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Quantifying Bioturbation of a Simulated Ash Fall Event

Authors:
  • University of St Andrews and Scottish Association for Marine Science (SAMS)

Abstract and Figures

Tephrochronology allows the establishment of ‘isochrons’ between marine, lacustrine, terrestrial and ice cores, typically based on the geochemical fingerprint of the tephra. The development of cryptotephrochronology has revealed a vast inventory of isochrons which hold the potential to improve stratigraphic correlation and identify systemic leads and lags in periods of rapid climate change. Unfortunately, bioturbation acts to blur these isochrons, reducing the temporal resolution in marine and lacustrine records. In order to better resolve these event horizons, we require a better understanding of bioturbative processes, and the depth and time over which they operate. To this end, an ash fall event was simulated on the intertidal zone of the Eden Estuary, Fife, Scotland and sediment cores were collected over 10 days. A novel approach to tephra quantification was developed, using the imaging software ImageJ. Our results showed limited bioturbation (mixed depth=18 mm), most likely owing to the fine grain size, low-energy environment and the resulting faunal composition of the sediments. These results imply a strong ecological control on bioturbation, and suggest that inferences may be made about palaeoenvironments from the observed bioturbation profiles. Supplementary material The ImageJ macro used in this study, as well as raw tephra concentration data and details of the method validation are available at http://www.geolsoc.org.uk/SUP18725 .
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Geological Society, London, Special Publications Online First
February 5, 2014; doi 10.1144/SP398.9 , first publishedGeological Society, London, Special Publications
Joe A. Todd, William E. N. Austin and Peter M. Abbott
Quantifying bioturbation of a simulated ash fall event
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Quantifying bioturbation of a simulated ash fall event
JOE A. TODD1,2*, WILLIAM E. N. AUSTIN1, 3 & PETER M. ABBOTT1,4
1
School of Geography and Geosciences, University of St Andrews, St Andrews,
Fife, Scotland KY16 9AL, UK
2
Present address: Department of Geography, Scott Polar Research Institute,
University of Cambridge, Lensfield Road, Cambridge CB2 1ER, UK
3
Present address: Scottish Marine Institute, Scottish Association for Marine Science,
Oban PA37 1QA, UK
4
Present address: Department of Geography, College of Science, Swansea University,
Singleton Park, Swansea SA2 8PP, UK
*Corresponding author (e-mail: jat71@cam.ac.uk)
Abstract: Tephrochronology allows the establishment of ‘isochrons’ between marine, lacustrine,
terrestrial and ice cores, typically based on the geochemical fingerprint of the tephra. The develop-
ment of cryptotephrochronology has revealed a vast inventory of isochrons which hold the poten-
tial to improve stratigraphic correlation and identify systemic leads and lags in periods of rapid
climate change. Unfortunately, bioturbation acts to blur these isochrons, reducing the temporal res-
olution in marine and lacustrine records. In order to better resolve these event horizons, we require
a better understanding of bioturbative processes, and the depth and time over which they operate.
To this end, an ash fall event was simulated on the intertidal zone of the Eden Estuary, Fife,
Scotland and sediment cores were collected over 10 days. A novel approach to tephra quantification
was developed, using the imaging software ImageJ. Our results showed limited bioturbation
(mixed depth ¼18 mm), most likely owing to the fine grain size, low-energy environment and the
resulting faunal composition of the sediments. These results imply a strong ecological control on
bioturbation, and suggest that inferences may be made about palaeoenvironments from the
observed bioturbation profiles.
Supplementary material: The ImageJ macro used in this study, as well as raw tephra concen-
tration data and details of the method validation are available at http:// www.geolsoc.org.uk/
SUP18725.
In most marine or lacustrine benthic habitats, the
surficial sediment layer is very likely to be mixed
and reworked by its epifauna and infauna, creatures
living on and in the sediment, respectively (e.g.
Berger & Heath 1968), as well as by any fish or
mammals which come into contact with it (Biles
et al. 2002). The collective mixing effect of this bio-
logical activity is known as bioturbation. In terms
of the processes involved, bioturbation occurs
largely through burrowing, feeding, defecation and
locomotion.
Bioturbation processes are of interest to re-
searchers in many fields. For marine ecologists, bio-
turbation is an essential set of processes that
enhance nutrient release from the sediment (Solan
et al. 2004a) as well as increasing the surface area
of the sedimentwater interface (Biles et al. 2002).
Within the context of evolutionary theory, bio-
turbation is a classic example of ecosystem engin-
eering, the alteration of a habitat by its inhabitants
(Meysman et al. 2006). However, to palaeoceano-
graphers, bioturbation presents a problem because
the processes of bioturbation act to mix younger
material into the older sediments below, and vice
versa. Bioturbation therefore acts to obfuscate the
geological sedimentary record. This makes it dif-
ficult to identify boundaries between strata which
may have been relatively clear at the time of
deposition.
Previous bioturbation investigations (Solan
et al. 2004b) have focussed on bioturbation at the
scale of individual events using, for example, time
lapse photography. However, carrying out such an
investigation is expensive; furthermore, while indi-
vidual bioturbation events are of interest to ecolo-
gists, geochronology tends to be concerned with
the net effect of repeat events. Unlike ecologists,
geochronologists are not primarily interested in
the individual bioturbation events but, rather, the
integrated result of this process through time.
From:Austin, W. E. N., Abbott, P. M., Davies, S. M., Pearce,N.J.G.&Wastega
˚rd, S. (eds) Marine
Tephrochronology. Geological Society, London, Special Publications, 398, http://dx.doi.org/10.1144/SP398.9
#The Geological Society of London 2014. Publishing disclaimer: www.geolsoc.org.uk/pub_ethics
by guest on February 6, 2014http://sp.lyellcollection.org/Downloaded from
Guinasso & Schink (1975) reviewed biotur-
bation from an oceanographic perspective, and
described it in terms of three principle parameters:
an eddy diffusion rate parameter, D; a maximum
mixing depth, L; and sediment deposition rate,
n. They also defined a dimensionless bioturba-
tion index:
bioturbation index =
D
Lv
whose value describes the homogeneity of the sur-
face mixed layer, with low values describing lim-
ited mixing and vice versa. An important fact
highlighted by this bioturbation index is that the
extent of mixing is affected not only by the pro-
cesses of bioturbation, but also by the rate of
sediment burial.
Tephrochronology
Tephrochronology uses tephra layers from past
volcanic eruptions as isochronous marker hori-
zons, layers of the same age in different geological
records. On geological time-scales, tephra depo-
sition by a volcanic eruption is effectively synchro-
nous and can occur over a wide geographical area,
making it especially useful in studying the (a)syn-
chronicity of rapid climate transitions, between
disparate sequences and where traditional dating
methods lack sufficient resolution (Mangerud et al.
1984; Haflidason et al. 2000; Austin et al. 2004;
Austin & Abbott 2010). For example, Austin et al.
(2004) demonstrated how the correlation of the
rhyolitic component (II-Rhy-I) of North Atlantic
Ash Zone II between the GISP2 ice-core and
a Northeast Atlantic marine core (MD95-2006)
suggested the regional synchroneity of the abrupt
cooling at the end of Greenland Interstadial-15.
One of the great values of tephrochronology
lies in the recognition of globally synchronous
ash fall events. Unfortunately, an inability to pre-
cisely define the position of a tephra isochron in
a marine sequence owing to various source, trans-
port, depositional and post-depositional processes,
including bioturbation, may sometimes arise. This
makes bioturbation particularly problematic for
tephrochronologists, especially in the analysis of
cryptotephras, whose tephra deposits are invisible
to the naked eye. While a non-bioturbated cryp-
totephra may be detected in a sediment core as a
distinct peak in shard concentration, it is often the
case that shards from the same population are
found through a considerable depth of the core. In
these cases, there is some confusion in the litera-
ture as to where to define the actual depth of the
marker horizon (i.e. isochrons; Lowe 2011; Davies
et al. 2012).
The situation is further complicated by the fact
that bioturbation is a highly variable process; the
rate and maximum extent of bioturbation depends
not only on the collection of species which make
up the benthos and their abundance, but also on
the thickness of the ash layer and the subsequent
rate of deposition. The work of Carter et al. (1995)
suggested that thicker (.1 cm) ash layers tend to
smother the benthos, minimizing bioturbation. It
also suggested that, if rapid deposition occurs after
the ash fall event, the tephra layer will be isolated
before the benthos can be re-established, also
minimizing bioturbation.
By simulating an ash fall event on a marine
estuary and then studying the bioturbation of tephra
over a period of 10 days, this paper aims to pro-
duce a better understanding of the factors which
affect the rate and extent of bioturbation, within
the wider context of marine tephrochronology.
Methods
Site description
In order to explore the questions outlined above, an
ash fall event was simulated in the intertidal zone
of the Eden Estuary, Fife (56.35358N, 2.83908W,
Fig. 1) in July 2010. The decision to study biotur-
bation in an estuarine environment was made for
several reasons. From a practical perspective, inter-
tidal zones are easily accessible and are often well
documented; in this case, a commissioned report
by Scottish Natural Heritage (Bates et al. 2004)
outlines the spatial extent of different biotopes on
the Eden Estuary, which are shown in Figure 1. This
is particularly useful when studying ecosystem
processes as it eliminates the need for a full site
survey. Furthermore, unlike high-energy coastal
systems where bioturbation is limited and disrupted
by wave and tide activity (Cade
´e 2001), estuaries
are relatively low-energy environments, analogous
to the deep sea-bed.
Our study site is a sheltered estuarine mud-
flat, with minimal wave activity, making it ideal
for investigating bioturbation. The site is exposed
for approximately 7 h of every tidal cycle (Austin
2003).
As illustrated in Figure 1, the study site is located
near the shoreline, in a biotope classified as ‘LMU.
HedMac’ (Connor et al. 1997a,b). This classifi-
cation refers to a well-sheltered intertidal zone com-
prising sandy mud characterized by the presence
of Nereis (Hediste diversicolor) and Baltic clam
(Macoma baltica), as well as other oligochaetes,
polychaetes and bivalves (Bates et al. 2004). A com-
prehensive database of all biotopes identified in
Figure 1 can be found online at www.marlin.ac.uk.
Previous efforts to quantify sediment bioturbation
J. A. TODD ET AL.
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have suggested that the annelids (polychaetes and
oligochaetes) play a significant role in estuarine
bioturbation (Biles et al. 2002). Therefore, the dom-
inance of Nereis and the presence of other anne-
lids at this site suggested that bioturbation would
indeed occur.
Characterization of tephra
Ash was collected from Seljavellir, South Ice-
land (63.68N 19.78W) in June 2010 following the
main eruptions of Eyjafjallajo
¨kull earlier in the
year. Laser grain size analysis was carried out on a
tephra sample using a Beckman Coulter LS 230
Laser Diffraction Particle Size Analyzer at the
Facility for Earth and Environmental Analysis at
the University of St Andrews. Riffle box splitting
was used to ensure a representative sub-sample was
obtained. The results (Fig. 2) show that this prox-
imal tephra sample is fairly coarse (
x=299.4mm,
median ¼228.3 mm). This is coarser material than
would be expected to occur in distal ash fall depo-
sits (e.g. Abbott et al. 2011) as the size of airfall
material decreases exponentially with distance
from eruptive source (Sparks et al. 1981). The
tephra was found to be a mix of pumacious and
glassy shards containing vesicles. There was no
specific or diagnostic morphology; a mixture of
spherical and elongate, platy and blocky shards
was observed.
Simulating an ash fall event
Ash was spread in 20 ×20 cm square quadrats
directly onto the exposed intertidal estuarine sedi-
ments. We visited the study site at low tide on 22
July and seeded 18 quadrats with 60 g (37.8 cm
3
)
of ash each, equivalent to an ash layer of 0.95 mm
thickness. So that results were comparable, quadrats
were placed in a grid with 1 m spacing between
each. This ensured that all quadrats were placed
within an ecologically homogenous area and that
all experienced the same tide and wave effects.
Closer spacing was considered, but it was felt that
this might lead to inter-quadrat ash contamination.
Additionally, the possibility of a raised edge on
the quadrat was considered, to prevent outwashing
of tephra by waves and tide; however, it was felt
that this would significantly increase the ecosystem
disturbance. Furthermore, in such a low-energy
environment, tephra loss is likely to be minimal.
This point is addressed further in the Discussion.
Fig. 1. Eden Estuary Biotopes. Adapted from Bates et al. (2004). OS Content: #Crown Copyright/database right
2011. An Ordnance Survey/EDINA supplied service.
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Figure 3 shows a typical quadrat with signs of
burrowing clearly visible in the bottom half of
the image.
Field sampling and laboratory sub-sampling
Coring was carried out after 0, 2, 5 and 10 days,
using a sample tube of 26 mm diameter with
the base removed. This relatively simple setup
allowed cores of 60 mm depth to be taken, from
the middle of each quadrat. On day 0, six quadrats
were cored and one control core was taken from
an adjacent location on the mudflat, unseeded with
tephra. The main purpose of the day 0 cores was
to test the coring method; any ash found below the
surface section of the day 0 cores will represent dis-
turbance through corer insertion into the sediment.
Three of these ‘day 0’ cores were frozen and three
were maintained at room temperature, in order to
determine the best method of storage before sub-
sampling. However, it quickly became apparent
that, if cores were not frozen, bioturbation would
continue after collection, invalidating the resultant
experimental data. Therefore, the three unfrozen
cores were discarded. On days 2, 5 and 10, four
replicate cores were taken and frozen immediately
after collection. Cores were coded in a ‘day-sample
number’ format (i.e. Core 0-2 refers to the second
core taken on day 0). Frozen cores were sliced
into 3 mm sections using a three-way clamp, and
the sections were prepared for analysis as outlined
in Figure 4. The samples were prepared for
microscopy by wet sieving (63 mm) to remove the
fine fractions; this facilitates the drying, disaggre-
gation and counting of the samples. The aim of
this process was to produce samples which could
be accurately and rapidly counted by the process
outlined below.
Quantifying bioturbation
As discussed above, we treat bioturbation as a diffu-
sive process. Thus, we sought to analyse the pres-
ence of tephra such that it could be expressed as a
change in concentration through depth and time.
Therefore, we determined the number of tephra
grains at specific depths in the cores relative to the
overall number of mineral grains at these depths
and expressed these as percentage counts. Typi-
cally, this counting is carried out manually using
a picking tray and a tally counter. Repeated counts
are carried out until a statistically reliable value
is attained for tephra shard concentration. This
method is extremely time-consuming; we estimate
that to process all 300 sub-sampled sections, each
requiring the counting of 15 squares, would take
up to 400 h (i.e. 50 standard working days). In
order to reduce the analysis time, the possibility of
a faster, semi-automated method was investigated.
Costa & Yang (2009) presented a solution to a
similar problem involving the counting of pollen
grains. Rather than counting manually, they used
Fig. 2. Particle size distribution for tephra collected from Eyjafjallajo
¨kull.
J. A. TODD ET AL.
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Fig. 3. Microcosm on Eden Estuary (20 ×20 cm) at (a) day 0 and (b) day 2. By day 2, tephra is barely visible at
the surface.
QUANTIFYING BIOTURBATION OF TEPHRA
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ImageJ, an open-source Java-based image analy-
sis program to count thousands of grains at a time.
Furthermore, they developed a macro for the pro-
gram which would automatically open a specified
series of microscope images, count all the pollen
grains in each image and record the results in
Excel format. They estimated a 5- to 60-fold sav-
ing in time using this method, depending on the
number of grains in each image.
In order to determine the applicability of ImageJ
to the problem of determining tephra shard con-
centration, a series of trials was carried out. The
optimized process resulting from these trials is
described below and illustrated in Figure 5, and
the parameters and algorithms of choice are outlined
in the macro file available in the Supplementary
Material.
Using image analysis to quantify tephra
concentrations
The first stage of automated counting of particles
was image capture. Material from each processed
section was placed on a piece of white paper to
enhance contrast, then placed under a Zeiss Stemi
2000 optical stereomicroscope. Using an attached
Deltapix Infinity X-21 CMOS camera, 10 unique
images were taken of each sub-sampled section,
each with a field of view of 10.67 ×8.53 mm
(1280 ×1024 pixels). Although ImageJ can han-
dle clustered particles, it does not deal well with
large amalgamations of grains, and so care was
taken to ensure that grain density was sufficiently
low (,500 grains per image) that minimal clus-
tering occurred. Care was also taken to ensure that
the microscope’s light source produced a rela-
tively uniform intensity across the field of view, as
the performance of ImageJ is enhanced when
analysing particles on a constant background. It
should be noted, however, that the program is
capable of ‘subtracting’ the image background.
As illustrated in Figure 5, particle analysis in
ImageJ is a multistage process. First, the image is
sharpened to better delineate the outline of indi-
vidual grains. Then the image background is
‘subtracted’. ImageJ carries out background sub-
traction by identifying the predominant trend in
colour, saturation and hue across the image, based
on the assumption of a light background. Follow-
ing background subtraction, the image is converted
from RGB to 8-bit greyscale. The example in Figure
5a shows an image that has undergone the sharp-
ening, background subtraction and 8-bit conver-
sion, which are prerequisites for ‘autothresholding’
(Fig. 5b).
Autothresholding describes the use of an algor-
ithm that automatically distinguishes particles from
background without user input. It converts the grey-
scale image in Figure 5a into a binary image (Fig.
5b) where black represents ‘particle’ and white rep-
resents ‘background’. This feature is one of the two
automatic functions that make ImageJ so useful for
particle analysis, the second being the watershed
function (Fig. 5c). The watershed function takes
the dark patches on a light background produced
by autothresholding and determines, based on their
geometry, which patches are likely to be multiple
particles touching each other. Finally, the program
counts, measures and labels the particles (Fig. 5d)
based on a preset size threshold (area .100
pixels/6940 mm
2
). This threshold corresponds, for
a perfectly round particle, to a diameter of 93 mm;
this is sufficiently above the 63 mm sieve size to
ensure that small particles present owing to incom-
plete sieving are not counted.
Performing the individual steps shown in
Figure 5 on each of the 3000 images in turn would
still be very time-consuming; therefore, a macro
was written, based on that of Costa & Yang
(2009), which first prompts the user to select a direc-
tory containing images, and then proceeds to open
each image in turn, perform each of the steps in
Figure 5 and then save the results in an appropriately
named Excel file. In this way, the images are pro-
cessed at roughly one per second and all 3000
images can be processed in under an hour. Including
the few hours required to capture all the images
under the microscope, this represents an almost
100-fold saving in laboratory time and introduces
an improved uniformity of analysis.
The method outlined above is suitable only
for counting the total number of grains; identifi-
cation of tephra shards in bulk sediment by eye is
an acquired skill and could not be readily automated
with this image analysis software. As such, the final
stage of analysis in ImageJ is manual identification
Fig. 4. Laboratory procedure for preparation of sections.
J. A. TODD ET AL.
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of tephra shards in the processed images. ImageJ is
equipped with the software equivalent of a tally
counter, and so this is simply a process of clicking
on all the tephra shards in each image in turn and
appending these counts to the Excel files produced
by the macro described above.
In addition to automatic grain counting, ImageJ
is also able to determine shard size automatically,
based on edge detection. Thus, data were collected
for shard size distribution for each of the sections,
to determine if the rate of bioturbation affects the
observed shard size or vice versa. For example, are
smaller grains more readily bioturbated, leading to a
varying size distribution of tephra through the depth
of the core influenced by the mixing process?
Testing the accuracy of the image analysis
The automatic nature of particle analysis in ImageJ
has the advantage of being a significantly less
labour-intensive alternative to the traditional
manual counting method. However, the automatic
counting process is not completely accurate; in par-
ticular, the watershed function calculates ‘probable’
breaks, and sometimes cuts large particles into a
few smaller particles, as can be seen in the bottom
right side of the example in Figure 5d.
Furthermore, accuracy is also affected by the
ability of the user to identify tephra shards from a
2D photograph. Sometimes, the distinction between
tephra and bulk sediment is not clear and so the tra-
ditional counting method often involves inspec-
tion at higher magnification or turning particles in
order to better distinguish the features thereof. Ana-
lysing still 2D images makes this process more dif-
ficult and, as such, it is to be expected that the rate
of misidentification may be higher.
The above caveats to this new approach to tephra
shard concentration analysis require that it be tested
and compared with the traditional method to quan-
tify accuracy and ensure validity. To accomplish
this, repeat counts were carried out using both the
Fig. 5. Particle analysis in ImageJ involves some pre-processing owing to the poor quality of the original photography.
First the image is sharpened, converted to 8-bit color and the background subtracted (a). Particle detection is
carried out using automatic thresholding (b). A watershed analysis is performed to split up grains which are touching
(c), before the particles are counted and labelled (d).
QUANTIFYING BIOTURBATION OF TEPHRA
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traditional and ImageJ method, to determine the
error associated with each. A detailed description
of the tests carried out is provided in the Supple-
mentary Material and the results are discussed
below.
Accuracy v. efficiency in image
analysis of tephra
Our analysis of the ImageJ method of tephra identi-
fication, available in the Supplementary Material,
suggests that it is less accurate than the traditional
method. However, we must consider that the
observed error of 23% is relative to the traditional
method, which has itself been shown to have an
inherent error of around 12% (see Supplementary
Material). This figure, therefore, may be an exagger-
ation of the true error. Undoubtedly, with greater
replication and an optimization of the image cap-
ture and processing protocols, this error could be
considerably reduced. For example, images could
be captured at a higher effective resolution, either
by photographing at a higher magnification or by
using a more specialized microscope camera. In
particular, the possibility of taking ‘stacks’ of images
with progressively greater depths of focus has been
suggested; this could potentially allow 3D stack
analysis to be carried out in ImageJ, which would
better represent the morphology of grains and
allow easier identification of tephra. This would
make the structure of the shards (and their often
conchoidal surfaces) more readily identifiable.
While the disadvantage of the ImageJ method is
the potential loss of accuracy, the advantage is the
speed at which analysis can be performed. The ana-
lysis takes roughly two orders of magnitude less
time than the traditional method. This vast saving
in time means that many more images could be ana-
lysed for each section, which would translate into a
reduction in the associated error. For example, one
could carry out four times as many analyses on
each section, which would result in a halving of
the margin of error. This would result in a compar-
able error to the manual counting method, but a 25-
fold saving in time. Our results show that errors
tend to be large when tephra shard concentrations
are low. In these cases, it would be advisable to
analyse considerably more images of each section.
Results
Rate and maximum extent of bioturbation
Average tephra concentration profiles for each
sampling day were produced by taking the mean
tephra concentration from all the replicates at each
depth. For each depth, one-way ANOVA was
carried out to test for a significant change in
tephra shard concentration over time. Where homo-
geneity of variance was not met, Welch’s ANOVA
was also carried out. Post-hoc analysis was carried
out using Tukey’s test to determine which sample
days have significantly different tephra shard con-
centrations at each depth. Raw data are available
in the Supplementary Material.
Visual inspection of the experimental quadrats
on day 2 initially suggested that physical trans-
port (i.e. advection) by wave and tide activity had
largely removed the tephra from the quadrat sur-
faces. Figure 3 shows that, after only 2 days, tephra
appears to be almost completely absent. However,
the percentage tephra in the surface (i.e. 03 mm
section) of quadrat 2-2, for example, is 13.41%,
which is comparable with the percentage tephra
found at the surface of all the day 0 cores
(mean ¼13.42%).
One would expect that physical mixing by wave
and tide action would be associated with at least
some degree of horizontal displacement of the
tephra. However, the high tephra retention rate
seen in the surface layer of successively sampled
cores suggests that minimal horizontal displace-
ment has occurred, and that displacement is primar-
ily vertical. This suggests that, rather than having
been removed by wave or tide activity, the tephra
have largely been bioturbated downwards through
the first 3 mm of the sediment. Similarly high
tephra shard concentrations were found at the sur-
face of all cores (Fig. 6), suggesting that, despite
fears that open quadrats would lead to significant
tephra loss, physical transport of tephra was actu-
ally a relatively minor process in this environment
at the time of the experiment.
Figure 6a shows the tephra concentration pro-
files for all of the 15 cores investigated; Figure 6b
shows tephra concentration profiles averaged for
each sampling day. No tephra was found anywhere
in the control core. Day 0 cores have a high percen-
tage of tephra in the first 3 mm, which immediately
drops to less than 1% at 36 mm depth; no tephra
was found in day 0 cores below the 6 –9 mm sec-
tion. This suggests that the coring process causes
only minimal downward disturbance.
Cores from days 2, 5 and 10 show progressively
more tephra at increasing depths, down to a
maximum depth of 1518 mm. This pattern is inter-
preted as the result of progressive bioturbation
and is illustrated in Figure 6. There appears to be
little difference, at any depth, between cores from
day 5 and day 10. Disregarding the day 0 control
cores, the least bioturbation occurs in core 2-4,
while the most bioturbation occurs in core 5-1;
this implies a degree of spatial heterogeneity in the
extent of the bioturbation processes in the intertidal
environment.
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Fig. 6. (a) Percentage tephra through the depth of all 15 cores. % Tephra ¼percentage of identified grains which are
tephra. Quoted depths correspond to the top of each section. (b) Same as (a), but averaged for each sampling day. Error
bars represent standard error of the mean (SEM).
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Analysis of variance showed that, at the surface
(03 mm), there was no significant difference
between any of the sampling days. This supports
the idea that tephra loss through physical transport
away from each quadrat was minimal. At 3 6 mm
depth, Welch’s one-way ANOVA found a signifi-
cant difference in means (F¼9.652, p¼0.012).
Tukey’s test showed a significant difference (90%
confidence interval) between tephra concentration
at days 0 and 5 ( p¼0.064). At 6– 9 mm depth,
one-way ANOVA found a significant difference
in means (F¼3.587, p¼0.050). Tukey’s test
showed a significant difference (90% confidence
interval) between tephra concentration at days 0
and 10 (p¼0.056). Below this depth, no statis-
tically significant differences were found. The
tephra concentration data and associated analysis
of variance are therefore compatible with bioturba-
tion of tephra from the surface to sub-surface layers
at all sites.
Shard size analysis of the tephra grains revealed
no statistical difference through the depth of any of
the cores, suggesting that the rate of bioturbation is,
in this case at least, independent of shard size. The
data also suggest that the bioturbation process
(downwards mixing) does not preferentially favour
the size sorting of tephra.
Discussion
Accurate quantification of bioturbation, in terms of
both rate and maximum depth, is essential to the
development of the discipline of tephrochronology,
as it allows an opportunity to ‘work back’ from an
observed tephra shard concentration profile to ident-
ify the point of initial deposition. While previous
studies have quantified bioturbation using lumino-
phores (Biles et al. 2002; Solan et al. 2004b)or
radioactive tracers (Gerino et al. 1998), this study
represents the first direct investigation of bioturba-
tion of a simulated ash fall event.
Perhaps the most striking feature of our results is
the relatively shallow depth over which bioturbation
has occurred. Our work suggests that bioturbation
occurs over a maximum ‘mixed depth’ of 18 mm.
The global dataset for bioturbation, however,
seems to support the hypothesis of a global mean
mixed depth of 9.8 cm (+4.5 cm, 1
s
), largely inde-
pendent of ecosystem type (Boudreau 1998). Of
course, 18 mm lies within 2
s
of this global mean
and so is not statistically at odds with this obser-
vation. However, as described above (under ‘Site
description’), our study site is dominated by
Nereis and other active bioturbators. A previous
investigation of bioturbation in an estuarine
environment demonstrated the burrowing activity
of polychaete worms down to 15 cm (Smith &
Schafer 1999), presumably highlighting the highly
variable nature of bioturbation and bioturbation
depths within estuarine environments.
Bioturbation in low-energy environments
Our site on the Eden Estuary was chosen as an
ideal site for studying bioturbation based on the
low energy level. Investigating in a low-energy
environment minimizes the physical mixing signal
which, in the context of a bioturbation study,
could be regarded as a significant source of exper-
imental ‘noise’. However, the relationship between
energy, physical mixing and bioturbation is not
straightforward, as illustrated by Figure 7 (Cade
´e
2001). While it is true that physical mixing does
increase linearly with energy, bioturbation is actu-
ally greatest in mid-energy environments. If the
energy of the environment is too high, vigorous
wave and current activity make it difficult for
infauna to survive, and so bioturbation is minimal.
However, low energy levels also curtail biologi-
cal activity. Our study site is mostly a very low-
energy environment; not only does it lie in a shel-
tered estuary, but it also lies at the high-intertidal
edge. Therefore, despite the presence of several
species of active bioturbators, bioturbation depth
is apparently severely restricted.
Our study site was chosen for ease of repeat
access. However, future investigations into marine
bioturbation should choose a sheltered site in the
sub-tidal zone. Although this will make data collec-
tion significantly more challenging, it is also more
likely to represent a clearer analogue to the deep
sea, and any potential ‘washing out’ of tephra
material by tidal activity may be reduced.
Bioturbation and sediment grain size
Previous research into bioturbation and nutrient
fluxes suggests that grain size exerts a control on
the extent of bioturbation. Winston & Anderson
(1971) conducted a semi-quantitative investigation
of bioturbation in an estuarine environment and
showed that more bioturbation occurred at the
sandy study sites than at the fine-grained silt sites.
Furthermore, in a quantitative study of gas transport
in bioturbated sediments, Kristensen & Hansen
(1999) showed that the transport of ammonia and
carbon dioxide through sediment profiles is depen-
dent on grain size. They found that, in coarser-
grained sediments, gas transport fitted an eddy diffu-
sive model. In other words, burrowing and loco-
motion led to physical movement of porewater,
gases and sediment. However, in fine-grained sedi-
ments, this eddy diffusive model overestimated
gas exchange and so was replaced with a molecular
diffusive model. Implicit in the molecular diffusive
J. A. TODD ET AL.
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model is the lack of physical particle mixing by
biological activity; the nonporous and cohesive
nature of finer-grained sediments therefore tends
to restrict vertical mixing.
Qualitatively, the sediment material at the
study site clearly contains a high silt content, and
the Scottish Natural Heritage ecological survey
reports that the entire lower Eden Estuary is mud-
flats, while LMU.HedMac is defined as ‘sandy
mud shores’ (Bates et al. 2004).
The importance of epifauna
Our results echo those of Solan et al. (2004b), who
carried out bioturbation research in Gullmarsfjord,
Sweden. They used time-lapse image analysis to
investigate the rate and depth of bioturbation over
a 16 h period. They found that, despite the abun-
dance of several active infaunal bioturbators, it
was actually the locomotion of a single crab of the
species Hyas araneus that was responsible for
almost all bioturbation. Epifaunal bioturbation of
this type takes the form of a few discrete events,
as opposed to an ongoing diffusive process, as is
usually considered for infaunal bioturbation. No
evidence of epifaunal activity was found at any of
our experimental quadrats. Both this study and
theirs, therefore, suggest that, over the relatively
short time-scales considered, those infaunal species
typically considered to be active bioturbators are
incapable of mixing below a depth of c. 20 mm.
This would imply that future studies investigating
infaunal bioturbation would need to do so over
longer time-scales (i.e. months rather than days).
However, Figure 6 appears to imply that bio-
turbation halted after day 5 of the experiment.
This would be at odds with the idea that infaunal
bioturbation occurs over longer time periods. In
fact, it is unlikely that the similarity of the profiles
at days 5 and 10 represents a real cessation of bio-
turbation; we would expect that, once the maxi-
mum mixed depth has been reached, the tephra
concentration would homogenize over the mixed-
depth. We do not see this, which suggests that, for
some reason, bioturbation has ‘paused’ or signifi-
cantly slowed between days 5 and 10. This may,
in fact, be a coincidental result, and might imply
that future investigations would benefit from using
a greater number of replicate quadrats or longer field
sampling intervals.
The effects of community structure on
bioturbation
In this investigation, we purposely chose to investi-
gate a single biotope, LMU.HedMac, which des-
cribes sheltered, sandy mud shores dominated by
Hediste diversicolor and Macoma balthica. Investi-
gating a single biotope reduces the biological
variable from the investigation, allowing a more
detailed focus on how bioturbation progresses over
time following a simulated ash fall event. How-
ever, the Eden Estuary and similar environments
would make ideal study sites for future investi-
gations into the role of ecosystem type on biotur-
bation. As shown in Figure 1, the estuary contains
many different biotopes. Furthermore, the devel-
opment and successful application of the new,
Fig. 7. Relation between energy and both physical mixing and bioturbation. Bioturbation is reduced at both extremes,
and most important at mid-energy levels. Modified after Cade
´e (2001).
QUANTIFYING BIOTURBATION OF TEPHRA
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semi-automated method of tephra concentration
analysis outlined here makes it feasible to carry
out considerably more analyses than would previ-
ously have been possible, making a wider ranging
study entirely feasible. It would be particularly
interesting to consider how grain size varies along
the length of the estuary, how this affects commu-
nity structure and, in turn, the rate and extent of
bioturbation. The same, of course, applies to the
study of bioturbation in sub-tidal habitats.
Investigating tephra burial
The tephra concentration profiles resulting from the
present study represent, in reality, only half of a bio-
turbation profile; it is equally important to con-
sider how a tephra marker horizon is bioturbated
upwards following burial. It would, for example,
be incorrect to assume that the original marker
horizon occurs at the highest point in the core
where tephra is found. Is it therefore correct to
assume that the peak tephra concentration rep-
resents the original marker horizon? Future research
should seek to answer this question. For example,
Winston & Anderson (1971) described an investi-
gation where an area of estuarine sediment is exca-
vated, a marker horizon is lain and then re-buried.
Their research was not quantitative, but there is no
reason why the approach followed in this paper
could not, for example, be applied to a buried
marker horizon.
Conclusions
Our results demonstrate that bioturbation of tephra
begins immediately following deposition, even in
a low-energy mid-estuarine environment. The rate
of bioturbation does not appear to be dependent
on the grain size of the tephra present. It is clear
that the processes responsible for bioturbation are
significantly depth-limited in the biotope (LMU.
HedMac) studied. Future investigations into bio-
turbation of tephra in low-energy environments
should seek to study the process over longer time
periods, perhaps over an entire seasonal cycle.
Over this time period, we would expect to see
tephra penetration to a maximum mixed depth,
and this would be confirmed by the progressive
homogenization of the tephra concentration profile
over said mixed depth.
The extent to which these results are applicable
to sub-tidal marine, as opposed to estuarine, biotur-
bation is uncertain. Certainly, the interrelated
factors of sediment grain size distribution and the
energy level of the system appear to play a critical
role in determining the rate of bioturbation. The
sediment at the study site had an oxic layer thickness
of the order of 1 mm, underlain by dark anoxic sedi-
ments; this is typical of fine sediments with high
organic content and a dense and active biofilm. It
is likely that this very thin oxic layer impacts biotur-
bation rates and maximum extent. In this study, the
depth of bioturbation may also have been limited by
the fact that the study site is above the low-tide line,
and is thus exposed for several hours a day; this
effect is a subject worthy of further investigation.
Automatic image analysis using ImageJ was pre-
viously employed by Costa & Yang (2009) to carry
out pollen counts, and it has been adapted here to
count all types of particles, as well as assist in
measuring and counting tephra particles. Our analy-
sis of the accuracy of this new method suggests that
it has a fairly high counting error associated with it.
However, this reported error should be taken as a
tentative figure, because the traditional method,
against which our new method is tested, is far
from error-free. Our results also suggest the need
for more replication in order to produce statistically
robust results. The new particle analysis method
demonstrated in this paper has high significance
and future applicability.
We measured significantly slower bioturbation
rates than previous studies in other marine envi-
ronments (Boudreau 1998), and we attribute this
to the fine grain size and the low energy level.
These two factors play a significant role in deter-
mining community structure and abundance. This
strong ecological control on bioturbation implicitly
hints at the possibility of developing a ‘bioturba-
tion index’, and using it to infer information
about palaeoenvironments, which is an exciting
possibility for the future development of marine
tephrochronology.
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QUANTIFYING BIOTURBATION OF TEPHRA
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... The bioturbation of tephra is a phenomenon most commonly associated with marine sediments (e.g. Carter., et al., 1995;Andrews et al., 2002;van den Bergh et al., 2003;Todd et al., 2014), but it also occurs in terrestrial deposits and can be identified by its effects on tephra layers. Earthworms have the ability to mix fine-grained tephras with enclosing sediments, as do larger burrowing animals such as the Mazama pocket gopher (Thomomys mazama) that are currently remobilising near-surface layers of the 1980 Mt St Helens tephra across Washington State. ...
... A limited number of such studies have taken place (e.g. Payne and Gehrels, 2010;Todd et al., 2014;Blong et al., 2017), but we suggest experiments which cover a wider range of environments and tephra characteristics may give valuable insights into the processes that alter tephra while it is on the surface. ...
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... Crucially for loess deposits, as tephra material is unconsolidated it is possible for it to be recycled and redeposited. To ensure the horizon represents primary ash fallout, field investigations should take into account the geomorphological position of the loess profile, spatial continuity of tephra, and potential for reworking (Manville and Wilson, 2004;Alloway et al., 2013;Todd et al., 2014). Secondly, as multiple eruptions from the same volcano, or from the same volcanic belt, may have a very similar geochemical signature identification, establishing the source and exact timing of an eruption may not be straightforward or possible (Brendryen et al., 2010;Lane et al., 2012). ...
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... In contrast, two bulk samples of Lepué Tephra from ODP core 1233D (core depths of 14.68 m and 14.80 m, each analysed in triplicate) shows Rb concentrations about twice the average of proximal bulk and accretionary lapilli samples. The high Rb in the ODP 1233D core sample seems most likely to result from the mixing of marine clays, generally rich in Rb (Li and Schoonmaker, 2003) into the tephra layer by bioturbation and/or co-deposition (Todd et al., 2014). Because of this, the analysis of a bulk sample of this marine occurrence of distal tephra (a mixture of tephra and marine clay) is likely to not be fully representative of the deposit as a whole, but no samples of the enclosing marine sediment were analysed in this study, and no sediment composition data from ODP core 1233D have been published. ...
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... Sediment on the surface of the seafloor may be locally mixed up by bioturbation (Teal et al., 2008;Thornalley et al., 2010;Todd et al., 2014;Griggs et al., 2015). This is substantial in regions of low sedimentation rates, where burrowing can cause intermixing of up to 10 cm/ka of the entire sediment body (Thornalley, D., personal communication, 2016) and thus can have a relevant influence on the mixing of the surface sediment with deeper sediment layers even within a short period of time. ...
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... Tephra deposits in the marine environment, however, are particularly vulnerable to secondary transport and reworking processes such as bioturbation or sediment loading [e.g., Ruddiman and Glover, 1972]. These processes may displace or blur the lower contact of the tephra horizon by either drawing material upward and/or downward through the profile, decreasing the concentration of the peak in glass shards [Ruddiman and Glover, 1972;McCave, 1988;Bromley, 1996;Todd et al., 2014;Cassidy et al., 2014]. Positioning the tephra isochron, therefore, may be problematic. ...
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... Marine cores, especially from locations downwind of eruption centres, may also contain detailed records of tephra layers or cryptotephras intercalated with sediments (e.g., Gudmundsdóttir et al., 2012;Abbott et al., 2013;Ponomareva et al., 2013b;Austin et al., 2014). Possible reworking of tephras (by currents, ice-rafting, bioturbation) adds complexity in some cases (Brendryen et al., 2010;Larsen et al., 2014;Todd et al., 2014). ...
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Extract [derived from published article – for internet/library purposes only] Tephrochronology is the use of primary, characterized tephras or cryptotephras as chronostratigraphic marker beds to connect and synchronize geological, paleoenvironmental, or archaeological sequences or events, or soils/paleosols, and, uniquely, to transfer relative or numerical ages or dates to them using stratigraphic and age information together with mineralogical and geochemical compositional data, especially from individual glass-shard analyses, obtained for the tephra/cryptotephra deposits. To function as an age-equivalent correlation and chronostratigraphic dating tool, tephrochronology may be undertaken in three steps: (i) mapping and describing tephras and determining their stratigraphic relationships, (ii) characterizing tephras or cryptotephras in the laboratory, and (iii) dating them using a wide range of geochronological methods. Tephrochronology is also an important tool in volcanology, informing studies on volcanic petrology, volcano eruption histories and hazards, and volcano-climate forcing. Although limitations and challenges remain, multidisciplinary applications of tephrochronology continue to grow markedly.
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