Janeiro, Brazil. Hydrobiologia 638, 55–66.
Macroconsumers are more important than specialist macroinvertebrate shredders in leaf processing in urban forest streams of Rio de Janeiro, Brazil.Crossref | GoogleScholarGoogle Scholar |

Olson, J. S. (1963). Energy storage and the balance of producers and decomposers in ecological systems. Ecology 44, 322–331.
Energy storage and the balance of producers and decomposers in ecological systems.Crossref | GoogleScholarGoogle Scholar |

Peixoto, A. L., and Lírio, E. J. (2015). Monimiaceae. In ‘Lista de Espécies da Flora do Brasil’. (Jardim Botanico do Rio de Janeiro: Rio de Janeiro, Brazil.) Available at http://floradobrasil.jbrj.gov.br/jabot/floradobrasil/FB10101 [Verified 16 June 2017].

Petersen, R. C., and Cummins, K. W. (1974). Leaf processing in a woodland stream. Freshwater Biology 4, 343–368.
Leaf processing in a woodland stream.Crossref | GoogleScholarGoogle Scholar |

Poff, N. L., Brinson, M. M., and Day, J. W. (2002). Aquatic ecosystems and global climate change. Potential impacts on inland freshwater and coastal wetland ecosystems in the United States. (Pew Center on Global Climate Change: Arlington, VA, USA.) Available at https://www.c2es.org/site/assets/uploads/2002/01/aquatic.pdf [Verified 24 March 2018].

Preston, C. M., Trofymow, J. A., and Flanagan, L. B. (2006). Decomposition, δ13C, and the ‘lignin paradox’. Canadian Journal of Soil Science 86, 235–245.
Decomposition, δ13C, and the ‘lignin paradox’.Crossref | GoogleScholarGoogle Scholar |

Rajashekhar, M., and Kaveriappa, K. M. (2000). Effects of temperature and light on growth and sporulation of aquatic hyphomycetes. Hydrobiologia 441, 149–153.
Effects of temperature and light on growth and sporulation of aquatic hyphomycetes.Crossref | GoogleScholarGoogle Scholar |

Ribeiro, A. F., Messana, J. D., Dian, P. H., Reis, R. A., Ruggieri, A. C., Malheiros, E. B., and Berchielli, T. T. (2014). Chemical composition, in vitro digestibility and gas production of Brachiaria managed under different forage allowances. Italian Journal of Animal Science 13, 3034.
Chemical composition, in vitro digestibility and gas production of Brachiaria managed under different forage allowances.Crossref | GoogleScholarGoogle Scholar |

Riet-Correa, B., Castro, M. B., Lemos, R. A., Riet-Correa, G., Mustafa, V., and Riet-Correa, F. (2011). Brachiaria spp. poisoning of ruminants in Brazil. Pesquisa Veterinaria Brasileira 31, 183–192.
Brachiaria spp. poisoning of ruminants in Brazil.Crossref | GoogleScholarGoogle Scholar |

Rodrigues, A. L., Sampaio, I. B., Carneiro, J. C., Tomich, T. R., and Martins, R. G. (2004). Degradabilidade in situ da matéria seca de forrageiras tropicais obtidas em diferentes épocas de corte. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 56, 658–664.
Degradabilidade in situ da matéria seca de forrageiras tropicais obtidas em diferentes épocas de corte.Crossref | GoogleScholarGoogle Scholar |

Ruzicka, J., and Hansen, E. H. (1981). ‘Flow Injection Analysis’, 2nd edn. (Wiley Interscience: New York, NY, USA.)

Sales, M. A., Gonçalves, J. F., Dahora, J. S., and Medeiros, A. O. (2015). Influence of leaf quality in microbial decomposition in a headwater stream in the Brazilian Cerrado: a 1-year study. Microbial Ecology 69, 84–94.
Influence of leaf quality in microbial decomposition in a headwater stream in the Brazilian Cerrado: a 1-year study.Crossref | GoogleScholarGoogle Scholar |

Santos, E. D. G., Paulino, M. F., Queiroz, D. S., Valadares Filho, S. C., Fonseca, D. D., and Lana, R. P. (2004). Avaliação de pastagem diferida de Brachiaria decumbens Stapf.: 1. Características químico-bromatológicas da forragem durante a seca. Revista Brasileira de Zootecnia 33, 203–213.
Avaliação de pastagem diferida de Brachiaria decumbens Stapf.: 1. Características químico-bromatológicas da forragem durante a seca.Crossref | GoogleScholarGoogle Scholar |

Saunders, D. L., Meeuwig, J. J., and Vincent, A. C. J. (2002). Freshwater protected areas: strategies for conservation. Conservation Biology 16, 30–41.
Freshwater protected areas: strategies for conservation.Crossref | GoogleScholarGoogle Scholar |

Scheirs, J., De Bruyn, L., and Verhagen, R. (2001). A test of the C3–C4 hypothesis with two grass miners. Ecology 82, 410–421.

Schweizer, M., Fear, J., and Cadisch, G. (1999). Isotopic (13C) fractionation during plant residue decomposition and its implications for soil organic matter studies. Rapid Communications in Mass Spectrometry 13, 1284–1290.
Isotopic (13C) fractionation during plant residue decomposition and its implications for soil organic matter studies.Crossref | GoogleScholarGoogle Scholar |

Setzer, J. (1966). ‘Atlas Climático e Ecológico do Estado de São Paulo.’ (Comissão, Interestadual da Bacia Paraná-Uruguai: São Paulo, Brazil.)

Silva, A. M., Casatti, L., Álvares, C. A., Leite, A. M., Martinelli, L. A., and Durrant, S. F. (2007). Soil loss and habitat quality in streams of a meso-scale river basin. Scientia Agrícola 64, 336–343.
Soil loss and habitat quality in streams of a meso-scale river basin.Crossref | GoogleScholarGoogle Scholar |

Silva-Junior, E. F., Moulton, T. P., Boëchat, I. G., and Gücker, B. (2014). Leaf decomposition and ecosystem metabolism as functional indicators of land use impacts on tropical streams. Ecological Indicatiors 36, 195–204.
Leaf decomposition and ecosystem metabolism as functional indicators of land use impacts on tropical streams.Crossref | GoogleScholarGoogle Scholar |

Solórzano, L. (1969). Determination of ammonia in natural waters by the phenolhypochlorite method. Limnology and Oceanography 14, 799–801.

Sousa Neto, E., Carmo, J. B., Keller, M., Martins, S. C., Alves, L. F., Vieira, S. A., Piccolo, M. C., Camargo, P., Couto, H. T. Z., and Joly, C. A. (2011). Soil–atmosphere exchange of nitrous oxide, methane and carbon dioxide in a gradient of elevation in the coastal Brazilian Atlantic Forest. Biogeosciences 8, 733–742.
Soil–atmosphere exchange of nitrous oxide, methane and carbon dioxide in a gradient of elevation in the coastal Brazilian Atlantic Forest.Crossref | GoogleScholarGoogle Scholar |

Sparovek, G., Berndes, G., Barretto, A. G. O. P., and Klug, I. L. F. (2012). The revision of the Brazilian Forest Act: increased deforestation or a historic step towards balancing agricultural development and nature conservation? Environmental Science & Policy 16, 65–72.
The revision of the Brazilian Forest Act: increased deforestation or a historic step towards balancing agricultural development and nature conservation?Crossref | GoogleScholarGoogle Scholar |

Talbot, J. M., and Treseder, K. K. (2012). Interactions among lignin, cellulose, and nitrogen drive litter chemistry–decay relationships. Ecology 93, 345–354.
Interactions among lignin, cellulose, and nitrogen drive litter chemistry–decay relationships.Crossref | GoogleScholarGoogle Scholar |

Talbot, J. M., Yelle, D. J., Nowick, J., and Treseder, K. K. (2012). Litter decay rates are determined by lignin chemistry. Biogeochemistry 108, 279–295.
Litter decay rates are determined by lignin chemistry.Crossref | GoogleScholarGoogle Scholar |

Tank, J. L., Rosi-Marshall, E. J., Griffiths, N. A., Entrekin, S. A., and Stephen, M. L. (2010). A review of allochthonous organic matter dynamics and metabolism in streams. Journal of the North American Benthological Society 29, 118–146.
A review of allochthonous organic matter dynamics and metabolism in streams.Crossref | GoogleScholarGoogle Scholar |

Trevisan, A., and Hepp, L. U. (2007). Dinâmica de componentes químicos vegetais e fauna associada ao processo de decomposição de espécies arbóreas em um riacho do norte do Rio Grande do Sul. Neotropical Biology and Conservation 2, 54–60.

Velásquez, P. A. T., Berchielli, T. T., Reis, R. A., Rivera, A. R., Dian, P. H. M., and Teixeira, I. A. M. D. A. (2010). Composição química, fracionamento de carboidratos e proteínas e digestibilidade in vitro de forrageiras tropicais em diferentes idades de corte. Revista Brasileira de Zootecnia 39, 1206–1213.
Composição química, fracionamento de carboidratos e proteínas e digestibilidade in vitro de forrageiras tropicais em diferentes idades de corte.Crossref | GoogleScholarGoogle Scholar |

Wanderley, M. D. G. L., Shepherd, G. J., Melhem, T. S. A., Giulietti, A. M., Martins, S. E., and Kirizawa, M. (2002). Chapter 2 – Mollinedia schottiana. In ‘Flora Fanerogâmica do Estado de São Paulo. Vol 4’. pp. 185–194. (RiMa: São Paulo, Brazil.)