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Instability and breakdown of the coral–algae symbiosis upon exceedence of the interglacial pCO2 threshold (>260 ppmv): the ‘‘missing’’ Earth-System feedback mechanism

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  • Catchment to Reef Management Solutions, Newcastle Australia

Abstract and Figures

Changes in the atmospheric partial pressure of CO2 (pCO2) leads to predictable impacts on the surface ocean carbonate system. Here, the importance of atmospheric pCO2 <260 ppmv is established for the optimum performance (and stability) of the algal endosymbiosis employed by a key suite of tropical reef-building coral species. Violation of this symbiotic threshold is revealed as a prerequisite for major historical reef extinction events, glacial-interglacial feedback climate cycles, and the modern decline of coral reef ecosystems. Indeed, it is concluded that this symbiotic threshold enacts a fundamental feedback mechanism needed to explain the characteristic dynamics (and drivers) of the coupled land-ocean-atmosphere carbon cycle of the Earth System since the mid-Miocene, some 25 million years ago.
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UNCORRECTED PROOF
REPORT
1
2Instability and breakdown of the coral–algae symbiosis
3upon exceedence of the interglacial pCO
2
threshold (>260 ppmv):
4the ‘‘missing’’ Earth-System feedback mechanism
5Scott A. Wooldridge
1
6Received: 19 September 2016 / Accepted: 22 May 2017
7ÓSpringer-Verlag Berlin Heidelberg 2017
8Abstract Changes in the atmospheric partial pressure of
9CO
2
(pCO
2
) leads to predictable impacts on the surface ocean
10 carbonate system. Here, the importance of atmospheric
11 pCO
2
\260 ppmv is established for the optimum perfor-
12 mance (and stability) of the algal endosymbiosis employed by
13 a key suite of tropical reef-building coral species. Violation of
14 this symbiotic threshold is revealed as a prerequisite for
15 major historical reef extinction events, glacial–interglacial
16 feedback climate cycles, and the modern decline of coral reef
17 ecosystems. Indeed, it is concluded that this symbiotic
18 threshold enacts a fundamental feedback mechanism needed
19 to explain the characteristic dynamics (and drivers) of the
20 coupled land–ocean–atmosphere carbon cycle of the Earth
21 System since the mid-Miocene, some 25 million yr ago.
22
23 Keywords CO
2
limitation Coral bleaching Ocean
24 acidification Zooxanthellae density Gaia Drowned reef
25 Introduction
26 The high productivity and extensive accretion of skeletal
27 calcium carbonate (CaCO
3
) by shallow-water tropical reef
28 ecosystems is testament to the evolutionary success of the
29
symbiotic association between scleractinian (reef-building)
30
corals and unicellular dinoflagellate algae of the genus Sym-
31
biodinium (zooxanthellae) (Fig. 1;Stanley2006). Within this
32
association, the zooxanthellae reside in great profusion within
33
the endodermal tissues of the coral host and perform intensive
34
photosynthetic carbon fixation (Electronic supplementary
35
material, ESM, Fig. S1a). Under the optimal conditions pro-
36
vided by warm, nutrient-poor tropical seawater, the majority
37
of this assimilated organic carbon (photosynthate) is translo-
38
cated to the coral, contributing substantially to its energy
39
needs (Yellowlees et al. 2008). Put simply, the energetic
40
advantage from the algal photosymbionts permit reef-building
41
corals to prosper in nutrient-limited tropical environments that
42
otherwise could not support them.
43
The diversification of the coral–algae symbiosis to
44
include the myriad fast-growing branching and plating
45
architectures that dominate modern coral reef ecosystems
46
began *25 million yr ago (Renema et al. 2016). During this
47
period of the Earth’s climate history, the atmospheric partial
48
pressure of CO
2
(pCO
2
) dropped below 260 parts per million
49
by volume (ppmv) for the first time in possibly 250 million
50
yr (Fig. 2; Pearson and Palmer 2000). Since that time, the
51
upper limit of atmospheric pCO
2
has been constrained to
52
return below this threshold upon its exceedence; that is, until
53
the most recent anomalous interference from human-related
54
CO
2
emissions. The impact dynamic of this Earth-System
55
constraint is most graphically detailed across the Pleistocene
56
climate cycles of the past two million yr. During interglacial
57
(warm) periods, such as the Holocene (roughly the past
58
10,000 yr), the atmospheric pCO
2
is typically near
59
260–280 ppmv. During peak glacial (cold) periods, such as
60
the Last Glacial Maximum about 18,000 yr ago, atmo-
61
spheric pCO
2
is 180–200 ppmv, or roughly 80–100 ppmv
62
lower (Fig. 3a; Monnin et al. 2001). The regularity of the
63
pCO
2
variations, and the consistency of the upper and lower
A1 Topic Editor Dr. Anastazia Banaszak
A2 Electronic supplementary material The online version of this
A3 article (doi:10.1007/s00338-017-1594-5) contains supplementary
A4 material, which is available to authorized users.
A5 &Scott A. Wooldridge
A6 swooldri23@gmail.com
A7
1
Catchment to Reef Management Solutions, PMB 5, Belmont,
A8 NSW 2280, Australia
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Coral Reefs
DOI 10.1007/s00338-017-1594-5
Author Proof
UNCORRECTED PROOF
64 termination limits through multiple 100-kyr cycles (Fig. 3b;
65 Sigenthaler et al. 2005) are suggestive of a well ordered, but
66 currently unexplained (‘‘missing’’) set of dominant control
67
mechanisms—the so-called holy grail of Earth-System sci-
68
ence (Sigman and Boyle 2000).
69
Due to rapid air–sea gas exchange, atmospheric pCO
2
is
70
directly linked to the dissolved seawater CO
2(aq)
concen-
71
tration in the upper ocean (Najjar 1992). Indeed, it is
72
generally agreed that oceanic processes must ultimately
73
regulate glacial–interglacial changes in atmospheric pCO
2
74
(Broecker and Henderson 1998). The fundamental mech-
75
anism(s) underpinning this coupling, however, remains a
76
source of considerable debate (Archer et al. 2000; Sigman
77
and Boyle 2000). One suite of mechanisms that can alter
78
atmospheric pCO
2
by a sufficient extent is to change the
79
alkalinity of the whole ocean. Alkalinity, in particular
80
carbonate ion (CO
3
2-
), is added to the ocean largely by the
81
weathering of emergent carbonates on land and is removed
82
largely by the biogenic precipitation and burial of CaCO
3
.
83
The climatic relevance of ocean-wide alkalinity changes
84
arises as a consequence of the aqueous carbonate equilib-
85
rium operating in the ocean:
CO2þCO2
3þH2O,2HCO
3ð1Þ
8787For example, any increase in [CO
3
2-
] at the ocean
88
surface will induce lower atmospheric CO
2
by shifting the
89
aqueous carbonate equilibrium to the right. In this way, an
90
inverse relationship exists between surface [CO
3
2-
] and
91
pCO
2
, which helps to explain: (1) why CaCO
3
deposition
92
by coral reefs is a source of CO
2
to the atmosphere
93
(Frankignoulle et al. 1994; Kawahata et al. 1997); and (2)
94
why large-scale demise of shallow-water coral reef CaCO
3
95
production, by increasing [CO
3
2-
] at the ocean surface,
96
acts to lower atmospheric pCO
2
with a ‘‘carbonate com-
97
pensation’ time *2.5 kyr (Berger 1982).
Fig. 1 a Often called ‘‘rainforests of the sea’’ shallow-water tropical
coral reefs are built by, and made up of thousands of tiny animals,
coral polyps. bCoral polyps have a sac-like body and an opening, or
mouth, encircled by tentacles. The polyp uses calcium and bicarbon-
ate ions from seawater to build itself a hard, protective (cup-shaped)
skeleton made of calcium carbonate (CaCO
3
). The brilliant colour of
corals comes from the zooxanthellae (tiny algae) living inside their
tissues. Several million zooxanthellae live in just one square inch of
coral. The photosynthetic pigments contained within the zooxanthel-
lae are visible through the clear body of the polyp and are what gives
corals their colour
Fig. 2 Evolutionary history of modern tropical corals. A mid-
Miocene explosion of coral species that adopt fast-growing, branch-
ing and plating growth forms opened up new ecospace for the
evolution of the myriad of creatures that now comprise modern coral
reefs. The origination event coincided with global cooling and a fall
in pCO
2
below 260 ppmv for the first time in possibly 250 million yr.
Late Cenozoic extinction and origination events on Caribbean coral
reefs are synchronised around this 260 ppmv threshold. Note, the
pCO
2
reconstruction is based on the lower-bound, error-considered
predictions of Pearson and Palmer (2000)
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98 Recently, Wooldridge (2012) invoked this biophysical
99 linkage between coral CaCO
3
production and atmospheric
100 pCO
2
to propose widespread coral reef mortality as the
101 biological agent responsible for the consistent interglacial
102 pCO
2
termination limit. In this scenario, known low-lati-
103 tude coral ‘‘reef gaps’’ in the geological record when
104 pCO
2
[260 ppmv (e.g. between 11.5 and 9 kyr BP; Fig. 3a
105 after Montaggioni 2000,2005;*125 kyr BP; Kiessling
106 et al. 2012) are attributed to periods of global coral mor-
107 tality that would have resembled modern global mass coral
108 bleaching events (as per Sheppard 2003; Wooldridge et al.
109 2005). Significantly, new evidence from the analysis of
110 fossil corals that were alive during this period supports the
111
existence of extensive mass coral bleaching *11.5 kyr BP
112
(Dishon et al. 2015). Such coherence between prediction
113
and observation suggests that further investigation into the
114
theory outlined by Wooldridge (2012) is warranted.
115
In this paper, I synthesise new experimental evidence
116
that significantly improves the biological underpinnings of
117
the interglacial coral reef demise hypothesis of Wooldridge
118
(2012). In particular, the new evidence provides mecha-
119
nistic support for the extreme bleaching sensitivity of a key
120
suite of tropical reef-building coral species due to the
121
combination of pCO
2
[260 ppmv, nutrient-replete seawa-
122
ter conditions, and elevated low-latitude insolation (*100-
123
kyr Milankovitch cycle-scale; Fig. 3c). Beyond providing a
Fig. 3 Pleistocene climate
cycles. aDeglacial rise in
atmospheric pCO
2
as recorded
by ice core samples at
Antarctica Dome C (Monnin
et al. 2001). A notable ‘‘reef
gap’’ in the geological record
corresponds with exceedence of
pCO
2
[260 ppmv between 11.5
and 9 kyr BP (Montaggioni
2000,2005). bExtended
records of atmospheric pCO
2
highlight the consistency of the
upper and lower termination
limits through multiple 100-kyr
cycles (Sigenthaler et al. 2005).
cMaximum daily mean
insolation at tropical latitudes
through multiple 100-kyr
Milankovitch cycles
(Ashkenazy and Gildor 2008)
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124 new level of determinism for the coupled land–ocean–at-
125 mosphere carbon cycle of the Earth System, the improved
126 biological understanding helps to explain the global demise
127 of modern coral reef ecosystems, including the labelling of
128 many important reef-building species as the ‘‘living dead.’
129 Symbiont densities influence coral bleaching
130 susceptibility
131 The interglacial coral reef demise hypothesis of Wool-
132 dridge (2012) builds on recent advancements in the theo-
133 retical conception of the coral–algae endosymbiosis. Far
134 from being strictly beneficial, the ‘‘producer-in-consumer’
135 arrangement of the coral–algae symbiosis is increasingly
136 conceived as a dynamic reciprocal exploitation (Wool-
137 dridge 2010; Lesser et al. 2013). In this way, the nature of
138 the symbiotic interaction can readily switch from beneficial
139 to parasitic (for either partner) depending on specific
140 (changeable) environmental conditions that differentially
141 favour either partner.
142 For example, enrichment of seawater with an excess of
143 bioavailable nutrients can inhibit the ability of the coral
144 host to maintain demographic control of its algal sym-
145 bionts, resulting in an enlarged, fast-growing symbiont
146 population that is ultimately a net carbon sink (parasite) for
147 the energetic resources of the coral (Wooldridge
148 2013,2016). In this case, as densities increase, the photo-
149 synthetic capacity per zooxanthella (P) progressively de-
150 creases due to CO
2
limitation and self-shading within the
151 host cell, while the associated respiratory/maintenance cost
152 to the symbiosis (R) increases (linearly) per zooxanthella
153 added (Fig. 4; Anthony et al. 2009; Hoogenboom et al.
154 2010). In this way, it is understood that there exists an
155 optimum zooxanthellae density that maximises the auto-
156 trophic capacity (P:R) of the symbiosis, i.e. every zoox-
157 anthella added beyond this optimum reduces the potential
158 autotrophic energy transferred to the coral host.
159 For thin-tissued genera with branching and plating
160 morphologies (e.g. Acropora,Stylophora,Seriatopora and
161 Pocillopora) the optimum symbiont density for building
162 host energy reserves is *1.0–1.5 910
6
algal cells cm
-2
163 of host tissue (Wooldridge 2016). This specific density is
164 commonly observed in a wide range of tropical cnidarian–
165 dinoflagellate symbioses (Fig. 5a; Drew 1972). In terms of
166 the symbiotic architecture, this corresponds to a single
167 zooxanthella cell per host (gastrodermal) cell, the so-called
168 cell-specific density (CSD, Muscatine et al. 1998). For
169 many tropical cnidarian–dinoflagellate symbioses, a
170 CSD &1 can thus be understood to maximise light har-
171 vesting and minimise intraspecific competition for resour-
172 ces, such as intracellular CO
2
. Nutrient enrichment acts to
173 disrupt this optimal configuration, with the CSD
174
typically [2–3 (i.e. doublet and triplets predominate)
175
(Muscatine et al. 1998).
176
Healthy corals with a CSD &1 build superior host
177
tissue energy reserves, which makes them better equipped
178
to combat prolonged periods of stress, e.g. due to thermal
179
stress and bleaching (Wooldridge 2016; Wooldridge et al.
180
2017). Nutrient-enriched corals with excess zooxanthellae
181
have lower host tissue energy reserves, bleach more
182
severely, and bleach at lower temperatures (Wooldridge
183
2016; Wooldridge et al. 2017). This response profile is
184
graphically portrayed by the field observations of Cunning
185
and Baker (2013) who tracked symbiont densities in
186
Pocillopora damicornis colonies (n=53) across a
Fig. 4 Energetic benefit that reef-building corals receive from their
algal partner is not always guaranteed. Elevated seawater nutrient
concentrations that permit enlarged zooxanthellae population densi-
ties can ultimately cause photo-autotrophic energy transfers to decline
as aphotosynthetic energy gains (P) decrease, whilst bthe respiratory
costs (R) of hosting ‘‘excess’’ zooxanthellae increase with each
zooxanthella added. cThe metabolic optimum zooxanthellae density
coincides with a maximum P:R ratio. Details of the methods used to
collect this dataset are outlined in Hoogenboom et al. (2010). For the
coral samples used, an optimal zooxanthellae density of 0.9 910
6
cells (mg protein)
-1
corresponds with *1.8 910
6
zooxanthellae
cells cm
-2
of host tissue
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187 4-month summer warming period (Fig. 5b). In this case,
188 colonies with near-optimal zooxanthellae densities
189 (*1.2 910
6
algal cells cm
-2
) experienced no zooxan-
190 thellae loss across the warming period. In contrast, the
191 degree of zooxanthellae loss (bleaching) was directly
192 related to the pre-stress number of zooxanthellae over the
193 optimum level in colonies that had enlarged zooxanthellae
194 densities.
195 In tropical reef locations, elevated zooxanthellae den-
196 sities are commonly associated with an excess of
197 bioavailable dissolved inorganic nitrogen (DIN =ni-
198 trate ?nitrite ?ammonium). On the Great Barrier Reef
199 (Australia), the specific DIN threshold of concern
200 is *1lM (Bell 1992), which is linked with a seawater
201 concentration of chlorophyll-a[0.45 lgL
-1
(Wooldridge
202 et al. 2015; Wooldridge 2016). Reef locations that peri-
203 odically exceed this threshold are *2–4 times more sen-
204 sitive to bleaching at each progressive level of thermal
205 stress (Wooldridge 2016). Nutrient-enriched run-off from
206 land use dominated by human agricultural activities is the
207 most common source of nutrient excess on coastal reefs
208 (Wooldridge et al. 2006). However, exceedence of
209 chlorophyll-a[0.45 lgL
-1
can equally be triggered by
210 natural shelf-edge upwelling events (Wooldridge et al.
211 2017). Crucially, the residual symbiotic impact of a nutri-
212 ent spike due to a flood plume or upwelling can last for
213 several months (ESM Fig. S2; Falkowski et al. 1993). This
214 means that exposed corals remain pre-conditioned with
215 high thermal bleaching sensitivity well beyond the physical
216 occurrence of the specific enrichment events.
217 Beyond the role of nutrients, the symbiotic possibility of
218 maintaining algal densities in excess of the metabolic
219 optimum has also been theoretically linked to a sufficient
220
seawater concentration of dissolved CO
2(aq)
needed for the
221
‘dark reactions’’ of algal photosynthesis (Wooldridge
222
2012). By analogy, this constraint is highlighted by the
223
growth dynamics of the free living unicellular alga Du-
224
naliella viridis when subject to external seawater manipu-
225
lations of CO
2(aq)
and ammonium (NH
4
?
) (Gordillo et al.
226
2003). In this case, elevated NH
4
?
only acts to significantly
227
increase algae cell densities under conditions of CO
2(aq)
228
sufficiency (ESM Fig. S3). The intracellular location of
229
zooxanthellae makes the direct demonstration of this sea-
230
water CO
2(aq)
impact more difficult. Yet, Wooldridge
231
(2012) argues that the constraints imposed on the intra-
232
cellular zooxanthellae by the (intermediary) CO
2
supply
233
mechanisms of the coral host can be used to establish the
234
fundamental importance of excess dissolved seawater
235
CO
2(aq)
in permitting symbiont densities beyond the opti-
236
mum level.
237
Specifically, Wooldridge (2012) explains that although
238
seawater CO
2(aq)
can freely diffuse across the lipid bilayers
239
of the coral host, at typical seawater pH (8.1), it represents
240
only a small fraction (1–2%) of the dissolved inorganic
241
carbon (DIC) available from seawater. The much more
242
abundant HCO
3
-
, however, is largely inhibited from dif-
243
fusing into the host cells due to its ionic charge. To
244
enhance the delivery of CO
2(aq)
to its endosymbionts, many
245
coral species thus implement a range of CO
2
-concentrating
246
mechanisms (CCMs), which facilitate the dehydration of
247
HCO
3
-
into CO
2
in the presence of carbonic anhydrase
248
(CA) (ESM Fig. S4). The CCMs provide access to the large
249
pool of seawater HCO
3
-
, but require the expenditure of
250
metabolic energy in the form of adenosine triphosphate
251
(ATP). For most symbiotic corals, the ATP needed to
252
activate the CCMs is ultimately derived from the
Fig. 5 a Symbiont densities *1.0–1.5 910
6
algal cells cm
-2
of
host tissue represent a metabolic optimum for a wide range of tropical
cnidarian–dinoflagellate symbioses, including the sea anemone Aip-
tasia sp. (Starzak et al. 2014). Note, a P:R \1 when integrated over a
24-h period indicates that more organic carbon is consumed by the
symbiosis than was produced. bCorals with optimum zooxanthellae
densities build superior host tissue energy reserves that are better
equipped to combat prolonged periods of thermal stress with no
bleaching (Cunning and Baker 2013; for additional details see ESM
A)
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UNCORRECTED PROOF
253 transferred photosynthates of the zooxanthellae (Al-Horani
254 et al. 2003). This metabolic link ensures that the zooxan-
255 thellae indirectly play a role in generating the CO
2(aq)
that
256 they themselves require for photosynthesis, thus repre-
257 senting a strong disincentive for zooxanthellae to shift
258 towards parasitism (cheating). In essence, stability is
259 maintained because ‘‘exploiters’’ become victims of their
260 own success. If the zooxanthellae fail to transfer energy to
261 the host, they generate local selection, i.e. intracellular CO
2
262 limitation ?expulsion ?replacement (ESM Fig. S1b;
263 Wooldridge 2009,2010).
264 This CCM disruption ?CO
2
limitation bleaching
265 mechanism makes obvious that any ‘‘excess’’ zooxanthellae
266 supported beyond the maximum autotrophic energy status
267 (P:R) of the coral symbiosis (=metabolic optimum) must not
268 be using HCO
3
-
as their CO
2
source. If they were, the
269 maximum zooxanthellae density should stabilise around the
270 P:R maximum dehydration rate of seawater HCO
3
-
271 achieved by the ATP-dependent host CCMs. Instead, any
272 ‘excess’’ zooxanthellae must be supported by the dissolved
273 seawater CO
2(aq)
fraction of seawater DIC. Seawater CO
2(aq)
274 is transferred between the host and the surrounding water via
275 diffusion, with this diffusive flux being inversely propor-
276 tional to the boundary layer thickness and directly propor-
277 tional to the bulk seawater CO
2(aq)
concentration (Denny
278 1988). Despite representing only a small component (1–2%)
279 of the available seawater DIC at present seawater pH (8.1),
280 [CO
2(aq)
] has nonetheless risen almost twofold between the
281 early 1800s (pCO
2
*280 ppmv) and present day
282 (pCO
2
*400 ppmv), and is projected to increase fourfold
283 by 2100 (pCO
2
*750 ppmv) (Wolf-Gladrow et al. 1999).
284 Not every symbiotic coral relies solely on photo-au-
285 totrophic energy transfers to power the ATP-dependent
286 CCMs (Wooldridge 2014a). Isotopic evidence suggests
287 that, in general, the most reliant species are characterised
288 by fast-growing, thin-tissued branching and plating mor-
289 phologies (e.g. Acropora,Stylophora,Seriatopora and
290 Pocillopora), while the least reliant species are charac-
291 terised by slow-growing, thick-tissued massive and
292 mounding morphologies (e.g. Porites, Faviids) (Wool-
293 dridge 2014a). Enhanced heterotrophic feeding capacity
294 and/or the ability to catabolise stored tissue reserves in
295 thick-tissued massive and mounding morphologies is a
296 likely contributor this response, among other biophysical
297 attributes (Wooldridge 2014a). Indeed, Wooldridge
298 (2014b) explained that catabolism of heterotrophic carbon
299 sources provides both an additional cellular energy source
300 for the ATP-dependent CCMs and a reliable (continuous)
301 supply of metabolic CO
2
. In this way, the ability to draw on
302 heterotrophic carbon can help to forestall the predicted
303 onset of intracellular CO
2
limitation during periods of
304 autotrophic stress, thereby enhancing bleaching resistance
305 (Wooldridge 2014b).
306
This distinction delivers a biophysical mechanism for
307
the general dichotomy that corals with branching mor-
308
phologies (and thin tissue layers) are generally more ther-
309
mally sensitive than corals with massive morphologies
310
(and thick tissue layers) (c.f. Loya et al. 2001). Put simply,
311
branching and plating species are at much greater risk from
312
the disruptive influence of an enhanced ‘‘passive’’ supply
313
of CO
2(aq)
, since it provides the opportunity for an ever
314
increasing (‘‘excess’’) proportion of the zooxanthellae
315
population to exist beyond the metabolic optimum imposed
316
by the photosynthate feedback operation of the CCMs.
317
In essence, the ‘‘excess’’ fraction is released from host
318
control to behave as parasitic freeloaders. Far from benign,
319
they are easily conceived to destabilise the optimal func-
320
tioning of the symbiosis, since they would be extremely
321
vulnerable to intracellular CO
2
limitation during periods of
322
excessive irradiance-driven CO
2(aq)
demand, particularly
323
when coupled with a flow-mediated reduction in passive
324
CO
2(aq)
supply. Notably, this physical combination is the
325
characteristic feature of the doldrum weather conditions
326
that normally precede mass bleaching events (Gleason and
327
Wellington 1993). Indeed, the CCM disruption ?CO
2
-
328
limitation bleaching mechanism projects that, at best
329
(moderate ocean surface temperature ?moderate irradi-
330
ance), the continuous daily turnover (expulsion ?(re)-
331
growth) of the CO
2
-limited portion of the zooxanthellae
332
population greatly reduces the capacity of the coral host to
333
build energy storage reserves (e.g. as needed to combat
334
stress and disease). At worst (anomalous ocean surface
335
temperature ?extreme irradiance ?low water move-
336
ment), a self-perpetuating cycle of zooxanthellae expulsion
337
is triggered that escalates into extreme coral bleaching and
338
mortality (ESM Fig. S5; Wooldridge 2009,2013,2014a).
339
Enlarged (suboptimal) symbiont densities require
340
pCO
2
>260 ppmv and nutrient-replete seawater
341
conditions
342
Experimental data are essential for substantiating these
343
theoretical arguments. Here, I synthesise the findings from
344
recently published laboratory experiments that improve the
345
validation of the central tenets of the CCM disrup-
346
tion ?CO
2
-limitation coral bleaching mechanism
347
(Wooldridge 2009), and thus, also improve the biological
348
underpinning of the interglacial coral reef demise hypoth-
349
esis (Wooldridge 2012). Specifically, the data confirm that:
350
(1) for thin-tissued tropical branching species, the optimal
351
symbiotic configuration converges to a CSD &1
352
(*1.0–1.5 910
6
algal cells cm
-2
), and (2) any ‘‘excess’’
353
zooxanthellae beyond this optimum level require atmo-
354
spheric pCO
2
[260 ppmv in addition to nutrient-replete
355
seawater conditions.
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356 For an experimental design to be considered suitable for
357 testing the CCM disruption ?CO
2
-limitation bleaching
358 mechanism, several criteria are necessary. First, the seawater
359 supply in the treatments must be nutrient replete to permit
360 algal proliferation (i.e. mitotic cell division). Second,
361 changes in the dissolved CO
2(aq)
concentration of the sea-
362 water supply should be achieved naturally by infusing CO
2
-
363 enriched or CO
2
-depleted air. Third, the adopted tempera-
364 ture and irradiance scheme should not trigger excessive
365 intracellular CO
2(aq)
demand/limitation (e.g. typical of
366 summer bleaching conditions), but rather be characteristic of
367 non-bleaching, tropical winter-to-spring conditions (i.e.
368 water temperature \26 °C; irradiance \450 lmol pho-
369 tons m
-2
s
-1
)(Yentschetal.2002). Finally, the experiment
370 must be run long enough (weeks not days) to ensure that
371 zooxanthellae demographic parameters have sufficient time
372 to stabilise in response to changing seawater parameters.
373 Two studies currently exist that meet these experimental
374 criteria. The first study was undertaken at the Monaco
375 Oceanographic Institute using colonies of the branching tropi-
376 cal coral Stylophora pistillata (Reynaud et al. 2003). The
377 study was conducted in covered aquaria for 5 weeks (temper-
378 ature =25 °C, irradiance =380 lmol photons m
-2
s
-1
,
379 photoperiod 12:12). Although the nutrient status of the exper-
380 imental seawater was not specified, earlier studies using the
381 identical experimental set-up describe DIN concentrations
382 of *1lM (Grover et al. 2002), a threshold commonly seen as
383 representing nutrient-enriched conditions in tropical coral reef
384 ecosystems (Bell 1992;Lapointeetal.1993). The second study
385 wasundertakenattheHeronIslandResearchStationusing
386 colonies of the branching tropical coral Acropora millepora
387 (Kaniewska et al. 2015). This study was conducted in outdoor
388 aquaria, and also ran for 5 weeks (temperature =24 °C,
389 average irradiance =430 lmol photons m
-2
s
-1
,
390
photoperiod 12:12). In this case, the seawater supply was taken
391
straight from a reef flat with a known nutrient-replete lagoonal
392
seawater source (Hoegh-Guldberg et al. 2004).
393
Notably, by plotting the impact of pCO
2
enrichment on
394
symbiont densities from both studies, the theoretical pre-
395
dicted significance of the pCO
2
*260 ppmv threshold for
396
maintaining optimal symbiont densities under nutrient-re-
397
plete conditions is clearly established (Fig. 6a). Put simply,
398
‘excess’’ zooxanthellae beyond the optimum level also
399
requires atmospheric pCO
2
[260 ppmv.
400
pCO
2
<260 ppmv reduces the risk of coral
401
bleaching regardless of nutrient status
402
Two suitable experimental studies also exist to confirm the
403
associated bleaching risk initiated by the ‘‘excess’’ zoox-
404
anthellae fraction, especially when coupled with summer
405
irradiance and surface temperature regimes. Both studies
406
were undertaken at the Heron Island Research Station and
407
employed the same nutrient-replete lagoonal seawater
408
source as Kaniewska et al. (2015).
409
The first of these studies was run for 8 weeks, using
410
colonies of the branching tropical coral Acropora inter-
411
media (Anthony et al. 2008). Notably, the adopted seawater
412
temperatures were warmer (25–29 °C) and irradiance
413
levels higher (noon irradiance [1000 lmol pho-
414
tons m
-2
s
-1
). In this case, the impact of pCO
2
enrichment
415
was manifested through its impact upon bleaching sensi-
416
tivity, with maximum bleaching observed in the highest
417
pCO
2
treatments, and minimal bleaching predicted for
418
pCO
2
\260 ppmv, even at 28–29 °C (Fig. 6b).
419
The theoretical prediction that this bleaching risk is
420
mediated by intracellular CO
2
limitation initiated by the
Fig. 6 a pCO
2
enrichment of nutrient-replete Acropora millepora
and Stylophora pistillata colonies indicates that ‘‘excess’’ zooxan-
thellae beyond the optimal density (*1.0–1.5 910
6
algal cells
cm
-2
) requires atmospheric pCO
2
[260 ppmv (for additional details
see ESM B). bpCO
2
enrichment of nutrient-replete Acropora
intermedia colonies causes the severity of coral bleaching to increase
at a constant temperature (28–29 °C) (Anthony et al. 2008). Minimal
bleaching is predicted when pCO2 \260 ppmv
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421 ‘excess’’ zooxanthellae fraction is given support by the
422 finding of the second study. In this case, colonies of the
423 branching tropical coral Acropora formosa were removed
424 from Heron Island reef flat (Crawley et al. 2010). Based on
425 observations at the same location (viz. Anthony et al. 2008;
426 Kaniewska et al. 2015), it is reasonable to assume that the
427 symbiont densities within these A. formosa colonies were
428 initially elevated beyond the optimal range. Notably, for
429 present-day conditions (pCO
2
*400 ppmv), the photo-
430 synthetic apparatus of the intracellular zooxanthellae were
431 significantly CO
2
-limited at typical summer irradiance
432 levels ([925 lmol photons m
-2
s
-1
) (Crawley et al.
433 2010). An identical result has been described for the
434 ‘bleaching-sensitive’’ La Saline reef (La Re
´union Island,
435 western Indian Ocean; Naim 1993). At this reef site,
436 nutrient-enriched groundwater discharge (mainly nitrate)
437 supports an enlarged (*3 times) zooxanthellae population
438 that is CO
2
-limited at normal summer irradiance levels
439 (Chauvin et al. 2011).
440 Thus, when considered from the theoretical standpoint
441 provided by the CCM disruption ?CO
2
-limitation coral
442 bleaching model (ESM Fig. S1b), the new suite of exper-
443 imental data helps to repose coral ‘‘bleaching risk’’ in terms
444 of an envelope of environmental conditions that is incon-
445 gruous with the ability of the coral host to maintain
446 demographic control of its algal partner, which is funda-
447 mental for ensuring that the net benefit of hosting algal
448 symbionts exceeds the associated costs (Wooldridge
449 2010). This envelope, which may subsequently be refined
450 by targeted (species-specific) experiments, currently indi-
451 cates the following preconditions: pCO
2
[260 ppmv,
452 DIN [1lM, sea surface temperature (SST) [28 °C, and
453 irradiance [925 lmol photons m
-2
s
-1
(Fig. 7). It is
454 important to note that the use of minimum (absolute) SST
455 and irradiance thresholds represents a simplifying proxy for
456 the dynamics of the bleaching process, which is a more
457 integrated relationship involving the time (days to weeks)
458
above specific SST and irradiance combinations for a given
459
Symbiodinium ‘type’’ (for further details see Wooldridge
460
2013).
461
Limiting any one of these environmental preconditions
462
may help forestall the risk of coral bleaching, which helps
463
to explain why worldwide reef locations that exhibit high
464
([33 °C) bleaching thresholds are united by strongly
465
oligotrophic surface waters during the warm summer
466
months [e.g. northern Red Sea—no summer river run-off
467
(Fine et al. 2013); western Pacific warm pool—restricted
468
upwelling due to strong thermal stratification (Barber and
469
Chavez 1991)]. It is also likely to explain the conflicting
470
results of pCO
2
enrichment experiments on branching
471
corals at the Institute for Marine Science (Eliat, Israel)
472
research facility, which draws its water supply from the
473
nutrient-limited surface water of the northern Red Sea. For
474
example, after a 6-month incubation period at 25 °C,
475
colonies of S. pistillata showed no significant change in
476
zooxanthellae densities in response to elevated pCO
2
477
conditions, even at pCO
2
[2000 ppmv (Krief et al. 2010).
478
A new narrative for interglacial termination
479
sequences
480
Most tropical coral reefs that existed just prior to 11.5 kyr
481
BP are at present encountered as ‘‘drowned’’ relict features
482
and terraces at depths of 40–70 m along the outer edges of
483
most tropical continental shelves (reviewed by Montag-
484
gioni 2000,2005). The new bleaching risk construct
485
(Fig. 7) strengthens the original hypothesis of Wooldridge
486
(2012), which links this drowning event with the demise of
487
symbiotic corals that employ active CCMs. Specifically,
488
the new construct predicts, and observational evidence
489
supports (Dishon et al. 2015), a high likelihood of extreme
490
bleaching and mortality events at tropical reef locations
491
during the period that bounds the resultant ‘‘reef gap’
Fig. 7 Representation of the
nutrient, pCO
2
and sea surface
temperature (SST)/irradiance
threshold conditions that govern
the risk profile for mass coral
bleaching. Limiting any one of
these environmental
preconditions can help forestall
the risk of coral bleaching
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492 (11.5–9 kyr BP). For example, pCO
2
exceeds the
493 260 ppmv threshold (Fig. 3a, b), and irradiance levels
494 exceed the 925 lmol photons m
-2
s
-1
threshold (Fig. 3c).
495 Equally important, proxy records indicate that surface
496 nutrient concentrations were significantly enriched (Hal-
497 lock and Schlager 1986), as driven by an intensification of
498 equatorial upwelling during the Younger Dryas event (YD,
499 from 12.9 to 11.7 kyr BP) (Hughen et al. 1996; Kienast
500 et al. 2006; Calvo et al. 2011; Kubota et al. 2014). This
501 change in upwelling rate (and hence nutrient supply) dur-
502 ing the YD is linked to increased trade-wind strength,
503 which in turn, is influenced by predictable SST-related
504 alterations in thermohaline circulation patterns (c.f.
505 Hughen et al. 1996).
506 Previous explanation for the reef drowning event
507 at *11.5 kyr BP has centred on a proposed rapid rise in
508 sea level associated with an ice-melt discharge (so-called
509 meltwater pulse 1B; Fairbanks 1989). However, the global
510 extent and significance of this sea level rise is controversial
511 and contested, especially in terms of its exclusive role in
512 halting reef growth (Bard et al. 2010; Stanford et al. 2010).
513 Part of the confusion in interpreting the eustatic sea level/
514 reef accretion record may relate to the (bleaching-induced)
515 mortality response predicted herein. For example, at rare
516 sites where continuous glacial–interglacial reef growth is
517 recorded (e.g. nutrient-limited Vanuatu; Cabioch et al.
518 2003), an abrupt rise in sea level *11.5 kyr BP is inferred
519 by the rapid change in the shallow-water community
520 composition from a branching Acropora-dominated
521 assemblage, to (an assumed deeper) massive Porites-
522 dominated assemblage. Yet this rapid community switch is
523 equally predicted by the proposed differential selection
524 against branching growth forms as seawater pCO
2
exceeds
525 260 ppmv. Similarly, for the Caribbean fossil reef record, a
526 rapid rise in sea level *11.5 kyr BP is predicated on
527 Acropora palmata colonies remaining in their usual 1–5-m-
528 depth habitat. However, it is an expectation of the new
529 bleaching risk construct that branching corals will be dri-
530 ven deeper (=lower irradiance) to combat pCO
2
[260 -
531 ppmv and nutrient-replete conditions. Notably, A. palmata
532 is known to be capable of surviving at depths down to 20 m
533 (Hubbard 2009).
534 Wooldridge (2012) outlined a consequential sequence
535 by which large-scale coral bleaching/mortality of low-lat-
536 itude reefs between 11.5 and 9 kyr BP would terminate the
537 post-glacial rise in pCO
2
, including the likely duration of
538 the present interglacial. The key response driver is the
539 ocean alkalinity equilibrating mechanism of ‘‘carbonate
540 compensation’ (Eq. 1; Broecker and Peng 1987; Hodell
541 et al. 2001), which dictates that the geological signature of
542 low-latitude reef demise between 11.5 and 9 kyr BP is
543 ultimately recorded in the deep-sea CaCO
3
preservation
544 record and its associated link to global atmospheric pCO
2
.
545
In summary, for ocean basins linked to the transport of
546
tropical waters: (1) reef demise starting at 11.5 kyr BP
547
triggers a transient increase in surface water alkalinity (i.e.
548
increased [CO
2
-3
]), as evidenced by a conspicuous increase
549
in the productivity of calcifying plankton (e.g. coccol-
550
ithophores; Flores et al. 2003); (2) shallow-to-deep ocean
551
ventilation of this high-alkalinity water mass with a mixing
552
lag of *2.5 kyr (Berger 1982) acts to deepen the calcite
553
lysocline around 7–9 kyr BP, as evidenced by a deep-sea
554
CaCO
3
preservation event (Broecker et al. 1993; Hodell
555
et al. 2001; Marchitto et al. 2005; Klo
¨cker and Henrich
556
2006); (3) the inverse relationship between the carbonate
557
ion content of the deep ocean and atmospheric pCO
2
558
(Broecker and Peng 1987) links this lysocline deepening
559
with the recorded drawdown in atmospheric pCO
2
between
560
7 and 9 kyr BP. It this way, the timing of major global
561
cooling (e.g. the 8.2 kyr BP cooling event; Alley et al.
562
1997) is consistent with the proposed reef demise-triggered
563
pCO
2
drawdown sequence.
564
Are modern branching corals ‘‘the living dead’’?
565
Because of their fast growth and high abundance, branch-
566
ing and plating corals contribute disproportionately to
567
CaCO
3
production on modern tropical reefs. For example,
568
predictions based on model data indicate that carbonate
569
production in healthy reef systems is cut by half after the
570
loss of branching corals (Perry et al. 2012). Prior to the
571
post-Miocene explosion of branching morphologies (i.e.
572
pCO
2
\260 ppmv), coral communities were dominated by
573
slow-growing, thick-tissued massive and encrusting growth
574
forms (Edinger and Risk 1995).
575
The post-Miocene origination and differential success of
576
branching versus massive corals species fits with the theory
577
outlined herein, which identifies fast-growing corals with
578
active CCMs (e.g. branching corals) as optimal and
579
stable competitors when constrained by pCO
2
\260 ppmv
580
(Fig. 7). However, their enhanced vulnerability to nutrient
581
enrichment when pCO
2
[260 ppmv is further reinforced
582
by the Caribbean extinction event (*50% of reef-building
583
corals) at the Pliocene–Pleistocene boundary
584
(pCO
2
*300 ppmv; Fig. 2), which culminated in a peak
585
extinction rate from 2–1 Ma (Budd and Johnson 1999;
586
Budd 2000). Consistent with expectation, species with
587
massive or platy shapes were much more likely to survive
588
than species with free living or branching shapes (Johnson
589
et al. 1995; Budd and Johnson 1999). The conditional
590
importance of nutrient enrichment in addition to
591
pCO
2
[260 ppmv for initiating the demise/extinction of
592
branching corals is supported by fossil data showing that
593
global reef locations that are most depleted in surface
594
nutrients (e.g. Sinai, northern Red Sea; Vanuatu, western
Coral Reefs
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595 Pacific warm pool) did not experience region-wide
596 extinction events across the entire Pleistocene (Mewis
597 2016).
598 The transferred logic can be employed to understand the
599 global demise of thin-tissued branching and plating species
600 during the present human-dominated (Anthropocene) era of
601 the Earth System (see, e.g. Renema et al. 2016). The new
602 bleaching risk construct (Fig. 7) makes clear that increas-
603 ing SST ([28 °C) and rising pCO
2
([400 ppmv) are
604 incongruous to the long-term persistence of branching
605 coral communities in nutrient-replete (i.e. coastal or
606 upwelling) settings. Or conceptualised differently, warm-
607 ing ocean temperatures and rising pCO
2
[400 ppmv have
608 served to make previously acceptable seawater nutrient
609 levels (e.g. DIN [1lM) now unacceptable and destabil-
610 ising to the underpinning coral–algae symbiosis. The
611 preferential loss of branching coral communities in nutri-
612 ent-replete settings has been well documented. For exam-
613 ple, upwelling coral reef ecosystems in the tropical eastern
614 Pacific (e.g. Galapagos, Panama) were among the first to
615 experience widespread mass coral bleaching and mortality
616 dating back to the early 1980s (Glynn 1990). The simplest
617 inference is that a global extinction event is already
618 underway that has the potential to rival the Pliocene–
619 Pleistocene and Oligocene–Miocene events.
620 The new bleaching risk construct (Fig. 7) also makes
621 clear which global reef locations are best positioned to
622 function as refuge areas for bleaching-sensitive branching
623 and plating corals—specifically, reef locations with a
624 limited supply of external nutrients from river run-off or
625 upwelling, especially during the warmer summer period
626 (e.g. northern Red Sea, western Pacific warm pool). It
627 remains to be seen whether successful agricultural man-
628 agement practices can be implemented at the regional scale
629 necessary to return enriched coastal nutrient levels below
630 the critical threshold (see, e.g. Wooldridge et al.
631 2012,2015,2017). Mesotrophic (deeper, lower light) reef
632 habitats may offer some benefits, but periods of above-
633 average surface irradiance combined with clear water
634 transparency could still trigger deleterious bleaching events
635 at great depths if nutrients are not limiting (Nir et al. 2014).
636 Whether symbiotic corals are optimal competitors for
637 available substratum at deeper depths is also not obvious
638 (reviewed by Bongaerts et al. 2010).
639 Future prospects
640 The theory and observational evidence outlined in this
641 manuscript support the conclusion that for roughly
642 20 million yr before recent anthropogenic interference the
643 stability of Earth’s atmospheric CO
2
concentration below
644 260–280 ppmv was maintained by the symbiotic
645
functioning of a key suite of tropical reef-building corals.
646
This is an intriguing proposition on many levels.
647
First, that such a large-scale Earth-System feedback
648
mechanism can result from natural selection of an environ-
649
ment-altering trait at the individual level is truly remarkable.
650
Second, in terms of Pleistocene climate cycles, this proposi-
651
tion draws attention to the fundamental importance
652
of *100 kyr low-latitude (tropical) insolation cycles
653
(Fig. 3c; Berger et al. 2006; Ashkenazy and Gildor 2008).
654
This is despite the well-observed fact that glacial–interglacial
655
climate variability is much greater in the polar regions (e.g.
656
Northern Hemisphere glaciations). Indeed, beyond its sug-
657
gested role in interglacial termination sequences
658
(pCO
2
*260–280 ppmv), the coherence of equatorial inso-
659
lation with the *100 kyr periodicity of glacial–interglacial
660
climate cycles (Fig. 3c) also alludes to the fundamental
661
importance of a tropical driver for the opposing
662
glacial ?interglacial climate transition (pCO
2
*180–200
663
ppmv). Increased coral reef growth (beyond glacial minima)
664
in response to increasing sea level (substrate availability) and
665
growth temperatures has previously been highlighted as a
666
positive internal feedback within the Earth’s climate system
667
(Berger 1982;Ridgwelletal.2003;VecseiandBerger2004).
668
While palaeoceanographic evidence argues against coral reef
669
growth being the sole contributor to the 80–100 ppmv dif-
670
ference in atmospheric pCO
2
between glacial and interglacial
671
periods, the importance of imposed constraints on reef-
672
building corals, be they biological (interglacial symbiosis
673
breakdown) or environmental (reduced glacial substrate
674
availability), does provide a holistic explanation for both
675
termination sequences.
676
Finally, at a more profound level, the identified impor-
677
tance of a biological system component (i.e. symbiotic
678
corals) for maintaining the Earth’s atmospheric CO
2
con-
679
centration within a homeostatic range optimal for biolog-
680
ical life leads to arresting questions as to the why of
681
science. Most evolutionary biologists tend to minimise the
682
question of ‘‘why’’ by resting in the randomness and
683
chance that underpins the evolutionary process. Yet could
684
it be that the Earth System, by design or otherwise, actively
685
pursues homeostatic balance with the goal of keeping
686
conditions optimal for life (c.f. Lovelock and Margulis
687
1974)? This intriguing proposition is left for future debate.
688
689
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... There is an optimal symbiont density at which the coral host benefits most from translocation of excess photosynthetic carbon products, reflected by the highest ratio between symbiont photosynthesis and holobiont respiration (Hoogenboom et al. 2010;Wooldridge 2017). Notwithstanding this, the symbiont density range that is suited for a mutualistic symbiosis is wide and varies among coral and symbiont species. ...
... This effect is exacerbated under thermal stress. When symbiont respiration increases under increasing temperatures, the translocation of organic carbon to the host will be even further reduced to a critical level where the symbionts become commensalistic and maybe even parasitic instead of mutualistic (Wooldridge 2017;Baker et al. 2018). Such a shift towards a parasitic symbiosis has often been proposed to be a prelude to thermal bleaching (Cunning and It is not well known if corals can adapt to excessive enrichment with nutrients. ...
Article
Ocean warming has severe impacts on coral reef ecosystems with frequent incidences of coral bleaching. In addition, eutrophication poses an increasing threat to coral reef environments and has been found to increase the vulnerability of corals to thermal bleaching. Eutrophication has accelerated in recent years with coastal nutrient loads expected to continue to increase under global change. However, the mechanisms by which nutrient pollution affects corals and coral reefs are still under debate, in particular with regard to nitrogen. The main objective of this paper is to review mechanisms by which nitrogen pollution affects coral health and corresponding strategies to reduce the impact of nitrogen pollution. Different coral species possess varying tolerance thresholds for nitrogen enrichment and corals show differential responses to enrichment with nitrate and ammonium. Nitrate assimilation increases oxidative stress in corals, promotes growth of the phototrophic symbionts in corals, and induces phosphate starvation in these symbionts, which further impairs the symbiosis. In contrast, a moderate supply of ammonium is mostly beneficial for coral development. In addition, combined nitrogen and phosphorous enrichment can indirectly compromise coral health by enhancing macroalgae growth and increasing the incidence of coral diseases caused by predation on corals. It must be realized that both levels of nutrient pollution and the stoichiometric ratios of C: N: P: Fe availabilities determine the ultimate effect of nutrients on coral health. We confirm the strategy to conserve coral reefs via coral-targeted water quality management, in particular by including a reduction of the nitrate influx and by proper management of fish stocks to facilitate healthy reef ecology.
... Alternatively, an increased number of symbiont cells may not maximize host benefits as high densities of commensal symbionts may not equal the high densities of more selfish symbionts in terms of net benefits to the host coral. A reduction in nutrient translocation at elevated temperatures by symbionts has been postulated in other Symbiodiniaceae-coral symbioses (Cunning & Baker 2014;Wooldridge 2017) but not demonstrated with experimentally evolved symbionts. However, studies examining nutrient translocation in wild-type symbionts show changes in carbon and nitrogen can coincide with bleaching events, suggesting changes in translocation and the nutrient dynamics may be part of host-symbiont rebalancing upon exposure to heat stress Cui et al. 2019). ...
... no increased growth Restoration Ecology or survival). The lack of improvement in growth and survival at 32.5 C in SS-juveniles but maintenance of photosynthetic efficiencies suggests that heat conditioning may have induced SS to share less photosynthate, which has been documented in other systems including insects (Bronstein 1994;Herre et al. 1999;Wooldridge 2017). Other factors such as light can also influence the ability for symbionts to survive in response to temperature stress, as seen in corals sourced from inshore locations (Jones et al. 2016). ...
Full-text available
Article
Projected increases in sea surface temperatures will exceed corals' ability to withstand heat stress within this century. Experimental evolution of cultured symbionts (Symbiodiniaceae) at high temperatures followed by reintroduction into corals can enhance coral heat tolerance. Several studies have selected for enhanced tolerance in Cladocopium goreaui (C1) over multiple timescales and then compared the performance of coral juveniles infected with the heat‐tolerant C1 selected strain (SS) to the performance of juveniles infected with the C1 wild type (WT). To derive lessons about host benefits when symbionts are experimentally selected, here we compare the performance of SS‐and WT‐juveniles after 21 cell generations of heat selection versus longer periods (73–131) in recently published experiments. After 21 generations, we found rapid improvement in heat tolerance of SS through an overall shift in the mean tolerance to temperature. This did not translate to improved growth and survivorship of the coral. Specifically, survival did not differ significantly between juveniles of Acropora tenuis hosting WT versus SS at any temperature. Juveniles infected with WT exhibited greater skeletal growth than those infected with SS at 27 and 31°C but not at 32.5°C. SS‐juvenile symbiont cell densities increased significantly at 27°C relative to SS‐juveniles in the 31°C and 32.5°C. Photosynthetic efficiencies in SS‐juveniles were higher compared to WT‐juveniles at 31°C, equal at 27°C and lower at 32.5°C. These results suggest that selection over longer generation (>130) times will be needed to confer host benefits and will be dependent on the stability of this association being maintained in nature. This article is protected by copyright. All rights reserved.
... Coral reefs are tropical marine ecosystems with exceptionally high productivity and biodiversity Carpenter et al. 2011;Rinkevich 2015;Wooldridge 2017). Reef-forming (scleractinian) corals have an important role in life underwater as well as for the many human communities which depend on the ecosystem services they provide (Hoegh-Guldberg et al. 2019;Woodhead et al. 2019). ...
... Reef-forming (scleractinian) corals have an important role in life underwater as well as for the many human communities which depend on the ecosystem services they provide (Hoegh-Guldberg et al. 2019;Woodhead et al. 2019). However, the condition of coral reefs is in decline, due to many disrupting factors, most of which are related to direct and indirect anthropogenic activities such as the effects of destructive fishing, increased nutrient concentrations and pollution due to landbased activities, sedimentation, marine debris, anthropogenic climate change, and ocean acidification, all of which threaten their geo-ecological and provisioning functions (Green et al. 2014;Hoegh-Guldberg et al. 2019;Wooldridge 2017;Perry and Filip 2019;Woodhead et al. 2019). Marine tourism can also pose threats to coral reefs, not only from direct damage (e.g. ...
Full-text available
Article
Scleractinian corals can reproduce in several ways, with two main sexual reproduction modes known as brooding and broadcast spawning. In this study, we described patterns of genetic variation within and connectivity between coral populations in western Indonesia (Seribu Archipelago), central Indonesia (Spermonde Archipelago), and eastern Indonesia (Ambon). We sampled two readily identifiable corals popular in the marine aquarium trade, one species widely reported as a brooder (Euphyllia glabrescens), the other as a broadcast spawner (Lobophyllia corymbosa). The mitochondrial COI genome was amplified for 117 samples. Within-population genetic variation was high, especially at the eastern Indonesia (Ambon) site. The genetic connectivity patterns were similar for the two corals, with high connectivity between the Seribu and Spermonde Archipelagos (despite a geographical separation of more than 1,000 km) and a lack of connectivity between these two sites and Ambon. These results indicate a potential barrier to gene flow between coral populations in western/central Indonesia and those to the east of Sulawesi Island.
... Coral reefs are tropical marine ecosystems with exceptionally high productivity and biodiversity Carpenter et al. 2011;Rinkevich 2015;Wooldridge 2017). Reef-forming (scleractinian) corals have an important role in life underwater as well as for the many human communities which depend on the ecosystem services they provide (Hoegh-Guldberg et al. 2019;Woodhead et al. 2019). ...
... Reef-forming (scleractinian) corals have an important role in life underwater as well as for the many human communities which depend on the ecosystem services they provide (Hoegh-Guldberg et al. 2019;Woodhead et al. 2019). However, the condition of coral reefs is in decline, due to many disrupting factors, most of which are related to direct and indirect anthropogenic activities such as the effects of destructive fishing, increased nutrient concentrations and pollution due to landbased activities, sedimentation, marine debris, anthropogenic climate change, and ocean acidification, all of which threaten their geo-ecological and provisioning functions (Green et al. 2014;Hoegh-Guldberg et al. 2019;Wooldridge 2017;Perry and Filip 2019;Woodhead et al. 2019). Marine tourism can also pose threats to coral reefs, not only from direct damage (e.g. ...
Full-text available
Article
Scleractinian corals can reproduce in several ways, with two main sexual reproduction modes known as brooding and broadcast spawning. In this study, we described patterns of genetic variation within and connectivity between coral populations in western Indonesia (Seribu Archipelago), central Indonesia (Spermonde Archipelago), and eastern Indonesia (Ambon). We sampled two readily identifiable corals popular in the marine aquarium trade, one species widely reported as a brooder (Euphyllia glabrescens), the other as a broadcast spawner (Lobophyllia corymbosa). The mitochondrial COI genome was amplified for 117 samples. Within-population genetic variation was high, especially at the eastern Indonesia (Ambon) site. The genetic connectivity patterns were similar for the two corals, with high connectivity between the Seribu and Spermonde Archipelagos (despite a geographical separation of more than 1,000 km) and a lack of connectivity between these two sites and Ambon. These results indicate a potential barrier to gene flow between coral populations in western/central Indonesia and those to the east of Sulawesi Island.
... It should be noted that despite the fluctuations in local nutrient assimilation due to density, the potential for long-range (at the scale of centimetres) as well as directed transport to regenerating tissue are macroscale phenomena that demonstrate that the host is not exclusively influenced by localized input [61][62][63]. The previous suggestion about an optimal symbiont density to meet the metabolic demands of their coral host [64] was not confirmed here. The concept of a 'metabolic optimum' [64] still has insufficient data support, mainly due to the limited number of measured colonies and due to the lack of a clear differentiation between oxygen production and carbon assimilation when relating photosynthesis to density. ...
... The previous suggestion about an optimal symbiont density to meet the metabolic demands of their coral host [64] was not confirmed here. The concept of a 'metabolic optimum' [64] still has insufficient data support, mainly due to the limited number of measured colonies and due to the lack of a clear differentiation between oxygen production and carbon assimilation when relating photosynthesis to density. The crucial and yet unresolved issue is whether coral gross photosynthesis responds linearly (this study) [12,65] or asymptotically [66,67] to symbiont density. ...
Full-text available
Article
The density of dinoflagellate microalgae in the tissue of symbiotic corals is an important determinant for health and productivity of the coral animal. Yet, the specific mechanism for their regulation and the consequence for coral nutrition are insufficiently understood due to past methodological limitations to resolve the fine-scale metabolic consequences of fluctuating densities. Here, we characterized the physiological and nutritional consequences of symbiont density variations on the colony and tissue level in Stylophora pistillata from the Red Sea. Alterations in symbiont photophysiology maintained coral productivity and host nutrition across a broad range of symbiont densities. However, we demonstrate that density-dependent nutrient competition between individual symbiont cells, manifested as reduced nitrogen assimilation and cell biomass, probably creates the negative feedback mechanism for symbiont population growth that ultimately defines the steady-state density. Despite fundamental changes in symbiont nitrogen assimilation, we found no density-related metabolic optimum beyond which host nutrient assimilation or tissue biomass declined, indicating that host nutrient demand is sufficiently met across the typically observed range of symbiont densities under ambient conditions.
... Coral bleaching occurs when increases in sea-surface temperature (SST) cause a disruption in functioning of symbiotic algae, Symbiodiniaceae, that live within the coral tissue and are the primary source of energy for corals (Muscatine 1990;Gates et al. 1992). Loss of symbionts results in coral host mortality if SSTs persist at levels above a local bleaching threshold (Gates et al. 1992;Wooldridge 2017). Corals will usually bleach 2-6 weeks after elevated SSTs and coral mortality can occur in the subsequent 2-20 weeks (Baird and Marshall 2002). ...
Article
Coral reefs are degrading worldwide. This study explored the benthic community structure (biotic and abiotic benthic cover and coral composition) at three islands (Rasdhoo, Maayafushi and Vihamaafaru) in the central Maldivian archipelago, 2 years after the 2016 El Niño–Southern Oscillation (ENSO) and the associated mass-bleaching events. Hence, we assessed benthic cover on the same GPS sites and depth (10 m) of a subset of reefs that had been previously studied. The islands represent a range of management categories and oceanic influence. Average live coral cover in 2018 was lowest on Maayafushi reefs (0.65±0.41%), a resort island with minimal exposure to oceanic influence. At Rasdhoo, a community island with south-eastern oceanic exposure, live coral cover was 14.70±3.20% and 90% of the colonies were less than 20 cm in diameter. At Vihamaafaru, an uninhabited island with oceanic exposure from the west, reefs assessed had a live coral cover of 17.9± 6.80%, Acropora spp. remained the dominant taxa, and 35% of colonies were 20 cm or greater in diameter. This evident trend, in variation of live coral cover and size of the coral colonies, among the three island settings indicates the greatest potential for recovery of coral cover on reefs with more exposure to oceanic influence.
... Coral reefs, rich in both biodiversity and economic value, are severely affected by global change (4). The branching and plating corals that have been the dominant carbonate producers and framework builders on tropical coral reefs for almost 2 million years may be "living dead" in the midst of a major Anthropocene extinction event (5). ...
Full-text available
Article
Observations of coral reef losses to climate change far exceed our understanding of historical degradation before anthropogenic warming. This is a critical gap to fill as conservation efforts simultaneously work to reverse climate change while restoring coral reef diversity and function. Here, we focused on southern China’s Greater Bay Area, where coral communities persist despite centuries of coral mining, fishing, dredging, development, and pollution. We compared subfossil assemblages with modern-day communities and revealed a 40% decrease in generic diversity, concomitant to a shift from competitive to stress-tolerant species dominance since the mid-Holocene. Regions with characteristically poor water quality—high chl-a, dissolved inorganic nitrogen, and turbidity—had lower contemporary diversity and the greatest community composition shift observed in the past, driven by the near extirpation of Acropora. These observations highlight the urgent need to mitigate local stressors from development in concert with curbing greenhouse gas emissions.
... During the growth of Reef 4, proxy records show an increase in global and Pacific pCO 2 (Kubota et al., 2014;Monnin et al., 2001) as the vertical accretion rate decreases. Wooldridge (2012Wooldridge ( , 2017 attempted to link an apparent gap in the reef record around this time, from 11.5 to 9 ka, with two factors: the exceedance of the optimal pCO 2 threshold for algal endosymbiosis with corals (pCO 2 < 260 ppm) and the high nutrient concentration in the ocean. ...
Article
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... Global increases in seawater temperature have triggered extensive coral bleaching and mass mortality events across most tropical regions (Baker, Glynn, & Riegl, 2008). Bleaching is a stress response that implies the loss of photosynthetically active dinoflagellate algae (zooxanthellae) from their hermatypic coral hosts and results in reduced calcium carbonate accretion (Gates, Baghdasarian, & Muscatine, 1992;Wooldridge, 2017). While corals can recover from moderate bleaching, severe or prolonged bleaching is often lethal. ...
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Global climate change has increased the frequency and intensity of extreme heat anomalies and consequent mass coral bleaching events. Long term dynamics of hard coral cover, bioconstruction potential, carbonate deposition, and reef accretion were monitored over a 20‐year period on Maldivian coral reefs in order to investigate the effects of high‐temperature anomalies on coral reef accretion and their recovery potential. Changes experienced by shallow reefs between 1997 and 2017 were evaluated by considering five different bioconstructional guilds and the BioConstruction Potential index (BCP), a proxy for the constructional capacity of reefs. Abnormally high temperatures in 1998 and 2016 led to severe coral bleaching and consequent mortality, especially of the primary builders. Renewed carbonate deposition was not documented until 2‐3 years after the bleaching, and 6‐9 years passed until constratal (i.e., low relief) growth was achieved. Finally, 14‐16 years were required to reach accretion rates high enough to ensure superstratal (i.e., high relief) growth. Coral mortality in the Maldives during the 2016 bleaching event was lower than in 1998, and the initial recovery was faster and occurred via a different trajectory than in 1998. Rising levels of anthropogenic carbon emissions are predicted to accelerate sea level rise and trigger severe coral bleaching events at least twice per decade, a frequency that will 1) prevent coral recovery, 2) nullify reef accretion, and, consequently 3) result in the drowning of Maldivian reefs under the worst climate projections. This article is protected by copyright. All rights reserved.
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The scleractinian coral is common along the Red Sea coast, and its reproductive mode and period of reproduction were assessed using histological preparations. the sexuality, and reproductive mod timing of reproductive of pocillopora damicornis from adjacent to the fringing reefs of the Ubhur Creek in the Red Sea, were assessed using a serial histological section. Sexual reproduction in pocillopora damicornis a shallow water hermatypic coral was studied from December 2011 to November 2012. pocillopora damicornis is a simultaneous hermaphrodite with ovary and testis in the project into the body cavity on the same mesentery. Sperm and eggs were usually released simultaneously from the same polyp. The onset of the reproductive period of pocillopora damicornis was found to be limited (April to May). In the number of eggs and testes observed in this period, the gonads were found in the polyps. The pocillopora damicornis egg size ranged from 49.80 µm (in March) to 125.0 µm (in May). Four stages were chosen, to reflect very immature ovaries, the early stages of oocyte development, ova near maturity, and mature ova, and also four distinct stages of sperm development were identified. The state of gonads development (eg. testis and eggs) was measured by a calibrated eyepiece micrometer of a compound light microscope. Zooxanthellae were presented in the mature oocytes in pocillopora damicornis. This study aimed to examine the reproduction mode and timing of pocillopora damicornis.
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While biogeochemical and physical processes in the Southern Ocean are thought to be central to atmospheric CO2 rise during the last deglaciation, the role of the equatorial Pacific, where the largest CO2 source exists at present, remains largely unconstrained. Here we present seawater pH and pCO2 variations from fossil Porites corals in the mid equatorial Pacific offshore Tahiti based on a newly calibrated boron isotope paleo-pH proxy. Our new data, together with recalibrated existing data, indicate that a significant pCO2 increase (pH decrease), accompanied by anomalously large marine (14)C reservoir ages, occurred following not only the Younger Dryas, but also Heinrich Stadial 1. These findings indicate an expanded zone of equatorial upwelling and resultant CO2 emission, which may be derived from higher subsurface dissolved inorganic carbon concentration.
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Coral reefs occupy only ~ 0.1 percent of the ocean's habitat, but are the most biologically diverse marine ecosystem. In recent decades, coral reefs have experienced a significant global decline due to a variety of causes, one of the major causes being widespread coral bleaching events. During bleaching, the coral expels its symbiotic algae, thereby losing its main source of nutrition generally obtained through photosynthesis. While recent coral bleaching events have been extensively investigated, there is no scientific data on historical coral bleaching prior to 1979. In this study, we employ high-resolution femtosecond Laser Ablation Multiple Collector Inductively Coupled Plasma Mass Spectrometry (LA-MC-ICP-MS) to demonstrate a distinct biologically induced decline of boron (B) isotopic composition (δ11B) as a result of coral bleaching. These findings and methodology offer a new use for a previously developed isotopic proxy to reconstruct paleo-coral bleaching events. Based on a literature review of published δ11B data and our recorded vital effect of coral bleaching on the δ11B signal, we also describe at least two possible coral bleaching events since the Last Glacial Maximum. The implementation of this bleaching proxy holds the potential of identifying occurrences of coral bleaching throughout the geological record. A deeper temporal view of coral bleaching will enable scientists to determine if it occurred in the past during times of environmental change and what outcome it may have had on coral population structure. Understanding the frequency of bleaching events is also critical for determining the relationship between natural and anthropogenic causes of these events.
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