[Coral-List] Continual failures in experimental designs for determining the impact of symbiont density on coral health and bleaching susceptibility

[Scott Wooldridge]

Dear Coral Listers,



I draw your attention to an excellent recent paper by Krueger et al.
(2020), which confirms the decades long expectation that coral symbionts in
hospite are nitrogen-limited and that their population size is primarily
regulated by nitrogen availability. More controversially, the paper also
explains that “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”.



Krueger et al. (2020) Intracellular competition for nitrogen controls
dinoflagellate population density in corals. Proc Roy Soc Biological
Sciences
https://royalsocietypublishing.org/doi/10.1098/rspb.2020.0049



In layman’s terms, this means that symbiont densities were found to
increase with nitrogen availability, and that gross coral photosynthesis
was found to increase linearly with symbiont density. Which by broad
assumption, can be taken to mean that increased symbiont densities are
beneficial for coral health.



I have previously argued that intracellular carbon (CO2) limitation will
never allow gross coral photosynthesis to continuously increase linearly
with symbiont density. Instead, carbon limitation will ultimately act to
cause coral gross photosynthesis to asymptote with increasing symbiont
density. See Figs. 1,2,3,4 in:



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



An important consequence of this asymptotic response behaviour is the
necessary existence of an metabolic optimum symbiont density for coral
health during summer periods of maximum irradiance and temperatures. And,
that an any excess availability of nitrogen, by enhancing densities beyond
this optimum, reduce coral health and increase bleaching susceptibility.



Now both a linear and asymptotic response model can’t simultaneously be
correct – OR CAN THEY?



Indeed, they CAN both be correct, with an important co-determining factor
being light intensity (i.e. photon flux through the symbionts
photosystems). This should not surprise us, since internal cellular CO2
demand (election sink) is ultimately linked to the total number of
photoreceptors (i.e. symbiont density) and the light-dependent photon flux
rate through these photoreceptors.



The asymptotic nature of this light-dependent behaviour for a given
symbiont density is well illustrated by Fig. 2 in Yentsch et al (2002). See:



http://www.cmep.ca/jcullen/publications/2002/Yentsch_et_al.2002.pdf



Up until a photon flux intensity of ~300-400 umols/m2/s, gross
photosynthesis increases linearly with light intensity. Whilst beyond 400
umols/m2/s gross photosynthesis decreases with increasing light intensity –
presumably in part due to CO2 limitation, as per the findings of Muscatine
et al. (1989) Resource partitioning by reef corals as determined from
stable isotope composition. Mar. Biol. 100:185–93.



It is therefore, absolutely consist to discover that the experiments
undertaken by Kruger et al. (2020) were conducted between 300 – 400
umols/m2/s. The conclusion of Kruger et al (2020) could thus read, “for
light intensities of less than 400 umols/m2/s no symbiont-density-related
metabolic optimum is evident”.



The important thing is that we have an accurate picture of what 300 – 400
umols/m2/s corresponds too in terms of normal summer irradiance conditions,
i.e., when corals are at most risk of CO2-limitation and coral bleaching.
Again, the above Yentsch et al. (2002) paper provides us with excellent
understanding. Their Fig. 3 shows that for the Dry Tortugas, a value of 400
umols/m2/s is only 50% of the typical maximum experienced by a coral at a
depth of 3m, and less than 25% of the maximum experienced by corals in
water depths of less than 1 m. Or put differently, for corals at a depth of
3m, an irradiance level of 300-400 umols/m2/s is typical of that
experienced by corals at 8am in the morning!!!!



Like I have argued previously (see Wooldridge (2017) in link below) if we
want to understand the impacts of symbiont density on coral health and
bleaching susceptibility we need to be using (as a minimum) experimental
irradiance levels of >800-1000 umols/m2/s.



I have spoken at length to the experimental scientists as to why they don’t
use these natural summer irradiance regimes. And the answer always returns,
that at these levels, the corals are not “happy” as they become pale (i.e.
bleach) and die roughly 20 days into experiments. This broadly corresponds
to the time duration we would expect that it would take for somatic host
tissue (energy reserves) to become depleted. Well isn’t that a surprise.
Basically, the symbiont population is behaving as a net energy sink when
irradiance levels exceed 800-1000 umols/m2/s.



But instead of embracing this result, we cheat ourselves of relevant
physiological understanding by continuing to shade our experiments and/or
perform them in winter when irradiance levels are lower and the corals are
“happy”.



It is not my intention to be critical of the Kruger et al. (2020)
manuscript. Rather, I think it is a very good paper. But if we are looking
to extrapolate its relevance for understanding future climate impacts –
then it is rather limited. Indeed, this is true for any experimental work
using irradiance levels of less than 800-1000 umols/m2/s. At the risk of
stirring the pot just a little too hard, I especially draw your attention
to the fantastic and extensive (but misguided) work of the French, who
continue to show us again and again that nutrients and excess symbionts are
beneficial to coral health, whilst always using irradiance values <400
umols/m2/s. Lets be very clear, the CO2-limitation-coral bleaching
mechanism will never be a significant feature of coral physiology at
irradiance levels  <400 umols/m2/s.



My challenge is for use to get real with our experiments.



When we do, I am absolutely certain that the importance of optimal
(light-dependent) symbiont thresholds for coral health and bleaching
susceptibility will become self-evident. Moreover, beyond the identified
importance of excess nutrients in disturbing the delicate balance, the
additional co-importance of ambient seawater CO2 concentration will be
understood as an additional crucial driver. See Figs. 4,5,6,7 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_''missing''_Earth-System_feedback_mechanism



For your consideration,

scott wooldridge