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You are here: Home Volume VI April 2007 Feature Article: An Update on Zooxanthellae (Symbiodinium spp.) What a Difference a Year Makes!

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

By Dana Riddle Posted Apr 14, 2007 08:00 PM Pomacanthus Publications, Inc.
This article, the first of two parts, is a follow up on an article printed in Advanced Aquarist entitled ‘Lighting by Number’ and discusses Clades ‘A’ and ‘B’.

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)).

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.

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).

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).

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 sequences in assessing relationships among zooxanthellae and corals. Proc. 8th Int. Coral Reef Symp., Panama. 2: 1599-1602.
  22. Iglesias-Prieto, R. V. Beltrᮬ T. LaJeunesse, H. Reyes-Bonilla, and P. Thom鬠2004. Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proc. R. Soc. Lond. B., 271:1751-1763.
  23. Jeffrey, S., R. Mantoura and S. Wright, eds., 1997. Monographs on Oceanographic Methodology: Phytoplankton Pigments in Oceanography. UNESCO Publications, Paris. 661 pp.
  24. Kemp, D., C. Cook, T. LaJeunesse and W. Brooks, 2006. A comparison of thermal bleaching responses of the zoanthid Palythoa caribaeorum from three geographically different regions of south Florida. J. Exp. Mar. Biol. Ecol. 335: 266-276.
  25. Kirk, J.T.O., 1983. Light and Photosynthesis in Aquatic Ecosystems. Cambridge University Press, Cambridge. 401 pp.
  26. Kirk, N., J. Ward and Coffroth, 2005. Stable Symbiodinium composition in the sea fan Gorgonia ventalina during temperature and disease stress. Biol. Bull., 209: 227-234.
  27. Kuffner, I.B., M.E. Ondrusek and M.P. Lesser, 1995. Distribution of mycosporine-like amino acids in the tissues of Hawaiian scleractinia: a depth profile. In: Ultraviolet Radiation and Coral Reefs. D. Gulko and P.L. Jokiel, Eds. HIMB Tech. Report #41.
  28. LaJeunesse, T. and R. Trench, 2000. Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the inter-tidal anemone Anthopleura elegantissima (Brandt). Biol. Bull. 199: 126-134.
  29. -----------------, 2000b. Investigating the biodiversity, ecology and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region in search of a species level marker. J. Phycol., 37: 866-890.
  30. -----------------, 2002. Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar. Biol., 141: 387-400.
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