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Patterns of litter inputs, hyphomycetes and invertebrates in a Brazilian savanna stream: a process of degradative succession

Published online by Cambridge University Press:  11 October 2019

Renan de Souza Rezende*
Affiliation:
Program of Postgraduate in Environmental Sciences, Universidade Comunitária Regional de Chapecó, Avenida Senador Attílio Fontana, 591-E – Egapi. CEP 89809-000, Chapecó – SC, Brazil
Adriana Oliveira Medeiros
Affiliation:
Department of Botany Institute of Biology, Federal University of Bahia, CEP 40170-110 Salvador, Bahia, Brazil
José Francisco Gonçalves Júnior
Affiliation:
Department of Ecology, Institute of Biology, University of Brasilia, CEP 70910-900 Brasília, Federal District, Brazil
Maria João Feio
Affiliation:
MARE (Marine and Environmental Sciences Centre) & Department of Life Sciences, University of Coimbra, CEP 3004-517 Coimbra, Portugal
Elves Pereira Gusmão
Affiliation:
Department of Botany Institute of Biology, Federal University of Bahia, CEP 40170-110 Salvador, Bahia, Brazil Department of Zoology, Institute of Biology, Federal University of Bahia, CEP 40170-110 Salvador, Bahia, Brazil
Victor Ângelo de Andrade Gomes
Affiliation:
Department of Zoology, Institute of Biology, Federal University of Bahia, CEP 40170-110 Salvador, Bahia, Brazil
Adolfo Calor
Affiliation:
Department of Zoology, Institute of Biology, Federal University of Bahia, CEP 40170-110 Salvador, Bahia, Brazil
Juliana dos Santos Dahora Almeida
Affiliation:
Department of Botany Institute of Biology, Federal University of Bahia, CEP 40170-110 Salvador, Bahia, Brazil
*
*Author for correspondence: Renan de Souza Rezende, Email: [email protected]

Abstract

Litter breakdown is an important ecological process at the bottom of food webs in streams. Previous studies have been based only on a temporal interval of a single season, thus ignoring seasonal variation in litter input and community structure. We investigated organic matter input in a Brazilian savanna stream and the influence of its associated hyphomycetes on the invertebrate community. Organic matter input was sampled monthly and the leaves submitted to decomposition experiments. There were lower breakdown rates and higher invertebrate species richness and abundance during the dry season, which reached their maximum in July due to low stream discharge. Invertebrate composition was best explained by hyphomycetes (mainly by Flagellospora curvula and Anguillospora filiformis). Hyphomycetes have the capacity to degrade complex compounds of litter and to rapidly absorb nutrients by growing branched filaments, thus making the leaves more favourable for consumption by invertebrates. Shredder abundance was negatively related to litter richness, indicating possible species-specific relationships. We observed a sequential process with increased leaf litter input promoting an increase in hyphomycetes biomass, which in turn favoured invertebrate density.

Type
Research Article
Copyright
© Cambridge University Press 2019 

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References

Literature cited

Abelho, M (2001) From litterfall to breakdown in streams: a review. Scientific World Journal 1, 656680.CrossRefGoogle ScholarPubMed
Alvim, EAC, Medeiros, AO, Rezende, RS and Gonçalves, JF Jr (2015) Leaf breakdown in a natural open tropical stream. Journal of Limnology 74, 248260.Google Scholar
Bambi, P, Rezende, RS, Feio, MJ, Leite, GFM, Alvin, EAC, Quintão, JMB, Araújo, F and Gonçalves, JF Jr (2016) Temporal and spatial patterns in inputs and stock of organic matter in savannah streams of central Brazil. Ecosystems 20, 757768.CrossRefGoogle Scholar
Bärlocher, F (1992) Research on aquatic hyphomycetes: historical background and overview. In Bärlocher, F (ed.), The Ecology of Aquatic Hyphomycetes. Berlin: Springer-Verlag, pp. 115.CrossRefGoogle Scholar
Bärlocher, F (2005) Sporulation by aquatic hyphomycetes. In Graça, MAS, Bärlocher, F and Gessner, MO (eds), Methods to Study Litter Decomposition: A Practical Guide. Dordrecht: Springer, pp. 185187.CrossRefGoogle Scholar
Blanchet, FG, Legendre, P and Borcard, D (2008) Forward selection of explanatory variables. Ecology 89, 26232632.CrossRefGoogle ScholarPubMed
Borcard, D and Legendre, P (2002) All-scale spatial analysis of ecological data by means of principal coordinates of neighbour matrices. Ecological Modelling 153, 5168.CrossRefGoogle Scholar
Borcard, D and Legendre, P (2012) Is the Mantel correlogram powerful enough to be useful in ecological analysis? A simulation study. Ecology 93, 14731481.CrossRefGoogle ScholarPubMed
Boyero, L, Pearson, RG, Dudgeon, D, Graça, MS, Gessner, MO, Albarino, RJ, Ferreira, V et al. (2011) Global distribution of a key trophic guild contrasts with common latitudinal diversity patterns. Ecology 92, 18391848.CrossRefGoogle ScholarPubMed
Boyero, L, Pearson, RG, Swan, CM, Hui, C, Albariño, RJ, Arunachalam, M, Callisto, M et al. (2015) Latitudinal gradient of nestedness and its potential drivers in stream detritivores. Ecography 38, 949955.CrossRefGoogle Scholar
Brittain, JE and Sartori, M (2009) Ephemeroptera. In Resh, VH and Cardé, R (eds), Encyclopedia of Insects, 2nd edn. New York, NY: Academic Press, pp. 328333.CrossRefGoogle Scholar
Chauvet, E and Suberkropp, K (1998) Temperature and sporulation of aquatic hyphomycetes. Applied and Environmental Microbiology 64, 15221525.Google ScholarPubMed
Crawley, MJ (2007) The R Book. Chichester: Wiley, pp. 511526.CrossRefGoogle Scholar
Cummins, K, Merritt, R and Andrade, P (2005) The use of invertebrate functional groups to characterize ecosystem attributes in selected streams and rivers in south Brazil. Studies on Neotropical Fauna and Environment 40, 6989.CrossRefGoogle Scholar
Dray, S, Legendre, P and Peres-Neto, PR (2006) Spatial modelling: a comprehensive framework for principal coordinate analysis of neighbour matrices (PCNM). Ecological Modelling 196, 483493.CrossRefGoogle Scholar
Dufrêne, M and Legendre, P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecological Monographs 67, 345366.Google Scholar
Durães, L, Roque, FO, Siqueira, T, Santos, AM, Borges, MA and Rezende, RS (2016) Simulating the role of connectivity in shaping stream insect metacommunities under colonization cycle dynamics. Ecological Modelling 334, 1926.CrossRefGoogle Scholar
Feio, MJ, Almeida, SFP, Craveiro, SC and Calado, ANJ (2007). Diatoms and macroinvertebrates provide consistent and complementary information on environmental quality. Fundamental and Applied Limnology 169, 247258. Stuttgart: Schweizerbart’sche Verlagsbuchhandlung.Google Scholar
Ferreira, V and Graça, MAS (2006) Do invertebrate activity and current velocity affect fungal assemblage structure in leaves? International Review of Hydrobiology 91, 114.CrossRefGoogle Scholar
Ferreira, V, Encalada, AC and Graça, MAS (2012) Effects of litter diversity on decomposition and biological colonization of submerged litter in temperate and tropical streams. Freshwater Science 31, 945962.CrossRefGoogle Scholar
Ferreira, V, Castagneyrol, B, Koricheva, J, Gulis, V, Chauvet, E and Graça, MAS (2014) A meta-analysis of the effects of nutrient enrichment on litter decomposition in streams. Biological Reviews of the Cambridge Philosophical Society 90, 669688.CrossRefGoogle ScholarPubMed
Ferreira, V, Castela, J, Rosa, P, Tonin, AM, Boyero, L and Graça, MAS (2016) Aquatic hyphomycetes, benthic macroinvertebrates and leaf litter decomposition in streams naturally differing in riparian vegetation. Aquatic Ecology 50, 711725.CrossRefGoogle Scholar
Ferreira, WR, Ligeiro, R, Macedo, DR, Hughes, RM, Kaufmann, PR, Oliveira, LG and Callisto, M (2014) Importance of environmental factors for the richness and distribution of benthic macroinvertebrates in tropical headwater streams. Freshwater Science 33, 860871.CrossRefGoogle Scholar
Flindt, MR and Lillebø, AI (2005) Determination of total nitrogen and phosphorus in leaf litter. In Graça, MAS, Bärlocher, F and Gessner, MO (eds), Methods to Study Litter Decomposition: A Practical Guide. Dordrecht: Springer, pp. 5359.CrossRefGoogle Scholar
França, JS, Gregorio, RS, De Paula, JD, Gonçalves, JF Jr, Ferreira, FA and Callisto, M (2009) Composition and dynamics of allochthonous organic matter inputs and benthic stock in a Brazilian stream. Marine and Freshwater Research 60, 990998.CrossRefGoogle Scholar
Gonçalves, JF Jr and Callisto, M (2013) Organic-matter dynamics in the riparian zone of a tropical headwater stream in Southern Brasil. Aquatic Botany 109, 813.CrossRefGoogle Scholar
Gonçalves, JF Jr, Couceiro, SRM, Rezende, RS, Martins, RT, Ottoni-Boldrini, BMP, Campos, CM, Silva, JO and Hamada, N (2016) Factors controlling leaf litter breakdown in Amazonian streams. Hydrobiologia 792, 195207.CrossRefGoogle Scholar
Graça, MAS, Ferreira, V, Canhoto, C, Encalada, AC, Guerrero-Bolaño, F, Wantzen, KM and Boyero, L (2015) A conceptual model of litter breakdown in low order streams. International Review of Hydrobiology 100, 112.CrossRefGoogle Scholar
Graça, MAS, Hyde, K and Chauvet, E (2016) Aquatic hyphomycetes and litter decomposition in tropical–subtropical low order streams. Fungal Ecology 19, 182189.CrossRefGoogle Scholar
Gregório, RS, Valentin, G, Ferreira, FA, Aleixo, LA, França, JS, Gonçalves, JF Jr, Callisto, M, Batista, ML, Gaspar, RO and Rodello, CM (2007) Contribuição foliar alóctone de espécies vegetais num córrego de 2a ordem na Estação Ambiental de Peti (CEMIG) – MG. Revista Brasileira de Biociências 5, 3335.Google Scholar
Hamada, N, Nessimian, JL and Querino, RB (2014) Insetos aquáticos na Amazônia brasileira: taxonomia, biologia e ecologia. Manaus: Editora INPA. 724 pp.Google Scholar
Hatje, V, Pedreira, RMA, Rezende, CE, Schettini, CAF, Souza, GC, Marin, DC and Hackspacher, PC (2017) The environmental impacts of one of the largest tailing dam failures worldwide. Scientific Reports 7, 10706.CrossRefGoogle ScholarPubMed
Hauer, FR and Benke, AC (1987) Influence of temperature and river hydrograph on black fly growth rates in a subtropical blackwater river. Journal of the North American Benthological Society 6, 251261.CrossRefGoogle Scholar
Hepp, LU, Landeiro, VL and Melo, AS (2012) Experimental assessment of the effects of environmental factors and longitudinal position on alpha and beta diversities of aquatic insects in a Neotropical stream. International Review of Hydrobiology 97, 157167.CrossRefGoogle Scholar
Hepp, LU and Melo, AS (2013) Dissimilarity of stream insect assemblages: effects of multiple scales and spatial distances. Hydrobiologia 703, 239246.CrossRefGoogle Scholar
Lamouroux, N, Dolédec, S and Gayraud, S (2004) Biological traits of stream macroinvertebrate communities: effects of microhabitat, reach, and basin filters. Journal of the North American Benthological Society 23, 449466.2.0.CO;2>CrossRefGoogle Scholar
Legendre, P and Legendre, L (1998) Numerical Ecology. English Edition. London: Elsevier. 852 pp.Google Scholar
Leite, GFM, Silva, FTC, Navarro, FKSP, Rezende, RS and Gonçalves, JF Jr (2016) Leaf litter input and electrical conductivity may change density of Phylloicus sp. (Trichoptera: Calamoceratidae) in a Brazilian savannah stream. Acta Limnologica Brasiliensia 28, e12.CrossRefGoogle Scholar
Martins, RT, Melo, AS, Gonçalves, JF Jr, Campos, CM and Hamada, N (2016) Effects of climate change on leaf breakdown by microorganisms and the shredder Phylloicus elektoros (Trichoptera: Calamoceratidae). Hydrobiologia 789, 3144.CrossRefGoogle Scholar
Medeiros, AO, Pascoal, C and Graça, MAS (2009) Diversity and activity of aquatic fungi under low oxygen conditions. Freshwater Biology 54, 142149.CrossRefGoogle Scholar
Navarro, FKSP and Gonçalves, JF Jr (2017) Effect of leaf decomposition stage and water temperature on fragmentation activity of a shredder invertebrate species in lotic ecosystems. Iheringia Série Zoologia 107, e2017017.CrossRefGoogle Scholar
Niu, S and Dudgeon, D (2011) The influence of flow and season upon leaf-litter breakdown in monsoonal Hong Kong streams. Hydrobiologia 663, 205215.CrossRefGoogle Scholar
Oksanen, J, Blanchet, FG, Kindt, R, Legendre, P, Minchin, PR, O’Hara, RB, Simpson, GL, Solymos, P, Stevens, H and Wagner, H (2013) Community Ecology Package: Ordination, Diversity and Dissimilarities. Version 2.0-8.Google Scholar
Peres-Neto, PR, Legendre, P, Dray, S and Borcard, D (2006) Variation partitioning of species data matrices: estimation and comparison of fractions. Ecology 87, 26142625.CrossRefGoogle ScholarPubMed
Rezende, RS, Gonçalves, JF Jr and Petrucio, MM (2010) Leaf breakdown and invertebrate colonization of Eucalyptus grandis (Myrtaceae) and Hirtella glandulosa (Chrysobalanaceae) in two Neotropical lakes. Acta Limnologica Brasiliensia 22, 2334.CrossRefGoogle Scholar
Rezende, RS, Petrucio, MM and Gonçalves, JF Jr (2014a) The effects of spatial scale on breakdown of leaves in a tropical watershed. PLoS ONE 9, e97072.CrossRefGoogle Scholar
Rezende, RS, Santos, AM, Henke-Oliveira, C and Gonçalves, JF Jr (2014b) Effects of spatial and environmental factors on a benthic macroinvertebrate community. Zoologia (Curitiba) 31, 426434.CrossRefGoogle Scholar
Rezende, RS, Leite, GFM, De-Lima, AKS, Silva-Filho, LAB, Chaves, CVC, Prette, ACH, Freitas, JS and Gonçalves, JF Jr (2015) Effects of density and predation risk on leaf litter processing by Phylloicus sp. Austral Ecology 40, 693700.CrossRefGoogle Scholar
Rezende, RS, Graça, MAS, Santos, AM, Medeiros, AO, Santos, PF, Nunes, YR and Gonçalves, JF Jr (2016) Organic matter dynamics in a tropical gallery forest in a grassland landscape. Biotropica 48, 301310.CrossRefGoogle Scholar
Rezende, RS, Correia, PRS, Gonçalves, JF Jr and Santos, AM (2017a) Organic matter dynamics in a savanna transition riparian zone: input of plant reproductive parts increases leaf breakdown process. Journal of Limnology 76, 502511.Google Scholar
Rezende, RS, Sales, MA, Hurbath, F, Roque, N, Gonçalves, JF Jr and Medeiros, AO (2017b) Effect of plant richness on the dynamics of coarse particulate organic matter in a Brazilian savannah stream. Limnologica – Ecology and Management of Inland Waters 63, 5764.CrossRefGoogle Scholar
Rezende, RS, Santos, AM, Medeiros, AO and Gonçalves, JF Jr (2017c) Temporal leaf litter breakdown in a tropical riparian forest with an open canopy. Limnetica 36, 445459.Google Scholar
Rosa, J, Ferreira, V, Canhoto, C and Graça, MAS (2013) Combined effects of water temperature and nutrients concentration on periphyton respiration – implications of global change. International Review of Hydrobiology 98, 1423.CrossRefGoogle Scholar
Rueda-Delgado, G, Wantzen, KM and Tolosa, MB (2006) Leaf-litter decomposition in an Amazonian floodplain stream: effects of seasonal hydrological changes. Journal of the North American Benthological Society 25, 233249.CrossRefGoogle Scholar
Sales, MA, Goncalves, JF Jr, Dahora, JS and Medeiros, AO (2015) Influence of leaf quality in microbial decomposition in a headwater stream in the Brazilian cerrado: a 1-year study. Microbial Ecology 69, 8494.CrossRefGoogle Scholar
Santos-Fonseca, AL, Bianchini, I, Pimenta, CMM, Soares, CBP and Mangiavacchi, N (2012) The flow velocity as driving force for decomposition of leaves and twigs. Hydrobiologia 703, 5967.CrossRefGoogle Scholar
Siqueira, T, Bini, LM, Roque, FO and Cottenie, K (2012) A metacommunity framework for enhancing the effectiveness of biological monitoring strategies. PLoS ONE 7, e43626.CrossRefGoogle ScholarPubMed
Sridhar, KR and Sudheep, NM (2010) Diurnal fluctuation of spores of freshwater hyphomycetes in two tropical streams. Mycosphere 1, 89101.Google Scholar
Tank, JL, Rosi-Marshall, EJ, Griffiths, NA, Entrekin, SA and Stephen, ML (2010) A review of allochthonous organic matter dynamics and metabolism in streams. Journal of the North American Benthological Society 29, 118146.CrossRefGoogle Scholar
Tonin, AM, Gonçalves, JF Jr, Bambi, P, Couceiro, SRM, Lorrane, A, Leite, GFM, Lemes-Silva, AL, Lisboa, LK et al. (2017) Plant litter dynamics in the forest-stream interface: precipitation is a major control across tropical biomes. Scientific Reports 7, 10799.CrossRefGoogle ScholarPubMed
Wantzen, KM and Mathooko, JM (2008) Organic matter processing in tropical streams. In Dudgeon, D (ed.), Tropical Stream Ecology. Amsterdam: Elsevier, pp. 4364.CrossRefGoogle Scholar