Post on 15-May-2023
PRIMARY RESEARCH PAPER
The effect of in-stream gravel extraction in a pre-alpinegravel-bed river on hyporheic invertebrate community
Natasa Mori • Tatjana Simcic • Simon Lukancic •
Anton Brancelj
Received: 2 August 2009 / Revised: 10 August 2010 / Accepted: 21 August 2010 / Published online: 4 March 2011
� Springer Science+Business Media B.V. 2011
Abstract We investigated the effect of in-stream
gravel extraction in a pre-alpine gravel-bed river on
hyporheic invertebrate community, together with
changes in the hyporheic geomorphology, physico-
chemistry and biofilm activity. Hyporheic inverte-
brates were collected, together with environmental
data, on seven sampling occasions from June 2004 to
May 2005, at two river reaches—at the site of in-
stream gravel extraction and at a site 2.5 km
upstream. The hyporheic samples were taken from
the river bed and from the gravel bars extending
laterally from the stream channel. The invertebrate
community was dominated by insect larvae (occa-
sional hyporheos), followed by meiofauna (perma-
nent hyporheos). Stygobionts were present at low
species richness and in low densities. Gravel extrac-
tion from the stream channel led to changes in the
patterns of water exchange between surface and
subsurface and changes in the sediment composition
at the site. Immediate reductions in density and
taxonomic richness of invertebrates were observed,
together with changes in their community composi-
tion. The hyporheic invertebrate community in the
river recovered relatively fast (in 2.5 months) by
means of density and taxonomic richness, while by
means of community composition invertebrates
needed 5–7 months to recover. The impact of fine
sediments (\0.1 mm) on biofilm activity measured
through ETS activity and hyporheic invertebrate
density and taxonomic richness was strongly con-
firmed in this study.
Keywords Disturbance � In-stream gravel
extraction � Pre-alpine river � Hyporheic zone �Invertebrates � Biofilm
Introduction
Rivers and streams continuously transport and
deposit sediments of a range of granulation through-
out their length. These sediments are often exten-
sively managed or exploited, especially the gravel
(2–64 mm) and sand (0.063–2 mm) fractions. The
extraction of sediments directly from river channels
is usually carried out for commercial reasons (min-
ing), or for maintenance or remediation (Jensen &
Mogensen, 2000).
The consequences of in-stream gravel extraction
include alteration of geomorphological and hydro-
logical characteristics of the river channel and
Electronic supplementary material The online version ofthis article (doi:10.1007/s10750-011-0648-x) containssupplementary material, which is available to authorized users.
Handling editor: Robert Bailey
N. Mori (&) � T. Simcic � S. Lukancic � A. Brancelj
Department of Freshwater and Terrestrial Ecosystems
Research, National Institute of Biology, Vecna pot 111,
1001 Ljubljana, Slovenia
e-mail: natasa.mori@nib.si
123
Hydrobiologia (2011) 667:15–30
DOI 10.1007/s10750-011-0648-x
impacts on aquatic organisms and biogeochemical
processes in the sediments (Jensen & Mogensen,
2000). The impacts are usually referred to under the
general term of ‘mechanical pollution’ (Rivier &
Seguier, 1985). Extraction involves changes in chan-
nel morphology, river-bed elevation (i.e. reduction),
substrate composition and stability, deposit of in-
stream roughness elements (large woody debris,
boulders, etc.), depth, turbidity, sediment transport,
flow velocity and temperature (Jensen & Mogensen,
2000). In-stream sediment mining can disrupt the
balance between sediment supply and transporting
capacity, resulting in channel incision and river-bed
degradation (Kondolf, 1997). Degradation and ero-
sion can extend both upstream and downstream of an
individual extraction operation (Rivier & Seguier,
1985).
The complex and dynamic physical impacts of
gravel extraction influence the chemical and biolog-
ical elements of a riverine ecosystem. Such changes
result in changes in biodiversity and community
composition of microorganisms and invertebrates, as
well as of fish, macrophytes and riparian vegetation.
The scarce ecological studies have shown that river
bed (RB) incision impedes biofilm development and
activity in the sediment (as a result of changes in
vertical distribution of bacteria and biofilm activi-
ties), decreases the efficiency of oxygen consumption
and dissolved organic carbon mobilization in sedi-
ment (Barlocher & Murdoch, 1989), and decreases
nitrate production (Claret et al., 1998). Suspended
sediments can clog up the natural interstices in
substratum, which are of vital importance to certain
species of invertebrates and fish (Rivier & Seguier,
1985). Removal or reduction of existing habitats
leads to depletion of suitable spawning habitats for
fish and decreases benthic invertebrate abundance
and taxonomic richness (Pearson & Jones, 1975;
Rivier & Seguier, 1985; Brown et al., 1998; Kelly
et al., 2005).
Alluvial sediments, which extend vertically and
laterally from the river channel are recognized as a
hyporheic zone (Orghidan, 1959) and are an impor-
tant area of active exchange of water and dissolved
material between river and groundwater. From the
ecological point of view, the hyporheic zone consti-
tutes an ecotone between surface and groundwater
environments and between terrestrial and subterra-
nean aquatic systems on the banks of the river (Gibert
et al., 1990; Vervier et al., 1992). The hyporheic zone
acts as a mechanical, biological and chemical filter
(Vervier et al., 1992). The sediment particles impede
the flow of silt and particulate organic matter,
dissolved minerals and metals are precipitated and
trapped here and the microbial biofilm coating the
sediments takes up or transforms organic compounds
(Hancock, 2002). The hyporheic zone thus contrib-
utes significantly to the metabolism of stream
ecosystems (Grimm & Fisher, 1984), and the biolog-
ical self-purification capacity of the stream is
increased by the contribution of an intact and active
hyporheic zone (Pusch, 1996). Moreover, the porous
sediments in banks adjacent to rivers can act as
buffers to rising water levels and reduce, delay, or
even prevent the occurrence of flooding (Brunke &
Gonser, 1997).
The hyporheic zone is also a habitat for many
surface and groundwater dwelling invertebrates
(Gibert et al., 1994), a site of spawning and egg
incubation for some salmonid species (Geist &
Dauble, 1998), a site of wintering and reproduction
for some benthic fish species (Cobitidae) (Shimizu,
2002; Kawanishi et al., 2010), as well as a nursery
site for some insect taxa, such as Leuctridae and
Heptageniidae (Malard et al., 2003). The hyporheic
sediment pores can act as a refuge for invertebrates
during periods of drought (Williams, 1977), and can
be used by early instars of benthic insects as a refuge
against strong currents (shear stress) and extreme
temperatures, offering stable substrates during bed
load movement (Schwoerbel, 1964; Ward, 1992).
Ecological studies on gravel extraction impacts are
scarce. However, since gravel-bed rivers are often
heavily exposed to in-stream gravel extraction, and
the hyporheic zone plays an important role in-stream
metabolism, it is important to obtain more detailed
information on the consequences of that kind of
activity. The main objectives of our study were to
determine how in-stream gravel extraction affects
the geomorphology and patterns of hydrological
exchange in the hyporheic zone, the hyporheic water
chemistry, and the biofilm activity and structural and
functional biodiversity of the hyporheic invertebrate
community. We hypothesised that (a) down-welling
will increase due to channel incision, followed by
decrease of hydraulic conductivity due to fine sedi-
ment loading, (b) biofilm activity will decrease
following gravel extraction, and (c) invertebrate
16 Hydrobiologia (2011) 667:15–30
123
taxonomic richness and density will decrease signif-
icantly and community composition will change
following gravel extraction.
Materials and methods
Study area
The study was carried out in a downstream section of
the fourth order gravel-bed river Baca in western
Slovenia (SE Europe) (Fig. 1). Its catchment area is
about 145 km2, with geology of predominantly
limestone and dolomite, and a river length of about
25 km. The Baca River is a run-off fed stream, with
torrential nature, where discharge is primarily a
function of rainfall. The mean monthly discharges
over a 13-year period (1991–2004) ranged from
3.15 m3 s-1 (July/August) to 11.34 m3 s-1 (October/
November). Peak discharge reached 243 m3 s-1 in
the same period. Due to the high precipitation rates in
the area, steep relief, and erosion-prone rock in the
catchment, the Baca River is aggrading, with high
production of sand (0.0625–2 mm) and gravel
(2–64 mm).
Sample collection
Two sampling sites, located 2.5 km apart, were
selected: an upstream reference (Site 1 in Fig. 1)
and an impacted site (Site 2 in Fig. 1). Sampling was
carried out seven times from June 2004 to May 2005
Fig. 1 Maps of the study area (above) and sampling stations at reference and impacted sites (below). RB river bed, GB gravel bars
Hydrobiologia (2011) 667:15–30 17
123
(Fig. 2). The first sampling was conducted on 11 June
2004 (pre-disturbance data). Gravel extraction activ-
ities started on 23 October 2004 and finished on 28
October 2004, by which time an area of 10 9 100 m
was excavated to a depth of 3 m. The extraction was
followed by flood event due to heavy rain lasting
from 30 October to 2 November (peak discharge
44 m3 s-1). Post-disturbance sampling was carried
out 8, 15, 23, 77, 139 and 208 days after.
Six stations were installed along the 50 m long
reach at each site. Since hyporheic community is
highly variable within the stream sediments and
depends on the hydrological patterns occurring there,
three hyporheic samples were taken from depths
30–60 cm in the RB and three from depths 60–90 cm
in the gravel bars (GB) in order to adequately
represent the sampling sites (Downes et al., 2002).
Samples from RB and GB constitute observations
from two distinct habitat units in the hyporheic zone,
where habitats in RB are in better hydrological
connection with surface water in comparison with GB
(Fig. 1).
At each sampling station, 10 l mixture of water,
sediment and invertebrates was extracted using a
piston pump fixed on a mobile steel pipe (Ø45 mm)
with a perforated distal end (apertures of Ø10 mm in
a length of 30 cm) (Bou & Rouch, 1967). The method
is not strictly quantitative because faunal density and
diversity cannot be expressed per volume of hypor-
heic sediment. Nevertheless, comparisons between
samples of equal volume and equal depth are still
possible with caution (Malard et al., 2002b). The
mixture of water and sediment was gently elutriated
five times in order to separate invertebrates and
particulate organic matter from the sediment. A hand
net (mesh size 100 lm) was used to filter the water.
The sediment was stored and taken to the laboratory.
Part of this sediment was used as a coarse fraction for
further measurements of biofilm activity. Since the
biofilm in oligotrophic systems frequently disturbed
by flood is thin, the pumping and gentle elutriation of
sediments should not affect its structure. The portion
of the water filtered through the hand net was stored
in 1 l plastic bottles to give hyporheic water and, after
Fig. 2 Mean daily discharge (m3 s-1, grey columns) and
surface water temperatures (�C, black line) of the Baca River
during the study period. Arrows indicate the sampling dates
(preD pre-disturbance sampling, postD1-6 post-disturbance
sampling) and the period of gravel extraction
18 Hydrobiologia (2011) 667:15–30
123
settling, a fine sediment fraction (\0.1 mm) for
measurement of microbial activity. The samples were
refrigerated and taken to the laboratory where
measurements were conducted within 24 h. Another
sample of hyporheic water was stored in a plastic
bottle and taken to the laboratory for chemical
analyses. After collecting the biological samples,
oxygen (WTW Multiline P4, CellOx 325) and
conductivity (WTW Multiline P4, TetraCon 325)
were measured in the hyporheic water in the steel
pipes. Hydraulic head measurements in the RB were
conducted with a T-bar (Malard et al., 2002b).
Laboratory analyses
pH of water samples was measured using a WTW pH
540 GLP, with a TetraCon 325 probe. Nitrate and
sulphate were measured by ion chromatography
(Metrohm, 761 Compact IC; precision ±0.01 ppm).
Coarse sediments extracted from each sampling
station were dried and measured as volume per 10 l
of sample. The amount of fine sediment fraction
(\0.1 mm) in 1 l of water was measured after all
particles had settled in the bottle (after 24 h). The
amount of organic matter was estimated by loss on
ignition (Pusch & Schwoerbel, 1994). After removing
the invertebrates, the particulate organic matter
([0.1 mm) was dried (24 h, 105�C), weighed, burned
(2 h, 520�C) and weighed again. The difference in
weight gave the amount of organic matter in 10 l of
sample.
Electron transport system (ETS) activity was
measured in both surface and hyporheic water, in
the fine (\0.1 mm) and coarse ([0.1 mm) sediment
fractions (Packard, 1971; G.-Toth, 1999) in order to
estimate the microbial activity in the water, and on
the two sediment fractions. Water samples were
filtered through a 100 lm mesh to remove larger
particles, then through a membrane filter (pore size
0.2 lm; Millipore) which was used in analyses.
Water and solid samples were homogenized in 4 ml
final volume of ice-cold homogenization buffer,
using an ultrasonic homogenizer (Cole-Parmer) for
3 min at 40 W, then centrifuged for 4 min at 0�C at
8,5009g (2K15, Sigma). Homogenate incubation and
measurement of formazan production were per-
formed according to the procedure described in
Simcic & Brancelj (2003). ETS activity was mea-
sured as the rate of tetrazolium dye reduction, which
was converted to equivalents of oxygen utilized per
wet mass in a given time interval (ll O2
gWW-1 h-1) (Kenner & Ahmed, 1975).
Oxygen consumption, as a measurement of biofilm
activity, was estimated under laboratory conditions
using the closed bottle method (Lampert, 1984).
Ground glass stoppered bottles (160 ml) were filled
with water aerated in advance for 24 h. About 1 g
wet mass of sediment was added to each of three
bottles for oxygen consumption measurement, and
three bottles without sediment served as controls. All
bottles were closed and kept in the dark at 20�C.
After 48 h, the concentration of dissolved oxygen
was measured using a polarographic oxygen elec-
trode (OXI 96, WTW).
Invertebrates were counted and identified.
Taxa were assigned to the three ecological catego-
ries—permanent hyporheos, occasional hyporheos
(Williams, 1984), and stygobionts (Ginet & Decou,
1977; Botosaneanu, 1986). The classification is based
on their affinity for the hyporheic habitat. Permanent
hyporheos were classified as species that may be
present during all life stages, either in the hyporheic
or benthic habitat, but predominantly in the former.
Occasional hyporheos were classified as larvae of
aquatic insects that spend part of their aquatic-stage
in the surface environment (in addition to the obligate
aerial stage) and part in the hyporheic zone (early
stages). Stygobionts were considered as true ground-
water taxa, completing their entire life cycle in
subsurface water.
Data analyses
A three-way analysis of variance (ANOVA) was used
to test the influence of site, date and habitat type on
differences in physico-chemical characteristics, bio-
film activity and hyporheic invertebrate density and
diversity. A three-way ANOVA consists of seven
significance tests: a test for each of the three main
effects, a test for each of the three two-way interac-
tions and a test of the three-way interaction. Only
significant interactions are presented in the results.
Data were normalized by log10(x ? 1) (for environ-
mental data and invertebrate density) and bypðxþ
3=8Þ (for taxonomic richness) transformations. Cor-
relation between biofilm activity (ETS on fine
sediments) and fine sediment amounts was calculated
using Pearson’s correlation coefficient. Spearman’s
Hydrobiologia (2011) 667:15–30 19
123
rank correlation coefficient was used to search for
relationships between invertebrate diversity and den-
sity and the following environmental characteris-
tics—temperature, conductivity, oxygen, fine and
coarse sediment amounts, organic matter and meta-
bolic activity of biofilm. The analyses were per-
formed using SPSS for Windows, Version 17.0.
Principal component analysis (PCA) was used to
examine the variation in community composition
between reference and impacted sampling sites, pre-
disturbance and post-disturbance sampling occasions
and habitat types. Relationships between environ-
mental data (habitat type, sampling occasion—pre- or
post-disturbance, temperature, conductivity, oxygen,
nitrate, sulphate, fine and coarse sediment amounts,
organic matter contents, biofilm activity) and the
abundances of invertebrate taxa were explored using
canonical correspondence analysis (CCA) (ter Braak
& Prentice, 1988). An unrestricted random Monte
Carlo permutation test under null model was per-
formed to determine the statistical significance of
individual environmental variables. The PCA and
CCA analyses were conducted using the computer
program CANOCO version 4.5 (ter Braak & Smil-
auer, 2002). The invertebrate data were normalized
by log10(x ? 1) in PCA as well as in CCA analyses.
Results
Physical and chemical characteristics
of the hyporheic zone
Temperature, dissolved oxygen, pH, nitrate and sul-
phate concentrations in surface water and hyporheic
water from the RB and GB were similar indicating
good permeability of sediments in the hyporheic zone
and the short retention times of the water in the
sediments (Table 1). However, there was a significant
difference in conductivity between RB and GB and
seasonal variation in temperature, oxygen and con-
ductivity at both sites (Table 3).
Vertical hydrological exchange, sediment
composition and particulate organic matter
The hydraulic heads of the sampling stations were
close to or below zero, indicating a constant flow of
surface water into the RB sediments (Table 1). At the
impacted site, stronger down-welling occurred after
gravel extraction at all sampling stations (-4.8 ±
7.6 cm), the greatest increase being at sampling station
RB3 at the downstream end of the sampling area
(RB3; -30 cm). The mean volume of fine sediments
(\0.1 mm) extracted with the Bou-Rouch pump varied
from 13 to 493 ml 10 l-1 at reference site and from 33
to 180 ml 10 l-1 at impacted site, while the amounts of
coarse sediments ([0.1 mm) ranged from 17 to 712 ml
10 l-1 at reference and from 183 to 1,203 ml 10 l-1 at
impacted site (Fig. 3a, b). After gravel extraction, the
amounts of coarse sediments increased and were
higher in the RB than in GB at impacted site, while
at reference site the amounts were significantly lower
from the impacted site and higher in GB than in RB
(three-way ANOVA, interaction site*habitat, F =
11.28, P \ 0.01) (Table 3). The amount of particulate
organic matter (POM [ 0.1 mm) significantly chan-
ged over the time (Table 3, P \ 0.001) with mean
values ranging from 46 to 748 mgDW 10 l-1 at
Table 1 Average values (±SD) for physical and chemical characteristics of surface water and hyporheic water from the river bed
(depth 30–60 cm) and gravel bars (depth 60–90 cm)
Reference site Impacted site
Surface water River bed Gravel bars Surface water River bed Gravel bars
Vertical hydrological gradient (cm) -1.2 ± 3.4 -4.8 ± 7.6
Temperature (�C) 9.2 ± 4.1 9.7 ± 4.3 10.4 ± 4.6 10.5 ± 5.0 10.8 ± 4.9 11.0 ± 5.8
Dissolved oxygen (%) 106 ± 6 90 ± 13 82 ± 12 100 ± 4 94 ± 7 82 ± 15
Conductivity (lS cm-1) 273 ± 7 275 ± 12 281 ± 13 273 ± 8 271 ± 9 280 ± 16
pH 8.3 ± 0.1 8.1 ± 0.1 8.1 ± 0.1 8.3 ± 0.1 8.2 ± 0.1 8.1 ± 0.1
NO3- (mg l-1) 4.3 ± 0.6 4.1 ± 0.2 4.1 ± 0.5 3.9 ± 0.2 4.0 ± 0.6 4.2 ± 0.4
SO4- (mg l-1) 7.6 ± 1.7 7.2 ± 0.5 7.8 ± 0.9 7.1 ± 0.7 7.5 ± 1.5 7.4 ± 1.6
20 Hydrobiologia (2011) 667:15–30
123
reference site and from 42 to 1,250 mgDW 10 l-1 at
impacted site and being the lowest in the samples from
May 2005 (Fig. 3c).
Biofilm activity
The mean values of ETS activity of hyporheic water,
fine and coarse sediments ranged from 3.12 to 6.50 ll
O2 l-1 h-1, 2.80 to 3.69, and 0.19 to 0.26 ll O2
gWW-1 h-1, respectively. Mean oxygen consump-
tion rates were from 1.44 to 2.39 ll O2 gWW-1 h-1
for fine and from 0.15 to 0.24 ll O2 gWW-1 h-1 for
coarse sediments (Table 2). Oxygen consumption
rates of fine and coarse sediments significantly
changed over the time (P \ 0.05 and \ 0.001,
respectively) and oxygen consumption rates of coarse
Fig. 3 The average of a volume of fine sediments (\0.1 mm),
b volume of coarse sediments ([0.1 mm), and c dry weight of
organic matter extracted with a Bou-Rouch pump from six
sampling stations (RB and GB) at the reference and impacted
sites on seven sampling occasions (n = 3). Error barsrepresent 1 SE
Table 2 Average values (±SD) for ETS activity and oxygen consumption rates (R) in the hyporheic water, and fine and coarse
sediments from the river bed (depth 30–60 cm) and gravel bars (depth 60–90 cm)
Reference site Impacted site
River bed Gravel bars River bed Gravel bars
ETS activity—hyporheic water (ll O2 l-1 h-1) 3.12 ± 2.03 No data 4.91 ± 3.68 6.50 ± 3.94
ETS activity—fine sediments (ll O2 gWW-1 h-1) 2.80 ± 2.99 No data 3.69 ± 3.84 2.88 ± 1.34
ETS activity—coarse sediments (ll O2 gWW-1 h-1) 0.26 ± 0.20 No data 0.20 ± 0.11 0.19 ± 0.09
R—fine sediments (ll O2 gWW-1 h-1) 1.44 ± 0.94 No data 2.39 ± 1.28 2.39 ± 1.37
R—coarse sediments (ll O2 gWW-1 h-1) 0.24 ± 0.15 No data 0.18 ± 0.15 0.15 ± 0.05
Hydrobiologia (2011) 667:15–30 21
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sediments were significantly lower at impacted site
(P \ 0.01) (Table 3). The amounts of fine sediments
and ETS activity of fine sediments were negatively
correlated (r = -0.60, P \ 0.001) (Fig. 4).
Hyporheic invertebrate community
The most frequent taxa in the majority of samples were
Chironomidae, Leuctra sp. and Baetoidea (occasional
hyporheos), and Nematoda, Oligochaeta and juvenile
Cyclopoida (permanent hyporheos). The most fre-
quent stygobitic species was Diacyclops languidoides
(Lilljeborg, 1901). Stygobionts occurred in much
lower abundance and frequency than occasional and
permanent hyporheos (Supplementary material—
Appendix A).
Total invertebrate density ranged from 96 to 1,309
individuals 10 l-1 at reference site and from 10 to
1,191 individuals 10 l-1 at impacted site, while
taxonomic richness at reference site was from 8 to
19 taxa and at impacted site 4 to 16 taxa 10 l-1
(Fig. 5). Total invertebrate density, density of occa-
sional and permanent hyporheos, as well as total
taxonomic richness and number of taxa of occasional
and permanent hyporheos did not differ between RB
and GB, but significantly changed over the time
(decreased after flood and gravel extraction). The
density and number of stygobitic taxa did not
significantly change over the time. The impact of
the site was significant for the density of permanent
hyporheos and stygobionts, total taxonomic richness
and taxa number of all three ecotypes, but not for
total density and density of occasional hyporheos
(Table 4).
Significant correlations were found for the
amounts of fine sediments (\0.1 mm) extracted from
Table 3 Analysis of variance of physico-chemical and biofilm characteristics in the hyporheic zone, using a factorial design (dates,
sites and habitats as fixed factors)
Source of variation df MS F P df MS F P df MS F P
Temperature
(n = 52, log transformed)
Oxygen
(n = 43, log transformed)
Conductivity
(n = 51, log transformed)
Site 1 0.02 3.62 0.07 1 0.00 0.25 0.62 1 0.00 2.87 0.10
Date 6 0.36 80.40 \0.001 6 0.03 5.17 \0.01 5 0.00 10.19 \0.001
Habitat type 1 0.00 0.03 0.86 1 0.01 1.87 0.18 1 0.00 4.88 \0.05
Date*site 3 0.02 4.50 <0.05
Organic matter
(n = 75, log transformed)
Fine sediments (\0.1 mm)
(n = 61, log-transformed)
Coarse sediments ([0.1 mm)
(n = 75, log transformed)
Site 1 0.09 0.57 0.45 1 1.08 3.12 0.09 1 0.77 2.30 0.14
Date 6 1.45 9.47 \0.001 5 0.15 0.43 0.82 6 0.19 0.56 0.76
Habitat type 1 0.14 0.89 0.35 1 0.04 0.11 0.74 1 0.01 0.02 0.90
Site*habitat 1 3.79 11.28 \0.01
ETS—hyporheic water
(n = 54, log transformed)
ETS—fine sediments
(n = 45, log transformed)
ETS—coarse sediments
(n = 51, log transformed)
Site 1 0.19 1.97 0.17 1 0.30 2.31 0.14 1 0.04 0.52 0.48
Date 5 0.09 0.94 0.47 5 0.13 1.04 0.41 5 0.06 0.91 0.49
Habitat type 1 0.27 2.90 0.10 1 0.02 0.14 0.71 1 0.01 0.08 0.78
Oxygen consumption rate—fine sediments
(n = 36, log transformed)
Oxygen consumption rate—coarse sediments
(n = 36, log transformed)
Site 1 0.30 3.48 0.08 1 0.23 11.56 \0.01
Date 5 0.35 4.04 \0.05 5 0.22 10.96 \0.001
Habitat type 1 0.00 0.05 0.82 1 0.00 0.00 0.99
Site*habitat 5 0.24 11.97 \0.001
The significance tests are shown only for the three main effects and significant interactions
df degrees of freedom, MS mean square, F F-statistics, P probability
22 Hydrobiologia (2011) 667:15–30
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the hyporheic zone and total invertebrate density and
taxonomic richness, as well as densities and taxo-
nomic richness of all three ecotypes, while the
amounts of coarse sediments were in significant
correlation with total density, and density and taxa
number of occasional hyporheos (Table 5).
Principal component analysis ordination resulted
in the clustering of the November samples (SD1–3)
and the samples from the January and March (SD4–5)
from the impacted site into two relatively homoge-
neous and distinct groups, while the samples from the
pre-disturbance date and May samples (SD6) from
the impacted site grouped together with the samples
from the reference site. The samples SD4 and SD5
were associated with higher densities of Baetoidea,
while the samples from the reference site were the
most distinct from the other two groups due to the
presence of Acanthocyclops gmeineri Pospisil 1989,
Hydracarina, Dytiscidae and Polycentropodidae
(Fig. 6).
Canonical correspondence analysis conducted on
data from the impacted site explained 44.9% of the
community variability. The first axis correlates
positively with conductivity, nitrates and sulphates
and accounts for 18.7% of the species–environment
relationship. The second axis represents a gradient of
decreasing organic matter and coarse sediments, and
increasing ETS activity in the hyporheic water and
accounts for further 14.1% of the species–environ-
ment relationship (Fig. 7). CCA indicates that inver-
tebrate community at the impacted site was
significantly related to sampling occasion (pre- or
Fig. 4 Relationship
between the amount of fine
sediment in 10 l of sample
(particles \0.1 mm) and
ETS activity of the fine
sediment fraction in
samples from the hyporheic
zone of the Baca River
(n = 46)
Fig. 5 The average of a hyporheic invertebrate densities and b taxonomic richness at the reference and impacted sites on seven
sampling occasions (n = 3). Error bars represent 1 SE
Hydrobiologia (2011) 667:15–30 23
123
post-disturbance dates), temperature, conductivity
and nitrate. In contrast, at the reference site, where
CCA explained 54.7% of the community variability,
invertebrates were significantly related to sampling
occasion, conductivity, fine sediment amounts and
ETS of hyporheic water.
Table 4 Analysis of variance in various descriptors of hyporheic invertebrate community, using a factorial design (dates, sites and
habitats as fixed factors)
Source of variation df MS F P df MS F P
Total density
(n = 75, log-transformed)
Total number of invertebrate taxa
(n = 75, square root-transformed)
Site 1 0.47 1.57 0.22 1 3.49 7.74 \0.01
Date 6 2.38 7.90 \0.001 6 1.83 4.06 \0.01
Habitat type 1 0.00 0.01 0.91 1 0.00 0.00 0.98
Density of permanent hyporheos
(n = 75, log-transformed)
Number of taxa—permanent hyporheos
(n = 75, square root-transformed)
Site 1 1.67 5.37 \0.05 1 1.22 4.05 \0.05
Date 6 3.58 11.55 \0.001 6 1.19 3.94 \0.01
Habitat type 1 0.07 0.22 0.64 1 0.10 0.34 0.57
Density of occasional hyporheos
(n = 75, log-transformed)
Number of taxa—occasional hyporheos
(n = 75, square root-transformed)
Site 1 0.03 0.09 0.77 1 1.10 4.27 \0.05
Date 6 1.88 5.12 \0.001 6 0.79 3.06 \0.05
Habitat type 1 0.14 0.39 0.54 1 0.39 1.52 0.22
Density of stygobionts
(n = 75, log-transformed)
Number of taxa—stygobionts
(n = 75, square root-transformed)
Site 1 3.56 12.83 \0.001 1 0.91 5.18 \0.05
Date 6 0.22 0.80 0.57 6 0.36 2.07 0.07
Habitat type 1 0.61 2.21 0.14 1 0.05 0.31 0.58
The significance tests are shown only for the three main effects. The tests for interactions were not significant and are not presented
df degrees of freedom, MS mean square, F F-statistics, P probability
Table 5 Spearman rank correlation coefficients between selected physico-chemical and biofilm characteristics in the hyporheic zone
and hyporheic community descriptors
n Total
density
Total taxa
number
PH
density
PH taxa
number
OH
density
OH taxa
number
Sty
density
Sty taxa
number
Temperature 52 -0.20 -0.11 0.18 0.01 -0.36** -0.15 -0.24 -0.25
Conductivity 51 -0.07 0.06 -0.33* -0.03 0.07 0.04 0.24 0.22
Oxygen 43 0.20 0.11 -0.04 0.07 0.37* 0.10 0.14 0.21
Organic matter 75 0.22 0.28* 0.04 0.18 0.31** 0.29* 0.19 0.20
Fine sediments 63 0.42** 0.44** 0.38** 0.29* 0.37** 0.39** 0.39** 0.36**
Coarse sediments 75 0.27* 0.21 0.14 0.07 0.31** 0.24* 0.15 0.16
ETS—fine sediments 46 0.22 -0.02 0.09 -0.03 0.22 -0.01 -0.01 -0.03
ETS—coarse sediments 51 0.06 0.00 0.06 -0.05 0.06 0.08 0.06 -0.03
R—fine sediments 36 -0.18 -0.28 -0.32 20.42* -0.08 -0.17 -0.05 -0.06
R—coarse sediments 50 -0.10 -0.12 0.06 -0.20 -0.22 -0.02 -0.14 -0.09
ETS respiratory electron transport system activity of biofilm, R oxygen consumption rate of biofilm, PH permanent hyporheos,
OH occasional hyporheos; Sty stygobionts
Significance level: * P \ 0.05, ** P \ 0.01
24 Hydrobiologia (2011) 667:15–30
123
Discussion
Characteristics of the hyporheic zone in the river
Baca
The measurements of vertical hydraulic gradient
(VHG) and physico-chemical characteristics (temper-
ature, conductivity, oxygen) of surface and hyporheic
water from the RB and GB in the river Baca indicate
high rates of surface–subsurface exchange, vertically
(into the RB) and laterally (into GB), as well as short
retention times of stream water in the hyporheic zone
due to the high permeability (hydraulic conductivity)
of sediments. Moreover, the measurements of nutrient
concentrations revealed relatively low trophic level of
this river system. Consequently, the biofilm activity
measured as respiratory ETS activity and oxygen
consumption rates were relatively low in all three
fractions (water, fine and coarse sediments). From
previous studies it is well known that sediment grain
size, as well as hydrological exchange patterns and
sediment stability, influence biogeochemical pro-
cesses in the hyporheic zone and shape the hyporheic
invertebrate communities (Gibert et al., 1994;
Findlay, 1995; Brunke & Gonser, 1997; Mulholland
& DeAngelis, 2000; Boulton, 2007; Datry et al.,
2007). The hyporheic zone of the river Baca, was
inhabited by a highly resilient hyporheic invertebrate
community composed mainly of Cyclopoida (with
predominance of copepodites), and Chironomidae,
Leuctra sp. and Baetoidea larvae. Cyclopoida have
been reported as a major component of hyporheos
(Boulton et al., 1992; Hunt & Stanley, 2003), and
juvenile Copepods were found to dominate in the
hyporheic zone (72% of all individuals), in which harsh
environmental conditions shape the community compo-
sition (Malard et al., 2003). Stygobionts (groundwater
dwelling species) were present at low density and low
taxonomic richness, as found by Fowler & Death (2001)
in river sediments frequently disturbed by flood.
The effect of gravel extraction on hydrologic
exchange and biogeochemical processes
In-stream gravel extraction caused structural changes
in the river channel (incision and change in grain size
Fig. 6 PCA ordination
diagram of species (arrows)
and samples (points) from
the hyporheic zone
collected before and after
gravel extraction at
reference and impacted site.
Filled square reference site,
pre-disturbance date; filledcircle reference site, post-
disturbance dates; opensquare impacted site, pre-
disturbance date; opencircle impacted site, post-
disturbance dates
Hydrobiologia (2011) 667:15–30 25
123
distribution). The upper layer of mostly gravel (3 m in
depth) was replaced by finer sediments, originating
from upstream. The incision altered the pattern of
hydrological exchange at the impacted site with
increased input of surface water into the hyporheic
zone (strong down-welling). The sediment composi-
tion at the sampling stations was estimated by the
volume of sediment extracted by the Bou-Rouch
pump, a method that has been shown to be a good
indicator of permeability and rate of consolidation of
RB sediments (Malard et al., 2002b). The particles of
the size 5 mm were the largest particles, which were
still possible to extract with the piston pump. The
amounts of sediment extracted do not show the true
sediment composition in the hyporheic zone, but they
give the information about the proportion of small
gravel and sands (\5 mm) there. Since grain size
distribution is linked to permeability (Malard et al.,
2002a), increased amounts of extracted sediments
probably led to decreased permeability at the impacted
site. Changes in hydrological exchange and sediment
permeability (hydraulic conductivity) can affect the
residence time of water in the hyporheic zone (Freeze
& Cherry, 1979), and the residence time of advected
channel water within the subsurface influences the
type of biogeochemical processes operating within the
site (Malard et al., 2002a). In our study the assumed
decrease in hydraulic conductivity at impacted site
have not been found to affect the mayor physical and
chemical characteristics, as well as have not influ-
enced a respiratory ETS activity of microorganisms in
the hyporheic water and those attached to the
sediments. However, the oxygen consumption rates
(R) on coarse sediments have been shown to be
significantly lower at impacted than at reference site in
a month after gravel extraction (SD1–3). Those results
indicated the link between permeability and biofilm
activity. The reason that significant differences were
found (sites, P \ 0.01; time P \ 0.001) in oxygen
consumption rates but not in ETS activity is probably
due to the fact that the ETS activity of microbes
responds more slowly to environmental change than
respiration rate (Bamstedt, 1980). Relatively small
and insignificant variations in ETS activity could be
explained by the low values of POM and low water
temperatures (10.1 ± 4.3�C in 2004/2005). This is in
agreement with the results of Craft et al. (2002), who
found equivalent aerobic microbial activity on a
macro-scale (metres to kilometres) in an oligotrophic
gravel-bed river. However, the analysis of ETS
Fig. 7 CCA biplot of
hyporheic samples taken at
impacted site on seven
occasions relative to 15
environmental parameters.
The value (%) under each
axis label represents the
percentage of the species–
environment relationship
accounted for by that axis.
Open square pre-
disturbance date, RB; filledsquare pre-disturbance date,
GB; open circle post-
disturbance dates, RB; filledcircle post-disturbance
dates, GB
26 Hydrobiologia (2011) 667:15–30
123
activity on different sediment fractions and in surface
and hyporheic water showed that different fractions
contribute differently to the total mineralization in the
areas of different intensity of surface–subsurface
water exchange and the consolidation rate of sedi-
ments (Simcic & Mori, 2007). Hyporheic water and
fine sediment particles (\0.1 mm) are more important
components for mineralization in more consolidated
sediments, in which water exchange is less intense,
while coarser sediment particles (0.1–5 mm) contrib-
ute significantly to the mineralization in less consol-
idated sediments. Furthermore, we observed a strong
negative correlation between the volume of fine
sediment (\0.1 mm) and ETS activity (R = -0.60,
P \ 0.001), suggesting that increased fine sediment
amounts could impede biofilm activity, probably as a
result of consolidation and clogging of interstices as
shown by Songster-Alpin & Klotz (1995). Clogging of
the sediments with silt (colmation) fills interstitial
spaces and impairs hydrological exchange with the
overlying water, reducing the influx of dissolved
oxygen, nutrients and organic matter in the hyporheic
zone (Brunke & Gonser, 1997).
The response of the hyporheic invertebrate
community
Stream invertebrates from the rivers frequently
disturbed by floods are characterized by high resis-
tance and resilience (Townsend & Hildrew, 1994).
The previous observations of recovery rates due to
flood in the hyporheic zone are highly variable. Dole-
Olivier et al. (1997) observed the recovery of
hyporheic invertebrates in 7 days, Olsen & Townsend
(2005) in one month and Hancock (2006) in four and
a half months. The differences in recovery rates
occurred most probably due to different hydrological
regimes in the rivers studied (Hancock, 2006). The
hyporheic community of the Baca River recovered
after gravel extraction in two and a half month by
means of density and taxonomic richness. However,
the community composition recovered much later
(after 7 months). Due to the fact that coincidently a
flood occurred 2 days after gravel extraction (Fig. 2),
we had the opportunity to compare the effect of
anthropogenic disturbance versus natural one. Our
results suggest that density and taxonomic richness
was more seriously affected after anthropogenic
disturbance than after flood, and that recovery in
taxonomic richness after spate occurred sooner
(1–2 weeks) than that after gravel extraction
(2.5 months), while density needed 2.5 months at
both sites to recover. The former was previously
shown by Matthaei et al. (1997), who demonstrated
that experimental disturbance has more severe
impacts on benthic invertebrates than flood. The
reason could be that experimental disturbances,
which can be comparable in some way to gravel
extraction, are very sudden, whereas discharge
increases more gradually during a spate and inverte-
brates are able to search for refugee in the spatial
heterogenic structure of the RB. Moreover, during
gravel extraction, the whole upper layer of the river
sediments is suddenly removed over larger area (in
this study—100 m in length), in this way little or no
refugees is left for invertebrates. The invertebrate
community at the site of that kind of impact is most
probably recovered by colonization through drift and
upstream and downstream migration through the
sediments, which took in our case between one to two
and a half months. Invertebrate density and taxo-
nomic richness recovered in 2.5 months while the
community composition needed between 5 to
7 months to recover. The samples collected in a first
month after gravel extraction were characterized by
low densities in general, and January and March
samples (SD4–5) at impacted site were composed
mainly of large numbers of Baetoidea larvae (occa-
sional hyporheos).
Canonical correspondence analysis of environ-
mental and invertebrate data revealed the importance
of sampling occasion and conductivity for the
hyporheic community at both sites. It seems that
the hyporheic invertebrate community exhibited great
seasonal variation due to high variation in discharge
and a range of different annual life cycles and
reproductive patterns of occasional and permanent
hyporheos, while the populations of stygobionts
remains more stable and more likely respond to
changes in surface–subsurface water flow. Since
conductivity is indirect indicator of surface–subsur-
face hydrological exchange (Pospisil, 1994) this
could be the reason why this parameter was recog-
nized as an important factor for shaping the inverte-
brate community. Moreover, at impacted site,
temperature and nitrate contents, and at reference
site, fine sediments and ETS activity in the hyporheic
water revealed as important factor for invertebrates.
Hydrobiologia (2011) 667:15–30 27
123
Temperature is also an indicator of hydrological
exchange between surface water and groundwater
(Pospisil, 1994), while the other factors suggest
the importance of food resources in shaping the
hyporheic community. The majority of stygobionts
and permanent hyporheos at the impacted site
occurred along the gradient of decreasing biofilm
activity and organic matter content, and in the areas
with coarser sediments (decreasing amounts of sed-
iment extracted). In the samples where finer sedi-
ments prevailed and organic matter content and
biofilm activity were higher, occasional hyporheos
dominated. The great importance of the presence of
the fine sediment fraction (particles\0.1 mm) for the
composition of the hyporheic community is also
indicated in our study. Olsen & Townsend (2003)
found similar correlations between fine sediment
(0.063–1 mm) and hyporheic invertebrate distribu-
tion. Furthermore, analysis of hyporheic communities
from Oklahoma (USA) streams revealed the impor-
tance of substrate composition in determining the
composition and abundance of invertebrates (Hunt &
Stanley, 2003). Fine sediment may have a direct
effect on invertebrates through its particular habitat
characteristics, such as pore size, or by restricting
their ability to feed, respire or move (Olsen &
Townsend, 2003). Indirect effects of increasing
amounts of fine sediment include lowering the
permeability and residence time of water, which
affects the physical and chemical conditions in the
hyporheic zone (Jones & Holmes, 1996), and conse-
quently biofilm activity as noted earlier. Biofilm is a
potential food resource for many invertebrates inhab-
iting the hyporheic zone. Those observations were
supported by the correlation between the amount of
fine sediment and its ETS activity. The latter
decreased following an increase in fine sediment
amounts in the hyporheic zone, which probably
resulted in decrease in the food resources for
invertebrates.
The results of this study indicate that discharge
and gravel extraction activities in the river channel
were the major forces in shaping the hyporheic
invertebrate community in the river Baca. The in-
stream gravel extraction has been shown to affect
surface–subsurface water exchange (increased down-
welling) and to change the sediment composition at
the impacted site. Removal of the upper sediment
layer and the consequent changes in permeability led
to short-term decrease in biofilm activity (measured
as oxygen consumption rates) and invertebrate den-
sity and richness. Occasional hyporheos revealed to
be more resilient than stygobionts and permanent
hyporheos, most probably due to higher mobility and
habitat generalist traits of the former taxa. Moreover,
the shift in invertebrate community composition was
observed following gravel extraction at impacted site
with higher proportion of occasional hyporheos in
comparison with reference site. The above observa-
tions suggest that in-stream gravel extraction could
be more severe distraction for hyporheic invertebrate
community than extreme flood events that occur
every few years.
Acknowledgments The authors thank C. Fiser, C. Meisch, I.
Sivec, B. Sket, G. Urbanic, and D. Zabric for their help in
determining Ostracoda, Amphipoda, Isopoda, Plecoptera,
Trichoptera and Ephemeroptera and A. Jerebic for chemical
analyses of water samples. Special thanks go to D. Jesensek
from Tolmin Angling Club for providing information about
gravel extraction activities in the river Baca. Critical and
constructive comments from the reviewers and an editor
greatly improved the manuscript. The research was supported
by the Slovenian Ministry of Higher Education, Science and
Technology.
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