shell loss rates in carbonate environments are greater as
a result of bioerosion and dissolution, which implies
greater compositional bias in the surviving skeletal material and leads to the taphonomic trade-off that shells in carbonate sediments show less time-averaging but greater
taxonomic bias. Similarly, other studies from Panamanian
and the Belize Barrier Reefs also demonstrated the high
level of shell damage and dissolution compared to shells
in other environments (Best, 2008; Hauser et al., 2009).
The results of these time-averaging studies demonstrate
that bioturbation-related selective shell burial favors shells
that remain burried through their early taphonomic history. Although buried shells may be brought back up to
the surface intermittently by bioturbation or physical
reworking (e.g., storms, currents), this exposure is often
only for short periods of time. This taphonomic model
explains the striking similarities in time-averaging among
different types of organisms and the lack of correlation
between time-since-death and shell taphonomy. Hence,
age estimates in these depositional settings are sensitive
to taxon choice and quantify a taxon-dependent bias in
shell longevity and death assemblage formation. Most
importantly, these conclusions of stratigraphic disorder
are not restricted to modern carbonate reefal sediments
as studies from other environmental settings, such as tidal
flats, etc. have demonstrated (e.g., Best, 2008; Flessa
et al., 1993; Tomasovych and Zuschin, 2009). In summary, greater understanding of biases imposed by bioturbation on preservation will ultimately be key to
understanding apparent contradictions in modern and past
sedimentary records (see also O’Leary et al., 2009).
Geochemical aspects of bioturbation
Vertical transport and surface sediment mixing mechanisms also profoundly influence biogeochemical processes, microbial communities and hence early diagensis
(e.g., Alongi, 1989; Berner, 1980; Pischedda et al.,
2008). In carbonate environments, dissolution of carbonate grains is highest in extensively bioturbated areas
(e.g., Aller, 1982; Callender et al., 2002) or very close to
the sediment-water interface (Tudhope and Risk, 1985)
where oxygen is abundant. Chemical dissolution of particles is accelerated by microboring algae and fungi, which
are abundant in coral reef environments. A dissolution
study from Davies Reef (Great Barrier Reef, Australia)
showed that molluscan shells lost 3% weight over 1 year.
Such rates equate to 350 g of dissolved CaCO 3 /m
2
lagoonal floor/year and represent 18–30% of the sediment
influx rate during the Holocene (Tudhope and Risk,
1985).
Bioturbation and bioirrigation (e.g., the exchange of
water masses) largely controls the penetration depth of
oxygen and organic material into the surface sediments,
whilst the consumption of oxygen is influenced by respiration of the benthic organisms as they oxidize organic
carbon. In contrast, anaerobic oxidation is almost exclusively mediated by bacterial activity (Berner, 1980). In
reef sediments of Davies Reef (GBR, Australia), sulfate
reduction accounted only for 5% of the total organic matter degradation within the top 12 cm with reduction rates
averaged 0.622 mmol sulfate m
2
/day (Nedwell and Blackburn, 1987). The importance of the biogenic dwellings
and structures in carbonate sediment environment lies in
the creation of three-dimensional mosaics of oxic/anoxic
interfaces in the sediments thus multiplying by several
times the volume of the oxygenated sediment (e.g.,
Kristensen, 2000). Several field and laboratory studies
showed that sediment reworking and burrowing activities
extended the depth of the oxidized zone (see, for example,
Krantzberg (1985) for summary) and are able to create
oxidized microenvironments below the aerobic zones
(e.g., Myers, 1977; Ziebis et al., 1996). The various bioturbation organisms in reefal environments have distinct
bioturbation behavior patterns, which create oxygen distribution heterogeneity. It has been shown that the gallery-builders produced greater spatial heterogeneity due
to their complex ventilated structures compared to the burrower species (Pischedda et al., 2008). Moreover, oxygen
distribution heterogeneity affects the diffusive oxygen
flux as organisms enhance the oxygen exchanges between
water and sediments (Ziebis et al., 1996). This outweighs
the reduced oxygen flux due to the physical presence of
organisms in the biogenic structures or the deposition of
mucus along the borrow walls by worms, etc., which
may act as a barrier to solute diffusion (Hannides et al.,
2005). Furthermore, the process of bioturbation and
bioirrigation also actively influences other conditions,
such as pH, nutrient status, ammonia, phosphorous,
nitrate, and metals contents (see Krantzberg (1985) for
summary). Alteration of the diffusive oxygen flux through
bioturbation processes by dwelling benthos, such as conveyor-belt feeders or the callianassid shrimps (Ziebis
et al., 1996), may also dramatically influence mineralization processes in sediments. Additionally, bioturbation
affects biogeochemistry including organic matter mineralization, nutrient and sulfur cycling as shown by a study
from the Philippines of alpheid shrimps Alpheus
macellarius (Holmer and Heilskov, 2008). There, high
sediment turnover rates by the shrimps stimulated the mineralization rate.
Summary and conclusion
Bioturbation refers to particle mixing within unconsolidated sediments through the activities of biological organisms most commonly at or close to the water-sediment
interface. In reefal ecosystems, the implications of this process go far beyond simply mixing the substrate as sediment
particle preservation, food availability, and geochemical
composition within the substrate are all affected, including
increasing the effective sediment-water interface that
enhanced chemical fluxes (i.e., oxygen, nutrients, sulfur
cycling, oxic and anoxic mineralization) between the
sediment and the water column. The effective or total
bioturbation, part of early diagenesis processes, largely
BIOTURBATION
161
a result of bioerosion and dissolution, which implies
greater compositional bias in the surviving skeletal material and leads to the taphonomic trade-off that shells in carbonate sediments show less time-averaging but greater
taxonomic bias. Similarly, other studies from Panamanian
and the Belize Barrier Reefs also demonstrated the high
level of shell damage and dissolution compared to shells
in other environments (Best, 2008; Hauser et al., 2009).
The results of these time-averaging studies demonstrate
that bioturbation-related selective shell burial favors shells
that remain burried through their early taphonomic history. Although buried shells may be brought back up to
the surface intermittently by bioturbation or physical
reworking (e.g., storms, currents), this exposure is often
only for short periods of time. This taphonomic model
explains the striking similarities in time-averaging among
different types of organisms and the lack of correlation
between time-since-death and shell taphonomy. Hence,
age estimates in these depositional settings are sensitive
to taxon choice and quantify a taxon-dependent bias in
shell longevity and death assemblage formation. Most
importantly, these conclusions of stratigraphic disorder
are not restricted to modern carbonate reefal sediments
as studies from other environmental settings, such as tidal
flats, etc. have demonstrated (e.g., Best, 2008; Flessa
et al., 1993; Tomasovych and Zuschin, 2009). In summary, greater understanding of biases imposed by bioturbation on preservation will ultimately be key to
understanding apparent contradictions in modern and past
sedimentary records (see also O’Leary et al., 2009).
Geochemical aspects of bioturbation
Vertical transport and surface sediment mixing mechanisms also profoundly influence biogeochemical processes, microbial communities and hence early diagensis
(e.g., Alongi, 1989; Berner, 1980; Pischedda et al.,
2008). In carbonate environments, dissolution of carbonate grains is highest in extensively bioturbated areas
(e.g., Aller, 1982; Callender et al., 2002) or very close to
the sediment-water interface (Tudhope and Risk, 1985)
where oxygen is abundant. Chemical dissolution of particles is accelerated by microboring algae and fungi, which
are abundant in coral reef environments. A dissolution
study from Davies Reef (Great Barrier Reef, Australia)
showed that molluscan shells lost 3% weight over 1 year.
Such rates equate to 350 g of dissolved CaCO 3 /m
2
lagoonal floor/year and represent 18–30% of the sediment
influx rate during the Holocene (Tudhope and Risk,
1985).
Bioturbation and bioirrigation (e.g., the exchange of
water masses) largely controls the penetration depth of
oxygen and organic material into the surface sediments,
whilst the consumption of oxygen is influenced by respiration of the benthic organisms as they oxidize organic
carbon. In contrast, anaerobic oxidation is almost exclusively mediated by bacterial activity (Berner, 1980). In
reef sediments of Davies Reef (GBR, Australia), sulfate
reduction accounted only for 5% of the total organic matter degradation within the top 12 cm with reduction rates
averaged 0.622 mmol sulfate m
2
/day (Nedwell and Blackburn, 1987). The importance of the biogenic dwellings
and structures in carbonate sediment environment lies in
the creation of three-dimensional mosaics of oxic/anoxic
interfaces in the sediments thus multiplying by several
times the volume of the oxygenated sediment (e.g.,
Kristensen, 2000). Several field and laboratory studies
showed that sediment reworking and burrowing activities
extended the depth of the oxidized zone (see, for example,
Krantzberg (1985) for summary) and are able to create
oxidized microenvironments below the aerobic zones
(e.g., Myers, 1977; Ziebis et al., 1996). The various bioturbation organisms in reefal environments have distinct
bioturbation behavior patterns, which create oxygen distribution heterogeneity. It has been shown that the gallery-builders produced greater spatial heterogeneity due
to their complex ventilated structures compared to the burrower species (Pischedda et al., 2008). Moreover, oxygen
distribution heterogeneity affects the diffusive oxygen
flux as organisms enhance the oxygen exchanges between
water and sediments (Ziebis et al., 1996). This outweighs
the reduced oxygen flux due to the physical presence of
organisms in the biogenic structures or the deposition of
mucus along the borrow walls by worms, etc., which
may act as a barrier to solute diffusion (Hannides et al.,
2005). Furthermore, the process of bioturbation and
bioirrigation also actively influences other conditions,
such as pH, nutrient status, ammonia, phosphorous,
nitrate, and metals contents (see Krantzberg (1985) for
summary). Alteration of the diffusive oxygen flux through
bioturbation processes by dwelling benthos, such as conveyor-belt feeders or the callianassid shrimps (Ziebis
et al., 1996), may also dramatically influence mineralization processes in sediments. Additionally, bioturbation
affects biogeochemistry including organic matter mineralization, nutrient and sulfur cycling as shown by a study
from the Philippines of alpheid shrimps Alpheus
macellarius (Holmer and Heilskov, 2008). There, high
sediment turnover rates by the shrimps stimulated the mineralization rate.
Summary and conclusion
Bioturbation refers to particle mixing within unconsolidated sediments through the activities of biological organisms most commonly at or close to the water-sediment
interface. In reefal ecosystems, the implications of this process go far beyond simply mixing the substrate as sediment
particle preservation, food availability, and geochemical
composition within the substrate are all affected, including
increasing the effective sediment-water interface that
enhanced chemical fluxes (i.e., oxygen, nutrients, sulfur
cycling, oxic and anoxic mineralization) between the
sediment and the water column. The effective or total
bioturbation, part of early diagenesis processes, largely
BIOTURBATION
161