Hydrobiologia (2013) 716:5–20 DOI 10.1007/s10750-013-1539-0
PRIMARY RESEARCH PAPER
Do non-native Platanus hybrida riparian plantations affect leaf litter decomposition in streams? M. Mene´ndez • E. Descals • T. Riera O. Moya
•
Received: 14 February 2013 / Revised: 12 April 2013 / Accepted: 4 May 2013 / Published online: 15 May 2013 Ó Springer Science+Business Media Dordrecht 2013
Abstract In forest headwater streams where the riparian canopy limits autochthonous primary production, leaf litter decomposition is a key process controlling nutrient and carbon cycling. Any alteration of the riparian vegetation may influence litter decomposition and detrital food webs. We evaluated the effect of non-native Platanus hybrida riparian plantations on leaf litter decomposition in Mediterranean streams. The experiment was conducted in six headwater streams; three lined by native riparian vegetation and three crossing P. hybrida plantations. We have characterized the processing rates of alder leaves and the assemblages of shredder macroinvertebrates and fungi. Litter decomposition was significantly faster in the P. hybrida than in the reference streams. Although the dissolved inorganic nitrogen concentration was higher in P. hybrida, no significant effect was observed in decomposition rates. Differences in decomposition rates reflected the macroinvertebrate and shredder colonization in alder litter, with higher
Handling editor: Luz Boyero M. Mene´ndez (&) T. Riera Department d’Ecologı´a, Universitat de Barcelona, Barcelona, Spain e-mail:
[email protected] E. Descals O. Moya Instituto Mediterra´neo de Estudios Avanzados de las Baleares, IMEDEA (CSIC-UIB), Esporles, Mallorca, Spain
abundance and richness in the P. hybrida streams. However, aquatic hyphomycete sporulation rate was higher in reference streams, suggesting that the variation in decomposition rates is a direct consequence of shredder abundance. Our findings support part of the substrate quality-matrix quality (SMI) hypothesis, which expects that high-quality litter will show increased decomposition rates in a low-quality litter matrix. Keywords Litter breakdown Exotic riparian vegetation Macroinvertebrates Aquatic hyphomycetes
Introduction Riparian habitats are highly susceptible to proliferation and invasion by exotic species (Sher et al., 2002). The particular dynamics of riparian ecosystems that are subject to frequent fluctuations in water flow destabilizes the streamside and favours the establishment of new species (Planty-Tavacchi et al., 1996). Downstream flow also favours the natural dispersal of seeds and rhizomes. In addition, anthropogenic disturbances, frequent in riparian sites, may favour germination of invading species (Beerling et al., 1994). In forest headwater streams where the riparian canopy limits autochthonous primary production, detritus derived from terrestrial riparian vegetation is the dominant source of energy (Vannote et al., 1980;
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Wallace et al., 1997). Here, leaf litter processing constitutes the basis of the detrital food chain (Webster & Benfield, 1986; Grac¸a, 2001). The main microorganisms involved in this process are the aquatic hyphomycetes (Ba¨rlocher, 1992; Gessner & Chauvet, 1994; Hieber & Gessner, 2002), which quickly colonize the leaf litter, decomposing and conditioning the detritus so as to increase its palatability for macroinvertebrate shredders (Cummins et al., 1989; Suberkropp, 1992; Grac¸a et al., 1993). The quantity, quality and diversity of litter accumulated in a stream highly depend on the type of riparian vegetation bordering the stream (Laitung et al., 2002; Laitung & Chauvet, 2005). Therefore, changes in the riparian vegetation can potentially affect litter colonization and decomposition by the aquatic hyphomycetes, as well as consumption by detritivores (Ferreira et al., 2006a). Laitung & Chauvet (2005) showed a positive relationship between riparian vegetation richness and that of aquatic hyphomycetes in woodland streams in France. A similar result was reported by Lecerf et al. (2005), who also showed that microbial richness can regulate leaf litter decomposition through interactions with macroinvertebrate. However, Leroy & Marks (2006) and Schindler & Gessner (2009) have suggested that species composition of litter mixtures can affect decomposition to a greater extent than litter species richness per se. In a study in a softwater forested stream in Germany, Schindler & Gessner (2009) found that recalcitrant and labile leaf litter decomposed slower and faster, respectively, in litter mixtures comprising litter of different decay categories than in homogenous mixtures composed of a single decay category or in singlespecies litter bags. Therefore, the replacement of native riparian flora can have negative, neutral or positive effects on food web fluxes depending on the degree and direction of the differences in litter chemistry of exotic versus native species (Hladyz et al., 2009). The potential effect of exotic riparian vegetation on leaf litter decomposition and on decomposer and detritivorous organisms has received considerable attention. Boyero et al. (2012) have pointed out that the effect of non-native riparian plants on leaf litter breakdown might be more noticeable in temperate than in tropical streams due to the higher specialization of shredders at higher latitudes. These authors suggested that this effect may vary depending on
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assemblage composition, the nature and timing of litter fall, and the interactions with climate. In headwater streams of the Iberian Peninsula it has been noticed that substitution of deciduous forests with eucalyptus plantations affects the composition of macroinvertebrate communities, decreasing the abundance and species richness of macroinvertebrates in the sediment (Abelho & Grac¸a, 1996) and the density of macroinvertebrate colonizing decomposing leaf litter (Basaguren & Pozo, 1994). In Portugal, species richness and evenness of fungal communities were reported to be lower in streams affected by eucalyptus plantations than in deciduous ones (Ba¨rlocher & Grac¸a, 2002; Ferreira et al., 2006a), but not so in Spain (Chauvet et al., 1997; Ferreira et al., 2006a). Since aquatic hyphomycetes and macroinvertebrates play a key role in leaf decomposition, the modification of riparian vegetation can potentially affect litter decomposition. Abelho & Grac¸a (1996) reported lower decomposition rates of Castanea sativa leaves in eucalyptus than in deciduous streams in central Portugal. Nevertheless, Pozo et al. (1998) and Ferreira et al. (2006a) have not observed any effect of eucalyptus plantations on shredders nor on decomposition rates. Other studies examining the effect of forest plantations on the decomposition of native leaf litter in streams have also shown contrasting results. In a temperate humid woodland stream in SE Ireland, Kominoski et al. (2011) recently observed that the effect of conifer plantations on decomposition rates depends on the quality of the decomposing leaf litter. They observed that the processing rate of labile litter (Alnus rubra) by shredders was more affected by the substitution of native deciduous forest with conifer plantations than that of more refractory litter (Tsuga heterophylla). However, in central England, Riipinen et al. (2010) did not find any effect of conifer plantations on decomposition rates of native deciduous litter, either labile (Alnus glutinosa) or tougher leaf species (Quercus robur). Platanus hybrida (hispanica) Brot. was planted in Mediterranean riparian systems (Casas & Gessner, 1999) due to its remarkable resistance to diseases and herbivores as well as higher growth rates compared to native riparian species. Streams in NE Iberian Peninsula run through abundant plantations of P. hybrida (1301 Ha in Catalonia, INE, Censo Agrario, 2009) exploited for lumber. These cause great accumulations
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of leaf litter at the end of summer, autumn and winter, covering the entire streambeds of headwater streams (Fig. 1), while the leaf input of the most abundant natural deciduous riparian vegetation, A. glutinosa and Populus nigra in the studied Mediterranean streams, peaks in August (Acun˜a et al., 2007). Annual leaf inputs into stream beds in P. hybrida reaches between 2001 and 2003 ranged from 0.22 to 0.32 kg C m-2 year-1, and were mainly composed of P. hybrida (40%), P. nigra (12%) and A. glutinosa (10%) (Acun˜a et al., 2007). The leaf litter of P. hybrida is very refractory (Casas & Gessner, 1999), with high lignin concentration (30.9%; Gessner & Chauvet, 1994) and low N and P concentrations (C/N: 73.6, C/P: 49236; this study). Shredder macroinvertebrates in streams have low C:N ratios (6.2–7.1) compared with their leaf litter food resources (67–73) (Cross et al., 2003; Hladyz et al., 2009). Therefore, the replacement of a natural riparian vegetation by P. hybrida plantations, which change the timing as well as the quality and quantity of leaf litter resources in streams, might increase the C:N imbalance between consumers and resources, with consequences for ecosystem functioning. The objective of the present study was to assess the effects of exotic riparian plantations of P. hybrida in the decomposition of native leaf litter in Mediterranean headwater streams. In a previous study of litter breakdown conducted in 12 streams crossing native riparian vegetation in 4 different regions in Spain (Casas et al., 2013), we found the lowest decomposition rate in P. hybrida, when compared with pine and native leaf litter. Among the European species of Platanus, some studies have shown that P. hispanica has by far the lowest decomposition rate (Casas & Gessner, 1999) and enzymatic activity (Artigas et al., 2004) when compared with native species. Moreover, feeding tests with leaves of P. orientalis have shown that they were not eaten by aquatic shredders, even if they came from the native geographical range of the species (island of Crete) (Maliky, 1990). We predicted that (1) alder litter would decay faster in P. hybrida than in native riparian streams due to the lack of more palatable litter for shredders in P. hybrida streams and that (2) macroinvertebrate and shredder abundance and richness associated to alder litter in P. hybrida streams would be higher than in reference streams due to an island effect. We have tested these predictions in six forest headwater streams, three lined by native
7
Fig. 1 Photograph of Castanyet (CN) stream lined by P. hybrida plantations showing the great accumulation of P. hybrida leaf litter in the channel
riparian vegetation (reference) and three lined by P. hybrida plantations. Alder (Alnus glutinosa (L.) Gaertn.), which is present along all the reaches selected, was incubated in all streams and decomposition and associated detritivores and aquatic hyphomycetes were evaluated.
Materials and methods Study sites This study was conducted in six low order streams (orders 2–3) in the Tordera and in the Beso`s river basins of Catalonia (NE Spain). The P. hybrida sites are referred to as Arbu´cies, Castanyet and Fuirosos (AR, CN, FS, respectively) in the Tordera, and the reference sites as Avenco´, Ca`noves and Llobina (AV,
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Table 1 Location, catchment area and physical and chemical characteristics of the water at the studied streams Stream (acronym)
Latitude, N
Longitude, E
Altitude (m.a.s.l.)
Order
Ca`noves (CA)
41°430 1400
2°200 3000
562
3
00
Catchment area (Ha)
Water temperature (°C) 7.6 (6.5–9.1)a
725
Llobina (LLO)
41°32 49
446
2
530
6.9 (6.1–8.1)c
Avenco´ (AV)
41°270 4400
2°090 4800
515
2
1,260
5.9 (5.1–7.0)d
Arbucies (AR)
41°290 3800
2°160 1500
451
2
1,335
8.8 (8.0–9.7)b
Castanyet (CN)
41°450 7700
2°160 1100
170
2
630
8.7 (8.1–9.7)b
Fuirosos (FS)
41°410 4800
2°340 4500
120
2
1,270
7.7 (7.1–8.8)a
0
00
0
2°13 45
Acronym
Alkalinity (meq l-1)
pH
CA
1.1 (0.5–1.5)a
7.3 (.6.6–7.6)a 7.5 (7.1–7.9) 7.1 (6.1–7.9)
a
O2 (mg l-1)
141 (74–176)a
11.6 (9.3–12.3)a
8.8 (5.0–13.9)a
a
a
462 (338–581)ab
a
235 (192–275)
bc
197 (149–256)
ab
SRP (lg P l-1)
DIN (lg N l-1) 229 (178–354)a
1.9 (1.3–2.4)
bc
AV
1.5 (1.1–2.1)
abc
12.2 (4.8–18.8)
212 (173–233)a
AR
2.0 (1.9–2.1)cd
7.7 (7.5–8.1)a
214 (207–222)b
11.4 (9.8–13.0)a
11.4 (8.2–14.7)a
651 (530–727)b
CN
2.6 (2.3–2.8)d
7.3 (6.4–7.7)a
296 (284–314)c
11.8 (10.5–13.9)a
10.1 (6.6–13.8)a
775 (447–1189)b
FS
1.2 (1.0–1.5)ab
7.0 (6.4–7.2)a
263 (236–283)bc
11.3 (5.3–16.5)a
11.3 (5.3–16.5)a
1,971 (197–3,753)b
LLO
a
Conductivity (lS cm-1)
11.9 (9.8–13.0)
12.7 (10.8–14.8)
23.4 (6.4–66.7) a
Mean (range), n = 6 SRP soluble reactive phosphorus, DIN dissolved inorganic nitrogen Ammonium and nitrite were always low (B8 lg l-1). Bold cells indicate reference streams. Different letters indicate significant differences among streams (ANOVA, Tukey HSD test, P \ 0.05)
CA and LLO, respectively) in the Beso`s (Table 1). The streams were similar in size (mean channel width 6.1 ± 1.1 m and catchment area between 530 and 1,260 ha) and flowed mainly over siliceous substrate, through areas with scarce human settlements or activities (Table 1). During the study period (November 2009–February 2010) the mean air temperatures ranged from 2.0 to 9.2°C and the total rainfall was 251 mm.
manual salicylate method (Krom, 1980), nitrite by the sulphanylamide method and SRP by the molybdate method (APHA, 2005). In order to characterize the riparian vegetation, for each experimental stream five random perpendicular transects (10 m long and 1 m wide) were established on each side of 50 m long reaches. In each transect shrub and tree species were quantified in order to calculate riparian richness, density and percentage of exotic species.
Environmental variables Litter bags and decomposition During the study period (autumn–winter 2009–2010) and in all streams, the water temperature was continuously monitored with HOBO Pendant (Onset Computer Corporation, Bourne, MA, USA) temperature loggers. Conductivity, pH and dissolved oxygen were measured with a WTW multiparametric sensor (Weilheim, Germany). The instantaneous river flow was calculated from the instantaneous water velocity measured with a digital water velocity meter (FP311 flow probe) and the average stream section for each reach. Water was sampled and filtered through preashed glass fiber filters (Whatman GF/F) for nutrient and alkalinity analyses. Alkalinity was determined by titration to a pH endpoint of 4.5 (APHA, 2005). Nitrate concentration was determined by ion chromatography (COMPACT IC1.1 Metrohm), ammonium by the
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Alder leaves were collected in the banks of the Agu¨era river (Biscay-Cantabria) just after abscission in autumn 2009, air-dried to constant weight and stored until needed. Portions of 5.0 ± 0.25 g were weighed, moistened with a garden atomizer and placed in mesh bags (15 9 20 cm, 5 mm mesh). On 24 November 2009 leaf bags (20 in each stream) were tied with nylon lines to five iron bars driven into the streambed along an experimental 50 m reach in each stream. An extra set of five bags was immersed for 24 h in the most oligotrophic stream (AV) in order to correct the initial mass values for leaching. Five bags were retrieved (one bag per bar) after 7 days and, thereafter, on dates that roughly corresponded to 20 (t20), 50 (t50) and 70% (t70) loss of the initial mass. Incubation
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lasted 47–56 and 84–86 days in P. hybrida and reference streams, respectively. These sampling dates were estimated from exponential decomposition rates (k) recalculated from previous sampling data for each experimental site (Mene´ndez et al., 2011). The initial mass was considered to be the initial ash-free dry mass (AFDM) corrected for leaching. After retrieval, each litter bag was placed in individual zip-lock bags and transported in refrigerated containers to the laboratory, where they were immediately processed. The leaf material from each bag was rinsed with filtered stream water, and fauna from t20 and t50 samplings, which generally coincided with colonization peaks in alder leaves (Hieber & Gessner, 2002), were preserved in 70% ethanol for later analyses. Individuals, except chironomids, were identified to genus with a dissecting microscope, counted and sorted into functional feeding groups following Merritt & Cummins (1996) and Tachet et al. (2002). Individuals within each feeding group were dried at 70°C to constant weight (72 h) for biomass determinations. For aquatic hyphomycete sporulation rate determination, a set of five leaf disks (12 mm diam.) was cut with a flamed cork borer from each bag at t20 (2–3 weeks after immersion), which often coincides with the peak of conidial production on alder leaves (Pascoal & Ca´ssio, 2004). Leaf disks were incubated in 100 ml Erlenmeyer flasks with 25 ml filtered stream water (glass fiber Whatman GF/F filters) on a shaker (60 rpm) for 48 h at 10°C. The conidial suspensions were decanted into 50 ml centrifuge tubes, flasks rinsed twice with distilled water, and conidia fixed with 2 ml 37% formalin and stained with a few drops of Trypan Blue in lactic acid (ca. 0.05%), to be later counted and identified. For conidial identification, an aliquot of the suspension (calibrated depending on conidial concentration) was filtered onto Millipore SMWP nitrocellulose filters (5 lm pore size, opaque). Filters were further stained by placing them on a drop of Trypan Blue in lactic acid on a microscope slide and covered with 25 mm diam. coverslips. One quarter of each filter was scanned for conidia, which were identified and counted with bright-field microscopy at 2509. Counting effort was significantly reduced with the assistance of voice recognition and Excel data entry generator software (Mene´ndez et al., 2011). Sporulation rates were expressed as numbers of conidia released lg-1 AFDM day-1.
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The remaining material in each litter bag and the leaf disks were oven-dried (70°C, 72 h) and weighed, a portion used for nutrient analyses, and the rest ashed (550°C, 4 h) to determine the remaining AFDM. Data analyses Differences in physicochemical variables between streams were tested by a General Linear Model (GLM, mixed Type III) Nested analysis of variance (ANOVA), with streams nested within riparian forest type and riparian forest type as factor. Subsequent pair-wise comparisons were performed using Tukey’s Honest Significant Difference (HSD) test (Zar, 1999). Differences in riparian vegetation density and richness between P. hybrida and reference reaches were examined with Impaired Student’s t tests. After correcting the leaf litter initial mass for leaching, decomposition rates were estimated for comparative purposes by linear regressions of both lntransformed (negative exponential model Mt = M0* e-kt, where M0 is the initial AFDM, Mt is the remaining AFDM at time t, and k is the decomposition rate) and non-transformed data (negative linear model Mt = M0 - bt, where b is the decomposition rate). As streams differed in their water temperatures, decomposition rates were expressed in terms of time (days, d) and accumulated heat, replacing time by the sum of the mean daily temperatures accumulated by the sampling day (degree days, dd) (Stout, 1989). Analysis of covariance (two-way ANCOVA, test for homogeneity of slopes) was used to compare the effects of riparian vegetation (reference vs. P. hybrida) on leaf litter decomposition rate (% AFDM remaining as the dependent variable), using degree days as a covariate. Evenness (Buzas & Gibson’s index: eH/S, being H the Shannon diversity and S the species richness; Buzas & Hayek, 2005) of fungal communities associated with decomposing alder leaves was calculated from conidial abundances (PAST). Abundance and taxa richness of total macroinvertebrates and shredders (at t20 and t50), shredder biomass (at t50), sporulation rates of aquatic hyphomycetes and species richness and evenness of fungal communities (at t20) associated with leaf litter, were compared between P. hybrida and reference reaches by nested analysis of variance (ANOVA; streams nested within riparian forest
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type, riparian forest type and sampling time in macroinvertebrate abundance and richness, as factors). The influence of several variables that could be potential predictors of the decomposition rate was tested. A simple linear regression was fitted independently for all variables, with the decomposition rate as a response variable. Data were arcsine [% AFDM, dissolved inorganic nitrogen (DIN)] or log-transformed (shredder abundance and biomass) when needed to ensure normality, and tested for homogeneity of variance with the Levene test (P [ 0.05) (Legendre & Legendre, 1998). Statistical calculations were made with the CSS Statistica package. Non-metric multidimensional scaling (NMDS) ordination method based on the Bray–Curtis similarity matrix of relative abundance of aquatic hyphomycetes and macroinvertebrates (all samples) was performed with PAST (Hammer et al., 2001). Differences in hyphomycete and macroinvertebrate communities between reference and P. hybrida reaches were assessed by analysis of similarities (ANOSIM; Clarke, 1993) in the same program.
Hydrobiologia (2013) 716:5–20 Table 2 Results of the nested analyses of variance for physicochemical variables during the experiment
Riparian type
1
4
179.61 \0.0001
Stream (riparian type) Riparian type
4
24
25.47 \0.0001
1
4
0.94
0.34
Stream (riparian type)
4
24
1.21
0.33
DIN
123
Riparian type
1
4
21.33
Stream (riparian type)
4
24
1.83
0.0001 0.15
pH
Riparian type
1
4
0.01
0.91
4
24
1.79
0.16
Alkalinity
Stream (riparian type) Riparian type
1
4
11.33
0.002
Stream (riparian type)
4
24
12.66
0.0001
Riparian type
1
4
Stream (riparian type)
4
24
28.63 \0.0001 8.84
0.0002
Oxygen
Riparian type
1
4
1.89
0.24
4
24
0.67
0.52
Water flow
Stream (riparian type) Riparian type
1
4
2.41
0.13
Stream (riparian type)
4
24
5.65
0.002
Site characterization Physical and chemical characteristics in the streams did not significantly differ between riparian vegetation types (reference vs. P. hybrida) (Table 1), but differed among individual streams in DIN concentration, conductivity, alkalinity and temperature (Table 2). The only significant difference in stream flow was observed for AR (Tukey HSD, P \ 0.05) (Table 2). The riparian vegetation richness (t4 = -0.75, P [ 0.05) and density (t4 = 0.93, P [ 0.05) were not significantly different between P. hybrida and reference reaches. In reference reaches, no exotic riparian vegetation was observed, whereas in the P. hybrida reaches, the density of P. hybrida varied between 10.9 and 42.8%. The riparian canopy cover of P. hybrida ranged from 70.9 to 85.2% (Table 3) and the instream percentage cover of P. hybrida leaf litter in November was between 50% (AR) and 70% (FS) (data not shown). A. glutinosa was the only riparian tree species common to all six study reaches (Table 3).
P
Water temperature
Conductivity
Results
F
Source of variation
SRP
df1
df2
Variable
SRP soluble reactive phosphorus, DIN dissolved inorganic nitrogen
Litter decomposition, macroinvertebrates and aquatic hyphomycetes After 24 h of leaching, mass loss was 14 ± 0.65% (mean ± SE) and the decomposition dynamics were better adjusted to a linear (R2 = 0.91–0.97) than to an exponential model (R2 = 0.77–0.95) for all streams. Leaf litter decomposition was significantly faster (0.208–0.221% AFDM dd-1) in P. hybrida than in reference reaches (0.126–0.164% AFDM dd-1) (F1,156 = 51.5, P \ 0.00001; Fig. 2). Although the
Hydrobiologia (2013) 716:5–20 Table 3 Riparian vegetation species richness, density and percentage of P. hybrida density and canopy riparian cover in the studied reaches
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% P. hybrida density
% P. hybrida canopy cover
Stream
Riparian species
Richness
Density (trees m-2)
AV
Alnus glutinosa
6
0.39
0
0
6
0.28
0
0
6
0.33
0
0
4
0.21
42.8
72.8
6
0.35
28.6
85.2
6
0.46
10.9
70.9
Corylus avellana Buxus sempervirens Fraxinus angustifolia Ilex aquifolium Quercus Ilex LLO
Alnus glutinosa Buxus sempervirens Arbutus unedo Erica sp. Ilex aquifolium Pinus sylvestris
CA
Alnus glutinosa Corylus avellana Fraxinus angustifolia Juniperus oxycedrus Quercus Ilex Salix atrocinerea
CN
Alnus glutinosa Corylus avellana Platanus hybrida Pinus sylvestris
FS
Alnus glutinosa Corylus avellana Platanus hybrida Quercus ilex Fraxinus anguistifolia Quercus robur
AR
Alnus glutinosa Corylus avellana Platanus hibrida Ficus carica Salix atrocinerea
Bold cells indicate reference streams
Robinia pseudoacacia
DIN concentration was higher in P. hybrida than in reference streams, no significant relationship was observed between the decomposition rate and the DIN concentration (R2 = 0.42, P = 0.057). Total macroinvertebrate and shredder abundance and taxonomic richness (at the family level) were significantly higher in P. hybrida reaches (Fig. 3; Table 4). No significant difference in shredder biomass was observed between P. hybrida and reference reaches (Table 4). A
total of 34 macroinvertebrate taxa were identified associated with the litter bags. The NMDS analysis shows some differences in macroinvertebrate communities between P. hybrida and reference streams (ANOSIM, P = 0.0002 and R = 0.17, Fig. 4a), although there are some overlap. Plecopterans of the family Nemouridae were more abundant in P. hybrida streams and odonates were found only in reference streams (Table 5). Chironomidae were found in all the streams
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Hydrobiologia (2013) 716:5–20 F1.156=51.5, P<0.00001
0.25 0.2 0.15 0.1 0.05
ef er en ce
P.
R
br id a
0 hy
Decomposition rate (% AFDM dd -1)
12
Fig. 2 Alnus glutinosa decomposition rate mean ± SE) in P. hybrida and reference reaches
b
700 600
Macroinvertebrate richness (number families bag -1)
P. hybrida Reference
500 400 300 200 100
Shredder abundance (ind bag-1)
c
0
t20
d
80 70
16 14 12 10
Discussion
8 6 4 2 t20
t50
9 8
60 50 40 30 20 10 0
18
0
t50
Shredder richness -1 (number families bag )
-1
Macroinvertebrate abundance (ind bag )
a
(k dd-1,
7 6 5 4 3 2 1
t20
t50
0
t20
t50
Fig. 3 Total macroinvertebrate richness (a) and abundance (b), and shredder richness (c) and abundance (d) (mean ± SE) in litter bags in P. hybrida and reference reaches
but were most abundant in FS. We observed a significantly positive relationship (excluding the FS stream) between both average macroinvertebrate (R2 = 0.98,
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P = 0.0008, Fig. 5a) and average shredder richness (R2 = 0.81, P = 0.037, Fig. 5b) in t50 litter bags and decomposition rate. Aquatic hyphomycete sporulation rates were lower in P. hybrida streams (Fig. 6a), but no significant differences were found in conidia richness (Fig. 6b; Table 4). Species evenness of aquatic hyphomycetes associated with alder litter was significantly higher in P. hybrida streams (Fig. 6c; Table 4). A total of 25 species were identified across streams (Table 6). The dominant taxon was Flagellospora curvula except in CN, where F. curvula and Alatospora acuminata were codominants. Some differences were found in the aquatic hyphomycete communities between reference and P. hybrida reaches although some overlap was observed (ANOSIM, P = 0.003 and R = 0.18, Fig. 4b). Five fungal species associated with alder leaf litter were present only in P. hybrida streams: Lemonniera alabamensis, L. aquatica, L. cornuta, Tumularia aquatica and T. tuberculata. Geniculospora inflata was the only species found exclusively in reference streams though, in only one of them (CA), and with a very low abundance (Table 6).
Our results corroborate the hypothesis that replacement of the native riparian vegetation by P. hybrida increases the decomposition rate of A. glutinosa leaf litter. The higher DIN concentration found in P. hybrida streams could have stimulated microbial activity and decomposition. Many studies have documented positive effects of high stream nutrient concentrations on the leaf-associated microbial community and leaf breakdown (e.g. Elwood et al., 1981; Ferreira et al., 2006b). A higher DIN concentration would normally be expected to increase fungal activity (Suberkropp & Chauvet, 1995; Mene´ndez et al., 2011). However, the sporulation rates of aquatic hyphomycetes were lower in P. hybrida than in reference streams, and no significant relationship was observed between decomposition rates and DIN concentrations in this study, suggesting that differences in DIN concentration between streams do not explain the differences observed in decomposition rates. Differences in litter decomposition between stream types reflected the differences in macroinvertebrate
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Table 4 Results of the nested analyses of variance for biological variables: aquatic hyphomycete (t20) sporulation rate, species richness and evenness, macroinvertebrate and Variable Sporulation rate Hyphomycete richness Hyphomycete evenness Macroinvertebrate abundance
Macroinvertebrate richness
Shredder abundance
Shredder richness
Macroinvertebrate biomass Shredder biomass
Source of variation
shredder (t20 and t50) abundance and richness, and macroinvertebrate and shredder biomass (t50) df1
df2
F
P
Riparian type
1
4
13.46
0.001
Stream (riparian type)
4
24
9.09
0.0001
Riparian type
1
4
0.11
0.73
Stream (riparian type)
4
24
20.86
\0.0001
Riparian type
1
4
8.89
0.006
Stream (riparian type)
4
24
0.90
0.47
Riparian type
1
4
25.82
\0.0001
Stream (riparian type)
4
50
5.07
Sampling time
1
4
1.15
Riparian type
1
4
13.29
\0.0001
Stream (riparian type) Sampling time
4 1
50 4
18.62 0.17
\0.0001 [0.05
Riparian type
1
4
19.34
\0.0001
Stream (riparian type)
4
50
4.16
Sampling time
1
4
2.82
Riparian type
1
4
38.99
\0.0001
Stream (riparian type)
4
50
7.37
\0.0001
Sampling time
1
4
2.66
[0.05
Riparian type
1
4
0.09
0.76
Stream (riparian type)
4
50
0.98
0.43
Riparian type
1
4
1.52
0.23
Stream (riparian type)
4
24
1.54
0.22
and shredder colonization of alder litter; abundance and richness were higher in P. hybrida streams. Accordingly, a positive relationship was observed between decomposition rate and total macroinvertebrate and shredder richness. Alder litter might have attracted shredders in the reaches impacted by P. hybrida, where the main component of the litter is very refractory; alder litter is poorer in lignin (8 vs. 30.9% leaf dry mass, Gessner & Chauvet, 1994) and richer in nitrogen (2.55 vs. 0.52% leaf dry mass, Gessner & Chauvet, 1994; 3.05 vs. 0.73% leaf dry mass, this study) than P. hybrida litter, and is thus more palatable for shredders. This behaviour has been observed by other authors in streams lined by lowquality litter (e.g. beech, conifers), where the alder in the litter bags acts as an attractant for the more motile shredders (Rowe & Richardson, 2001; Zhang et al., 2003; Lecerf et al., 2005; Riipinen et al. 2009). This could explain the abundance of stoneflies of the family
0.001 [0.05
0.005 [0.05
Nemouridae in the litterbags in P. hybrida reaches. Reinhart & VandeVoort (2006) also reported more plecopterans of the family Nemouridae in litter in streams impacted by Acer platanoides in Montana. Hisabae et al. (2011) also reported a positive effect of conifer plantations on decomposition of the deciduous Euptelea polyandra litter and shredder abundance in Japanese streams, suggesting that the greater accumulation of leaf litter in the stream reach could be responsible for the higher abundance of benthic shredders in the conifer-lined streams. In the studied P. hybrida streams, we also observed a higher accumulation of P. hybrida leaf litter, which remained on the stream bed during the whole winter (Fig. 1), while there was no high accumulation of leaves in the reference streams. These differences in litter standing stock can be attributed to differences in the leaf fall timing between P. hybrida and reference streams (Acun˜a et al., 2007), to the lower retention of leaves of
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Hydrobiologia (2013) 716:5–20
a Stress:0.12 20
20 20
20
20
20 50
50
50 50
50
20 50 50 50
AV CN CA AR LLO FU
20 20
20 20 20 50 50 20 50 5050 50 5050 20 50 20 20 20 20 20 20 20 50 20 20 5050
50 50 50 20 20 20 5020 50 5050
50 50
50
b
Stress:0.07
Fig. 4 NMDS ordination plots of a macroinvertebrates and b fungal assemblages colonizing alder litter incubated in P. hybrida (filled symbols) and reference (open symbols) streams. The number behind the symbol in (a) represents the sampling time (t20 and t50)
native species due to their smaller size (Buxus sempervirens) and to their faster decomposition rate (Alnus glutinosa, Corylus avellana, fast and medium leaf decomposing categories, respectively, Lecerf et al., 2005). Our results corroborate the recent hypothesis (substrate quality-matrix quality interaction, SMI) formulated by Freschet et al. (2012), who predicted that high-quality leaf litter substrates will decompose faster than expected when incubated in a decomposing matrix of poor-quality litter (ecosystems receiving low-quality organic matter). In contrast, it expects the reverse trend from low-quality litter, which will show reduced decomposition rates in highquality matrices and increased rates in low-quality matrices. Therefore, in our case, the effects of P. hybrida plantations on stream ecosystems are not due
123
to changes in riparian species richness, as the riparian vegetation richness is not different between P. hybrida and reference reaches, but rather to changes in identity/quality of the contributing species to the detritus food web. When considering Fuirosos stream, the lack of a correlation between decomposition rate and richness of total macroinvertebrates and shredders is probably owed to the great abundance of Chironomidae larvae, which constituted 90% of the macroinvertebrates in the litter bags. Fuirosos is a temporary stream with a median discharge of 1.2 l s-1 (2001–2002; Bernal, 2006), and dry in summer. The contribution of chironomid larvae in accelerating plant litter decay and nutrient exchange was reported for shallow lakes and lagoons and for large rivers (Andersen & Jensen, 1991; Alvarez et al., 2001; Mene´ndez et al., 2003; Callisto et al., 2007). The hydrological conditions (average water flow of 4.1 l s-1) and trophic structure (high DIN concentration) at the end of the fall in this intermittent Mediterranean stream were very similar to those observed in shallow lakes and large rivers, mainly along their banks, where leaf litter accumulates. Therefore, the burrowing and gathering activities of these chironomid larvae may contribute significantly to detritus decomposition in this stream. This results supports the hypothesis that in some cases the rates of aquatic ecosystem processes are mainly determined by the activity of a single species (Wardle et al., 2002), either due to its direct influence on certain processes (Taylor et al., 2006) or through interspecific interactions (Boyero et al., 2007). Although a greater decomposition rate of alder leaves was observed in P. hybrida streams, there was no effect of vegetation type on sporulation rates; on the contrary, the aquatic hyphomycete activity was significantly higher in reference streams, suggesting that the variation in decomposition rates is a direct consequence of shredder abundance (Jonsson & Malmqvist, 2000; Zhang et al., 2003; Lecerf et al., 2005). These results suggest a bottom-up control of shredders by the characteristics of the riparian vegetation. Note, however, that we did not use fine mesh litter bags to separate decomposition mediated exclusively by microorganisms. Therefore our observations reflect the interactions among macroinvertebrate and aquatic hyphomycetes. Nevertheless, if the fungal activity had been assessed on
Hydrobiologia (2013) 716:5–20
15
Table 5 Percentage contribution of aquatic macroinvertebrate taxa in each experimental reach (based on the total number of macroinvertebrates after a 50% mass loss in the litter bags (t50) Family taxa
Order
FG
AV
LLO
CA
Capniidae
Plecoptera
Shr
0.8
1.0
Leuctridae
Plecoptera
Shr
0.7
2.4
0.3
Nemouridae
Plecoptera
Shr
1.1
3.8
0.5
Gammaridae
Crustacea
Shr
Sericostomatidae
Trichoptera
Shr
0.1
Limnephilidae
Trichoptrea
Shr
0.2
Odontoceridae
Trichoptera
Shr
Calamoceratidae
Trichoptera
Shr
Tipulidae
Diptera
Shr
Curculionidae
Coleoptera
Shr
Perlidae
Plecoptera
Pre
CN 10.0
1.0 10.6
0.8
2.2 0.6
0.7
2.6
0.9
0.5 0.1
0.2
Pre
0.1 0.5
Rhyacophilidae
Trichoptera
Pre
Athericidae Empididae
Diptera Diptera
Pre Pre
Ceratopogonidae
Diptera
Pre
Aeschnidae
Odonata
Pre
0.4 0.3
5.6
0.1
0.4
0.4
0.3
0.5
2.0 1.2 3.8
6.4 0.8
0.8 1.0
0.4
0.1
2.4
0.5
0.1
0.1
0.2
0.1
0.2
Calopterygidae
Odonata
Pre
Dytiscidae
Coleoptera
Pre
Glossiphoniidae
Hirudinea
Pre
Gomphidae
Ephemeroptera
Col-Gat
0.2
Leptophlebiidae
Ephemeroptera
Col-Gat
1.3
Heptageniidae
Ephemeroptera
Col-Gat
Oligochaeta
Oligochaeta
Col-Gat
0.1
Chironomidae
Diptera
Col-Gat
69.2
Psychodidae
Diptera
Col-Gat
Baetidae
Ephemeroptera
Col-Gat-Scr
Elmidae
Coleoptera
Col-Gat-Scr
0.1
Hydropsychidae Simuliidae
Trichoptera Diptera
Col-Filt Col-Filt
1.0 0.9
Ancylidae
Mollusca
Scr
0.2
0.2
22.8
5.3
Scr
Total number of taxa
0.3 0.1
Pre
Scr
0.1
0.1
Plecoptera
Mollusca
14.8
0.5
4.8
Trichoptera
Colleoptera
5.5
0.5
Polycentropodidae
Scirtidae
AR
2.8
Chloroperlidae
Bithyniidae
FS
1.6 0.0
0.5
1.1 1.2
68.8
1.1 3.9
1.9
0.5
1.0
0.3
0.2
0.1
0.4
76.0
63.6
90.1
0.1 0.4
0.8
0.4 0.1
2.6
0.6
0.6
2.1
1.2 0.7
0.8 13.1
63.6
0.1 0.1
19
14
14
23
8
25
Families are ordered by functional group (FG) AV Avenco´, LLO Llobina, CA Canovas, CN Castanyet, FS Furiosos, AR Arbucies, Shr shredder, Pred predator, Col collector, Gat gatherer, Filt filterer, Scr scraper Bold cells indicate reference streams
native leaf litter of lower quality (e.g. beech, Fagus sylvatica, or oak, Quercus robur), we hypothesize that the effect of fungal activity on litter
decomposition might have been stronger, due to the scarcity of more palatable leaf litter, such as that of alder.
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Hydrobiologia (2013) 716:5–20
Fig. 5 Linear relationship between alder decomposition rate and a average macroinvertebrate and b average shredder richness after a 50% litter mass was lost (t50) in bags (n = 5). Fuirosos (filled triangle) is bracketed, as it is considered an outlier
a
b
Decomposition rate (% AFDM dd -1)
0.25
( )
( ) 0.20 0.15 0.10 y = 0.007x + 0.096 R 2 = 0.98, P =0.0008
0.05 0.00
0 5 10 15 20 Average macroinvertebrate richness
b 4 3 2 1
14 12 10 8 6 4 2
P.
hy br id a
0
0.5 0.4 0.3 0.2 0.1
P.
Re fe re nc e
0 hy br id a
c
Aquatic hyphomycete eveness
P.
hy br id a
Re fe re nc e
0
16
Re fe re nc e
Aquatic hyphomycete richness (number species bag-1)
5
-1
-1
Sporulation rate (spores µ g d )
a
Fig. 6 Aquatic hyphomycete a sporulation rate, b species richness and c Buzas & Gibson’s evenness (mean ± SE) in P. hybrida and reference reaches
As reported in other studies (Laitung & Chauvet, 2005), fungal communities are composed of a few core species and a higher number of species of lower
123
y = 0.028x + 0.093 R 2 = 0.81, P =0.037
0
1 2 3 4 5 Average shredder richness
abundance. Flagellospora curvula dominated fungal assemblages in the streams studied, except in CN where it co-dominated with Alatospora acuminata. Both species can be very common in streams worldwide and have the capacity to release high numbers of conidia, which guarantee the quick colonization of new substrates (Webster & Descals, 1981). Some differences were observed in the aquatic hyphomycete community colonizing alder litter between streams. Although species richness was unaffected by P. hybrida riparian plantations, a significant effect was observed in evenness, and this effect is more evident if the temporary stream, FS, is not included. In north Spain, Ferreira et al. (2006a) also found a high evenness in aquatic hyphomycete communities associated with leaf litter in streams lined by eucalyptus plantations but with an understory of deciduous native species than in litter decomposing in streams crossing mixed deciduous forests. These authors suggested that a diversified leaf litter from deciduous trees and eucalyptus plantations might support a higher fungal diversity in eucalyptus streams; this could also have been the case here. P. hybrida streams, containing a diversified leaf litter quality might support a more diverse aquatic hyphomycete community, although riparian vegetation species richness per se was not different to reference streams. Also, the P. hybrida leaf litter could remain on the streambed for longer periods of time, owing to
Hydrobiologia (2013) 716:5–20
17
Table 6 Percentage contribution of aquatic hyphomycete species in each experimental reach (based on the total number of conidia, after a 20% mass loss in the litter bags (t20) Species
AV
Alatospora acuminata Ingold (sensu neotype)
LLO
CA
0.03 a
CN
FS
AR
0.07
0.03
9.94
7.50
0.82
24.85
0.30
Alatospora acuminata Ingold: pulchelloid morphotypea
1.83
0.07
0.70
2.48
0.04
Alatospora flagellata
0.01
0.01
Alatospora acuminata Ingold: subulate morphotype
Anguillospora longissima
0.05
0.01
Articulospora tetracladia Ingold
0.05
0.01
5.92 2.13 0.08
0.24
0.56 0.01
0.04
0.22
Clavariopsis aquatica de Wild.
0.45
0.01
2.38
0.16
7.08
Clavatospora longibrachiata Ingold
0.05
1.79
0.02
0.17
0.01
80.99
27.98
98.28
61.04
Flagellospora curvula Ingold
77.05
88.80
Geniculospora inflata (Ingold) Marvanova´ & S.V. Nilsson
0.01
Goniopila/Margaritisporaa
0.01
0.01
Heliscus lugdunensis Heliscella stellata (Ingold & Cox) Marvanova´
0.02
0.13
0.77
0.01 0.22
0.21
0.03
0.05
0.03
0.11
0.12
0.03
0.99
Lemonniera alabamensis Sinclair & Morgan-Jones
0.39
Lemonniera aquatica De Wild. Lemonniera cornuta Ranzoni Lemonniera terrestris Tubaki
7.07
0.10
4.46
1.07
Lunulospora curvula Ingold
0.74
0.18
0.14
0.11
1.32
0.03
14.31
Stenocladiella neglecta (Marvanova´ & Descals) Marvanova´ & Descals
0.36 0.03
0.12
0.03
1.57
0.01
1.20
1.88
Tetrachaetum elegans Ingold
1.19
6.69
7.96
5.52
Tetracladium marchalianum De Wild.
0.38
0.03
3.18
0.11
7.21
Tricladium chaetocladium Ingold
0.36
1.83
0.79
18.04
3.79
Tricladium angulatum
0.52
0.14
Tumularia aquatica
0.05
Tumularia tuberculata (Go¨nczo¨l) Descals & Marvanova´ Total number of species
0.02 17
13
16
16
14
21
Bold cells indicate reference streams a
cf. footnote in Table 6 of Pozo et al. (2011)
its lower breakdown rates, thus increasing leaf litter retentiveness and providing a steadily available resource for aquatic fungi.
Conclusions Our results suggest that the substitution of natural riparian plant species by P. hybrida plantations has a significant effect on ecosystem processes of the forested Mediterranean headwaters we have studied, by increasing alder litter decomposition rates. This result was probably due to the attraction of shredders to the nutrient richer alder leaf litter in the P. hybrida reaches, where most of the accumulated litter has low
N and P concentrations. From field observations in Mediterranean streams in Greece, Maliky (1990) described a change in feeding habits of amphipods and limnephilid larvae from shredding to scraping if no leaf litter except P. hybrida was available. This aspect would also be evidence of the limited quality of litter as a food source for shredders in streams impacted by P. hybrida. Considering that in such streams, most leaf litter inputs were of P. hybrida, the shredders are presumably limited by the availability of good quality leaf litter. Our findings support part of the SMI hypothesis, which expects that high-quality materials (e.g. alder leaf litter) will show increased decomposition rates in a low-quality matrix (i.e. P. hybrida litter, accumulated in the stream). Overall, we
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18
predict that the replacement of a natural riparian vegetation by P. hybrida plantations in Mediterranean streams, which change the timing as well as the quality and quantity of leaf litter resources in streams, might increase the C:N imbalance between consumers and resources, affecting the food web and ecosystem functioning. Acknowledgments This study was funded by the Spanish Ministry of Education and Science (projects CGL2007-462 66664-C04 and CGL2011-30474-C02). We are grateful to Antoni Gili for help with field work and two anonymous reviewers and the associate editor for comments on an earlier version of the paper. We thank the ‘‘Parc Natural del Montseny, Diputacio´ de Barcelona’’ for sampling permits.
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