[Coral-List] Warming makes Symbiodinium selfish

[Scott Wooldridge]

Thank you Mark Warner for your response. In many ways I concur with your
sentiment. As I outlined in my 2013 Biogeosciences manuscript, it is not my
intention to cast any doubt on the central importance of the
photoinhibition model of coral bleaching that you have helped champion.
Indeed, two decades worth of empirical observations overwhelmingly support
the predicted bleaching sequence of algal photoinhibition, oxidative damage
and subsequent zooxanthellae expulsion. This necessitates that some,
perhaps most, of the expelled zooxanthellae will be photodamaged/degraded.
The fact that some are not photodamaged, however, does permit us to
question the prevailing belief that the photosynthetic machinery of the
zooxanthellae is the 'weak link' in the coral bleaching sequence. This
fact, being in addition to other lines of inquiry.


I am always drawn back, again and again, to the excellent study of
Titlyanov et al. (1996), which is so rich in information. This is not a
bleaching study per se. But provides valuable insight into the loss and
replacement of degraded (and healthy) zooxanthellae under normal summer
(high light) conditions. The value of this experiment is that it was
undertaken with natural sunlight (midday >1000 umol.m-2.s-1) and within a
running (seawater flow-through) aquarium. If you are a young scientist, I
urge you to start discriminating the bleaching response experiments you
read by whether the adopted irradiance levels are naturally realistic
(>1000 u.mol.m-2.s-1) levels, whether it is a flow-through aquarium with
seawater taken straight off the reef, and whether the zooxanthelle are
in-symbio or in culture. I contend that only in-symbio experiments with
natural irradiance >1000umol.m-2.s-1 and flow through aquaria provide
useful results for understanding the combined impacts of pCO2, nutrients,
light and temperature on bleaching sensitivity. See Fig. 7 in:

https://www.researchgate.net/publication/317100418_Instability_and_breakdown_of_the_coral-algae_symbiosis_upon_exceedence_of_the_interglacial_pCO2_threshold_260_ppmv_the_%27%27missing%27%27_Earth-System_feedback_mechanism


In this way the Titlyanov et al. (1996) study is very informative. It
highlights that expulsion of degraded zooxanthellae from coral branches is
maximal around the midday peak in irradiance. See their Fig. 5:

https://www.researchgate.net/project/Figures-for-CoralList-responses


This is consistent with the findings from other researchers (Stimson and
Kinzie 1991; Jones and Yellowlees 1997). The value of the Titylanov et al.
(1996) paper, is that they also measured the resultant change in the
proportion of remnant zooxanthellae cells diving, the so called Mitotic
Index (MI, %). In summary, in response to the degraded zooxanthellae being
expelled, the growth of the remnant zooxanthellae increases
proportionately. When plotted for x6 different shallow water species, the
trend is clearly evident. See:

https://www.researchgate.net/project/Figures-for-CoralList-responses


Under normal conditions, this may well be deemed beneficial. But during the
warm high irradiance (doldrum) conditions that precipitates mass bleaching
events it is a massive problem for the coral host, especially in corals
whose resident symbiont population has been unnaturally enlarged by
elevated seawater nutrients and pCO2. This is because the MI(%) of the
zooxanthellae is a crucial parameter for understanding whether the outlined
dynamic expulsion and regrowth process represents a significant carbon
(energy) sink. The problem arises when a large number of zooxanthellae are
expelled (per day) and then subsequently produced (per day). In this case,
as shown by the recent Baker et al. (2018) paper, the zooxanthellae
population becomes a parasite to the coral, i.e. a net carbon sink. An
inverse relationship between between photosynthate transfer and symbiont
MI(%) has also been documented in sea anemones (Verde and McClosky 1996)
and jellyfish (Sachs and Wilcox 2006).


I have previously explained how a warming sea temperature exacerbates this
scenario by thermally enhancing the background MI(%) of the zooxanthellae –
ultimately leading to an uncontrollable (spiralling) loss of zooxanthellae
as host energy reserves progressively diminish across sustained periods of
warming temperature / high light. For summary, see Fig 3:

https://www.researchgate.net/publication/258607389_Breakdown_of_the_coral-algae_symbiosis_Towards_formalising_a_linkage_between_warm-water_bleaching_thresholds_and_the_growth_rate_of_the_intracellular_zooxanthellae/figures


Also interesting from the Titlyanov et al. (1996) paper is the recognition
of a size-based differentiation of various zooxanthellae 'types'. With the
smaller zooxanthellae types having a lower inherent MI(%). As seen by
plotting their findings for shallow coral species:

https://www.researchgate.net/project/Figures-for-CoralList-responses


Like other forms of unicellular algae (e.g. diatoms, Geider et al. 1986)
there appears to exist a general size-dependent relationship, with smaller
zooxanthellae types corresponding with higher MI(%). And confirming the
importance of zooxanthellae MI(%) to the bleaching process, the smaller
(higher MI) types confer lower bleaching tolerance on the coral host, as
compared to the larger (lower MI) types. See Fig. 4 in:

https://www.researchgate.net/publication/258607389_Breakdown_of_the_coral-algae_symbiosis_Towards_formalising_a_linkage_between_warm-water_bleaching_thresholds_and_the_growth_rate_of_the_intracellular_zooxanthellae/figures


The clear implication being, that large, slow growing zooxanthellae types
are an adaptive solution for coral hosts in warm(ing) conditions. However,
as I suggested in my originally post, and has been observed in the field
and lab – this in not a panacea for saving corals from climate change.
Since it presents a problem for the coral. An ideal candidate symbiont
would have a low growth rate during warming conditions. But this would
equally be a poor candidate during 'normal' conditions or back through the
cooler seasons. I have previously discussed these issues:

https://www.researchgate.net/publication/258607389_Breakdown_of_the_coral-algae_symbiosis_Towards_formalising_a_linkage_between_warm-water_bleaching_thresholds_and_the_growth_rate_of_the_intracellular_zooxanthellae


The BIZILLION DOLLAR QUESTION? So how are we meant to interpret  and
respond to what is happening during the present Anthropocene era of
recurrent mass coral bleaching events???? Here is my take, all of which I
have previously published.


Key Point 1: The coral-algae symbiosis has never been mutually beneficial.
It is always in a constant struggle between the partners. Thus, what
we previously
considered to be 'normal' symbiotic functioning wherein the bulk of algae
photosynthates are transferred to the coral host is actually the host
maintaining dominance (a controlled parasitism). See for details:

https://www.researchgate.net/publication/44644540_Is_the_coral-algae_symbiosis_really_%27mutually_beneficial%27_for_the_partners


Key Point 2: This host dominance (controlled parasitism) is predicated on
the capacity of the coral host to constrain the population parameters of
its intracellular algae symbionts (population size and growth rate). Two
environmental attributes interact to conspire against the host. Firstly,
there must be a low seawater availability of inorganic nutrients (N,P)
required for algae growth. Secondly, there must be a low seawater
availability of dissolved CO2 such that the intracellular symbionts are
largely reliant on the coral host to supply the CO2 they need for
photostnthesis. For details, and key nutrient and pCO2 thresholds see:

https://www.researchgate.net/publication/317100418_Instability_and_breakdown_of_the_coral-algae_symbiosis_upon_exceedence_of_the_interglacial_pCO2_threshold_260_ppmv_the_%27%27missing%27%27_Earth-System_feedback_mechanism


https://www.researchgate.net/publication/308746785_Excess_seawater_nutrients_enlarged_algal_symbiont_densities_and_bleaching_sensitive_reef_locations_1_Identifying_thresholds_of_concern_for_the_Great_Barrier_Reef_Australia


Key Point 3: When either of these environmental constraints are not
limiting, the intacellular algae can start to behave as autonomous
parasites, using photosynthetic carbon/energy for their own cellular
growth/multiplication – at the expense of energy sent to the host. This
leads to a destabilisation and ultimate breakdown of the
host-controlled-parasitsim under high light / high temperature conditions.
Thus, the coral host parasitism (under low nutrients/pco2 conditions) is
lost and the algal symbionts regain their “freedom” as they are expelled
(perhaps they have Scottish ancestry like me – that's a joke). Obviously,
the algae nor the host have anthropomorphic intent, and are just responding
to their evolutionary history/responses. And it is easily argued that the
expelled zooxanthellae will not fair well in their new “free” seawater
home. Though still so little is know about this.


Sorry for the length of this diatribe. My hope is that it provokes the
thought process of a younger eager scientist. I am convinced that any slim
hope for saving coral reefs during the Anthropocene lies in understanding
these issues in much more detail than is presently known. It was for this
reason I commend to you the excellent study of Baker et al. (2018) that
initiated my original post. See:

https://www.nature.com/articles/s41396-018-0046-8


scott

https://www.researchgate.net/profile/Scott_Wooldridge



CITED LITERATURE

Geider et al. (1986) Size dependence of growth and photosynthesis in
diatoms: a synthesis. Mar Ecol Progr Ser 30:93-104.

Jones and Yellowlees (1997) Regulation and control of intracellular algae
(=zooxanthellae) in hard corals. Phil Trans Roy Soc Lond B Biol Sci
352:457-468

Sachs and Wilcox (2006) A shift to parasitism in the jellyfish symbiont
Symbiodinium microadriaticum. Proc R Soc Lond B 273:425-429

Stimson and Kinzie (1991) The temporal pattern and release of zooxanthellae
from the reef coral Pocillopora damicornis under nitrogen-enrichment and
control conditions. J Exp Mar Biol Ecol 153:63-74

Titlyanov et al. (1996) (1996) Degradation of zooxanthellae and regulation
of their density in hermatypic corals. Mar Ecol Progr Ser 139:167-178.

Verde and McCloskey (1996) Photosynthesis and respiration of two species of
algae in the Anemone Anthopleura elegantissima. J Exp Mar Biol Ecol
195:187-202


Message: 6
Date: Sat, 10 Feb 2018 16:59:06 +0000
From: "Warner, Mark E." <mwarner at udel.edu>
Subject: Re: [Coral-List] Coral-List Digest, Vol 114, Issue 3
To: "coral-list at coral.aoml.noaa.gov" <coral-list at coral.aoml.noaa.gov>
Message-ID: <1DD9075F-1F79-4564-B9BC-76F9B05B66B9 at udel.edu>
Content-Type: text/plain; charset="us-ascii"

Scott,
Your statement recently posted to the coralist is simply not correct
or supported by the existing data. You make the same erroneous
statement in your 2013 Biogeosciences paper (which you cite on the
list and link to) in which you provide two citations to back up this
statement (Ralph et al. 2001 and Bhagooli and Hidaka 2004). Two
citations do not make a trend or warrant such a blanket statement.

The reality is that the thermal response of many cnidarians is
complicated by many things, including the rate of thermal heating and
the susceptibility of the animal and the resident Symbiodinium. While
it is true that there are some cases of thermal stress resulting in
the rapid expulsion of Symbiodinium that are photochemically unaltered
(I've measured this myself), there are many many other examples of
photochemically damaged Symbiodinium released from heated corals as
well as many studies with cultured Symbiodinium showing their thermal
sensitivity with no host interaction and well within the range of
temperatures known to cause natural bleaching.

Kind regards,
Mark Warner