litter decomposition in a temperate and a tropical stream: the effects of species mixing, litter...

Litter decomposition in a temperate and a tropical stream:the effects of species mixing, litter quality and shredders

ANDREAS BRUDER* , † , ‡ , MARKUS H. SCHINDLER*† , MARCELO S. MORETTI§ AND

MARK O. GESSNER* , † , ¶ , * *

*Swiss Federal Institute of Aquatic Science and Technology (Eawag), D€ubendorf, Switzerland†Institute of Integrative Biology (IBZ), Swiss Federal Institute of Technology (ETH), Zurich, Switzerland‡Department of Zoology, University of Otago, Dunedin, New Zealand§Laboratory of Aquatic Insect Ecology, University of Vila Velha, Vila Velha, Brazil¶Department of Experimental Limnology, Leibniz Institute of Freshwater Ecology and Inland Fisheries (IGB), Stechlin, Germany

**Department of Ecology, Berlin Institute of Technology (TU Berlin), Berlin, Germany

SUMMARY

1. The current rapid decline in biodiversity has led to concerns about the consequences for stream

ecosystem processes, one of which is the decomposition of leaf litter derived from riparian vegeta-

tion.

2. We conducted field experiments in a tropical and a temperate stream to test for the effects of

mixing leaf species differing in resource quality on the decomposition of leaf litter and on the

colonisation of the litter by leaf-shredding invertebrates.

3. The effects of litter mixing were minor compared with the effects of litter quality and the presence

or absence of shredders. Low shredder abundance in the tropical stream and poor quality of the

tropical leaf species, particularly in terms of phosphorus content and toughness, were associated with

low decomposition rates in the tropical compared with the temperate stream. This is especially true

when considering the 20 °C temperature differences between the two streams.

4. In the presence of shredders, the decomposition rate of a standard litter type, leaves of Alnus

glutinosa, was 2.6-fold faster in the temperate stream, whereas rates were similar when shredders

were absent. This indicates that differences in environmental conditions other than temperature had

a strong effect. Differences in water chemistry, such as higher concentrations of dissolved nutrients

in the temperate stream, might account for this effect.

5. In conclusion, despite a lack of clear effects of litter mixing on decomposition, our results highlight

the importance of litter identity and environmental conditions for both microbial and shredder-

mediated litter decomposition, suggesting that changes in riparian vegetation and other stream

characteristics will affect stream ecosystems in the face of widespread environmental change.

Keywords: biodiversity and ecosystem functioning, leaf breakdown, leaf mixing, litter quality, shredders,streams

Introduction

Growing concern over the consequences of a global

decline in biodiversity (Dudgeon et al., 2006; Naeem,

Duffy & Zavaleta, 2012) for ecosystem processes has

prompted extensive research into the relationships

between them (Cardinale et al., 2012). Central to this

question is the role of interactions among species with

direct or indirect effects on ecosystem processes, such as

primary production, organic matter decomposition and

various other processes involved in the cycling of energy

and nutrients (Gessner et al., 2010; Hooper et al., 2012).

In forest streams, as in numerous other ecosystems,

communities strongly rely on allochthonous energy and

nutrient inputs from terrestrial vegetation (Wallace et al.,

1997), because riparian canopies limit instream primary

Correspondence: Andreas Bruder, Department of Zoology, University of Otago, PO Box 56, Dunedin, New Zealand.

E-mail: [email protected]

© 2013 John Wiley & Sons Ltd 1

Freshwater Biology (2013) doi:10.1111/fwb.12276

production and supply large amounts of organic matter

during litter fall (Webster, 2007). Leaf litter represents

the most important fraction of allochthonous inputs; it is

readily colonised and used by aquatic decomposers,

notably fungi and detritivores classified as shredders

(Gessner, Chauvet & Dobson, 1999; Tank et al., 2010).

However, there are substantial differences in the

resource quality of litter, because leaves of different

riparian tree species vary in concentrations of chemical

constituents such as lignin, tannins, nitrogen and phos-

phorus (Gessner & Chauvet, 1994; H€attenschwiler, Coq

& Handa, 2011). Litter quality in turn controls the activ-

ity and abundance of microbial decomposers and shred-

ders associated with the litter and hence litter

decomposition rate (Gessner & Chauvet, 1994; Hladyz

et al., 2009).

In mixed-species litter, the quality of a given leaf

species not only determines its own decomposition rate

but might also influence the decomposition of other spe-

cies included in the mixture (Gessner et al., 2010; Lecerf

et al., 2011). Such neighbour effects can be mediated, for

instance, through transfer of nutrients (Schimel &

H€attenschwiler, 2007; Lummer, Scheu & Butenschoen,

2012) or soluble inhibitory substances (McArthur et al.,

1994). Furthermore, litter mixtures can give rise to situa-

tions in which microbial decomposers and shredders

can benefit from the availability of complementary

resources, thus increasing decomposer activity and

decomposition rate (H€attenschwiler, Tiunov & Scheu,

2005; Gessner et al., 2010). Because of their ability to

select high-quality litter, shredders might play a particu-

larly important role in generating litter-mixing effects on

decomposition (Sanpera-Calbet, Lecerf & Chauvet, 2009).

However, although observed in both terrestrial

(H€attenschwiler et al., 2005) and aquatic ecosystems

(Kominoski et al., 2010; Lecerf et al., 2011), synergistic

effects on decomposition resulting from litter mixing

remain relatively weak overall (Hooper et al., 2012) and

insufficiently understood (Gessner et al., 2010).

Part of this difficulty could be due to variation in

environmental context, which determines the set of

mechanisms potentially leading to mixing effects (McKie

et al., 2009; Lecerf et al., 2011). Geographic location

encapsulates key dimensions of context dependency by

dictating not only physicochemical environmental

conditions (e.g. temperature and nutrient supply) but

also the quality of litter supplied to streams, and the

composition and relative importance of microbial

decomposer and shredder communities (Boyero et al.,

2011a). Therefore, comparative experiments at different

locations could help elucidate the factors responsible for

litter-mixing effects on decomposition. Particularly

useful might be comparisons of tropical and temperate

systems (Grac�a et al., 2001; Wantzen & Wagner, 2006;

Grac�a & Cressa, 2010; Ferreira, Encalada & Grac�a, 2012)because of large systematic differences in environmental

conditions such as temperature (Boyero et al., 2011a),

litter quality (H€attenschwiler et al., 2011) and the impor-

tance of shredders (Irons et al., 1994; Boyero et al.,

2011b).

In this study, we assessed litter-mixing effects on

decomposition and the relative role of microbial and

shredder-mediated decomposition in a tropical and a

temperate forest stream, using identical methods. We

hypothesised that litter-mixing effects are more pro-

nounced in the temperate than the tropical stream

because of large differences in shredder prevalence and

litter quality. Specifically, our rationale was that the

general scarcity of shredders in tropical streams (Boyero

et al., 2011b) narrows the scope of potential mechanisms

causing litter-mixing effects, and that the prevalence of

tropical tree species with well-defended leaves

(H€attenschwiler et al., 2011) reduces differences in the

quality of dominant litter types in spite of high tree

diversity in the tropics. Thus, by comparing the decom-

position of litter mixtures in a tropical and a temperate

stream, we aimed at comparing the importance of litter-

mixing effects in two contrasting situations.

Methods

Study sites

Experiments were conducted in a temperate upland and

a tropical lowland stream chosen for contrast in terms of

environmental conditions, the occurrence of shredders

and the quality of leaf litter supplied by riparian vegeta-

tion. The same experimental design and identical proce-

dures were applied at both locations. The study in the

temperate zone was conducted in the Steina, a third-

order stream draining a catchment of managed forest

(mainly spruce, Picea abies) in the Black Forest of south-

western Germany (47°47′51″N, 8°19′28″E; Table 1). The

riparian vegetation was composed of mixed deciduous

tree species dominated by black alder, Alnus glutinosa.

The experiment was started in early November 2006,

shortly after peak leaf fall, and lasted until early January

2007. The tropical study was conducted in a second-

order stream draining a catchment near Petit Saut,

French Guyana (5°04′05″N, 53°00′28″W; Table 1). The

site was located in unmanaged lowland rainforest with

high tree species richness (H€attenschwiler et al., 2011).

© 2013 John Wiley & Sons Ltd, Freshwater Biology, doi: 10.1111/fwb.12276

2 A. Bruder et al.

The experiment extended from early May to early July

2007, corresponding to a period of increased litter fall,

although seasonal patterns of litter fall were not pro-

nounced. Water temperature was recorded at hourly

intervals throughout the experiments in both streams.

Experimental design and procedures

Naturally fallen leaf litter of three tree species common

in the riparian vegetation of the respective stream was

collected upon abscission near the study sites. The litter

species were chosen to cover a gradient in litter quality

and decomposition rates to increase the potential for

mixture effects to occur (Table 2). The species exposed

in the temperate stream included beech (Fagus sylvatica),

maple (Acer platanoides) and ash (Fraxinus excelsior). The

species used in the tropics were Eperua falcata, Vochisia

densiflora and Qualea rosea. In addition, black alder

(A. glutinosa), collected from the ground immediately

after natural abscission, was exposed in both streams as

a standard leaf material to enable comparisons between

locations independently of local litter quality.

Leaf litter was dried at 40 °C and weighed to the

nearest 5 mg in batches of 3.0 � 0.1 g for single-species

litter and of 3.0 � 0.3 g for species mixtures. The

batches were then wetted to avoid fragmentation of

leaves during handling and placed in coarse-mesh (10-

mm aperture) and fine-mesh (0.28-mm aperture) bags

(size: 17 9 25 cm). Mixed-species litter bags consisted of

equal proportions (by mass) of the three constituent spe-

cies. Alder was not exposed in species mixtures. The

bags were closed with nylon cord (coarse-mesh bags) or

hot glue (fine-mesh bags), kept moist until transport to

the field the next morning and submerged in the

streams in three adjacent riffles.

Three replicate fine-mesh and coarse-mesh bags were

retrieved from the temperate stream after 14, 28 and

56 days and after 14, 26 and 55 days from the tropical

stream. During retrieval, litter bags were placed in sub-

merged plastic bags held downstream of the litter bags

to minimise loss of associated invertebrates. The

retrieved litter was gently cleaned under flowing tap

water in the laboratory, and the material retained by a

0.25-mm mesh screen sorted according to leaf species.

The sorted litter was oven-dried to constant weight

(65 °C) and weighed to the nearest 5 mg. Conversion

factors relating the initial mass of litter dried at 65 °C

and 40 °C were established for each species from extra

litter of the same batches used in the field studies. Fur-

thermore, mass loss due to leaching was estimated by

submerging three weighed litter batches of each species

in flowing tap water for 24 h and subsequently drying

and weighing.

The invertebrates retained by the 0.25-mm mesh

screen were preserved in 70% ethanol and later identified

to the lowest possible taxonomic level under a dissecting

microscope and assigned to functional feeding groups

based on various literature sources (Iversen, 1988; Mug-

nai, Nessimian & Baptista, 2009). Body length of the

invertebrates from the temperate stream was measured

to the nearest 0.5 mm and head capsule width of the

tropical invertebrates to the nearest lm. These data were

converted to biomass (dry mass) using established allo-

metric relationships for the same or related taxa (e.g.

Meyer, 1989). Invertebrate abundance was also estimated

Table 1 Characteristics of the temperate and tropical study

streams

Parameter

Temperate stream Tropical stream

Mean SD N Mean SD N

Stream order 3 – – 2 – –

Altitude (m a.s.l) 750 – – 35 – –Duration of

experiment (d)

56 – – 55 – –

Water

temperature (°C)4.2 2.2 1344 24.4 0.3 1320

Alkalinity (mM) 0.57 0.1 8 0.23 – 1

Oxygen (mg L�1) 10.9 0.9 8 n.d. n.d. 0

pH 6.6 0.1 8 7.7 – 1

Conductivity (lS cm�1) 97 13 8 19 – 1

NO3� (lg N L�1) 691* 44 4 <20.0 – 1

NH4+ (lg N L�1) 7.6* 1.1 4 <5.0 – 1

PO43� (lg P L�1) 15.8* 0.7 4 <1.0 – 1

SD, standard deviation; N, number of measurements.

*Data from autumn 2007 (A. Frainer, M.S. Moretti, W. Xu, M.O.

Gessner, unpublished data).

Table 2 Characteristics of the four temperate and three tropical

litter species used in the experiments. Nutrient and lignin concen-

trations are reported in per cent of litter dry mass. Values represent

means � 1 standard deviation (N = 3, except for leaf toughness

where N = 5)

Litter

species N (%) P (%) Lignin (%)

Toughness

(g)

Temperate species

Alnus glutinosa 2.32 � 0.28 0.068 � 0.007 9.12 � 0.67 136 � 38

Fraxinus excelsior 1.41 � 0.02 0.186 � 0.032 3.92 � 0.60 148 � 17

Acer platanoides 0.57 � 0.09 0.071 � 0.008 16.9 � 1.96 97 � 6

Fagus sylvatica 0.53 � 0.10 0.013 � 0.006 32.3 � 2.73 171 � 16

Tropical species

Eperua falcata 1.28 � 0.05 0.036 � 0.001 29.2 � 1.80 213 � 49

Vochisia densiflora 0.92 � 0.08 0.023 � 0.003 20.6 � 1.16 249 � 40

Qualea rosea 0.75 � 0.05 0.010 � 0.004 7.79 � 0.50 330 � 119


Litter decomposition in a temperate and a tropical stream 3

from 90 litter packs similar in size to our experimental

packs collected from nine other streams of the same type

(i.e. stream order, riparian vegetation, human impact in

the catchment) in several catchments near the tropical

stream used in the decomposition experiment.

Initial litter quality was assessed from litter material

of the original batches that had been ground with a

planetary mill (Retsch PM 400, Hahn, Germany). Nitro-

gen content was determined with a Thermo-Finnigan

NC EA 1112 elemental analyser (Strada Rivoltana,

Milan, Italy) and phosphorus with the molybdate blue

method following digestion with peroxodisulphate

(Ebina, Tsutsui & Shirai, 1983). Lignin was determined

by the Van Soest forage fibre method as described in

Gessner (2005). In addition, leaf toughness was esti-

mated for five intact leaves per species that had been

soaked in water before making measurements with a

precision penetrometer (C-2006 MkII, Townsville, Aus-

tralia; Pearson & Connolly, 2000) fitted with a blunt steel

pin 1.55 mm in diameter. The weight pushing the pin

down through the leaf tissue was gradually increased by

adding water to a beaker that was placed on a platform

connected to the steel pin. Five measurements were

made per leaf, avoiding the principal and secondary

veins. Reported means and standard deviations are

based on averaged values of the individual leaves.

Data analysis

Exponential decay rates were estimated by nonlinear

regression analysis using data on litter mass remaining.

Starting values for the nonlinear regressions were

obtained from the respective linear regression models

with log-transformed data. In addition, decay rates were

determined by regressing litter mass remaining against

thermal sums (degree-days), rather than elapsed time in

days, with thermal sums calculated by summing average

daily temperatures. Values from mixed and monospe-

cific litter bags were pooled for these regression models,

and intercepts were not fixed because the estimates were

close to 100% initial mass (i.e. within �6%).

Data on litter mass remaining and invertebrate bio-

mass were analysed using sequential linear models.

These models tested for effects of location, litter species

nested in location, litter mixing, mesh size, exposure

time in the streams and the interactions of these vari-

ables. Because of nesting of species in location, the effect

of location was tested against species, all other factors

and interactions against the residual error. For litter

mass loss, exposure time was log-transformed and

included in the model as a covariate, reflecting exponen-

tial decay of the litter (Boulton & Boon, 1991). Since

alder was not included in the litter mixtures, mass loss

of this species was tested with a separate model omit-

ting the litter species and litter-mixing terms. Effects on

litter mass loss were tested with both uncorrected data

and data corrected for initial leaching losses.

Because of very low invertebrate numbers in the tropi-

cal samples (e.g. six individuals of shredders in total),

statistical tests for effects on invertebrate biomass were

restricted to samples from the temperate stream (coarse-

mesh litter bags only) using a three-way ANOVA testing

for effects of litter-mixing, litter treatment (N = 5: all

four litter species alone plus the three-species mixture)

and sampling date. Because of nesting, the litter treat-

ment term was tested against the litter-mixing term. This

analysis was based on the assumption that sampling

dates were independent, because the data structure did

not allow alternative analyses. In particular, a repeated-

measures analysis could not be applied because some

litter bags were lost from some experimental blocks.

Pairwise differences were tested by Tukey’s HSD tests.

The statistical analyses were performed separately for

shredder and non-shredder biomass.

Model assumptions (i.e. normal distribution of residu-

als and homoscedasticity) were checked by diagnostic

plots, and the response variables were transformed

when necessary. Data for the model testing for effects

on mass loss of local litter species were Box–Cox trans-

formed [Y′ = (Y1.7�1)/1.7] using the R package MASS

(Venables & Ripley, 2002), whereas the model testing for

effects on mass loss of alder litter did not require trans-

formation. The invertebrate biomass data were trans-

formed using the natural logarithm [Y′ = loge(Y + 1)] for

both shredders and non-shredders. All statistical analy-

ses were performed with R 2.11.1 (R Development Core

Team, 2010).

Results

Litter mass loss varied greatly among litter species

(Fig. 1). Mass loss at the end of the experiment in

the temperate stream ranged from 95.4 � 3.8%

(mean � 95% CI) for ash in single-species litter bags

with coarse mesh to 17.8 � 6.0% for beech in mixed-

species bags with fine mesh. In the tropics, litter mass

loss ranged from 50.7 � 11.0% for Qualea rosea in mixed-

species, coarse-mesh bags to 20.7 � 12.1% for Eperua

falcata in single-species, fine-mesh bags. Litter mass loss

due to leaching also varied substantially among species

(Fig. 1), ranging from an estimated 31.5 � 11.8% in ash

to 0.0 � 2.5% in beech. Average mass loss rates across


4 A. Bruder et al.

litter species were of the same magnitude in the tropical

and temperate stream; however, rates differed greatly

when expressed on a degree-day basis (Table 3). Mass

loss in the temperate stream conformed to an exponen-

tial decay model, whereas the fit was relatively poor for

the tropical species (Fig. 1). Mixing litter species rarely

affected litter mass loss, and any significant effects

varied with location, elapsed time and decomposer com-

munities (Fig. 1; Table 4). Therefore, the effect of litter

mixing was small compared with those of the other

factors tested (i.e. stream, litter species, decomposer

community and decomposition stage).

Effects of mesh size differed between locations and

among litter species at both locations, resulting in an up

to 43.4% greater mass loss of leaves from coarse-mesh

compared with fine-mesh litter bags after 8 weeks

(maple litter in the temperate stream; Fig. 2). However,

the strength of the mesh-size effect varied among litter

species. In beech litter, for example, the difference in

mass loss from coarse- and fine-mesh bags was less than

3.5%. In the tropical stream, a clear mesh-size effect was

not apparent (Fig. 1). Results were very similar when

statistical tests were performed based on data corrected

for initial leaching losses (data not shown).

The mass loss of alder litter was similar in fine-mesh

bags at both locations and also between coarse-mesh

and fine-mesh bags in the tropical stream (Fig. 3;

Table 5). In contrast, alder litter decomposed about

2.6-fold faster in coarse-mesh bags exposed in the tem-

perate stream, resulting in 33% less litter mass remain-

ing at the end of the experiment than in fine-mesh bags

(Fig. 3; Table 3). The difference in decomposition rate

Litte

r mas

s re

mai

ning

(%)

Eperua falcataVochisia densifloraQualea rosea50

60

70

80

90

100

Eperua falcataVochisia densifloraQualea rosea 50

60

70

80

90

100

Time (d)Time (dd)

0

20

40

60

80

100

Litte

r mas

s re

mai

ning

(%)

1 56

0

20

40

60

80

100

1 56

Fagus sylvaticaAcer platanoidesFraxinus excelsior

F. sylvaticaAcer platanoidesFraxinus excelsior

Time (d)Time (dd) 237

1 14 26 55 1 14 26 55370 664 1369 370 664 1369

14 28 14 28 85 164 85 164 237

(a) (b)

(c) (d)

Fig. 1 Leaf litter dry mass remaining in coarse-mesh (a, c) and fine-mesh (b, d) bags retrieved from a temperate (a, b) and a tropical stream

(c, d) as a function of litter species, litter mixing and elapsed time in days (d) or thermal sums in degree-days (dd). Open symbols and

dashed lines represent litter exposed in mixed-species bags, full symbols and solid lines represent single-species litter bags. Grey symbols

denote mass loss during 24-h leaching in the laboratory. Values are means � 1 SE (N = 3). When error bars are not shown, they are smaller

than the symbols. Note the differences in the y-axis range between the top and the bottom panels.



between coarse-mesh bags in the tropical and temperate

stream increased to a factor of 10.8 when expressed

per degree-day, due to the large temperature differ-

ences (Table 1). Similarly, the decomposition rate in

fine-mesh litter bags, similar when calculated based on

elapsed time, differed greatly (i.e. fivefold) between

the tropical and temperate stream when expressed

per degree-day.

Total invertebrate abundance and biomass were negli-

gible in fine-mesh bags retrieved from both the tropical

and temperate stream. In coarse-mesh bags retrieved

–10

0

10

20

30

40

50

0 56Time (d)Time (dd)

14 2885 164 237

Fagus sylvaticaAcer pseudoplatanus

Fraxinus excelsior

Shre

dder

-med

iate

d m

ass

loss

(%)

*

**

Alnus glutinosa

Fig. 2 Litter mass loss attributed to shredders in a temperate

stream as a function of litter species, litter mixing and elapsed time

in days (d) or thermal sums in degree-days (dd). Open symbols

and dashed lines represent mass loss of litter from mixed-species

bags, full symbols and solid lines represent mass loss from single-

species litter bags. Values are means � 1 SE (N = 3). When error

bars are not shown, they are smaller than the symbols.

Table 5 Effects of location (L), mesh size (M), litter exposure time

(T) and the interactions of these factors on mass loss of alder litter

in two contrasting streams

Source of variation d.f. SS F P

Location (L) 1 1329 20.3 <0.001

Mesh size (M) 1 1565 23.9 <0.001

Time (T) 1 7187 109.6 <0.001

L 9 M 1 1484 22.6 <0.001

L 9 T 1 288 4.4 0.045

M 9 T 1 332 5.1 0.032

L 9 M 9 T 1 175 2.7 0.113

Residual error 28 1835

Total 213 14 198

Significant probability values (P < 0.05) are highlighted in bold

characters.

Table 3 Exponential litter decay rates calculated as a function of

time in days (kd) and of thermal sums in degree-days (kdd). Values

represent means � 95% confidence intervals (N = 24, except for Al-

nus glutinosa, where N = 12, and for Fraxinus excelsior and Fagus

sylvatica, where N = 23 because a litter bag was lost)

Litter species Mesh kd kdd

Temperate stream

Alnus glutinosa Coarse 0.0506 � 0.0106 0.00909 � 0.00214

Alnus glutinosa Fine 0.0193 � 0.0052 0.00403 � 0.00089

Fraxinus excelsior Coarse 0.0608 � 0.0071 0.01040 � 0.00104

Fraxinus excelsior Fine 0.0316 � 0.0070 0.00613 � 0.00105

Acer platanoides Coarse 0.0213 � 0.0039 0.00423 � 0.00098

Acer platanoides Fine 0.0097 � 0.0015 0.00210 � 0.00034

Fagus sylvatica Coarse 0.0046 � 0.0006 0.00102 � 0.00013

Fagus sylvatica Fine 0.0038 � 0.0006 0.00090 � 0.00011

Tropical stream

Alnus glutinosa Coarse 0.0210 � 0.0064 0.00084 � 0.00024

Alnus glutinosa Fine 0.0201 � 0.0055 0.00080 � 0.00020

Qualea rosea Coarse 0.0114 � 0.0020 0.00046 � 0.00008

Qualea rosea Fine 0.0086 � 0.0020 0.00035 � 0.00008

Vochisia densiflora Coarse 0.0061 � 0.0010 0.00025 � 0.00004

Vochisia densiflora Fine 0.0062 � 0.0010 0.00025 � 0.00004

Eperua falcata Coarse 0.0049 � 0.0009 0.00020 � 0.00004

Eperua falcata Fine 0.0047 � 0.0008 0.00019 � 0.00003

Table 4 Effects of location (L), litter mixing (X), litter species

nested in location (S), mesh size (M), litter exposure time (T) and

the interactions of these factors on litter mass loss in two contrast-

ing streams. Alder litter was excluded from this analysis

Source of variation d.f. SS (9104) F P

Location (L) 1 709.6 1.7 0.26

Mixing (X) 1 0.1 0.1 0.78

Species(Location) (S) 4 1677.0 345.0 <0.001

Mesh size (M) 1 47.7 39.2 <0.001

Time (T) 1 708.4 583.0 <0.001

L 9 X 1 0.6 0.5 0.49

L 9 M 1 17.4 14.3 < 0.001

L 9 T 1 4.1 3.3 0.069

X 9 S 4 4.2 0.9 0.48

X 9 M 1 1.4 1.2 0.28

X 9 T 1 0.0 0.0 0.84

S 9 M 4 30.8 6.3 <0.001

S 9 T 4 58.5 12.0 <0.001

M 9 T 1 7.1 5.8 0.017

L 9 X 9 M 1 0.4 0.4 0.55

L 9 X 9 T 1 0.6 0.5 0.48

L 9 M 9 T 1 4.5 3.7 0.057

X 9 S 9 M 4 2.1 0.4 0.78

X 9 S 9 T 4 3.2 0.7 0.63

X 9 M 9 T 1 1.2 1.0 0.33

S 9 M 9 T 4 8.0 1.7 0.16

L 9 X 9 M 9 T 1 5.1 4.2 0.043

X 9 S 9 M 9 T 4 7.7 1.6 0.18

Residual error 166 201.7

Total 213 3501.4

Significant probability values (P < 0.05) are highlighted in bold

characters.


6 A. Bruder et al.

from the tropical stream, both abundance and biomass

were exceedingly low. Similarly, low abundances of

invertebrates, and especially shredders (total of six indi-

viduals in 90 samples from nine similar streams), were

also found in natural litter packs. By contrast, shredders

accounted for most of the total invertebrate abundance

(66.5%) and biomass (63.5%; Fig. 4) in the coarse-mesh

bags from the temperate stream, ranging from near zero

on alder and ash litter after 56 days to almost 37 mg per

litter bag in maple after 28 days. Mixed-species litter in

the temperate stream attracted a biomass of shredders

similar to that in bags of the component species

(F1,27 = 0.06, P = 0.82; Fig. 4a) but differed among the

five litter treatments (F3,27 = 4.03, P = 0.017), sampling

dates (F2,27 = 4.59, P = 0.019) and the interaction of these

factors (F6,27 = 4.01, P = 0.005). Significant differences in

shredder biomass between litter treatments were due to

differences between shredder biomass collected from

maple and alder litter on the second sampling date

(Tukey’s HSD test, P = 0.048; Figs 4a,c). Biomass of non-

shredders was similar between different litter-mixing

levels (F1,27 = 0.98, P = 0.40; Fig. 4b) but differed signifi-

cantly among litter treatments (F3,27 = 4.13, P = 0.016)

but not among sampling dates or the interaction of these

factors (P > 0.1). The only significant difference of non-

shredder biomass was detected between beech and alder

litter on the third sampling date (Tukey’s HSD test,

P = 0.04; Fig. 4b,c).

Ald

er li

tter m

ass

rem

aini

ng (%

)

0

20

40

60

80

100

Time (d)Time (dd)

Coarse meshFine meshLeached0

20

40

60

80

100

1 56 1 14 26 55 370 664 1369

14 28 85 164 237

Coarse meshFine meshLeached

(a) (b)

Fig. 3 Dry mass of alder litter remaining in a temperate (a) and a tropical stream (b) as a function of elapsed time in days (d) or thermal

sums in degree-days (dd). Full symbols and solid lines represent alder litter exposed in coarse-mesh litter bags, open symbols and dashed

lines represent litter from fine-mesh bags. Grey symbols denote mass loss during 24-h leaching in the laboratory. Values are means � 1 SE

(N = 3). When error bars are not shown, they are smaller than the symbols.

0

0

10

20

30

40

50

Inve

rtebr

ate

biom

ass

(mg)

0

10

20

30

40

50

Time (d)Time (dd)

56237

0 56237

Fagus sylvaticaAcer pseudoplatanusFraxinus excelsiorLitter mixtures

Fagus sylvaticaA. pseudoplatanusF. excelsiorLitter mixtures

0

0

10

20

30

40

50

5614 2885 164

14 2885 164

14 2885 164 237

ShreddersOthers

(a) (b) (c)

Fig. 4 Dry mass of shredders (a) and all other functional feeding groups (b) as a function of litter species, litter mixing and elapsed time in

days (d) or thermal sums in degree-days (dd), as well as dry mass of invertebrates from alder litter (c). Data are means � 1 SE (N = 3) for

coarse-mesh litter bags retrieved from a temperate stream. When error bars are not shown, they are smaller than the symbols.



Discussion

Litter-mixing effects

Distinct variation in decomposition rates among litter

species is a prerequisite for mixing effects to arise in

experiments on the relationship between biodiversity

and ecosystem processes (Gessner et al., 2010; Lecerf

et al., 2011). This condition was met in the tropical and

especially in the temperate stream of the present study.

The temperate stream also had an abundance of shred-

ders (Table 6) that strongly promote decomposition

(Hieber & Gessner, 2002), as further demonstrated by a

much faster mass loss from coarse-mesh compared with

fine-mesh bags in the present study. In contrast, the

tropical stream had much lower shredder abundance

(Table 7), reflecting a broad biogeographical pattern

across latitude (Boyero et al., 2011b, 2012), although

exceptions to the rule of poor shredder representation in

the tropics have recently been reported, mostly from

streams at higher altitudes (Camacho et al., 2009; Yule

et al., 2009; Encalada et al., 2010; Ferreira et al., 2012).

In spite of the ‘favourable’ conditions for litter-mixing

effects to occur at least in the temperate stream, such

effects proved unimportant in any of the four situations

we examined, that is, exclusion or inclusion of shredders

by means of fine-mesh and coarse-mesh litter bags,

respectively, in both our temperate and tropical stream.

This outcome reinforces a growing body of evidence

(LeRoy & Marks, 2006; Bastian et al., 2007; Lecerf et al.,

2007; Moretti, Gonc�alves & Callisto, 2007; Schindler &

Gessner, 2009; Dudgeon & Gao, 2011) suggesting that

pronounced litter-mixing effects on decomposition in

streams are rarely apparent on short temporal scales

(but see Lecerf et al., 2011).

This lack of a clear litter-mixing effect also agrees with

results from another comparative study on litter decom-

position in a temperate and a tropical stream, which used

a similar experimental design and also failed to detect

effects of species richness effects per se on litter mass loss

Table 6 Invertebrate abundance and biomass (dry mass) of all

litter samples retrieved from the temperate stream

Taxon FFG

Biomass Abundance

(mg) (%) (�) (%)

Ephemeroptera

Habroleptoides modesta COL 13.5 1.2 18 1.0

Epeorus sylvicola SCR 12.6 1.1 10 0.6

Rhithrogena sp. SCR 12.0 1.1 33 1.8

Baetis sp. SCR 7.9 0.7 41 2.3

Ephemerella sp. COL 4.6 0.4 26 1.5

Plecoptera

Protonemura sp. SHR 582.8 51.9 784 43.9

Nemoura sp. SHR 60.7 5.4 214 12.0

Leuctra sp. SHR 47.2 4.2 171 9.6

Isoperla sp. PRE 35.9 3.2 164 9.2

Nemurella sp. SHR 13.6 1.2 47 2.6

Taeniopteryx hubaultii SHR 13.5 1.2 7 0.4

Perlodidae PRE 4.0 0.4 4 0.2

Trichoptera

Hydropsyche sp. FIL 226.1 20.1 132 7.4

Rhyacophila sp. PRE 54.0 4.8 31 1.7

Limnephilidae SHR 5.1 0.5 7 0.4

Sericostoma personatum SHR 3.0 0.3 3 0.2

Diptera

Simuliidae FIL 8.9 0.8 45 2.5

Chironomidae* COL 8.9 0.8 42 2.4

Dicranota sp. PRE 4.0 0.4 4 0.2

Atherix ibis PRE 3.6 0.3 2 0.1

Coleoptera

Elmidae (ad.) SCR 1.0 0.1 1 0.1

Hydraena sp. (ad.) COL 0.2 < 0.1 1 0.1

Total 1123.1 1787

FGG, functional feeding group; COL, collector–gatherers; SCR,scrapers; SHR, shredders; PRE, predators; FIL, collector–filterers.

*Few Tanypodinae.

Table 7 Invertebrate abundance and biomass (dry mass) of all

litter samples retrieved from the tropical stream

Taxon FFG

Biomass Abundance

(mg) (%) (�) (%)

Ephemeroptera

Leptophlebiidae COL* 1.5 10.7 8 19.5

Plecoptera

Macrogynoplax sp. PRE 5.4 39.9 1 2.4

Trichoptera

Phylloicus sp. SHR 0.1 0.9 1 2.4

Polycentropodidae FIL† 1.0 7.1 3 7.3

Diptera

Ceratopogonidae PRE 0.1 0.4 1 2.4

Chironominae COL 1.9 14.0 16 39.0

Stenochironomus sp. SHR 0.8 5.5 4 9.8

Tanypodinae PRE 0.2 1.3 2 4.9

Tipulidae SHR n.a. n.a. 1 2.4

Coleoptera

Elmidae (ad.) SCR 1.5 10.8 1 2.4

Megaloptera

Corydalus sp. PRE n.a. n.a. 1 2.4

Odonata

Coenagrionidae PRE 1.3 9.5 2 4.9

Total 13.7 41

FGG, functional feeding group; COL, collector–gatherers; PRE,predators; SHR, shredders; FIL, collector–filterers; SCR, scrapers.

*Mouthparts of the nymphs suggested a collector–gatherer ratherthan a scraper feeding mode.†Mouthparts suggested a collector–filterer rather than a predator

feeding mode.


8 A. Bruder et al.

(Ferreira et al., 2012). However, of particular combina-

tions of litter species on the decomposition of component

species were noted in that study, due particularly to

nitrogen-rich alder leaves. Ferreira et al. (2012) could test

for such effects because their experimental design, unlike

ours, included more than one type of litter mixture.

Therefore, similar outcomes cannot be ruled out in the

present study. Importantly, however, the lack of mixing

effects in our study was not a consequence

of concomitant, positive and negative effects on differ-

ent species in the mixtures because, unlike most

other studies (recent exceptions are Sanpera-Calbet et al.,

2009; Schindler & Gessner, 2009; Bruder, Chauvet & Gess-

ner, 2011; Ferreira et al., 2012), we separately determined

decomposition rates for each of the component species.

In addition to effects arising from mixing litter of con-

trasting quality, litter decomposition might also be sensi-

tive to variation in other diversity components, such as

the diversity of microbial decomposers and of shredders

(Gessner et al., 2010; Jabiol et al., 2013a). Furthermore,

seasonal variation in the supply of different litter species

in the tropics provides scope for litter-mixing effects

emerging on long temporal scales (Franc�a et al., 2009; see

also Lecerf et al., 2011), and interactive effects of diver-

sity at different trophic levels of decomposer food webs

might also be important (Jabiol et al., 2013a). However,

these aspects were not addressed in the present study

focussing on litter mixing and the presence or absence of

shredders over a time scale of weeks to a few months.

Effects of litter quality

Resource quality of the tropical litter we used was

clearly lower than that of three of the four temperate

litter species (ash, maple and alder), particularly in terms

of litter P concentration and toughness (Table 2),

although temperate beech litter also had low N and P

concentrations and high toughness. This pattern reflects

the observation that resource quality of leaf litter is often,

although not invariably lower in tropical than in tempe-

rate ecosystems (Grac�a et al., 2001; Wantzen & Wagner,

2006; Ardon, Pringle & Eggert, 2009; Ferreira et al., 2012)

because tropical forest soils tend to be nutrient poor and

many tree species growing on these soils have evolved

efficient nutrient resorption mechanisms and well-

defended leaves (H€attenschwiler et al., 2011). The higher

mean growth rate of a tropical shredder feeding on tem-

perate rather than on tropical litter species also suggests

that the resource quality of litter in tropical streams

tends to be lower (Grac�a & Cressa, 2010).

Importance of environmental conditions

Results of microcosm experiments (Chauvet & Suberkropp,

1998; Dang et al., 2009), and a correlative global study

across a broad latitudinal gradient (Boyero et al., 2011a),

concur with theoretical expectations that the activity of

microbial litter decomposers in streams is strongly con-

trolled by temperature. Accordingly, decomposition

should be substantially faster in warm tropical streams

(here 24.4 °C) than in temperate streams, where tempera-

tures drop during the period of decomposition following

autumnal leaf fall (here 4.2 °C on average; Table 1). How-

ever, despite the large temperature differences between

our two study sites, microbial decomposition rates of the

standard litter we used (i.e. alder) were surprisingly

similar, and hence much lower in the tropical stream

when normalised for temperature (Fig. 3; Table 3; see

also Dudgeon & Gao, 2011 and Ferreira et al., 2012). It is

unlikely that this result was caused by the fact that alder

is a foreign species in our tropical study stream, because

there are no indications in the literature that the origin of

species (i.e. exotic versus native) matters to aquatic

hyphomycetes that colonise and decompose leaf litter in

streams (B€arlocher & Grac�a, 2002; Jabiol et al., 2013b).

Notably, the dominant species sporulating on leaves in

the tropical stream was Flagellospora curvula (Jabiol et al.,

2013b), a cosmopolitan species that readily colonises

alder litter (e.g. Gessner et al., 1993; Gulis, 2001).

The striking discrepancy of our data with the positive

relationship between temperature and microbial decom-

position rate in the global correlative study by Boyero

et al. (2011a) might be reconciled when considering that a

considerable portion of the variation in that large-scale

analysis was left unexplained. This suggests that environ-

mental factors other than temperature can distinctly

influence microbial decomposition as well and could be

strong enough to override positive temperature effects on

microbial decomposition, even when temperature differ-

ences are large. Differential responses of fungal decom-

posers (Dang et al., 2009) adapted to local temperature

conditions are unlikely to play a notable role, because (i)

temperature differences between the two streams were

very large, (ii) temperature-response characteristics of

aquatic hyphomycetes are broadly similar (optima for

growth and sporulation activity between 20 and 25 °C

and minima at or below 5 °C; Suberkropp, 1984; Chauvet

& Suberkropp, 1998) and (iii) the fungal community on

litter in our tropical experiment was dominated by Flagel-

lospora curvula, which is also common in temperate

streams (e.g. Gessner et al., 1993; Jabiol et al., 2013b).



One alternative reason for the reduced microbial activ-

ity in the tropical stream was a short supply of nutrients

in stream water (Table 1), which can be a crucial N and

P pool for microbial decomposers of leaf litter in streams

especially on low-nutrient litter (Rosemond et al., 2002;

Suberkropp et al., 2010; Niu & Dudgeon, 2011). In our

experiment, low microbial activity was reflected by low

fungal biomass (A. Bruder et al., unpubl. data) and spor-

ulation rate (Jabiol et al., 2013b) in the litter exposed in

the tropical stream. Additionally, low conductivity of

the tropical stream water (Table 1) suggests that limita-

tion by other biologically important ions, such as cal-

cium (Suberkropp & Klug, 1980), could have played a

role as well. Regardless of the specific limiting factor,

our comparative data suggest that limitation of microbial

decomposition in the tropics was strong enough to com-

pensate for a near 20 °C temperature difference com-

pared with the temperate stream, which would result in

fourfold higher decay rates in the tropical stream

according to standard Q10 or similar relationships relat-

ing temperature to metabolic rate.

Usefulness of the litter-bag approach

In addition to our findings on the relative importance of

factors governing litter decomposition in our study

streams, the presented results provide information on

the application of the litter-bag approach to study litter

decomposition in streams. Similar decomposition rates in

both types of litter bags in the tropics, where shredders

were rare, reveal (i) that any potential negative effect of

the fine-mesh size on microenvironmental conditions

(e.g. oxygen or nutrient supply) was unimportant for

microbial decomposition and (ii) that physical losses

from coarse-mesh bags were also insignificant. At the

same time, faster decomposition in coarse-mesh bags in

the temperate stream, where litter-consuming inverte-

brates were abundant, concurs with the idea that shred-

ders can have large effects on litter mass loss. This

suggests that the widely used, but sometimes criticised,

litter-bag approach is suitable to test the relative impor-

tance of microbial versus shredder-mediated decomposi-

tion and the influence of environmental factors in stream

ecosystems.

In conclusion, our closely coordinated experiments in

a temperate and a tropical stream revealed a lack of

clear litter-mixing effects on decomposition rates, which

might be more common in terrestrial (forests) than aqua-

tic (forest streams) ecosystems (Gessner et al., 2010).

However, litter species identity is clearly important in

determining decomposition rates in both the presence

and absence of shredders (Petersen & Cummins, 1974;

Webster & Benfield, 1986) and can also affect decompo-

sition of specific combinations of litter species (e.g.

Ferreira et al., 2012). Consequently, changes in the spe-

cies composition of riparian vegetation, including losses

in diversity, are most likely to affect stream ecosystems

in spite of our inability to detect litter-mixing effects in

the two contrasting streams we investigated.

Acknowledgments

We gratefully acknowledge the field and laboratory

assistance by D. Steiner, D. Hohmann, N. R€othlin,

S. H€attenschwiler, L. Br�echet, S. K€appeli and E. Couteau.

We are also grateful to R. Illi and the AUA laboratory

for water–chemical analyses and to D. Dudgeon and

two anonymous reviewers for constructive comments.

This research was funded by the Swiss National Science

Foundation (SNF grant 31ED30-114213) through the

European Science Foundation’s (ESF) EURODIVERSITY

programme, which supported BioCycle as a collabora-

tive research project. BioCycle has been endorsed by

DIVERSITAS as contributing to its biodiversity research

priorities. The work also profited from a project coordi-

nated by L. Boyero and supported by the National Geo-

graphic Society (Grant 7980-06).

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(Manuscript accepted 27 October 2013)


12 A. Bruder et al.

litter decomposition in a temperate and a tropical stream: the effects of species mixing, litter...

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