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First published online March 2, 2007
Journal of Experimental Biology 210, 1006-1014 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.000570
Oxygen dynamics around buried lesser sandeels Ammodytes tobianus (Linnaeus 1785): mode of ventilation and oxygen requirements
Marine Biological Laboratory, University of Copenhagen, Strandpromenaden 5, DK-3000 Helsingør, Denmark
* Author for correspondence (e-mail: rnglud{at}bi.ku.dk)
Accepted 23 January 2007
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Summary |
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30 min the oxic plume was replenished by
oxygen-depleted water from the gills. The potential for cutaneous respiration
by the buried fish was thus of no quantitative importance. Calculations
derived by three independent methods (each with N=3) revealed that
the oxygen uptake of sandeel buried for 6–7 h was 40–50% of
previous estimates on resting respirometry of non-buried fish, indicating
lower O2 requirements during burial on a diurnal timescale. Buried
fish exposed to decreasing oxygen tensions gradually approached the sediment
surface, but remained in the sediment until the inspired water reached
5–10% air saturation.
Key words: sandeel, Ammodytes tobianus, oxygen imaging, sediment, oxygen uptake, ventilation, hypoxia
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Winslade, 1974b;
Winslade, 1974c;
Freeman et al., 2004).
Sandeels prefer sandy sediments to those with more gravel, silt or mud, as
evident from both laboratory choice experiments and field observations
(Meyer et al., 1979;
Pinto et al., 1984;
Wright et al., 2000;
Holland et al., 2005). This
might be due to high energy requirements for burying in gravel and the oxygen
depleted environment of silt and mud (Glud
et al., 2003). Sandy sediments preclude the option of having a
permanent opening to the overlying water and the hypothesis that sandeels
obtain oxygen from the porewater was based on early presumptions that sandy
interstices contain plenty of oxygen
(Pinto et al., 1984;
Quinn and Schneider, 1991;
Holland et al., 2005). Studies
have indeed documented that advective porewater transport facilitates solute
transport through sand and that oxygen occasionally can extend several cm into
permeable sandy sediment (Huettel and
Webster, 2001; de Beer et al.,
2005; Cook et al.,
2007). However, this is not generally the case, and changes in
wave actions, flow characteristics and bottom topography affect oxygen
penetration and such sediments are characterized by a dynamic mosaic of oxic
and anoxic compartments (Ziebis et al.,
1996; de Beer et al.,
2005). During calm periods oxygen penetration in sand will be
constrained to only a few mm (de Beer et
al., 2005; Cook et al.,
2007).
With sediment characteristics like those described above it is questionable
whether buried sandeels can rely on porewater to provide sufficient oxygen to
sustain their requirements, not least considering that average winter
densities are 60 m–2, with up to 200 m–2, in
the central North Sea (Høines and
Bergstad, 2001). Despite the enormous abundance of sandeels in
near-shore waters and their importance for commercial fisheries
(Gislason and Kirkegaard,
1998), only sparse information is available on the behaviour and
physiology related to their peculiar lifestyle. This is presumably because
technical difficulties have limited our insight into oxygen dynamics around
living and mobile creatures buried in the sediment. The introduction of planar
oxygen optodes to aquatic biology has now made it possible to obtain
fine-scale, two-dimensional oxygen distributions in benthic communities and
around buried structures and animals (Glud
et al., 1996; Wenzhöfer
and Glud, 2004; Precht et al.,
2004; Franke et al.,
2006; Frederiksen and Glud,
2006).
The standard metabolic rate (SMR), which is the minimum oxygen requirements
for maintenance of a resting, post-absorptive fish, and the
Scrit (the `critical oxygen saturation', below which the
basal O2 requirements can no longer be met) are key parameters
affecting the ability of fish to cope with oxygen limitation. A recent study
employing conventional respirometry showed that despite their small size, the
lesser sandeel Ammodytes tobianus has a SMR of 72 mg
O2 kg–1 h–1 at 10°C for fish
weighing 3 g. However, their tolerance to hypoxia appears to be no better than
that of many other fish with a Scrit of 20% at
10°C and a salinity of 30
(Behrens and Steffensen, 2006).
It has been speculated that their burrowing behaviour lowers predation
pressure, but also represents a strategy for conservation of energy
(Reay, 1973;
Quinn and Schneider, 1991;
Wright et al., 2000). The idea
of reduced oxygen requirements during burial lacks experimental evidence,
however, but has been based on the observation that fish do survive on limited
fat deposits for extended periods of dormancy during winter
(Robards et al., 1999).
Through the use of planar oxygen optodes, the present study investigated the mechanism by which sandeels buried in sandy sediment obtain oxygen and estimate their oxygen requirements on a diurnal basis. Furthermore, behavioural responses to declining water oxygen levels, e.g. emergence from or relocation in the sediment, were investigated.
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Materials and methods |
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salinity in recirculating, fully oxygenated
seawater. The light regime followed a 12 h:12 h light:dark cycle. The bottom
of the tank was covered by a 20 cm layer of medium fine sand, allowing
the fish to maintain their burying behaviour. The fish were fed with frozen
Artemia or live Mysis shrimps and allowed to acclimate to
the laboratory conditions for approximately 2 months before the experiments
were initiated. Fish were starved for approximately 48 h before the
experiments began to exclude any increased oxygen consumption associated with
digestion and defecation. Prior to the experiments fish were transferred to
glass chambers (height 21 cm, width 14 cm, depth 3 cm) equipped with a planar
O2 optode along one of the sides and filled with sediment from the
sampling site. The water column, of fresh seawater, was maintained at a height
of 9–14 cm (Fig. 1). The
chambers were kept in a 12 h:12 h light:dark cycle and the fish typically
buried in the sand 10–20 min after the transfer
(Fig. 1). The chambers were
then placed in a flow-though aquarium filled with 40 l of seawater at constant
temperature and salinity (10±0.2°C and 30, respectively),
and the fish were left to acclimatize before any measurements were performed
(Fig. 2). Details of the
acclimation procedures for each experiment are described below.
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Planar optodes
The measuring principle of planar oxygen optodes has previously been
described in detail (Glud et al.,
1996; Holst et al.,
1998) and is therefore only briefly presented below. The planar
optode sensor consisted of an oxygen quenchable fluorophore,
Ruthenium(II)-tris-4,7-diphenyl-1,10-phenatholine perchlorate, that was
immobilized in plasticized PVC on a transparent oxygen-impermeable polyester
support foil (total thickness 175 µm). The luminophore was excited by
blue LEDs (Luxeon, Calgary, Alberta, Canada), equipped with short-pass
excitation filters (C-54, Linos, Garches, France). The emitted,
oxygen-sensitive, red luminescent light-signals were imaged with a 12-bit
digital CCD camera (PCO Computer Optics, Kelheim, Germany). The camera was
equipped with a 17 mm/f1.4 lens covered by a long-pass emission filter (OG
570, Schott, Warwick, UK) to remove any reflected blue light from the
excitation source (Fig. 2). The
Peletier cooled camera chip consisted of 1280x1024 pixels which, at the
given optical configuration (pixel binning of 2), gave a pixel resolution of
150 µm pixel–1. To quantify the oxygen distribution
in front of the planar optode we applied a lifetime-based sensing scheme
(Holst et al., 1998). The
luminescent light was measured after the eclipse of the excitation light in
two well-defined time windows (4 µs), separated by a short interval (0.2
µs). Window one was opened 0.2 µs after the first excitation cycle and
window two was opened 4.2 µs after the second excitation cycle. The
luminescent lifetime was calculated from these images assuming a
mono-exponential decay curve. The lifetime images were calibrated into oxygen
images by a two-point calibration procedure using a modified
Stern–Volmer equation:
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and 0 represent the luminescent lifetime at a
given oxygen concentration (C) and at anoxia, respectively.
Ksv is a constant expressing the quenching efficiency of
the immobilized luminophore and a represents the non-quenchable fraction of
the luminescence, which was set to the empirically derived image constant of
0.2.
The lifetime approach made it possible to use transparent optodes
(Holst and Grünwald,
2001), facilitating the alignment between oxygen images, the
position of the fish and the sediment surface. The CCD camera and LED light
source were positioned perpendicular to the side of the aquarium hosting the
experimental chamber (Fig. 2).
Data acquisition and image analysis were performed with custom-made software
(Molliview v 1.85 and CalMolli v 0.93). All planar optode images were taken in
darkness to avoid any potential artefacts induced by ambient light.
Sandeel-mediated flow patterns
To visualize any flow patterns in the interstice around the buried sandeel,
and to estimate the ventilatory flow rate of the fish, an isotonic dye
solution (Rhodamine) was added to the sediment surface of the experimental
chamber and digital colour films were obtained as the tracer percolated
through the sand (Fig. 3). The
ventilatory flow rate (ml min–1) was estimated from the
tracer percolation rate, the volume of the dyed sediment, and the sediment
porosity.
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Hypoxia experiment
Buried fish were acclimatised overnight in normoxic water in the open
experimental chamber (Fig. 1).
The following morning, water exchange with the ambient aquarium was stopped
and the overlying water recirculated with an adjacent deoxygenation-tower kept
at a lower, constant air-saturation level by regulated nitrogen bubbling. The
deoxygenation-tower ensured rapid and precise adjustment of air-saturation
level without disturbing the fish, and water exchange with the experimental
chamber was ensured by a small flow-pump
(Fig. 2). The oxygen saturation
was monitored continuously with a galvanic oxygen probe (Oxyguard, Tjele,
Denmark), located in the ambient aquarium. The signal of the probe was used to
automatically regulate the nitrogen injection in the deoxygenation-tower.
Oxygen uptake measurements
Three different, independent procedures were used to determine the oxygen
uptake 
O2 of the
buried fish. The methods are described below and in the following text
referred to as `method 1', `method 2' and `method 3'.
Method 1
Sediment was ignited overnight at 680°C and subsequently autoclaved for
1 h at 120°C. After cooling, the sediment was bubbled with compressed air
and then added to the experimental chamber. A fish was added and soon buried
in the sterilized fully aerated, oxygenated sand. After 1 h of acclimation,
the incubation was initiated by stopping the recirculating flow and closing
the chamber lid (Fig. 1).
During incubations the overlying water was continuously mixed by the central
stirrer (Fig. 1). The oxygen
uptake rate of the fish was calculated from the concentration decrease in
oxygenation of overlying water in the experimental chamber, as monitored by
the section of the calibrated planar oxygen optode exposed to the overlying
water phase. To minimize the likelihood of cutaneous oxygen uptake from the
sediment, only images obtained after the fish had been buried for 4–5 h
were used for calculations. At this stage, local anoxia had evolved around the
fish as the oxic porewater was replenished by oxygen-depleted water leaving
the gills. In parallel, a conventional oxygen polarographic mini-electrode,
connected to a picoampere-meter and a strip-chart-recorder, followed the
oxygen concentration in the water phase of the closed chamber; the two
independent determinations of the oxygen decline rate never deviated by more
than 3%. Incubations of the sterile, aerated sediment without fish
confirmed a low oxygen uptake probably induced by microbial biofilms
establishing on chamber walls. This background value was always less than
15% of values from incubations including fish and was corrected for
during the oxygen uptake calculations. Individual rates of oxygen uptake for 3
g fish (O2(3g))
were calculated as
O2(3g)=O2(measured)x(Mb/0.003)(1–A),
where
O2(measured) is
the measured rate of oxygen consumption, Mb is the mass of
the fish in kg, and A is a scaling exponent of 0.8
(Clarke and Johnston, 1999),
i.e. the relationship between metabolic rate and size.
Method 2
Method 2 is based on measurements of fish buried in natural sediments. Here
we subtract the calculated sediment related O2 uptake (see below)
from the total O2 uptake of incubated experimental chambers hosting
sediment and buried fish. The diffusive oxygen uptake (DOU) of the
sediment was calculated from one-dimensional microprofiles extracted from the
oxygen images in areas not affected by the fish using Fick's first law of
diffusion:
DOU=–
xDsedxdC/dz,
where is the sediment porosity, Dsed is the porosity
corrected, oxygen sediment diffusion coefficient at the given temperature and
salinity (Li and Gregory,
1974; Boudreau,
1997) and 
C/z is the steepest
linear concentration gradient right below the sediment surface (see also
Fig. 4C). The average
volume-specific sediment respiration rate of the aerobic sediment
(Rvol) along the sediment surface was calculated by
dividing the DOU with the oxygen penetration depth, assuming 0-order
kinetics for the oxygen consumption rate
(Glud et al., 2003). The total
oxygen uptake related to the oxic sediment was subsequently calculated by
multiplying Rvol with the oxygenated volume of the
sediment, i.e. the volume along the primary interface plus the volume induced
by the advection of the fish. The latter volume was estimated from the
oxygenated volume in front of the fish (see above) and the spherical plume
around the gills. The respective values for the O2 concentration in
the two compartments could be directly inferred from the O2 images.
On average, 69±4% (N=3) of the sediment uptake was related to
the primary interface while 26±5% (N=3) was related to the
fraction of sediment oxygenated by the fish activities. To calculate the
oxygen uptake related to the metabolism of the fish uptake, the sediment
related uptake was subtracted from the total oxygen decline in the overlying
water during subsequent incubations of experimental chambers. The
weight-normalized metabolism was calculated as described for `method 1'.
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Method 3
In method 3, the O2 consumption of the fish was approached by
simple Fick'ian calculations, multiplying the ventilatory flow rate with the
O2 extraction efficiency as reflected in the O2
images.
All three methods are independent and rely on different measurements. One-way ANOVA was used to compare the estimated oxygen uptake rates obtained from the three different calculation procedures described above. All values are mean ± s.d. and significance was accepted at P<0.05.
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0.5% (dry mass) of organic matter. When sandeel were added to the
experimental chamber they initially moved around, pausing in different
positions, but after less than 5 min they buried 1–4 cm below the
sediment surface orienting the snout upward. The tracer showed that buried
fish induced a water flow from the sediment surface, through the interstice
and into the mouth. Subsequently, water was ejected from the gills leading to
a diffuse coloured sphere evolving around the gill area. Later the sphere
developed into a gradually growing ring as the tracer was replenished by
uncoloured water ejected from the gills
(Fig. 3). The ventilatory flow
rate was estimated to be 0.26±0.02 ml min–1
(N=3), corresponding to 86.9± 7.3 ml min–1
kg–1.
Oxygen images
The ventilatory activity of the gills advected oxygen from above the
sediment towards the mouth of the fish and created a funnel of oxygenated
sediment (Fig. 4A,B). Microbial
respiration consumed 5–10% of the available oxygen during the passage of
the interstice and before the water entered the mouth of the fish, as shown
(profile 1 in Fig. 4C). This
was also directly evident from the O2 recordings in the ventilated
funnel created by the fish. During this quasi-steady ventilation mode the fish
extracted an average of 86.2±4.8% (N=7) of the oxygen from the
inspired water, as evident from the low oxygen saturations in the water,
leaving the gills percolating into the surrounded anoxic porewater
(Fig. 4B,C). However,
occasionally some fish made a wriggling body movement and this channelled a
pocket of oxygenated water down along the body, a phenomenon here referred to
as `plume ventilation'. With time the plume dispersed away from the fish as
the water was replenished and diluted by oxygen-depleted water leaving the
gills. During sediment percolation the oxygen was gradually consumed by the
interstitial microbes and chemical oxidation processes. The effect of the
undulatory movements generally lasted 20–30 min and during this period
there were significant horizontal and temporal variations in the sediment
oxygen distributions (Fig. 5).
These events were nevertheless unusual. Only 13% of fish (2 out of 15)
displayed undulatory movements and then only 3 or 4 times during a 12 h
period. Thus, these fish experienced an oxygenated environment in the sediment
for 8–17% of the time they were buried. In conclusion, ignoring the
minor oxygen depleted plume around the gills, fish were completely surrounded
by anoxic sediment for the vast majority of time.
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;
Lomholt and Johansen, 1979;
Steffensen et al., 1982;
Randall and Daxboeck, 1984).
Being confined by the sediment, sandeels must employ constant gill movements
to maintain water flow into the mouth and this could involve high costs
apparently compensated by the efficient oxygen extraction. The mean
ventilatory flow rate of 86.9±7.3 ml min–1
kg–1 (N=3) for sandeel is very comparable to values
estimated for partially buried flounder and plaice (87–108 ml
min–1 kg–1) at equivalent temperature
(Kerstens et al., 1979;
Steffensen et al., 1982). The
sandeel were largely embedded in anoxic sediment, and thus the possibility of
oxygen uptake across the skin is generally excluded, but the plume events
presumably enable the skin to act as an additional respiratory surface when
oxygen-rich water surrounded the fish's body, as known from non-burying fish
(Kirsch and Nonnotte, 1977;
Steffensen et al., 1981;
Steffensen and Lomholt, 1985).
These events were, however, only observed for 13% of the fish and lasted for a
maximum of 17% of the time for these fish. This suggests that cutaneous
respiration generally is of minor importance for buried sandeels and the
contribution to O2 requirements of the fish can presumably be
ignored.
Both in situ and laboratory based measurements have shown that the
oxygen distribution in sandy sediments can be extremely dynamic
(de Beer et al., 2005;
Precht et al., 2004;
Cook et al., 2007).
Hydrodynamic forcing, interrelating with the topographic relief of the
sediment surface, can induce extensive oxygen oscillations in the top 10 cm of
the sediment, and it remains to be proven if sandeels benefit from this
intermittent oxygenation of the interstitial water when taking refugee in sand
during night or during winter dormancy. In intertidal areas, pockets of air
trapped in the sediment could act as an oxygen reservoir for buried sandeels.
In deeper waters, high densities of buried sandeel are often seen in sand
banks characterised by ripples, intense wave actions and strong bottom
currents (Wright et al., 2000;
Freeman et al., 2004). In
these areas, interactions between flow velocity gradients and topographic
structures enhance advective water exchange, augmenting the sediment
oxygenation (Forster et al.,
1996; Ziebis et al.,
1996), which may explain fish aggregation in such areas. The fish
will, however, experience periods where hydrodynamics of the overlying water
and ripple movement will leave the sediment anoxic hence excluding the option
of exploiting oxygen in the interstitial water during such periods.
Behavioural strategies towards hypoxia
The majority of buried sandeels (6 of 8) showed no fleeing response when
exposed to a gradual decline in the ambient oxygen levels down to 5–8%
air-saturation, but they remained buried despite ventilating severely
oxygen-depleted water. With the ultimate aim to survive under such
unfavourable conditions, the fish balances between two strategies; the need to
reach more oxygenated waters or to save energy and hence avoid major
physiological stress. Different species vary in their behavioural response
when exposed to low ambient oxygen levels; some increase swimming speed as an
escape strategy (Bejda et al.,
1987; Van Raaij et al.,
1996; Domenici et al.,
2000; Johansen et al.,
2006) whereas others exhibit a more quiescent behaviour presumable
to maintain physiological homeostasis
(Metcalfe and Butler, 1984;
Fischer et al., 1992;
Nilsson et al., 1993;
Dalla Via et al., 1998;
Cech and Crocker, 2002).
Apparently, sandeels generally employ a `sit and wait for better times'
strategy, relying on endurance until oxygen conditions improve. Maybe this is
a consequence of their lifestyle, being very stationary after settling in a
sandy area, to which they will return after feeding in deeper waters during
daytime (Meyer et al., 1979;
Pinto et al., 1984;
Wright et al., 2000;
Holland et al., 2005). This
strategy may, however, be maladaptive during extensive and prolonged oxygen
depletion events, as has been observed during recent years in the inner Danish
waters (HELCOM, 2003;
Conley et al., 2007), where,
for periods of weeks, water oxygen levels reached values critical for sandeels
(Scrit=20% at 10°C).
Comparative oxygen uptake rates
The present results provide evidence that sandeels indeed have a reduced
oxygen uptake while buried. This was confirmed by three independent approaches
for estimating the oxygen consumption. Combining all three approaches, the
average O2 uptake of the buried fish amounted to 33.1±4.4 mg
O2 kg–1 h–1 (N=9),
corresponding to 46% of the value obtained for similar sized sandeels by
conventional resting respirometry at equivalent temperature
(Behrens and Steffensen, 2006).
Diffusion of oxygen into epidermal cells can occur despite low ambient oxygen
levels (Steffensen et al.,
1981), but care was taken in the calculations in method 1 only to
use oxygen images after deoxygenated sediment had developed around the fish in
the otherwise sterile and aerated sediment (see
Fig. 7D). In addition,
considering that there was no significant difference between the results from
the present three methods (Table
1), where the two latter exclude the possibility of cutaneous
oxygen uptake (ignoring the small circle of oxygenated water around the
gills), we conclude that the present study provides evidence that buried
sandeels have lower oxygen uptake than fish enclosed in a respiration
chamber.
There are three factors that, alone or in combination, can explain this
observation. (1) Buried fish may express lower oxygen requirements due to
metabolic depression. If so, this supports earlier speculations that burying
represents a strategy for energy conservation
(Quinn and Schneider, 1991;
Wright et al., 2000). (2) The
oxygen uptake of buried fish may not balance its energy requirements. If this
is the case and the fish supplements its energy requirements with anaerobic
metabolism, it will `push the problem ahead' by developing an oxygen debt,
which can then be repaid when the fish leaves the sediment. In case of such a
strategy the preset estimates of oxygen uptake will underestimate the actual
energy use of buried fish. The routine metabolism of swimming sandeels has a
considerable anaerobic component, which could favour this idea
(Behrens and Steffensen, 2006).
Being buried has the obvious advantage of being hidden but despite that, an
anaerobic metabolic component could be a necessary consequence, or adaptation,
of this behaviour. However, we find it unlikely that a 50% decrease in the
O2 requirements can be explained by anaerobic metabolism, as this
would require massive accumulation of lactate, well above previous
measurements for other fish (Milligan and
Wood, 1987; Baker et al.,
2005). (3) We cannot exclude elevated oxygen uptake of specimens
confined in a small respirometer where they cannot bury. Visual inspection of
the fish concluded, however, that enhanced stress-induced O2 uptake
of this magnitude was unlikely as no obvious signs of stress were observed. We
therefore conclude that the reduced oxygen uptake during burial is caused, at
least in part, by lower energy requirements through metabolic depression,
potentially in combination with a gradual accumulation of lactate.
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Acknowledgments |
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References |
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|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Baker, D. W., Wood, A. M., Litvak, M. K. and Kieffer, J. D. (2005). Haematology of juvenile Acipenser onyrinchus and Acipenser brevirostrum at rest and following forced activity. J. Fish Biol. 66,208 -221.
Behrens, J. W. and Steffensen, J. F. (2006). The effect of hypoxia on behavioural and physiological aspects of lesser sandeel, Ammodytes tobianus (Linnaeus, 1785). Mar. Biol. doi:10.1007/s00227-006-0456-4 .
Bejda, A. J., Studholme, A. L. and Olla, B. L. (1987). Behavioural responses of red hake, Urophycis chuss, to decreasing concentrations of dissolved oxygen. Environ. Biol. Fish. 19,261 -268.[CrossRef]
Boudreau, B. P. (1997). Diagenetic Models and their Implementation: Modelling Transport and Reactions in Aquatic Sediments. Berlin: Springer Verlag.
Cech, J. J. and Crocker, C. E. (2002). Physiology of sturgeon: effects of hypoxia and hypercapnia. J. Appl. Ichthyol. 18,320 -324.[CrossRef]
Clarke, A. and Johnston, N. M. (1999). Scaling of metabolic rate with body mass and temperature in teleost fish. J. Animal. Ecol. 68,893 -905.[CrossRef]
Conley, D. J., Carstensen, J., Ærtebjerg, G., Christensen, P. B., Dalsgaard, T., Hansen, J. L. S. and Josefson, A. B. (2007). Long-term changes and impacts of hypoxia in Danish coastal waters. Ecol. Appl. In Press.
Cook, P. L. M., Wenzhöfer, F., Glud, R. N., Janssen, F. and Huettel M. (2007). Benthic solute exchange and carbon mineralization in two shallow subtidal sandy sediments: Impact of advective porewater exchange. Limnol. Oceanogr. In Press.
Dalla Via, J., van den Thillart, G., Cattani, O. and Cortesi, P. (1998). Behavioural responses and biochemical correlates in Solea solea to gradual hypoxic exposure. Can. J. Zool. 76,2108 -2113.
de Beer, D., Wenzhöfer, F., Ferdelman, T. G., Boehme, S. E., Huettel, M., van Beusekom, J. E. E., Böttcher, M. E., Musat, N. and Dubilier, N. (2005). Transport and mineralization rates in North Sea sandy intertidal sediments, Sylt-Rømø Basin, Wadden Sea. Limnol. Oceanogr. 50,113 -127.
Domenici, P., Steffensen, J. F. and Batty, R. S. (2000). The effect of progressive hypoxia on swimming activity and schooling in Atlantic herring. J. Fish Biol. 57,1526 -1538.
Fischer, P., Rademacher, K. and Kils, U. (1992). In situ investigations on the respiration and behaviour of the eelpout Zoarces viviparous under short-term hypoxia. Mar. Ecol. Prog. Ser. 88,181 -184.
Forster, S., Huettel, M. and Ziebis, W. (1996). Impact of boundary layer flow velocity on oxygen utilization in coastal sediments. Mar. Ecol. Prog. Ser. 143,173 -185.
Franke, U., Polerecky, L., Prect, E. and Huettel, M. (2006). Wave tank study of particulate organic matter degradation in permeable sediments. Limnol. Oceanogr. 51,1084 -1096.
Frederiksen, M. S. and Glud, R. N. (2006). Oxygen dynamics in the rhizosphere of Zostera marina: a two-dimensional planar optode study. Limnol. Oceanogr. 51,1072 -1083.
Freeman, S., Mackinson, S. and Flatt, R. (2004). Diel patterns in the habitat utilisation of sandeels revealed using integrated acoustic surveys. J. Exp. Mar. Biol. Ecol. 305,141 -154.[CrossRef]
Gislason, H. and Kirkegaard, E. (1998). Is the industrial fishery in the North Sea sustainable? In Northern Waters: Management Issues and Practice. Fishing News Books (ed. D. Symes), pp. 195-208. Oxford: Blackwell.
Glud, R. N., Ramsing, N. B., Gundersen, J. K. and Klimant, I. (1996). Planar optrodes: a new tool for fine scale measurements of two-dimensional O2 distribution in benthic communities. Mar. Ecol. Prog. Ser. 140,217 -222.[CrossRef]
Glud, R. N., Gundersen, J. K., Røy, H. and Jørgensen, B. B. (2003). Seasonal dynamics of benthic O2 uptake in a semi enclosed bay: importance of diffusion and fauna activity. Limnol. Oceanogr. 48,1265 -1276.
HELCOM (2003). The 2002 oxygen depletion event in the Kattegat, Belt Sea and Western Baltic. Baltic Sea. Environ. Proc. 90,1 -64.
Høines, Å. S. and Bergstad, O. A. (2001). Density of wintering sand eel in the sand recorded by grab catches. Fish Res. 49,295 -301.[CrossRef]
Holland, G. J., Greenstreet, S. P. R., Gibb, I. M., Fraser, H. M. and Robertson, M. R. (2005). Identifying sandeel Ammodytes marinus sediment habitat preferences in the marine environment. Mar. Ecol. Prog. Ser. 303,269 -282.
Holst, G. and Grünwald, B. (2001). Luminescence lifetime imaging with transparent oxygen optodes. Sens. Actuators B Chem. 74, 78-90.[CrossRef]
Holst, G., Kohls, O., Klimant, I., König, B., Kühl, M. and Ricter, T. (1998). A modular luminescence lifetime imaging system for mapping oxygen distribution in biological samples. Sens. Actuators B Chem. 51,163 -170.[CrossRef]
Huettel, M. and Webster, I. T. (2001). Porewater flow in permeable sediments. In The Benthic Boundary Layer (ed. B. P. Boudreau and B. B. Jørgensen), pp.144 -179. Oxford: Oxford University Press.
Johansen, J. L., Herbert, N. A. and Steffensen, J. F. (2006). The behavioural and physiological response of Atlantic cod (Gadus morhua L.) to short-term acute hypoxia. J. Fish Biol. 68,1918 -1924.
Kerstens, A., Lomholt, J. P. and Johansen, K.
(1979). The ventilation, extraction and uptake of oxygen in
undisturbed flounders, Platichtys flesus: responses to hypoxia
acclimation. J. Exp. Biol.
83,169
-179.
Kirsch, R. and Nonnotte, G. (1977). Cutaneous respiration in three freshwater teleosts. Respir. Physiol. 29,339 -354.[CrossRef][Medline]
Li, Y. H. and Gregory, S. (1974). Diffusion of ions in sea water and deep sea sediments. Geochim. Cosmoschim. Acta 38,703 -714.
Lomholt, J. P. and Johansen, K. (1979). Hypoxia acclimation in carp – how it affects O2 uptake, ventilation, and O2 extraction from water. Physiol. Zool. 52,38 -49.
Metcalfe, J. D. and Butler, P. J. (1984).
Changes in activity and ventilation in response to hypoxia in unrestrained,
unoperated dogfish (Scyliorhinus canicula L.). J. Exp.
Biol. 108,411
-418.
Meyer, T. L., Cooper, R. A. and Langton, R. W. (1979). Relative abundance, behaviour, and food habits of the American sand lance, Ammodytes americanus, from the Gulf of Maine. Fish. Bull. Wash. D. C. 77,243 -253.
Milligan, C. L. and Wood, C. M. (1987).
Regulation of blood oxygen transport and red cell pHi after
exhaustive activity in rainbow trout (Salmo gairdneri) and starry
flounder (Platichthys stellatus). J. Exp.
Biol. 133,263
-282.
Nilsson, G. E., Rosen, P. R. and Johansson, D. (1993). Anoxic depression of spontaneous locomotor activity in crucian carp quantified by a computerized imaging technique. J. Exp. Biol. 180,153 -162.[Abstract]
Pinto, J. M., Pearson, W. H. and Anderson, J. W. (1984). Sediment preferences and oil contamination in the Pacific sand lance Ammodytes hexapterus. Mar. Biol. 83,193 -204.[CrossRef]
Precht, E., Franke, U., Polerecky, L. and Huettel, M. (2004). Oxygen dynamics in permeable sediments with wave-driven pore water exchange. Limnol. Oceanogr. 49,149 -159.
Quinn, T. and Schneider, D. E. (1991). Respiration of the teleost fish Ammodytes hexapterus in relation to its burrowing behaviour. Comp. Biochem. Physiol. 98A, 71-75.
Randall, D. J. and Daxboeck, C. (1984). Oxygen and carbon dioxide transfer across fish gills. In Fish Physiology. Vol. X (ed. W. S. Hoar and D. J. Randall), pp. 263-314. New York: Academic Press.
Reay, P. J. (1973). Some aspects of the biology of the sandeel, Ammodytes tobianus L., in Langstone Harbour, Hampshire. J. Mar. Biol. 53,325 -346.
Robards, M. D., Anthony, J. A., Rose, G. A. and Piatt, J. F. (1999). Changes in proximate composition and somatic energy content for Pacific sand lance (Ammodytes hexapterus) from Kachemak Bay, Alaska relative to maturity and season. J. Exp. Mar. Biol. Ecol. 242,245 -258.
Steffensen, J. F. and Lomholt, J. P. (1985). Cutaneous oxygen uptake and its relation to skin blood perfusion and ambient salinity in the plaice, Pleuronectes platessa. Comp. Biochem. Physiol. 81A,373 -375.[CrossRef][Medline]
Steffensen, J. F., Lomholt, J. P. and Johansen, K. (1981). The relative importance of skin oxygen uptake in the naturally buried plaice, Pleuronectes platessa, exposed to graded hypoxia. Respir. Physiol. 44,269 -275.[CrossRef][Medline]
Steffensen, J. F., Lomholt, J. P. and Johansen, K. (1982). Gill ventilation and O2 extraction during graded hypoxia in two ecologically distinct species of flatfish, the flounder (Platicthys flesus) and the plaice (Pleuronectes platessa). Environ. Biol. Fish. 7,157 -163.
Van Raaij, M. T. M., Pitt, D. S. S., Balm, P. H. M., Steffens, A. B. and van den Thillart, G. (1996). Behavioural strategy and the physiological stress response in rainbow trout exposed to severe hypoxia. Horm. Behav. 30, 85-92.[CrossRef][Medline]
Wenzhöfer, F. and Glud, R. N. (2004). Small-scale spatial and temporal variability in coastal benthic O2 dynamics: effects of fauna activity. Limnol. Oceanogr. 49,1471 -1481.
Winslade, P. (1974a). Behavioural studies on lesser sandeel Ammodytes marius (Raitt). I. The effect of food availability on activity and the role of olfaction in food detection. J. Fish Biol. 6,565 -576.[CrossRef]
Winslade, P. (1974b). Behavioural studies on lesser sandeel Ammodytes marius (Raitt). II. The effect of light intensity on activity. J. Fish Biol. 6, 577-586.[CrossRef]
Winslade, P. (1974c). Behavioural studies on lesser sandeel Ammodytes marius (Raitt). III. The effect of temperature on activity and the environmental control of the annual cycle of activity. J. Fish Biol. 6, 587-599.[CrossRef]
Wright, P. J., Jensen, H. and Tuck, I. (2000). The influence of sediment type on the distribution of lesser sandeel, Ammodytes marius. J. Sea Res. 44,243 -256.[CrossRef]
Ziebis, W., Huettel, M. and Forster, S. (1996). Impacts of bioenergetic sediment topography on oxygen fluxes in permeable seabeds. Mar. Ecol. Prog. Ser. 140,227 -237.
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