Leaf-litter breakdown in pasture and deciduouswoodland streams: a comparison among three Europeanregions

SALLY HLADYZ* , 1 , SCOTT D. TIEGS †, ‡, 2 , MARK O. GESSNER †, ‡, PAUL S. GILLER*, GETA

RI SNOVEANU § , ELENA PREDA § , MARIUS NISTORESCU § , MARKUS SCHINDLER †, ‡ AND

GUY WOODWARD*, –

*Environmental Research Institute, Department of Zoology, Ecology & Plant Science, University College Cork, Cork, Ireland†Department of Aquatic Ecology, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Uberlandstrasse, Dubendorf‡Institute of Integrative Biology (IBZ), ETH Zurich, Zurich, Switzerland§Department of Systems Ecology and Sustainability, University of Bucharest, Splaiul Indepedentei, Bucharest, Romania–School of Biological & Chemical Sciences, Queen Mary University of London, London, U.K.

SUMMARY

1. Human land-use has altered catchments on a large scale in most parts of the world, with

one of the most profound changes relevant for streams and rivers being the widespread

clearance of woody riparian vegetation to make way for livestock grazing pasture.

Increasingly, environmental legislation, such as the EU Water Framework Directive (EU

WFD), calls for bioassessment tools that can detect such anthropogenic impacts on

ecosystem functioning.

2. We conducted a large-scale field experiment in 30 European streams to quantify

leaf-litter breakdown, a key ecosystem process, in streams whose riparian zones and

catchments had been cleared for pasture compared with those in native deciduous

woodland. The study encompassed a west–east gradient, from Ireland to Switzerland

to Romania, with each of the three countries representing a distinct region. We used

coarse-mesh and fine-mesh litter bags (10 and 0.5 mm, respectively) to assess total,

microbial and, by difference, macroinvertebrate-mediated breakdown.

3. Overall, total breakdown rates did not differ between land-use categories, but in some

regions macroinvertebrate-mediated breakdown was higher in deciduous woodland

streams, whereas microbial breakdown was higher in pasture streams. This result suggests

that overall ecosystem functioning is maintained by compensatory increases in microbial

activity in pasture streams.

4. We suggest that simple coefficients of breakdown rates on their own often might not

be powerful enough as a bioassessment tool for detecting differences related to land-use

such as riparian vegetation removal. However, shifts in the relative contributions to

breakdown by microbial decomposers versus invertebrate detritivores, as revealed by the

ratios of their associated breakdown rate coefficients, showed clear responses to land-use.

Keywords: agricultural streams, decomposition, functional ecosystem integrity, land-use change,Water Framework Directive

Correspondence: Dr Guy Woodward, School of Biological & Chemical Sciences, Queen Mary University of London, London, E1 4NS,

U.K. E-mail: g.woodward@qmul.ac.uk1Present address: CSIRO Land and Water, The Murray-Darling Freshwater Research Centre, PO Box 991, Wodonga, Victoria, 3689,

Australia.2Present address: Department of Biological Sciences, Oakland University, Rochester, Michigan, 48309, U.S.A.

Freshwater Biology (2010) 55, 1916–1929 doi:10.1111/j.1365-2427.2010.02426.x

1916 � 2010 Blackwell Publishing Ltd

Introduction

Impacts of past and present land-use practices on

stream ecosystem functioning are only beginning to

be understood, even though the often-reported

negative impacts on biodiversity are now all too

familiar (Malmqvist & Rundle, 2002; Foley et al., 2005;

Dudgeon et al., 2006). It is commonly assumed that

anthropogenic alterations to the landscape reduce the

ecological integrity of natural ecosystems, a concept

that encompasses structural attributes of ecosystems

as well as ecosystem processes. Bioassessment of

land-use impacts on streams and rivers has relied

primarily on metrics relating to community structure

(e.g. Davies, 2000; Bonada et al., 2006), most of which

quantify compositional changes within species assem-

blages (mainly fish, macroinvertebrates and diatoms)

relative to reference conditions. However, focused as

they are on structural patterns, these methods might

not detect impacts of stressors that alter ecosystem

processes, such as primary production and leaf-litter

breakdown (Gessner & Chauvet, 2002; Sandin &

Solimini, 2009). Therefore, assessments of the func-

tional integrity of ecosystems are required if the

responses of streams to anthropogenic stressors are to

be characterised fully (Bunn & Davies, 2000; Gessner

& Chauvet, 2002). To date, this requisite has been

largely ignored (but see Young & Collier, 2009;

Fellows et al., 2009; Riipinen et al., 2010), despite being

enshrined increasingly in regulatory legislation, such

as the EU Water Framework Directive (EU WFD;

European Commission, 2000) and the U.S. Clean

Water Act (Adler, Landman & Cameron, 1993).

Leaf-litter breakdown has been proposed as a

useful measure of ecosystem functioning in streams,

especially in low-order woodland streams (Webster &

Benfield, 1986; Wallace et al., 1997; Gessner & Chau-

vet, 2002) because of the critical importance of leaf-

litter as a basal food resource (Woodward, Speirs &

Hildrew, 2005; Young, Matthaei & Townsend, 2008).

The rate at which leaf-litter is broken represents an

integrated response to microbial degradation, inver-

tebrate feeding and physical processes (i.e. abrasion

and leaching) (Webster & Benfield, 1986), highlighting

its potential as a bioassessment tool (Young, Huryn &

Townsend, 1994; Gessner & Chauvet, 2002; Young

et al., 2008; McKie & Malmqvist, 2009), although

reservations have been expressed about their useful-

ness (Bird & Kaushik, 1992; Hagen, Webster &

Benfield, 2006).

The loss of woody vegetation from riparian zones

(and the wider catchment) because of the clearing of

land for pasture has occurred widely across Europe

and other parts of the world for centuries and has

intensified dramatically in recent decades in many

areas (Fujisaka et al., 1996). This continental-scale

removal of native woodland can have many poten-

tially profound effects on streams (Sweeney et al.,

2004) by altering productivity (Quinn et al., 1997),

water chemistry (Lenat & Crawford, 1994; Townsend

et al., 1997; Huryn et al., 2002), channel morphology

(Sweeney, 1993; Sweeney et al., 2004), community

structure (Sweeney, 1993; Lenat & Crawford, 1994;

Townsend et al., 1997) and reducing allochthonous

inputs and standing stocks of organic matter (Camp-

bell et al., 1992; Sweeney, 1993; Murphy & Giller, 2000;

Scarsbrook et al., 2001). The latter impact is particu-

larly significant as changes in riparian vegetation will

alter the fluxes of energy and nutrients at the base of

stream food webs, with potentially profound impacts

on ecosystem functioning (Murphy & Giller, 2001;

Woodward, 2009).

In this study, we measured breakdown rates of leaf-

litter in a coordinated field experiment over a broad

west to east (i.e. climatic) gradient across Europe to

assess the impact of riparian tree removal for pasture

on ecosystem functioning. We measured these rates in

paired pasture and woodland streams in 30 streams

across three European regions, from the western edge

of the continent to the east (Ireland to the Swiss

Plateau to the Danube Plains in Romania), to test the

hypothesis that leaf breakdown would be impaired in

pasture streams relative to those in native woodland.

The three selected regions are located within ecore-

gion 17 (‘Ireland and Northern Ireland’), at the border

of ecoregions 4 (‘Alps’) and 8 (‘Western Highlands’),

and in ecoregion 12 (‘Pontic Province’) of the EU

(WFD), which are distinguished based on macroin-

vertebrate distributions in rivers and streams and

abiotic criteria such as altitude, catchment area and

geology (European Commission, 2000). The study

regions were chosen because they experience

widespread clearance of riparian woody vegetation

for grazing pasture, which represents one of the main

anthropogenic alterations to streams in large parts of

Europe and elsewhere.

Litter breakdown in woodland and pasture streams 1917

� 2010 Blackwell Publishing Ltd, Freshwater Biology, 55, 1916–1929

Methods

Study sites

A large coordinated field experiment was carried out

in 10 streams in each of the three European regions, to

compare leaf-litter breakdown in deciduous wood-

land streams with those flowing through pasture. All

streams were first to third order, 1–5 m wide, <50 cm

deep at winter baseflow, with hard substrata. A priori

pairing of woodland and pasture streams was carried

out to maximise statistical power and was based on

overall similarities in physical and chemical site

characteristics such as channel width, water depth

and grain size distribution of the substratum. Streams

were standardised across the study area as far as

possible for physicochemical variables. The study was

undertaken during the late autumn and early winter

of 2002–03 and ran for 2–4 months, depending on the

timing of local leaf fall and breakdown rates.

Field experiments

In each region, leaves of two common native trees,

alder (Alnus glutinosa (L.) Gaertn.) and oak (Quercus

robur L.), were collected immediately after abscission

and air-dried to constant mass. These species were

chosen because they are widespread in Europe and

because they differ markedly in terms of resource

quality, with the former having lower lignin content

and carbon ⁄nutrient ratios, which make it less

recalcitrant (Hladyz et al., 2009) and more palatable

to consumers than oak litter. Five grams (±0.25 g) of

air-dried leaf material was added to experimental

plastic-mesh bags of two mesh aperture sizes, 0.5 and

10 mm, to measure microbial breakdown and total

breakdown caused jointly by microorganisms, inver-

tebrates and physical processes. Six metal stakes were

anchored into the streambed within six separate riffles

(i.e. one stake per riffle) with four leaf bags (one

representative of each mesh and leaf type) attached to

each stake.

Of the 10 streams chosen per region, five were

bordered with deciduous woodland and five with

pasture. All of these streams were sampled on one date

per leaf type (6 replicates · 2 mesh sizes · 2 leaf spe-

cies · 10 streams · 3 regions), and two of these

streams per region were also sampled on four addi-

tional occasions (4 replicates · 2 mesh sizes · 2 leaf

species · 2 streams · 3 regions). Thus, a total of 1104

leaf bags were exposed in the 30 streams. The streams

sampled once offered a snapshot of breakdown across a

spatial gradient, while the streams sampled on multiple

occasions provided more detailed insight into temporal

changes occurring during the breakdown process.

Breakdown rates in the deciduous woodland

streams sampled at multiple dates were used to

determine the point at which approximately 50% ash-

free dry mass (AFDM) would have been lost (i.e. T50)

in each region. On this date, leaf bags were collected

from all 10 streams. Exposure was thus standardised

(as far as possible) for breakdown stage rather than

absolute duration, resulting in variable exposure

times among regions and between leaf species (e.g.

T50 for alder was 35 days in Ireland but 53 days in

Switzerland).

On the collection date, the retrieved leaf bags were

placed individually in plastic bags and returned to the

laboratory, where litter was separated from extrane-

ous material and dried to constant mass at 105 �C,

after which a subsample was ashed at 550 �C (4 h) in a

muffle furnace to calculate AFDM. In total, 81% of the

initial 1104 leaf bags were retrieved successfully.

Flood disturbance caused the loss of most litter bags

from the two Swiss streams used in the temporal

study, necessitating their exclusion from the analysis

of the time-series data. Similarly, one woodland

stream site was excluded from the Romanian spatial

study because of a flood event. Correction factors

derived for leaching losses (determined after 24 h

under running tap water in the laboratory) and

moisture content were applied to the initial air-dry

masses, to calculate post-leaching AFDM loss over

time (Hladyz et al., 2009).

Conductivity and pH of stream water were mea-

sured in the field at T50, and filtered water samples

(Whatman GF ⁄F, 0.7 lm average pore size) were

analysed in the laboratory for alkalinity, ammonium

(NHþ4 ), total oxidised nitrogen (TON ¼ NO�3 þNO�2 )

and soluble reactive phosphorus (SRP). Stream tem-

peratures were measured every 30 min throughout

the experiment using cross-calibrated data loggers

(Smartbutton, ACR Systems Inc., BC, Canada).

Statistical analyses

MANOVAMANOVA was used on water chemical parameters to

test for differences among regions and between land-

uses. As there was strong multi-collinearity among

1918 S. Hladyz et al.

� 2010 Blackwell Publishing Ltd, Freshwater Biology, 55, 1916–1929

some of the variables (e.g. conductivity, pH, alkalin-

ity) only four uncorrelated variables were included in

this analysis [SRP, Total Oxidised Nitrogen (TON),

ammonium and conductivity]. All variables were

log10 transformed to meet assumptions of parametric

statistical analyses, which were performed using

MINITAB version 13.32 (MINITAB, 2000).

Breakdown rate coefficients (k) were calculated

assuming an exponential decay model (Petersen &

Cummins, 1974; Boulton & Boon, 1991) and compared

among regions, land-uses and leaf species. When

samples were repeatedly retrieved from the study

streams, breakdown coefficients (k) were obtained

using nonlinear regression analyses on AFDM data

with the initial leaf mass at day 0 fixed at 100%.

ANCOVAANCOVA (comparison of slopes) following log trans-

formation of the litter mass remaining data was used

to test for differences between land-use categories

within regions with time as the covariate (Boulton &

Boon, 1991).

For litter retrieved from the streams on the single

sampling date, k was calculated thus:

�k ¼lnðAFDMremaining=AFDMinitialÞ

Duration

where AFDMinitial (g) is the initial post-leaching

AFDM in the litter bag, AFDMremaining (g) is the mass

remaining after exposure in the stream, and Duration

is either the number of exposure days, to calculate

mass loss per day (kd), or the thermal sum over the

exposure time, to calculate mass loss per degree-day

(kdd). The latter measure was used to correct for

potential temperature effects across streams and

regions. Both types of rate coefficients were calculated

for total breakdown in the coarse-mesh bags (ktotal)

and for microbial breakdown in fine-mesh bags

(kmicrobial). Macroinvertebrate-mediated breakdown

was calculated as the difference between per cent

mass remaining in coarse-mesh and fine-mesh bags,

which was then also converted to a breakdown

coefficient (kinvert). Finally, a dimensionless metric

was calculated as the ratio of invertebrate-mediated

breakdown coefficient to microbial breakdown coeffi-

cient (i.e. kinvert ⁄kmicrobial).

To test for differences in breakdown, linear mixed

effects models (LMEM) were used to account (i) for

the hierarchical nature of the experimental design,

with litter bags nested within riffles, riffles nested

within individual streams and streams nested within

pairs and (ii) for the incorporation of both fixed and

random effects in the design. The following variables

were fitted as fixed effects in the analyses: region,

land-use and leaf species. Riffles (i.e. blocks), streams

and stream pairs were fitted as random effects. Since

our experimental design was unbalanced because of

the loss of some litter bags during field exposure, we

used the restricted maximum likelihood method to

estimate error terms. Non-significant interactions and

main factors were removed from the model in a

stepwise approach until all terms were significant

(Crawley, 2007). Pairwise comparisons on main fixed

effects were performed using Tukey post hoc tests. The

statistical analyses described earlier were performed

with R version 2.9.2 (R Development Core Team,

2009).

Breakdown rates (k-values) were log10 transformed

to stabilise variances and normalise residuals, and

then compared among regions, land-use categories

and leaf species. The same tests were also performed

using log10-transformed breakdown rate coefficients

per degree-day (log10 kdd) as the response variable, to

explore potential geographical differences that were

not driven by temperature per se. Because variances

could not be stabilised between the two mesh types,

even following logarithmic transformation, LMEMs

were run separately for each.

A similar LMEM model to the one mentioned

earlier was used to examine differences in the ratio of

invertebrate-mediated breakdown and microbial

breakdown among regions, leaf species and land-use

category. However, stream means were used as the

lowest level of replication in this model, to minimise

the effect of missing bags from pairs of coarse-mesh

versus fine-mesh litter bags, and k ratios were also

log10 transformed to normalise the residuals.

Partial least-squares (PLS) regression was used to

determine the relative importance of measured phys-

icochemical variables (Table 1) on breakdown rates

(log10 transformed) among and within regions to

elucidate potential drivers not necessarily related to

our categorical main effects. Temperature was

excluded from the kdd analyses as this metric already

corrects for temperature. PLS extracts components

from a set of variables which, as in principal compo-

nents analysis, are orthogonal and so eliminates

multicollinearity. In addition, PLS maximises the

explained covariance between the variables. The

Litter breakdown in woodland and pasture streams 1919

� 2010 Blackwell Publishing Ltd, Freshwater Biology, 55, 1916–1929

constructed components are used to create a model

for the response variable with the relative importance

of the predictor variables ranked with variable

importance on the projection values (Eriksson et al.,

1999). PLS analyses were conducted using SIMCA-P

(version 12.0; Umetrics AB, Umea, Sweden). Addi-

tional components were extracted until the increase in

variance fell below 10%. The analysis used stream site

means for leaf breakdown data, as most of the

physicochemical variables were measured at this

level.

Results

Water chemistry

All streams were slightly above neutral (group mean:

pH 7.7 ± 0.2 SE; alkalinity 131 ± 62 mg CaCO3 L)1)

and not unusually nutrient-enriched, relative to

regional standards (group means ± SE: TON 927 ±

506 lg L)1; SRP 5.1 ± 0.1 lg L)1; NHþ4 27.1 ± 7.7

lg N L)1; conductivity 299 ± 82 lS cm)1). Overall,

water chemistry differed significantly among regions

(MANOVAMANOVA F8,40 = 14.1, P < 0.0001), but not between

land-use categories (MANOVAMANOVA F4,20 = 0.19, P = 0.9).

The differences among regions were mainly explained

by TON concentrations and alkalinity, although they

are also reflected in conductivity (Table 1).

Land-use and leaf-litter breakdown rates: spatial

gradient

Litter breakdown rates from the spatial study differed

significantly among regions and leaf species, but not

between land-use categories (Table 2; Fig. 1a–d).

Thus, despite being biogeographically distinct from

one another, the three study regions responded in a

consistent manner to the different land-use types.

Romania exhibited faster breakdown rates than both

Ireland and Switzerland for coarse-mesh bags. For

fine-mesh bags, Romania exhibited faster breakdown

rates than Ireland, with Switzerland not differing

from either region. There were also significant two-

way, but not three-way, interactions for both mesh

types. Interactions apparent for leaf breakdown in the

coarse-mesh bags were region · leaf species and land-

use category · leaf species. The land-use cate-

gory · leaf species interaction arose because alder

breakdown was fastest in deciduous woodland

streams in Ireland and Romania, whereas in Switzer-

land, oak broke down faster in pasture streams than in

woodland streams. In the fine-mesh bags, only the

region · leaf species interaction was significant.

Table 1 Mean (±1 SE) chemical characteristics and temperature for streams in each land-use category by region

Variable

Ireland Swiss plateau Romanian danube plains

Woodland Pasture Woodland Pasture Woodland Pasture

SRP (lg L)1) 4.4 (0.5) 6.1 (1.6) 4.7 (0.9) 5.4 (0.8) 4.7 (1.2) 5.1 (2.2)

TON (lg L)1) 121 (33) 42 (7) 1870 (480) 1800 (5770) 341 (91) 1230 (290)

NHþ4 (lg N L)1) 25 (8) 18 (4) 15 (5) 20 (7) 24 (5) 58 (16)

pH 7.3 (0.1) 7.4 (0.0) 7.9 (0.0) 7.9 (0.0) 7.7 (0.1) 7.8 (0.1)

Alkalinity (mg CaCO3 L)1) 34 (7) 23 (5) 238 (6) 246 (14) 89 (11) 150 (35)

Conductivity (lS cm)1) 166 (17) 124 (11) 449 (15) 394 (42) 249 (23) 398 (88)

Temperature (�C) 5.8 (0.1) 5.4 (0.1) 6.6 (0.5) 7.3 (0.2) 4.9 (0.1) 4.5 (0.5)

SRP = soluble reactive phosphorus; TON = total oxidised nitrogen (i.e. nitrate + nitrite).

Table 2 Linear mixed effects model results of comparisons of

standard (kd) and temperature-normalised (kdd) breakdown rate

coefficients of litter in coarse-mesh and fine-mesh bags across

regions and land-uses

Mesh size

F ratio

Comparison d.f.N d.f.D log10 kd log10 kdd

Region C 2 12 5.33* 70.49***

Land-use C 1 12 2.39ns 2.67ns

Leaf species C 1 112 272.96*** 263.54***

Region ·leaf species

C 2 112 10.93*** 13.71***

Land-use ·leaf species

C 1 112 6.67** 6.38**

Region F 2 11 10.33** 107.63***

Land-use F 1 12 2.85ns 2.60ns

Leaf species F 1 125 370.87*** 345.48***

Region ·leaf species

F 2 125 10.26** 14.77***

Three-way interactions were non-significant and therefore

omitted.

*P < 0.05, **P < 0.01., ***P < 0.001, nsP > 0.05.

1920 S. Hladyz et al.

� 2010 Blackwell Publishing Ltd, Freshwater Biology, 55, 1916–1929

Correcting for temperature effects by using degree

days for breakdown rates increased the effect of

region for both coarse-mesh and fine-mesh litter bags.

The ratio of invertebrate-mediated breakdown to

microbial breakdown differed significantly among

regions and between land-use category (Fig. 1e,f;

Table 3). Ireland had a higher kinvert ⁄kmicrobial ratio than

Switzerland, whereas the ratio for Romania did not

differ from those of the other two regions. Overall,

ratios were significantly higher in the deciduous

woodland streams than in the pasture streams.

Land-use and leaf-litter breakdown rates: temporal

dynamics

Breakdown rates in Irish and Romanian deciduous

woodland and pasture streams sampled repeatedly

were generally well characterised by exponential

decay models for both leaf species and mesh types

(Fig. 2; Table 4). Within Ireland, breakdown rates did

not differ between land-use categories for leaf species

or mesh type (coarse-mesh alder F1,9 = 1.48, P = 0.26,

coarse-mesh oak F1,6 = 4.3, P = 0.08, fine-mesh alder

F1,6 = 0.65, P = 0.45, fine-mesh oak F1,6 = 1.89,

P = 0.22 Fig. 2a–d). Within Romania, breakdown rates

in coarse-mesh bags for both leaf species did not differ

between land-use categories (coarse-mesh alder

F1,4 = 1.37, P = 0.31, coarse-mesh oak F1,6 = 1.98,

P = 0.21; Fig. 2e,g), but breakdown in fine-mesh bags

was faster in the pasture stream than in the deciduous

stream (fine-mesh alder F1,6 = 7.26, P = 0.04, fine-

mesh oak F1,6 = 10.93, P = 0.02; Fig. 2f,h).

Patterns of leaf-litter breakdown among and within

regions

The PLS analyses of breakdown rates in coarse-mesh

bags among regions revealed that the physicochemical

variables only predicted a small amount of variation

(R2Y = 0.17) in the breakdown rates for oak (positive

associations with SRP, TON and conductivity) and no

variation for alder (Table 5). For fine-mesh bags, the

physicochemical variables explained a small amount

of variation in the breakdown rates for alder

(R2Y = 0.30) with both SRP and TON being important

predictors of breakdown rates among regions. Five

k tota

l (da

y–1)

0.00

0.04

0.08

0.12

k mic

robi

al (d

ay–1

)

0.00

0.01

0.02

0.03

0.04

Alder

0.00

0.01

0.02

0.03

0.04

0.000

0.004

0.008

0.012

k inve

rt / k m

icro

bial

0

1

2

3

(a)

(c)

(e)

(b)

(d)

(f)

Oak

Ireland Swissplateau

Region Region

Romaniandanube plains

Ireland Swissplateau

Romaniandanube plains

Fig. 1 Alder and oak leaf breakdown in

woodland (black bars) and pasture (white

bars) streams of three European regions:

(a, b) total breakdown rates (coarse-mesh),

(c, d) microbial breakdown rates (fine-

mesh), (e, f) ratio of invertebrate-mediated

to microbial breakdown rates. Individual

values were averaged using streams as

replicates and data presented show mean

values of streams ± 1 SE.

Litter breakdown in woodland and pasture streams 1921

� 2010 Blackwell Publishing Ltd, Freshwater Biology, 55, 1916–1929

variables (SRP, TON, conductivity, alkalinity and pH)

were identified as important predictors of oak break-

down rates among regions in fine-mesh bags

(R2Y = 0.75).

When examining patterns within rather than among

regions, physicochemical variables generally pre-

dicted a greater amount of variation in breakdown

rates (Table 6). Within Ireland, conductivity, TON and

alkalinity were important for alder breakdown but no

significant model was found for oak. SRP and TON

were important in Switzerland for both alder and oak

in coarse-mesh and fine-mesh bags. Finally, in Roma-

nia, stream temperature was a common predictor for

alder and oak leaf-litter breakdown in fine-mesh and

for alder in coarse-mesh bags, but no significant

model was identified for oak breakdown in coarse-

mesh bags. Correcting for temperature effects by

using degree days for breakdown rates did not

generally alter the amount of explained variation for

Table 3 Linear mixed effects model results of comparisons of

the ratio of invertebrate-mediated breakdown rates and micro-

bial breakdown rates (log10 kinvert ⁄ kmicrobial) across regions and

land-use categories

Comparison d.f. N d.f.D F ratio

Region 2 11 4.78*

Land-use 1 12 10.9**

Leaf species 1 22 0.07ns

Interactions were non-significant and therefore omitted.

*P < 0.05, **P < 0.01, nsP > 0.05.

0

25

50

75

100

0

25

50

75

100

0 20 40 60

AF

DM

rem

aini

ng (

%)

0

25

50

75

100

Time (day)

0 20 40 600

25

50

75

100

0 20 40 60 80 100 120

(h)(f)

Alder coarse Oak coarse

Alder coarse Oak coarse

Alder fine Oak fine

Alder fine Oak fine

(e)

(c)(a)

(d)(b)

(g)

Fig. 2 Total and microbial only break-

down of alder and oak leaves in paired

woodland (black symbols) and pasture

(white symbols) streams in Ireland (a–d)

and Romania (e–h). Individual values

were averaged using litter bags as repli-

cates, and the data presented show mean

values of litter bags ± 1 SE. Data for the

Swiss streams were unavailable because

of losses of litter bags during a flood

event.

1922 S. Hladyz et al.

� 2010 Blackwell Publishing Ltd, Freshwater Biology, 55, 1916–1929

breakdown rates (Tables S1 & S2 in Supporting

Information).

Discussion

Land-use and leaf-litter breakdown rates

There were no consistent differences in total leaf

breakdown between land-use categories, but the

relative importance of shredders versus microbes as

the principal agents of breakdown changed markedly.

This study thus adds empirical evidence in support of

Gessner & Chauvet’s (2002) suggestion that simple

coefficients of absolute leaf-litter breakdown rates

might not be sufficiently sensitive for bioassessment

if compensatory mechanisms operate within the

decomposer assemblage. That is, impaired activity

of certain groups of organisms (e.g. shredders)

appeared to be mitigated by elevated activity among

others (e.g. fungi) to such an extent that total rates

of litter breakdown were statistically indistinguish-

able between impacted and reference sites.

The maintenance of ecosystem process rates

observed here despite a fundamental shift in the

composition of the riparian zone has been reported in

a few other studies. Bird & Kaushik (1992) observed

similar breakdown rates within a single stream in

Canada and suggested the higher abundance of

Table 4 Leaf breakdown rate coefficients per day for alder and oak leaf-litter decomposing in coarse-mesh and fine-mesh bags in

streams of two regions and different land-uses

Region Land-use

Alder Oak

Coarse-mesh Fine-mesh Coarse-mesh Fine-mesh

k r2 k r2 k r2 k r2

Ireland Woodland )0.0382 0.97*** )0.0122 0.96** )0.0100 0.98** )0.0049 0.79*

Pasture )0.0420 0.97*** )0.0146 0.96** )0.0166 0.92** )0.0072 0.89*

Romanian Danube Plains Woodland )0.0328 0.86* )0.0181† 0.98*** )0.0117 0.96*** )0.0069† 0.87*

Pasture )0.0229 0.96* )0.0271† 0.92* )0.0135 0.93** )0.0095† 0.99***

*P < 0.05, **P < 0.01 and ***P < 0.001 denote significance for regression lines for breakdown rates.†Denotes slopes that are significantly different between land-use categories (P < 0.05). Outliers were removed before analysis (Ireland;

oak coarse-mesh and alder fine-mesh 19-day values, oak fine-mesh 9-day values, Romania; alder coarse-mesh 34-day values, oak fine-

mesh woodland 105-day values).

Table 5 Partial least-squares (PLS) regression output for leaf breakdown rate coefficients (kd) among European regions

Type of breakdown Leaf species Variable VIP Slope Components R2Y

ktotal Alder n.s.

Oak log10 SRP 1.50 0.15 1 0.17

log10 TON 1.33 0.14

log10 Cond 1.06 0.11

Constant )8.99

kmicrobial Alder log10 SRP 1.87 0.35 1 0.30

log10 TON 1.39 0.26

Constant )7.38

Oak log10 SRP 1.21 0.45 2 0.75

log10 TON 1.20 0.26

log10 Cond 1.19 0.24

Alkalinity 1.08 0.13

pH 1.02 0.10

Constant )8.63

n.s., no significant model identified.

Variables are listed with their regression slopes in descending VIP (variable importance to the projection) index order. Slope coeffi-

cients are not independent (unlike MLR), as the variables may be collinear. The VIP values reflect the importance of terms in the model

with respect to both y and x (the projection). VIP is normalised and the average squared value is 1, so terms in the model with a VIP > 1

are important (other variables are not shown). R2Y is the % of the variation of y explained by the model.

Litter breakdown in woodland and pasture streams 1923

� 2010 Blackwell Publishing Ltd, Freshwater Biology, 55, 1916–1929

shredders drove breakdown in the forested reach,

whereas microbial activity and physical abrasion

governed breakdown in the pasture reach. Similarly,

no consistent differences in litter breakdown rates

were found between forested and pasture reaches

within a south-eastern Australian stream (Danger &

Robson, 2004), and similar drivers were invoked as in

the Bird & Kaushik (1992) study, with physical

abrasion and microbial activity again suggested to

be relatively more important in the pasture reaches

(which lacked invertebrate shredders). Tuchman &

King (1993) concluded that shredders and microbial

processes governed breakdown rates in woodland

reaches within a Michigan stream, whereas abrasion

was thought to be the major process causing faster

breakdown in pasture reaches because of increased

surface run-off and variation in discharge. Huryn

et al. (2002) found no differences in breakdown rates

between pasture and forested streams in Maine,

U.S.A. and ascribed this to the confounding factors

of shredders and nutrients, insofar as streams in land-

use categories with low nutrients usually contained

Table 6 Partial least-squares (PLS) regression output for leaf breakdown rate coefficients (kd) within European regions

Region Type of breakdown Leaf species Variable VIP Slope Components R2Y

Ireland ktotal Alder log10 Cond 1.53 0.29 1 0.56

log10TON 1.33 0.25

log10SRP 1.08 0.20

Alkalinity 1.07 0.20

Constant )10.37

Oak n.s.

kmicrobial Alder log10 Cond 1.58 0.30 1 0.60

Alkalinity 1.24 0.23

log10 TON 1.08 0.20

Constant )15.14

Oak n.s.

Swiss Plateau ktotal Alder log10 TON 1.47 0.57 2 0.89

Temp 1.32 )0.65

log10 SRP 1.04 0.21

Constant )6.27

Oak log10 TON 1.51 0.33 1 0.71

log10 NH4 1.45 0.32

log10 SRP 1.33 0.29

Constant )8.28

kmicrobial Alder log10 SRP 1.88 0.45 1 0.86

log10 TON 1.35 0.32

Constant )7.05

Oak log10 SRP 1.56 0.38 1 0.80

log10 TON 1.53 0.36

Constant )10.60

Romanian Danube Plains ktotal Alder Temp 1.44 0.25 1 0.67

Alkalinity 1.31 )0.23

log10 NH4 1.12 )0.20

log10 SRP 1.08 0.19

Constant )3.85

Oak n.s.

kmicrobial Alder Temp 1.40 0.55 2 0.89

log10 NH4 1.02 )0.33

log10 Cond 1.00 0.41

Constant )6.93

Oak Temp 1.46 0.43 2 0.94

Alkalinity 1.28 )0.30

log10 SRP 1.14 0.37

log10 Cond 1.07 0.42

Constant )18.03

n.s., no significant model identified.

1924 S. Hladyz et al.

� 2010 Blackwell Publishing Ltd, Freshwater Biology, 55, 1916–1929

large numbers of shredders (i.e. forest streams),

whereas streams with few shredders usually had

high nutrient concentrations (i.e. pasture streams).

Among the studies that have found differences in

breakdown rates between pasture and forested

streams, the differences have been attributed to higher

nutrient concentrations in agricultural streams (e.g.

Young et al., 1994; Niyogi, Simon & Townsend, 2003)

and ⁄or differences in shredder assemblages (e.g.

Sponseller & Benfield, 2001; Hagen et al., 2006).

Experimental addition of dissolved P and N to stream

water can stimulate breakdown rates (e.g. Robinson &

Gessner, 2000; Ferreira, Gulis & Graca, 2006), and in

the study of Paul, Meyer & Couch (2006), which

included pasture and forested streams with similar

shredder densities, elevated rates of litter breakdown

in pasture streams were also ascribed to higher

nutrient concentrations. Another study examining a

land-use gradient ranging from forest to intensive

agriculture found that shredder richness and density,

which were generally higher in light-moderate agri-

cultural streams than in forested or heavy-agricultural

streams, were positively correlated with breakdown

rate (Hagen et al., 2006). Finally, the study by Spon-

seller & Benfield (2001) in a total of eight streams in

the eastern U.S.A. found slower breakdown rates in

streams with reduced forest cover and lower shredder

densities. Our results from a larger sample of

European streams revealed that total breakdown rates

were generally similar between land-use categories,

whereas the relative contributions of the different

agents (microbes versus invertebrates) differed mark-

edly. Nutrient concentrations did not differ between

land-use categories and, although we are cautious

about the use of spot measurements that might not be

wholly representative of average conditions, the lack

of consistent differences in the measured nutrient

concentrations suggests that some other driver was

responsible for this result.

The Swiss Plateau was the only region where total

breakdown rates differed between land-use catego-

ries. Specifically, breakdown was faster in woodland

streams for alder litter in coarse-mesh bags, although

microbial breakdown rates were similar for both land-

use categories. This suggests the differences observed

in the coarse-mesh bags reflect differences in detriti-

vore assemblages between woodland and pasture

streams (e.g. biomass, abundance, diversity), but

further study is required to test this hypothesis. It

also indicated that alder litter, which is a relatively

attractive food for shredders (Canhoto & Graca, 1995;

Hladyz et al., 2009), might be more sensitive for

gauging invertebrate-mediated breakdown than the

more recalcitrant oak litter.

The kinvert ⁄kmicrobial metric we used detected clear

shifts in the contribution of invertebrates and micro-

bial decomposers, with the former being a dominant

agent in forested streams and the latter apparently

driving breakdown in the pasture streams. It is

difficult to ascribe the actual mechanisms for these

patterns unequivocally without additional data

from our study streams on shredder and microbial

identity, abundance and assemblage composition,

which can all influence leaf breakdown rate. Infor-

mation on these potential drivers would be useful

in future studies, especially in the light of our

evidence for increased microbial activity in pasture

streams.

Invertebrate shredders are widely perceived as

important agents of litter breakdown in forested

streams (Graca, 2001), which has been related to their

density, biomass (Hieber & Gessner, 2002), richness

(McKie et al., 2009) or the presence of key taxa

(Dangles et al., 2004; Tiegs et al., 2008). It is not

uncommon, however, to find certain shredder taxa,

such as gammarid shrimps and nemourid stoneflies,

in high abundances in pasture streams (Hawkins,

Murphy & Anderson, 1982; Ormerod et al., 1993;

Harrison & Harris, 2002; Woodward et al., 2008),

where litter types other than leaves from riparian

trees may be present (Menninger & Palmer, 2007).

Further, many of these taxa function as trophic

generalists (Friberg & Jacobsen, 1994; Dangles, 2002;

Albarino & Villanueva, 2006) that can, for example,

also graze benthic algae (Ledger & Hildrew, 2000).

Consequently, these herbivore-detritivores may be

able to sustain themselves on an alternative basal

resource in the absence of significant litter inputs and

yet still exploit leaf-litter if and when it becomes

available (Robinson, Gessner & Ward, 1998). Such

generalist feeding could mitigate the potential effects

of large-scale clearance of riparian woody vegetation.

Substitution of grass and forb litter for riparian tree

leaves and facultative exploitation of algal and fine

detrital matter might, therefore, account for the

invertebrate activity evident in the pasture streams,

albeit at a reduced level relative to the woodland

streams.

Litter breakdown in woodland and pasture streams 1925

� 2010 Blackwell Publishing Ltd, Freshwater Biology, 55, 1916–1929

The kinvert ⁄kmicrobial metric we used provides an

indication of how community structure (i.e. charac-

teristics of macroinvertebrate and microbial assem-

blages) affects litter breakdown, in that it implies

different mechanisms for the similar breakdown

rates observed between land-use types. Differences

in this ratio could therefore not only provide a

useful metric for gauging impacts on functional

attributes of stream ecosystems but also hint at

the structural basis of impairment. Since changes

in structure are not necessarily mirrored by changes

in functioning, and vice versa (Sandin & Solimini,

2009), and both ecosystem functioning and structure

can be affected by anthropogenic stresses, use of this

ratio could aid development of a more integrated

approach to stream bioassessment than is currently

the case (Gessner & Chauvet, 2002; Sandin & Solimini,

2009).

Patterns of leaf-litter breakdown rates among and within

regions

Although breakdown rates did not differ between

land-use categories, they varied markedly among

regions, generally being faster in Romania than in

Ireland and Switzerland, at least for coarse bags. For

these bags, the physicochemical variables measured in

this study explained little of the variation in break-

down rates among regions. Therefore, regional differ-

ences in breakdown rates could be because of

unknown differences in shredder assemblages (e.g.

Hagen et al., 2006; Paul et al., 2006) and ⁄or to physi-

cochemical variables. Similarly, even after measuring

an extensive suite of physicochemical parameters,

51% of variation in leaf breakdown rate across

multiple sites in 12 streams was still left unexplained

(Tiegs, Akinwolw & Gessner, 2009). This was attrib-

uted to local variation in shredder activity, which was

not measured in that study. Secondly, different

physicochemical variables are potentially constraining

breakdown rates within different regions: in our

study, water chemistry did not differ between land-

use categories, but it did vary among regions and

more variation was often accounted for by physico-

chemical variables within than among regions. For

instance, the physicochemical variables we measured

explained 30% of the variation in alder breakdown in

fine-mesh bags when comparing among regions,

whereas this increased to 60% within Ireland.

The potential for using leaf-litter breakdown as a

bioassessment tool for detecting anthropogenic

impacts has been highlighted repeatedly in recent

years (Webster & Benfield, 1986; Gessner & Chauvet,

2002; Sandin & Solimini, 2009). Our results indicate

that simple coefficients of total breakdown rates alone

might not be sensitive enough to detect responses to

land-use, partly because of compensatory responses

from detritivore invertebrates and microbial decom-

posers. The use of derived metrics, such as ratios of

breakdown coefficients (Gessner & Chauvet, 2002),

could prove more effective by providing insights into

the role of potential compensatory mechanisms. This

offers a potentially valuable basis for future stream

bioassessment, especially where functional measures

can complement other metrics, including those

based on structural attributes of stream assemblages

(e.g. diversity indices). The next step is to combine

these approaches into an integrative methodology

for assessing structural and functional ecosystem

integrity simultaneously and thus develop a more

complete and powerful tool for detecting anthropo-

genic impacts in running waters.

Acknowledgments

We thank the European Commission (contract no.

EVK1-CT-2001-00088) and Swiss State Secretariat

for Research and Education (grant no. 01.0087)

for funding the RivFunction project under the E.U.

5th Framework Programme. We are indebted to

Carmen Postolache, Richard Illi and the AUA labora-

tory for nutrient analyses of stream water, and

Warren Paul at La Trobe University for advice in

statistical analyses.

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Supporting Information

Additional Supporting Information may be found in

the online version of this article:

Table S1 Partial least-squares (PLS) regression

output for leaf breakdown rate coefficients (kdd)

among European regions. n.s., no significant model

identified.

Table S2 Partial least-squares (PLS) regression out-

put for leaf breakdown rate coefficients (kdd) within

European regions. n.s., no significant model identified.

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(Manuscript accepted 4 March 2010)

Litter breakdown in woodland and pasture streams 1929

� 2010 Blackwell Publishing Ltd, Freshwater Biology, 55, 1916–1929