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Excess seawater nutrients, enlarged algal symbiont densities and bleaching sensitive reef locations: 1. Identifying thresholds of concern for the Great Barrier Reef, Australia

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  • Catchment to Reef Management Solutions, Newcastle Australia

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Here, I contribute new insight into why excess seawater nutrients are an increasingly identified feature at reef locations that have low resistance to thermal stress. Specifically, I link this unfavourable synergism to the development of enlarged (suboptimal) zooxanthellae densities that paradoxically limit the capacity of the host coral to build tissue energy reserves needed to combat periods of stress. I explain how both theoretical predictions and field observations support the existence of species-specific ‘optimal’ zooxanthellae densities ~1.0–3.0 × 10^6 cells cm−2. For the central Great Barrier Reef (GBR), excess seawater nutrients that permit enlarged zooxanthellae densities beyond this optimumrange are linkedwith seawater chlorophyll a N 0.45 μg·L−1; a eutrophication threshold previously shown to correlate with a significant loss in species for hard corals and phototrophic octocorals on the central GBR, and herein shown to correlate with enhanced bleaching sensitivity during the1998 and 2002 mass bleaching events.
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Excess seawater nutrients, enlarged algal symbiont densities and bleaching sensitive
reef locations: 1. Identifying thresholds of concern for the Great Barrier Reef, Australia
Scott A. Wooldridge
Catchment to Reef Management Solutions, Newcastle, NSW 2280, Australia
abstractarticle info
Article history:
Received 7 December 2015
Received in revised form 30 March 2016
Accepted 26 April 2016
Available online xxxx
Here, I contribute new insight into why excess seawater nutrients are an increasingly identied feature at reef
locations that have low resistance to thermal stress. Specically, I link this unfavourable synergism to the devel-
opment of enlarged (suboptimal) zooxanthellae densities that paradoxicallylimit the capacity of the host coral to
build tissue energy reserves needed to combat periods of stress. I explain how both theoretical predictions and
eld observations support the existence of species-specicoptimalzooxanthellae densities ~ 1.03.0 × 10
6
cells cm
2
. For the central Great Barrier Reef (GBR), excess seawater nutrients that permit enlargedzooxanthel-
lae densities beyond this optimum range are linked with seawater chlorophyll aN0.45 μL
1
; a eutrophication
threshold previously shown to correlate with a signicant loss in species for hard corals and phototrophic
octocorals on the central GBR, and herein shown to correlate with enhanced bleaching sensitivity during the
1998 and 2002 mass bleaching events.
© 2016 Elsevier Ltd. All rights reserved.
Keywords:
Coral health
Bleaching resistance
Water quality
Resilience
Symbiosis
1. Introduction
In warm, nutrient-poor tropical seawater, the endosymbiotic rela-
tionship between corals and dinoagellate algae of the genus
Symbiodinium (zooxanthellae)(Fig. 1a) is characterised by an excess
translocation of xed-carbon photosynthetic products from the zooxan-
thellae to the coral host (reviewed by Yellowlees et al., 2008). These
photo-autotrophic carbon products form the basis of the daily energy
balance for most corals, and are thus fundamental to numerous homeo-
static processes that maintain the stable functioning of the symbiosis
(reviewed by Wooldridge, 2010). Under this stable symbiotic arrange-
ment, the coral host is able to build and maintain large energy stores
within thick colony tissue layers (e.g. lipids, protein, carbohydrates),
precipitate strong (dense) calcium carbonate skeletons, and generate
a plentiful supply of gametes for reproduction (Yellowlees et al., 2008;
Wooldridge, 2010, 2014a, 2014b).
The stability of the cora l-algae symbiosis is, h owever, extremely sen-
sitive to heat stress, and sea temperatures as little as 12 °C above the
average summer maximum can often trigger the breakdown of the
symbiosis and resultant mass expulsion of the algal partner so called
coral bleaching (reviewed by Brown, 1997). By measuring the incre-
mental impact of elevated sea temperatures on the photosynthetic
(P) and respiration (R) rates from a range of symbiotic reef corals,
Coles and Jokiel (1977) were the rst to document the diminished auto-
trophic capacity (P:R ratio) that underpins the thermal bleaching re-
sponse. In this case, respiration rates are observed to increase much
more rapidly than photosynthesis as temperatures increase, leading to
a lower P:R ratio with increasing temperatures (Fig. 1b). This scenario
is magnied upon the exceedance of thermal stress thresholds, wherein
photosynthetic yields progressively diminish whilst at the same time
energetic costs (e.g. associated with cellular damage repair) rapidly
increase.
AP:Rratiob1 when extrapolated over 24 h indicates that the coral
algal association produced less organic material (energy) than it con-
sumed. This autotrophic energy crisisnecessitates that host tissue en-
ergy reserves are mobilised to supplement the respiratory carbon
needed to maintain the stability and function of the symbiosis; that is,
unless offset by a drastic increase in heterotrophic feeding acapacity
that is not equally effectual in all corals (Hughes and Grottoli, 2013).
Stored lipids reserves tend to be catabolised initially, however, should
the period of thermal disruption be prolonged and lipid reserves de-
pleted, then the coral host may alsostart sacricing somatic (structural)
tissues reserves (Szmant and Gassman, 1990; True, 2005; Ainsworth
et al., 2008).
The thermal bleaching sequence for a eld-population of massive
Porites spp. highlights the homeostatic importance of stored tissue re-
serves in maintaining the stability of the symbiosis during periods of
thermal stress. In this case, mass expulsion of zooxanthellae during a
period of prolonged (~weeks) thermal stress only occurred upon the
depletion of tissue reserves below a common lower (2 mm of tissue
thickness) threshold (True, 2005). A similar pre-bleaching sequence
has also been noted for a branching Acropora spp. (Ainsworth et al.,
2008), wherein the authors observed signicant, and continuous reduc-
tions in coral tissue thickness across several days before the ultimate
mass expulsion (N50%) of symbionts. Moreover, this phenomenon
Marine Pollution Bulletin xxx (2016) xxxxxx
E-mail address: swooldri23@gmail.com.
MPB-07667; No of Pages 8
http://dx.doi.org/10.1016/j.marpolbul.2016.04.054
0025-326X/© 2016 Elsevier Ltd. All rights reserved.
Contents lists available at ScienceDirect
Marine Pollution Bulletin
journal homepage: www.elsevier.com/locate/marpolbul
Please cite this article as: Wooldridge, S.A., Excess seawater nutrients, enlarged algal symbiont densities and bleaching sensitive reef locations: 1.
Identifying thresholds of ..., Marine Pollution Bulletin (2016), http://dx.doi.org/10.1016/j.marpolbul.2016.04.054
likely explains: (i) the enhanced bleaching risk of coral species with thin
colony tissue thickness layers (Loya et al., 2001; Wooldridge, 2014b),
and (ii) empirical bleaching relationships that are characterised by
species-specic temperature-duration relationships (Berkelmans,
2002). In this latter case, the deleterious impact of elevated tempera-
tures in driving autotrophic capacity (P:R) lower dictates that progres-
sively less time is required at higher temperatures before the host's
energy storage reserves fall below the level that triggers the onset of
bleaching; being commensurate with the conclusion of Coles and
Jokiel (1977) that corals with the highest respiration rates are (ulti-
mately) the most sensitive to thermal bleaching and mortality.
All-other-things-being-equal, an obvious consequence of this ther-
mal disruption in coralalgae energy relations, is that reef conditions
which favour the pre-stress development of superior host tissue energy
reserves, are better equipped to combat prolonged periods of thermal
stress and reduced autotrophic capacity; thereby increasing resistance
to bleaching and mortality (Thornhill et al., 2011). In this paper, I inves-
tigate the utility of this suggestion for helping to explain why poor
water quality, particularly an excess availability of bioavailable dis-
solved inorganic nitrogen (DIN = nitrate + nitrite + ammonium), is
an increasingly identied feature at reef locations that have low resis-
tance to thermal stress (Wooldridge, 2009a; Wooldridge and Done,
2009; Wagner et al., 2010; Wiedenmann et al., 2012; Vega-Thurber
et al., 2014). Specically, I endeavour to link this unfavourable syner-
gism with the development of enlarged (suboptimal) zooxanthellae
densities that disrupt the autotrophic energy relations of the coral
algae symbiosis. I explain how both theoretical predictions and eld ob-
servations support the existence of species-specicoptimalzooxan-
thellae densities, wherein the bleaching syndrome is best resisted at
presently accepted upper natural limits for temperature and irradiance.
The existence of such a biological threshold highlights the benetof
identifying eutrophication thresholds that pre-dispose the proliferation
of suboptimal endosymbiont densities for the task of identifying
bleaching-sensitive reef locations. I highlight this benet for the Great
Barrier Reef (GBR, Australia) by demonstrating an improved ability to
discriminate severe thermal bleaching impacts based on whether aver-
age summer seawater chlorophyll-aN0.45 μg·L
1
.
1.1. Symbiont densities inuence coralalgae energy relations
Far from being strictly benecial, emerging evidence indicates that
the producer-in-consumerarrangement of the coralalgae symbiosis
(Fig. 1a) is best viewed as a dynamic reciprocal exploitation
(Wooldridge, 2010; Lesser et al., 2013). Thus, the nature of the symbi-
otic interactions can readily switch from benecial to parasitic (for ei-
ther partner) depending on specic (changeable) environmental
conditions that differentially favour either partner. For example, enrich-
ment of seawater with anexcess of bioavailable nutrients can inhibit the
ability of the coral host to maintain demographic control of its algal
symbionts, resulting in an enlarged, fast-growing symbiont population
that is ultimately a net carbon sink (= parasite) for the energetic re-
sources of the coral (this paper, Wooldridge, 2012, 2013, 2014a). In
this case, as densities increase, the photosynthetic capacity per zooxan-
thella (P) progressively decreases (possibly due to increased self-
shading and/or CO
2
-limitation within the host cell) whilst the associ-
ated respiratory/maintenance cost to the symbiosis (R) increases (line-
arly) per zooxanthella added (Anthony et al., 2009; Hoogenboom
et al., 2010). In this way, it is understood that there exists an optimum
zooxanthellae density that maximises autotrophic capacity (P:R),
i.e., every zooxanthella added beyond this optimum reduces the poten-
tial autotrophic energy transferred to the coral host (Fig. 1c). This is im-
portant, since lipids can only be stored when surplus energy is available
(P:R ratio 1; Muscatine et al., 1981). The existence of an optimum zo-
oxanthella density ts with other observational data showing that:
(i) photosynthetic yields (Zhu et al., 2010), (ii) autotrophic capacity
(P:R ratio) (Nir et al., 2014), and (iii) photosynthate transfer rates
Fig. 1. (a) Under optimal environ mental conditions, reef-building corals receive an energetic benet from the endosymbiotic rela tionship they maintain with photo-autotrophic
dinoagellate algae (=zooxanthellae). The energetic benet for the animal host, however, is not guaranteed under suboptimal conditions. (b) Elevated seawater temperatures can
cause photo-autotrophic energy transfers to diminish as algal photosynthesis rates decrease whilst metabolic respiration rates increase (Castillo and Helmuth, 2005). (c) Elevated
seawater nutrient concentrations that permit enlarged zooxanthella population densities can also cause photo-autotrophic energy transfers to decline as the metabolic cost of hosting
excesszooxanthellae exceeds the photosynthetic energy gains.
2S.A. Wooldridge / Marine Pollution Bulletin xxx (2016) xxxxxx
Please cite this article as: Wooldridge, S.A., Excess seawater nutrients, enlarged algal symbiont densities and bleaching sensitive reeflocations: 1.
Identifying thresholds of ..., Marine Pollution Bulletin (2016), http://dx.doi.org/10.1016/j.marpolbul.2016.04.054
(Davy and Cook, 2001)areall enhanced when endosymbiont densities
are restricted most often facilitated by a limitation of essential nutri-
ents required for algal proliferation (i.e. mitotic cell division).
The linear relationship between the increased respiratory cost to the
symbiosis (R) per zooxanthella added means that any additional factor
(s) that add to the respiratory load of the symbiosis has the potential to
alter the optimal size of the zooxanthellae population. For example, the
well-known effects of increasing background-ambient sea water tem-
perature on: (i) respiratory metabolism (so-called Q
10
effects; see
e.g., Edmunds, 2008), and (ii) energetic costs associated with the
basal-rate of cellular damage repair, and/or consumption (scavenging)
of molecular oxygen during the formation of active oxygen (Lesser,
2004), allude to the contributing role of higher ambient seawater tem-
peratures in enhancing the detrimental impact of excess zooxanthellae
on autotrophic capacity. Such observationstwithboththeoreticalpre-
dictions (Wooldridge 2013a) and eld observations. For example,
Muller-Parker et al. (1994) found that DIN-enlarged zooxanthellae den-
sities actually beneted coral tissue growth at sea temperatures b26 °C;
a result also observed by Atkinson et al. (1995) in an aquarium setting.
This is in contrast to the negative impacts of an enlarged, fast-growing
symbiont populations on host tissue reserves during warmer (N27 °C)
conditions (see next; also Koop et al., 2001; Cruz-Pinon et al., 2003;
Loya et al., 2004).
1.2. Excess symbiont densities lower host tissue energy reserves
To highlight the impact of excess symbionts on the health of the
coral host and by inference its energetic capacity to resist thermal (au-
totrophic) stress, I re-examine the observations from three previous
eld studies undertaken at reef locations that span the Atlantic, Indian
and Pacicoceans.
1.3. Study #1: Coral health monitoring at Lee Stocking Island, Atlantic
Ocean (Bahamas)
The rst study was undertaken in the vicinity of Lee Stocking Island
in the Bahamas (Atlantic Ocean; 23°32N, 75°46W). The study investi-
gated various coral health indicators over the course of a 4-year period
(19951999), wherein samples were collected at 3-month intervals.
Specic details of the study and sampling regime are described in Fitt
et al. (2000). Here, I summarise the response proles for three different
coral species, which span a gradient of coral morphologies: Acropora
cervicornis (thin tissue thickness, ne-branching), Orbicella annularis
(moderate tissue thickness, columnar), and Orbicella faveolata (thick tis-
sue thickness, massive).
Fig. 2 highlights the variation in tissue biomass (ash free dryweight,
mg cm
2
) plotted against changes in symbiont density across the
course of the sampling. By making the reasonable assumption that tis-
sue biomass (=surrogate for host energy stores) would (ultimately)
trend toward zero in photoautotrophic-dependent species as a result
of the mass loss of symbionts (see e.g., Grottoli and Rodrigues, 2011),
it becomes apparent that a species-specicoptimalsymbiont density
exists that helps to maximise the accumulation of host energy reserves.
The optimaldensity increases across the thin-tissue ne-branching
(viz. A. cervicornis ~1.01.2 × 10
6
cells cm
2
), moderate-tissue colum-
nar (O. Annularis ~1.52.0 × 10
6
cells cm
2
), and thick-tissue massive
(viz. O. faveolata ~ 2.53.0 × 10
6
cells cm
2
) morphological gradient.
Beyond the optimallevels, tissue biomass declines in near proportion
to the excesszooxanthellae. The most parsimonious inference is that
energy-rich algal photosynthate transfer rates to the host are lowest at
both very low zooxanthellae densities (due to low densities per se)
and very high zooxanthellae densities (due to low per capita rates).
Wooldridge (2014b) recently reviewed the bio-physiological differ-
ences which are predicted to underpin the lower average density of zo-
oxanthellae (per cm
2
) in thin-tissue- branching corals versus thick-
tissue-massive corals (e.g., reduced host tissue shading, reduced host
metabolic CO
2
supply, reduced host tissue concentration of uorescent
pigments etc). Ultimately, these bio-physiological differences are pre-
dicted to enhance the risk of damaging photoinhibition within thin-
tissue branching morphological coral types during periods of high irra-
diance thereby limiting the maximum permitted zooxanthellae den-
sity (Wooldridge, 2009b, 2014). This same biological reasoning can be
used to explain the observed increase in optimalsymbiont population
density across the thin-tissue-ne-branching versus thick-tissue-
massive morphological gradient.
1.4. Study #2: Coral health monitoring at Ningaloo Reef, Indian Ocean
(North-Western Australia)
The second study was undertaken at Ningaloo Reef, along the North-
West Cape of Western Australia (Indian Ocean; 22.23°S, 113.84°E). The
study investigated various coral health indicators over the course of a
12-month sampling period, which notably included an extreme (La
Nińa) weather event wherein oceanic conditions were warmer and
more nutrient-rich than for a typical summer in this region. Specicde-
tails of the study and sampling regime are described in Hinrichs et al.
(2013a, 2013b). Here, I concentrate on the results for the compact
branching coral Acropora digitifera, which was identied during the
study as being a representative of coral species that are heavily reliant
on autotrophy for the development of their long-term energy stores.
Fig. 3 highlights the variability in two coralhealth indicators (protein
concentration and lipid ratio) plotted against changes in symbiontden-
sity across the course of the sampling. Protein concentration has been
applied with some success as indicators of nutritional condition and
Fig. 2. Coralhealth Study #1 (cf.Fitt et al., 2000). Coral tissue biomass (ash freedry weight, mg cm
2
, lagged by 3-months) indicatethat species-specicoptimalsymbiont densities exist
that maximise the health benet for the coral host. Beyond thisoptimal populationdensity the symbiotic benets for the coral hostdecline in near proportion with the number of excess
zooxanthellae. The s ize of the optimaldensity increases across the thin-tissue ne-branching (A. cervicornis ~1.01.2 × 10
6
cells cm
2
), moderate -tissue column ar (O. faveolata ~1.5
2.0 × 10
6
cells cm
2
), and thick-t issue massive (O. faveolata ~2.53.0 × 10
6
cells cm
2
) morphological gradient. The identied regression relationships are statistically signicant at a
p-value b0.05 level. Dashed lines represent approximate 90% condence intervals. Note: species-specic data was pooled across the depth range (013 m), and data collected during
the extreme summer bleaching events in 1995 and 1998 was removed from the analysis.
3S.A. Wooldridge / Marine Pollution Bulletin xxx (2016) xxxxxx
Please cite this article as: Wooldridge, S.A., Excess seawater nutrients, enlarged algal symbiont densities and bleaching sensitive reef locations: 1.
Identifying thresholds of ..., Marine Pollution Bulletin (2016), http://dx.doi.org/10.1016/j.marpolbul.2016.04.054
potential for tissue growth (Dahlhoff, 2004). Lipid analysis describes the
ratio between storage lipids (wax esters and triacylglycerin), which are
stored by corals whenenvironmental conditionsare favourable and sur-
plus energy is available (Harland et al., 1992), and structural lipids
(phospholipids and cholesterol), which are used for maintaining cell
structureandarethereforeknowntobemorestablethanstoragelipids
(Saunders et al., 2005). Again, by making the reasonable assumption for
this species that lipid and protein resources would trend to zero as a re-
sult of the mass loss of symbionts (=bleaching), it is evident that both
health indicators initially increase per zooxanthella added until an opti-
mum threshold ~1.52.0 × 10
6
cells cm
2
. Beyond this optimum range,
both indicators decline in near proportion to the excesszooxanthellae
permitted by the nutrient-enriching (~0.35 ± 0.1 μg·L
1
Chlorophyll-
a)LaNińa upwelling event. Given the compact branching morphology
of A. digitifera, this response prole falls consistently within the ob-
served morphological-dependent optimalsymbiont density gradient
established in Study 1.
1.5. Study #3: Coral health monitoring on the Great Barrier Reef, Coral Sea
(North-Eastern Australia)
The third study was undertaken along regional water quality gradi-
ents on the Great Barrier Reef (GBR, Coral Sea; 2023°S, 148151°E).
The water gradients (poor good) are established based on distance
away from the mouth of major rivers, which drain catchments that
are dominated by agricultural land uses with high application rates of
nitrogen-rich fertiliser. The study investigated various coral health indi-
cators on eightseparate reefs with signicantly different water qualities
during August (winter) 2004. Specic details of the study and sampling
regime are described in Fabricius et al. (2012). Here, I concentrate on
the results for massive Porites spp. corals in water depths less than
5 m. Two health indicators are considered: (i) colour intensity (pigmen-
tation) of the upward facing colony surface, measured to the nearest
half-score on a colour reference chart with six graduations (1being al-
most bleached-white, 6being very dark; Siebeck et al., 2006; Cooper
and Fabricius, 2012), and (ii) tissue thickness of upper surfaces, as sam-
pled with a 25 mm hole-saw drill (Barnes and Lough, 1992). For
shallow-water reef corals, an increase in colour intensity is a common
response to enhanced nutrients, most often facilitated by an increase
in zooxanthella density (see e.g., Dubinsky et al., 1990; Falkowski
et al., 1993). To help conrm this response for this study, I also
Fig. 3. Coral health Study #2 (cf. Hinrichs et al., 2013a, 2013b). Tissue protein and lipid
levels in A. digitifera indicate that the energetic health benet of hosting algal symbionts
increases to a max imum ~1.52. 0 × 10
6
cells cm
2
. Beyond this optimal population
density the symb iotic benets for the c oral host decline in ne ar proportion with the
number of excesszooxanthellae. The identied regression relationships are statistically
signicant at a p-value b0.05 level.
Fig. 4. Coral health Study #3 (cf. Fabricius et al.,2012). Colony tissue thickness levels of shallow water (b5m)massivePorites spp. along GBR waterquality gradients. (a) Tissuethickness
increases to a max imum at mid-level colour intensity values ~ 3.5. (b) Zooxanthellae density measurements indicate that this optimal co lour intensity corre sponds with ~ 1.5
2.0 × 10
6
cells cm
2
in co-located P. damicornis colonies. Beyond this population density the symbiotic benets for the coral host decline in near proportion with the number of
excesszooxanthellae. The identied relationships are statistically signicant at a p-value b0.05 level.
4S.A. Wooldridge / Marine Pollution Bulletin xxx (2016) xxxxxx
Please cite this article as: Wooldridge, S.A., Excess seawater nutrients, enlarged algal symbiont densities and bleaching sensitive reeflocations: 1.
Identifying thresholds of ..., Marine Pollution Bulletin (2016), http://dx.doi.org/10.1016/j.marpolbul.2016.04.054
considered zooxanthella density measurements from the clumping
(cauliower) branches of co-located Pocillopora damicornis corals.
As conrmed by the statistics from the original analysis, the colony
colour of massive Porites becomes signicantly darker and tissue thick-
ness decreases toward the nutrient-enriched coastal zone; at the same
time the symbiont density in P. damicornis increases ~3 fold (Fabricius
et al., 2012). When considered collectively, it is evident that Porites tis-
sue thickness (=surrogate for host energy stores; True, 2005) increases
to a maximum (optimum) at a colour intensity ~3.5, before decreasing
at progressively darker colony colours (Fig. 3a). By using P. damicornis
as a surrogate, it is also evident that changes in Porites colony colour
were most likely dominated by changes in zooxanthellae densities,
and that the optimum colour intensity ~ 3.5 corresponds with
~1.5 × 10
6
cells cm
2
in P. damicornis (Fig. 3b). This result is similar to
that observed for A. cervicornis (Study 1) and A. digitifera (Study 2),
and suggests that ~1.02.0 × 10
6
cells cm
2
is the near optimalsymbi-
ont density for thin-tissue branching morphologies, i.e. the optimal
symbiotic arrangement to maximise light harvesting and minimise
intraspecic competition for resources, such as intracellular CO
2
(see
Fig. 1c).
1.6. Critical eutrophication thresholds for enhanced bleaching sensitivity on
the GBR
In tropical reef waters, measures of phytoplankton biomass usually
provide a better indicator of eutrophication status than actual measured
nutrient concentrations, since fast growing phytoplankton populations
quickly respond to, and subsequently deplete, all available stocks of bio-
available nutrients; resulting in localised blooms in population densities
(Edwards et al., 2003; Furnas et al., 2005). Concentrations of the photo-
synthetic pigment, chlorophyll-a(chl-a), is the most commonly used
measure of phytoplankton biomass, and has been adopted as the eco-
system indicator for eutrophication impacts within GBR coastal reef wa-
ters (De'ath and Fabricius, 2008; Great Barrier Reef Marine Park
Authority, 2010; Wooldridge et al., 2015).
Fig. 5. (a) Impact of DIN-enrichment, as indicated by a seawater chlorophyll-aconcentration, on Porites spp. colour intensity. Chlorophyll-aN0.45μg·L
1
corresponds with darker Porites
colonies that have reduced colonytissue thickness levels. The N0.45 μg·L
1
threshold has previously beenshown to trigger a signicantloss of species in: (b) hard corals, and (c) photo-
autotrophic octocorals (after De'ath and Fabricius, 2008).
Fig. 6. (a) Aerialsurveys duringthe mass coral bleachingevents in 1998 and 2002(Berkelmans et al.,2004) indicate thatthe majority of reefs with strongthermal bleaching impacts(N10%
coral cover) were pre-conditionedby reef waters that exceed the chlorophyll-aN0.45 μg·L
1
threshold at least 1 in every 5 years (darkgreen area). Sites with no bleaching were mostly
pre-conditioned by reef waters that exceedthe 0.45 μg·L
1
thresholdless than 1 in every 10 years. (b) Likelihood of coral bleaching (N10% coral cover; as per observations in 5a) depend
on the degree of heat stress (DHW) and whether the reef site exceeds (or not) the 0.45 μg·L
1
trigger threshold at least 1 in every 5 years.
5S.A. Wooldridge / Marine Pollution Bulletin xxx (2016) xxxxxx
Please cite this article as: Wooldridge, S.A., Excess seawater nutrients, enlarged algal symbiont densities and bleaching sensitive reef locations: 1.
Identifying thresholds of ..., Marine Pollution Bulletin (2016), http://dx.doi.org/10.1016/j.marpolbul.2016.04.054
Concurrent water quality measurements conrm the direct relation-
ship between nutrient-enriched oceanicconditions, as indicated by ele-
vated seawater chlorophyll-aand the darker Porites colony colours
observed in Study 3 (Fig. 5a). Notably, the recorded decline in tissue
thickness beyond the optimum colour intensity ~3.5 is matched with
seawater chlorophyll-aN0.45 μg·L
1
. Seawater chlorophyll-
ab0.45 μg·L
1
has previously been identied as fundamental for the
maintenance of a healthy reef status on the GBR, with a signicant
loss in species for hard corals and phototrophic octocorals beyond this
triggering threshold (Fig. 5b, c; De'ath and Fabricius, 2008; Great
Barrier Reef Marine Park Authority, 2010). This response has often
been linked to the possibility that seawater chlorophyll-
aN0.45 μg·L
1
results in green waterthat may limit light penetration
and hence photosynthetic yields (De'ath and Fabricius, 2008). However,
given the context provided by the results in this manuscript, it appears
reasonable to conclude that thelinkage between healthy reef status and
seawater chlorophyll-ab0.45 μg·L
1
on the GBR may also include the
enhanced capacity for corals to build tissue energy reserves, and there-
fore combat prolonged periods of autotrophic stress; be it due to high/
low temperatures, aerial exposure at low tides, or freshwater inunda-
tion from river plumes (Wooldridge, 2009b).
Here, I test the signicance of the 0.45 μg·L
1
trigger value for
explaining regional differences in bleaching sensitivity on the central
GBR during the1998 and 2002 thermal stress events on the GBR. The re-
gional bleaching surveys were facilitated by aerial surveys, and best rep-
resent the response patterns of spatially dominant shallow-water
(b10 m) branching and plating Acropora spp. (c.f. Berkelmans and
Oliver, 1999; Berkelmans et al., 2004). By using an earlier developed
empirical relationship between summer seawater chlorophyll-aand
modelled river-plume dilution extents (19692003) (described in
Wooldridge et al., 2006) it is visually apparent that reefs which exceed
the 0.45 μg·L
1
threshold with an average recurrence interval (ARI)
of at least 1 in every 5 years were much more likely to record signicant
bleaching (N10% coral cover) during the anomalously hot summers of
1998 and 2002 (Fig. 6a). In comparison, those reefs that exceed the
threshold less than 1 in every 10 years did not experience signicant
bleaching impacts, despite many of these reefs experiencing anomalous
heating stress (Berkelmans et al., 2004).
To counter the argument that this response could simply be ex-
plained by the possibility that the inshore reef areas were exposed to
higher thermal anomalies, I utilised satellite-derived sea surface tem-
peratures (SSTs) to calculate the Degree Heating Week(DHW) metric
(Liu et al., 2003) for a spatial resolution of 4 km (for method details, see
Heron et al., 2010; Wooldridge et al., 2015). Typically, a DHW N4 °C-
weeks predicts a likely bleaching event(Liu et al., 2003). However,
when the pooled DHW response for the 1998 and 2002 bleaching
events is disaggregated in terms of reef sites that exceed (or not) the
0.45 μg·L
1
threshold at least 1 in every 5 years, it is evident that
bleaching sensitivity for the central GBR is strongly co-determined by
DIN enrichment; with the more DIN-enriched sites being ~24 times
more sensitive to bleaching at progressive levels of thermal stress
(Fig. 6b).
The simplest logic suggests that end-of-river DIN improvements that
help lower the encounter rate of the 0.45 μg·L
1
threshold on reef wa-
ters to beyond 1 in every 5 years may assist in raising the SSTthresholds
that currently cause corals to bleach, thereby reducing the bleaching
risk probability across the whole range of temperatures predicted on
the GBR by 2100 (cf., Wooldridge et al., 2012). Mechanistically, this
can be understood in terms of restoring a more optimal zooxanthella
density that benets the building/maintenance of tissue energy stores
to offset periods of thermal (autotrophic) disruption. It has also been
suggested that reduced zooxanthella densities may assist more directly
in raising thermal bleaching thresholds by lowering the total intracellu-
lar oxidative stressload that contributes to the host cellulardamage that
ultimately triggers the bleaching syndrome (Nesa and Hidaka, 2009;
Wooldridge, 2012; Cunning and Baker, 2013). Notably, both the
theoretical predictions and experimental ndings indicate the existence
of an optimal zooxanthella density, wherein signicant bleaching is best
resisted at presently accepted upper natural limits for temperature and
irradiance (Wooldridge, 2012; Cunning and Baker, 2013).
The conceptual logic is strengthened by recent eld manipulations
which highlight that DIN-enrichment signicantly increases thermal
bleaching sensitivity, but the detrimental inuence is lost only 1-year
subsequent to the DIN loading being removed (Vega-Thurber et al.,
2014). Algal endosymbiont growth is extremely dynamic in response
to DIN loading (e.g., population densities can double in 23weeks;
Dubinsky et al., 1990; Falkowski et al., 1993), but this enhancement
(relative to host animal growth) can only be maintained whilst external
DIN remains in excess. Without an external DIN source, symbiont den-
sities return to normal levels within a relatively short time frame
(weeksmonths) (Falkowski et al., 1993). This response dynamic may
also explain the previously challenging observation, that during the
summer of 2004, many inshore reef locations on the GBR exceeded the
time-integrated thermal bleaching thresholds that successfully pre-
dicted bleaching in 1998 and 2002, yet no bleaching was recorded
(Berkelmans, 2009). Notably, drought conditions resulted in little dis-
charge from the major rivers for the three wet seasons preceding (and
including) the summer of 2004 (Australian Government, Bureau of Me-
teorology, 2015). The inference is that improved bleaching resistance
can be restored in as little as ~13 years upon removal of excess river
DIN loading.
It is important to note that the suggested GBR seawater eutrophica-
tion trigger level (chlorophyll-aN0.45 μg·L
1
) is unlikely to be a uni-
versal value at other global reef locations, since this proxy indicator
value is ultimately linked to the relative availability of other essential
nutrients necessary for photoplankton growth (e.g., phosphorus). The
GBR is most often heavily nitrogen-limited with respect to the availabil-
ity of phosphorus (Furnas et al., 2005, 2011). For other global reef loca-
tions this scenario may be different, including the potential for the
alternative case, whereby nitrogen availability doesn't limit phyto-
plankton growth (i.e. chlorophyll-a), but rather phosphorus, or indeed
iron (Fe) (see Moore et al., 2013).
2. Concluding comments and future prospects
The potential for nutrient-enriched oceanic conditions to promote
unhealthy reef environments that are characterised by weak (porous)
skeletons, low reproductive output, and enhanced riskof bleaching, dis-
ease and mortality have been well documented (reviewed by Fabricius,
2005). Yet, the mechanism(s) underpinning this etiology have not been
well attributed. This lack of mechanistic understanding limits the iden-
tication of biologically-relevant, eutrophication thresholds that are
needed for the region-specic design of effective management strate-
gies. In this paper, I have demonstrated how the underpinning instabil-
ity of the coralalgae symbiosis toexcess seawater nutrients canhelp to
unify these various stress sensitivities via the development of enlarged
(suboptimal) zooxanthella densities that limit the autotrophic capacity
of the symbiosis; and hence the capacity of the host coral to build tissue
energy reserves needed to combat periods of stress. In this case, excess
seawater nutrients that permit zooxanthella densities to proliferate be-
yond species-specic optimum levels (~1.03.0 × 10
6
cells cm
2
)have
been shown to restrict the host's capacity to build and maintain opti-
mum energy reserves. For the central GBR, this eutrophication thresh-
old has been linked with seawater chlorophyll-aN0.45 μg·L
1
,a
threshold previously shown to correlate with a signicant loss in species
for hard corals and phototrophic octocorals on the central GBR, and
herein shown to correlate with enhanced bleaching sensitivity during
the 1998 and 2002 mass coral bleaching events.
Based on this mechanism, it is understood that warmer/warming
background ambient temperature regimes have the potential to en-
hance the detrimental impact of excess zooxanthellae on autotrophic
capacity across regional and global scales. Similarly, rising global
6S.A. Wooldridge / Marine Pollution Bulletin xxx (2016) xxxxxx
Please cite this article as: Wooldridge, S.A., Excess seawater nutrients, enlarged algal symbiont densities and bleaching sensitive reeflocations: 1.
Identifying thresholds of ..., Marine Pollution Bulletin (2016), http://dx.doi.org/10.1016/j.marpolbul.2016.04.054
atmospheric CO
2
concentrations that increase seawater pCO
2
and per-
mit larger background zooxanthella densities when excess seawater
nutrients prevail, further increase this inherent vulnerability
(Wooldridge, 2012). The cumulative risk posed by global climate
change to the underpinning health of the coralalgae symbiosis is thus
pervasive. However, the benet of nutrient-impoverished (oligotro-
phic) seawater that enforces pre-mitotic control of zooxanthella prolif-
eration rates is universal; making efforts to limit coastal eutrophication
a clear local management objective.
Acknowledgments
I am grateful to Dr Saskia Hinrichs (University of Western Australia)
for providing the Ningaloo coralhealth response data (cf. 3) and Dr Tim
Cooper and Dr Katharina Fabricius (Australian Institute of Marine Sci-
ence; AIMS) for providing the GBR-water quality gradient data and
linked coral health response data (cf. Figs. 4, 5). I also thank Dr Ray
Berkelmans (AIMS) for providing the aerial bleaching survey data and
Dr Scott Heron (NOAA) the DHW data (cf. Fig. 6).
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Identifying thresholds of ..., Marine Pollution Bulletin (2016), http://dx.doi.org/10.1016/j.marpolbul.2016.04.054
... Nutrient influences can be episodic and dependent on the coincidence of several factors. For example, the influence of nutrient enrichment on coral bleaching susceptibility is episodic at three-to five-year intervals during high-temperature periods, for example, in El Niño years in summer (December-March) (Wooldridge, 2016;Wooldridge et al., 2017). During periods of prolonged elevated sea surface temperature, coral reefs are more susceptible to coral bleaching if these conditions coincide with degraded water quality (e.g. ...
... Elevated nutrient concentrations have been identified as one of the most important (aside from sea surface temperature) (Carilli et al., 2009;Carilli et al., 2010;Wagner et al., 2010;Wooldridge, 2009;Wooldridge and Done, 2009). DIN availability is important in the functioning of the coral-algae symbiosis, and elevated DIN concentrations can cause changes that disrupt the ability of the coral host to maintain an optimal population of algal symbionts (Wooldridge, 2016). Together with increased temperature, elevated DIN concentrations and changes in nitrogen:phosphorus ratios can increase the susceptibility of corals to coral bleaching (Wooldridge, 2016;Wooldridge et al., 2017;Vega Thurber et al., 2013;Wiedenmann et al., 2013;D'Angelo and Wiedenmann, 2014). ...
... DIN availability is important in the functioning of the coral-algae symbiosis, and elevated DIN concentrations can cause changes that disrupt the ability of the coral host to maintain an optimal population of algal symbionts (Wooldridge, 2016). Together with increased temperature, elevated DIN concentrations and changes in nitrogen:phosphorus ratios can increase the susceptibility of corals to coral bleaching (Wooldridge, 2016;Wooldridge et al., 2017;Vega Thurber et al., 2013;Wiedenmann et al., 2013;D'Angelo and Wiedenmann, 2014). Fabricius et al. (2013b) propose a conceptual framework that synthesises the apparently inconsistent result of recent studies that suggest either greater or reduced thermal tolerance in response to changes in nutrient status. ...
... Typically, stored lipid reserves in the tissue are utilized when the stable symbiotic environment is disturbed (e.g., Szmant and Gassman, 1990;Ainsworth et al., 2008). Although shortlived, thermally induced bleaching has been linked to depletion of coral lipid reserves (e.g., Hughes and Grottoli, 2013), and excess nutrient loading can also shift the stability of the coral-algae symbiosis, thereby reducing stored tissue reserves (Wooldridge, 2016). According to , up to 11 m 3 d −1 of dissolved inorganic nitrogen are discharged onto the West Maui reef as the result of receiving and treating over 15 000 m 3 d −1 of sewage. ...
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... Large symbiont populations and high organic and lipid reserves may indicate enhanced coral holobiont functioning through higher photosynthetic rates (Browne et al., 2015). Optimal symbiont densities have been suggested to be betweeñ 10 and 30 × 10 5 cells cm − 2 (Wooldridge et al., 2016). All corals of A. tenuis within this study did not exceed the suggested values and symbiont densities peaked in B1 in June 2013 at 18.5 × 10 5 cells cm − 2 , indicating these inshore corals may not be at increased risk of bleaching due to high symbiont densities alone. ...
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Thesis
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In this paper I challenge the notion that a healthy and resilient coral is (in all cases) a fast-growing coral, and by inference, that a reef characterised by a fast trajectory toward high coral cover is necessarily a healthy and resilient reef. Instead, I explain how emerging evidence links fast skeletal extension rates with elevated coral-algae (symbiotic) respiration rates, most-often mediated by nutrient-enlarged symbiont populations and/or rising sea temperatures. Elevated respiration rates can act to reduce the autotrophic capacity (photosynthesis:respiration ratio) of the symbiosis. This restricts the capacity of the coral host to build and maintain sufficient energy reserves (e.g. lipids) needed to sustain essential homeostatic functions, including sexual reproduction and biophysical stress resistance. Moreover, it explains the somewhat paradoxical scenario, whereby at the ecological instant before the reef-building capacity of the symbiosis is lost, a reef can look visually at its best and be accreting CaCO3 at its maximum.
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It is well established that different coral species have different susceptibilities to thermal stress, yet it is less clear which biological or physical mechanisms allow some corals to resist thermal stress, whereas other corals bleach and die. Although the type of symbiont is clearly of fundamental importance, many aspects of coral bleaching cannot be explained solely by differences in symbionts amongst coral species. Here, I use the CO2 (sink) limitation model of coral bleaching to repose various host traits believed to influence thermal tolerance (e.g. metabolic rates, colony tissue thickness, skeletal growth form, mucus production rates, tissue concentration of fluorescent pigments and heterotrophic feedings capacity) in terms of an integrated strategy to reduce the likelihood of CO2 limitation around its intracellular photosymbionts. Contrasting observational data for the skeletal vital effect on oxygen isotope composition (δ18O) partitions two alternate evolutionary strategies. The first strategy is heavily reliant on a sea water supply chain of CO2 to supplement respiratory CO2(met). In contrast, the alternate strategy is less reliant on the sea water supply source, potentially facilitated by increased basal respiration rates and/or a lower photosynthetic demand for CO2. The comparative vulnerability of these alternative strategies to modern ocean conditions is used to explain the global-wide observation that corals with branching morphologies (and thin tissue layers) are generally more thermally sensitive than corals with massive morphologies (and thick tissue layers). The life history implications of this new framework are discussed in terms of contrasting fitness drivers and past environmental constraints, which delivers ominous predictions for the viability of thin-tissued branching and plating species during the present human-dominated (“Anthropocene”) era of the Earth System.
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Coral bleaching occurs when environmental stress induces breakdown of the coral-algae symbiosis and the host initiates algae expulsion. Two types of coral bleaching had been thoroughly discussed in the scientific literature; the first is primarily associated with mass coral bleaching events; the second is a seasonal loss of algae and/or pigments. Here, we describe a phenomenon that has been witnessed for repeated summers in the mesophotic zone (40-63 m) in the northern Red Sea: seasonal bleaching and recovery of several hermatypic coral species. In this study, we followed the recurring bleaching process of the common coral Stylophora pistillata. Bleaching occurred from April to September with a 66% decline in chlorophyll a concentration, while recovery began in October. Using aquarium and transplantation experiments, we explored environmental factors such as temperature, photon flux density and heterotrophic food availability. Our experiments and observations did not yield one single factor, alone, responsible for the seasonal bleaching. The dinoflagellate symbionts (of the genus Symbiodinium) in shallow (5 m) Stylophora pistillata were found to have a net photosynthetic rate of 56.98-92.19 µmol O2 cm(-2) day(-1). However, those from mesophotic depth (60 m) during months when they are not bleached are net consumers of oxygen having a net photosynthetic rate between -12.86 - (-10.24) µmol O2 cm(-2) day(-1). But during months when these mesophotic corals are partially-bleached, they yielded higher net production, between -2.83-0.76 µmol O2 cm(-2) day(-1). This study opens research questions as to why mesophotic zooxanthellae are more successfully meeting the corals metabolic requirements when Chl a concentration decreases by over 60% during summer and early fall.
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Thermally induced bleaching has caused a global decline in corals and the frequency of such bleaching events will increase. Thermal bleaching severely disrupts the trophic behaviour of the coral holobiont, reducing the photosynthetically derived energy available to the coral host. In the short term this reduction in energy transfer from endosymbiotic algae results in an energy deficit for the coral host. If the bleaching event is short-lived then the coral may survive this energy deficit by depleting its lipid reserves, or by increasing heterotrophic energy acquisition. We show for the first time that the coral animal is capable of increasing the amount of heterotrophic carbon incorporated into its tissues for almost a year following bleaching. This prolonged heterotrophic compensation could be a sign of resilience or prolonged stress. If the heterotrophic compensation is in fact an acclimatization response, then this physiological response could act as a buffer from future bleaching by providing sufficient heterotrophic energy to compensate for photoautotrophic energy losses during bleaching, and potentially minimizing the effect of subsequent elevated temperature stresses. However, if the elevated incorporation of zooplankton is a sign that the effects of bleaching continue to be stressful on the holobiont, even after 11 months of recovery, then this physiological response would indicate that complete coral recovery requires more than 11 months to achieve. If coral bleaching becomes an annual global phenomenon by mid-century, then present temporal refugia will not be sufficient to allow coral colonies to recover between bleaching events and coral reefs will become increasingly less resilient to future climate change. If, however, increasing their sequestration of zooplankton-derived nutrition into their tissues over prolonged periods of time is a compensating mechanism, the impacts of annual bleaching may be reduced. Thus, some coral species may be better equipped to face repeated bleaching stress than previously thought.
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Rising ocean temperatures associated with global climate change are causing mass coral bleaching and mortality worldwide. Understanding the genetic and environmental factors that mitigate coral bleaching susceptibility may aid local management efforts to help coral reefs survive climate change. Although bleaching susceptibility depends partly on the genetic identity of a coral's algal symbionts, the effect of symbiont density, and the factors controlling it, remain poorly understood. By applying a new metric of symbiont density to study the coral Pocillopora damicornis during seasonal warming and acute bleaching, we show that symbiont cell ratio density is a function of both symbiont type and environmental conditions, and that corals with high densities are more susceptible to bleaching. Higher vulnerability of corals with more symbionts establishes a quantitative mechanistic link between symbiont density and the molecular basis for coral bleaching, and indicates that high densities do not buffer corals from thermal stress, as has been previously suggested. These results indicate that environmental conditions that increase symbiont densities, such as nutrient pollution, will exacerbate climate-change-induced coral bleaching, providing a mechanistic explanation for why local management to reduce these stressors will help coral reefs survive future warming.
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Impairment of the photosynthetic machinery of the algal endosymbiont ("zooxanthellae") is the proximal trigger for the thermal breakdown of the coral-algae symbiosis ("coral bleaching"). Yet, the primary site of thermal damage is not well resolved. In this perspective essay, I consider further a recent hypothesis which proposes an energetic disruption to the carbon-concentrating mechanisms (CCMs) of the coral host, and the resultant onset of CO2-limitation within the photosynthetic "dark reactions", as a unifying cellular mechanism. The hypothesis identifies the enhanced retention of photosynthetic carbon for zooxanthellae (re)growth following an initial irradiance-driven expulsion event as the cause of the energetic disruption. If true, then it implies that the onset of the bleaching syndrome and setting of upper thermal bleaching limits are emergent attributes of the coral symbiosis that are ultimately underpinned by the characteristic growth profile of the intracellular zooxanthellae; which is known to depend not just on temperature, but also external (seawater) nutrient availability and zooxanthellae genotype. Here, I review this proposed bleaching linkage at a variety of observational scales, and find it to be parsimonious with the available evidence. This provides a new standpoint to consider the future prospects of the coral symbiosis in an era of rapid environmental change, including the now crucial importance of reef water quality in co-determining thermal bleaching resistance.
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Nutrient loading is one of the strongest drivers of marine habitat degradation. Yet, the link between nutrients and disease epizootics in marine organisms is often tenuous and supported only by correlative data. Here, we present experimental evidence that chronic nutrient exposure leads to increases in both disease prevalence and severity and coral bleaching in scleractinian corals, the major habitat-forming organisms in tropical reefs. Over 3 years, from June 2009 to June 2012, we continuously exposed areas of a coral reef to elevated levels of nitrogen and phosphorus. At the termination of the enrichment, we surveyed over 1200 scleractinian corals for signs of disease or bleaching. Siderastrea siderea corals within enrichment plots had a twofold increase in both the prevalence and severity of disease compared with corals in unenriched control plots. In addition, elevated nutrient loading increased coral bleaching; Agaricia spp. of corals exposed to nutrients suffered a 3.5-fold increase in bleaching frequency relative to control corals, providing empirical support for a hypothesized link between nutrient loading and bleaching-induced coral declines. However, 1 year later, after nutrient enrichment had been terminated for 10 months, there were no differences in coral disease or coral bleaching prevalence between the previously enriched and control treatments. Given that our experimental enrichments were well within the ranges of ambient nutrient concentrations found on many degraded reefs worldwide, these data provide strong empirical support to the idea that coastal nutrient loading is one of the major factors contributing to the increasing levels of both coral disease and coral bleaching. Yet, these data also suggest that simple improvements to water quality may be an effective way to mitigate some coral disease epizootics and the corresponding loss of coral cover in the future.