and particulate organic nutrients, more than corals do.
Macroalgae use photosynthesis to obtain carbon and meet
their nutrient demand through uptake of dissolved inorganic nutrients, plus, in some species, through demineralization of particulate organic matter deposited on their
fronds (Schaffelke, 1999). In the absence of control by
herbivores, some groups of macroalgae are nutrient limited and increase in growth and biomass at minute
increases in dissolved inorganic nutrients and particulate
organic matter (Littler and Littler, 2007). Similar to the
widely observed symptoms of eutrophication in other
aquatic ecosystem, macroalgae dominate coral reefs with
high nutrient availability, including in areas of eutrophication (Smith et al., 1981; Lapointe et al., 2004; Lapointe
and Bedford, 2007). Long-term data have shown that
expanding (Cuet et al., 1988) or declining (Smith et al.,
1981) macroalgal cover coincides with increasing and
declining nutrient availability, respectively. These time
series data indicate a causal link between macroalgal
abundances and nutrient availability. On the Great Barrier
Reef, total macroalgal cover increases 5-fold from highest
to lowest water clarity and additionally 1.4-fold from lowest to highest chlorophyll, 3.3-fold from offshore to
inshore, and 3.1-fold from northern to southern reefs
(De’ath and Fabricius, 2010). Macroalgae also tend to
flourish in areas of nutrient upwelling, on eastern sides
of continents or large islands where more rivers originate
than in the west (Birkeland, 1988), and towards higher latitudes, as do nutrient concentrations (Johannes et al.,
1983). These large-scale geographic data all add evidence
that nutrient levels influence macroalgal biomass. However, increases in macroalgal biomass are only observed
in areas where grazing by herbivorous fishes or invertebrates is too low to control abundances (McCook, 1999;
Littler and Littler, 2007) and where light levels are
sufficient.
All dense macroalgal assemblages, be it low and often
ephemeral mats, or taller and often perennial stands, suppress coral recruitment through space occupancy, allelopathy, silt-trapping, or shading (Connell et al., 1997;
Szmant, 2002). Mat-forming macroalgae tend to also
damage or kill understorey corals by restricting gas
exchange and creating hypoxia when mats collapse
(Loya et al., 2004). Tall perennial macroalgae, such as
Sargassum spp., do not usually kill corals, but they
can reduce coral growth by shading and tissue abrasion
(Littler and Littler, 2007). As a result, corals may be
outcompeted by macroalgae that grow best in highnutrient environments – as long as light is not limiting.
Another severe consequence of eutrophication is the
increased probability of outbreaks of the coral eating
crown-of-thorns starfish Acanthaster planci (Birkeland,
1982; Brodie et al., 2005). A. planci has been the most
prominent cause of coral mortality throughout many tropical Indo-Pacific regions in the last four decades. The
pelagic planktotrophic larvae of this starfish filter-feed
on large phytoplankton, and experiments suggest that
these larvae are food limited: their survivorship in the
laboratory increases steeply with increasing availability
of suitable food at environmentally relevant concentrations (Fabricius et al., 2010). In the field, increased nutrient availability can increase the abundance of large
phytoplankton cells: a strong temporal and spatial relationship exists between drought-breaking floods from
high continental islands and outbreaks of this starfish
(Birkeland, 1982). New research further strengthens the
evidence that more frequent outbreaks of A. planci are
linked to high nutrient levels (Brodie et al., 2005; Houk
et al., 2007). After primary A. planci outbreaks have
formed in a region with high phytoplankton concentrations, many of their numerous larvae may be transported
by currents to remote regions, hence secondary A. planci
outbreaks may form far away from areas of
eutrophication.
Benthic filter feeders, including sponges, bryozoans,
bivalves, barnacles, and ascidians, are important components of reef ecosystems. Most filter feeders feed on the
smallest fraction of plankton and few obtain a positive carbon balance in oligotrophic waters (Birkeland, 1988).
Most benthic filter feeders live in crevices or bore holes
into coral skeletons to avoid predation, and as cryptofauna
they are not associated with photosynthetic endosymbionts. Fewer live on the reef surface, and these often contain photosynthetic endosymbionts, possibly accelerating
growth thus enabling them to compete with hard corals
and algae for space. Filter-feeder densities increase in
response to nutrient enrichment, but surface-inhabiting filter feeders rarely outcompete corals for space even in
eutrophic environments (Aerts and Van Soest, 1997).
The few observed cases of space monopolization by
a filter feeder were restricted to areas of low light, high
plankton productivity, and organic enrichment (Smith
et al., 1981; Brock and Smith, 1983), i.e., conditions that
are unsuitable for corals. The demise of corals and the
establishment of filter feeders are therefore largely independent symptoms of eutrophication, with the fate of each
group determined by altered trophic conditions rather than
by altered balances in space competition.
Many cryptic filter feeders are macro-bioeroders
that actively bore into or chemically erode the calcium
carbonate skeletons of live corals and dead reef substrata.
They include boring sponges (e.g., Cliona spp.), bivalves
(e.g., Lithophaga spp.), sipunculans, and polychaetes
(Hutchings, 1986). Several studies have documented
abundances of internal macro-bioeroders increasing
in response to increased nutrient availability (Rose and
Risk, 1985; Hallock, 1988; Cuet et al., 1988), and abundances of most internal macro-bioeroders are higher
in productive inshore environments than they are offshore.
Increased bioerosion in areas of nutrient enrichment can
substantially weaken the structure of coral framework
and increase storm damage. This, combined with reduced
coral growth, diminished skeletal densities, and lower
recruitment rates, can mean that reef erosion exceeds
calcium carbonate accretion due to eutrophication
(Pari et al., 2002).
NUTRIENT POLLUTION/EUTROPHICATION
725
Macroalgae use photosynthesis to obtain carbon and meet
their nutrient demand through uptake of dissolved inorganic nutrients, plus, in some species, through demineralization of particulate organic matter deposited on their
fronds (Schaffelke, 1999). In the absence of control by
herbivores, some groups of macroalgae are nutrient limited and increase in growth and biomass at minute
increases in dissolved inorganic nutrients and particulate
organic matter (Littler and Littler, 2007). Similar to the
widely observed symptoms of eutrophication in other
aquatic ecosystem, macroalgae dominate coral reefs with
high nutrient availability, including in areas of eutrophication (Smith et al., 1981; Lapointe et al., 2004; Lapointe
and Bedford, 2007). Long-term data have shown that
expanding (Cuet et al., 1988) or declining (Smith et al.,
1981) macroalgal cover coincides with increasing and
declining nutrient availability, respectively. These time
series data indicate a causal link between macroalgal
abundances and nutrient availability. On the Great Barrier
Reef, total macroalgal cover increases 5-fold from highest
to lowest water clarity and additionally 1.4-fold from lowest to highest chlorophyll, 3.3-fold from offshore to
inshore, and 3.1-fold from northern to southern reefs
(De’ath and Fabricius, 2010). Macroalgae also tend to
flourish in areas of nutrient upwelling, on eastern sides
of continents or large islands where more rivers originate
than in the west (Birkeland, 1988), and towards higher latitudes, as do nutrient concentrations (Johannes et al.,
1983). These large-scale geographic data all add evidence
that nutrient levels influence macroalgal biomass. However, increases in macroalgal biomass are only observed
in areas where grazing by herbivorous fishes or invertebrates is too low to control abundances (McCook, 1999;
Littler and Littler, 2007) and where light levels are
sufficient.
All dense macroalgal assemblages, be it low and often
ephemeral mats, or taller and often perennial stands, suppress coral recruitment through space occupancy, allelopathy, silt-trapping, or shading (Connell et al., 1997;
Szmant, 2002). Mat-forming macroalgae tend to also
damage or kill understorey corals by restricting gas
exchange and creating hypoxia when mats collapse
(Loya et al., 2004). Tall perennial macroalgae, such as
Sargassum spp., do not usually kill corals, but they
can reduce coral growth by shading and tissue abrasion
(Littler and Littler, 2007). As a result, corals may be
outcompeted by macroalgae that grow best in highnutrient environments – as long as light is not limiting.
Another severe consequence of eutrophication is the
increased probability of outbreaks of the coral eating
crown-of-thorns starfish Acanthaster planci (Birkeland,
1982; Brodie et al., 2005). A. planci has been the most
prominent cause of coral mortality throughout many tropical Indo-Pacific regions in the last four decades. The
pelagic planktotrophic larvae of this starfish filter-feed
on large phytoplankton, and experiments suggest that
these larvae are food limited: their survivorship in the
laboratory increases steeply with increasing availability
of suitable food at environmentally relevant concentrations (Fabricius et al., 2010). In the field, increased nutrient availability can increase the abundance of large
phytoplankton cells: a strong temporal and spatial relationship exists between drought-breaking floods from
high continental islands and outbreaks of this starfish
(Birkeland, 1982). New research further strengthens the
evidence that more frequent outbreaks of A. planci are
linked to high nutrient levels (Brodie et al., 2005; Houk
et al., 2007). After primary A. planci outbreaks have
formed in a region with high phytoplankton concentrations, many of their numerous larvae may be transported
by currents to remote regions, hence secondary A. planci
outbreaks may form far away from areas of
eutrophication.
Benthic filter feeders, including sponges, bryozoans,
bivalves, barnacles, and ascidians, are important components of reef ecosystems. Most filter feeders feed on the
smallest fraction of plankton and few obtain a positive carbon balance in oligotrophic waters (Birkeland, 1988).
Most benthic filter feeders live in crevices or bore holes
into coral skeletons to avoid predation, and as cryptofauna
they are not associated with photosynthetic endosymbionts. Fewer live on the reef surface, and these often contain photosynthetic endosymbionts, possibly accelerating
growth thus enabling them to compete with hard corals
and algae for space. Filter-feeder densities increase in
response to nutrient enrichment, but surface-inhabiting filter feeders rarely outcompete corals for space even in
eutrophic environments (Aerts and Van Soest, 1997).
The few observed cases of space monopolization by
a filter feeder were restricted to areas of low light, high
plankton productivity, and organic enrichment (Smith
et al., 1981; Brock and Smith, 1983), i.e., conditions that
are unsuitable for corals. The demise of corals and the
establishment of filter feeders are therefore largely independent symptoms of eutrophication, with the fate of each
group determined by altered trophic conditions rather than
by altered balances in space competition.
Many cryptic filter feeders are macro-bioeroders
that actively bore into or chemically erode the calcium
carbonate skeletons of live corals and dead reef substrata.
They include boring sponges (e.g., Cliona spp.), bivalves
(e.g., Lithophaga spp.), sipunculans, and polychaetes
(Hutchings, 1986). Several studies have documented
abundances of internal macro-bioeroders increasing
in response to increased nutrient availability (Rose and
Risk, 1985; Hallock, 1988; Cuet et al., 1988), and abundances of most internal macro-bioeroders are higher
in productive inshore environments than they are offshore.
Increased bioerosion in areas of nutrient enrichment can
substantially weaken the structure of coral framework
and increase storm damage. This, combined with reduced
coral growth, diminished skeletal densities, and lower
recruitment rates, can mean that reef erosion exceeds
calcium carbonate accretion due to eutrophication
(Pari et al., 2002).
NUTRIENT POLLUTION/EUTROPHICATION
725