depend on the structural complexity derived from coral
skeletons, and the ecological condition of coral reefs is,
therefore, a direct function of the physiological health of
hard corals. Hard corals are highly competitive in lownutrient environments, for three reasons. First, they are
remarkably efficient in internally recycling nutrients
between host and zooxanthellae. Second, they occupy
most trophic levels simultaneously (Houlbreque and
Ferrier-Pages, 2009): the photosynthesis of the zooxanthellae makes them efficient phototrophs; they can absorb
dissolved nutrients, graze on large phytoplankton, prey
upon zooplankton, and feed on detritus and other
decompositional material (Rosenfeld et al., 1999). Third,
some species of hard coral can rapidly adapt to varying
light and food availability, maximizing energy gains
throughout their lifetime (Anthony and Fabricius, 2000).
Despite the high adaptability of corals to a range of environmental conditions, reports of coral reef degradation
from eutrophication exist from many places around the
world (reviewed in Fabricius, 2005). However, the natural
variability in background conditions and the paucity of
historical data make it often difficult to ascertain causal
relationships between eutrophication and reef degradation. Furthermore, other disturbances (e.g., overfishing,
coral bleaching, storms, and floods) complicate the assessments. Epidemiological tools originally developed to
assess the weight of evidence that smoking causes lung
cancer (U.S. Department of Health, 1964) have now been
applied to coral reef studies to create a causal link between
reef degradation and increased exposure to nutrient pollution in the central Great Barrier Reef (Fabricius and
De’ath, 2004).
Eutrophication degrades coral reefs through three pathways (a) trophic changes from the increased availability of
nutrients and organic matter; (b) decreasing light availability in deeper water; and (c) altered sediment properties. The following sections briefly review the available
information on how these three pathways, alone and in
combination, directly and indirectly affect corals, other
reef-associated organisms, and the ecological balances of
coral reef ecosystems.
Effects of the increased availability of nutrients and
organic matter
Eutrophication increases the availability of nutrients and
organic matter both in the water and in the sediments.
Dissolved and particulate and organic and inorganic nutrients are often treated separately, as their biological effects
differ fundamentally. For example, dissolved inorganic
nutrients such as phosphate, nitrate, and ammonium are
highly bioavailable and therefore get quickly depleted,
whereas many forms of dissolved organic nutrients are
largely unusable as food even for bacteria and therefore
often accumulate to high concentrations. However,
cycling between the different forms of nutrients is fast
and complex, due to uptake, excretion, and decomposition
in benthic and pelagic food webs that ensure continuous
conversions between dissolved and particulate and
between organic and inorganic forms of nutrients.
Studies of eutrophication effects on corals have often
focused on enrichment with dissolved inorganic nutrients
(e.g., Stambler et al., 1994; Dubinsky and Stambler, 1996;
Koop et al., 2001; Szmant, 2002). Exposure to dissolved
inorganic nitrogen may lead to declining calcification,
higher concentrations of photopigments (affecting the
energy and nutrient transfer between zooxanthellae and
host; Marubini and Davies, 1996), and higher rates of
coral diseases (Bruno et al., 2003). In areas of nutrient
upwelling or in heavily polluted locations, chronically
increased levels of dissolved inorganic nutrients may alter
coral physiology and calcification, causing noticeable
changes in coral communities (Birkeland, 1997). However, although high levels of dissolved inorganic nitrogen
and phosphorus can cause significant physiological
changes in corals, they do not kill or greatly harm individual coral colonies (reviewed in Fabricius, 2005). Furthermore, biological uptake by bacteria, phytoplankton, and
the benthos rapidly convert dissolved inorganic nutrients
into particulate organic matter (especially detritus, bacteria, phytoplankton, and marine snow), hence their concentrations in the water column are often low even in areas of
eutrophication.
The main pathway how dissolved inorganic nutrients
affect coral reefs is by organic enrichment of suspended
particulate matter and sediments. Pelagic particulate
organic matter is often measured using chlorophyll, total
suspended solids, and/or particulate nitrogen and phosphorus as proxies. Particulate organic matter may alter
benthic irradiance, may organically enrich sediments,
and may lead to hypoxia in sediments. These secondary
effects are, additionally to nutrient enrichment, significant
eutrophication effects. Particulate organic matter is used
by corals as food, and their tissue thickness, photosynthetic pigment concentrations, and calcification increase
in response to feeding on particulate organic matter. At
moderate levels of eutrophication, some hard coral species
can compensate for lost photosynthetic carbon gains by
increasing particle feeding, while other species become
saturated at low particle concentrations and are unable to
compensate for light loss (Anthony and Fabricius, 2000).
At even higher levels of eutrophication, gross photosynthesis and respiration, tissue thickness, and calcification
start to decline in all species as light attenuation outweighs
further energy gains from particle feeding. Photosynthesis, tissue thickness, and calcification therefore change in
a modal fashion along eutrophication gradients (Tomascik
and Sander, 1985; Marubini and Davies, 1996). In contrast, photosynthetic pigment concentrations in corals further increase with increasing eutrophication, and have,
therefore, been suggested as a useful measure for eutrophication (Marubini, 1996; Cooper et al., 2009).
While corals are not directly harmed by dissolved inorganic nutrients and, within bounds, benefit from particulate organic matter, both macroalgae and heterotrophic
filter feeders greatly benefit from dissolved inorganic
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NUTRIENT POLLUTION/EUTROPHICATION
skeletons, and the ecological condition of coral reefs is,
therefore, a direct function of the physiological health of
hard corals. Hard corals are highly competitive in lownutrient environments, for three reasons. First, they are
remarkably efficient in internally recycling nutrients
between host and zooxanthellae. Second, they occupy
most trophic levels simultaneously (Houlbreque and
Ferrier-Pages, 2009): the photosynthesis of the zooxanthellae makes them efficient phototrophs; they can absorb
dissolved nutrients, graze on large phytoplankton, prey
upon zooplankton, and feed on detritus and other
decompositional material (Rosenfeld et al., 1999). Third,
some species of hard coral can rapidly adapt to varying
light and food availability, maximizing energy gains
throughout their lifetime (Anthony and Fabricius, 2000).
Despite the high adaptability of corals to a range of environmental conditions, reports of coral reef degradation
from eutrophication exist from many places around the
world (reviewed in Fabricius, 2005). However, the natural
variability in background conditions and the paucity of
historical data make it often difficult to ascertain causal
relationships between eutrophication and reef degradation. Furthermore, other disturbances (e.g., overfishing,
coral bleaching, storms, and floods) complicate the assessments. Epidemiological tools originally developed to
assess the weight of evidence that smoking causes lung
cancer (U.S. Department of Health, 1964) have now been
applied to coral reef studies to create a causal link between
reef degradation and increased exposure to nutrient pollution in the central Great Barrier Reef (Fabricius and
De’ath, 2004).
Eutrophication degrades coral reefs through three pathways (a) trophic changes from the increased availability of
nutrients and organic matter; (b) decreasing light availability in deeper water; and (c) altered sediment properties. The following sections briefly review the available
information on how these three pathways, alone and in
combination, directly and indirectly affect corals, other
reef-associated organisms, and the ecological balances of
coral reef ecosystems.
Effects of the increased availability of nutrients and
organic matter
Eutrophication increases the availability of nutrients and
organic matter both in the water and in the sediments.
Dissolved and particulate and organic and inorganic nutrients are often treated separately, as their biological effects
differ fundamentally. For example, dissolved inorganic
nutrients such as phosphate, nitrate, and ammonium are
highly bioavailable and therefore get quickly depleted,
whereas many forms of dissolved organic nutrients are
largely unusable as food even for bacteria and therefore
often accumulate to high concentrations. However,
cycling between the different forms of nutrients is fast
and complex, due to uptake, excretion, and decomposition
in benthic and pelagic food webs that ensure continuous
conversions between dissolved and particulate and
between organic and inorganic forms of nutrients.
Studies of eutrophication effects on corals have often
focused on enrichment with dissolved inorganic nutrients
(e.g., Stambler et al., 1994; Dubinsky and Stambler, 1996;
Koop et al., 2001; Szmant, 2002). Exposure to dissolved
inorganic nitrogen may lead to declining calcification,
higher concentrations of photopigments (affecting the
energy and nutrient transfer between zooxanthellae and
host; Marubini and Davies, 1996), and higher rates of
coral diseases (Bruno et al., 2003). In areas of nutrient
upwelling or in heavily polluted locations, chronically
increased levels of dissolved inorganic nutrients may alter
coral physiology and calcification, causing noticeable
changes in coral communities (Birkeland, 1997). However, although high levels of dissolved inorganic nitrogen
and phosphorus can cause significant physiological
changes in corals, they do not kill or greatly harm individual coral colonies (reviewed in Fabricius, 2005). Furthermore, biological uptake by bacteria, phytoplankton, and
the benthos rapidly convert dissolved inorganic nutrients
into particulate organic matter (especially detritus, bacteria, phytoplankton, and marine snow), hence their concentrations in the water column are often low even in areas of
eutrophication.
The main pathway how dissolved inorganic nutrients
affect coral reefs is by organic enrichment of suspended
particulate matter and sediments. Pelagic particulate
organic matter is often measured using chlorophyll, total
suspended solids, and/or particulate nitrogen and phosphorus as proxies. Particulate organic matter may alter
benthic irradiance, may organically enrich sediments,
and may lead to hypoxia in sediments. These secondary
effects are, additionally to nutrient enrichment, significant
eutrophication effects. Particulate organic matter is used
by corals as food, and their tissue thickness, photosynthetic pigment concentrations, and calcification increase
in response to feeding on particulate organic matter. At
moderate levels of eutrophication, some hard coral species
can compensate for lost photosynthetic carbon gains by
increasing particle feeding, while other species become
saturated at low particle concentrations and are unable to
compensate for light loss (Anthony and Fabricius, 2000).
At even higher levels of eutrophication, gross photosynthesis and respiration, tissue thickness, and calcification
start to decline in all species as light attenuation outweighs
further energy gains from particle feeding. Photosynthesis, tissue thickness, and calcification therefore change in
a modal fashion along eutrophication gradients (Tomascik
and Sander, 1985; Marubini and Davies, 1996). In contrast, photosynthetic pigment concentrations in corals further increase with increasing eutrophication, and have,
therefore, been suggested as a useful measure for eutrophication (Marubini, 1996; Cooper et al., 2009).
While corals are not directly harmed by dissolved inorganic nutrients and, within bounds, benefit from particulate organic matter, both macroalgae and heterotrophic
filter feeders greatly benefit from dissolved inorganic
724
NUTRIENT POLLUTION/EUTROPHICATION