C3 and C4 plant leaf breakdown and assimilation by aquatic macroinvertebrates in streams of the Brazilian Atlantic Forest
Fernanda G. Augusto A B , Aline F. Figueiredo A , Plinio B. Camargo A , Luciana D. Coletta A , Edmar A. Mazzi A and Luiz 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, CEP 13416-000, Piracicaba, SP, Brazil.
B Corresponding author. Email: fernandagaudio@gmail.com
Marine and Freshwater Research 71(7) 814-823 https://doi.org/10.1071/MF18430
Submitted: 8 April 2019 Accepted: 8 August 2019 Published: 12 November 2019
Abstract
The breakdown of allochthonous plants is of great importance in providing energy and nutrients in streams. In this regard, shredder macroinvertebrates play an important role in decomposing organic matter. Changes in land use strongly influence the type of material entering a stream, which ultimately affects the food chain dependent on this material. This study compared the decay of C3 (Mollinedia schottiana) and C4 (Brachiaria brizantha) plants in the montane Atlantic Forest of Brazil using litterbag experiments in two streams draining watersheds of different land uses. Concomitantly, we investigated the colonisation and assimilation of these plant detritus by aquatic macroinvertebrates. The breakdown of C4 plants in the forest stream was faster than that of C3 plants; however, aquatic macroinvertebrates did not assimilate the C4 carbon. These results support other studies that have shown a greater abundance of shredders in montane tropical streams (lower temperature) than in lowland streams. Moreover, the findings of this study support the view that changes in land use alter the structure of the benthic community, and that these changes can alter the leaf breakdown process.
Additional keywords: aquatic invertebrates, land use changes, leaf decomposition, organic matter processing, shredders.
References
Alves, L. F., Vieira, S. A., Scaranello, M. A., Camargo, P. B., Santos, F. A. M., Joly, C. A., and Martinelli, L. A. (2010). Forest structure and live aboveground biomass variation along an elevational gradient of tropical Atlantic moist forest (Brazil). Forest Ecology and Management 260, 679–691.| Forest structure and live aboveground biomass variation along an elevational gradient of tropical Atlantic moist forest (Brazil).Crossref | GoogleScholarGoogle Scholar |
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 |
Barbehenn, R. V., Chen, Z., Karowe, D. N., and Spickard, A. (2004). 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 |
Bertaso, T. R. N., Spies, M. R., Kotzian, C. B., and Flores, M. L. T. (2015). Effects of forest conversion on the assemblages’ structure of aquatic insects in subtropical regions. Revista Brasileira de Entomologia 59, 43–49.
| Effects of forest conversion on the assemblages’ structure of aquatic insects in subtropical regions.Crossref | GoogleScholarGoogle Scholar |
Boyero, L., Ramírez, A., Dudgeon, D., and Pearson, R. G. (2009). Are tropical streams really different? Journal of the North American Benthological Society 28, 397–403.
| Are tropical streams really different?Crossref | GoogleScholarGoogle Scholar |
Boyero, L., Pearson, R. G., Dudgeon, D., Ferreira, V., Graça, M. A. S., Gessner, M. O., Boulton, A. J., Chauvet, E., Yule, C. M., Albarinho, R. J., Ramirez, A., Helson, J. E., Callisto, M., Arunachalam, M., Chará, J., Figueroa, R., Mathooko, J. M., Gonçalves, J. F., Moretti, M. S., Chará-Serna, A. M., Davies, J. N., Encalada, A., Lamothe, S., Buria, L. M., Castela, J., Cornejo, A., Li, A. O. Y., M’Erimba, C., Villanueva, V. D., Zúñiga, M. C., Swan, C. M., and Barmuta, L. A. (2012). Global patterns of stream detritivore distribution: implications for biodiversity loss in changing climates. Global Ecology and Biogeography 21, 134–141.
| Global patterns of stream detritivore distribution: implications for biodiversity loss in changing climates.Crossref | GoogleScholarGoogle Scholar |
Boyero, L., Pearson, R. G., Hui, C., Gessner, M. O., Pérez, J., Alexandrou, M. A., Graça, M. A. S., Cardinale, B. J., Albariño, R. J., Arunachalam, M., Barmuta, L. A., Boulton, A .J., Bruder, A., Callisto, M., Chauvet, E., Death, R. G., Dudgeon, D., Encalada, A. C., Ferreira, V., Figueroa, R., Flecker, A. S., Gonçalves, J. F., Helson, J., Iwata, T., Jinggut, T., Mathooko, J., Mathuriau, C., M'Erimba, C., Moretti, M. S., Pringle, C. M., Ramírez, A., Ratnarajah, L., Rincon, J., and Yule, C. M. (2016). Biotic and abiotic variables influencing plant litter breakdown in streams: a global study. Proceedings of the Royal Society of London – B. Biological Sciences 283, 20152664.
| Biotic and abiotic variables influencing plant litter breakdown in streams: a global study.Crossref | GoogleScholarGoogle Scholar |
Brannstrom, C., and Oliveira, A. M. S. (2000). Human modification of stream valleys in the western plateau of São Paulo, Brazil: implications for environmental narratives and management. Land Degradation & Development 11, 535–548.
| Human modification of stream valleys in the western plateau of São Paulo, Brazil: implications for environmental narratives and management.Crossref | GoogleScholarGoogle Scholar |
Carpenter, S. R., Stanley, E. H., and Vander Zanden, M. J. (2011). State of the world’s freshwater ecosystems: physical, chemical, and biological changes. Annual Review of Environment and Resources 36, 75–99.
| State of the world’s freshwater ecosystems: physical, chemical, and biological changes.Crossref | GoogleScholarGoogle Scholar |
Caswell, H., Reed, F., Stephenson, S. N., and Werner, P. A. (1973). Photosynthetic pathways and selective herbivory: a hypothesis. American Naturalist 107, 465–480.
| Photosynthetic pathways and selective herbivory: a hypothesis.Crossref | GoogleScholarGoogle Scholar |
Clapcott, J. E., and Bunn, S. E. (2003). Can C4 plants contribute to aquatic food webs of subtropical streams? Freshwater Biology 48, 1105–1116.
| Can C4 plants contribute to aquatic food webs of subtropical streams?Crossref | GoogleScholarGoogle Scholar |
Corbi, J. J., and Trivinho-Strixino, S. (2008). Relationship between sugar cane cultivation and stream macroinvertebrate communities. Brazilian Archives of Biology and Technology 51, 569–579.
| Relationship between sugar cane cultivation and stream macroinvertebrate communities.Crossref | GoogleScholarGoogle Scholar |
de Carvalho, A. P. C., Gücker, B., Brauns, M., and Boëchat, I. G. (2015). High variability in carbon and nitrogen isotopic discrimination of tropical freshwater invertebrates. Aquatic Sciences 77, 307–314.
| High variability in carbon and nitrogen isotopic discrimination of tropical freshwater invertebrates.Crossref | GoogleScholarGoogle Scholar |
Domínguez, E., and Fernández, H. R. (2009). ‘Macroinvertebrados bentónicos sudamericanos: sistemática y biologia’, 1nd edn. (Fundación Miguel Lillo: Tucumán, Argentina.)
Encalada, A. C., Calles, J., Ferreira, V., Canhoto, C. M., and Graça, M. A. S. (2010). Riparian land use and the relationship between the benthos and litter decomposition in tropical montane streams. Freshwater Biology 55, 1719–1733.
| Riparian land use and the relationship between the benthos and litter decomposition in tropical montane streams.Crossref | GoogleScholarGoogle Scholar |
Fellerhoff, C., Voss, M., and Wantzen, K. M. (2003). Stable carbon and nitrogen isotope signatures of decomposing tropical macrophytes. Aquatic Ecology 37, 361–375.
| Stable carbon and nitrogen isotope signatures of decomposing tropical macrophytes.Crossref | GoogleScholarGoogle Scholar |
Figueiredo, A. F., Augusto, F. G., Coletta, L. D., Duarte-Neto, B. P. J., Mazzi, E. A., and Martinelli, L. A. (2018). 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. Marine and Freshwater Research 69, 1397–1407.
| 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.Crossref | GoogleScholarGoogle Scholar |
Fisher, S. G., and Likens, G. E. (1973). Energy flow in Bear Brook, New Hampshire: an integrative approach to stream ecosystem metabolism. Ecological Monographs 43, 421–439.
| Energy flow in Bear Brook, New Hampshire: an integrative approach to stream ecosystem metabolism.Crossref | GoogleScholarGoogle Scholar |
Gonçalves, J. F., Rezende, R. S., Martins, N. M., and Gregório, R. S. (2012). Leaf breakdown in an Atlantic Rain Forest stream. Austral Ecology 37, 807–815.
| Leaf breakdown in an Atlantic Rain Forest stream.Crossref | GoogleScholarGoogle Scholar |
Graça, M. A. S. (2001). The role of invertebrates on leaf litter decomposition in streams – a review. International Review of Hydrobiology 86, 383–393.
| The role of invertebrates on leaf litter decomposition in streams – a review.Crossref | GoogleScholarGoogle Scholar |
Graça, M. A. S., Barlocher, F., and Gessener, M. O. (2005). ‘Methods to Study Litter Decomposition: a Practical Guide’, 1nd edn. (Springer: Dordrecht, Netherlands.)
Hepp, L. U., and Santos, S. (2009). Benthic communities of streams related to different land uses in a hydrographic basin in southern Brazil. Environmental Monitoring and Assessment 157, 305–318.
| Benthic communities of streams related to different land uses in a hydrographic basin in southern Brazil.Crossref | GoogleScholarGoogle Scholar | 18843547PubMed |
Howard-Williams, C., and Junk, W. J. (1976). The decomposition of aquatic macrophytes in the floating meadows of a central Amazonian várzea lake. Biogeographica 7, 115–123.
Kiffer, W. P. (2009). Influência das folhas de Eucalyptus sp. e Coffea arabica sobre a assembléia de invertebrados aquáticos. M.Sc. Thesis, Centro Universitário Vila Velha, Vila Velha, Brazil.
König, R., Hepp, L. U., and Santos, S. (2014). Colonisation of low- and high-quality detritus by benthic macroinvertebrates during leaf breakdown in a subtropical stream. Limnologica 45, 61–68.
| Colonisation of low- and high-quality detritus by benthic macroinvertebrates during leaf breakdown in a subtropical stream.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 system.Crossref | GoogleScholarGoogle Scholar |
Leite-Rossi, L. A., and Trivinho-Strixino, S. (2012). Are sugarcane leaf-detritus well colonized by aquatic macroinvertebrates? Acta Limnologica Brasiliensia 24, 303–313.
| Are sugarcane leaf-detritus well colonized by aquatic macroinvertebrates?Crossref | GoogleScholarGoogle Scholar |
Leite-Rossi, L. A., Saito, V. S., Cunha-Santino, M. B., and Trivinho-Strixino, S. (2016). How does leaf litter chemistry influence its decomposition and colonization by shredder Chironomidae (Diptera) larvae in a tropical stream? Hydrobiologia 771, 119–130.
| How does leaf litter chemistry influence its decomposition and colonization by shredder Chironomidae (Diptera) larvae in a tropical stream?Crossref | GoogleScholarGoogle Scholar |
Li, A. O. Y., Ng, L. C. Y., and Dudgeon, D. (2009). Effects of leaf toughness and nitrogen content on litter breakdown and macroinvertebrates in a tropical stream. Aquatic Sciences 71, 80–93.
| Effects of leaf toughness and nitrogen content on litter breakdown and macroinvertebrates in a tropical stream.Crossref | GoogleScholarGoogle Scholar |
Liao, C., Peng, R., Luo, Y., Zhou, X., Wu, X., Fang, C., Chen, J., and Li, B. (2008). Altered ecosystem carbon and nitrogen cycles by plant invasion: a meta-analysis. New Phytologist 177, 706–714.
| Altered ecosystem carbon and nitrogen cycles by plant invasion: a meta-analysis.Crossref | GoogleScholarGoogle Scholar | 18042198PubMed |
Ligeiro, R., Moretti, M. S., Gonçalves, J. F., and Callisto, M. (2010). What is more important for invertebrate colonization in a stream with low-quality litter inputs: exposure time or leaf species? Hydrobiologia 654, 125–136.
| What is more important for invertebrate colonization in a stream with low-quality litter inputs: exposure time or leaf species?Crossref | GoogleScholarGoogle Scholar |
Lopes, M. P., Martins, R. T., Silveira, L. S., and Alves, R. G. (2015). The leaf breakdown of Picramnia sellowii (Picramniales: Picramniaceae) as index of anthropic disturbances in tropical streams. Brazilian Journal of Biology 75, 846–853.
| The leaf breakdown of Picramnia sellowii (Picramniales: Picramniaceae) as index of anthropic disturbances in tropical streams.Crossref | GoogleScholarGoogle Scholar |
Mann, K. H. (1988). Production and use of detritus in various freshwater, estuarine, and coastal rnarine ecosystems. Limnology and Oceanography 33, 910–930.
Martins, S. C., Sousa Neto, E., Piccolo, M. D. C., Almeida, D. Q. A., Camargo, P. B. D., Do Carmo, J. B., Porder, S., Lins, S. R. M., and Martinelli, L. A. (2015). Soil texture and chemical characteristics along an elevation range in the coastal Atlantic Forest of southeast Brazil. Geoderma Regional 5, 106–116.
| Soil texture and chemical characteristics along an elevation range in the coastal Atlantic Forest of southeast Brazil.Crossref | GoogleScholarGoogle Scholar |
Merritt, R. W., Cummins, K. W., and Berg, M. (2008). ‘An Introduction to the Aquatic Insects of North America’, 4nd edn. (Kendall/Hunt: Dubuque, IO, USA.)
Minshall, G. W. (1967). Role of allochthonous detritus in the trophic structure of a woodland springbrook community. Ecology 48, 139–149.
| Role of allochthonous detritus in the trophic structure of a woodland springbrook community.Crossref | GoogleScholarGoogle Scholar |
Moore, J. W., and Semmens, B. X. (2008). Incorporating uncertainty and prior information into stable isotope mixing models. Ecology Letters 11, 470–480.
| Incorporating uncertainty and prior information into stable isotope mixing models.Crossref | GoogleScholarGoogle Scholar | 18294213PubMed |
Moretti, M. S., Goncalves, J. J. F., Ligeiro, R., and Callisto, M. (2007). Invertebrates colonization on native tree leaves in a neotropical stream (Brazil). International Review of Hydrobiology 92, 199–210.
| Invertebrates colonization on native tree leaves in a neotropical stream (Brazil).Crossref | GoogleScholarGoogle Scholar |
Mortillaro, J. M., Passarelli, C., Abril, G., Hubas, C., Alberic, P., Artigas, L. F., Benedetti, M. F., Thiney, N., Moreira-Turcq, P., Perez, M. A. P., Vidal, L. O., and Meziane, T. (2016). The fate of C4 and C3 macrophyte carbon in central Amazon floodplain waters: insights from a batch experiment. Limnologica 59, 90–98.
| The fate of C4 and C3 macrophyte carbon in central Amazon floodplain waters: insights from a batch experiment.Crossref | GoogleScholarGoogle Scholar |
Moulton, T. P., Magalhães-Fraga, S. A. P., 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 |
Myers, N., Mittermeier, R. A., Mittermeie, C. G., Da Fonseca, G. A. B., and Kent, J. (2000). Biodiversity hotspots for conservation priorities. Nature 403, 853–858.
| Biodiversity hotspots for conservation priorities.Crossref | GoogleScholarGoogle Scholar | 10706275PubMed |
Nelson, D. J., and Scott, D. C. (1962). Role of detritus in the productivity of a rock outcrop community in a piedmont stream. Limnology and Oceanography 7, 396–413.
| Role of detritus in the productivity of a rock outcrop community in a piedmont stream.Crossref | GoogleScholarGoogle Scholar |
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., and Moulton, T. P. (2017). Allochthonous and autochthonous carbon flows in food webs of tropical forest streams. Freshwater Biology 62, 1012–1023.
| Allochthonous and autochthonous carbon flows in food webs of tropical forest streams.Crossref | GoogleScholarGoogle Scholar |
Nessimian, J. L., Venticinque, E. M., Zuanon, J., De Marco, P., Gordo, M., Fidelis, L., D’arc Batista, J., and Juen, L. (2008). Land use, habitat integrity, and aquatic insect assemblages in Central Amazonian streams. Hydrobiologia 614, 117–131.
| Land use, habitat integrity, and aquatic insect assemblages in Central Amazonian streams.Crossref | GoogleScholarGoogle Scholar |
Parreira de Castro, D. M., Reis de Carvalho, D., dos Santos Pompeu, P. D., Moreira, M. Z., Nardoto, G. B., and Callisto, M. (2016). Land use influences niche size and the assimilation of resources by benthic macroinvertebrates in tropical headwater streams. PLoS One 11, e0150527.
| Land use influences niche size and the assimilation of resources by benthic macroinvertebrates in tropical headwater streams.Crossref | GoogleScholarGoogle Scholar | 26934113PubMed |
Pereira, A. L. (2012). Fontes de carbono e nitrogênio para consumidores da Mata Atlântica utilizando-se isótopos estáveis. Ph.D. Thesis, Universidade de São Paulo, Piracicaba, SP, Brazil.
Ramírez, A., and Gutiérrez-Fonseca, P. E. (2014). Functional feeding groups of aquatic insect families in Latin America: a critical analysis and review of existing literature. International Journal of Tropical Biology and Conservation 62, 155–168.
| Functional feeding groups of aquatic insect families in Latin America: a critical analysis and review of existing literature.Crossref | GoogleScholarGoogle Scholar |
Ribeiro, M. C., Metzger, J. P., Martensen, A. C., Ponzoni, F. J., and Hirota, M. M. (2009). The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation 142, 1141–1153.
| The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation.Crossref | GoogleScholarGoogle Scholar |
Santos, I. G. A., and Rodrigues, G. G. (2015). Colonização de macroinvertebrados bentônicos em detritos foliares de um riacho de primeri ordem na Floresta Atlântica do NE brasileiro. Iheringia. Série Zoologia 105, 84–93.
| Colonização de macroinvertebrados bentônicos em detritos foliares de um riacho de primeri ordem na Floresta Atlântica do NE brasileiro.Crossref | GoogleScholarGoogle Scholar |
Saulino, H. H. L., Corbi, J. J., and Trivinho-Strixino, S. (2014). Aquatic insect community structure under the influence of small dams in a stream of the Mogi–Guaçu river basin, state of São Paulo. Brazilian Journal of Biology 74, 79–88.
| Aquatic insect community structure under the influence of small dams in a stream of the Mogi–Guaçu river basin, state of São Paulo.Crossref | GoogleScholarGoogle Scholar |
Siegloch, A. E., Suriano, M., Spies, M., and Fonseca-Gessner, A. (2014). Effect of land use on mayfly assemblages structure in neotropical headwater streams. Anais da Academia Brasileira de Ciências 86, 1735–1747.
| Effect of land use on mayfly assemblages structure in neotropical headwater streams.Crossref | GoogleScholarGoogle Scholar | 25590712PubMed |
Silva-Junior, E. F., and Moulton, T. P. (2011). Ecosystem functioning and community structure as indicators for assessing environmental impacts: leaf processing and macroinvertebrates in Atlantic forest streams. International Review of Hydrobiology 96, 656–666.
| Ecosystem functioning and community structure as indicators for assessing environmental impacts: leaf processing and macroinvertebrates in Atlantic forest streams.Crossref | GoogleScholarGoogle Scholar |
Stock, B. C., and Semmens, B. X. (2016). MixSIAR GUI user manual. Version 3.1. (Scripps Institution of Oceanography, University of California—San Diego: San Diego, CA, USA.) Available at https://github.com/brianstock/MixSIAR/raw/master/Manual/mixsiar_manual.pdf [Verified 2 November 2019].
Suga, C. M., and Tanaka, M. O. (2013). Influence of a forest remnant on macroinvertebrate communities in a degraded tropical stream. Hydrobiologia 703, 203–213.
| Influence of a forest remnant on macroinvertebrate communities in a degraded tropical stream.Crossref | GoogleScholarGoogle Scholar |
Tanaka, M. O., Fernandes, J. de F., Suga, C. M., Hanai, F. Y., and de Souza, A. L. T. (2015). Abrupt change of a stream ecosystem function along a sugarcane–forest transition: integrating riparian and in-stream characteristics. Agriculture, Ecosystems & Environment 207, 171–177.
| Abrupt change of a stream ecosystem function along a sugarcane–forest transition: integrating riparian and in-stream characteristics.Crossref | GoogleScholarGoogle Scholar |
Tonello, G., Loureiro, R. C., Krause, P., Silva, C., Ongaratto, R. M., Sepp, S., Restello, R. M., and Hepp, U. (2014). Colonização de invertebrados durante a decomposição de diferentes detritos vegetais em um riacho subtropical. Brazilian Journal of Biosciences 12, 98–105.
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, Brasil. Neotropical Biology and Conservation 2, 55–60.
Valente-Neto, F., Koroiva, R., Fonseca-Gessner, A. A., and Roque, F. de O. (2015). The effect of riparian deforestation on macroinvertebrates associated with submerged woody debris. Aquatic Ecology 49, 115–125.
| The effect of riparian deforestation on macroinvertebrates associated with submerged woody debris.Crossref | GoogleScholarGoogle Scholar |
Valle, I., Buss, D., and Baptista, D. (2013). The influence of connectivity in forest patches, and riparian vegetation width on stream macroinvertebrate fauna. Brazilian Journal of Biology 73, 231–238.
| The influence of connectivity in forest patches, and riparian vegetation width on stream macroinvertebrate fauna.Crossref | GoogleScholarGoogle Scholar |
Wallace, J. B., Eggert, S. L., Meyer, J. L., and Webster, J. R. (1997). Multiple trophic levels of a forest stream linked to terrestrial litter inputs. Science 277, 102–104.
| Multiple trophic levels of a forest stream linked to terrestrial litter inputs.Crossref | GoogleScholarGoogle Scholar |
Webster, J. R., and Benfield, E. F. (1986). Vascular plant breakdown in freshwater ecosystems. Annual Review of Ecology and Systematics 17, 567–594.
| Vascular plant breakdown in freshwater ecosystems.Crossref | GoogleScholarGoogle Scholar |
Wilson, J., and Hattersley, P. (1989). Anatomical characters and digestibility of leaves of Panicum and other grass genera with C3 and different types of C4 photosynthetic pathway. Australian Journal of Agricultural Research 40, 125.
| Anatomical characters and digestibility of leaves of Panicum and other grass genera with C3 and different types of C4 photosynthetic pathway.Crossref | GoogleScholarGoogle Scholar |
Yule, C. M., Leong, M. Y., Liew, K. C., Ratnarajah, L., Schmidt, S., Wong, H. M., Pearson, R. G., and Boyero, L. (2009). Shredders in Malaysia: abundance and richness are higher in cool upland tropical streams. Journal of the North American Benthological Society 28, 404–415.
| Shredders in Malaysia: abundance and richness are higher in cool upland tropical streams.Crossref | GoogleScholarGoogle Scholar |
