BIOTURBATION
D. H. Shull, Western Washington University,
Bellingham, WA, USA
& 2009 Elsevier Ltd. All rights reserved.
Introduction
Activities of organisms inhabiting seafloor sediments
(termed benthic infauna) are concealed from visual
observation but their effects on sediment chemical and
physical properties are nevertheless apparent. Sediment ingestion, the construction of pits, mounds, fecal
pellets, and burrows, and the ventilation of subsurface
burrows with overlying water significantly alter rates
of chemical reactions and sediment–water exchange,
destroy signals of stratigraphic tracers, bury reactive
organic matter, exhume buried chemical contaminants, and change sediment physical properties such
as grain size, porosity, and permeability. Biogenic
sediment reworking resulting in a detectable change in
sediment physical and chemical properties is termed
bioturbation. It is critical to account for bioturbation
when calculating chemical fluxes at the sediment–
water interface and when interpreting chemical profiles in sediments. In the narrowest sense, bioturbation
refers to the biogenic transport of particles that destroys stratigraphic signals. In the broader sense it can
refer to biogenic transport of pore water and changes
in sediment physical properties due to organism
activities as well. Bioturbation and its effects on sediment chemistry and stratigraphy is a natural consequence of adaptation by organisms to living and
foraging in sediments.
Particle Bioturbation
Deposit feeding, the ingestion of particles comprising
sedimentary deposits, is the dominant feeding strategy in muddy sediments. In fact, since the vast majority of the ocean is underlain by muddy sediments,
deposit feeding is the dominant feeding strategy on
the majority of the Earth’s surface. Because digestible
organic matter typically comprises less than 1% of
sediments by mass, to meet their metabolic needs
deposit feeders exhibit rapid sediment ingestion
rates, averaging roughly three body weights per day.
Deposit feeders adapted to living in sediments with
relatively low organic matter concentrations tend to
exhibit elevated ingestion rates; there is no free lunch
even for deposit feeders. Rates of deposit feeding of
individual organisms increase with increasing body
size so that bioturbation rates in some sedimentary
deposits may be controlled by a handful of larger
species. Deposit feeders employ a wide variety of
strategies to collect particles for food, but reworking
modes due to deposit feeding can be broken down
into the following categories: conveyor-belt feeding
where particles are collected at depth and deposited
at the sediment surface; subductive feeding, where
particles are collected at or near the sediment surface
and deposited at depth; and interior feeding where
particles are collected and deposited within the
sediment column. These feeding modes transport
particles the length of the organism’s body or the
length of its burrow. Some species of deposit feeders
also ingest and egest sediment near the sediment
surface, resulting in horizontal movement of particles but limited vertical displacement. Due to rapid
particle ingestion rates and relatively large horizontal
and vertical transport distances, deposit feeding is
considered to be the primary agent of bioturbation.
Benthic organisms also rework sediments through
burrow formation. Muddy sediments behave more
like elastic solids than granular material. A benthic
burrower in muddy sediments uses its burrowing
apparatus (bivalve foot, polychaete proboscis, amphipod carapace, or other burrowing tool) like a
wedge to create and propagate cracks in sediments.
After an organism passes through a crack, sediments
tend to rebound viscoelastically resulting in relatively
little net movement of particles compared to deposit
feeding. An exception to this generality is burrowing
by large epibenthic predators including skates, rays,
and benthic-feeding marine mammals such as gray
whales and walrus, which can cause extensive reworking in sediment patches where they are feeding.
From a particle’s perspective, bioturbation consists
of relatively short-lived intervals of particle movement due to deposit feeding or burrowing interspersed by relatively long periods during which the
particles remain at rest. When particles pass through
animal guts, in addition to changing location, the
particles may be aggregated into fecal pellets (particles surrounded by or embedded in mucopolymers).
When constructing burrows, some infauna produce
mucopolymer glue to form sturdy burrow walls,
locking particles into place for an extended period of
time. Transport of subsurface particles to the sediment surface by conveyor-belt feeding results in
downward gravitative movement of particles within
the sediment column as subsurface feeding voids are
395
396
BIOTURBATION
filled with sediment from above. Within a particular
sedimentary habitat many particle reworking mechanisms occur simultaneously.
There are many ways to quantify mathematically
the ensemble of particle motions that results in
bioturbation. Traditionally, bioturbation has been
modeled as though it were analogous to diffusion.
This means that the collection of particle motions
resembles a large number of small random displacements. Under these assumptions, bioturbation
is included in the general diagenetic equation as a
biodiffusion coefficient, DB. Ignoring vertical gradients in porosity and sediment compaction, the rate of
change of a chemical tracer, C, in the vertical spatial
dimension, x, can be represented as follows:
@C
@2C
@C X
¼ DB 2 u
þ
R;
@t
@x
@x
xoL
½1
where DB is the biodiffusion coefficient (cm2 yr 1),
u is the sediment accumulation rate (cm yr 1), and
P
R represents the sum of chemical reactions. In the
absence of specific information on bioturbation
mechanisms, it is often assumed that DB is constant
throughout the reworked layer to the depth L. Below
the depth L, DB is zero. The advantage of this
formulation is that all the various particle reworking
processes are quantified by one parameter, DB.
The nondimensional Peclet number, Pe ¼ uLDB 1 ,
quantifies the relative importance of bioturbation
and sediment accumulation in determining the profile of C within the reworked layer. Values of Pe less
than 1 indicate a strong influence of bioturbation.
Table 1 summarizes the general pattern of variation
in DB, u, L, and Pe among benthic provinces at
different water depths. The depth of the reworked
layer, L, shows little systematic variation among
habitats, averaging 10 cm. Although we would expect considerable variation in Pe, the low values in
each province indicate that bioturbation is generally
important throughout the ocean. An easy-to-
Table 1 Variation in the biodiffusion coefficient, DB, sedimentation rate, u, and the Peclet number, Pe, characteristic of
different benthic environments. A Peclet number greater than 1
indicates sediment accumulation is more important than
bioturbation
DB
Shallow water
Cont. Shelf
Slope
Deep sea
10
0.1
0.05
0.01
u
100
10
1
0.5
0.1
0.01
0.001
0.0001
L
1
0.5
0.05
0.01
10
10
10
10
Pe
0.01
0.01
0.01
0.002
1
50
10
10
A Peclet number less than 1 indicates that bioturbation is more
important for transport relative to sedimentation.
remember rule of thumb regarding bioturbation rates
is that DB varies from c. 0.01 to 100 cm2 yr 1 from
deep-sea to shallow-water depths. This variation is
correlated with increased abundance of infauna,
greater rates of food supply, and (with the exception
of polar regions) elevated average bottom-water
temperatures with decreasing water depth.
Because bioturbation mechanisms can transport
particles relatively large distances, roughly the length
of the reworked zone, L, and because particle trajectories are often nonrandom, the biodiffusion coefficient is not appropriate for modeling the effects of
bioturbation on transport of some tracers. A more
general model of particle mixing that includes
longer-distance, nonrandom particle trajectories is
the nonlocal bioturbation model. Again neglecting
variation in porosity:
@C
¼
@t
ZL
Kðx0 ; x; tÞCðx0 Þdx
0
CðxÞ
ZL
@C X
þ
R ½2
Kðx; x0 ; tÞdx0 u
@x
0
where K is the exchange function (dimensions:
time 1) that quantifies the rate of particle movement
from one depth, x, to any other depth, x0 . The first
term on the right-hand side gives the concentration
change at depth x due to the delivery of a particle
tracer from other depths, x0 . The second term gives
the concentration change at depth x due to transport
of a tracer from depth x to other depths x0 . The other
terms are defined as in eqn [1]. The exchange function, K, can potentially quantify a complex ensemble
of bioturbation mechanisms. Analogs of eqn [2] that
rely on discrete mathematics exist. In one dimension,
nonlocal transport can be modeled as a transition
matrix in which the rows of the transition matrix
correspond to depths in the sediment and the matrix
elements quantify the probability of transport of
a tracer among depths. Multiple-dimensional automaton models can simulate complex modes of
particle transport in both vertical and horizontal
dimensions. These more complex models can better
capture the complexities of bioturbation but sacrifice
the one-parameter simplicity of eqn [1].
There are two common approaches for determining
the values of the bioturbation parameters in these
models. Mixing parameters can be estimated from
direct measurements of deposit-feeder ingestion rates
and organism burrowing rates. More often, these
parameters are estimated by measuring sedimentbound tracers with known inputs to the sediment and
BIOTURBATION
P
known reaction rates ( R). Mixing parameters are
then calculated by fitting measured tracer profiles to
profiles calculated by use of the appropriate mathematical model. Useful bioturbation tracers include
excess activities of naturally occurring particlereactive radionuclides such as 234Th, 210Pb, or 7Be.
These radionuclides have a relatively continuous
source either from the atmosphere or from the overlying water column, are rapidly scavenged onto particles, and sink to the seafloor (see Sediment
Chronologies). In addition, chlorophyll a, artificial
tracers added to the sediment surface as an impulse
such as glass beads or fluorescent luminophores, or
other exotic identifiable material with a known rate of
input are used as tracers of bioturbation. The profile
of excess 210Pb in Figure 1 illustrates several effects
of bioturbation on a tracer profile. The rate of
bioturbation in the top 6 cm is rapid enough to
completely mix excess 210Pb within this layer. The
subsurface peak at 15–16 cm indicates subsurface
deposition of surficial material. Below 16 cm, the
slope of the profile is set by the rate of sediment accumulation and radioactive decay of 210Pb.
Bioturbation has important consequences for
sediment stratigraphy, chemistry, and biology. Bioturbation can homogenize tracers within the reworked layer (Figure 1). Bioturbation acts as a
low-pass filter, destroying information deposited on
short timescales, but preserving longer-term trends.
Bioturbation makes it generally difficult or impossible to resolve timescales of less than 103 years
stratigraphically in deep-sea sediment cores. If the
bioturbation mechanism is not known, it is difficult
to separate changes in the input signal from changes
due to mixing (Figure 2). If mixing is not complete,
and the bioturbation mechanism is known, it may be
possible to deconvolve the input signal to the stratigraphic record, although detailed information will be
lost. If bioturbation in the surface reworked zone
completely homogenizes a tracer, then knowing the
mixing mechanism is unimportant. Once pancake
batter is thoroughly mixed, for example, it no longer
contains information on how the mixing was
performed.
Bioturbation has important consequences for
sediment geochemistry. Bioturbation buries reactive
organic matter. Subductive deposit feeders selectively
feed on organic-rich particles near the sediment surface and deposit them at depth, perhaps as food
caches. In the presence of horizontal transport of
organic matter, or suspension-feeding benthos that
locally enhance organic matter deposition through
biodeposit formation, bioturbation can greatly
enhance the organic matter inventory in sediments.
Burial of organic matter exposes it to different
oxidants, changing the degradation pathway. In
particular, reworking of Mn and Fe oxides cycles
them between oxidative and reducing environments,
Excess 210 Pb (dpm g−1)
0
5
10
397
Tracer concentration
15
0
0
0.2
0.4
0.6
0.8
1
0
Well-mixed surface layer
5
5
15
10
Subduction of
surficial 210 Pb
20
Sediment accumulation
below reworked layer
Depth (cm)
Depth (cm)
10
15
20
25
25
30
30
Figure 1 Excess 210Pb activity vs. depth in a sediment core
from Narragansett Bay, Rhode Island. Data with permission from
Shull DH (2001) Transition-matrix model of bioturbation and
radionuclide diagenesis. Limnology and Oceanography 46(4):
905–916. Copyright (2001) by the American Society of Limnology
and Oceanography, Inc.
Figure 2 Changes in the profile of a hypothetical conservative
tracer present initially as two narrow subsurface peaks, as
predicted from eqn [1]. DB ¼ 0.1 cm2 yr 1, u ¼ 0.1 cm yr 1,
L ¼ 10 cm. Solid line: tracer profile at t ¼ 0. Dotted line:
t ¼ 25 years. Dashed line: t ¼ 150 years.
398
BIOTURBATION
resulting in enhanced anaerobic degradation of organic matter.
Bioturbation changes sediment properties as well.
Pelletization changes the sediment grain size distribution. Furthermore, bioturbation rates are particlesize-dependent. Size-selective feeding by deposit
feeders results in biogenic graded bedding with lag
layers of large sediment particles either at the sediment surface or at depth, depending upon the bioturbation mechanism. Formation of pellets and
burrows increases sediment porosity, counteracting
the effects of sediment compaction. Sediment surface
manifestations of bioturbation such as pits, mounds,
and tubes alter seafloor roughness and flow characteristics of the benthic boundary layer, roughly
doubling the drag compared to a hydrodynamically
smooth bed.
Pore-Water Bioirrigation
Most benthic infauna maintain a burrow that connects to the sediment–water interface to facilitate
respiration, feeding, defecation, and other metabolic
processes. These burrows exist in a range of geometries including vertical cylinders, U- or J-shaped
tubes, or branching networks. In deep-sea sediments,
dissolved oxygen can penetrate 30 m into the sediment. Near the shore, however, oxygen penetration
is quite variable and in muddy sediments it often
penetrates no farther than a few millimeters. To meet
their metabolic requirements for oxygen, infauna
ventilate their burrows by thrashing their bodies,
flapping their appendages, by peristalsis, by beating
cilia, or by oscillating like pistons in their tubes.
These ventilation mechanisms result in intermittent
burrow flushing, which exchanges a portion of the
fluid inside the burrow with overlying water. In this
way, organisms in the sediment can flush out metabolic wastes and toxins such as hydrogen sulfide that
have accumulated in their burrows and they can restock the burrow water with dissolved oxygen. Observations of organisms in artificial tubes maintained
in the laboratory indicate that burrow ventilation is
episodic, with ventilation frequencies ranging from
once per hour to 10 or more ventilation events per
hour. Deposit-feeding infauna generally ventilate less
frequently than suspension-feeding infauna, which
pump water through their burrows for both respiration and food capture.
The sediments into which these burrows are built
are mixtures of particles and interconnected pore
water. Surficial sediments may possess porosities
(defined as the volume of interconnected pore water
per unit volume of sediment) in excess of 90%. Thus,
surface sediments generally contain more pore water
than particles. The rate of molecular diffusion of
solutes through pore water is reduced relative to
diffusion in a free solution because the solutes must
follow a winding path through the particles, called
sediment tortuousity. Particle bioturbation mechanisms redistribute this pore water along with the
particles, but since rates of pore-water transport,
inferred from dissolved tracer distributions, are
typically an order of magnitude higher than rates of
particle bioturbation, particle reworking is a relatively unimportant mechanism for transporting pore
water. Rather, burrow ventilation seems to be the
most important biogenic mechanism of pore-water
transport. The consequences of burrow ventilation
on pore-water transport in the surrounding sediments (termed bioirrigation) depend upon sediment
permeability.
Sandy sediment typically possesses high enough
permeability to allow advective flow of pore water
through the interconnected pore space surrounding
sediment particles. Under these conditions, the
pressure head within a burrow created by burrow
ventilation activities can drive pore-water flow from
the burrow into surrounding sediments. The velocity
of this flow can be calculated using Darcy’s law:
k
ud ¼ ðrP rgrxÞ
m
½3
where ud is the Darcy velocity, k is sediment permeability, m is the dynamic viscosity of pore water, P
is pressure, r is the pore-water density, g is gravity,
and r is a gradient operator (e.g., @/@x, @/@y). The
velocity of pore water, u, is related to the Darcy
velocity, ud ¼ uj 1, where j ¼ porosity. Substituting
eqn [3] into the general diagenetic equation gives the
expected change in concentration of a pore-water
tracer subjected to an advection velocity driven by
burrow ventilation, molecular diffusion, and chemical reactions:
@C
@2C
@C X
¼ D0M 2 u
þ
R;
@t
@x
@x
xoL
½4
where D0 M is the molecular diffusion coefficient,
corrected for tortuousity.
In contrast to sandy sediments, permeability of
mud is generally too low to permit significant porewater advection so that u ¼ 0. Thus, pore-water
transport in muddy sediments is dominated by molecular diffusion. Burrow ventilation in muddy
sediments enhances pore-water transport by changing the diffusive geometry. Figure 3 shows the
geometry of idealized equally spaced vertical
BIOTURBATION
(a)
(b)
399
(c)
r
x
Figure 3 Idealized burrow geometry underlying eqn [5]. (a) Burrows as close-packed cylinders. (b) Rectangular plane intersecting
an average burrow microenvironment. (c) The x r domain of eqn [5]. The shaded rectangle represents the burrow, while the
unshaded rectangle represents the surrounding sediment. Reproduced from Aller RC (1980) Quantifying solute distributions in
the bioturbated zone of marine sediments by defining an average microenvironment. Geochimica et Cosmochimica Acta 44(12):
1955–1965, with permission from Elsevier.
burrows embedded into sediment. If these burrows
were rapidly flushed so that the solute concentration
within the burrows were equal to the solute concentration in the overlying water, then the corresponding diagenetic equation governing pore-water
transport in the vertical dimension, x, and in the
radial dimension, r, would be given by
½5
The diffusion operator within the parentheses is
similar to the diffusion operator in eqn [4], but
quantifies molecular diffusion in both the x and r
dimensions. A one-dimensional diagenetic model
that incorporates the effects of bioirrigation on porewater transport can be derived from eqn [5]:
X
@C
@2C
¼ D0M 2 aðC C0 Þ þ
R
@t
@x
1
0
0
0.05
activity (dpm ml−1)
0.1
0.15
0.2
0.25
5
Depth (cm)
2
X
@C
@ C 1 @ @C
0
¼ DM
r
þ
þ
R
@t
@x2
r @r @r
222 Rn
10
15
Measured 222 Rn activity
20
Supported 222 Rn activity
Nonlocal model solution
½6
where a(day ) is the coefficient of nonlocal bioirrigation, and C0 is the concentration of the solute
tracer in overlying water. The nonlocal bioirrigation
coefficient, a, in eqn [6] treats bioirrigation as both a
source and a sink for solutes at depth.
The value of the bioirrigation exchange rate, a, is
usually determined by measuring dissolved porewater tracers with known inputs and reaction kinetics. The most commonly used radionuclide tracer
of bioirrigation is 222Rn. Produced within sediments
from the decay of its parent 226Ra, 222Rn is a soluble
noble gas. Pore-water exchange with overlying water
results in lower 222Rn activity in sediment pore
waters than would be expected, compared to the
activity of its parent 226Ra. The shape of the 222Rn
profile and the magnitude of the 222Rn deficit relative
to 226Ra are used to determine rates of bioirrigation
25
Figure 4 Measured 222Rn activity and supported 222Rn activity
(produced from the decay of 226Ra within sediment particles) vs.
depth in a sediment core from Boston Harbor, Massachusetts.
Horizontal error bars represent standard error from three
replicate cores. The bioirrigation rate, a (day 1), was modeled
as the exponential function. a ¼ 3.8e x, and the modeled profile
was calculated from eqn [6]. Data from Shull DH, previously
unpublished.
(Figure 4). Other tracers of pore-water exchange
include inert solutes such as bromide or dissolved
nutrients such as ammonium, nitrate, or silicate, if
reaction kinetics can be estimated.
Bioirrigation has important implications for sediment geochemistry. Bioirrigation accelerates sediment–
water fluxes, changes rates of elemental cycling,
catalyzes oxidation reactions in the sediment, changes
vertical and horizontal gradients of pore-water solutes,
elevates levels of dissolved oxygen, and reduces
400
BIOTURBATION
exposure of organisms to metabolic wastes. By changing the redox geometry of sediments, bioirrigation
can significantly alter rates of redox-sensitive reactions
that occur in sediments such as nitrification, denitrification, sulfate reduction, and mercury methylation.
influenced subsequent development of animal body
plans during the Cambrian. Bioturbation also made a
new food resource, buried organic matter, accessible
to deposit feeders while radically changing the geochemistry of the seafloor.
Bioturbation and the Ecology and
Evolution of Benthic Communities
See also
Bioturbation has numerous effects on benthic community structure. In muddy sediments, bioturbation
by deposit feeders appears to reduce densities of
suspension feeders. Conveyor-belt bioturbation can
displace surface-dwelling benthos. Bioturbation
changes the depth distribution of organic matter and
can increase the inventory and quality of food for
deposit feeders in sediments. It can increase nutrient
fluxes leading to elevated rates of benthic primary
production and increased microbial productivity as
well. Furthermore, elevated nutrient recycling between sediments and overlying water helps to
maintain water-column productivity in estuaries and
other shallow-water marine environments.
Marine benthic habitats of the late Neoproterozoic and early Phanerozoic (600–500 Ma) were very
different from benthic habitats that existed later.
Seafloors at this time were characterized by welldeveloped microbial mats, as suggested by studies of
sedimentary fabric preserved in the geologic record.
These extensive microbial mats and associated seafloor fauna, such as immobile suspension-feeding
helicopacoid echinoderms, became scarce or extinct
in the Cambrian. The substantial change that occurred in seafloor communities around this time,
termed the ‘Cambrian substrate revolution’, is
thought to be caused by the development of bioturbation. It is hypothesized that the emergence of
both bioturbation and predation around this time
led to the extinction of nonburrowing taxa and
Macrobenthos. Ocean Margin Sediments. Sediment
Chronologies. Sedimentary Record, Reconstruction
of Productivity from the. Uranium-Thorium Decay
Series in the Oceans Overview. Uranium-Thorium
Series Isotopes in Ocean Profiles.
Further Reading
Aller RC (1980) Quantifying solute distributions in the
bioturbated zone of marine sediments by defining an
average microenvironment. Geochimica et Cosmochimica Acta 44(12): 1955--1965.
Aller RC (1982) The effects of macrobenthos on chemical
properties of marine sediments and overlying waters.
In: McCall PL and Tevesz MJS (eds.) Animal–Sediment
Relations, pp. 53--102. New York: Plenum.
Boudreau BP and Jorgensen BB (2001) The Benthic
Boundary Layer: Transport Processes and Biogeochemistry. Oxford, UK: Oxford University Press.
Dorgan KM, Jumars PA, Johnson BD, Boudreau BP, and
Landis E (2005) Burrowing by crack propagation:
Efficient locomotion through muddy sediments. Nature
433: 475.
Lohrer AM, Thrush SF, and Gibbs MM (2004) Bioturbators
enhance ecosystem function through complex biogeochemical interactions. Nature 431: 1092--1095.
Meysman F, Boudreau BP, and Middelburg JJ (2003)
Relations between local, non-local, discrete and
continuous models of bioturbation. Journal of Marine
Research 61: 391--410.
Shull DH (2001) Transition-matrix model of bioturbation
and radionuclide diagenesis. Limnology and Oceanography 46(4): 905--916.