An Update on Zooxanthellae (Symbiodinium spp.) What a Difference a Year Makes!

Coral biologists have been very busy recently, and
with good reason. The understanding of the adaptability of corals and their
symbiotic zooxanthellae to various environmental stressors has taken on a
new sense of urgency due to shifts in global weather patterns. For
aquarists, some findings are rather surprising and have the potential, in
certain instances, to profoundly change (or at least cause a re-examination
of) husbandry techniques for many symbiotic invertebrates.


intro_photo.jpg

A photomicrograph of a zooxanthella. The culture of this
symbiotic algae can ‘make or break’ a coral reef aquarium.

This article, the first of two parts, is a follow up on an article
printed in Advanced Aquarist entitled ‘Lighting by Number’ ( www.advancedaquarist.com/2006/1/aafeature1
) and discusses Clades ‘A’ and ‘B’ (Part Two will examine those
zooxanthellae, mostly ‘C’ Clades, but along with other clades, from the
Pacific). A review of the 2006 article is recommended if you are not
familiar with it. This article will update the database presented in the
previous article, which has been expanded from about 800 entries to over
1,700. Many stony corals and their respective symbionts have been added,
but there is also much new information on zooxanthellae symbionts of soft
corals. Geographically-important symbioses are also added, including
corals/clades from Indonesia (one of the major coral-exporting regions),
which includes data on some of the more exotic stony corals (such as the
‘Superman’ Montipora (M. danae)).

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Perhaps the most surprising information reveals that infection of a
given host by zooxanthellae is not universal, that there is geographic
partitioning of symbioses. We often think of the soft coral
Stereonephthya as being void of zooxanthellae, yet this is not the
case. Some individuals do contain Symbiodinium (Barneah, 2004),
while the same species from another locale do not (apparently,
differentiation of zooxanthellate and azooxanthellate
Stereonephthya specimens is simple – those without zooxanthellate
are mostly ‘whitish’ in color). This is certainly big news in the small
pond of reefkeeping, especially as it approaches its 35th
birthday in North America. We have a lot to learn!

Comments on the Database

The structure and presentation of information will take a different
format from that one of the first article, all in an effort to make the
database easier to use. To use the database, find the coral genus or
species in Column 2 (listed alphabetically) and the appropriate column will
then provide information concerning associated zooxanthellae clade, locale,
and journal reference (which is very similar to that presented in the first
article). Since the database size was becoming unwieldy, I’ve chosen to
list pertinent information of each clade categorically in the following
text below.

I’ve tried to make this database as concise as possible, and a couple of
the abbreviations require an explanation. USVI = U.S. Virgin Islands; GBR =
Great Barrier Reef, Australia; W = western, C = central or
Caribbean, and so on.

Before beginning, we, as hobbyists, owe a great deal of gratitude to
prominent genetic scientists, including Todd LaJeunesse, Madeleine van
Oppen, Mark Warner, Andrew Baker and numerous others. Their intensive
efforts to further understand the diversity of the dinoflagellates
Symbiodinium are indeed remarkable.

Method of Coral Reproduction – Does It Make a Difference in Symbiont
Clade?

Corals, and how they infect their spawn with zooxanthellae, have at
least two general classifications known as ‘vertical’ and ‘horizontal’.
Horizontal reproduction is by broadcast spawning, that is, eggs and sperm
are ejected into the water column where fertilization takes place. The
coral planulae larvae then obtain their symbiotic zooxanthellae from the
environment. It is generally believed that those corals produced by
horizontal reproduction have more ‘flexibility’ in obtaining type(s) of
symbionts. On the other hand, vertical reproduction involves fertilization
of a coral egg within the parent colony, and these particular corals
produce planulae that are already ‘seeded’ with an appropriate clade
zooxanthellae. In contrast to horizontal reproducers, vertical reproducers
are generally thought to have rather specific requirements for
zooxanthellae symbionts. While a convenient generalization, there are
exceptions to this rule of thumb.

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Just Any Old Zooxanthellae Will Do?

In order for the symbiosis between the host coral and symbiotic
zooxanthellae to successfully occur, the host must recognize the symbiont
as ‘self’ and not reject it. Conversely, the symbiont must shield itself
from attack by the host. This is accomplished by protective shields called
“symbiosome membranes”. Wakefield and Kempf (2001) report multiple
symbiosome membranes can be present in the cnidarian-dinoflagellate
symbiosis, and are generated by both host and symbiont. They report
macro-molecules associated with these membranes potentially determine which
symbiotic zooxanthellae can infect and successfully inhabit corals.

Natural Sunscreens – PAR and Ultraviolet Radiation Protectants Now
Thought to be Universal in Zooxanthellae

A recent and very interesting paper (Banaszak et al., 2006) discusses
the likelihood that many (if not all) zooxanthellae clades can produce
natural sunscreens to protect themselves and their hosts from ultraviolet
radiation. These researchers now believe that major clade groups (A, B, C,
D and E) can produce these colorless, protective substances called
mycosporine-like amino acids (MAAs). This contradicts previous beliefs
based on research conducted with symbionts isolated from hosts and then
cultured under relatively low light intensity (~70 µmole photons·m²·sec).
It now seems that higher light intensities and/or ultraviolet radiation are
needed in order for the zooxanthellae to make these pigments (the coral
host can not, since shikimate pathway is known to occur only in plants and
bacteria. However, MAAs can be obtained through diet by corals).

Does this change the opinion that aquarium lamps, especially metal
halides and mercury vapors, should be shielded with a UV-absorbing lens? No
– the results of Banaszak’s research only reinforces the notion that we
should shield our aquarium inhabitants from potentially harmful UV
radiation. For instance, a coral, grown in a dimly lighted portion of an
aquarium, could be exposed to relatively intense UV radiation if it is
moved only a few inches into a ‘brighter’ spot. These researchers also note
the production of MAAs is an energetically expensive process (they quote a
figure that 19% of a cell’s total energy budget is required for production
of the MAA Palythine – energy that otherwise could be used for growth and
reproduction).

In addition, it is now believed that all symbiotic zooxanthellae have,
to varying degrees, the ability to produce xanthophylls. Xanthophylls
(diadinoxanthin and diatoxanthin) act as photoprotectants, absorbing
visible light (mostly in the violet/blue portion of the spectrum) and
‘dumping’ this energy as non-radiant heat. In effect, the conversion of
these two xanthophylls under conditions of high light intensities act as a
‘safety’ valve and channel light energy away from the photosynthetic
apparatus in zooxanthellae.

Clade Nomenclature

Unfortunately, there is not a universally recognized protocol for
identifying different zooxanthellae clades. Generally, however, a clade is
identified by n alphanumeric tag – a primary capitalized alphabetical
symbol (A, B, C, etc.) followed by a numerical ID, sometimes a lower case
letter and, rarely, a second lower case letter (as in C3ha). Not all
researchers have followed this code and have labeled newly discovered
strains by a capitalized letter and a symbol unique to that clade (e.g.,
C+, C·). It seems certain that most works use the former method of
classification, and that the latter identification symbols will eventually
conform to a widely-accepted standard.

Be aware that there are several interchangeable names for ‘clade’,
including ‘group’, ‘type’, ‘phylotype’, etc. (LaJeunesse, 2001).

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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 Australia’s Great
Barrier Reef, the Red Sea and the western Pacific (Korea).

Reported Species in Clade “A”:

Clade A1. Symbiodinium microadriaticum
subspecies microadriaticum. Found within tissues of jellyfish
species, including Cassiopeia xamachana, C. andromeda,
Red Sea stony coral Stylophora pistillata (LaJeunesse, 2001) and
Acropora valida, Mombasa, Kenya, 0.3-8m, (Visram and Douglas,
2006). 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 µmol·m²·sec;
Iglesias-Prieto and Trench, 1997).

This cladeis considered thermally tolerant (26ºC – 78.8ºF – was the
experimental temperature) by Hennige et al., 2006. Robinson and Warner
(2006) also report Clade A1 is tolerant of temperature as high as 32ºC
(89.6ºF), but demonstrated a reduction in photosynthetic activity as well
as growth (possibly due to resources being devoted to repair of
zooxanthellae photosystem(s)). Even so, Clade A1 apparently has a capacity
to ‘process’ absorbed light energy (photons), thus preventing a ‘traffic
jam’ of electrons between zooxanthellae Photosystems I and II, thus
preventing chronic Photoinhibition (Hennige et al., 2006). A1 is known to
produce to produce at least two mycosporine-like amino acids
(mycosporine-glycine and shinorine, Banaszak et al., 2006).

Clade A1.1. Symbiodinium microadriaticum
subspecies condylactis. Clade A1.1 is also called Symbiodinium
cariborum
(LaJeunesse, 2001). Hennige et al., 2006 report this clade
is considered to be stressed by higher temperature (26ºC – 78.8ºF (!) – was
the experimental temperature). Robinson and Warner (2006) also report this
clade is sensitive to temperature (experiment condition was 32ºC or
89.6ºF), which is exacerbated in ‘high’ light conditions. A1.1 is found in
the jellyfish Jamaican Cassiopeia frondosa and, not surprisingly,
Condylactis gigantea specimens.

Clade A2 includes several Symbiodinium
‘species’, including: 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 (diadinoxanthin
and diatoxanthin) 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
. It is now considered Clade A2 (LaJeunesse, 2001).

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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. S. corculorum is now
considered Clade A2 (LaJeunesse, 2001).

Besides those animals listed above, Clade A2 is also reported to be
found in Gorgonia ventalina (Puerto Rico and Jamaica), the anemone
Bartholomea annulata, a Pacific hydrocoral Heliopora, and
the ‘giant clam’ Tridacna gigas.

A3 – Tolerant of higher light levels (Hennige et al.,
2006). Known hosts include the jellyfish Cassiopeia mertensii from
Hawaii (LaJeunesse, 2001; LaJeunesse et al., 2004), a Tridacna
clam (species unreported, Baille et al., 2000), Tridacna crocea,
T. maxima, T. derasa, T. gigas, and another
‘giant clam’ (Hippopus hippopus; LaJeunesse, 2001), Montastrea
faveolata
(Belize, across a depth range of 2 to 8m), a Belizean stony
coral (Siderastrea intersepta, @ 8-15m; Warner et al., 2006), the
anemone Condylactis gigantea, stony corals Acropora
palmata
, shallow-water Acropora cervicornis, and
Stephanocoenia michelini. A3 zooxanthellae are known to produce 1
ultraviolet-absorbing compound – the MAA mycosporine-glycine (Banaszak et
al., 2006).

A3a – Found in a ‘giant clam’ (Tridacna sp.)
from the Philippines (LaJeunesse, 2005).

A3b – Reported symbiont of the stony coral
Siderastraea intersepta (Belize, 8-15m; Warner et al., 2006).

A4 – Clade A4, also called Symbiodinium
(=Gymnodinium) linucheae, is found in the Thimble
jellyfish (Linuche unguiculata). A4 is also found in the Caribbean
sea whip Plexaura homomalia (LaJeunesse, 2001), Porites
astreoides
corals from Belize (depth of 2-8m; Warner et al., 2006) and
the anemone Condylactis (LaJeunesse, 2002).

A4a – Porites astreoides, Belize 8-15m (Warner
et al., 2006), the ‘fire coral’ Millepora alcicornis,
anemones Condylactis gigantea and Stichodactyla
helianthus
(LaJeunesse, 2002).

A5 – Found in Tridacna squamosa ‘giant clam’
specimens from Palau (LaJeunesse, 2001). This is possibly the same clade
found in the Pacific ‘soft coral’ Capnella (van Oppen et al.,
2005).

A6 – This zooxanthella was isolated from mantle tissues
of the ‘giant clam’ Tridanca collected from waters off Okinawa,
Japan (depth of 1-10m; LaJeunesse et al., 2004).

A7 – LaJeunesse et al., 2003 reports this clade from
the fire coral Millepora platyphyllia.

A9/A9a – Acropora longicyathus contains these
zooxanthellae clades (LaJeunesse et al., 2003).

A11 – A specialist zooxanthella, found exclusively in
Red Sea Turbinaria corals (Barneah et al., 2007).

A12 – LaJeunesse (2005) found this clade in an unknown
host from a reef aquarium.

A13 – Isolated from a Caribbean Porites
astreoides
(LaJeunesse, 2005).

A14 – A14 is a symbiont of the Caribbean stony coral
Madracis miribalis (LaJeunesse, 2005).

Summary: Generally, Clade A zooxanthellae seem tolerant of high light
intensity, and likely produce protective xanthophylls (for protection from
predominantly ‘blue’ light) and mycosporine-like amino acids (that can
absorb ultraviolet energy). Its existence is sometimes correlated with
shallow back reefs. The number of hosts containing Clade A zooxanthellae
populations are noted to decrease with increasing depth.

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 gorgonians (sea fans, sea whips, etc.), but is
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 the stony
coral Pocillopora damicornis (probably as a cryptic symbiont –
Santos et al., 2004).


figure1.jpg

Figure 1. Phylogenetic radiations of Clade B symbionts
from progenitor Clades B1 and B19. These are mostly from the Caribbean,
although ‘B’ clades are not particularly uncommon in some Pacific
invertebrates (After LaJeunesse, 2005, with additional information from
Thornhill et al., 2005).

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 µmole photons·m²·sec as the sub-saturating intensity, and 250 µmole
photons·m²·sec as the super-saturating light intensity). Banaszak (2006)
detected the presence of MAAs (UV-absorbing compounds) in this
zooxanthella.

Symbiodinium bermudense. A symbiont of the ‘pest’ anemone
Aiptasia pallida. This species apparently produces MAAs under
‘proper’ conditions (Banaszak et al., 2006).

Symbiodinium muscatinei. Also called Clade B4. 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), but instead
acquires them through diet. 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
µmole photons·m²·sec. The compensation point for these algae was about 73
µmole photons·m²·sec.

Symbiodinium californium. This species does not produce
mycosporine-like amino acids in culture (in Shick et al., 2002), but other
evidence suggests S. californium can perhaps do so under
conditions of high light and/or UV intensities. 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: Synthesis of UV protectants
(mycosporine-like amino acids) seems dependent upon environmental
conditions (though this is open to debate). Clade B also seems relatively
tolerant of higher light intensities.

B Clades and Sub-Clades

B1 – Common to many Caribbean invertebrates, including
the pest anemone Aiptasia (from Hawaii, LaJeunesse, 2001), the sea
fan Gorgonia ventalina (Kirk et al., 2005), Oculina
diffusa
(western Atlantic, LaJeunesse, 2001), Caribbean stony coral
Diploria clivosa (Banaszak et al., 2006), Diploria
strigosa
, Favia fragum, the ‘rose’ coral Manicina
areolata
, Montastrea annularis (LaJeunesse, 2002), the stony
coral Pocillopora damicornis in Hawaii, and others, including
Pseudopterogorgia bipinatta and various ‘pesky’ anemones
(Caribbean Aiptasia spp.). Hennige et. al. (2006) report Clade B1
is sensitive to temperatures as low as 26º C (78.8º F), while Robinson and
Warner (2006) report thermally-sensitive B1 demonstrated severe decreases
in photosynthetic activity when exposed to ‘high’ light and a temperature
of 32º C (89.6º F). In the same vein, Gorgonia ventalina specimens
from Florida contained less zooxanthellae when exposed to a temperature of
30.5ºC (86.9ºF), or when the host was infected with fungi Aspergillus
sydowii
. However, the sea fans retained the same clade throughout the
experimental procedures and did not ‘switch’ symbionts. Clade B1 is
equivalent to clade ‘B184’ (based on analysis of the 23S-rDNA; Kirk et al.,
2005).

B1a – Caribbean gorgonians Plexaura homomalia
and Plexaurella nutans. Closely related to clade B1. LaJeunesse,
2004.

B1c – Caribbean corals, LaJeunesse, 2004. Closely
related to clade B1.

B1d – Caribbean corals, LaJeunesse, 2004. Closely
related to clade B1.

B1e – Caribbean corals, LaJeunesse, 2004. Closely
related to clade B1.

B1g – Caribbean corals, LaJeunesse, 2004. Closely
related to clade B1.

B1i – Caribbean corals, LaJeunesse, 2004. Closely
related to clade B1.

B2 – From Caribbean ‘corals’ including Plexaura
flexuosa
and stony Montastraea faveolata. Descended
from Clade B19. LaJeunesse, 2004.

B2.1 – This clade is found in some stony coral
Oculina diffusa specimens from Bermuda, (LaJeunesse, 2001).

B3 – LaJeunesse, 2001, reports B3 is found in the
Caribbean ‘jellyfish’ Dichotomia.

B4 – B4 is Symbiodinium muscatinei, reportedly
found in the temperate/cold water anemoneAnthopleura elegantissima
(LaJeunesse, 2001).

B5 – A specialist zooxanthellae found only in the
Caribbean coral Siderastraea radians. LaJeunesse, 2004.

B5a – Specialist zooxanthellae clade found only in
Siderastrea (Thornhill et al., 2006).

B6 – Colpophyllia natans from the
western Caribbean. Descended from Clade B19. LaJeunesse, 2004.

B7 – Madracis decactis (Family
Pocilloridae) from southern and western Caribbean, LaJeunesse, 2004.

B8 – Caribbean gorgonian Pseudoplexaura
flexuosa
(LaJeunesse, 2004). Closely related to clade B1.

B9 – Isolated from Caribbean hosts
Colpophyllia natans and Eunicea mammosa.
Descended from Clade B19. LaJeunesse, 2004.

B10 – A specialist zooxanthella clade fromCaribbean
corals Montastrea annularis, M. faveolata and
M. franksi (Thornhill et al., 2005). Closely related to clade B1
(LaJeunesse, 2004).

B11 – Caribbean corals, LaJeunesse, 2004.

B12 – Caribbean corals, LaJeunesse, 2004. Closely
related to clade B1.

B13 – A specialist clade from Madracis spp.
from southern Caribbean, LaJeunesse, 2004.

B13a – A specialist clade from stony coral
Madracis spp. (those collected from the northeast Caribbean,
LaJeunesse, 2004).

B14 – Caribbean corals, LaJeunesse, 2004.

B16 – Caribbean corals, LaJeunesse, 2004. Closely
related to clade B1.

B17Montastraea faveolata in Belize and
Caribbean corals, LaJeunesse, 2004. Closely related to clade B1.

B19 – B19 is believed to be an ancestor to many ‘B’
Clades. It has been isolated from a newly settled polyp of the Caribbean
‘soft coral’ Briareum, LaJeunesse, 2005.

B19a – Zooxanthella found in Colpophyllia,
from the NE Caribbean – Descended from Clade B19. LaJeunesse, 2004.

B19b – Caribbean corals. Descended from Clade B19.
LaJeunesse, 2004.

B20 – Caribbean corals, LaJeunesse, 2004. Closely
related to clade B1.

B21 – Caribbean corals, Descended from Clade B19.
LaJeunesse, 2004.

B22Colpophyllia – Descended from Clade B19.
LaJeunesse, 2004.

B23 – Caribbean corals, Descended from Clade B19.
LaJeunesse, 2004.

B24 – Caribbean corals, LaJeunesse, 2004. Closely
related to clade B1.

B25 – Isolated from a newly settled polyp of the
Caribbean (Florida) ‘soft coral’ Briareum, LaJeunesse, 2005.

B26 – From the gorgonian Plexaura kuna
collected in the Panamanian Caribbean. Descended from Clade B19
(LaJeunesse, 2004).

For now, this ends our discussion of diversity and distribution of
zooxanthellae clades ‘A’ and ‘B’ and their respective sub-clades. Next
time, we’ll examine those clades found mainly- but not exclusively – in the
Pacific (clades C, D, E, F and G).

References and Further Reading

  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. ———–, 2003. Flexibility and specificity in coral/algal
    symbiosis: Diversity, ecology and biogeography of Symbiodinium. Annu.
    Rev. Ecol. Syst., 34:661-689.
  4. ———–, In Press. Symbiont diversity on coral reefs and its
    relationship to bleaching resistance and resilience.
  5. ———— 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. ————-, 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.., M. Santos, T. LaJeunesse and M. Lesser, 2006. The
    distribution of mycosporine-like amino acids (MAAs) and the phylogenetic
    identity of symbiotic dinoflagellates in cnidarian hosts from the Mexican
    Caribbean. J. Exp. Mar. Biol. Ecol., 337:131-146.
  8. ——————, 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.
  9. Barneah, O., V. Weis, S. Perez and Y. Benayahu, 2004. Diversity of
    dinoflagellates symbionts in Red Sea soft corals: Mode of acquisition
    matters. Mar. Ecol. Prog. Ser., 275: 89-95.
  10. ————-, I. Brickner, M. Hodge, V. Weiss, T. LaJeunesse, and Y.
    Behahayu, 2007. Three party symbiosis: Acoelomorph worms, corals and
    unicellular algal symbionts in Eilat (Red Sea). Mar. Biol.
  11. 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.
  12. 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.
  13. Coffroth, M. and S. Santos, 2005. Genetic diversity of symbiotic
    dinoflagellates in the genus Symbiodinium. Protist,
    156:19-34.
  14. 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.
  15. 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.
  16. Garren, M., S. Walsh, A. Caccone and N. Knowlton, 2006. Patterns of
    association between Symbiodinium and members of the
    Montastraea annularis species complex on spatial scales ranging
    from within colonies to between geographical regions. Coral Reefs, 25:
    503-512.
  17. Gosliner, T., D. Behrens and G. Williams, 1996. Coral Reef
    Animals of the Indo-Pacific
    . Sea Challengers, Monterey, Ca. 314
    pp.
  18. Goulet, T. and M. Coffroth, 2004. The genetic identity of
    dinoflagellates symbionts in Caribbean octocorals. Coral Reefs, 23:
    465-472.
  19. 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.
  20. Hennige, S., D. Suggett, M.Warner and D. Smith, 2006.
    Photoacclimation of Symbiodimium revisited: Variation of
    strategies with thermal tolerance? Natural Environment Research Council,
    University of Essex.
  21. Hunter, C.L., C.W. Morden, and C.M. Smith, 1997. The utility of ITS
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