Abstract
In forested headwater streams, decomposition of allochthonous organic matter is a fundamental process driven by aquatic microbes and invertebrate shredders. We examined how season and eutrophication affect leaf decomposition and the associated decomposer communities by immersing leaves of a late deciduous species (Quercus robur) in five streams in Portugal along a gradient of eutrophication in autumn and spring. We found hump-shaped relationships between leaf decomposition and total nitrogen and phosphorus in stream water in both seasons. Leaf decomposition and shredder biomass were higher during spring in streams with moderate levels of eutrophication. Fungal sporulation and biomass were stimulated at moderate levels of eutrophication and inhibited at low or high levels of eutrophication. Fungal assemblage composition shifted between seasons and along the gradient of eutrophication. Tricladium chaetocladium increased its contribution to total conidial production in spring, while Dimorphospora foliicola was dominant in the most eutrophic streams where Articulospora tetracladia was almost absent. Invertebrate shredders were the primary decomposers of leaves in streams with moderate levels of eutrophication, particularly in the warmest season. Although the presence of late deciduous plant species, such as oak, in the riparian corridors may help to mitigate food depletion to freshwater decomposers in spring, our results suggest that moderate eutrophication can accelerate decomposition further reducing litter standing stocks in the warmer seasons.
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References
Abelho M, Graça M (1998) Litter in a first-order stream of a temperate deciduous forest (Margaraça Forest, central Portugal). Hydrobiol 386:147–152. doi:10.1023/A:1003532921432
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46. doi:10.1046/j.1442-9993.2001.01070.x
Bärlocher F, Corkum M (2003) Nutrient enrichment overwhelms diversity effects in leaf decomposition by stream fungi. Oikos 101:247–252. doi:10.1034/j.1600-0706.2003.12372.x
Basaguren A, Riano P, Pozo J (2002) Life history patterns and dietary changes of several caddisfly (Trichoptera) species in a northern Spain stream. Arch für Hydrobiol 155:23–41
Box EO, Fujiwara K (2015) Warm-Temperate Deciduous Forests around the Northern Hemisphere. Spring International Publishing, Switzerland
Boyero L, Pearson RG, Gessner MO et al (2011) A global experiment suggests climate warming will not accelerate litter decomposition in streams but might reduce carbon sequestration. Ecol Lett 14:289–294. doi:10.1111/j.1461-0248.2010.01578.x
Brown JH, Gillooly JF, Allen AP et al (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789. doi:10.1890/03-9000
Chauvet E, Suberkropp K (1998) Temperature and sporulation of aquatic hyphomycetes. Appl Environ Microbiol 64:1522–1525
Duarte S, Pascoal C, Cássio F, Bärlocher F (2006) Aquatic hyphomycete diversity and identity affect leaf litter decomposition in microcosms. Oecologia 147:658–666. doi:10.1007/s00442-005-0300-4
Duarte S, Pascoal C, Cássio F (2008) High diversity of fungi may mitigate the impact of pollution on plant litter decomposition in streams. Microb Ecol 56:688–695. doi:10.1007/s00248-008-9388-5
Duarte S, Pascoal C, Garabetian F et al (2009) Microbial decomposer communities are mainly structured by trophic status in circumneutral and alkaline streams. Appl Environ Microbiol 75:6211–6221. doi:10.1128/AEM.00971-09
Duarte S, Fernandes I, Nogueira MJ et al (2013) Temperature alters interspecific relationships among aquatic fungi. Fungal Ecol 6:187–191. doi:10.1016/j.funeco.2013.02.001
Duarte S, Bärlocher F, Trabulo J et al (2015) Stream-dwelling fungal decomposer communities along a gradient of eutrophication unraveled by 454 pyrosequencing. Fungal Divers 70:127–148. doi:10.1007/s13225-014-0300-y
Duarte S, Bärlocher F, Pascoal C, Cássio F (2016) Biogeography of aquatic hyphomycetes: current knowledge and future perspectives. Fungal Ecol 19:169–181. doi:10.1016/j.funeco.2015.06.002
Dudgeon D, Arthington AH, Gessner MO et al (2006) Freshwater biodiversity: importance, threats, status and conservation challenges. Biol Rev 81:163–182. doi:10.1017/S1464793105006950
Fernandes I, Seena S, Pascoal C, Cássio F (2014) Elevated temperature may intensify the positive effects of nutrients on microbial decomposition in streams. Freshw Biol 59:2390–2399. doi:10.1111/fwb.12445
Fernandes I, Pereira A, Trabulo J et al (2015) Microscopy- or DNA-based analysis: which methodology gives a truer picture of stream-dwelling decomposer fungal diversity? Fungal Ecol 18:130–134. doi:10.1016/j.funeco.2015.08.005
Ferreira V, Canhoto C (2014) Effect of the experimental and seasonal warming on litter decomposition in a temperate stream. Aquat Sci 76:155–163. doi:10.1007/s00027-013-0322-7
Ferreira V, Chauvet E (2011) Synergistic effects of water temperature and dissolved nutrients on litter decomposition and associated fungi. Glob Chang Biol 17:551–564. doi:10.1111/j.1365-2486.2010.02185.x
Ferreira V, Elosegi A, Gulis V et al (2006a) Eucalyptus plantations affect fungal communities associated with leaf-litter decomposition in Iberian streams. Arch für Hydrobiol 166:467–490. doi:10.1127/0003-9136/2006/0166-0467
Ferreira V, Graça MAS, de Lima JLMP, Gomes R (2006b) Role of physical fragmentation and invertebrate activity in the breakdown rate of leaves. Arch für Hydrobiol 165:493–513. doi:10.1127/0003-9136/2006/0165-0493
Ferreira V, Gulis V, Graça MAS (2006c) Whole-stream nitrate addition affects litter decomposition and associated fungi but not invertebrates. Oecologia 149:718–729. doi:10.1007/s00442-006-0478-0
Friberg N, Dybkjær JB, Olafsson JS et al (2009) Relationships between structure and function in streams contrasting in temperature. Freshw Biol 54:2051–2068. doi:10.1111/j.1365-2427.2009.02234.x
Gessner MO (2005) Ergosterol as measure of fungal biomass. In: MAS Graça, Bärlocher F, Gessner MO (eds) Methods to study litter Decompos. a Pract. Guid. Springer, The Netherlands, pp 189–195
Gessner MO, Chauvet E (1993) Ergosterol-to-biomass conversion factors for aquatic hyphomycetes. Appl Environ Microbiol 59:502–507
Gessner MO, Gulis V, Kuehn KA, et al (2007) Fungal decomposers of plant litter in aquatic ecosystems. In: Kubicek CP, Druzhinina IS (eds) Mycota Environ. Microb. relationships, 2nd edn. Springer, Berlin, pp 301–321
Gonçalves AL, Graça MAS, Canhoto C (2013) The effect of temperature on leaf decomposition and diversity of associated aquatic hyphomycetes depends on the substrate. Fungal Ecol 6:546–553. doi:10.1016/j.funeco.2013.07.002
González JM, Graça MAS (2003) Conversion of leaf litter to secondary production by a shredding caddis-fly. Freshw Biol 48:1578–1592. doi:10.1046/j.1365-2427.2003.01110.x
González E, Pozo J (1996) Longitudinal and temporal patterns of benthic coarse particulate organic matter in the Agüera stream (northern Spain). Aquat Sci 58:355–366. doi:10.1007/BF00877475
Graça MAS, Canhoto C (2006) Leaf litter processing in low order streams. Limnetica 25:1–10
Gulis V, Suberkropp K (2003) Leaf litter decomposition and microbial activity in nutrient-enriched and unaltered reaches of a headwater stream. Freshw Biol 48:123–134. doi:10.1046/j.1365-2427.2003.00985.x
Gulis V, Ferreira V, Graça MAS (2006) Stimulation of leaf litter decomposition and associated fungi and invertebrates by moderate eutrophication: implications for stream assessment. Freshw Biol 51:1655–1669. doi:10.1111/j.1365-2427.2006.01615.x
Jabiol J, Chauvet E (2012) Fungi are involved in the effects of litter mixtures on consumption by shredders. Freshw Biol 57:1667–1677. doi:10.1111/j.1365-2427.2012.02829.x
Lecerf A, Usseglio-Polatera P, Charcosset J-Y et al (2006) Assessment of functional integrity of eutrophic streams using litter breakdown and benthic macroinvertebrates. Arch für Hydrobiol 165:105–126. doi:10.1127/0003-9136/2006/0165-0105
Lima-Fernandes E, Fernandes I, Pereira A et al (2015) Eutrophication modulates plant-litter diversity effects on litter decomposition in streams. Freshw Sci 34:31–41. doi:10.1086/679223
Malmqvist B, Rundle S (2002) Threats to the running water ecosystems of the world. Environ Conserv 29:134–153. doi:10.1017/S0376892902000097
Medeiros AO, Pascoal C, Graça MAS (2009) Diversity and activity of aquatic fungi under low oxygen conditions. Freshw Biol 54:142–149. doi:10.1111/j.1365-2427.2008.02101.x
Nikolcheva LG, Bärlocher F (2005) Seasonal and substrate preferences of fungi colonizing leaves in streams: traditional versus molecular evidence. Environ Microbiol 7:270–280. doi:10.1111/j.1462-2920.2004.00709.x
Nikolcheva LG, Bourque T, Bärlocher F (2005) Fungal diversity during initial stages of leaf decomposition in a stream. Mycol Res 109:246–253. doi:10.1017/S0953756204001698
Pascoal C, Cássio F, Marcotegui A et al (2005a) Role of fungi, bacteria, and invertebrates in leaf litter breakdown in a polluted river. J North Am Benthol Soc 24:784–797. doi:10.1899/05-010.1
Pascoal C, Cássio F, Marvanová L (2005b) Anthropogenic stress may affect aquatic hyphomycete diversity more than leaf decomposition in a low-order stream. Arch Fur Hydrobiol 162:481–496
Rosemond AD, Benstead JP, Bumpers PM et al (2015) Experimental nutrient additions accelerate terrestrial carbon loss from stream ecosystems. Science 347:1142–1145. doi:10.1126/science.aaa1958
Suberkropp K (1984) Effect of temperature on seasonal occurrence of aquatic hyphomycetes. Trans Br Mycol Soc 82:53–62. doi:10.1016/S0007-1536(84)80211-9
Suberkropp K (1998) Microorganisms and organic matter decomposition. In: Naiman RJ, Bilby RE (eds) River Ecol. Manag. lessons from Pacific Coast. ecoregion. Springer, New York, pp 120–143
Suberkropp K, Arsuffi TL, Anderson JP (1983) Comparison of degradative ability, enzymatic activity, and palatability of aquatic hyphomycetes grown on leaf litter. Appl Environ Microbiol 46:237–244
Swan CM, Palmer MA (2004) Leaf diversity alters litter breakdown in a Piedmont stream. J North Am Benthol Soc 23:15–28. doi:10.1899/0887-3593(2004)023<0015:LDALBI>2.0.CO;2
Tachet H, Richoux P, Bournaud M, Usseglio-Polatera P (2010) Invertebrés d’eau douce. Systématique, biologie, écologie. CNRS Editions, Paris, France
Webster JR, Benfield EF (1986) Vascular plant breakdown in freshwater ecosystems. Annu Rev Ecol Syst 17:567–594
White TJ, Bruns S, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protoc. A Guid. to Methods Appl. Academic Press, pp 315–322
Woodward G, Gessner MO, Giller PS et al (2012) Continental-scale effects of nutrient pollution on stream ecosystem functioning. Science 336:1438–1440. doi:10.1126/science.1219534
Zar JH (2010) Biostatistical analysis. Prentice-Hall, Englewood-Cliffs
Acknowledgments
FEDER-POFC-COMPETE (FCOMP-01-0124-FEDER-013954) and the Portuguese Foundation for Science and Technology (FCT) I.P. supported this study (PTDC/AAC-AMB/113746/2009, PTDC/AAC-AMB/117068/2010 and through the strategic funding UID/BIA/04050/2013). Financial support given by FCT to SD (SFRH/BPD/47574/2008, SFRH/BPD/109842/2015) and IF (SFRH/BPD/97656/2013) is also acknowledged. We also want to thank to two anonymous reviewers and to the editorial board for the comments and suggestions made on an earlier version of the manuscript.
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Pereira, A., Trabulo, J., Fernandes, I. et al. Spring stimulates leaf decomposition in moderately eutrophic streams. Aquat Sci 79, 197–207 (2017). https://doi.org/10.1007/s00027-016-0490-3
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DOI: https://doi.org/10.1007/s00027-016-0490-3