SpringerLink
Log in

Stream environmental conditions are homogenised outside a protected area, but fungal beta diversity remains unchanged

  • Original Article
  • Published:
Mycological Progress Aims and scope Submit manuscript

Abstract

Matter and energy fluxes and ecosystem services in streams rely on fungi associated with leaf litter. However, the species diversity of this microbial group may differ between a protected area and its surroundings. Thus, to understand how beta diversity may depend on the conservation status of an area, we aimed to evaluate the structure and diversity (α, β, and γ) of the aquatic fungal community from a subtropical area and how it is distributed in streams from a protected area and from a farmland area. Hence, we compared eight streams inside with eight streams outside of a protected area. This is one of the first studies testing the biotic homogenisation hypothesis for fungi associated with leaf litter in streams. We found new records of fungal species from a global biodiversity hotspot. The gamma diversity of aquatic fungi was surprisingly high. Our analyses indicated a process of environmental homogenisation of streams outside the national park. Intriguingly, neither α nor β diversity differed between areas. Environmental variables presented large differences, especially regarding nutrients, which influence the aquatic fungal community. Altogether, this national park seems to be effective in protecting the environmental heterogeneity of streams to some extent; however, the national park was likely suffering from pollution, which requires further investigation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  • Akridge RE, Koehn RD (1987) Amphibious hyphomycetes from the San Marcos river in Texas. Mycologia 79:228–233

    Article  Google Scholar 

  • Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM, Sparovek G (2013) Köppen’s climate classification map for Brazil. Meteorol Zeitschrift 22:711–728

    Article  ADS  Google Scholar 

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  • Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62:245–253

    Article  MathSciNet  PubMed  Google Scholar 

  • Anderson MJ, Ellingsen KE, McArdle BH (2006) Multivariate dispersion as a measure of beta diversity. Ecol Lett 9:683–693

    Article  PubMed  Google Scholar 

  • Anderson MJ, Walsh DCI (2013) PERMANOVA, ANOSIM and the Mantel test in the face of heterogeneous dispersions: what null hypothesis are you testing? Ecol Monogr 83:557–574

    Article  Google Scholar 

  • Barbosa FR, Silva SS, Fiuza PO, Gusmão LFP (2011) Conidial fungi from the semi-arid Caatinga biome of Brazil, new species and records for Thozetella. Mycotaxon 115:327–334

    Article  Google Scholar 

  • Bärlocher F (1985) The role of fungi in the nutrition of stream invertebrates. Bot J Linn Soc 91:83–94

    Article  Google Scholar 

  • Bärlocher F (2000) Water-borne conidia of aquatic hyphomycetes: seasonal and yearly patterns in Catamaran Brook, New Brunswick, Canada. Canad J Bot 78:157–167

    Article  Google Scholar 

  • Bärlocher F, Boddy L (2016) Aquatic fungal ecology - how does it differ from terrestrial? Fungal Ecol 19:5–13

    Article  Google Scholar 

  • Bärlocher F, Rosset J (1981) Aquatic hyphomycetes spora of two black forest and two Swiss Jura streams. Trans Br Mycol Soc 76:479–483

    Article  Google Scholar 

  • Barros J, Seena S (2022) Fungi in freshwaters: prioritising aquatic hyphomycetes in conservation goals. Water 14:1–16

    Article  ADS  Google Scholar 

  • Baudoin JM, Guérold F, Felten V, Chauvet E, Wagner P, Rousselle P (2008) Elevated aluminium concentration in acidified headwater streams lowers aquatic hyphomycete diversity and impairs leaf-litter breakdown. Microb Ecol 56:260–269

    Article  CAS  PubMed  ADS  Google Scholar 

  • Baudy P, Zubrod JP, Konschak M, Röder N, Nguyen TH, Schreiner VC, Baschien C, Schulz R, Bundschuh M (2021) Environmentally relevant fungicide levels modify fungal community composition and interactions but not functioning. Environ Pollut 285:117234

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  ADS  Google Scholar 

  • Biasi C, Fontana LE, Restello RM, Hepp LU (2020) Effect of invasive Hoveniadulcis on microbial decomposition and diversity of hyphomycetes in Atlantic forest streams. Fungal Ecol 44:100890

    Article  Google Scholar 

  • Brasil (2006) Decreto de 23 de março de 2006. Cria o Parque Nacional dos Campos Gerais, no Estado do Paraná, e dá outras providências. Publicado no Diário Oficial da União de 24 de março de 2006. Available online at http://www.planalto.gov.br/ccivil_03/_ato2004-2006/2006/dnn/Dnn10796.htm#:~:text=DNN%2010796&text=DECRETO%20DE%2023%20DE%20MARÇO,que%20lhe%20confere%20o%20art. Accessed 01 Feb 2017

  • Cadastro Nacional de Unidades de Conservação (CNUC) do Ministério do Meio Ambiente (2018). Available online at http://www.mma.gov.br/areas-protegidas/cadastro-nacional-de-ucs. Accessed 01 Feb 2018

  • Czeczuga B, Orłowska M (1997) Hyphomycetes fungi in rainwater falling from building roofs. Mycoscience 38:447–450

    Article  Google Scholar 

  • Chan SY, Goh TK, Hyde KD (2000) Ingoldian fungi in Hong Kong. In: Hyde KD, Ho W-H, Pointing SB (eds) Aquatic mycology across the millennium. Fungal Diversity Press p, Hong Kong, pp 89–107

    Google Scholar 

  • Chauvet E (1991) Aquatic hyphomycete distribution in South-Western France. J Biogeogr 18:699–706

    Article  Google Scholar 

  • Cornut J, Ferreira V, Gonçalves AL, Chauvet E, Canhoto C (2015) Fungal alteration of the elemental composition of leaf litter affects shredder feeding activity. Freshw Biol 60:1755–1771

    Article  CAS  Google Scholar 

  • Crawford RH, Carpenter SE, Harmon ME (1990) Communities of filamentous fungi and yeast in decomposing logs of Pseudotsuga menziesii. Mycologia 82:759–765

    Article  Google Scholar 

  • Cruz ACR, Gusmão LFP (2009) Fungos conidiais na Caatinga: espécies associadas ao folhedo. Acta Bot Bras 23:999–1012

    Article  Google Scholar 

  • Cruz ACR, Gusmão LFP (2009) Fungos conidiais na Caatinga: espécies lignícolas. Acta Bot Bras 23:1133–1144

    Article  Google Scholar 

  • Cruz ACR, Marques MFO, Gusmão LFP (2007) Fungos anamórficos (Hyphomycetes) da Chapada Diamantina: novos registros para o Estado da Bahia e Brasil. Acta Bot Bras 21:847–855

    Article  Google Scholar 

  • Danger M, Gessner MO, Bärlocher F (2016) Ecological stoichiometry of aquatic fungi: current knowledge and perspectives. Fungal Ecol 19:100–111

    Article  Google Scholar 

  • Dudley N (2008) Guidelines for applying protected area management categories. IUCN, Gland Switzerland

    Book  Google Scholar 

  • Esteves FA, Gonçalves JFJr, (2011) Etapas do metabolismo aquático. In: Esteves FA (ed) Fundamentos de Limnologia. Interciência p, Rio de Janeiro, pp 119–124

    Google Scholar 

  • Fellows CS, Valett HM, Dahm CN, Mulholland PJ, Thomas SA (2006) Coupling nutrient uptake and energy flow in headwater streams. Ecosystems 9:788–804

    Article  CAS  Google Scholar 

  • Fiuza PO, Gusmão LFP (2013) Ingoldian fungi from the semi-arid Caatinga biome of Brazil. Mycosphere 4:559–565

    Article  Google Scholar 

  • Fiuza PO, Ottoni-Boldrini BMP, Monteiro JS, Catena NR, Hamada N, Gusmão LFP (2015) First records of Ingoldian fungi from the Brazilian Amazon. Braz J Bot 38:615–621

    Article  Google Scholar 

  • Fiuza PO, Catillo-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

    Article  Google Scholar 

  • Gessner MO, Thomas M, Jean-Louis A-M, Chauvet E (1993) Stable successional patterns of aquatic hyphomycetes on leaves decaying in a summer cool stream. Mycol Res 97:163–172

    Article  Google Scholar 

  • Gessner MO, Gulis V, Kuehn KA, Chauvet E, Suberkropp K (2007) Fungal decomposers of plant litter in aquatic ecosystems. In: Kubicek CP, Druzhinina IS (eds) Environmental and microbial relationships. Springer p, Berlin, pp 301–324

    Google Scholar 

  • Gibbons SM, Jones E, Bearquiver A, Blackwolf F, Roundstone W, Scott N, Hooker J, Madsen R, Coleman ML, Gilbert JA (2014) Human and environmental impacts on river sediment microbial communities. Plos One 9:1–9

    Article  Google Scholar 

  • Goh TK, Hyde KD (1996) Biodiversity of freshwater fungi. J Ind Microbiol Biotechnol 17:328–345

    Article  CAS  Google Scholar 

  • Gönczöl J, Csontos P, Révay A (2003) Catchment scale patterns of aquatic hyphomycetes: the role of physicochemical variables and substrate composition in structuring conidial communities. Arch Hydrobiol 157:249–266

    Article  Google Scholar 

  • Gönczöl J, Révay A (2002) Treehole fungal communities: aquatic, aero-aquatic and dematiaceous hyphomycetes. Fungal Divers 12:19–34

    Google Scholar 

  • Graça MAS, Bärlocher F, Gessner MO (2005) Methods to study litter decomposition: a practical guide. Springer, Berlin

    Book  Google Scholar 

  • Graça MAS, Hyde K, Chauvet E (2016) Aquatic hyphomycetes and litter decomposition in tropical - subtropical low order streams. Fungal Ecol 19:182–189

    Article  Google Scholar 

  • Green JL, Holmes AJ, Westoby M, Oliver I, Briscoe D, Dangerfield M, Gillings M, Beattie AJ (2004) Spatial scaling of microbial eukaryote diversity. Nature 432:747–750

    Article  CAS  PubMed  ADS  Google Scholar 

  • Gulis V (1999) Preliminary list of aquatic hyphomycetes from central Belarus. Mycotaxon 72:227–230

    Google Scholar 

  • Heathwaite AL (2010) Multiple stressors on water availability at global to catchment scales: understanding human impact on nutrient cycles to protect water quality and water availability in the long term. Freshw Biol 55:241–257

    Article  Google Scholar 

  • Jabiol J, Bruder A, Gessner MO, Makkonen M, McKie BG, Peeters ETHM, Vos VCA, Chauvet E (2013) Diversity patterns of leaf-associated aquatic hyphomycetes along a broad latitudinal gradient. Fungal Ecol 6:439–448

    Article  Google Scholar 

  • Jackson DA (1993) Stop** rules in principal components analysis: a comparison of heuristical and statistical approaches. Ecology 74:2204–2214

    Article  Google Scholar 

  • Koleff P, Gaston KJ, Lennon JJ (2003) Measuring beta diversity for presence-absence data. J Animal Ecol 72:367–382

    Article  Google Scholar 

  • Krauss GJ, Solé M, Krauss G, Schlosser D, Wesenberg D, Bärlocher F (2011) Fungi in freshwaters: ecology, physiology and biochemical potential. FEMS Microbiol Rev 35:620–651

    Article  CAS  PubMed  Google Scholar 

  • Kumar U, Nayak AK, Shahid M, Gupta VVSR, Panneerselvam P, Mohanty S, Kaviraj M, Kumar A, Chatterjee D, Lal B, Gautam P, Thipathi R, Panda BB (2018) Continuous application of inorganic and organic fertilizers over 47 years in paddy soil alters the bacterial community structure and its influence on rice production. Agric Ecosyst Environ 262:65–75

    Article  Google Scholar 

  • Laurance WF, Sayer J, Cassman KG (2014) Agricultural expansion and its impacts on tropical nature. Trends Ecol Evol 29:107–116

    Article  PubMed  Google Scholar 

  • Mathuriau C, Chauvet E (2002) Breakdown of leaf litter in a neotropical stream. J North Am Benthol Soc 21:384–396

    Article  Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    Article  CAS  PubMed  ADS  Google Scholar 

  • McKinney ML, Lockwood JL (1999) Biotic homogenization: a few winners replacing many losers in the next mass extinction. Trends Ecol Evol 14:450–453

    Article  CAS  PubMed  Google Scholar 

  • Medeiros AO, Pascoal C, Graça MAS (2009) Diversity and activity of aquatic fungi under low oxygen conditions. Freshw Biol 54:142–149

    Article  Google Scholar 

  • Morris EK, Caruso T, Buscot F, Fischer M, Hancock C, Maier TS, Meiners T, Müller C, Obermaier E, Prati D, Socher SA, Sonnemann I, Wäschke N, Wubet T, Wurst S, Rillig MC (2014) Choosing and using diversity indices: insights for ecological applications from the German biodiversity exploratories. Ecol Evol 4:3514–3524

    Article  PubMed  PubMed Central  Google Scholar 

  • Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2017) vegan: community ecology package. R package version 2.4-4. https://CRAN.R-project.org/package=vegan. Accessed 28 Oct 2017

  • Olden JD, Comte L, Giam X (2016) Biotic homogenisation. In eLS, John Wiley & Sons, Ltd, Chichester

  • Olden JD, Rooney TP (2006) On defining and quantifying biotic homogenization. Glob Ecol Biogeogr 15:113–120

    Article  Google Scholar 

  • Paradis E, Schliep K (2019) ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35:526–528

    Article  CAS  PubMed  Google Scholar 

  • Oliveira EA (2012) O Parque Nacional dos Campos Gerais: processo de criação, caracterização ambiental e proposta de priorização de áreas para regularização fundiária. Setor de Ciências Agrárias da Universidade Federal do Paraná. p 297

  • Pascoal C, Marvanová L, Cássio F (2005) Aquatic hyphomycete diversity in streams of Northwest Portugal. Fungal Divers 19:109–128

    Google Scholar 

  • Pattee E, Chergui H (1995) The application of habitat templets and traits to hyphomycete fungi in a mid-European river system. Freshw Biol 33:525–539

    Article  Google Scholar 

  • Petsch DK (2016) Causes and consequences of biotic homogenization in freshwater ecosystems. Int Rev Hydrobiol 101:113–122

    Article  Google Scholar 

  • R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.r-project.org/. Accessed 01 Dec 2017

  • Rodrigues JLM, Pellizari VH, Mueller R, Baek K, Jesus EC, Paula FS, Mirza B, Hamaoui GS, Tsai SM, Feigl B, Tiedje JM, Bohannan BJM, Nüsslein K (2013) Conversion of the Amazon rainforest to agriculture results in biotic homogenization of soil bacterial communities. Proc Natl Acad Sci 110:988–993

    Article  CAS  PubMed  ADS  Google Scholar 

  • Shearer CA, Descals E, Kohlmeyer B, Kohlmeyer J, Marvanová L, Padgett D, Porter D, Raja HA, Schmit JP, Thorton HA, Voglymayr H (2007) Fungal biodiversity in aquatic habitats. Biodivers Conserv 16:49–67

    Article  Google Scholar 

  • Suberkropp K, Chauvet E (1995) Regulation of leaf breakdown by fungi in streams: influences of water chemistry. Ecology 76:1433–1445

    Article  Google Scholar 

  • Stein A, Gerstner K, Kreft H (2014) Environmental heterogeneity as a universal driver of species richness across taxa, biomes and spatial scales. Ecol Lett 17:866–880

    Article  PubMed  Google Scholar 

  • Tank JL, Rosi-Marshall EJ, Griffiths NA, Entrekin SA, Stephen ML (2010) A review of allochthonous organic matter dynamics and metabolism in streams. J North Am Benthol Soc 29:118–146

    Article  Google Scholar 

  • Tant CJ, Rosemond AD, Mehring AS, Kuehn KA, Davis JM (2015) The role of aquatic fungi in transformations of organic matter mediated by nutrients. Freshw Biol 60:1354–1363

    Article  CAS  Google Scholar 

  • Tuomisto H (2010) A diversity of beta diversities: straightening up a concept gone awry. Part 1. Defining beta diversity as a function of alpha and gamma diversity. Ecography 33:2–22

    Article  ADS  Google Scholar 

  • UNEP-WCMC and IUCN (2016) Protected Planet Report 2016. Cambridge UK and Gland Switzerland: UNEP-WCMC and IUCN. Available online on the website: https://resources.unep-wcmc.org/products/WCMC_RT062. Accessed 27 Jan 2018

  • Vannote RL, Minshall GW, Cummins KW, Sedell JR, Cushing CE (1980) The river continuum concept. Can J Fish Aquat Sci 37:130–137

    Article  Google Scholar 

  • Whittaker RH (1960) Vegetation of the Siskiyou Mountains, Oregon and California. Ecol Monogr 30:280–338

    Article  Google Scholar 

  • Wong MKM, Goh T-K, Hodgkiss IJ, Hyde KD, Ranghoo VM, Tsui CKM, Ho W-H, Wong WSW, Yuen T-K (1998) Role of fungi in freshwater ecosystems. Biodivers Conserv 7:1187–1206

    Article  Google Scholar 

  • Wood-Eggenschwiler S, Bärlocher F (1985) Geographical distribution of Ingoldian fungi. Verh Internat Verein Limnol 22:2780–2785

    Google Scholar 

Download references

Acknowledgements

The authors thank the Ecological Energetics Laboratory, Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura (NUPELIA), Universidade Estadual de Ponta Grossa (UEPG), Universidade Tecnológica Federal do Paraná (UTFPR), Campos Gerais National Park, Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio), Regiane Silva, Edivando Vitor do Couto, and Rachel Calil de Oliveira.

Funding

This work was supported by the Fundação Araucária de Apoio ao Desenvolvimento Científico e Tecnológico do Estado do Paraná (FA) and Fundação Grupo Boticário de Proteção à Natureza (FGB) [grant number 45751 002/2016], the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) [141691/2020-4 to M.M.R.S., 152643/2016-8 to G.D.P, and 308522/2021-4 to E.B.], and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) [1614297 and 88881.690087/2022-01 to M.M.R.S.].

Author information

Authors and Affiliations

  1. Graduate Program in Ecology of Inland Water Ecosystems (PEA), State University of Maringá, Maringá, Brazil

    Matheus Maximilian Ratz Scoarize, Gisele Daiane Pinha, Laryssa Helena Ribeiro Pazianoto & Evanilde Benedito

  2. Research Nucleus in Limnology, Ichthyology and Aquaculture (NUPELIA), State University of Maringá, Maringá, Brazil

    Matheus Maximilian Ratz Scoarize & Evanilde Benedito

  3. Australian Rivers Institute (ARI), Griffith University, Brisbane, Australia

    Matheus Maximilian Ratz Scoarize

  4. Graduate Program in Biosystems, Federal University of Southern Bahia, Itabuna, Brazil

    Gisele Daiane Pinha

Authors
  1. Matheus Maximilian Ratz Scoarize
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gisele Daiane Pinha
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Laryssa Helena Ribeiro Pazianoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Evanilde Benedito
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study conception and design. Material preparation and data collection were performed by Matheus Maximilian Ratz Scoarize, Gisele Daiane Pinha, and Laryssa Helena Ribeiro Pazianoto. Analysis was performed by Matheus Maximilian Ratz Scoarize and Gisele Daiane Pinha. The first draft of the manuscript was written by Matheus Maximilian Ratz Scoarize, and all authors commented on previous versions of the manuscript. Funding acquisition was performed by Evanilde Benedito. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Matheus Maximilian Ratz Scoarize.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Section Editor: Claus Baessler

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 90 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Scoarize, M.M.R., Pinha, G.D., Pazianoto, L.H.R. et al. Stream environmental conditions are homogenised outside a protected area, but fungal beta diversity remains unchanged. Mycol Progress 23, 12 (2024). https://doi.org/10.1007/s11557-024-01952-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11557-024-01952-6

Keywords

Search

Navigation