[Coral-List] Heat;light, food, and bleaching, continued

Thomas Goreau goreau at bestweb.net
Fri Apr 13 13:51:43 EDT 2007

Estimado Pedro,

Thanks for your comments and reinvigorating this discussion, I'm just  
back from coral reef restoration projects in Micronesia and Polynesia  
and I had not seen many of the comments below. You are absolutely  
right that little is known and much more needs to be done on both  
carbon and energy metabolism in both bleached and normal corals, but  
this has never been a fad issue with funding agencies.

My parent's first work on the fate of C-14 incorporated by  
zooxanthella photosynthesis in the early 1950s showed that the coral  
retained very little of the released carbon, almost all went into  
mucus release. Later biochemical work (Trench and Muscatine, Cooksey  
& Cooksey, Battey & Patton, etc.) confirmed that almost all  
zooxanthellae release to the host were precursor biochemicals used in  
mucus synthesis. The loss of these precursors causes a much greater  
energy drain on bleached corals that must release mucus to deal with  
sedimentation and other stresses, and almost certainly changes the  
amount and chemical composition of mucus and the cost to the coral of  
producing it.

Since corals are specialized for different types of zooplankton prey  
(something we have long known, but which you won't find in the "peer"  
"reviewed" literature), their ability to make up loss of this will  
depend on their nutrition from predation. The heavy loss of mucus in  
bleaching must impose severe limitations on coral and their nutrition  
and environment must affect their ability to replace this. There is  
very little good work on this, but Andrea Grottoli and colleague's  
work is an important start.  A recent paper in Nature on the  
biochemical utilization of mucus release of corals by Wild et al. was  
done on corals that were releasing exceptional levels of mucus  
because they were in the first stages of severe bleaching, but this  
abnormal condition was not noticed by the authors, the reviewers, or  
the editors, who refused to publish our comment pointing this out!

In the late 1980s Ray Hayes and I took samples of coral mucus from  
bleached and unbleached portions of corals in Jamaica and Cayman,  
which were analyzed for the microbial community by Kim Ritchie and  
Garriet Smith. We found large amounts of a previously unknown Vibrio  
species on the mucus of bleached Montastrea annularis and Porites or  
Acropora (as I remember, I don't have it here) that did not occur on  
mucus of the unbleached portions of the same colonies. In 1991 we  
found large amounts of the same Vibrio found in the Caribbean on the  
mucus of bleached Acropora, Porites, and Montastrea in the South  
Pacific that again did not occur on the mucus from unbleached potions  
of the same colony. We published a couple of papers on this in the  
microbiological literature about 15 years ago. We assumed the Vibrio  
was an opportunist specializing on the mucus of changed composition,  
but were not able to follow through with biochemical measurements.  
Several types of Vibrio has been known to be abundant on coral mucus  
since the pioneering work of Hugh Ducklow and Ralph Mitchell in the  
early 1970s.

Later Rosenberg, Loya, Ben Haim, Kushmaro and colleagues found Vibrio  
associated with bleached corals and claimed it to be the cause of  
bleaching. We suspected (incorrectly) at the time it was probably the  
likely opportunist we had found rather than the cause of bleaching.  
Later work with James Cervino, Ray Hayes, Garriet Smith, Shawn and  
Sara Poulson, Rob Martinez, Fabiano Thompson, and myself have found  
another set of Vibrios closely related to the pathogenic shellfish  
poisoning Vibrios which cause Yellow Band Disease in Caribbean  
Monstastreas and in several other Pacific genera, and we have shown  
that this is not bleaching at all in that there is no expulsion of  
the algae. Instead the bacteria attack the zooxanthellae in situ and  
cause programmed cell death (apoptosis). Ben Haim and Rosenberg have  
since confirmed that the same takes place with their different Vibrio  
strains. So those Vibrios are a zooxanthella (not coral) disease, not  
bleaching, and quite separate from the opportunistic Vibrios on the  

Furthermore the ways in which carbon and energy are partitioned will  
differ between corals with different trophic pathways (an issue non  
long known to coral researchers but essentially absent from the  
published literature except for a paper by Jim Porter on niche  
partitioning by surface to volume ratios of polyps in the early 1970s  
and Grottoli et al's more recent work). Zac Forsman just showed me  
his experiments in Honolulu two days ago with the same species  
(Porites compressa and Montipora capitata)  that Andrea Grottoli  
worked on, and he has found (working I think with Cindy Hunter and  
Bob Richmond) that they also respond very differently to light stress  
and the speed of water circulation. Clearly there is much more to be  


On Apr 12, 2007, at 9:59 AM, Pedro Alcolado wrote:

> Dear Tom,
> Just today, quite late, I had the opportunity to read this  
> discussion chain.
> I think that in spite that the non bleached coral uses carbon fixed  
> by zooxanthellae to produce mucus, the bleached coral will still  
> need to produce mucus constantly, and then will be forced to get  
> Carbon from its reserves, tissue or zooplankton or other planktonic  
> source. I surmise that a bleached coral that stop producing mucus  
> would be in trouble. For that reason, under normal condition carbon  
> fixing by zooxantellae could be considered as an indirect carbon  
> source for coral tissue, as the coral will not need to use carbon  
> from their reserves or tissue for producing mucus when bleached.  
> Carbon fixed by zooxantellae is then involved in the whole carbon  
> budget of the coral by avoiding use of carbon from the coral tissue  
> for producing mucus. What for me seems to happens is that mucus and  
> tissue production seem to be functionally compartmentalized in non- 
> bleached coral, but not in bleached ones.
> You know my English is imperfect, so excuse me if my comment is not  
> clear enough.
> If you think it is worth you can share this message with the  
> colleagues involved in that nice discussion.
> Hugs,
> Pedro
> ----- Mensaje reenviado ----
> De: Georgina Bustamante <gbustamante at bellsouth.net>
> Para: Pedroyahoo <pmalcolado at yahoo.es>
> Enviado: jueves, 1 de junio, 2006 8:39:35
> Asunto: FW: [Coral-List] Heat;light, food, and bleaching, continued
> -----Original Message-----
> From: coral-list-bounces at coral.aoml.noaa.gov
> [mailto:coral-list-bounces at coral.aoml.noaa.gov]On Behalf Of Thomas
> Goreau
> Sent: Wednesday, May 31, 2006 10:58 PM
> To: coral-list at coral.aoml.noaa.gov
> Subject: [Coral-List] Heat;light, food, and bleaching, continued
> Heat, light, food, and bleaching, continued.
> I will be unable to respond from my regular email as I
> will be completely out of reach in the field in many
> countries almost all the time from now to at least the
> end to July, and likely well beyond, so I can't
> respond to list server enquiries directly for a long
> time. Could you please post these comments on the list
> server for me? Thanks!
> I'm a little sorry to have raised such fundamental
> issues and then have to effectively drop out before
> replying to the legitimate questions my post has
> raised . So I'd like to make some clarifying explanations
> here in response to the first thoughtful replies to my previous  
> posting.
> It is a serious error to assume that oxygen mass
> balance  tells you the carbon mass balance in a
> reciprocal way. The fact that corals are autotropic in
> carbon goes back to oxygen titrations by Afred Mayor
> and by Thomas F. Goreau's whole reef oxygen and carbon
> metabolism studies at Bikini Atoll in 1947
> (unpublished but I have all the data), and of course
> supported by later oxygen respirometry mentioned
> below.
> The fundamental error is to assume that the carbon
> fixed by the zooxanthellae and translocsted to the coral
> is in fact retained by the coral. In fact it is almost
> all used to make biochemical precursors for mucus
> synthesis and very rapidly excreted. This was shown in
> a long series of classic papers on coral physiology by
> Thomas F. Goreau and Nora I. Goreau in the 1950s, that
> pioneered the use of Carbon-14 and Calcium-45 tracers
> in marine biology. These findings were later supported
> by others, including Trench, Cooksey and Cooksey, and by Jim
> Battey. So the fixed carbon has long been known to
> make a minor to negligible contribution to coral nutrition.
> Yet because so few people bother to read the primary
> literature, this simple minded error of reciprocally
> conflating oxygen and carbon balances has been
> endlessly repeated and even taught as dogma by people
> and textbooks that should know better.
> The role of zooplankton feeding was pioneered by Sir
> Maurice Yonge during the Cambridge University Great
> Barrier Reef Expedition in the 1920s, and followed
> through by Thomas F. Goreau and Nora I. Goreau. The
> definitive paper on coral nutrition by Goreau, Goreau,
> and Yonge, shows the extremely diverse
> multi-trophic pathways of corals, acting as primary
> producer, herbivore, canrnivore, detritus feeder, and
> dissolved organic carbon scavenger, simultaneously,
> but arguing from
> the experimental physiology, enzymology, and functional anatomy
> that zooplankton feeding is the primary mode of carbon
> nutrition of the stony corals.
> Naturally, this must
> involve sub specialization of different corals on
> different components of zooplankton and other
> resources, as indicated by Jim Porter's work on
> trophic niche separation in corals as a function of
> polyp size and Ken Sebens and other's
> work on zooplankton capture. You can see this clearly
> by the different responses of different species to
> zooplankton at night. The role of feeding on survival
> from bleaching is therefore trivially obvious and
> readily seen in diffferential survival in the field in
> sites with higher and lower zooplankton availability
> and capture ability.
> Andrea Grottolli's point that thermal bleaching is different
> than dark bleaching is correct. It is thermal stress
> that kills heat shocked corals rather than bleaching per se, and
> feeding is able to counteract this in a
> species-specific manner that depends on local
> zooplankton availability, depending on the severity
> of heat shock.
> There is much more to be done by building on the shoulders
> of the giants who have prceceded us intstead of
> uncritically following shallow analogical errors, fads, and
> false claims of novelty. Yet the recent literature is
> riddled with the latter flaws. In my view every coral reef
> paper published in Science or Nature in the past 15
> years except for two by Mike Risk and
> colleagues have jargon-filled bogus claims of
> novelty that simply ignore the previous literature. This indicates
> a sitiuation much more serious than widespread
> ignorance of past knowledge by current researchers. It
> indicates a massive failure of competence by the
> "peer" "review" "system", and why there is little
> point even playing their game.
> While some won't appreciate my comments, they are certified free of
> expletives.
> No Risk® to circulate them on the server!
> Best wishes,
> Tom
> Thomas J. Goreau, PhD
> President
> Global Coral Reef Alliance
> 37 Pleasant Street, Cambridge MA 02139
> 617-864-4226
> goreau at bestweb.net
> http://www.globalcoral.org
> ------------------------------
> Message: 4
> Date: Tue, 30 May 2006 15:32:44 -0400
> From: Charles Booth <booth at easternct.edu>
> Subject: Re: [Coral-List] Thomas Goreau's comments
> about
>     coral-zooxanthellae    symbiosis
> To: "coral-list at coral.aoml.noaa.gov"
> <coral-list at coral.aoml.noaa.gov>
> Message-ID: <C0A2161C.8904%booth at easternct.edu>
> Content-Type: text/plain;    charset="ISO-8859-1"
> Thomas Goreau wrote:
> ?The fact that corals don't get their carbon from
> zooxanthellae is also very
> old knowledge, but for decades people have
> ignored the old literature and have mistaken the net
> oxygen balance to
> assume that corals are also autotrophic in carbon.
> This recent error has
> become dogma, despite being wrong, because nowadays
> people don't read the
> literature or ask those who know it. The first
> radiocarbon tracer
> experiments, done by Thomas F. Goreau and Nora I.
> Goreau more than 50
> years ago showed that very little zooxanthella carbon
> translocation
> contributed to coral carbon, and that corals relied on
> zooplankton for the
> vast bulk of their carbon needs.?
> I plead ignorance here as I?m not a coral specialist.
> But, it has been my
> understanding that zooxanthellae do make a significant
> contribution to the
> carbon requirements of the coral polyp, and I have
> been relating this ?fact?
> to my students for many years. My sources of
> information have been various
> textbooks and review articles, and, occasionally,
> original research
> articles, such as the following:
>   Falkowski et al (1984, BioScience 34: 705-709)
> described energy budgets for
> Stylophora pistillata based on O2 fluxes and relative
> biomasses of
> zooxanthellae and coral tissue, and concluded that
> ?carbon fixation and
> translocation by zooxanthellae contributes, on
> average, 140% of the coral
> animal?s daily carbon requirement for maintenance
> respiration.?
> [The original data were published by Dubinsky,
> Falkowsky, Muscatine et al; I
> presume these values, which were derived from net O2
> production, are the
> ones Dr. Goreau suggests have been interpreted
> incorrectly. However, I have
> not come across any published criticism of this method
> and the results;
> rather, the data appear to have been widely cited by
> various authors, such
> as:
> B.G. Hatcher (1988, Trends in Ecology and Evolution,
> 3: 106-111), who wrote
> ?...zooxanthellar production is able to meet the
> animal?s carbon
> requirements for growth as well as respiration.
> Shade-adapted corals fix
> less carbon..., and must depend on heterotrophy to
> make up the difference
> (refs: McCloskey et al, 1985, Proc. Fifth Int. Coral
> Reef Congr, vol. 4,
> Delesalle, B. ed, pp. 527-529; Muscatine, et al, 1984,
> Proc. R. Soc. London
> Ser. B. 222: 181-222).
> Even if the O2 flux-derived values for energy/carbon
> translocation are
> incorrect, subsequent studies using 14-CO2 tracer
> methods appear [to me, at
> least] to support a significant role of
> zooxanthellae-derived carbon for
> coral biomass production:
> In Barnes, R.S.K and K.H. Mann, eds., Fundamentals of
> Aquatic Ecology
> (Oxford/Blackwell, publication date was early 90s, I
> think ? I?m relying on
> a photocopy of the relevant pages) R.N. Hughes wrote
> (Chapter 11, p. 217)
>   ?Incubation with 14-CO2 has shown that as much as 50%
> of the carbon-14
> fixed daily by photosynthesis becomes incorporated
> into coral tissue, mostly
> as lipid and protein (Muscatine and Cernichiari, 1969,
> Biol. Bull. 137:
> 506-523; Kellogg and Patton, 1983, Mar. Biol. 75:
> 137-149).?
> In Barnes, R.S.K. and R.N. Hughes, An Introduction to
> Marine Ecology (3rd
> ed. Blackwell Science; published ~2000, as I recall-
> again, I?m relying on a
> photocopy w/o the publication date), the author(s)
> wrote (Chapter 6, p. 137)
> ?Estimating these proportions [of zooplankton- vs.
> zooxanthellae-derived
> energy] is not easy and data are rather uncertain, but
> the proportions of
> energy ultimately derived from photosynthesis ranges
> from over 95% in the
> ?autotrophic? corals down to somewhat over 50% in the
> more extreme
> ?heterotrophic? species....Incubation of Pocillopora
> damicornis with 14-CO2
> on the reef has shown that up to 50% of the 14-C fixed
> by the zooxanthellae
> during 24 h ends up in the coral tissue, mostly as
> lipid and protein.
> Evidently, the glycerol released by the algae is used
> by the animal in lipid
> synthesis.? [I presume the latter statements refer to
> the work by Muscatine,
> Cernichiari, Kellogg, and Patton cited above]
> More recently still, Lesser et al (2004, Science 305:
> 997-1000) wrote (p.
> 1000)
>   ?...it [glycerol] is the major carbon compound
> translocated from the
> symbiotic zooxanthellae to the host tissues (Muscatine
> , L. 1990, in Coral
> Reefs, Ecosystems of the World, Z. Dubinsky, ed.,
> Elsevier).?
> I may well be guilty of a cursory reading of the
> primary literature and an
> uncritical acceptance of secondary sources ? if so, I
> would like to bring
> myself up to date. Perhaps Dr. Goreau, or someone
> else, can direct me to the
> relevant literature that clarifies the current
> understanding of the role of
> zooxanthellae in the nutrition of coral polyps.
> Chuck Booth
> *   *   *   *   *   *   *
> Dr. Charles E. Booth
> Dept. of Biology
> Eastern Connecticut State University
> Willimantic, CT  06226
> Ph: 860-465-5260
> Email: booth at easternct.edu
> FAX:  860-465-5213
> ------------------------------
> Message: 5
> Date: Tue, 30 May 2006 15:37:10 -0400
> From: Andr?a Grottoli <grottoli.1 at osu.edu>
> Subject: [Coral-List] coral bleaching: response to
> Goreau
> To: coral-list at coral.aoml.noaa.gov, goreau at bestweb.net
> Message-ID:
> < at osu.edu>
> Content-Type: text/plain; charset="iso-8859-1";
> format=flowed
> Dear Tom,
> I read your contribution on the coral list about
> coral bleaching with interest.  As the lead
> author of the recent Nature paper on
> heterotrophic plasticity in bleached corals, I
> would like to comment.  You stated:
> "The recent paper that claims to have discovered "for
> the first time"
> that corals eat zooplankton and can survive bleaching
> better if fed is
> not new either. The fact that corals don't get their
> carbon from
> zooxanthellae is also very old knowledge, but for
> decades people have
> ignored the old literature and have mistaken the net
> oxygen balance to
> assume that corals are also autotrophic in carbon.
> This recent error has
> become dogma, despite being wrong, because nowadays
> people don't read
> the literature or ask those who know it. The first
> radiocarbon tracer
> experiments, done by Thomas F. Goreau and Nora I.
> Goreau more than 50
> years ago showed that very little zooxanthella carbon
> translocation
> contributed to coral carbon, and that corals relied on
> zooplankton for
> the vast bulk of their carbon needs. They kept corals
> completely
> bleached in the dark for years, feeding them on
> zooplankton. So survival
> of bleached fed corals has been known for over half a
> century and is not
> a "new discovery" at all. Like so much else in the
> current literature."
> I would like to point out that our paper showed
> that only one species, Montipora capitata,
> consumed enough zooplankton to meet all of its
> metabolic demand heterotrophically when
> bleached.   When healthy, M. capitata met less
> than 15% of its metabolic demand
> heterotrophically.  The other two species we
> studied, Porites compressa and Porites lobata,
> only met 21-35% of their daily metabolic demand
> heterotrophically when they were either healthy
> or bleached.   In all cases, our corals were
> exposed to naturally occurring zooplankton on the
> reef.  Thus under natural reef conditions, not
> all bleached corals can meet all of their
> metabolic needs heterotrophically.  Under
> artificially fed conditions (i.e., coral exposed
> to higher than ambient concentrations of
> zooplankton or brine shrimp in tanks), things can
> be quite different.   As you pointed out, the
> fact that corals do get some fixed carbon from
> zooplankton has been know for a very long
> time.  However, the fact that when bleached at
> least one species can  increase heterotrophic
> feeding to meet all of its metabolic needs while
> two others could not, is novel.  Our results
> suggest that not all species of corals would be
> able to meet their metabolic demand when
> maintained in the dark under natural
> concentrations and abundance of zooplankton (i.e,
> P compress and P lobata probably could not get
> all of their energy needs met heterotrophically
> when bleached under darkness... but this would
> need to be specifically tested).   In addition,
> bleaching induced by keeping corals in the dark
> is not necessarily the same as
> temperature-induced bleaching.  The chain of
> physiological stress responses that occur under
> high temperature include free radical and stress
> protein production, making any heterotrophic
> responses under tempreature-induced bleaching
> possibly quite different than hetertrophic
> responses under sustained darkness.
> Sincerely,
> Andrea Grottoli
> *******************************************************
> Andr?a G. Grottoli, Assistant Professor
> Ohio State University
> Department of Geological Sciences
> 125 South Oval Mall
> Columbus, OH 43210-1398
> office:  614-292-5782
> lab: 614-292-7415
> fax: 614-292-7688
> email: grottoli.1 at osu.edu
> web: www.geology.ohio-state.edu/~grottoli
> Office location: 329 Mendenhall Labs
> *******************************************************
> ------------------------------
> Message: 6
> Date: Tue, 30 May 2006 21:13:33 -0700 (PDT)
> From: shashank Keshavmurthy <iamshanky15 at yahoo.com>
> Subject: Re: [Coral-List] coral bleaching: response to
> Goreau
> To: "Andréa" Grottoli <grottoli.1 at osu.edu>,
>     coral-list at coral.aoml.noaa.gov, goreau at bestweb.net
> Message-ID:
> <20060531041333.31960.qmail at web31810.mail.mud.yahoo.com>
> Content-Type: text/plain; charset=iso-8859-1
> Dear Listers
> It is interesting to see that finally the debate
> on the coral energy aquisition has surfaced...
> most of the resarch papers till now say that
> there is major contribution of Carbon form
> zooxanthellae to corals....but, when in need the
> corals can adapt to the carbon aquisition
> heterotrophically....???????
> We all need to get lots of information from
> aquarists around the world....
> If you will see the book written by "Julian
> Spring" on the aquarium corals...it gives the
> mode of nutrition as autotrophy and heterotrophy
> to most of the corals described in his book....
> we as researchers may just dont know what really
> is happening out there....
> here i agree totally with Tom....we still need to
> get lots work done so as to understand the true
> feeding habits of corals...
> Recent paper by "Palardy et al, MEPS (2005) 300:
> 79-89, Effects of upwelling, depth, morphology
> and polyp size on feeding in three species of
> Panamanian corals"...looks at what corals are
> eating...
> Collaboration with aquarists is needed to really
> understand about the energy aquisition in corals
> in more detail...
> more and more people are looking at zooxanthellae
> since it is believed to be "the source of Carbon"
> and "the factor for/of coral bleaching
> response"...
> question is how much is the symbiotic dependency?
> there are many studies showing that the corals
> can survive without the presence of
> zooxanthellae...it may not be for long time and
> may not be see in natural enviroment....but we do
> see many sea anemones in coral reefs, bleached
> and still surviving....
> i think it is like, do corals want to feed on
> zooplankton when they loose zooxanthellae?
> does it take some time to switch between the
> modes of nutrition acquisition?
> combination of stress factors may be disturbing
> the switching between the modes
> for instance, when kept in aquarium tank in
> dark..it is only one stress and corals can
> survive with the zooplankton being fed...that
> means  they are able to switch between the
> modes..?
> hmm...its pretty complex out there..and coral
> physiology is more and more challenging...this is
> my view...
> Regards
> shashank
> "the role of infinitely small in nature is infinitely
> large"-Louis Pasteur
> Keshavmurthy Shashank
> phD candidate
> Kochi University, Graduate School of Kuroshio Science
> Laboratory of Environmental Conservation
> Otsu 200, Monobe, Nankoku-shi
> 783-8502, Kochi, Japan
> alt. id: shashank at cc.kochi-u.ac.jp
> phone: 81 080 3925 3889
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Thomas J. Goreau, PhD
Global Coral Reef Alliance
37 Pleasant Street, Cambridge MA 02139
goreau at bestweb.net

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