Advertisement

Aquatic Ecology

, Volume 53, Issue 2, pp 163–178 | Cite as

The longer the conditioning, the better the quality? The effects of leaf conditioning time on aquatic hyphomycetes and performance of shredders in a tropical stream

  • Cinthia G. Casotti
  • Walace P. KifferJr.
  • Larissa C. Costa
  • Pâmela Barbosa
  • Marcelo S. MorettiEmail author
Article

Abstract

In this study, we aimed to evaluate the effects of leaf conditioning time on aquatic hyphomycete assemblages and the performance of invertebrate shredders. We hypothesized that post-conditioning effects, i.e., that phase in which leaf nutritional quality no longer increase or even decline, occur late in tropical streams. Consequently, leaf quality would increase monotonously with fungal colonization and leaves conditioned for longer periods would promote higher growth and survival of shredders than leaves conditioned for shorter periods. Leaves of the tree species Miconia chartacea were conditioned for different time periods (7, 15, 30, 45 and 60 days) in an Atlantic Forest stream (Southeast Brazil) and offered to larvae of the caddisfly shredder Triplectides gracilis in food preference and monodietary experiments. Leaf toughness, total phenolics and tannins decreased with conditioning time. The leaves were poorly colonized by aquatic fungi, and sporulation rates were low. The larvae consumed leaves from all conditioning periods, but those conditioned for 30 days were preferred over those conditioned during the initial periods (7 and 15 days). In the monodietary trials, larval survival was high in all treatments, and the larvae fed leaves conditioned for 7 and 15 days had high growth rates. Our results show that leaves conditioned for longer periods did not constitute a better food resource for shredders, which did not corroborate the proposed hypothesis. The influence of leaf conditioning time on detritivore-mediated decomposition may be more relevant in streams with a high diversity of aquatic hyphomycetes that may colonize the leaves more effectively.

Keywords

Fungal biomass Sporulation rates Food preferences Growth rates Triplectides gracilis Atlantic Forest streams 

Notes

Acknowledgements

We are grateful to Adolfo Calor for Triplectides species identification. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001. The Fundação de Amparo à Pesquisa e Inovação do Espírito Santo (FAPES) provided M.M. with a research fellowship (T.O. # 0264/2016). Two anonymous reviewers provided insightful comments on a previous version of this manuscript.

Supplementary material

10452_2019_9680_MOESM1_ESM.docx (79 kb)
Supplementary material 1 (DOCX 78 kb)

References

  1. Abelho M, Cressa C, Graça MAS (2005) Microbial biomass, respiration, and decomposition of Hura crepitans L. (Euphorbiaceae) leaves in a tropical stream. Biotropica 37:397–402.  https://doi.org/10.1111/j.1744-7429.2005.00052.x CrossRefGoogle Scholar
  2. Albariño RJ, Villanueva VD, Canhoto C (2008) The effect of sunlight on leaf litter quality reduces growth of the shredder Klapopteryx kuscheli. Freshw Biol 53:1881–1889.  https://doi.org/10.1111/j.1365-2427.2008.02016.x CrossRefGoogle Scholar
  3. Alvim EACC, de Oliveira MA, Rezende RS, Gonçalves JF (2015) Small leaf breakdown in a Savannah headwater stream. Limnologica 51:131–138.  https://doi.org/10.1016/j.limno.2014.10.005 CrossRefGoogle Scholar
  4. Arce Funck J, Bec A, Perrière F et al (2015) Aquatic hyphomycetes: a potential source of polyunsaturated fatty acids in detritus-based stream food webs. Fungal Ecol 13:205–210.  https://doi.org/10.1016/j.funeco.2014.09.004 CrossRefGoogle Scholar
  5. Arroita M, Flores L, Larrañaga A et al (2018) Hydrological contingency: drying history affects aquatic microbial decomposition. Aquat Sci 80:1–12.  https://doi.org/10.1007/s00027-018-0582-3 CrossRefGoogle Scholar
  6. Arsuffi TL, Suberkropp K (1986) Growth of two stream caddisflies (Trichoptera) on leaves colonized by different fungal species. J North Am Benthol Soc 5:297–305.  https://doi.org/10.2307/1467482 CrossRefGoogle Scholar
  7. Bärlocher F (1980) Leaf-eating invertebrates as competitors of aquatic hyphomycetes. Oecologia 47:303–306.  https://doi.org/10.1007/BF00398521 CrossRefGoogle Scholar
  8. Bärlocher F (1985) The role of fungi in the nutrition of stream invertebrates. Bot J Linn Soc 91:83–94CrossRefGoogle Scholar
  9. Bärlocher F (2005) Sporulation by aquatic hyphomycetes. In: Graça MAS, Bärlocher F, Gessner MO (eds) Methods to study litter decomposition: a practical guide. Springer, Dordrecht, p 329Google Scholar
  10. Bärlocher F (2016) Aquatic hyphomycetes in a changing environment. Fungal Ecol 19:14–27.  https://doi.org/10.1016/j.funeco.2015.05.005 CrossRefGoogle Scholar
  11. Bärlocher F, Graça MAS (2005) Total phenolics. In: Graça MAS, Barlocher F, Gessner MO (eds) Methods to study litter decomposition: a practical guide, 1st edn. Springer, Dordrecht, pp 97–100CrossRefGoogle Scholar
  12. Bärlocher F, Kendrick B (1973) Fungi and food preferences of Gammarus pseudolimnaeus. Arch Hydrobiol 72:501–516Google Scholar
  13. Bärlocher F, Kendrick B (1975) Leaf-conditioning by microorganisms. Oecologia 20:359–362.  https://doi.org/10.1007/BF00345526 CrossRefGoogle Scholar
  14. Bärlocher F, Sridhar KR (2014) Association of animals and fungi in leaf decomposition. In: Gareth Jones EB, Hyde KD, Pang K-L (eds) Freshwater fungi and fungal-like organisms, 1st edn. De Gruyter, Berlin, pp 413–433Google Scholar
  15. Biasi C, Cerezer C, Santos S (2016) Biological colonization and leaf decomposition in a subtropical stream. Ecol Austral 26:189–199Google Scholar
  16. Biasi C, Graça MAS, Santos S, Ferreira V (2017) Nutrient enrichment in water more than in leaves affects aquatic microbial litter processing. Oecologia 184:555–568.  https://doi.org/10.1007/s00442-017-3869-5 CrossRefGoogle Scholar
  17. Boyero L, Barmuta LA, Ratnarajah L et al (2012) Effects of exotic riparian vegetation on leaf breakdown by shredders: a tropical–temperate comparison. Freshw Sci 31:296–303.  https://doi.org/10.1899/11-103.1 CrossRefGoogle Scholar
  18. Boyero L, Graça MAS, Tonin AM et al (2017) Riparian plant litter quality increases with latitude. Sci Rep 7:10562.  https://doi.org/10.1038/s41598-017-10640-3 CrossRefGoogle Scholar
  19. Canhoto CM, Graça MAS (2008) Interactions between fungi and stream invertebrates: back to the future. In: Sridhar KR, Bärlocher F, Hyde K (eds) Novel techniques and ideas in mycology. Hong Kong University Press, Hong KongGoogle Scholar
  20. Canhoto C, Gonçalves AL, Bärlocher F (2016) Biology and ecological functions of aquatic hyphomycetes in a warming climate. Fungal Ecol 19:201–218.  https://doi.org/10.1016/j.funeco.2015.09.011 CrossRefGoogle Scholar
  21. Casotti CG, Kiffer WP Jr, Moretti MS (2015a) Leaf traits induce the feeding preference of a shredder of the genus Triplectides Kolenati, 1859 (Trichoptera) in an Atlantic Forest stream, Brazil: a test with native and exotic leaves. Aquat Insects 36:43–52.  https://doi.org/10.1080/01650424.2014.1001399 CrossRefGoogle Scholar
  22. Casotti CG, Kiffer WPJ, Costa LC et al (2015b) Assessing the importance of riparian zones conservation for leaf decomposition in streams. Braz J Nat Conserv 13:178–182.  https://doi.org/10.1016/j.ncon.2015.11.011 CrossRefGoogle Scholar
  23. Chung N, Suberkropp K (2008) Influence of shredder feeding and nutrients on fungal activity and community structure in headwater streams. Fundam Appl Limnol/Arch Hydrobiol 173:35–46.  https://doi.org/10.1127/1863-9135/2008/0173-0035 CrossRefGoogle Scholar
  24. Chung N, Suberkropp K (2009a) Effects of aquatic fungi on feeding preferences and bioenergetics of Pycnopsyche gentilis (Trichoptera: Limnephilidae). Hydrobiologia 630:257–269.  https://doi.org/10.1007/s10750-009-9820-y CrossRefGoogle Scholar
  25. Chung N, Suberkropp K (2009b) Contribution of fungal biomass to the growth of the shredder, Pycnopsyche gentilis (Trichoptera: Limnephilidae). Freshw Biol 54:2212–2224.  https://doi.org/10.1111/j.1365-2427.2009.02260.x CrossRefGoogle Scholar
  26. Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143.  https://doi.org/10.1111/j.1442-9993.1993.tb00438.x CrossRefGoogle Scholar
  27. Cornut J, Ferreira V, Gonçalves AL et al (2015) Fungal alteration of the elemental composition of leaf litter affects shredder feeding activity. Freshw Biol 60:1755–1771.  https://doi.org/10.1111/fwb.12606 CrossRefGoogle Scholar
  28. Cummins KW, Petersen RC, Howard FO (1973) The utilization of leaf litter by stream detritivores. Ecology 54:336–345CrossRefGoogle Scholar
  29. Duarte S, Bärlocher F, Pascoal C, Cássio F (2016) Biogeography of aquatic hyphomycetes: current knowledge and future perspectives. Fungal Ecol 19:169–181.  https://doi.org/10.1016/j.funeco.2015.06.002 CrossRefGoogle Scholar
  30. Encalada AC, Calles J, Ferreira V et al (2010) Riparian land use and the relationship between the benthos and litter decomposition in tropical montane streams. Freshw Biol 55:1719–1733.  https://doi.org/10.1111/j.1365-2427.2010.02406.x Google Scholar
  31. Ferreira V, Chauvet E (2012) Changes in dominance among species in aquatic hyphomycete assemblages do not affect litter decomposition rates. Aquat Microb Ecol 66:1–11.  https://doi.org/10.3354/ame01556 CrossRefGoogle Scholar
  32. Ferreira V, Encalada AC, Graça MAS (2012) Effects of litter diversity on decomposition and biological colonization of submerged litter in temperate and tropical streams. Freshw Sci 31:945–962.  https://doi.org/10.1899/11-062.1 CrossRefGoogle Scholar
  33. Ferreira V, Castela J, Rosa P et al (2016) Aquatic hyphomycetes, benthic macroinvertebrates and leaf litter decomposition in streams naturally differing in riparian vegetation. Aquat Ecol 50:711–725.  https://doi.org/10.1007/s10452-016-9588-x CrossRefGoogle Scholar
  34. Fiuza PO, Cantillo-Pérez T, Gulis V, Gusmão LFP (2017) Ingoldian fungi of Brazil: some new records and a review including a checklist and a key. Phytotaxa 306:171–200.  https://doi.org/10.11646/phytotaxa.306.3.1 CrossRefGoogle Scholar
  35. Flindt MR, Lillebø AI (2005) Determination of total nitrogen and phosphorus in leaf litter. In: Graça MAS, Bärlocher F, Gessner MO (eds) Methods to study litter decomposition: a practical guide, 1st edn. Springer, Dordrecht, pp 53–59CrossRefGoogle Scholar
  36. Gessner MO (2005) Ergosterol as a measure of fungal biomass. In: Graça MAS, Bärlocher F, Gessner MO (eds) Methods to study litter decomposition: a practical guide. Springer, Berlin, pp 189–195CrossRefGoogle Scholar
  37. Gessner MO, Chauvet E, Dobson M (1999) A perspective on leaf litter breakdown in streams. Oikos 85:377–384CrossRefGoogle Scholar
  38. Ghate SD, Sridhar KR (2015) A new technique to monitor conidia of aquatic hyphomycetes in streams using latex-coated slides. Mycology 6:161–167.  https://doi.org/10.1080/21501203.2015.1110209 CrossRefGoogle Scholar
  39. Gomes PP, Medeiros AO, Gonçalves Júnior JF (2016) The replacement of native plants by exotic species may affect the colonization and reproduction of aquatic hyphomycetes. Limnologica 59:124–130.  https://doi.org/10.1016/j.limno.2016.05.005 CrossRefGoogle Scholar
  40. Gonçalves JFJ, França JS, Medeiros AO et al (2006) Leaf breakdown in a tropical stream. Int Rev Hydrobiol 91:164–177.  https://doi.org/10.1002/iroh.200510826 CrossRefGoogle Scholar
  41. Gonçalves JF, Graça MAS, Callisto M (2007) Litter decomposition in a Cerrado savannah stream is retarded by leaf toughness, low dissolved nutrients and a low density of shredders. Freshw Biol 52:1440–1451.  https://doi.org/10.1111/j.1365-2427.2007.01769.x CrossRefGoogle Scholar
  42. Gonçalves AL, Chauvet E, Barlocher F et al (2014) Top-down and bottom-up control of litter decomposers in streams. Freshw Biol 59:2172–2182.  https://doi.org/10.1111/fwb.12420 CrossRefGoogle Scholar
  43. Graça MAS (2001) The role of invertebrates on leaf litter decomposition in streams: a review. Int Rev Hydrobiol 86:383–394.  https://doi.org/10.1002/1522-2632(200107)86:4/5%3C383::AID-IROH383%3E3.0.CO;2-D CrossRefGoogle Scholar
  44. Graça MAS, Bärlocher F (2005) Radial diffusion assay for tannins. In: Graça MAS, Bärlocher F, Gessner MO (eds) Methods to study litter decomposition: a practical guide. Springer, Berlin, pp 101–105CrossRefGoogle Scholar
  45. Graça MAS, Cressa C (2010) Leaf quality of some tropical and temperate tree species as food resource for stream shredders. Int Rev Hydrobiol 95:27–41.  https://doi.org/10.1002/iroh.200911173 CrossRefGoogle Scholar
  46. Graça MAS, Zimmer M (2005) Leaf toughness. In: Graça MAS, Barlocher F, Gessner MO (eds) Methods to study litter decomposition: a practical guide, 1st edn. Springer, Dordrecht, pp 121–125CrossRefGoogle Scholar
  47. Graça MAS, Cressa C, Gessner MO et al (2001) Food quality, feeding preferences, survival and growth of shredders from temperate and tropical streams. Freshw Biol 46:947–957.  https://doi.org/10.1046/j.1365-2427.2001.00729.x CrossRefGoogle Scholar
  48. Graça MAS, Ferreira V, Canhoto C et al (2015) A conceptual model of litter breakdown in low order streams. Int Rev Hydrobiol 100:1–12.  https://doi.org/10.1002/iroh.201401757 CrossRefGoogle Scholar
  49. Graça MAS, Hyde K, Chauvet E (2016) Aquatic hyphomycetes and litter decomposition in tropical: subtropical low order streams. Fungal Ecol 19:182–189.  https://doi.org/10.1016/j.funeco.2015.08.001 CrossRefGoogle Scholar
  50. Gulis V, Suberkropp K (2003a) Effect of inorganic nutrients on relative contributions of fungi and bacteria to carbon flow from submerged decomposing leaf litter. Microb Ecol 45:11–19.  https://doi.org/10.1007/s00248-002-1032-1 CrossRefGoogle Scholar
  51. Gulis V, Suberkropp K (2003b) Interaction between stream fungi and bacteria associated with decomposing leaf litter at different levels of nutrient availability. Aquat Microb Ecol 30:149–157.  https://doi.org/10.3354/ame030149 CrossRefGoogle Scholar
  52. Gulis V, Suberkropp KF (2007) Fungi: biomass, production, and sporulation of aquatic hyphomycetes. In: Hauer FR, Lamberti GA (eds) Methods in stream ecology, 2nd edn. Elsevier, Amsterdam, pp 311–325CrossRefGoogle Scholar
  53. Gulis V, Marvanová L, Descals E (2005) An illustrated key to the common temperate species of aquatic hyphomycetes. In: Graça MAS, Bärlocher F, Gessner MO (eds) Methods to study litter decomposition: a practical guide. Springer, Berlin, pp 153–167CrossRefGoogle Scholar
  54. Harrop BL, Marks JC, Watwood ME (2009) Early bacterial and fungal colonization of leaf litter in Fossil Creek, Arizona. J North Am Benthol Soc 28:383–396.  https://doi.org/10.1899/08-068.1 CrossRefGoogle Scholar
  55. Harrop-Archibald H, Didham RK, Standish RJ et al (2016) Mechanisms linking fungal conditioning of leaf litter to detritivore feeding activity. Soil Biol Biochem 93:119–130.  https://doi.org/10.1016/j.soilbio.2015.10.021 CrossRefGoogle Scholar
  56. Hieber M, Gessner MO (2002) Contribution of stream detrivores, fungi, and bacteria to leaf breakdown based on biomass estimates. Ecology 83:1026–1038CrossRefGoogle Scholar
  57. Hutchings MJ, Booth KD, Waite S (1991) Comparison of survivorship by the logrank test: criticisms and alternatives. Ecology 72:2290–2293.  https://doi.org/10.2307/1941579 CrossRefGoogle Scholar
  58. Ingold CT (1975) An illustrated guide to aquatic and water-borne hyphomycetes (fungi imperfecti) with notes on their biology. Freshwater Biological Association n. 30, Ambleside, U.K.Google Scholar
  59. Jabiol J, Chauvet E (2012) Fungi are involved in the effects of litter mixtures on consumption by shredders. Freshw Biol 57:1667–1677.  https://doi.org/10.1111/j.1365-2427.2012.02829.x CrossRefGoogle Scholar
  60. Jabiol J, Bruder A, Gessner MO et al (2013) Diversity patterns of leaf-associated aquatic hyphomycetes along a broad latitudinal gradient. Fungal Ecol 6:439–448.  https://doi.org/10.1016/j.funeco.2013.04.002 CrossRefGoogle Scholar
  61. Jenkins CC, Suberkropp K (1995) The influence of water chemistry on the enzymatic degradation of leaves in streams. Freshw Biol 33:245–253.  https://doi.org/10.1111/j.1365-2427.1995.tb01165.x CrossRefGoogle Scholar
  62. Kiffer WP Jr, Mendes F, Rangel JV et al (2016) Size-mass relationships and the influence of larval and case size on the consumption rates of Triplectides sp. (Trichoptera, Leptoceridae). Fundam Appl Limnol/Arch Hydrobiol 188:73–81.  https://doi.org/10.1017/CBO9781107415324.004 CrossRefGoogle Scholar
  63. Kiffer WP Jr, Mendes F, Casotti CG et al (2018) Exotic Eucalyptus leaves are preferred over tougher native species but affect the growth and survival of shredders in an Atlantic Forest stream (Brazil). PLoS ONE 13:1–17.  https://doi.org/10.1371/journal.pone.0190743 CrossRefGoogle Scholar
  64. Komínková D, Kuehn KA, Büsing N et al (2000) Microbial biomass, growth, and respiration associated with submerged litter of Phragmites australis decomposing in a littoral reed stand of a large lake. Aquat Microb Ecol 22:271–282.  https://doi.org/10.3354/ame022271 CrossRefGoogle Scholar
  65. Krauss G, Solé M, Krauss G et al (2011) Fungi in freshwaters: ecology, physiology and biochemical potential. Fed Eur Microbiol Soc 35:620–651.  https://doi.org/10.1111/j.1574-6976.2011.00266.x Google Scholar
  66. Leite-Rossi LA, Saito VS, Cunha-Santino MB, 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.  https://doi.org/10.1007/s10750-015-2626-1 CrossRefGoogle Scholar
  67. Lisboa LK, Silva ALL, Siegloch AE et al (2015) Temporal dynamics of allochthonous coarse particulate organic matter in a subtropical Atlantic rainforest Brazilian stream. Mar Freshw Res.  https://doi.org/10.1071/mf14068 Google Scholar
  68. Medeiros AO, Callisto M, Graça MAS et al (2015) Microbial colonisation and litter decomposition in a Cerrado stream are limited by low dissolved nutrient concentrations. Limnetica 34:283–292Google Scholar
  69. Mendes F, Kiffer WP Jr, Moretti MS (2017) Structural and functional composition of invertebrate communities associated with leaf patches in forest streams: a comparison between mesohabitats and catchments. Hydrobiologia.  https://doi.org/10.1007/s10750-017-3249-5 Google Scholar
  70. Nawawi A (1985) Aquatic hyphomycetes and other water-borne fungi from Malaysia. Malay Nat J 39:75–134Google Scholar
  71. Pascoal C, Cássio F (2004) Contribution of fungi and bacteria to leaf litter decomposition in a polluted river. Appl Environ Microbiol 70:5266–5273.  https://doi.org/10.1128/AEM.70.9.5266 CrossRefGoogle Scholar
  72. Pérez J, Descals E, Pozo J (2012) Aquatic hyphomycete communities associated with decomposing alder leaf litter in reference headwater streams of the Basque Country (northern Spain). Microb Ecol 64:279–290.  https://doi.org/10.1007/s00248-012-0022-1 CrossRefGoogle Scholar
  73. Pérez J, Martínez A, Descals E, Pozo J (2018) Responses of aquatic hyphomycetes to temperature and nutrient availability: a cross-transplantation experiment. Microb Ecol 76:328–339.  https://doi.org/10.1007/s00248-018-1148-6 CrossRefGoogle Scholar
  74. Peterson CH, Renaud PE (1989) Analysis of feeding preference experiments. Oecologia 80:82–86.  https://doi.org/10.1007/BF00789935 CrossRefGoogle Scholar
  75. Ramesha C, Lakshmi H, Kumari SS et al (2012) Nutrigenetic screening strains of the mulberry silkworm, Bombyx mori, for nutritional efficiency. J Insect Sci 12:1–17.  https://doi.org/10.1673/031.012.1501 CrossRefGoogle Scholar
  76. Ratnarajah L, Barmuta LA (2009) The effects of leaf toughness on feeding preference by two Tasmanian shredders. Hydrobiologia 636:173–178.  https://doi.org/10.1007/s10750-009-9946-y CrossRefGoogle Scholar
  77. Ribblett SG, Palmer MA, Coats DW (2005) The importance of bacterivorous protists in the decomposition of stream leaf litter. Freshw Biol 50:516–526.  https://doi.org/10.1111/j.1365-2427.2005.01338.x CrossRefGoogle Scholar
  78. Rodrigues J, Michelin DC, Rinaldo D et al (2008) Antimicrobial activity of Miconia species (Melastomataceae). J Med Food 11:120–126.  https://doi.org/10.1089/jmf.2007.557 CrossRefGoogle Scholar
  79. Sales MA, Gonçalves JF, Dahora JS, Medeiros AO (2014) Influence of leaf quality in microbial decomposition in a headwater stream in the Brazilian Cerrado: a 1-year study. Microb Ecol 69:84–94.  https://doi.org/10.1007/s00248-014-0467-5 CrossRefGoogle Scholar
  80. Schoenlein-Crusius IH, Moreira CG, Bicudo DDC (2009) Aquatic hyphomycetes in the Parque Estadual das Fontes do Ipiranga - PEFI, São Paulo, Brazil. Rev Bras Bot 32:411–426.  https://doi.org/10.1590/S0100-84042009000300003 CrossRefGoogle Scholar
  81. Schoenlein-Crusius IH, Moreira CG, Takahashi JP, Gomes EPC (2014) Riqueza dos fungos ingoldianos e aquáticos facultativos do Parque Municipal do Ibirapuera, São Paulo, SP, Brasil. Hoehnea 41:61–76.  https://doi.org/10.1590/2236-8906-24/2018 CrossRefGoogle Scholar
  82. Singh N (1982) Cellulose decomposition by some tropical aquatic hyphomycetes. Trans Br Mycol Soc 79:560–561.  https://doi.org/10.1016/S0007-1536(82)80059-4 CrossRefGoogle Scholar
  83. Suberkropp K (1992) Aquatic hyphomycete communities. In: Carrol GC, Wicklow DT (eds) The fungal community, its organization and role in the ecosystem, 2nd edn. Marcel Dekker, New York, pp 729–747Google Scholar
  84. Suberkropp K (2001) Fungal growth, production, and sporulation during leaf decomposition in two streams. Appl Environ Microbiol 67:5063–5068.  https://doi.org/10.1128/AEM.67.11.5063 CrossRefGoogle Scholar
  85. Suberkropp K, Klug MJ (1980) The maceration of deciduous leaf litter by aquatic hyphomycetes. Can J Bot 58:1025–1031.  https://doi.org/10.1139/b80-126 CrossRefGoogle Scholar
  86. Suberkropp K, Gulis V, Rosemond AD, Benstead JP (2010) Ecosystem and physiological scales of microbial responses to nutrients in a detritus-based stream: results of a 5-year continuous enrichment. Limnol Oceanogr 55:149–160.  https://doi.org/10.4319/lo.2010.55.1.0149 CrossRefGoogle Scholar
  87. Tonin AM, Hepp LU, Restello RM, Gonçalves JF Jr (2014) Understanding of colonization and breakdown of leaves by invertebrates in a tropical stream is enhanced by using biomass as well as count data. Hydrobiologia 740:79–88.  https://doi.org/10.1007/s10750-014-1939-9 CrossRefGoogle Scholar
  88. Tonin AM, Gonçalves JF, Bambi P et al (2017) Plant litter dynamics in the forest-stream interface: precipitation is a major control across tropical biomes. Sci Rep 7:10799.  https://doi.org/10.1038/s41598-017-10576-8 CrossRefGoogle Scholar
  89. Vannote RL, Minshall GW, Cummins KW et al (1980) The river continuum concept. Can J Fish Aquat Sci 37:130–137.  https://doi.org/10.1139/f80-017 CrossRefGoogle Scholar
  90. Waldbauer GP (1968) The consumption and utilization of food by insects. Adv Insect Phys 5:229–288.  https://doi.org/10.1016/S0065-2806(08)60230-1 CrossRefGoogle Scholar
  91. Wallace JB, Webster JR, Cuffney TF (1982) Stream detritus dynamics: regulation by invertebrate consumers. Oecologia 53:197–200CrossRefGoogle Scholar
  92. Webster JR, Benfield EF (1986) Vascular plant breakdown in freshwater ecosystems. Annu Rev Ecol Syst 17:567–594CrossRefGoogle Scholar
  93. Yoshioka PM (2008) Misidentification of the Bray-Curtis similarity index. Mar Ecol Prog Ser 368:309–310.  https://doi.org/10.3354/meps07728 CrossRefGoogle Scholar
  94. Zar JH (2010) Biostatistical analysis, 5th edn. Pearson Prentice-Hall, Upper Saddle RiverGoogle Scholar
  95. Zemek J, Marvanová L, Kuniak L, Kadlečíková B (1985) Hydrolytic enzymes in aquatic hyphomycetes. Folia Microbiol (Praha) 30:363–372.  https://doi.org/10.1007/BF02927592 CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Laboratory of Aquatic Insect EcologyUniversidade Vila VelhaVila VelhaBrazil
  2. 2.Graduate Program in Ecosystem EcologyUniversidade Vila VelhaVila VelhaBrazil

Personalised recommendations