[Coral-List] Algae, DOC, microbes and corals

[John Bruno]

Dear Forest,

Thanks for commenting.  I really think an open dialogue can help move  
this science forward.  Ill try my best to be polite, clear and  
respectful in my response.

I don't entirely understand your points (below) which seem to  
contradict the arguments laid out in your past papers (e.g., Kuntz et  
al 2005, Kline et al 2006, Smith et al 2006, Sandin et al 2008) in  
which you suggested that by increasing benthic DOC concentrations,  
macroalgae influence microbial communities and landscape (whole reef)  
to regional patterns of coral disease including non-infectious  
bleaching.  Your argument (in your corallist post) that the  
hypothesized link between fishing-fish-macroalgae-DOC and coral  
disease only operates over a scale of microns-millimeters seems to me  
to be contradictory to your papers on the subject.  You now appear to  
be arguing for a different sort of mechanism that has more to do with  
macroalgae acting as reservoirs or vectors, requiring direct (or  
nearly so) contact with coral hosts.

You argue that our experiment was flawed because the algae treatments  
were too far away from the corals (> 3 cm), thus precluding microbe/ 
pathogen transfer.  I disagree for several reasons:

1) We were testing the hypothesis that macroalgal exudates (e.g., DOC)  
cause or exacerbate coral diseases.  Therefore we purposefully  
prevented direct contact, shading, abrasion, etc. by the algae (as in  
Box and Mumby 2007).  As outlined in your papers, the underlying  
mechanism does not require microbe/pathogen transfer between the algae  
and the coral host.  The idea is (or was) that by modifying ambient  
DOC, algae alter mucus microbe communities (Kuntz et al 2005, Smith et  
al 2006).

2) Your own work, which you interpreted as supporting a mechanistic  
link between fish, algae and coral disease, also did not include  
direct or proximate contact between corals and algae.  In Smith et al  
(2006) contact between the corals and macroalgae and microbe exchange  
were prevented in the experimental chambers via a 0.02 um filter; "The  
filter is fine enough to prevent the passage of bacteria and viruses  
while still allowing passage of dissolved compounds between the  
compartments." - Smith et al 2006.  In Kuntz et al 2005 and Kline et  
al 2006 there were no macroalgae in the chambers.  In Sandin et al  
2008 reef-wide macroalgal cover was compared to disease prevalence.

3) I don't agree that aquatic microbes, especially in a shallow, high  
flow, coastal environment (e.g., a coral reef), cannot disperse 3 cm  
over two months.  Are you familiar with the Diadema epizootic?  That  
disease/pathogen spread throughout the entire Caribbean in a matter of  
months.  The spatio-temporal dynamics of coral diseases don't suggest  
that the pathogens are unable to disperse.  A gigantic body of science  
defines the dispersal characteristics of passive particles in coastal  
flow environments and it doesn't support your idea of microbe non- 
movement.  Additionally, Thomas Kiorboe has argued that diffusion is  
basically irrelevant for microbes; he thinks they can swim much faster  
than they can diffuse.  Indeed, Mitchell et al (1995) found that  
microswarms of natural marine microbial communities travel at an  
average speed of 230 um/s or 3 cm in ~ 2 min.

4) You might be right about the scale of the effect of macroalgae on  
DOC.  That is concordant with what we found (although we obviously  
cannot rule out a larger-scale effect under different conditions).   
But your statement that "Vu et al completely misses the scale at which  
algae-DOC-microbe-coral dynamics work" isn't supported by any  
published science, other than our paper.  The scale at which algae-DOC- 
microbe-coral dynamics work has not been determined as far as I know  
(please correct me if I am wrong).  One would have to measure  
concentration gradients at varying distances from macroalgae, under  
different flow conditions, using various volumes and species of  
macroalgae in varying states, etc.  A pretty tall order.  This would  
make a great PhD dissertation!

But if algae cannot influence DOC at distances of only a few  
millimeters, as you argued, then isn't it also true that macroalgae  
cannot be an important cause of coral disease?  Even in the Caribbean,  
average macroalgal cover is only about 23%.  In the Pacific it is <  
10% (Bruno et al in press).  Given the relative rarity of macroalgae  
and the purported highly localized sphere of their influence on DOC  
and microbes, how could macroalgae be driving reef-wide, regional and  
indeed global patterns of microbe abundance on coral reefs and in turn  
coral disease and bleaching dynamics?

If you are correct (in arguing that marine microbes cannot move more  
than a few microns-millimeters), a general role for macroalgae as  
reservoirs or vectors of infectious disease also seems unlikely: with  
the exception of rare cases where macroalgal cover is very high,  
direct contact between macroalgae and adult corals is quite rare.  And  
I think we'd all agree that the frequency of existing and new coral  
lesions that occur within microns-millimeters of macroalgae is  
infinitesimally small.  Most disease lesions I have observed (e.g.,  
for black and yellow band) are (and certainly are initiated) in or  
near the center of an adult colony, making direct macroalgal contact  
even less likely.

5) Furthermore, your own work argued that the Fishing-Algae-Disease  
hypothesis does not require any microbe movement - only an increase in  
DOC conc. on the coral surface which would thus influence local  
microbe communities, e.g., in Smith et al (2006) you stated "Our  
results suggest that as human impacts increase and algae become more  
abundant on reefs a positive feedback loop may be created whereby  
compounds released by algae enhance microbial activity on live coral  
surfaces causing mortality of corals and further algal growth."  And  
in Kuntz et al (2005) you stated "We propose that variation in coral  
responses to stressors may be mediated by species-specific dynamics of  
the symbiont community (Rohwer & Kelley 2004), similar to the  
variation observed in bleaching based on zooxanthellae type (Rowan et  
al. 1997, Toller et al. 2001). Additional experiments are needed to  
determine how nutrient and organic carbon loading changes the  
composition and/or dynamics of the coral-associated microbial  
communities."  I.e., both papers concluded that the impacts of algae  
on coral disease were based on exudates (DOC) that hypothetically  
altered the coral mucus community and not via the transfer of  
pathogens from the algae to the corals.

Finally, could you explain your statement that; "In fact, the Vu et  
al. data more closely matches the proposed feedback between algae-DOC- 
microbe-coral (Smith et al. 2006. Ecology Letter), then their own  
conclusions". The reference nails are not in fact "covered with  
algae", as can be seen in the images in the manuscript here: http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0004514
The "bright green line" is microalgae that has colonized the dead  
portion of the coral skeleton.  [There is undoubtedly also some  
microalgae on the nails (and every other non-living surface on the  
reef), but your original hypothesis was about macroalgae, hence the  
link to herbivorous fish and overfishing.]  This is a common  
phenomena: when corals die, no matter the source, their skeletons get  
colonized by such epilithic filamentous turfs, which are common on  
reefs with high grazing pressure (Carpenter 1986), such as Media Luna  
(Diadema are common and macroalgal cover is ~ 2%).  Are you arguing  
that (a) instead of macroalgae, that such light turfs are responsible  
for disease and (b) these early successional turfs are actually the  
cause of coral mortality, and not simply opportunistic colonizers?

Sincerely,

John

>
> Date: Tue, 24 Feb 2009 09:03:36 -0800
> From: Forest Rohwer <frohwer at gmail.com>
> Subject: [Coral-List] Algae, DOC, microbes and corals
> To: Coral-List at coral.aoml.noaa.gov
>
> The recent paper by Vu et al completely misses the scale at which
> algae-DOC-microbe-coral dynamics work. Basically, the authors put  
> algae in
> bags and tacked them to corals. Then they expected the DOC to diffuse
> several centimeters to the corals. In the real world, diffusion only  
> works
> over very small distances. Other factors like mass transport rapidly  
> destroy
> any diffusional signal. In fact, Vu et al show that the DOC  
> enrichment does
> not occur at distances >3 cms from the algae.

>
> The dynamics that need to be investigated at occur in the micron- 
> millimeter
> range. If you look at Figure 1 in the Vu et al. paper, you can  
> clearly see
> the real/important coral-algal interface is the one that occurs  
> against the
> coral (i.e., the bright green line in the photo; not the algae in  
> the bag
> several cm away). Even the reference nails for the disease boundary  
> are
> covered with algae as the coral-algal interface advances. The algae  
> in the
> bag about 3 cms away should not have any influence, which is what the
> authors found. In fact, the Vu et al. data more closely matches the  
> proposed
> feedback between algae-DOC-microbe-coral (Smith et al. 2006. Ecology
> Letter), then their own conclusions.
>
> Similarly, the authors should not expect the algal-associated  
> pathogens (as
> described in a very nice paper by Nugues et al.) to easily "hop"  
> from the
> bagged algae. From a microbial point-of-view, 3 cm represents about  
> 6,000
> body lengths. That would be like a human hopping 10 kms.


John Bruno
Associate Professor
UNC Chapel Hill
www.brunolab.net

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