responses of aquatic fungal communities on leaf litter to temperature-change events

© 2009 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim 1434-2944/09/4-08-0410

Internat. Rev. Hydrobiol. 94 2009 4 410 –418

DOI: 10.1002/iroh.200811163

ISABEL FERNANDES, BEGÜM UZUN, CLÁUDIA PASCOAL and FERNANDA CÁSSIO*

Centre of Molecular and Environmental Biology (CBMA), Department of Biology,University of Minho, Campus de Gualtar, 4710-057 Braga, Portugal;

e-mail: [email protected]

Research Paper

Responses of Aquatic Fungal Communities on Leaf Litterto Temperature-Change Events

key words: streams, aquatic fungi, leaf decomposition, warming, freezing

Abstract

Increases of extreme weather events are predicted to occur with ongoing climate change, but impacts to freshwaters have rarely been examined. We assessed the effects of temperature on leaf-litter associ-ated fungi by exposing leaves colonized in a stream to 18 °C (control), 25 °C, or 18 °C after freezing. Treatments altered fungal dominance on leaves; Lunulospora curvula sporulation was stimulated by increased temperature and stopped by the freeze-thaw treatment. Fungal biomass and diversity decreased at 18 °C after freezing, but not at 25 °C. Leaf decomposition was retarded by the freeze-thaw treatment (k = –0.024 day–1) and stimulated at 25 °C (k = –0.069 day–1). Results suggest that occasional freez-ing may constrain fungal diversity and their ecological functions, while warming appears to accelerate plant-litter decomposition in streams.

1. Introduction

Ongoing climate change is considered a driving force for ecosystems in the 21st century (IPCC, 2007). Climate models show that an increase in extreme weather events will occur, such as increases in extreme high temperatures, decreases in extreme low temperatures, and increases in drought periods followed by intense rainfalls (EASTERLING et al., 2000; JENTSCH et al., 2007). In Europe, an increase in air temperature of 2.0–6.3 °C is estimated to occur by 2100 (EEA, 2004). Consequences of increasing temperature in several organisms point to changes in physiology, time of life cycle events, and distribution of individual species with shifts toward higher altitudes or latitudes (PARMESAN and YOHE, 2003; ROOT et al., 2003). It seems probable that, at least, some species will become extinct, either as a direct result of physiological stress or via alterations in competitive interactions with other species (HUGHES, 2000). Nevertheless, there is a limited number of species and ecological processes on which we have information on their responses to temperature and other related-climate change events.

There is a consensus in the scientific community that freshwater ecosystems are particu-larly vulnerable to climate change (CARPENTER et al., 1992; DUDGEON et al., 2006). This raises the significance of addressing how and in what extent climate change will affect fresh-

* Corresponding author

Fungal Communities and Temperature 411

© 2009 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.revhydro.com

water biota and ecosystem functions. Leaf litter decomposition is a key process in freshwa-ter ecosystems governed by microbial decomposers and invertebrate detritivores (GESSNER et al., 2007). Among microbial decomposers, fungi, particularly aquatic hyphomycetes, are known to play an important role in leaf litter decomposition in streams (BALDY et al., 2002; PASCOAL and CÁSSIO, 2004; GESSNER et al., 2007) and enhance leaf nutritional value for detritivores (GRAÇA, 2001).

Seasonal changes in stream water temperatures can lead to the replacement of winter aquatic hyphomycete communities (SUBERKROPP, 1984), and changes in the conidial density of temperate streams (BÄRLOCHER, 2000). Moreover, the structure of fungal communities on plant litter and their reproductive efforts are dependent on season, presumably through temperature effects (NIKOLCHEVA and BÄRLOCHER, 2005).

It has been hypothesized that global warming will lead to increased plant-litter decom-position rates in soils, both through direct and indirect temperature effects on litter quality and organisms (AERTS, 2006). Because most aquatic hyphomycetes have optimal growth at 15–25 °C (SUBERKROPP, 1984; SRIDHAR and BÄRLOCHER, 1993), increases in stream water temperature may stimulate fungal activity on plant litter in temperate streams. This is likely to shorten the residence time of available substrates for aquatic fungi and, therefore, decrease density and diversity of aquatic hyphomycetes in streams, as has been observed by BÄRLO-CHER et al. (2008) in hyporheic environments. In a manipulative experiment, a 5 °C increase in temperature changed the relative proportion of aquatic hyphomycete species on leaves, but effects on leaf decomposition depended on the identity of dominant species (DANG et al., 2009). However, studies on how aquatic hyphomycete species and their ecological func-tions respond to changes in temperature are scarce but are needed if we want to predict the impacts of global warming to freshwaters.

Because temperature is a main factor influencing metabolic activity of fungi, we hypoth-esized that increasing temperature would accelerate microbial decomposition of leaf lit-ter, while the exposure to a freezing temperature would retard this process. To test these hypotheses, leaves were immersed in a stream for 7 days to allow microbial colonization and then exposed to: i) 18 °C, a temperature commonly found in streams of Northwest Portugal between spring and autumn; ii) 25 °C to simulate a warming scenario; and iii) 18 °C after freezing, to simulate an extreme winter event. The effects of these temperature treatments were evaluated on leaf mass loss and leaf-associated fungal biomass, reproduc-tion and diversity.

2. Methods

2.1. Sampling Site and Stream Water

The study was carried out in the Algeriz stream located in the Cávado River basin (Northwest of Portugal, 41°35′ N and 8°20′ W). At the study site, the riparian vegetation is dominated by Quercus robur L., Pteridium aquilinum (L.) KUHN and Eucalyptus globulus LABILL. and the substrate is consti-tuted by boulders, pebbles and sand.

On 24th October 2007, temperature, pH, and conductivity of the stream water were measured in situ with field probes (Multiline F/set 3 no. 400327, WTW). Stream water was collected in sterile glass bottles, transported in a cool box and examined within 24 h for nitrate, nitrite, ammonia and phosphate concentrations (HACH kit; program 355, 371, 385 and 480, respectively). Stream water had circumneu-tral pH (6.2), low conductivity (45 μS cm–1), temperature around 14 °C (9 a.m.), moderate concentra-tion of nitrate (0.1 mg L–1), and low concentrations of nitrite (0.001 mg L–1), ammonia (0.01 mg L–1) and phosphate (0.01 mg L–1). Additional stream water samples were collected, filtered (filter pa-per, Macherey-Nagel) to retain suspended solids, and autoclaved (120 °C, 20 min) for microcosm assays.

412 I. FERNANDES et al.


2.2. Microcosm Assay

Alder leaves (Alnus glutinosa GAERTN.) were collected in October 2007 before abscission and dried at room temperature. Leaves were leached in deionised water for 48 h, cut into 12-mm-diameter disks, and sets of 20 disks were placed into 0.5 mm mesh bags (16 × 20 cm). On 24th October 2007, 56 leaf bags were immersed in the stream to allow microbial colonization. After 10 min of leaf immersion, four leaf bags were collected and taken to the laboratory to estimate the initial mass of leaf disks. After 7 days, the remaining 52 leaf bags were retrieved and transported to the laboratory in a cool box. Leaf disks from each bag were rinsed with deionised water and placed in 250 mL Erlenmeyer flasks with 100 mL of sterile stream water. The content of four leaf bags was used to determine leaf mass loss and fungal biomass at the beginning of the microcosm assay. Sets of 16 microcosms were exposed to 18 °C (control), to 25 °C (warming treatment) and to 18 °C after leaf disks had been frozen for a week (freeze-thaw treatment). The microcosms were incubated on a shaker (Certomat BS 3, B. Braun, Biotech International, Germany), at 120 rpm for 20 days, and stream water was changed every 5 days. After 5, 10, 15 and 20 days in micro-cosms, four replicates of each treatment were sacrificed to estimate leaf mass loss and fungal biomass.

2.3. Fungal Biomass and Sporulation Rates

Sets of 6 freeze-dried leaf disks from each microcosm were used to estimate ergosterol concentration as a measure of fungal biomass on decomposing leaves (GESSNER, 2005). Lipids were extracted from leaves by heating (80 °C, 30 min) in 0.8% of KOH/methanol, purified by solid-phase extraction and quantified by high performance liquid chromatography (HPLC) (Beckmann Gold System).

After 10 and 15 days in microcosms (corresponding to 17 and 22 days of total experiment, respectively), appropriate aliquots of conidial suspensions collected from each microcosm were mixed with 90 μL 0.5% Tween 80, filtered (5-μm pore size, Millipore), and the retained conidia were stained with 0.1% cotton blue in lactic acid. Approximately 300 conidia were identified and counted (400x; Leica Biomed, Heerbrug, Switzer-land) to determine the contribution of each aquatic hyphomycete species to the total conidial production.

2.4. Leaf Mass Loss

Sets of 14 leaf disks from each leaf bag or microcosm were dried at 60 °C to a constant mass (72 h ± 24 h) and weighed to the nearest 0.001 g.

2.5. Statistical Analyses

The remaining dry mass of alder leaves was fit to the exponential model: Wt = W0 × e–kt, where Wt is the leaf dry mass remaining at time t, W0 is the initial leaf dry mass, and k is the rate of leaf decomposi-tion. Regression lines of ln-transformed values of leaf dry mass were compared by ANCOVA followed by a Tukey post-test (ZAR, 1996).

Differences in fungal biomass, diversity and sporulation rates of aquatic hyphomycetes were assessed by two-way ANOVA with temperature and time as factors (ZAR, 1996). Differences between control and treatments were analysed by a Bonferroni post-test. Data were ln-transformed to achieve normal distribution and homocedasticity (ZAR, 1996).

Statistical analyses were done with Prism 4.0 for Windows (GraphPad software Inc., San Diego, CA).

3. Results

3.1. Leaf Mass Loss

At the end of the experiment (27 days), alder leaves lost 63% of their initial dry mass at 18 °C (control), 86% at 25 °C (warming treatment) and 45% at 18 °C after exposure to a



freezing treatment (Fig. 1). Decomposition rate of alder leaves was higher in the warming treatment (k = –0.069 day–1), intermediate in control (k = –0.041 day–1), and lower in the freeze-thaw treatment (k = –0.024 day–1) (Tukey test, P < 0.05; Table 1).

3.2. Fungal Biomass and Sporulation

Fungal biomass, as ergosterol concentration, attained maximum values after 17 days in control (320 μg g–1 dry mass) and the warming treatment (180 μg g–1 dry mass), and declined thereafter (Fig. 2). In the freeze-thaw treatment, fungal biomass was higher at the end of the experiment (90 μg g–1 dry mass). Temperature and time significantly affected fungal biomass on leaves (two-way ANOVA, P < 0.05, Table 2). Fungal biomass was significantly lower in the freeze-thaw treatment than in the control, but not in the warming treatment (Bonferroni test, P < 0.05 and P > 0.05, respectively).

Sporulation rates of aquatic hyphomycetes on leaves were significantly affected by tem-perature, time and interactions between these two factors (two-way ANOVA, P < 0.05, Table 2, Fig. 3). Sporulation rates were higher at 22 than at 17 days for all treatments. Moreover, sporulation rates were lower in the freeze-thaw treatment (at 17 and 22 days) and the warming treatment (22 days only) than in the control (Bonferroni test, P < 0.05).

Table 1. Breakdown rates (k) of alder leaves in microcosms exposed to 18 °C (C), 25 °C (W) and to 18 °C after a freezing treatment (F).

Treatment k (day–1) ± SE W0 (%) r2 n

C –0.041 ± 0.004a 104.8 0.80 24W –0.069 ± 0.005b 107.9 0.89 24F –0.024 ± 0.005c 100.8 0.55 24

SE, standard error; W0, initial leaf dry mass; r2, coefficient of determination; n, number of samples. Different superscript letters indicate significant differences (Tukey test, P < 0.05).

Figure 1. Leaf dry mass remaining (%) of decomposing alder leaves exposed to 18 °C (l), 25 °C (u), and to 18 °C after a freezing treatment (n). Data were fitted to the exponential decay model.

Mean ± SE; n = 4.



3.3. Fungal Diversity

A total of 12 aquatic hyphomycete species were identified sporulating on leaves over the entire study (Table 3). In control microcosms, the most contributors to the total conidial production were Articulospora tetracladia (36.2%), Lunulospora curvula (29.7%), and a

Figure 2. Fungal biomass (as ergosterol concentration) on decomposing alder leaves exposed to 18 °C (l), 25 °C (u), and to 18 °C after a freezing treatment (n). Mean ± SE; n = 4.

Table 2. Two-way ANOVAs on the effects of temperature and time on fungal biomass, sporulation rate and diversity.

Parameter Effect df SS MS F P

Fungal biomass Temperature 2 6.06 3.03 18.76 <0.01Time 4 9.46 2.37 14.65 <0.01Temperature × Time 8 2.44 0.31 1.892 0.08Residual 45 7.26 0.16

Sporulation rate Temperature 2 102.3 51.15 144.5 <0.01Time 1 3.72 3.72 10.50 <0.01Temperature × Time 2 104.9 52.46 148.2 <0.01Residual 18 6.37 0.35

Diversity Temperature 2 2.93 1.47 19.60 <0.01Time 1 0.23 0.23 3.11 0.09Temperature × Time 2 0.53 0.26 3.53 0.05Residual 18 1.35 0.07

Figure 3. Sporulation rates of aquatic fungi after 17 and 22 days of leaf decomposition at 18 °C (C), 25 °C (W) and 18 °C after a freezing treatment (F). Mean + SE; n = 4.



sigmoid species (27.7%). In the warming treatment, L. curvula and a sigmoid species con-tributed with about 80% to the total conidial production. In the freeze-thaw treatment A. tetracladia and Fusarium sp. were dominant species, contributing with more than 95% to the total conidial production. Sporulation of L. curvula and the sigmoid species was stopped by the freeze-thaw treatment.

The number of fungal species was significantly lowered by the freeze-thaw treatment at both times (two-way ANOVA, P < 0.05; Bonferroni test, P < 0.05; Table 2; Fig. 4). In the warming treatment, the number of fungal species on leaves appeared to decrease at 17 days, but increased at later times attaining values similar to those of control (Bonferroni test, P > 0.05).

4. Discussion

On a worldwide scale, temperature together with its influence on riparian vegetation in different climatic regions is the main factor determining aquatic hyphomycete distribution

Table 3. Percentage contributions of individual fungal species to total conidia produced after 17 and 22 days of leaf decomposition at 18 °C (C), 25 °C (W) and 18 °C after a

freezing treatment (F).

Treatment

Species C W F

Alatospora acuminata INGOLD < 0.1 – –Articulospora tetracladia INGOLD 36.2 13.4 56.2Dimorphospora foliicola TUBAKI – 3.0 –Flabellospora sp. – 0.2 –Fusarium sp. 1.6 1.3 40.6Lemonniera aquatica DE WILDEMAN 0.8 0.7 1.4Lunulospora curvula INGOLD 29.7 44.6 –Sigmoid 27.7 35.9 –Tetrachaetum elegans INGOLD 2.6 0.1 –Tetracladium setigerum INGOLD 0.2 0.4 1.6Tricladium splendens INGOLD 0.6 0.3 0.2Varicosporium elodeae KEGEL 0.5 0.2 –

Total number of taxa 10 11 5

Figure 4. Number of fungal species after 17 and 22 days of leaf decomposition at 18 °C (C), 25 °C (W) and 18 °C after a freezing treatment (F). Mean + SE; n = 4.



in streams (BÄRLOCHER, 1992). In temperate regions, seasonal changes in water temperature affect the occurrence and dominance of aquatic hyphomycetes with the highest reproduc-tive effort in autumn and spring (SUBERKOPP, 1984; BÄRLOCHER, 2000; NIKOLCHEVA and BÄRLOCHER, 2005).

In Northwest of Portugal, stream water temperature typically ranges from 6 to 12 °C in winter (PASCOAL et al., 2005; MESQUITA et al., 2007) and attains values between 17 and 21 °C in the warmer season (PASCOAL and CÁSSIO, 2004). In addition, during the cold season, small mountain streams can occasionally freeze for a short period of time (I. FERNANDES, per-sonal observations), with probable impacts to aquatic fungi and their ecological functions.

In our work, the exposure of a typical autumn fungal community to 25 °C or to 18 °C after a freezing treatment changed the species dominance on decomposing leaves. At 18 °C, A. tetracladia, L. curvula and a sigmoid species were dominant and the increase in tempera-ture augmented the contribution of the two latter species to the total conidial production. On the contrary, sporulation of L. curvula was completely inhibited by the freeze-thaw treat-ment, in which A. tetracladia and Fusarium sp. became dominant. This agrees with previous findings showing that the highest growth and sporulation rates of L. curvula occur at 25 °C, while maximum values for A. tetracladia occur at lower temperatures (15–20 °C) (CHAUVET and SUBERKROPP, 1998). Articulospora tetracladia is a dominant species on decomposing leaves in streams of our region throughout the year (PASCOAL and CÁSSIO, 2004; PASCOAL et al., 2005; DUARTE et al., 2004), while L. curvula is more common in warmer seasons (DUARTE et al., 2004). Previous research has reported L. curvula as a “summer species” and its spores rapidly decline in late autumn in streams (SUBERKROPP, 1984). The present study suggests that shifts in species composition may occur as a consequence of rising tempera-ture, with communities found in autumn/winter becoming more similar to those found in spring/summer.

In this study, the freeze-thaw treatment led to a reduction in leaf decomposition rate of almost two-times, together with a decline in fungal diversity, sporulation and biomass. These findings agree with other studies reporting retarded leaf decomposition accompanied by a decline in fungal reproduction and biomass in the cold season, when temperatures are nearly 0 °C (NIKOLCHEVA and BÄRLOCHER, 2005). In contrast, leaf decomposition rate increased almost twice when temperature was raised from 18 to 25 °C to simulate a warming scenario. This was not surprising since increased temperatures are expected to enhance biological activities. In our work, the stimulation of leaf decomposition could be the result of higher enzymatic activities of dominant species (e.g., L. curvula) at the highest temperature. Indeed, L. curvula is reported to have maximum cellulase activity at 28 °C (CHANDRASHEKAR and KAVERIAPPA, 1991).

Even though a stimulation of leaf decomposition was found at the warming treatment, we failed to detect higher overall fungal biomass or reproduction on leaves. It is possible that increased temperature had led to higher growth rates and greater biomass turnover. However, we cannot infer much about fungal growth and activity from ergosterol measurements alone, since ergosterol is a static measure of standing stock biomass. Results might be also related to the effects of temperature on the efficiency of fungi to use complex carbon sources, such as leaf litter. Differences in temperature dependence of bacterial production and respira-tion were found in a temperate salt-marsh estuary, in which increased temperature had a strong negative effect on bacterial growth efficiency (APPLE et al., 2006). Thus, if increased temperature had favoured a fungal community with lower growth efficiency (i.e., low ratio biomass buildup/respiration) this would probably contribute to explain the absence of fungal biomass stimulation under the warming treatment.

Overall, we found that changes in temperature altered fungal species composition and led to changes in leaf-litter decomposition. Results suggest that occasional freezing is likely to constrain diversity and the ecological functions of aquatic fungi, while warming appears to accelerate plant-litter decomposition in streams. Because warming may also affect plant



phenology, for instance by anticipating leaf unfold and delaying leaf abscission (PEÑUELAS et al., 2002; NORBY et al., 2003), aquatic fungi could experience later periods of litter fall. In addition to this, if faster leaf decomposition at increased temperature occurs in streams as found in this study, substrate availability for aquatic fungi would decrease (BÄRLOCHER et al., 2008) further compromising the functioning of detritus-based food webs in freshwa-ters.

5. Acknowledgement

This study was suported by the Portuguese Foundation for Science and Technology (PTDC/CLI/67180/2006).

6. References

AERTS, R., 2006: The freezer defrosting: global warming and litter decomposition rates in cold biomes. – J. Ecol. 94: 713–724.

APPLE, J. K., P. A. DEL GIORGIO and W. M. KEMP, 2006: Temperature regulation of bacterial produc-tion, respiration, and growth efficiency in a temperate salt-marsh estuary. – Aquat. Microb. Ecol. 43: 243–254.

BALDY, V., E. CHAUVET, J.-Y. CHARCOSSET and M. O. GESSNER, 2002: Microbial dynamics associated with leaves decomposing in the mainstem and floodplain pond of a large river. – Aquat. Microb. Ecol. 28: 25–36.

BÄRLOCHER, F., (ed.), 1992: The ecology of aquatic hyphomycetes. – Springer-Verlag, Berlin, Ger-many.

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

BÄRLOCHER, F., S. SEENA, K. P. WILSON and D. D. WILLIAMS, 2008: Raised water temperature lowers diversity of hyporheic aquatic hyphomycetes. – Freshw. Biol. 53: 368–379.

CARPENTER, S. R., S. G. FISHER, N. B. GRIMM and J. F. KITCHELL, 1992: Global change and freshwater ecosystems. – Annu. Rev. Ecol. Syst. 23: 119–139.

CHANDRASHEKAR, K. R. and K. M. KAVERIAPPA, 1991: Production of extracellular cellulase by Lunu-lospora curvula and Flagellospora penicillioides. – Folia Microbiol. 36: 249–255.

CHAUVET, E. and K. SUBERKROPP, 1998: Temperature and sporulation of aquatic hyphomycetes. – Appl. Environ. Microbiol. 64: 1522–1525.

DANG, C. K., M. SCHINDLER, E. CHAUVET and M. O. GESSNER, 2009: Temperature oscillation coupled with fungal community shifts can modulate warming effects on litter decomposition. – Ecology 90: 122–131.

DUARTE, S., C. PASCOAL and F. CÁSSIO, 2004: Effects of zinc on leaf decomposition by fungi in streams: studies in microcosms. – Microb. Ecol. 48: 366–374.

DUDGEON, D., A. H. ARTHINGTON, M. O. GESSNER, Z.-I. KAWABATA, D. J. KNOWLER, C. LÉVÊQUE, R. J. NAIMAN, A.-H. PRIEUR-RICHARD, D. SOTO, M. L. J. STIASSNY and C. A. SULLIVAN, 2006: Freshwater biodiversity: importance, threats, status and conservation challenges. – Biol. Rev. 81: 163–182.

EASTERLING, D. R., G. A. MEEH, C. PARMESAN, S. A. CHANGNON, T. R. KARL and L. O. MEARNS, 2000: Climate Extremes: Observations, Modeling, and Impacts. – Science 289: 2068–2074.

EEA (European Environment Agency), 2004: Impacts of Europe’s changing climate: an indicator-based assessment. Copenhagen, Denmark: European Environment Agency. – http://www.eea.europa.eu/pub-lications/climate_report_2_2004

GESSNER, M. O., 2005: Ergosterol as a measure of fungal biomass. – In: M. A. S. GRAÇA, F. BÄRLO-CHER and M. O. GESSNER (eds.), Methods to study litter decomposition: a practical guide. Springer, Dordrecht, Netherlands: pp. 189–196.

GESSNER, M. O., V. GULIS, K. A. KUEHN, E. CHAUVET and K. SUBERKROPP, 2007: Fungal decompos-ers of plant litter in aquatic habitats. – In: C. P. KUBICEK and I. S. DRUZHININA (eds.), The Mycota, Vol. IV: Environmental and microbial relationships, 2nd ed., Springer-Verlag, Berlin, Germany: pp. 301–324.



GRAÇA, M. A. S., 2001: The role of invertebrates on leaf litter decomposition in streams – a review. – Internat Rev. Hydrobiol. 86: 383–393.

HUGHES, L., 2000: Biological consequences of global warming: is the signal already. – Tree 15: 56–61.

IPCC, 2007: Climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. – http://www.ipcc.ch/ipccreports/ar4-wg1.htm

JENTSCH, A., J. KREYLING and C. BEIERKUHNLEIN, 2007: A new generation of climate change experi-ments: events, not trends. – Front. Ecol. Environ. 5: 315–324.

MESQUITA, A., C. PASCOAL and F. CÁSSIO, 2007: Assessing effects of eutrophication in streams based on breakdown of eucalypt leaves. – Arch. Hydrobiol. 168: 221–230.

NIKOLCHEVA, L. G. and F. BÄRLOCHER, 2005: Seasonal and substrate preferences of fungi colonizing leaves in streams: traditional versus molecular evidence. – Environ. Microbiol. 7: 270–280.

NORBY, R. J., J. S. HARTZ-RUBIN and M. J. VERBRUGGE, 2003: Phenological responses in maple to experimental atmospheric warming and CO2 enrichment. – Glob. Change Biol. 9: 1792–1801.

PARMESAN, C. and G. YOHE, 2003: A globally coherent fingerprint of climate change impacts across natural systems. – Nature 421: 37–42.

PASCOAL, C. and F. CÁSSIO, 2004: Contribution of fungi and bacteria to leaf litter decomposition in a polluted river. – Appl. Environ. Microbiol. 70: 5266–5273.

PASCOAL, C., F. CÁSSIO and L. MARVANOVÁ, 2005: Anthropogenic stress may affect aquatic hyphomycete diversity more than leaf decomposition in a low-order stream. – Arch. Hydrobiol. 162: 481–496.

PEÑUELAS, J., I. FILELLA and P. COMAS, 2002: Changed plant and animal life cycles from 1952 to 2000 in the Mediterranean region. – Glob. Change Biol. 8: 531–544.

ROOT, T. L., J. T. PRICE, K. R. HALL, S. H. SCHNEIDER, C. ROSENZWEIG and J. A. POUNDS, 2003: Fin-gerprints of global warming on wild animals and plants. – Nature 421: 57–60.

SRIDHAR, K. R. and F. BÄRLOCHER, 1993: Effect of temperature on growth and survival of five aquatic hyphomycetes. – Sydowia 45: 377–387.

SUBERKROPP, K., 1984: Effect of temperature on seasonal occurrence of aquatic hyphomycetes. – T. Brit. Mycol. Soc. 82: 53–62.

ZAR, J. H., 1996: Biostatistical analysis. 3rd ed., Prentice-Hall, Englewood Cliffs.

Manuscript received October 13th, 2008; accepted February 20th, 2009

responses of aquatic fungal communities on leaf litter to temperature-change events

Documents