Lighting by Number: “Types” of Zooxanthellae and What They Tell Us

We often see articles in hobby literature referring to
locations where corals and other photosynthetic invertebrates are
collected. These articles are informative, interesting and offer
a perspective of the environmental conditions required for coral
growth. But what if we could look at requirements, particularly
at genetically encoded requirements, of the symbiotic
dinoflagellates zooxanthellae within corals tissues? Though
genetic fingerprinting of zooxanthellae is very much in its
infancy, and with only limited (but rapidly expanding)
information from researchers, we, as hobbyists, can begin to
accurately piece together some zooxanthellae – and hence corals
– specific requirements for successful maintenance in captivity.
By extension, we can predict the lighting environment and
physical conditions required by other zooxanthellae/corals.

A need for information on zooxanthellae found within the
tissues of Hawaiian corals began innocently enough. The
information I required was in a recent issue of Coral
Reefs
, however I became curious about other available data.
I checked my available references and began tracking down their
cited journal articles, and the effort quickly became geometric.
I did not realize that so much research had recently been
conducted. My little project soon blossomed into a
time-consuming venture. The compiled database (presented in this
article)
lists symbiotic corals (stony and soft – often to the
species level), mollusks, false corals, anemones, flatworms, and
hydrocorals along with pertinent information. With over 800
entries of species and variations of subspecies (called clades),
I believe this to be the most complete listing readily available
to hobbyists.

Why should anyone be interested in a rather obscure subject
such as this? After all, we know that coral animals (hosts) and
zooxanthellae (symbionts) have a mutually beneficial
relationship. We realize zooxanthellae need light and either too
much, or not enough, photosynthetically active radiation will
cause problems. In the most severe cases, the coral animal will
eject its zooxanthellae in a process known as bleaching.
Bleaching is generally exacerbated by higher than normal water
temperature and ultraviolet radiation. This information is
elementary. It gets more involved. Much more involved.

The compiled database (presented in this article) lists symbiotic corals
(stony and soft – often to the species level), mollusks, false corals, anemones,
flatworms, and hydrocorals along with pertinent information. With over 800
entries of species and variations of subspecies (called clades), I believe
this to be the most complete listing readily available to hobbyists.

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Advances in DNA fingerprinting have allowed researchers to
identify many life forms to species and subspecies level. A
handful of dedicated scientists are devoting their careers to the
investigation of various types of zooxanthellae, and are
generating a great deal of data. We’ve known for some time that
there isnt just a single species of zooxanthellae
(Symbiodinium microadriaticum). We now know there are at
least 9 described species with many subspecies (variously called
clades, types or phylotypes). There are Clades A, B, C, D,
E, F, G and H. Of these, Clades A, B, C, D (and to a lesser
degree F and G) are of most interest to reef aquaria hobbyists
(see Figure 1). Symbiont populations tend to follow Fisher
log-normal distribution patterns characterized by
‘generalist’ zooxanthellae (common) and rare
zooxanthellae (‘specialists’) hosted by specific coral
species (Pochon et al., 2001). For instance, some zooxanthellae
clades are tolerant of high light intensity, while others have
higher thermal tolerances, and this is where it begins to get
interesting to hobbyists.

Each Clade contains sub-clades, and variations of sub-clades.
In the following database, zooxanthellae sub-clades are
designated by a numeral following the clade and, in some cases, a
lower case letter for further refinement (i.e., C1a indicates
Clade C, and the lower case letter indicates a variation of
subclade 1). The following listing reports more than 150 of
them. Information is also listed for accession numbers this
is a code assigned to genetic fingerprints in GenBanks database.
I have not attempted to distinguish between ITS (internal
transcribed spacer, only recently applied to zooxanthellae
Hunter et al., 1997) and any other methods accession number,
although its a good bet that most definitions beyond the clade
level (in this list anyway) were performed by fingerprinting the
ITS region (a less conserved portion of the rDNA). The accession
numbers were included in the original Excel file (available upon
request) in order to sort by GenBanks codes and determine common
host/symbiont relationships. For those really serious about
further information, a web search on a particular accession
number will occasionally turn up additional information.

Even with advances in DNA fingerprinting, there is a question
of speciation. What genetic markers determine if a certain clade
of zooxanthellae rises to the level of becoming a new species?
Until integrated examinations are completed, these questions will
remain unresolved (Takabayashi et al, 2004). This isnt that much
of an issue as far as hobbyists are concerned but it is causing
constant revisions in the taxonomy of symbiotic
dinoflagellates.

However, there is general not universal – agreement about
zooxanthellae clades. Atlantic and Caribbean corals usually
contain variations of Clade B (there are exceptions of course!)
with A and C making up the difference. On the other hand, Pacific
corals usually contain variations of Clade C (again with
exceptions to the rule). It is believed that closure of the
Central American seaway by the rise of the isthmus that is now
Central America created distinct zones for coral growth and
zooxanthellae specialization. The survival of Atlantic corals
during glaciation of the northern hemisphere (the Ice Age)
depended upon adaptation resulting in co-dominant zooxanthellae
clades, while Pacific corals enjoyed mostly tropical environs
during this period and C clades dominated.

Clades of Zooxanthellae

As mentioned earlier, taxonomy of zooxanthellae is constantly
revised, with elevation from clade level to species not
particularly uncommon. In addition, there is confusion created by
using cultures of zooxanthellae – Santos et al. (2001) report
that zooxanthellae cultured in vitro may not be
representative of the dominant in hospite zooxanthellae
clade since conditions within the culture vessel may favor the
growth of a sub-dominant clade. This is an important point to
consider when reviewing early research works. However, this list
is believed to be correct as of late 2005.

I have included zooxanthellae species under the appropriate
clade heading. Trends begin to develop and suggest (but do not
confirm) characteristics that are perhaps common to each
particular zooxanthellae clade.

For a general distribution map of clades, see Figure 2. For
populations within a given region, see Figures 3 and 4.

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Traits of Different Clades and Why They Are
Important

As mentioned, we begin to see traits common among
zooxanthellae clades. Two important traits are Xanthophyll
Production and production of Mycosporine-like Amino Acids (MAAs).
Again, assigning characteristics found in one clade species to
all zooxanthellae found within a particular clade is risky
business. However, trends do seem to develop upon close
examination, at least in Clade A and Clade B.

Xanthophylls are carotenoid pigments found within many species
of zooxanthellae, algae and higher plants. The two xanthophylls
found in some zooxanthellae are diadinoxanthin (Dn) and
diatoxanthin (DT) Brown et al., 1999. Dn and DT act as a
photoprotectants and shield those zooxanthellae containing them
from excessively high amounts of photosynthetically active
radiation in a process called Dynamic Photoinhibition. This is
simply a protective measure that prevents damage to Photosystem
II. In high light, Dn absorbs blue wavelengths (Jeffries, 1997)
and is converted to DT, thus shunting blue light energy away from
the photosynthetic apparatus. Zooxanthellae with the ability to
produce xanthophylls are equipped to endure higher light
intensities with a lessened chance of destruction of their light
harvesting proteins. (It should be noted that other energy
dissipation pathways may be available such as release of
non-radiant heat by the Photosystem II Reaction Center, or
perhaps spillover of energy from Photosystem II to Photosystem
I.)

While xanthophylls protect zooxanthellae from visible light
energy, mycosporine-like amino acids (MAAs) protect them from
ultraviolet radiation. So named because these amino acids were
first isolated from fungi, MAAs are produced by plants, fungi and
some bacteria. The chemical pathway leading to MAA production
(the shikimate pathway) is not known to occur in animals, so MAAs
can be obtained from zooxanthellae known to produce them. MAAs
can also be obtained through dietary means (ingestion of algae or
animals containing accumulated MAAs). Interestingly, Shick et al.
report that the temperate sea anemone Anthopleura
elegantissima
obtains certain MAAs from ocular lenses in
fishes it ingests. It is possible that bacteria and/or
cyanobacteria can translocate MAAs, or modify translocated or
ingested MAAs. It is also possible that translocated MAAs could
be modified by the host coral). In short, MAAs can be obtained
from sources other than zooxanthellae. However the ability to
produce and release these important compounds to the coral host
likely gives the coral a competitive edge in shallow
environments.

A gene tree of zooxanthellae clades

Figure 1. A gene tree of
zooxanthellae clades showing how different clades are related to
each another. This is a synthesis of works performed by Coffroth
and Santos (2005), and is based on ITS analyses.

Known locations of zooxanthellae clades

Figure 2. Known locations of zooxanthellae clades. Purple = Clade A; Yellow
= Clade B; White = Clade C; Red = Clade D; Dark Blue =Clade F and Black =
Clade G. Not surprisingly, identified clade locations are usually near research
stations.

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Clade “A”

Clade A zooxanthellae are generally considered relatively
hardy, and are found in scleractinian corals, octocorals,
hydrocorals, clams, anemones and zoanthids. Most hosts of Clade
A zooxanthellae are found in the Caribbean, with sporadic
reports of occurrences in Australias Great Barrier Reef, the Red
Sea and the western Pacific (Korea).

Reported Species in Clade A

Symbiodinium microadriaticum. Found within tissues
of the jellyfish Cassiopeia xamachana. This zooxanthella
species acclimates to high and low light levels and synthesizes
natural ultraviolet radiation sunscreens mycosporine-like amino
acids or MAAs – (even in the absence of UV), but has low
tolerance of temperature swings. Protective xanthophylls are
produced in super-saturating light intensities (this light
intensity = 250 molmsec; Iglesias-Prieto and Trench, 1997).
Considering that S. microadriaticum is found within a
motile host and subject to rapidly fluctuating environmental
conditions, it is not surprising that this species is tolerant of
a wide variety of parameters.

Symbiodinium pilosum. Found in the Caribbean
zoanthid Zoanthus sociatus. These are high light adapted
(they respond poorly to low light levels), tolerate high
temperatures swings and are able to produce and incorporate
protective xanthophylls into chlorophyll protein complexes.
Iglesias-Prieto and Trench, 1997, found this zooxanthella to be
the least adaptive in respect to light intensity of 6
zooxanthellae examined (high light is tolerated while low light
intensity is not).

Symbiodinium meandrinae. This zooxanthella was
discovered within the tissues of the Atlantic stony coral
Meandrina meandrites. Banaszak et al., 2000, found two
zooxanthellae clades (A and C) within M. meandrites,
Baker and Rowan (1997) report Clade B. This leads to confusion
over the actual identity of S. meandrinae Trench
(1997) clarifies the situation by listing S. meandrinae
as Clade A.

Symbiodinium corculorum. Isolated from the
photosynthetic Pacific clam Corculorum cardissa.
Iglesias-Prieto and Trench (1997) suggest this zooxanthella
species has limited photoacclimation capability and the
symbiont/host perform best under high light intensity. This clam
to limited to a depth of 10 meters (Gosliner et al., 1996) and is
thus considered tolerant of high light.

Symbiodinium cariborum. Found in the tissues of the
Caribbean anemone Condylactis gigantea.

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Summary: Clade A zooxanthellae seem tolerant of high light
intensity, and likely produce protective xanthophylls and
mycosporine-like amino acids.

Caribbean zooxanthellae population by clade

Figure 3. Caribbean zooxanthellae population by clade. From LaJeunesse,
2003.

Clade “B”

As with Clade A zooxanthellae, those of Clade B are
relatively resistant to bleaching episodes. Current information
suggests this clade is most common in Caribbean octocorals (sea
fans, sea whips, etc.), but also present in many (a dozen or
more) Atlantic stony coral genera and at least 8
Acropora species from the Great Barrier Reef. A subclade
(B1) has been found in Hawaiian Aiptasia anemones and
stony coral Pocillopora damicornis (probably as a
cryptic symbiont Santos et al., 2004).

Reported Species in Clade B

Symbiodinium pulchrorum. Found in the Hawaiian
anemone Aiptasia. Iglesias-Prieto and Trench (1997)
report S. pulchrorum has a high photoacclimatory
capability (their experiment used 40 molmsec as the
sub-saturating intensity, and 250 molmsec as the
super-saturating light intensity). Banaszak (2000) did
not find this species to synthesize MAAs. As a footnote
to these observations, I have noticed that Aiptasia
anemones do not fair well under high light intensity – they
retract into small blobs, probably in an effort to self-shade
their zooxanthellae from high PPFD (600 molmsec and higher)
and/or UV radiation.

Symbiodinium bermudense. A symbiont of the pest
anemone Aiptasia pallida. This species apparently does
not produce MAAs (Banaszak et al., 2000).

Symbiodinium muscatinei. This species has been
described as found in tissues of the temperate anemone
Anthopleura elegantissima. It is thought that this
species does not produce UV sunscreens (mycosporine-like amino
acids, Shick et al., 2002). S.
muscatinei
is sometimes listed as Clade E. (Santos et al.,
2001). Secord and Muller-Parker (2005) found that S.
muscatinei
and S. californium are tolerant of high
light intensity and photosynthetic saturation was not achieved at
540 molmsec. The compensation point for these algae was about
73 molmsec.

Symbiodinium californium. This species does not
produce mycosporine-like amino acids in culture (in Shick et al.,
2002). It is found within the Anthopleura elegantissima
anemone. S. californium is sometimes listed as Clade E
(Santos et al., 2001).

Summary for Clade B zooxanthellae species: Do not seem to
synthesize mycosporine-like amino acids, and are tolerant of
higher light intensities.

Clade “C”

Clade C is difficult to characterize, though Atlantic Clade
C zooxanthellae are found in deeper water, while bleaching is
often noted in Pacific corals containing Clade C symbionts.
Generally, most Clade C zooxanthellae/corals inhabit tropical
latitudes.

Clade C contains over 130 subclades, and, as a group, is
pandemic. It is found in some Caribbean corals, but most often in
the Pacific.

Some Clade Cs are thermally-tolerant (C15), others are
generalists exhibiting habitation over a broad range of depths
(C1, C3 and C21), C8a is found only in deeper waters, C7c is
limited to relatively shallow depths and in nature tolerates
light intensity up to about 700 molmsec. It is easy to see
why Tchernov et al., 2004 warn of assuming closely related sister
subclades will demonstrate similar traits (light and/or
temperature tolerances for example).

Reported Species in Clade C

Symbiodinium goreaui. Found within Ragactis
lucida
(in Trench, 1996) and expanded by LaJeunesse et al.,
2003 to the pandemic generalist zooxanthellae Clade C1.

Clade D

Phylotype “D” Relatively resistant to bleaching (in
comparison to many Clade C phylotypes), and, in fact, often
found in areas that have suffered recent, severe bleaching
episodes and hot environments. Chen et al., 2003, found this
clade within high latitude corals Oulastrea crispata and
Goniastrea aspera inhabiting marginal sites (extreme
temperatures, turbidity and irradiance) This zooxanthellae is
thus considered extremely stress tolerant. Clade D is the
proper classification for symbionts listed in earlier works by
Carlos et al. (1999) and Toller (2001 a, b).

Clade E

This clade is not known to occur in corals. Those
zooxanthellae listed as Clade E in Toller et al., (2001) have
been reclassified as Clade D. Symbiodinium muscatinei
and S. californium (from the anemone
Anthopleura) are sometimes listed as belonging to Clade
E; they are listed as Clade B (above).

Clade “F”

Normally found in foraminiferans, researchers were surprised
when Clade Fr2 was found in isolated ‘daisy coral’
specimens (Alveopora japonica) in Korea.
(Rodriguez-Lanetty et al., 2000). Clade F5 occurs in
Montipora capitata. F5 is not tolerant of
high light intensity, but there are reports of M.
capitata
containing MAAs. It is not known if these are
obtained through diet or translocation.

Reported Species in Clade F

Symbiodinium kawagutii. This zooxanthella species
(designated as Clade F5) is found within the Hawaiian coral
Montipora capitata (formerly M. verrucosa). No
protective xanthophylls are produced as a response to
super-saturating irradiance (Iglesias-Prieto and Trench, 1997),
and this zooxanthella (and host) does poorly in high light
intensity. It is interesting that both corals containing Clade F
are found at higher latitudes.

Clade G

Clade G has recently been found in soft corals (van Oppen,
2005a), stony corals (van Oppen 2005b) and giant sea anemones
(LaJeunesse, in Pochon, 2005).

Great Barrier Reef zooxanthellae population by clade

Figure 4. Great Barrier Reef zooxanthellae population
by clade. From LaJeunesse, 2003. This could be modified to
include Clade G.

Why Are Some Zooxanthellae Resistant to
Bleaching?

This question begs an answer why do some corals perform
better than others at higher light intensity and/or temperatures
and seem immune from the effects of radiation? There are many
reasons why a coral could be resistant to bleaching:

  1. Protection from UV Radiation. As we have
    seen, some zooxanthellae are able to protect themselves
    from ultraviolet radiation by production of mycosporine-like
    amino acids. Others can not produce these protectants, and
    hobbyists have no way of predicting which corals (or other
    animals for that matter) may be harmed by UV. See Riddle 2004a
    for reasons why we should eliminate ultraviolet radiation from
    aquaria.
  2. Protection from Intense Light. Some
    zooxanthellae are able to produce and incorporate xanthophylls to
    protect themselves from high light intensity. Not all do, and
    there are alternative protective pathways such as spillover or
    non-radiant heat dissipation once absorbed light energy enters
    the reaction center of Photosystem II (See Riddle, 2004b for
    details of high light intensity on captive corals). However some
    zooxanthellae apparently possess little, if any, means of coping
    with high light intensity. They will either do well in darker
    environments or merely survive in a hostile environment.
  3. Thylakoid Membrane Composition. Recent
    research suggests even more strategies to resist bleaching.
    Tchernov (2004) suggest the lipid saturation of the hydrophilic
    thylakoid membrane within the chloroplast determines resistance
    to compromise. In effect, the very composition of the
    light-collecting apparatus predetermines resistance to
    photodestruction and bleaching.
  4. Absorption of Heat.
    A newer paper by
    Fabricius (2006) found that darker pigmented corals can
    potentially gain radiant heat and become warmer than the
    surrounding water temperature. Obviously this could make the
    zooxanthellae potentially more susceptible to a bleaching event
    (this happens in aquaria too – Riddle, in press

How to Use This List

There are several approaches in using this list. The first,
and perhaps most simple, is applicable to those with an
established tank in which specimens are thriving. Any coral with
a matching zooxanthellae clade will probably do well within the
same aquarium. A more precise, though limited method, requires
use of a quantum or PAR meter. Compare the PAR measurement from
the corals intended place to the PAR measurements within the
list.

The list can be downloaded
in PDF format
. Please download Adobe Acrobat Reader if you do not have it installed on your system.

Column 1 contains accession numbers. These are of little
practical use to hobbyists, with the exception that they are a
researchable data point. I have included them for that reason
only.

Column 2. Animal hosts are most often listed using Latin names
– a necessity considering the confusion a list of this sort would
generate if common names (i.e., Bali green hairy mushroom) were
used. Use of the listing may therefore require some effort on the
hobbyists part for proper identification (at least to the genus
level). Such references are readily available to hobbyists. I
have also included clades when they are only casually mentioned
in a journal article and no coral host is mentioned (designated
as ?).

Column 3. Practical information is often included about the
regional location of the host invertebrate. It is soon realized
that Porites coral are pandemic, while some corals are
endemic to certain isolated areas (Hawaiian coral species are a
good example). Though it is not likely that Hawaiian corals are
found in home aquaria, it is possible a zooxanthellae clade is
not restricted to the Hawaiian Archipelago, and may be found in
host corals from other regions. Therefore this information is of
potential use since we have information on photosynthetic
saturation levels of some Hawaiian corals.

Abbreviations are: AC = Atlantic
Caribbean; C = Caribbean
(C, for Caribbean, is also used as a
prefix to identify location in countries with Atlantic and
Pacific shorelines, i.e., Panama); CC =
Central Caribbean; Central GBR =
Central Great Barrier Reef, eastern Australia;
CP = Central Pacific;
EC = Eastern Caribbean;
EP = Eastern Pacific;
GBR = Great Barrier Reef, eastern
Australia; IP = Indo-Pacific Ocean;
NC = Northern Caribbean;
P-Panama = Pacific shore of Panama;
RS = Red Sea;
Taiwan-KT = Kenting Island;
Taiwan-PI = Penghu;
WC = Western Caribbean;
WI = Western Indian Ocean; and
WP = Western Pacific.

Column 4. Where available, collection depths or ranges (in
meters) are listed for host animals. We will explore why this
information, when taken at face value, is of limited use in
determining lighting requirements for corals (depth preferences
may be due to skeletal strength and other factors). It is,
however, useful for estimating the range of light tolerances of
zooxanthellae clades when combined with other information. Note:
One reference lists a maximum depth of 90 meters I
suspect this is a typo (perhaps 90 feet) and would not interpret
it literally.

Column 5. Truncated comments are included for ease of
reference, along with journal references for further study.
During review, one will quickly realize how diverse the genus
Symbiodinium actually is. Instead of making things more
complicated, all this information will begin to make things
easier for hobbyists in that trends begin to evolve and, at
times, generalizations can be made. These, along with the quality
and quantity of rapidly evolving information, will some day
precisely answer many of the remaining questions about the
lighting requirements of those animals in our captive reefs.
Occasionally, I have added some light requirement information,
and have made an assumption that a particular subclade (C27, for
instance) will have the same range of light needs regardless of
location (and will react in the same manner to saturating light
intensity within an aquarium). This is based on P/I curves of
Hawaiian corals and cross-referenced with light ranges made in
the field by researchers referenced below. The saturation
numbers listed in this column are full-blown saturation levels
(not saturation onset numbers) where increasing light intensity
will not increase the rate of photosynthesis. Kirk (1983)
recommends saturation onset as the standardized method of
reporting photosynthetic saturation. I have chosen other wise,
since coral geometry is often highly irregular and subject to
shading. Using full saturation as the standard should ensure that
shaded areas have sufficient light.

Column 6. Appropriate journal references. Full information is
available below.

References

  1. Baillie, B., C. Belda-Baillie and T. Maruyama, 2000.
    Conspecificity and Indo-Pacific distribution of
    Symbiodinium genotypes (Dinophyceae) from giant clams.
    J. Phycol. 36:1153-1161.
  2. Baker, A., 2001. Reef corals bleach to survive change. Nature,
    401: 765-766.
  3. Baker, A., 2003. Flexibility and specificity in coral/algal
    symbiosis: Diversity, ecology and biogeography of Symbiodinium.
    Annu. Rev. Ecol. Syst., 34:661-689.
  4. Baker, A., In Press. Symbiont diversity on coral reefs and
    its relationship to bleaching resistance and resilience.
  5. Baker, A.C. and R. Rowan, 1997. Diversity of symbiotic
    dinoflagellates (zooxanthellae) in scleractinian corals of the
    Caribbean and eastern Pacific. Proc. 8th Int. Coral Reef Symp.,
    Panama. 2: 1301-1306.
  6. Baker, A.C., R. Rowan and N. Knowlton, 1997. Symbiosis
    ecology of two Caribbean Acroporid corals. Proc. 8th Int. Coral
    Reef Symp., Panama. 2:1295-1300.
  7. Banaszak, A., T. LaJeunesse and R. Trench, 2000. The synthesis
    of mycosporine-like amino acids (MAAs) by cultured, symbiotic
    dinoflagellates. J. Exp. Mar. Biol. Ecol., 249: 219-233.
  8. Baker, A., R. Rowan and N. Knowlton, 1997. Symbiosis ecology
    of two Caribbean Acroporid corals. Proc. 8th Int.
    Coral Reef Symp., 2:1295-1300.
  9. Baker, A.C., R. Rowan, 1997. Diversity of symbiotic
    dinoflagellates (zooxanthellae) in scleractinian corals of the
    Caribbean and eastern Pacific. Proc. 8th Int. Coral
    Reef Symp., Panama. 2: 1301-1306.
  10. Brown, B.E., I. Ambarsari, M.E. Warner, W.K. Fitt, R.P. Dunne,
    S.W. Gibb and D.G. Cummings, 1999. Diurnal changes in
    photochemical efficiency and xanthophyll concentrations in
    shallow water reef corals: evidence for photoinhibition and
    photoprotection. Coral Reefs, 18:99-105.
  11. Chen, C., Y-W Yang, N. Wei, W-S Tsai and L-S Fang, 2005.
    Symbiont diversity in scleractinian corals from tropical reefs
    and sub-tropical non-reef communities in Taiwan. Coral Reefs,
    24(1): 11-22.
  12. Coffroth, M. and S. Santos, 2005. Genetic diversity of
    symbiotic dinoflagellates in the genus Symbiodinium.
    Protist, 156:19-34.
  13. Costa, C., R. Sassi, and F. Amaral, 2005. Annual cycle of
    symbiotic dinoflagellates from three species of scleractinian
    corals from coastal reefs of Brazil. Coral Reefs, 24(2):
    191-194.
  14. Fabricius, K., 2006. Effects of irradiance, flow, and colony
    pigmentation on the temperature microenvironment around corals:
    Implications for coral bleaching? Limnol. Oceanogr., 51(1):
    30-37.
  15. Gosliner, T., D. Behrens and G. Williams, 1996. Coral Reef
    Animals of the Indo-Pacific
    . Sea Challengers, Monterey, Ca.
    314 pp.
  16. Goulet, T. and M. Coffroth, 2004. The genetic identity of
    dinoflagellates symbionts in Caribbean octocorals. Coral Reefs,
    23: 465-472.
  17. Grottoli-Everett, A.G. and L.B. Kuffner, 1995. Uneven
    bleaching within the colonies of the Hawaiian coral Montipora
    verrucosa
    . In: Ultraviolet Radiation and Coral
    Reefs
    . D. Gulko and P.L. Jokiel, eds. HIMB Tech. Report
    #41.
  18. Hunter, C.L., C.W. Morden, and C.M. Smith, 1997. The utility
    of ITS sequences in assessing relationships among zooxanthellae
    and corals. Proc. 8th Int. Coral Reef Symp., Panama. 2:
    1599-1602.
  19. Jeffrey, S., R. Mantoura and S. Wright, eds., 1997. Monographs on Oceanographic Methodology: Phytoplankton
    Pigments in Oceanography
    . UNESCO Publications, Paris. 661
    pp.
  20. Kirk, J.T.O., 1983. Light and Photosynthesis in Aquatic
    Ecosystems
    . Cambridge University Press, Cambridge. 401
    pp.
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