Aquacult Int (2013) 21:1–17

DOI 10.1007/s10499-012-9527-3

Bioturbation of sediments by benthic macroinvertebrates

and fish and its implication for pond ecosystems: a review

Zdeněk Adámek • Blahoslav Maršálek

Received: 6 September 2011 / Accepted: 21 March 2012 / Published online: 27 April 2012
 Springer Science+Business Media B.V. 2012

Abstract Bioturbation of bottom sediments at the sediment–water interface is currently

gaining more attention in studies dealing with the functioning of aquatic ecosystems. Such
bioturbation can be caused by a variety of benthic macroinvertebrates or benthivorous fish
that forage and burrow various bottom tubes, holes and pits. Thus, the processes involved
may either be a result of direct interception by benthic animals, e.g., through bioresus-
pension of particles or through food ingestion and biodeposition, or of other indirect
effects, e.g., changes in the physical properties of sediments or through the constructions
mentioned above, along with corresponding changes in pond ecosystem functioning. The
most distinct effect of benthivorous fish bioturbation activities is an increase in the tur-
bidity of the water, which can lead to many subsequent knock-on effects, including
inhibition of phytoplankton and submersed macrophyte growth with resulting alterations in
physico-chemical water conditions. The importance of benthic macroinvertebrates and fish
in bioturbation processes is also indicated by an increase in the numbers of resting
cyanobacterial colonies recruited due to bioturbation of bottom sediments.

Keywords Benthic macroinvertebrates
Benthivorous fish
Bottom-water interface

Nutrient cycling
Pond management

Introduction

The sediment–water interface in aquatic systems is a bridge connecting bottom sediments

with the overlying water column. The transition zone between oxygenated overlying water

Z. Adámek (&)
South Bohemian Research Centre of Aquaculture and Biodiversity of Hydrocenoses and Research
Institute of Fish Culture and Hydrobiology, Faculty of Fisheries and Protection of Waters, University
of South Bohemia in České Budějovice, Zátišı́ 728/II, 389 25 Vodňany, Czech Republic
e-mail: adamek@ivb.cz

B. Maršálek
Department of Experimental Phycology and Ecotoxicology, Institute of Botany,
Czech Academy of Sciences, Průhonice, Czech Republic

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and anoxic, or anaerobic, sediments takes place over a gradient of just a few millimetres
(Meijer and Avnimelech 1999; Phan-Van et al. 2008) and can easily be disturbed by
mechanical mixing (bioturbation). Bioturbation can be defined as the reworking and
mixing of sediment at the sediment–water interface, accomplished collectively by bur-
rowing, feeding, irrigation, resuspension, secretion, excretion and transporting activities of
benthic organisms and/or benthivorous fish, which alter the structure and properties of the
sediment and thereby influence diffusive and/or advective transport of both solutes and
particulate matters (De Haas et al. 2005; Meysman et al. 2006). Bioturbation, caused
predominantly by burrowing and foraging fish and invertebrates (worms, insect larvae,
crustaceans and molluscs) moving around, also frequently affects the underlying sediment
layers (Scheffer 1998; Avnimelech et al. 1999; Brönmark and Hansson 2005). Bioturbation
increases also turbidity from suspended sediment (Croel and Kneitel 2011) and initiates a
range of transportation activities mediated by benthic animals and benthivorous fish,
including advective transport of both solutes and particulate matter. These activities may
result in a considerable change in conditions and transfer mechanisms at the sediment–
water interface (Ritvo et al. 2004) and, subsequently, translocate nutrients across habitats.
As diagenetic processes progress, bioturbation influences solute exchange across the
sediment–water interface. Some authors consider the effect of mechanical mixing to be
zero (Lamarra 1975) or to have little effect (Keen and Gagliardi 1981) on phosphorus
release and increased phytoplankton development. Hrbáček and Procházková (1975),
however, have shown that mixing of sediment increases the release of nutrients consid-
erably. The effect of mechanical mixing of sediments is arguably dependant upon the
mechanism of mixing, as documented by Qin and Threlkeld (1990). They observed no
effect of mechanical mixing when applying five to six sweeps from a canoe paddle once a
week (sufficient to visibly increase turbidity and resuspend some benthic material);
however, mixing of sediment during common carp (Cyprinus carpio) feeding activity
(supported by airlift) resulted in increased nutrient levels, turbidity and seston particle
dynamics.
The sediment of aquatic ecosystems is widely known to act as a reservoir of nutrients,
organic compounds and a wide variety of solutes (Boyd 1995; Woodruff et al. 1999),
mainly due to the accumulation of organic matter of autochthonous and allochthonous
origin. Flux of such nutrients from sediment to overlying water as a result of decompo-
sition and mineralisation processes is a common phenomenon in aquatic habitats. Nutrient
concentrations in pond bottom soil are typically 2–4 orders of magnitude higher than in
water (Boyd 1995), with the amounts of most chemical components in a 1-cm superficial
pond soil layer being generally higher than those present in 1 m of overlying water
(Avnimelech et al. 1999). Under these circumstances, resuspension can represent a major
mechanism for material and nutrient transfer between sediment and water (Persson and
Svensson 2006).
Bioturbation affects the transport of nutrients, and particularly of phosphorus (P) and
nitrogen (N), through the sediment–water interface. Sediments often have lower oxygen
concentrations than the overlying water due to high rates of decomposition by bacteria.
The activity of bioturbating animals increases oxygen penetration into the sediment
(Brönmark and Hansson 2005), which enhances the mineralisation processes by which
nutrients (mainly phosphate and ammonia) are released to the overlying water (Fukuhara
and Sakamoto 1987; Jana and Das 1992; Jana and Sahu 1993; Hansen et al. 1998).
Bioturbation may provide a mechanism for the return of buried eggs to the sediment
surface (Kearns et al. 1996). The ecological and evolutionary dynamics of phytoplankton
(cyanobacteria in particular) and zooplankton are, in part, a function of the number and age

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of diapausing eggs hatching from aquatic sediments. Successful recruitment from this ‘‘egg
bank’’ depends upon the eggs being present at or near the sediment surface. Often, how-
ever, resting cells of diapausing cyanobacteria or zooplankton eggs are found as deep as
15–30 cm in the mud. Bioturbation and sediment mixing is of particular importance for the
recruitment of Microcystis colonies (Misson et al. 2011).
It is clear from the above, therefore, that opinions differ widely on the importance of
bioturbation for processes in water ecosystems and that a new review of the various
opinions is overdue. Reviews on bioturbation processes published in the 1970s and 80s
(Krantzberg 1985; Andersson et al. 1988) focused mainly on the effects of invertebrates on
oxygen content, redox potential discontinuity, metal distribution, nutrient cycling and
microbial activities (e.g. Petr 1977; Aller 1978; Håkansson and Jansson 1983; Matisoff
et al. 1985). Since then, much more effort has been put into studies of processes taking
place at the sediment–water interface, on turbidity and on the release of nutrients and
resting stages of zoo- and phytoplankton (cyanobacteria). Further, considerable attention is
now being given to the impact of bioturbation by benthivorous fish, an issue of particular
importance in fish pond management and measures aimed at reclamation of still water
health. The purpose of this paper, therefore, is to not only review recent knowledge about
the processes associated with bioturbation but also its background and consequences as
currently accepted and interpreted.

Invertebrates

Bioturbation, which may be caused by a variety of benthic macroinvertebrates, including

chironomids (e.g. Chironomus plumosus), oligochaetes (e.g. Tubifex, Limnodrilus), chao-
borids (Chaoborus), crustaceans (e.g. Lepidurus, Asellus, Gammarus, Astacidae), bivalves
(e.g. Pisidium, Sphaerium, Anodonta) and many others, can play an important role in
nutrient flux from sediments into the water column (Andersson et al. 1988; Mulsow et al.
1998; Risnoveanu et al. 2002, 2004). Benthic animals display a range of mechanical
activities in sediment and, therefore, they may affect solute exchange across the sediment–
water interface in different ways (Zhang et al. 2010). The processes involved in such
biologically mediated fluxes may be a result of direct interception by benthic animals, e.g.,
through bioresuspension of particles or food ingestion and biodeposition, or other indirect
effects such as changes in the physical properties of sediments or through constructions
such as tubes and pits and corresponding changes in physicochemical conditions of water
(Graf and Rosenberg 1997; Svensson 1998).

Material and nutrient flux

Invertebrates may mix sediment particles in a variety of ways. Tubificid worms (Tubifex
tubifex), for example, have been shown to enhance nutrient and organic matter processing
(Mermillod-Blondin et al. 2000). They are important ‘‘conveyor-belt’’ feeders because
dense populations can rapidly rework bottom deposits through selective ingestion of silt
and clay (Dafoe et al. 2011). They live head down in the sediment and excrete faeces at the
sediment surface, causing an upward movement of particles. Respiratory irrigation is
mediated through undulating movements of the posterior end but no permanent burrows
are constructed (Andersson et al. 1988).
Many chironomids feed or collect settling bioseston at the surface and excrete deeper
down, thereby causing a net downward transport of carbon. Since they differ greatly in

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their feeding and burrowing activities, certain chironomid species may play important roles
in driving nutrient cycling, as demonstrated by Jiang et al. (2010) who compared biotur-
bating efficiency in C. plumosus and Tanypus chinensis. Whilst burrowing activities of
T. chinensis larvae in the surface sediment had little effect on sedimentary oxygen demand,
C. plumosus produced significantly higher values. Nevertheless, the authors concluded that
both these chironomid species exerted distinct impacts on sedimentary metabolism, both in
terms of sedimentary oxygen demand and nutrient flux rates, in different ways.
A positive relation between the rate of phosphate liberation from sediment cores and the
amount of benthic macrofauna has been observed in several investigations (Holdren and
Armstrong 1980; Wisniewski and Planter 1985; Starkel 1985). Based on a number of
different studies regarding benthic invertebrates and phosphorus cycling, Andersson et al.
(1988) came to the reasonable conclusion that bioturbation is an important process for the
mineralisation of sedimented particulate organic material and for the subsequent return of
dissolved substances to water (Fig. 1); the increased release of phosphorus from sediment
to water in the presence of macroinvertebrates, however, is most likely the result of
physical mixing and not caused solely by excretion. Further, the release of phosphorus
from lake sediments may not be in direct proportion to bioturbation as phosphorus can be
sorbed at the sediment–water interface as a consequence of redox- or pH-sensitive
chemical reactions.
Bioturbation effects are obviously accentuated with increasing density of benthic bio-
turbators. The recruitment of chironomid larvae (2.0 individuals/cm2) resulted in a 21 and
19 % increase in aquatic orthophosphate and nitrate quanta, respectively, with a con-
comitant decrease in nutrient concentration in the sediment compared to macrofauna-free
controls under mesotrophic conditions (Biswas et al. 2009). This implies that the cost of
fertiliser for biological production could be curtailed by at least 19–21 % through recov-
ering nutrients stored in the sediment pool. Bioturbation-induced orthophosphate flux
under chironomid impacted mesotrophic treatment was approximately two times greater
than that under bioturbated eutrophic treatment, suggesting that the macrofaunal impact
was reduced in the presence of a higher nutrient load, perhaps due to physicochemical
stressors under eutrophic conditions. Nevertheless, chironomid larvae can further accel-
erate nutrient enrichment in a eutrophic system, possibly producing a ‘‘snowball effect’’

Fig. 1 The release rate of total phosphorus as a function of Chironomus tentans density (redrawn from
Gallepp 1979 in Andersson et al. 1988)

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resulting in hypereutrophic conditions. As shown by Henry and Santos (2008), however, both
release and excretion of ammonium and phosphate by Chironomus larvae must be considered
as important sources of these nutrients (2.014 ± 5.134 and 1.643 ± 3.974 lg m-2 day-1,
respectively, at a mean biomass of 34 mg m-2 dw of Chironomus).
The form and extent of galleries created by burrowing invertebrates influences sediment
structure, bioturbation and the flux of nutrients and contaminants between sediment and the
water column (Gosselin and Hare 2003). Also, both small (Pisidium, Sphaerium) and larger
bivalves (Anodonta, Unio, Synanodonta) cause bioturbation by ploughing through sub-
surface sediment layers (Jonasson 1972). In addition to such ‘‘macro-bioturbators,’’ smaller
invertebrates (Protozoa, Nematoda, Harpacticoida and Ostracoda) may also affect the
sediment water interface in the same manner. These are, however, of such a small size that
their ability to transport solutes and particulate matter is limited (Andersson et al. 1988).
Despite their limited ability to transport solutes and particulate matter per se, it is
necessary to keep in mind that the bioturbation processes performed by benthic inverte-
brates are strengthened, supported and complemented by the feeding habits of benthiv-
orous fish (see below) that target just such prey, i.e., oligochaetes, chironomid and phantom
midge fly larvae and other invertebrates, and hence function as bioturbators themselves. Of
these invertebrates, Biswas et al. (2009) identified chironomid larvae (the preferred food
item of cyprinid benthivorous fish) in particular as having a pivotal role as potential drivers
of nutrient dynamics in ponds under mesotrophic conditions. The authors concluded that
induced mobilisation of bound phosphate of subsurface sediments to the overlying water
confirmed the role of chironomids not only as an important source of food for benthic fish
but also as a major contributor to the phosphorus flux from sediments of ponds with
residual organic load. Further, sediment reworking and bioirrigation reduces the build-up
of toxic metabolites in the sediment and thus promotes positive specific interactions.

Oxygen transport and nutrient release

It is frequently said that the support of oxygen flux into hypoxic and/or anaerobic sedi-
ments is a key phenomenon in bioturbation caused by benthic macroinvertebrates. The
burrow of a chironomid larva, for example, is surrounded by oxygenated sediment, even if
the sediment as a whole is depleted in oxygen. The oxygenated microlayer is formed as a
result of the larva transporting oxygenated water into the burrow through respiration and
feeding movements. Burrowing activities of chironomid larvae are highly important for
mineralisation processes in sediments. Chironomus crassimanus larvae, for example,
induced a threefold increase in diffusive oxygen uptake by sediment, indicating stimulation
of organic matter mineralisation in the upper sediment layers (Lagauzere et al. 2011).
Though the oxygen input from a single larva may not be quantitatively important, the fact
that the abundance of chironomid larvae often reaches several thousand individuals per
square metre can mean that they have a significant influence on oxygen concentration, and
thereby on the chemistry, of surface sediments. The downward transport of oxygen and
other terminal electron acceptors into the sediment is an additional important effect of
bioturbation by benthic animals (Andersson et al. 1988). In the absence of larger animals,
molecular oxygen only penetrates to a depth of few mm in the sediment (Revsbech et al.
1980); benthic macroinvertebrates, however, substantially increase the downward oxygen
flux (Graneli 1979). Increased availability of terminal electron acceptors leads to more
efficient sediment mineralisation, resulting in an increase in the liberation of phosphate
from particulate organic material. At the same time, redox conditions, of vital importance

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for the phosphorus binding capacity of many types of sediment, may also be affected
(Andersson et al. 1988).
Among benthic macroinvertebrates, chironomid larvae and tubificids have been the
subject of considerable interest with respect to bioturbation processes. As shown by
Lewandowski and Hupfer (2005) and Lewandowski et al. (2007), the concentrations of
phosphate, iron(II) and ammonium ions were all significantly less around ventilated
burrows (54–24 %) of C. plumosus as bioirrigation caused a convective exchange of
pore-water enriched with dissolved oxygen compared with the overlying water. These
authors also found that, compared to a macrozoobenthos-free environment, the presence of
chironomids and tubificids influenced redox zonation in sediments.
An assessment of diffusive oxygen uptake in sediments inhabited by Chironomus
riparius and T. tubifex, complemented by measurements of bioturbation activity, showed
that these two invertebrate species significantly increased the diffusive oxygen uptake of
sediments after 72 h (by 13–14 %), though no temporal variation occurred thereafter
(Lagauzere et al. 2009). Similarly, Stief and de Beer (2006) reported that the presence
of C. riparius larvae increased the availability of O2 and NO3 in sediment pore-water
and inside chironomid burrows, suggesting promotion of nitrification and dissimilatory
NO3- reduction, particularly in the burrowing layer of a chironomid larva. At the
sediment surface (i.e. the feeding layer of C. riparius), however, nitrification was
inhibited by low NH4? availability and high chironomid grazing pressure. Consequently,
the nitrification rates decreased in the feeding layer. Inside burrows, no net nitrification
was detected, despite high NH4? availability and frequent O2 injections by larval
ventilation activities. Nitrifying bacteria increased measurably in the burrowing layer
with incubation time, but only in sediments in which larvae were able to construct and
ventilate stable burrows.
In microcosm experiments, whilst tubificid worms showed no effect, chironomid larvae
increased oxygen penetration depth in sediment, compared to the control treatment, and
their emergence enhanced sediment O2 uptake (Zhang et al. 2010). The oxidation of
ferrous iron in pore-water produced ferric iron oxyhydroxides that adsorbed soluble
reactive phosphorus from the overlying water and pore-water. Chironomid larvae built
obviously oxidised tubes of around 2 mm diameter and up to 6 cm in length in the
sediment and significantly decreased ferrous iron and soluble reactive phosphorus in the
pore-water compared to the control and worm treatments. In contrast to chironomids,
tubificid worm galleries were not visually oxidised and they did not significantly alter
soluble reactive phosphorus concentrations in pore-water relative to the control. The
adsorption of ferric iron oxyhydroxides onto soluble reactive phosphorus, caused by worms
and larvae, inhibited its release from the sediment. In comparison, tubificid worms
inhibited soluble reactive phosphorus release to a greater degree than chironomid larvae,
based on the same biomass, as they successively renewed ferric iron oxyhydroxides in the
rich oxidation layer through deposition. Mitraszewski and Uchmanski (1989) also docu-
mented a greater contribution of chironomid larvae to release of phosphorus from pond
sediments into water compared to tubificids. In accordance with their conclusions, Stief
and de Beer (2002) revealed that NO3- and NH4? conversion maxima were shifted
downwards and both microbial biomass and community respiration were increased in the
chironomid ventilation layer. Observed changes in vertical layering of the benthic
microbial community were ascribed to depth-specific larval behaviour via: (1) particle
ingestion and removal of adhering microorganisms in the deposit-feeding layer, and (2)
stimulation of subsurface microorganisms due to an increased supply of O2 and NO3-
along with larval ventilation.

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A comprehensive evaluation of bioturbation impacts upon phosphorus release from

sediment is complicated. As shown in the studies mentioned above, bioturbation provides
sediments with oxygen which, whilst diminishing anaerobia, should also result in reduced
phosphorus liberation. According to observations of Topçu and Pultasü (2008), sediment
phosphorus release was twofold lower under aerobic conditions than under anaerobia.
Unlike submersed plants (e.g. Myriophyllum spicatum or Elodea canadensis), which have
the potential to oxygenate sediment via their root system, tubificid worms significantly
increase the flux of nitrogen at the sediment–water interface (influx of nitrate, efflux of
ammonium). The difference in nitrogen flux between tubificid worms and plants is prob-
ably due to the bioirrigation process caused by T. tubifex, which increases water exchange
at the sediment–water interface. Tubifex tubifex and M. spicatum produced comparable
nutrient concentration reductions in pore-water and comparable stimulation of benthic
oxygen uptake and microbial communities (percentage of active bacteria and hydrolytic
activity). Elodea canadensis, on the other hand, had a very weak influence on these
variables (Mermillod-Blondin et al. 2008). The semi-permanent tubes of Chironomus
larvae may extend to more than 10 cm in depth and, although larvae are usually found
closer to the sediment surface (Andersson et al. 1988), their undulating respiratory
movements may contribute significantly to oxygen penetration into sediments. The results
of Svensson (1997) indicate that bioturbation by tube-dwelling chironomid larvae can have
a major impact on nitrogen turnover in lake sediments, mobilising ammonium into the
water and stimulating denitrification by reducing the diffusive barrier blocking nitrate from
reaching anoxic zones in the sediment. Under aerobic conditions, the bioturbated eutrophic
sediment acts as a more pronounced sink for inorganic nitrogen compared with non-
bioturbated sediment. Oxygen consumption is increased twofold in bioturbated sediment,
some 20 % of the increase being explained through chironomid respiration. With
ammonium release and increasing nitrate concentration, denitrification of nitrates coming
from the water increased to a greater extent in bioturbated than in non-bioturbated sedi-
ment. Another important invertebrate that burrows in soft sediments is the phantom midge
fly larvae (Chaoborus flavicans), which migrates between the water column, where they
feed at night on zooplankton, and the sediment, where they find refuge from predatory fish
during the day. Their burrowing visibly disturbs surface sediments and, once buried, larvae
do not remain in the thin oxic surface layer but burrow into anoxic sediment (Gosselin and
Hare 2003), thereby acting as efficient bioturbators.

Resting stages of phyto- and zooplankton

Resting cells and eggs of many zoo- and phytoplanktonic species deposited in the sediment
are redistributed by bioturbating animals; indeed, many such species rely on recruitment
from the sediment for their continued presence in the water. Bioturbation may transport
such resting stages either deeper in the sediment or, more frequently, closer to the surface,
thereby creating conditions favourable for hatching and entering the water column
(Brönmark and Hansson 2005). On the other hand, benthic invertebrates may also have a
negative effect on the number of algal recruits by destroying them through digestion
(Stahl-Delbanco and Hansson 2002).
Although resting stages of cyanobacteria have a lower density than sand and clay
particles, they are often found deep in the sediment as a result of bioturbation caused by
macroinvertebrates. For example, Stockner and Lund (1970) observed that the depth at
which viable resting stages could be found was partially correlated with the biomass of

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burrowing invertebrates, which implies that invertebrate bioturbating activities could affect
the vertical distribution of resting stages.
Some crustaceans act very efficiently in bioturbation processes. Activities of the
water louse (Asellus aquaticus), which moves on the sediment surface, enable Anabaena
(Cyanobacteria) to hatch in high numbers and to form dense populations in the water
column. Chironomids, however, which feed on the sediment surface, have no effect on
cyanobacterial recruitment to the water column (Stahl-Delbanco and Hansson 2002,
Fig. 2). This indicates that some invertebrates may be of importance in the initiation of
algal blooms. Their results also indicate that recruitment rates of resting stages of both
phyto- and zooplankton may be more pronounced in littoral areas, which are often dom-
inated by Asellus, rather than in the profundal areas of lakes, generally dominated by
chironomids (Gyllstrom et al. 2008).
The importance of bioturbation caused by the red swamp crayfish (Procambarus clarkii)
as regards cyanobacterial bloom dynamics has been evaluated by Yamamoto (2010). This
study found that the presence of crayfish increased the density of cyanobacteria such as
Microcystis spp. and Anabaena spp. Population densities of cyanobacteria began to decline
after the crayfish were removed, indicating that the bioturbation effect had been caused by
crayfish presence. In the author’s opinion, males play an active role in the initiation of
blooms in late spring, whilst females may contribute to the extension of such blooms in late
autumn. Both males and females contributed equally to the maintenance of the bloom in
the meantime, i.e. from summer to autumn.
In addition to cyanobacteria, the resting stages of zooplankton may also be directly
affected by bioturbation from invertebrates. The effect can be either negative or positive
depending on species composition of the benthos (Marcus and Schmidt-Gengenbach 1986;
Kearns et al. 1996). The role of bioturbation in copepod (Diaptomus sanguineus) egg bank
dynamics was principally influenced by the joint activities of tubificid oligochaetes and
chironomid larvae, which were responsible for the bidirectional (up and down) transport of
resting eggs in the top 2 cm of the sediment. In the study, no movement of beads, which
were used to simulate copepod eggs, was recorded below this depth. Thus, eggs in the top 2
centimetres of sediment were regularly exposed to conditions that stimulate hatching at the
sediment–water interface. At the site of experimental surveillance, these eggs had a mean
age of 12.2 years (based on Pb-210-dating). Eggs buried more deeply will only be returned
to the sediment surface through relatively rare, localised disturbances. The return of older
eggs to the surface in this manner has been shown to affect ecological and evolutionary
dynamics in a complex way (Kearns et al. 1996).

Fig. 2 Abundance (ind l-1) and recruitment (ind m-1 d-1) of Anabaena during weekly sampling in
treatments with (from left) Asellus and Chironomus plumosus, and in control (adapted from Stahl-Delbanco
and Hansson 2002)

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In a deep and wide ranging study, Gyllstrom et al. (2008) studied the impact of benthic
bioturbating invertebrates upon the recruitment (hatching) of zooplankton from the sedi-
ment and their persistence as differences in the zooplankton community, i.e. whether
bioturbation quantitatively stimulates benthic-pelagic coupling. They investigated the
interactions of four different benthic invertebrates A. aquaticus, C. plumosus and T. tubifex
in the presence or absence of a predatory alderfly larva (Sialis lutaria). In total, 45 zoo-
plankton taxa hatched from the sediment, with hatching success of some of these being
dependent on the species of bioturbating invertebrate. The predator Sialis reduced the
abundance of all three invertebrate species, but tended to positively influence zooplankton
recruitment rates, possibly through an increase in the activity of all bioturbating inverte-
brates (including the predator). The most striking effect of bioturbation on hatching rate
and the pelagic zooplankton community was that, on average, 11% more species hatched in
the Asellus treatment than in any other treatment. This was also mirrored in the zoo-
plankton community in the water column where, on average, 7 % more species established
a viable population in treatments with Asellus as bioturbator.

Fish

Benthivorous fish are potentially important regulators of aquatic community structure

through their direct and indirect influence on water transparency, nutrient recycling,
phytoplankton, macrophytes, zooplankton and benthic macroinvertebrates (Northcote
1988). In this context, it is important to stress that the different feeding habits of bent-
hivorous fish affect the bioturbation efficiency which, in this case, is expressed particularly
as the amount of nutrients and resting stages egested. Benthivorous fish expel large
quantities of nutrients into the water column (Fig. 3), thus enhancing phytoplankton pro-
duction (Kořı́nek et al. 1987; Andersson et al. 1988; Breukelaar et al. 1994; Matsuzaki
et al. 2007). This may be especially important in aquacultural ponds (Avnimelech et al.
1999), particularly in those with older carp that receive supplementary food from the onset
of the growing season (Kloskowski 2011). The conclusions of Northcote (1988) accord
well with these considerations, i.e. the most important effects of common carp are not
found in direct predation on aquatic invertebrates but the regulation of freshwater eco-
system structure through feeding activity and nutrient recycling via physical resuspension
(i.e. bioturbation). Ozbay (2008) reported that common carp caused significant increases in
turbidity and chlorophyll a levels and decreases in macrophyte density, though no effect
was recorded regarding total phosphorus, nitrate or ammonium concentrations. For that
matter, the rise in turbidity due to bioturbation caused by increased stocks of larger ([2?)
common carp is a common measure employed by Czech carp farmers to reduce unfa-
vourable pH values via decreased photosynthetic activity of phytoplankton (Adámek et al.
2010).
As evident from the majority of studies that have dealt with benthivorous carp and
planktonic community interactions, the main contribution of sediment stirring caused by
their feeding habits is the release of nutrients, usually resulting in increased development
of the phytoplankton community. The conclusions presented by Qin and Threlkeld (1990),
however, contradict the numerous observations of an obvious role played by benthivorous
fish in nutrient release and phytoplankton development. Their results falsify the hypothesis
that benthivorous fish affect phytoplankton solely by releasing sediment-bound nutrients,
though they did show that highest seston particle abundance and turbidity occurred in
treatment combinations where carp and sediment were present. Nevertheless, their

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Fig. 3 Relation between carp density and phosphorus loading rate 7–14 days after introduction of carp in
enclosures (redrawn from Lamarra 1975 in Andersson et al. 1988)

conclusions should be treated with a degree of caution as in one of their experiments they
declared enhanced algal chlorophyll fluorescence in carp and sediment combination, this
despite the authors’ claim in the discussion that ‘‘algal fluorescence …. did not respond to
sediment x fish interactions in either experiment.’’ Based on these conclusions, they pro-
nounced that the stimulatory effect of carp on algal biomass is not apparently related to
resuspension of nutrient-laden sediments and encourage the importance of more detailed
studies and re-evaluation of this process in natural lakes.
The importance of bioturbation is obvious particularly with respect to the fate of
nutrients introduced into ponds, which usually function very efficiently in trapping and
storage of nutrients. Bioturbation of bottom sediments by carp may damage macrophytes
(Sidorkewicj et al. 1999; Parkos et al. 2003; Miller and Crowl 2006). Resuspension of
sediments and algae reduces light penetration under water and hence its availability for
submersed vegetation (Hellström 1991). These effects may be stronger in the presence of
larger carp, which are capable of penetrating deeper into the substratum than smaller fish
(Panek 1987), and more intense in summer when carp take mainly benthic prey. Adult carp
(C. carpio) forage predominantly on benthic macroinvertebrates and, when doing so, they
induce severe bioturbation of the pond bottom (Costa-Pierce and Pullin 1989). Weber and
Brown (2009) have shown that the effects of carp on pond environmental conditions are
both size and density dependent.

Material and nutrient flux

Chakrabarty and Das (2007) determined bioturbation-induced phosphorous release, based on

soluble reactive phosphate, from an (insoluble) apatite source. Introduction of carp fry
resulted in a net increase of 0.09–0.10 mg l-1 of soluble reactive phosphate and a 64.8–90 %
influx of phosphate from bottom soil in the presence of phosphate rock but only about
6.3–7.2 % in its absence. Figures reported in a similar study of carp influence on increasing
values of phosphate rock (Jana et al. 1992) indicated values of 72–100 % influx of phosphate
from the bottom soil in the presence of phosphate rock but only 7–8 % in its absence.

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In a series of mesocosm experiments, Cline et al. (1994) proved that sediment resus-
pension by common carp increased nitrite and nitrate concentrations in the overlying
water, whilst Matsuzaki et al. (2007) demonstrated that carp can have dramatic direct and
indirect impacts on nutrient dynamics and littoral community structure through excretion
and bioturbation.

Oxygen transport and nutrient release

Different feeding habits of benthivorous fish affect the amount of sediment stirred, ingested
and, consequently, the amount of nutrients egested. Joyni et al. (2011) identified two types
of bottom soil bioturbation in experimental brackish water ponds: (1) site-specific digging
and soil displacement as performed by, for example, tilapia (Oreochromis mossambicus),
and (2) continuous stirring and resuspension, as in the case of the pearlspot (Etroplus
suratensis). Stirring of sediments by benthivorous fishes has two considerable effects on
pond hydrochemistry comparable with the impact of bioturbation caused by benthic
macroinvertebrates: (1) it increases diffusion rates across the sediment–water interface, and
(2) it increases aerobic decomposition by aerating anaerobic sediments (Graneli 1979;
Kadir et al. 2006; Phan-Van et al. 2008). It is generally accepted that bioturbation activity
by fish has the potential to improve bottom soil quality in aquacultural pond bottoms by
increasing oxygen supply to greater depths (Ritvo et al. 2004).
The suggestion that effects from bioturbation caused by the fish community are more
important than those caused by macroinvertebrates appears to be reasonable, as shown by
Svensson et al. (1999) who found that increased macroinvertebrate abundance due to fish
removal, and its effects on recirculation of nutrients over the sediment–water interface,
resulted in increased nitrogen retention in a lake. Average total N retention values before
and after reduction in fish biomass were 59 ± 5 and 82 ± 15 %, respectively. In addition,
Jepessen et al. (1998) noticed a substantial increase in N retention in sediment, and its
subsequent loss by denitrification, following a decline in cyprinid density.
The bottom feeding activities of carp are positively related to concentrations of total
phosphorus and suspended solids (primarily inorganic particles) in water and turbidity
(Roberts et al. 1995). They showed that a higher biomass of carp (476 kg ha-1) had a
greater effect on nutrients, turbidity and suspended solids than a low biomass
(174 kg ha-1). Besides the release of sediment-bound nutrients due to bioturbation, carp
could also have increased nutrient concentration through excretion and the destruction, and
subsequent decay, of aquatic macrophytes (Parkos et al. 2003). When evaluating the role of
fish in phosphorus availability to phytoplankton, Brabrand et al. (1990) concluded that the
phosphorus supply originating from bioturbation by fish was about double that of external
phosphorus loading, confirming the important role of sediment-feeding fish populations in
the eutrophication processes of lakes. In addition, concentrations of total dissolved sul-
phide, soluble manganese, easily oxidised matter and exchangeable NH4–N were lower
along the bottom soil profile in carp presence than in enclosures without fish (Ritvo et al.
2004). Moreover, carp stirred the sediment to such a degree that the bulk density of surface
soil in enclosures containing carp was significantly greater than that in the control,
meaning that carp presence led to an increase in bottom soil density and therefore an
increase in compaction of the soil. Bottom soil bulk density increased with increasing carp
abundance (from 0 to 7 fish per enclosure) and this phenomenon was more pronounced in
the uppermost 0–1 cm layer. In deeper layers (up to 3–5 cm layer), the differences between
zero and maximum (7 individuals) fish abundance were insignificant (P [ 0.05) but still
obvious. In the authors’ opinion, pond soil perturbation by common carp increased oxygen

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transfer to the soil, decreased the concentration of toxic reduced compounds and enabled
more efficient food web recycling and nutrient release. Degradation of the sedimenting
organic matter was accelerated by carp bioturbation, especially in the upper layer.
In an exclosure experiment at a pond with Nile tilapia (Oreochromis niloticus) domi-
nated polyculture, Riise and Roos (1997) demonstrated that oxygen uptake by sediment
corresponded to 8% of the oxygen respired by the planktonic community and ammonia
release averaged 13.2 ± 4.8 mmol NH4? m-2 day-1. The burial of particulate organic
carbon and particulate organic nitrogen averaged 25 and 60 % of the gross input,
respectively. Oligochaete numbers and biomass, as well as benthic metabolic rates, were
significantly higher when fish were excluded from sediment bioturbation. Inside the ex-
closure, the respiration quotient was approximately double that outside, indicating that the
exclusion of fish from sediment bioturbation increased the sediment flux of metabolites and
anaerobic respiration, including the denitrification process. The presence of benthivorous
fish reduced atmospheric nitrogen loss caused by denitrification by 50 %. Whereas Nile
tilapia is not typically a benthivorous fish, Phan-Van et al. (2008) have shown that they are
able to provide considerable bioturbation in waste water stabilisation ponds. Dissolved
oxygen saturation in a pond stocked with tilapia was significantly (P \ 0.05) higher than
that of a pond without fish. Nile tilapia’s bioturbation activity may also improve the
vertical distribution of temperature and dissolved oxygen in the water column, especially
in the lower layers of stabilisation ponds, which would lead to better treatment efficiency
of pollutants.
Sediment resuspension is a major process in carp and tilapia ponds, suggesting that
exchange of nutrients between the sediment and overlying water is intensive (Avnimelech
et al. 1999). The effect of resuspension on nutrient transfer from sediment to the water
column, however, may be more critical in lakes in which primary productivity is nutrient
limited than in fertilised or fed fish ponds. Resuspension of organic particles into the water
may accelerate organic matter mineralisation and nutrient regeneration and, therefore, it is
considered an important factor controlling oxygen and nutrient dynamics and the microbial
ecology of shallow aquacultural ponds. The resuspension of such organic particles from the
pond bottom into the water column can reduce sediment oxygen demand by displacing
decomposition from the sediment to the water column. On the other hand, the rising of
organic sediments into the water column supports their rapid and more efficient decom-
position resulting in nutrient release.
Stirring of pond bottoms by pool barb (punti, Puntius sophore) and common carp has
been shown to increase nutrient flow from sediments into the water column and to promote
nitrification, though only in the absence of silver carp (Hypohthalmichthys molitrix), which
decreases algal biomass through grazing and promotes nitrification through resuspension of
particles into the water column (Kadir et al. 2006). Modified total ammonium nitrogen
(TAN) concentrations are further important indicator of redox conditions in pond bottom
sediments influenced by fish bioturbation, as demonstrated by Joyni et al. (2011). In their
study, they found that a fish-free control treatment showed highest TAN concentrations. In
the bottom soil profile, the lowest TAN concentrations were recorded in the upper
(0–1 cm) sediment layer and increased downwards in the treatments with tilapia (Tilapia
sp.), mullet (Mugil cephalus), milkfish (Chanos chanos) and pearlspot (Etroplus surat-
ensis) (Fig. 4). As a result of fish feeding activities, therefore, there is a net release of
ammonium from bioturbated sediment into the overlying water.
According to data presented by Breukelaar et al. (1994), the effect of common bream
(Abramis brama) on sediment resuspension through bioturbation was, surprisingly, twice
that of carp. They found that bioturbation by benthivorous fish (bream and carp) resulted in

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Aquacult Int (2013) 21:1–17 13

Fig. 4 Concentrations of total ammonium nitrogen in different bottom soil layers, 105 days after stocking
(redrawn from Joyni et al. 2011)

suspended sediment concentrations that increased linearly with fish biomass. Bream caused
an increase of 46 g sediment m-2 day-1 per 100 kg bream ha-1 and a reduction of
0.38 m-1 in reciprocal Secchi disc depth. Assuming a linear relationship, chlorophyll
a level increased by 9.0 lg l-1, total P by 0.03 mg l-1 and Kjeldahl-N by 0.48 mg l-1 per
100 kg bream ha-1. These determinants, plus those for silicate, were all positively cor-
related with fish biomass, though those for orthophosphate showed no correlation. Results
have also indicated that large benthivorous fish are not the only source of increased nutrient
concentrations in the water column (Tarvainen et al. 2005). These authors showed that the
effects of smaller benthivores, such as ruffe (Gymnocephalus cernuus), must also be taken
into consideration when estimating internal nutrient loading.

Resting stages of phyto- and zooplankton

Carp bioturbation has an important impact on the persistence of aquatic communities as

elevated sediment concentrations can smother invertebrate eggs, suffocate fish embryos
and potentially reduce the respiratory capabilities of amphibian larvae by fouling their gills
(Gleason et al. 2003). The importance of fish in bioturbation processes is also supported by
observations showing an increase in the numbers of Microcystis colonies recruited and the
significantly different recruitment rates in shallow and deeper parts of a lake. Calculated
over the entire summer, Microcystis colonies corresponding to 50 % of the initial abun-
dance in surface sediments were recruited in a shallow bay, whereas recruitment from the
deep area was only 8 % (Brunberg and Blomqvist 2003). In the opinion of Verspagen et al.
(2004), the recruitment of Microcystis is more likely a passive process resulting from
resuspension by wind-induced mixing or bioturbation. Consequently, shallow areas of a
lake probably play a more important role in recruitment of benthic Microcystis than deep
areas.
These results indicate that shallow regions, which have been largely overlooked in
studies of phytoplankton recruitment, may be crucial to Microcystis dynamics in that they
play an important role as inoculation sites for pelagic populations (Brunberg and
Blomqvist 2003). The same is also true for Anabaena and Aphanizomenon colonies and

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some other phytoplankton species (Karlsson-Elfgren and Brunberg 2004; Rengefors et al.
2004). Thus, the feeding habits of benthivorous fish, which search for food predominantly
in the shallow littoral zone during the summer period (Persson and Nilsson 2007), can
certainly be considered as one of the important factors contributing to recruitment of
cyanobacterial colonies.
As obvious from a review of data from available literature and the current interest and
support for environmentally friendly aquaculture, knowledge of the role of aquatic
invertebrates and fish in bioturbation processes is of increasing importance. Maximum
feasible involvement of natural processes into the pond management is highly appreciated
as it represents the measures targeted on thorough utilisation of natural food resources and
supplementary feeds and also the way how to improve the quality of the final product (fish
flesh), i.e. its composition, taste, off-flavour absence, etc. In particular, there is increasing
interest in studies that focus on the fate of cyanobacteria resting stages under bioturbation
impacts. Such studies are of especial importance as regards the current interest and support
for environmentally friendly fish pond management. Pond management that recognises and
makes maximum use of natural processes and food resources will not only reduce impacts
on the environment, including cyanobacterial blooms, but will also improve the quality and
taste of the final product, i.e. fish.

Acknowledgments The study was supported by the South Bohemian Research Centre of Aquaculture and
Biodiversity of Hydrocenoses CENAKVA CZ.1.05/2.1.00/01.0024 and projects GA JU 047/2010/7,
AVOZ60050516 and FR-TI3/196.

References

Adámek Z, Helešic J, Maršálek B, Rulı́k M (2010) Aplikovaná hydrobiologie (Applied Hydrobiology).

FFPW USB Vodňany
Aller RC (1978) Experimental studies of changes produced by deposit feeders on pore water, sediment, and
overlying water chemistry. Am J Sci 278:1185–1234
Andersson G, Graneli W, Stenson J (1988) The influence of animals on phosphorus cycling in lake eco-
systems. Hydrobiologia 170:267–284
Avnimelech Y, Kochva M, Hargreaves JA (1999) Sedimentation and resuspension in earthen fish ponds.
J World Aquac Soc 30:401–409
Biswas JK, Rana S, Bhakta JN, Jana BB (2009) Bioturbation potential of chironomid larvae for the sedi-
ment-water exchange in simulated pond systems of varied nutrient enrichment. Ecol Eng
35:1444–1453
Boyd CE (1995) Bottom soils, sediments and pond aquaculture. Chapman and Hall, New York
Brabrand A, Faafeng BA, Nilssen JPM (1990) Relative importance of phosphorus supply to phytoplankton
production: fish excretion versus external loading. Can J Fish Aquat Sci 47:364–372
Breukelaar AW, Lammens EHRR, Breteler JGPK, Tatrai I (1994) Effect of benthivorous bream (Abramis
brama) and carp (Cyprinus carpio) on sediment resuspension and concentrations of nutrients and
chlorophyll a. Freshw Biol 32:113–121
Brönmark C, Hansson L-A (2005) The biology of lakes and ponds. Oxford University Press, Oxford
Brunberg A, Blomqvist P (2003) Recruitment of Microcystis (Cyanophyceae) from lake sediments: the
importance of littoral inocula. J Phycol 39:58–63
Chakrabarty D, Das SK (2007) Bioturbation-induced phosphorous release from an insoluble phosphate
source. Biosystems 90:309–313
Cline JMT, East TL, Threlkeld ST (1994) Fish interactions with the sediment-water interface. Hydrobio-
logia 275(276):301–311
Costa-Pierce BA, Pullin RSV (1989) Stirring ponds as a possible means of increasing aquaculture pro-
duction. Aquabyte 2:5–7
Croel RC, Kneitel JM (2011) Ecosystem-level effects of bioturbation by tadpole shrimp Lepidurus packardi
in temporary pond mesocosms. Hydrobiologia 665:169–181

123
Aquacult Int (2013) 21:1–17 15

Dafoe LT, Rygh AL, Yang B, Gingras MK, Pemberton SG (2011) A new technique for assessing tubificid
burrowing activities, and recognition of biogenic grading formed by these oligochaetes. Palaios
26:66–80
De Haas EM, Kraak MHS, Koelmans AA, Admiraal W (2005) The impact of sediment reworking by
opportunistic chironomids on specialised mayflies. Freshw Biol 50:770–780
Fukuhara H, Sakamoto M (1987) Enhancement of inorganic nitrogen and phosphate release from lake
sediment by tubificids worms and chironomid larvae. Oikos 48:312–320
Gallepp GW (1979) Chironomid influence on phosphorus release in sediment-water microcosms. Ecology
60:547–556
Gleason RA, Euliss NH Jr, Hubbard DE, Duffy WG (2003) Effects of sediment load on emergence of
aquatic invertebrates and plants from wetland soil egg and seed banks. Wetlands 23:26–34
Gosselin A, Hare I (2003) Burrowing behavior of Chaoborus flavicans larvae and its ecological significance.
J N Am Benthol Soc 22:575–581
Graf G, Rosenberg R (1997) Bioresuspension and biodeposition: a review. J Mar Syst 11:269–278
Graneli W (1979) The influence of Chironomus plumosus larvae on the oxygen uptake of sediment. Arch
Hydrobiol 87:385–407
Gyllstrom M, Lakowitz T, Bronmark C, Hansson LA (2008) Bioturbation as driver of zooplankton
recruitment, biodiversity and community composition in aquatic ecosystems. Ecosystems
11:1120–1132
Håkansson L, Jansson M (1983) Principles of lake sedimentology. Springer, Berlin
Hansen KS, Mouridsen S, Kristensen E (1998) The impact of Chironomus plumosus larvae on organic
matter decay and nutrient (N, P) exchange in a shallow eutrophic lake sediment following a phyto-
plankton sedimentation. Hydrobiologia 364:65–74
Hellström T (1991) The effect of resuspension on algal production in a shallow lake. Hydrobiologia
213:183–190
Henry R, Santos CM (2008) The importance of excretion by Chironomus larvae on the internal loads of
nitrogen and phosphorus in a small eutrophic urban reservoir. Braz J Biol 68:349–357
Holdren GC, Armstrong DE (1980) Factors affecting phosphorus release from intact lake sediment cores.
Environ Sci Technol 14:79–87
Hrbáček J, Procházková L (1975) Release of nitrogenous substances from bottom sediments under labo-
ratory conditions. Verh Intern Ver Limnol 19:1899–1906
Jana BB, Das SK (1992) Bioturbation induced changes of fertilizer value of phosphate rock in relation to
alkaline phosphatase activity. Aquaculture 103:321–330
Jana BB, Sahu SN (1993) Relative performance of three bottom grazing fishes (Cyprinus carpio, Cirrhinus
mrigala, Heteropneustes fossilis) in increasing the fertilizer value of phosphate rock. Aquaculture
115:19–29
Jana BB, Das SK, Chakrabarty D (1992) Use of common carp (Cyprinus carpio L.) in increasing the
fertilizer value of phosphate rock. J Appl Ichthyol 8:222–227
Jepessen E, Jensen JP, Sondergaard M, Lauridsen T, Moller FP, Sandby K (1998) Changes in nitrogen
retention in shallow eutrophic lakes following a decline in density of cyprinids. Arch Hydrobiol
142:129–151
Jiang PH, Ji L, Xiao WJ, Huang DZ, Liu YB, Song CL, Cao XY, Zhou YY (2010) Bioturbation of two
chironomid species on nutrient release at sediment-water interface in a Chinese shallow eutrophic lake.
Fresenius Environ Bull 19:902–910
Jonasson PM (1972) Ecology and production of the profundal benthos in relation to phytoplankton in Lake
Esrom. Oikos Suppl 14:1–148
Joyni MJ, Kurup BM, Avnimelech Y (2011) Bioturbation as a possible means for increasing production and
improving pond soil characteristics in shrimp-fish brackish water ponds. Aquaculture 318:464–470
Kadir A, Kundu RS, Milstein A, Wahab MA (2006) Effects of silver carp and small indigenous species on
pond ecology and carp polycultures in Bangladesh. Aquaculture 261:1065–1076
Karlsson-Elfgren I, Brunberg AK (2004) The importance of shallow sediments in the recruitment of Ana-
baena and Aphanizomenon (Cyanophyceae). J Phycol 40:831–836
Kearns CM, Hairston GJ, Kesler DH (1996) Particle transport by benthic invertebrates: Its role in egg bank
dynamics. Hydrobiologia 332:63–70
Keen WH, Gagliardi J (1981) Effect of brown bullheads on release of phosphorus in sediment and water
systems. Progr Fish Cult 43:183–185
Kloskowski J (2011) Differential effects of age-structured common carp (Cyprinus carpio) stocks on pond
invertebrate communities: implications for recreational and wildlife use of farm ponds. Aquacult Int
19:1151–1164

123
16 Aquacult Int (2013) 21:1–17

Kořı́nek V, Fott J, Fuksa J, Lellák J, Pražáková M (1987) Carp ponds of central Europe. In: Michael RG (ed)
Managed aquatic ecosystems. Elsevier Science Publishers, Amsterdam, pp 29–62
Krantzberg G (1985) The influence of bioturbation on physical, chemical and biological parameters in
aquatic environments: a review. Environ Pollut Ser A 39:99–122
Lagauzere S, Pischedda L, Cuny P, Gilbert F, Stora G, Bonzom J-M (2009) Influence of Chironomus
riparius (Diptera, Chironomidae) and Tubifex tubifex (Annelida, Oligochaeta) on oxygen uptake by
sediments. Consequences for uranium contamination. Environ Pollut 157:1234–1242
Lagauzere S, Moreira S, Koschorreck M (2011) Influence of bioturbation on the biochemistry of littoral
sediments of an acidic post-mining pit lake. Biogeosciences 8:339–352
Lamarra VA (1975) Digestive activities of carp as a major contributor to the nutrient loading of lakes. Verh
Intern Ver Limnol 19:2461–2468
Lewandowski J, Hupfer M (2005) Effect of macrozoobenthos on two-dimensional small-scale heterogeneity
of pore water phosphorus concentrations in lake sediments: a laboratory study. Limnol Oceanogr
50:1106–1118
Lewandowski J, Laskov C, Hupfer M (2007) The relationship between Chironomus plumosus burrows and
the spatial distribution of pore-water phosphate, iron and ammonium in lake sediments. Freshw Biol
52:331–343
Marcus NH, Schmidt-Gengenbach J (1986) Recruitment of individuals into the plankton: The importance of
bioturbation. Limnol Oceanogr 31:206–210
Matisoff G, Fisher JB, Matis S (1985) Effects of benthic macroinvertebrates on the exchange of solutes
between sediments and freshwater. Hydrobiologia 122:19–33
Matsuzaki SS, Usio N, Takamura N, Washitani I (2007) Effects of common carp on nutrient dynamics and
littoral community composition: roles of excretion and bioturbation. Fundam Appl Limnol 168:27–38
Meijer LE, Avnimelech Y (1999) On the use of micro-electrodes in fish pond sediments. Aquacult Eng
21:71–83
Mermillod-Blondin F, des Chatelliers MC, Gerino M, Gaudet JP (2000) Testing the effect of Limnodrilus sp.
(Oligochaeta, Tubificidae) on organic matter and nutrient processing in the hyporheic zone: a
microcosm method. Arch Hydrobiol 149:467–487
Mermillod-Blondin F, Lemoine D, Boisson JC, Malet E, Montuelle B (2008) Relative influences of sub-
mersed macrophytes and bioturbating fauna on biogeochemical processes and microbial activities in
freshwater sediments. Freshw Biol 53:1969–1982
Meysman FJR, Galaktionov OS, Gribsholt B, Middelburg J (2006) Bioirrigation in permeable sediments:
advective pore-water transport induced by burrow ventilation. Limnol Oceanogr 51:142–156
Miller SA, Crowl TA (2006) Effects of common carp (Cyprinus carpio) on macrophytes and invertebrate
communities in a shallow lake. Freshw Biol 51:85–94
Misson B, Sabart M, Amblard C, Latour D (2011) Involvement of microcystins and colony size in benthic
recruitment of the cyanobacterium Microcystis (Cyanophyceae). J Phycol 47:42–51
Mitraszewski P, Uchmanski J (1989) A numerical model of phosphorus exchange between the sediments
and the near bottom water in a lake. Ekologia Polska 36:317–346
Mulsow S, Boudreau BP, Smith JA (1998) Bioturbation and porosity gradients. Limnol Oceanogr 43:1–8
Northcote TG (1988) Fish in the structure and function of freshwater ecosystems: a top-down view. Can J
Fish Aquat Sci 45:361–379
Ozbay H (2008) An enclosure experiment to test the effects of common carp on the water quality in a
shallow Turkish soda lake. Fresenius Environ Bull 17:2078–2082
Panek FM (1987) Biology and ecology of carp. In: Cooper EL (ed) Carp in North America. American
Fisheries Society, Bethesda, pp 1–15
Parkos JJIII, Santucci VJ Jr, Wahl DH (2003) Effects of adult common carp (Cyprinus carpio) on multiple
trophic levels in shallow mesocosms. Can J Fish Aquat Sci 60:182–192
Persson A, Nilsson E (2007) Foraging behavior of benthic fish as an indicator of ecosystem state in shallow
lakes. Israel J Ecol Evol 53:407–421
Persson A, Svensson JM (2006) Effects of benthivorous fish on biogeochemical processes in lake sediments.
Freshw Biol 51:1298–1309
Petr T (1977) Bioturbation and exchange of chemicals in the mud-water interface. In: Golterman HL (ed)
Interactions between sediments and freshwater. Dr.W.J.Junk, The Hague, pp 216–226
Phan-Van M, Rousseau DPL, De Pauw N (2008) Effects of fish bioturbation on the vertical distribution of
water temperature and dissolved oxygen in a fish culture-integrated waste stabilization pond system in
Vietnam. Aquaculture 281:28–33
Qin JG, Threlkeld ST (1990) Experimental comparison of the effects of benthivorous fish and planktivorous
fish on plankton community structure. Arch Hydrobiol 119:121–141

123
Aquacult Int (2013) 21:1–17 17

Rengefors K, Gustafsson S, Stahl-Delbanco A (2004) Factors regulating the recruitment of cyanobacterial

and eukaryotic phytoplankton from littoral and profundal sediments. Aquat Microb Ecol 36:213–226
Revsbech NP, Sörensen J, Blackburn TH, Lomholt JP (1980) Distribution of oxygen in marine sediments
measured with microelectrodes. Limnol Oceanogr 25:403–411
Riise JC, Roos N (1997) Benthic metabolism and the effects of bioturbation in a fertilized polyculture fish
pond in northeast Thailand. Aquaculture 150:45–62
Risnoveanu G, Postolache C, Vadineanu A (2002) The role of tubificid communities in phosphorous budget
in shallow eutrophic lakes of the Danube Delta. Int Assoc Danub Res 34:689–696
Risnoveanu G, Postolache C, Vadineanu A (2004) Ecological significance of nitrogen cycling by tubificid
communities in shallow eutrophic lakes of the Danube delta. Hydrobiologia 524:193–202
Ritvo G, Kochba M, Avnimelech Y (2004) The effects of common carp bioturbation on fishpond bottom
soil. Aquaculture 242:345–356
Roberts J, Chick A, Oswald L, Thompson R (1995) Effect of carp, Cyprinus carpio, an exotic benthivorous
fish, on aquatic plants and water quality in experimental ponds. Mar Freshw Res 46:1171–1180
Scheffer M (1998) Ecology of shallow lakes. Kluwer Academic Publishers, Dordrecht, Boston, London
Sidorkewicj NS, Lopez Cazorla AC, Fernandez OA, Möckel GC, Burgos MA (1999) Effects of Cyprinus
carpio on Potamogeton pectinatus in experimental culture: the incidence of the periphyton. Hydro-
biologia 415:13–19
Stahl-Delbanco A, Hansson L-A (2002) Effects of bioturbation on recruitment of algal cells from the ‘‘seed
bank’’ of lake sediments. Limnol Oceanogr 47(6):1836–1843
Starkel WM (1985) Predicting the effect of macrobenthos on the sediment/water flux of metals and phos-
phorus. Can J Fish Aquat Sci 42:95–100
Stief P, de Beer D (2002) Bioturbation effects of Chironomus riparius on the benthic N-cycle as measured
using microsensors and microbiological assays. Aquat Microb Ecol 27:175–185
Stief P, de Beer D (2006) Probing the environment of freshwater sediment macrofauna implications of
deposit-feeding and bioirrigation for nitrogen cycling. Limnol Oceanogr 51:2538–2546
Stockner JG, Lund JWG (1970) Live algae in postglacial lake deposits. Limnol Oceanogr 15:41–58
Svensson JM (1997) Influence of Chironomus plumosus larvae on ammonium flux and denitrification
(measured by the acetylene blockage- and the isotope pairing-technique) in eutrophic lake sediment.
Hydrobiologia 346:157–168
Svensson JM (1998) Emission of NO2, nitrification and denitrification in a eutrophic lake sediment bio-
turbed by Chironomus plumosus. Aquat Microb Ecol 14:289–299
Svensson JM, Bergman E, Andersson G (1999) Impact of cyprinid reduction on the benthic macroinver-
tebrate community and implications for increased nitrogen retention. Hydrobiologia 404:99–112
Tarvainen M, Ventela AM, Helminen H, Sarvala J (2005) Nutrient release and resuspension generated by
ruffe (Gymnocephalus cernuus) and chironomids. Freshw Biol 50:447–458
Topçu A, Pultasü S (2008) The effect of dissolved oxygen on sediment-water phosphorus exchange in
Mogan Lake. In: Proceedings of the EIFAC symposium on interactions between social, economic and
ecological objectives of inland commercial and recreational fisheries and aquaculture, EIFAC Occa-
sional Paper No.44: 87–92
Verspagen JMH, Snelder EOFM, Visser PM, Huisman J, Mur LR (2004) Recruitment of benthic Micro-
cystis (Cyanophyceae) to the water column: internal buoyancy changes or resuspension? J Phycol
40:260–270
Weber MJ, Brown ML (2009) Effects of common carp on aquatic ecosystems 80 years after ‘‘Carp as a
dominant’’: ecological insights for fisheries management. Rev Fish Sci 17:524–537
Wisniewski RJ, Planter M (1985) Exchange of phosphorus across sediment-water interface (with special
attention to the influence of biotic factors) in several lakes of different trophic status. Verh Intern Ver
Limnol 22:3345–3349
Woodruff SL, House MEC, Leadbeater SC (1999) The effects of biofilms on chemical processes in surficial
sediments. Freshw Biol 41:73–89
Yamamoto Y (2010) Contribution of bioturbation by the red swamp crayfish Procambarus clarkii to the
recruitment of bloom forming cyanobacteria from sediment. J Limnol 69:102–111
Zhang L, Gu XZ, Fan CX, Shang JG, Shen QS, Wang ZD, Shen J (2010) Impact of different benthic animals
on phosphorus dynamics across the sediment-water interface. J Environ Sci–China 22:1674–1682

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