Steve Tyree - Articles and Papers

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          Scleractinian Corals in Nature and Captivity





          Part I - Coral Bleaching and Photoadaptation

                   Dynamics in Nature and Captivity 

                   including a recent Captive System 

                   Description.








 

                    Steve Tyree - Coral Breeder  


 
                     California, September 1995











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  This paper is being presented to the 1995 Marine Aquarium Conference
of North America [MACNA 95] via the Louisville Marine Aquarium Society 
on September 17th 1995. A verbal presentation covering the basics pre-
sented in this paper will also be given by the author during the 1995 
MACNA. Due to work constraints and the timeleness of the data contained 
within this paper, it has been submitted without formal review. The 
author and conference organizers accept no responsibility for the use 
or missuse of the data contained within. For correction submition see 
the ongoing errata section at the end of the paper. The Breeder's Regis-
try will be the distribution center for errata and reference exchanges.
The information contained in this paper is copyrighted by Steve Tyree 
and any redistribution of this information must first be approved by 
said author. Any non-profit use is exempt from these redistribution 
restrictions..


Copyright @ September 1st 1995 Steve Tyree.


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========================================================================
 Introduction
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 The art and science of keeping Hermatypic Scleractinian Stony Corals
in captivity has advanced quite dramatically in the past few years. Many
reefkeepers are stimulating natural coral growth rates, natural sexual
propagation and natural as well as artificially produced asexual pro-
pagation. Hermatypic corals are composed of a symbiosis between a coral
animal and plant algae _Symbiodinium (=Gymnodinium) microadriaticum_,
called zooxanthellae. In this paper, the current captive system method-
ology used by the author will be discussed in relation to other tech-
niques currently used around the world. 


 Recently, coral bleaching has become an important concern for corals 
inhabiting nature and researchers are exploring the causes and the 
resulting implications. Coral mortality in general has also been studied
in nature throughout this century. This paper includes a summary of that
scientific work and highlights and analyzes some of the major papers 
detailing the research. Captive held coral mortality and bleaching 
events, when they do occur, seem very similar in physiology to those 
events studied in nature. The implications of using captive systems to 
verify and test hypothesis or establish environmental parameter ex-
tremes for these symbiotic corals will also be explored in this paper.

 
 A rather extensive reference section is included and each listing is 
cited within the paper. This listing includes many of the major scien-
tific papers concerning coral bleaching, coral mortality and photoadap-
tation in nature. The author encourages captive reefkeepers to obtain
and study that research as most of the data is applicable to keeping
corals in captivity. There are however many captive system parameters
that are unique and these will require applied research by captive reef
maintainers to quantify.


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 Captive Support Systems Used to Maintain Corals in Captivity
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 There currently are three main approaches to maintaining tropical reef
invertebrates in captivity. Algal Turf Scrubbing, Jaubert's Live Sand
Bed and what has been referred to as the Berlin Methodology. All three
systems have many similarities. They keep inorganic nitrate levels low
and can support fish and soft octocorals quite adequately. All three of
these methodologies are based on the "Nature's System" developed by Eng
in the Phillipines during the late 60's and early 70's. Mr. Eng also
worked with Mr. Tan Soen Hway of Banguwangi who he credited as being a
pioneer in discovering this system (Eng 1961). The main theme is to 
duplicate nature as closely as possible. No mechanical filtration is 
utilized so that planktonic populations densities are kept near normal. 
Live rocks from the sea that contain microscopic plants and organisms 
are added prior to putting in higher order invertebrates. Mr. Eng also 
recommended using natural seawater but newer artificial brands available 
today seem to do an adequate job. 


 The three systems in current use differ in additional filtration method-
ology utilized and the resulting calcification potentials. While the
Algal Turf Scrubbing System can support natural calcification poten-
tials, the high dissolved organic compound levels and proliferating
algal growth in some of these captive systems, may inhibit that rate. 
In the United States, we are all still researching the Jaubert Live 
Sand Bed and should await Dr. Jaubert's presentation at Macna VII for 
furthur clarification. The Berlin Method (as it is known in the United 
States) utilizes a foam fractionator to remove dissolved organics and 
includes the addition of Ca(OH)2 via kalkwasser topoff water for calcium
replenishment. Recently, german reefkeepers have been experimenting with
a Calcium Carbonate Reactor termed the Lubbock Reactor. When utilizing 
a protein skimmer the potential for plankton stripping needs to be con-
sidered. Therefore, the flow through rate can become a critical adjust-
ment in such systems. 

 The author utilizes a Hybrid Berlin Methodology that is also based on 
the Eng Nature's System with the addition of a protein skimmer, a large 
live sand and live rock refugia and some very dynamic water flow due to 
the use of partially and completely submersed water pumps. Image 1 and 
Image 2 were taken at the start of September, 1995. The reef in Image 1 
(180 A) is a 684 liter system setup after a recent move in November of 
1994. Image 2 is of a second 684 liter system (180 B) setup in December 
of 1994. Both of these systems are connected to a common 684 liter sump
that holds 608 liters when operational. Figure 1 is a diagram illustrat-
ing how the two captive aquaria are connected to this sump. A large
counter current recirculating venturi foam fractionator with an 1 1/2
inch venturi valve is connected to the sump. Images 3-5 are closeups
of captive reef system 180 A taken in early September 1995.

 The total system water capacity of a captive system can be increased 
by using an extra reservoir or by allowing the water level to remain 
high in a oversized sump. Increasing the water volume has obvious 
benefits and by adding live sand and live rock to the sump, a refugia 
can be established that follows the basic principals in Adey and Love-
land (1991). The authors 684 liter sump is illustrated in figure 2. 
The added water capacity helps stabilize the daily environmental 
fluctuations, dissipates coral slime and increase the buffering capacity
of the system. When a reef with high coral density experiences a burst 
of natural calcification, the buffering system and calcium levels are 
severly altered. Additionally, corals release slime or mucus when 
stressed by movement, exposed to air, stung by adjacent corals or 
covered with settling particulate matter. Systems with small water to 
coral ratios, may need frequent water changes and large capacity protein
skimmers. The author is aware that many reefkeepers are attempting to 
keep these scleractinian stony corals without protein skimmers but the 
previously stated concerns should be taken into consideration. 


 Live sand is placed on the bottom of the refugia to act as a parti-
culate matter settling area. Some sand shifting fish and invertebrates 
have also been added. The main aquaria have bare bottoms due to the
strong dynamic water current that these types of corals demand. Since 
the live rock in the sump exists in a low light environment, a low 
light refugia has been established where sponges and other similar
organisms flourish. The main aquaria also contains a ridge of live
rock but as the corals grow, the rock beneath them is moved into the
sump. This allows large mother colonies to exist in the aquaria and
they are used as a source for producing asexual captive grown fragments.


 When positioning pump outputs to establish strong dynamic current
flows, do not direct a constant strong stream directly at an hermatypic
stony coral. You can eventually blast the tissue off. In fact, scientist
have used a water pick in the laboratory when coral tissue needed to be 
removed for analysis (Hoegh-Guldberg and Smith 1989). One way to create 
non-liner, dynamic or chaotic current flows, is by directing outputs of 
pumps so that water currents collide. Additionally, random or preset 
timers can control the pumps length of time on or the power ratio 
applied. The author has been experimenting with rotating pumps in each 
main aquaria that rotate through a 90 degree arc once per minute. They 
have worked very well and the polyp extension rate of most stony 
corals, including acropora tables, has increased.


 This year (1995) has been an exciting and confusing one for reef 
lighting systems. New 10,000 K and 20,000 K bulbs have appeared on 
the market that are manufactured in Germany and the US. The author
is employing 3 different lighting setups in three main aquaria. Reef
aquaria 180 A has 3-6500 K 175 watt metal halides that provide an 11 
hour daytime photoperiod. Two 160 watt VHO actinic 03's are also 
used for twilight and kept on all day to stimulate coral UV-A pig-
ments. In addition to these bulbs, 2-400 watt 20,000 K bulbs are on 
for a mid-day peak period of 6 hours. Reef aquaria 180 B has 3-175 
watt 10,000 K metal halides with 2-140 watt VHO fl bulbs. The front 
fluorescent is a daylight bulb and the back one is an actinic 03. This 
setup has kept many of the colorful pigments that the corals had when
they were imported. The tranship and fragment growout reef has 3-175 
watt 20,000 K metal halides with 2-110 watt VHO daylight bulbs. The 




new high color temperature metal halides provide a strong green, blue, 
violet and upper UV-A. The author has noted that the colored blue and
purple Acropora imported from Fiji, will ecomorph into a dark brown 
color if not kept under the higher color temperature bulbs. If lower 
temperature metal halide bulbs are used, then it is best to supplement 
with actinic fluorescent lights. The reason for this will be explained 
furthur into this paper.


 When replacing evaporated water in the authors semi-closed systems, 
Reverse Osmosis and Deionized water is utilized. This topoff water 
is mixed with Calcium Oxide or Hydroxide and forms kalkwasser that
is added every day via morning manual addition. Exercise caution when
using kalkwasser due to its caustic composition. When you achieve a 
high density of SPS corals growing rapidly in a semi-closed system, 
you will find that the calcium demand will increase dramatically. 
One may have to resort to Calcium Chloride, which requires adding 
additional buffer, or adding a highly concentrated or non-decanted 
Kalkwasser via a milky swirl. If this is done a pH meter is required 
to prevent a rise above 8.5. Fossa (1994) stated that many of the best
scleractinian reef tanks in Europe utilize CO2 injection to keep the 
pH below 8.5 in late afternoon when it is climbing to its peak value. 


 Some reefkeepers have also reported success with organic or chelated 
calcium additives. The author primarily uses Kalkwasser and Calcium 
Chloride but has begun experimenting with a chelated calcium product. 
Nilsen (1995) recently described the Lubbock Calcium Carbonate Reac-
tors being utilized in Germany. Calcareous gravel is placed inside the 
reactor where carbon dioxide in injected to bring the pH level down 
to 6.5. This allows the gravel to dissolve as replenishment water is 
pumped through and slowly added to the reef system. One could utilize 
2 separate pH controllers to regulate the CO2 addition and to make 
sure the pH in the reef does not drop too low. The current methodology
employed is to run the water through the reactor continuously along 
with a very slow injection of CO2. That could eliminate the need for 
two high quality pH controllers.


 In the authors high calcification demand reefs, the addition of 
Ca(OH)2 powder into the large sump during low pH periods has been
utilized in conjunction with adding typical kalkwasser makeup water. 
The powder method is used in the morning when pH is low and the effect 
on pH is kept to a minimum. The typical low morning pH helps dissolve 
the Ca(OH)2 powder into seawater. When using this method it is best to 
not elevate the calcium concentration of the reef too high as it then 
becomes difficult to dissolve additional calcium into the water. If 
this procedure is done correctly via a large sump. no cloudiness will 
enter the main reef. You may have to stir up the sump water to help 
dissolve the Ca(OH)2 powder. At night when pH is elevated and just 
starting to fall from its daytime peak, normal kalkwasser is added to 
replace evaporated water.


 Another item essential to long term success with captive sclerac-
tinian corals is herbivores. Each of the authors captive systems 
contain a few tangs and other algae eating organisms like astrea 
snails and hermit crabs. Adey (1994) noted that algae do hold a
competitive edge on the tropical reef and if herbivores are lacking, 
the algae can take over the reef. This has occurred in many Caribbean 
reefs, the Mediteranian Sea and isolated reefs in the pacific where 
nutrient levels have become elevated. Similar outbreaks of nuisance 
algae have occured in captive systems employing the current method-
ologies. In the major stony reef regions of the Indo-Pacific, nutrient 
levels are low and calcification potentials are high enough to limit 
the algal growth. Once the herbivores get control of the algal growth 
in semi-closed captive systems, supplemental feeding may have to be 
increased. These systems will typically have a high nutrient concen-
tration in the water. Herbivores can keep the micro and macro algal 
growths under control while the symbiotic coral zooxanthellae might
utilize the increased nutrients in the water. 





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 Typical Scleractinian Stony Coral Growth Achieved in Captivity 
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 Natural growth rates for Scleractinian stony corals have been achieved
in quite a few captive systems around the world. The authors first
_Acropora sp._ coral is shown in Image 6 which was taken on 7/5/92. The
first new branch can be seen in the lower right. Image 7 was taken on
9/16/92 and new branches are easily seen. Then the coral experienced 
a burst of growth and Image 8 was taken on 12/25/92. The coral then 
slowly continued to grow as shown in Image 9 taken on 9/13/93. Toward
the end of 1994 the author was forced to move and when this coral
finally ended up in its current reef aquaria (it took 3 people to move
it carefully) it was repositioned and is shown in Image 10 taken on 
1/1/95. The coral had lightened in color due to being held temporarily
in a very shallow reef with intense lighting. Many of the branch tips 
had receded but the coral survived and then ecomorphed into the new reef
where it is shown in Image 11 taken on 9/1/95. This coral is now very
healthy and beginning to grow at very good rates. Polyp extension during
the day gives the coral a fleshy type apearence.

 The author has had a couple of _Acropora sp._ tables grow at near 
natural rates. Image 12 was taken on 9/12/94. Note the small settled
_Pocillopora damicornis_ juvenile coral to the right of the table in
Image 13. This photograph was taken on 1/15/95. It is assumed that
the juvenile coral was spawned in the captive reef since quite a few 
other identical corals have appeared attached to the walls and PVC 
parts in the aquaria. The table measured 8 cm tall, 8 cm wide and 7
cm deep on 1/7/95. Image 14 was taken on 4/16/95 and many new branches can
be seen as the table shape is spreading out. Also note how the settled
_Pocillopora damicornis_ has grown. The last photograph, Image 15, was
taken on 9/1/95 and the table masured 8 cm tall, 14 cm wide and 19 cm
deep.

 During the move in late 1994, a large staghorn species of _Acropora_
started receding or suffering tissue necrosis due to relocation stress.
The author was able to save two fragments from this large coral. Image
16 was taken on 1/29/95 and shows one of the two fragments that had a
maximum width measurement of 37 mm. This fragments width measured 80
mm on 4/1/95. On 9/10/95 Image 17 was taken and the maximum width 
measurement was 150 mm. This growth occured in spurts and branch tips
were incidently broke on a few occasions. The second fragment is shown 
in Image 18 which was taken on 2/12/95. A maximum width measurement 
was 30mm. On 4/1/95 the maximum width was 63 mm. The fragment/colony 
is shown again in Image 19 on 9/10/95 and had a maximum width of 160 
mm. Many of the branches on this coral were broken accidentaly or in-
tentionally to try to take control over this species growth. Weedy 
corals like this can expand into an area quickly but are sensitive to 
fragmentation.

 A colorful _Acropora millepora_ is pictured in Image 20 which was taken
on 5/3/94. The coral is then shown in Image 21 on 8/8/94 just 3 months
later. Unfortunately, this coral did not survive the relocation. The
authors new reefs have been running for 10-11 months and current growth
rates are very fast.  

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 Coral Bleaching in Nature and Captivity 
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   The Symbiosis of the Coral Animal Host and Zooxanthellae Plant
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 The hermatypic SPS corals all contain zooxanthellae within their polyp 
tentacles and tissues, This symbiosis consists of a host animal (the 
coral) and symbiont plants (the zooxanthellae algae). The intimate 
association between living plant cells and animal cells or tissues is a 
phenomenon of widespread occurrence. Although plant-animal symbioses 
have been under study for over a century, progress has been remarkably 
slow, probably because these phenomena have often been relegated to the 
realm of "biological curiosities". By comparison, other areas of sym-
biosis such as parasitism have made many advances because of medical 
applications (Trench 1979).


 Corals that harbor symbiotic zooxanthellae are called hermatypic while
those that do not are called ahermatypic. Hermatypic corals are subject 
to "bleaching" events where the symbiont zooxanthellae leaves or are ex-
pelled and the resulting internal population is lower. The normal 
density of zooxanthellae per area of coral host ranges from 0.72 x 10^6 
to 2.48 x 10^6 cell/cm^2. (Drew 1972). These zooxanthellae appear brown 
to our eyes and their population density can be estimated by their brown
coloration intensity. Corals can also appear bleached if the zooxan-
thellae light collection pigments shrink due to a strong light field. 
The population density will remain unchanged or drop very little but 
the brown color appears lighter. The problem of regulation of symbiont 
numbers is basic, and our knowledge of this phenomenon is extremely 
primitive. Such regulation is probably closely linked to interactions 
between host and symbiont genomes, but we know virtually nothing about 
these phenomenon (Trench 1979). To fully understand the captive and 
natural behavior of this symbiosis, the plant and animal may sometimes 
require separate examination and discussion.


 Colonies of the coral _Stylophora pistillata_ growing in high light
environments can obtain all the reduced carbon needed for animal res-
piration from photosynthesis by symbiotic zooxanthellae. In contrast,
colonies in shaded reef areas must acquire 60 % of their reduced carbon
heterotrophically. More than 90 % of the carbon fixed by zooxanthellae
is translocated to the animal host in both light regimes, but very 
little is assimilated, apparently because the translocated products
are deficient in nitrogen. Thus, the coral's overall growth efficiency 
is similar to that of aquatic herbivores that forage actively (Falkow-
ski et al. 1984).


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    The History of Coral Bleaching and Mortality in Nature
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 Natural factors affecting corals have been documented in the scientific 
literature since early this century. The particular factors that were 
hypothesized as causing potential bleaching or death include- waves
generated by hurricanes and cyclones, salinity alteration from heavy
rainfall that often accompany tropical storms, siltation stress from
heavy rainfall, thermal stress and exposure to air from extreme low
tides (Jaap 1979). Recently, ultraviolet radiation has been hypothesized
as inducing corals to bleach (Gleason and Wellington 1993). It has also
been shown to cause coral mortality in increased dosages (Jokiel 1980).


 Bleaching of scleractinian corals (loss of color caused by the loss of
symbiotic zooxanthellae or their pigments) was reported in Vaughan 
(1911) when bleached heads of _Orbicella (=Montastrea) annularis_ were
caused by tidal emergence at Dry Totugas, Florida. "Bleaching", was 
furthur described by Vaughan (1914) as a stress response of corals 
resulting from exposure at low tide, salinity reduction or darkness 
(Jokiel and Coles 1990). A later incident was reported at Bird Key, 
Dry Tortugas, which had been apparently heated by several days of calm 
wind conditions. Fatalities occured amongst Octopus and fishes while 
corals were reported injured (Mayer, 1918).

 The Yonge and Nicholls (1931a,1931b) papers reported expulsions of 
zooxanthellae from _Favia_ and _Gonastrea_ at Low Isles reef, Australia 
that were attributed to natural thermal stress. Coral Bleaching in the 
laboratory was induced by stresses of heat, starvation, altered salinity 
and total deprivation of light (Yonge and Nicholls 1931b).




 In October 1963, hurricane Flora deposited 550 mm of rain on Port 
Royal, Jamaica. This was reported to have caused massive zooxanthellae
expulsion among hermatypic organisms inhabiting shallow reefs (Goreau
1964). Salinity stress was indicated as one of the most plausible 
factors inducing this bleaching.


 Growth studies on transplanted _Acropora cervicornis [Lamarck 1816]_
suffered zooxanthellae expulsion in late summer but regenerated their
symbionts when cooler temperatures returned (Shinn 1966). Glynn (1968)
reported massive mortalities among colonial zoanthid _Palythoa_ at
Caracoles reef flat, Puerto Rico that coincided with low tides at or
near midday. A later study revealed mortalities of _Porites furcata 
(Lamarck 1816)_ communities on shallow reefs near Magueyes Island, 
Puerto Rico (Glynn 1973).


 Scleractinian deaths on a reef flat in the Gulf of Eilat were reported
when synergistic meteorlogical and astronomical factors caused emergence 
of the reef flat in the heat of the day (Loya 1972). Zooxanthellae 
expulsion and coral mortality due to thermal addition from power plant 
cooling water discharges has been discovered in Kahe, Hawaii (Jokiel 
and Coles 1974) at Card Sound, Florida (Purkerson 1973) and at Tan- 
guisson, Guam (Jones et al. 1976).  


 During the 1980's minor localized bleaching and mortalities were re-
ported throughout the coral reef regions. In addition, four major 
bleaching events or complexes occured that encompassed unprecedented 
geographic scale and or frequency. These coincidentaly occured during a 
period of suspected global warming (Glynn 1991). Research on coral
bleaching was increased dramatically due to these large scale regional
events that will be summarized below.


 In 1979-1980 coral bleaching was reported in two areas of the Pacific, 
(The Great Barrier Reef, Australia and Ryukyu Island to the north) and 
2 areas of the Caribbean Province. The bleaching was extensive at
Ryukyu Island but restricted to specific sites (i.e.- to particular
islands or reefs) elsewhere during this bleaching complex (Glynn 1991).


 A remarkably strong El Nino-Southern Oscillation (ENSO) event occured
in 1982-1983. It was possibly the strongest event of this kind in the
past 200 years and caused intense and widespread ocean warming in the
equatorial eastern pacific (Glynn 1989). Severe bleaching and mass mor-
talities were reported around Coasta Rica, Panama, Columbia and Ecuador.
Overall, disturbances were reported across the entire Panamic Province,
at 12 sites in the Indo-Pacific Province and at five sites in the Cari-
bbean Province (Glynn 1991). 


 Another moderate ENSO event occurred in 1987 which caused the 1986-1987
bleaching complex that occurred at 12 sites around the globe. Reefs 
throughout the Red Sea were affected along with the entire extended
Caribbean Region including the Flower Garden Banks (Gulf of Mexico) and
Bermuda (Glynn 1991).


 The 1989-90 bleaching event was confined largely to the Caribbean 
Region. This had led to greater coral mortalities in parts of the 
Florida Keys and on the southern Puerto Rican coast (Glynn 1991).


 In addition to these recent large scale bleaching complexes that may 
have been associated with warming water, other recent bleaching events 
and incidences of coral mortality were documenting that may not be 
caused by warming water alone (Brown 1987). They will be summarized 
below.







 In the Indo-Pacific from January to March 1982, mass bleaching and 
extensive coral mortality occurred at Lizard Island, Great Barrier Reef
in depths of 2-9 m. A summer of unusually low rainfall, higher than 
average hours of sunshine and high water temperatures may have combined
synergistically to cause the bleaching and mortalities (Harriot 1985). 
In the Central and Northern Great Barrier Reef extensive bleaching of 
hard and soft corals occurred during the same time period. It has been 
suggested that bleaching in this region might be a seasonal phenomenon 
due to its occurrance in previous years. High temperature and high 
light levels have been hypothesized as being responsible (Oliver 1985).
A high incidence of bleaching and mortality on reef flats and shallow
reef slopes was reported from February to March 1982 at Myrmidon Reef,
Great Barrier Reef. The cause has been reported to be due to subaerial
exposure that induced abnormally high levels of solar radiation (Fisk
and Done 1985).


 In the Caribbean Florida Keys, Key Largo reefs and Key West reefs ex-
tensive coral bleaching and mortality occurred at depths of 13-14 m on
September 1983. The proposed casue of decline was increased seawater
temperature (~30 C) in Florida Bay 4-10 September in combination with
midday low tides August 31 to September 5 (Jaap 1985). At San Blas 
Islands off the Caribbean coast of Panama, extensive coral bleaching 
and mortality occurred in early June 1983. An exaggerated seasonal
warming with temperatures in excess of 29 degrees C, that lasted for
a duration of two months was probably the cause (Lasket et al. 1984). 
In St. Croix, US Virgin Islands a local widespread death of _Acropora 
palmata_, a major reef builder in the area, has been occuring since 
1977. Gladfelter (1982) has attributed the cause to "White Band" 
disease.


 Although the natural environmental factors affecting scleractinian 
stony corals have been studied quite extensively, there is still plenty
of research that needs to be undertaken. One area that could be investi-
gated furthur is synergistic or combined affects of multiple environ-
mental parameters. While some known causes of coral bleaching have been 
identified, species variability and the individuals corals ability to 
adapt to sudden or long term changes are additional areas where applied
research might be utilized. Captive systems could play a key role in 
determining the environmental limits each species and local ecomorph can 
tolerate. The applied research gained could be used to substantiate 
natural field research or might even be used as an indicator that an 
area has been exposed to an extreme environmental condition. Lauth 
(1994) described a method of applied research that consisted of poten-
tially exposing captive systems to simulated typical pollution releases 
by human societies.


 
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   Proposed Bleaching Definitions
------------------------------------------------------------------------



 Scleractinian stony corals and symbiotic zooxanthellae are considered
to be simple animals or plants when analyzed individually. However when
in symbiotic association, the symbiosis itself is very complex and this
is one of the main reasons that so little is known about bleaching. We
do know of specific and synergistic environmental parameters that can
induce bleaching. These are varied and the type of bleaching they induce
can also vary dramatically. The appearance of bleached corals has been
described in three degrees: 1) bleaching in which the colony loses all 
of its color, 2) bleaching in which the loss of color is in patches 
scattered over the surface of the colony, and 3) lightening or paling of 
the colony in which the color becomes lighter than normal, but does not 
disappear completely (Kobluk and Lysenko 1994). The most severe degree
of bleaching might be when corals are exposed to extreme environmental
conditions. A strong tissue retraction occurs that may reduce the en-
vironmental stress. Some corals might utilize this retraction to reduce 
the environmental rigors of life in shallow waters and intertidal areas
(Brown and Tissier 1992).





  The investigation of coral bleaching might be easier to undertake if 
the different known causes and different degrees of bleaching were 
defined or stated whenever bleaching is researched or discussed. This
author will utilize terminology that has appeared sporadically in the
scientific literature and also develop a few new terms to help convey
information. It is most practical to separate Tissue Necrosis or Tissue
Receding from the concept of bleaching. Tissue Necrosis and Receding 
occur when the coral animal tissue is dying or disintegrating. This can 
occur due to bacterial infections, protozoan infections or exposures to 
extremelly harmful environmental factors. Tissue Retraction, a strong
reaction when the coral animal is exposed to extreme environmental 
stress, also needs to be defined separately from bleaching. Typical 
bleaching occurs while the coral animal tissue is still intact and 
behaving normally, but either the algal symbiont (zooxanthellae) is 
expelled from the host or has lightened in color due to photoadaptation.
The author will attempt to separate "bleaching" from photoadaptation 
later in the article. 


 It has become common to define Zooxanthellae Expulsion Bleaching (the 
plant algae is expelled from the host coral animal) separately from 
Zooxanthellae Pigmentation Bleaching (the plant algae lightens in color
due to shrinking collection pigment areas). The zooxanthellae pigments 
and resulting coloration that occurs in the coral animal are not the 
only pigmentation in the symbiosis. The coral animal can create and 
maintain UV absorption substances, UV reflecting pigmentation and UV 
fluoresceing pigmentation (Catala-Stucki 1959)(Kawaguti 1969)(Logan 
et al. 1990)(Mazel 1995)(Dunlap and Chalker 1986)(Dunlop et al. 1988)
(Drollet et al. 1991)(Karentz et al. 1991). The bleaching or weakening
of these pigments can be described as Coral UV Pigmentation Bleaching.
When corals are exposed to extreme environmental conditions, one of 
the first indications can be a loss or expulsion of the coral animals 
UV pigmentation. When these pigments are expelled they can color the
water containing the coral in captivity or be seen leaving rapidly in
clouds from corals in larger water volumes. Corals imported into the
United States do usually suffer some form of minor or major zooxan-
thellae bleaching but also suffer coral uv pigmentation bleaching to 
an equal or greater extent. The term Coral UV Pigmentation Expulsion 
has been adopted by the author to describe the extreme situations. 


 Coral and zooxanthellae colors or pigments can not only bleach or 
lighten in appearance, but they can also darken or intensify. This re-
covering or adaptation has been termed "coloring" by the author. A
symbiosis might experience Zooxanthellae Pigmentation Coloring (plant
light collection pigments increase in size) or Zooxanthellae Expulsion
Coloring (new zooxanthelale are injected back into the animal). It is
still presently unknown whether corals can actively take in or inject
algae from the surrounding water, although many have assumed that it
is a method that corals do utilize. Alternatively, the only method a
coral might use to recolor from an expulsion bleaching, is to have
the few existing algae repopulate the coral animal through asexual
reproduction. No known phase of zooxanthellae sexual reproduction has
been discovered. Perhaps the term Zooxanthellae Internal Repopulation
of Zooxanthellae External Repopulation might more accurately describe
these situations. Coral UV Pigmentation Recoloring is used to identify
an increase in the reflecting and fluoresceing pigments.


 To better convey the information of a specific bleaching event, the
primary causes that induced the bleaching should also be used in the
bleaching description. A Zooxanthellae Temperature Expulsion Bleaching
could be used to describe an expulsion that was induced by a sudden
change in temperature. One could define the description more precisely
by adding whether it was induced by "Warm" or "Cold" temperature. 
Another example would be Coral Warm Temperature UV Pigmentation Bleach-
ing. Salinity stress has also been known to cause expulsion bleaching.
An example would be Zooxanthellae Low Salinity Expulsion Bleaching.
Zooxanthellae Sedimentation Expulsion Bleaching could define an expul-
sion that was induced by increased sedimentation. The effects of UV
light can also be described as Zooxanthellae UV Irradiance Expulsion
Bleaching or Coral UV Irradiance UV Absorption Recoloring for example.



 The justification for including the environmental stress that induced
the bleaching or recoloring into the description of the event, is due 
primarily to the possibility that many different types of stresses can 
cause distinct physiological responses in the symbiosis (Gates et al. 
1992). For example, the affects of salinity shock are different on the 
cellular level than the affects from a temperature shock but both may 
cause eventual zooxanthellae expulsion.


------------------------------------------------------------------------
   Zooxanthellae Expulsion Bleaching
------------------------------------------------------------------------


 In response to sudden environmental stress, corals can expel large 
numbers of their symbiotic zooxanthellae which leaves them weakened and 
could even possibly lead to death (Yonge and Nichols 1931a,b)(Goreau 
1964)(Glynn 1984)(Lasker at. al. 1984)(Fisk and Done 1985)(Harriot 1985)
(Oliver 1985)(Roberts 1987,1988). A possible regulatory function that 
controls zooxanthellae population densities living within corals, has 
not yet been identified (Gates 1990). Zooxanthellae Expulsion Bleaching 
appears as a loss of colouration that is probably associated with an 
overall reduction in algal population, involving either active expulsion
of the algal symbionts by the host, or migration of the zooxanthellae 
out of the host tissues and into the surrounding seawater (Hoegh-
Guldberg et al. 1987). One particular study did look for a normal daily 
expulsion rate of the algae symbiont. The rate was found to not exceed 
0.1 % of the total standing stock of symbiotic algae per day. This rate 
was also less than 4 % of the rate at which cells are added to symbiotic 
populations (Hoegh-Guldberg et al. 1987).

 When this expulsion of zooxanthellae is severe, the colony takes on a
pale white coloration. In partial or incomplete bleaching the colony
takes on a mottled appearance. The very first sign of bleaching can 
be the apearance of an area of lighter and/or mottled coloration.
The area where bleaching occurs and how it spreads to the rest of the
colony varies with species. In the Lasker et al.(1984) scientific
study, _Millepora_ and _Agaricia_ corals first whitened at their tips 
and then the bleached area extended toward the colony base. Some of 
these colonies uniformly paled, but most retained at least some pig-
mented tissue at the base of the colony. Tissue death due to this 
bleaching was most common at the tips of the blades. Massive _Montas-
trea annularis_ colonies bleached first at the base of the colony and 
then the bleaching expanded up the face of the colony. Other species 
became mottled and bleached in a seemingly random pattern. The severity
of the bleaching on a colony did not appear to be affected by colony 
size, with the exception that very small colonies were more likely to 
lose all coloration. Although many species became bleached during 1983 
in Panama, the researchers only found significant mortality among 
_Agaricia_ colonies. They also found some apparently healthy zooxan-
thellae remaining in all but the most severly necrotic colonies 
(Lasker et al. 1984). The duration and scale of the environmental
disturbances also dictates the severity of the bleaching response and 
the ability of the coral to recover its colouration (Japp 1979)
(Glynn 1984).

 Many of the studies involving zooxanthellae expulsion bleaching have 
determined that heated sea water was the most important environmental 
parameter inducing coral bleaching. The exact problems that raised sea 
water temperature caused for the corals have been speculated about for 
quite some time. Mayer (1918) commented that the toxic effect of heat 
might be due to carbonic acid accumulation and pH alteration in tissues.
Yonge and Nichols (1931b) speculated that the lowered metabolism of 
the coral host, caused by stress, reduces the available supply of 
nutrients primarily nitrites, nitrates, phosphates, sulfates and CO2 
for algal symbionts. Muscatine (1971) postulated that the triggering 
mechanism for zooxanthellae expulsion was the decrease in space caused
by atrophied host tissues during heat-salinity stresses that could 
stimulate rejection of symbionts. Stressed corals might also limit
the availability of nutrients thereby starving zooxanthellae. Coles 
(1973) discovered that as temperature went up - respiration increased 
faster than photosynthetic production. This allowed the determination
that some metabolic wastes were not being utilized in the photosynthetic
process of the zooxanthellae.





 The effects of sudden changes in temperature, light and salinity were
researched for the corals _Stylophora pistillata_ and _Seriatopora
hystrix_. Naturally bleached corals from the edge of Lizard Island 
lagoon were found to have decreased populations of zooxanthellae but the
Chl a/zooxanthellae content was not affected. In the laboratory sudden
exposures to full sunlight induced Zooxanthellae Pigmentation Bleaching
(low pigment content) but not Zooxanthellae Expulsion Bleaching. Exposure
to reduced salinities did not cause expulsions but rapid Expulsion
Bleaching occurred when the corals were exposed to sea water temperatures
in excess of 30 degrees C (Hoegh-Guldberg and Smith 1989)


 In captivity, expulsion bleaching is quite common when transporting 
corals held within small water volumes. This author has speculated that
temperature exposure is the most likely cause. After acclimation to 
captive systems, a few corals can sometimes partially bleach or fully 
bleach and this seems to occur at random times, When this bleaching or
lightening in color occurs over a short period of time of less than a
week, the coral was probably exposed to a sudden change in its environ-
ment. Corals will also photoadapt to lighting environments and this
can at times be confused with bleaching but will usually occur slowly
over a period of weeks. Therefore, Zooxanthellae Expulsion Bleaching is 
when the coral is exposed to sudden environmental changes that cause the
symbiotic zooxanthellae to be released or expelled into the surrounding
water. 


  Expulsion Bleaching has also been speculated to be a potential adap-
tive response by the coral animal host to assist repopulation with a 
different algal partner (Buddemeier and Fautin 1993). It appears that 
many different strains, types or species of zooxanthellae inhabit 
hermatypic corals. The evidence for diversity in zooxanthellae is 
summarized in (Buddemeier and Fautin 1993)(Buddemeier 1994). This study
also postulated that a less violent mechanism of loss/regulation induces
the adaptive form of bleaching. Many of the corals that have suffered 
mortality or severe stress due to bleaching were speculated as being 
extreme cases of a pathological form of bleaching.


------------------------------------------------------------------------
 Zooxanthellae Pigmentation Bleaching
------------------------------------------------------------------------

 A typical light spectrum representing irradiance at the waters surface
can be found in figures 3 and 4. As can be seen the amount of blue and
green light remains constant but the intensity of orange and red in the 
visible light part of the spectrum is less than that of blue and green.
Some UV and Infared irradiance travel through the atmosphere and arrive
at sea level. As light travels through water, different wavelengths
(or colors) are filtered at different rates or values. Figure 5 shows
what happens to light as it travels deeper into the sea. At 6 meters
red light is reduced by aproximately a factor of 10. At 20 meters and
deeper very little red light is found. Orange light is also filtered
out. Maximum transmission through seawater occurs at 480 nm.

 The color or quality of the light spectrum that a hermatypic coral 
receives is related to its depth underwater. Symbiotic zooxanthellae
have more than one light collection pigment. Table 1 lists 11 known
light collection pigments found in zooxanthellae. Chlorophyll a and c
are the most abundant pigments and the remaining pigments are comprised
of a collection of different Carotenoids. What complicates our under-
standing is that each pigment has from 1 to usually 3 different absorp-
tion maximas. These are points that are heavily absorbed by the pig-
ment or these maximas are the light best utilized by the structure of
the pigment. An examination of the table highlights the fact that the
fast majority of these maximas are in the blue part of the light spec-
trum with the two Chlorophyll's having some red absorption. Chlorophyll
c also absorbs some yellow. Table 2 lists the carotenoids by percentage
composition found in zooxanthellae.

              Table 1 Extracted from (Jeffrey and Haxo 1968)

              Table 2 extracted from (Jeffrey and Haxo 1968)

 An overall representation for the type of light absorbed by a zooxan-
thellae can be found in figure 6. A large maxima can be seen in blue 
with a smaller more narrower one in red. This curve is heavily affected
by the absorption curve for the Chlorophylls. One would guess that the 
isolated zooxanthellae was receiving sea surface quality light. Re-
searchers prefer to talk about PAR and PUR radiation or light. PAR is
Photosynthetically Available Radiation and this curve ignores UV and
infared light and considers the quality (or spectrum) of light reaching 
a coral. PUR is Photosynthetically Useable Radiation and this curve 
considers the light absorbed by the zooxanthellae in addition to con-
sidering the quality of light on an average sunny day (see figure 7). 
This curve shows that zooxanthellae from shallow waters absorb more 
light energy but this is somewhat compensated for by the increasing 
ability of deeper corals to use more of the light. Coral Zooxanthllae 
Pigments photoadapt or ecomorph into their environment. If light energy
is weak than pigments in the zooxanthellae are increased to compensate 
for the loss in light energy input (Dustan 1982).

------------------------------------------------------------------------
 Temperature Induced Bleaching
------------------------------------------------------------------------


 Numerous studies have determined that sea water temperature is a major 
factor in inducing Zooxanthellae Expulsion Bleaching. Experiments under-
taken on _Aiptasia pulchella_ and the reef coral _Pocillopora dami-
cornis_ were able to induce Zooxanthellae Expulsion Bleaching with cold
and heat stress. Muscatine et al. (1992) found intact expelled host
cells which implicated host cell adhesion dysfunction as the cause.
Cress et al. (1990) discovered that heat shock inhibited the ability of
cells to initiate and complete attachment onto new tissue culture sur-
face. The phase behavior of lipids and proteins comprising the host
biological membrane has been speculated as causing cell adhesion dys-
function (Quinn 1989). Gates et al. (1992) verified the discoveries of 
Muscatine et al. (1992) and also speculated that low salinity might 
cause Zooxanthellae Expulsion due to the mechanical disruption caused 
by hypoosmotic shock.


 Sea water cold shock caused 11 species of scleractinian corals in 
Hawaii to Zooxanthellae Expulsion Bleach. A 4 hour cold shock between
12 and 18 degrees C. In the laboratory a 4 hour cold shock at 4 degrees
C induced a 50 % Zooxanthellae Expulsion (Muscatine et al. 1991). In the
Southern Caribbean _Agaricia agaricites_ experienced ring bleaching 
during rapid water cooling. The bleached areas were composed of circular
ringed shapes (Kobluk and Lysenko 1994).

 
------------------------------------------------------------------------
 UV Induced Bleaching
------------------------------------------------------------------------


 The subject of Zooxanthellae UV Irradiance Expulsion Bleaching has been
researched by scientist recently and has been the source of much contro-
versy in discussions amongst captive aquarist. In this section I will 
attempt to summarize the scientific research performed and also report 
on suspected bleaching in captivity attributed to UV Irradiance and 
postulate on the validity of captive studies to date. The typical light
spectrum that reaches the ocean surface, (figures 3 and 4), can be ex-
amined for natural UV levels. This UV irradiance is lower than 400 nm in
wavelength. Hoegh-Guldberg (1989) did note that the evidence done in
earlier studies that suggested UV induced Expulsion Bleaching (Fisk and
Done 1985)(Harriot 1985)(Oliver 1985)(Goenaga et al. 1988) were based
on circumstantial evidence. These observations were based on (1) periods
of low turbidity and calm seas caused increased solar irradiance that
preceded some bleaching events; (2) corals tend to bleach on their
upper most sunlit surfaces first (Hoegh-Guldberg 1989).

 UV light is basically composed of three different regions (see figure
8). UV-A has a lower wavelength limit of 320 nm and upper limit at the
beginning of the visible light part of the spectrum at 400 nm. This is
the less harmful of the three regions of UV. UV-B is defined as the 
narrow band from 280 nm to 320 nm. This is the UV that has been shown 
to have an affect on DNA. The level of UV-B light that corals receive
in nature varies due to cloud patterns and ozone layer thickness. UV-C 
is the UV region that is below 280 nm and normally this light never 
reaches sea level and therefore corals have evolved no natural defense 
against its affects. Another definition of UV light is Middle UV or MUV 
that has a lower wavelength limit of 280 nm (same as UV-B) and the upper
limit is 340 nm (Baker et al. 1980). This MUV is more applicable to the 
affects caused by UV on hermatypic stony corals and the corals response 
to UV exposure will be examined later in this section. In figure 9 the
amount of predicted downwelling spectral MUV irradiance varies at the 
surface of the ocean at equatorial latitudes due to wavelength varia-
tions, solar zenith angle, ozone thickness, aerosol thickness and 
surface albedo. As is shown in the figure less than 10 % of the UV-B 
irradiance in the 295 nm to 305 nm wavelengths reaches the ocean surface 
at the latitude of 20 degrees. More than 50 % of the UV-A (>320 nm 
wavelengths) reaches the same area and no UV-B or UV-C in the wave-
lengths less than 295 nm arrives at the ocean surface at 20 degrees 
latitude. Massive coral reef development occurs between the latitudes 
of 30 degrees north and south due to sea water temperatures (Allen and 
Steene 1994).

 Another factor affecting the intensity of UV-B and UV-A irradiance 
reaching the ocean surface is the changing sun altitude in the daylight
sky. The visible wavelength range from 400 nm to 700 nm is called PAR
or Photosynthetically Available Radiation and the irradiance intensity
for PAR increase and decreases in a curve similar to the curve repre-
senting the rising and falling sun altitude (see figure 10). The curve
for UV-B (280-320 nm) has a steeper upward and downward slope and the
resulting irradiance intensity peaks more sharply than PAR. The curve
for UV-A and UV-B combined has slopes that are in between PAR and UV-B 
alone. This results in a shorter duration of exposure to 50 % or greater
intensity of UV-B than the exposure to 50 % or greater than PAR. So 
corals are experiencing drastic daily rhythmic variations in UV-B 
irradiance.

 Light reaching the oceans surface is also furthur affected by attenua-
tion when traveling through the water column over the reef. In figure
11 the typical attenuation coefficients for downward irradiance are
shown for two types of ocean water. One is typical for clear open ocean 
waters where productivity is low. The other curve is for moderately
productive waters with a relatively high concentration of dissolved
organics. This author believes that captive system water exhibits an
attenuation coefficient similar to the curve for moderately productive
waters with some organics. Some aquarist have reported coral bleaching
that occurred when carbon was used to filter out dissolved organics.
These reports have been limited to a few instances and the justifica-
tion for using the carbon in the first place have not been clearly
stated. A typical stony coral reef aquarist only uses carbon occasion-
ally and many times the use is stimulated due to some perceived down-
ward trend in the health of the captive system. The very shallow water
depth found in typical captive systems, makes attentuation by water 
much less of a factor than natural reefs but the degree of light inten-
sity changes (due to the inverse square law and reef structure shading)
under captive lights can drastically alter the energy over the entire 
spectrum when repositioning corals in captivity. If dissolved organic 
levels were attenuating the light spectrum strongly in captive systems,
the potential that protein skimmer (foam fractionator) efficiency could 
stimulate coral bleaching should have become apparent by now. The 
possibility of trace element depletion, potential leaching of compounds 
and the addition of carbon dust to the captive system are all possible 
explanations and further applied research needs to be undertaken in this 
area.

 Corals located at different water depths are exposed to light of dras-
tically different wavelength characteristics. The visible and UV light
absorption spectra for _Acropora formosa_ is shown in figure 12 for
three different natural depths. The spectra for 1 meter depth shows a
large absorption in the UV-B area termed S-320. This area is due to 3
protective UV absorbing agents found to exist in hermatypic corals. As
the depth increases the amount of irradiance absorbed decreases as one
would expect due to the waters attenuation coefficient and the resulting
weaker amount of UV-B light at depths. The PAR area of the spectrum
(400-700 nm) shows a dramatic increase in absorption due to the adapta-
tion that occurs which allows the zooxanthellae to use more of the 
available light.

 The UV-B absorbing agents that comprise S-320 are mycosporine-Gly 
(absorption maxima 310 nm), palythine (absorption maxima 320 nm) and 
palythinol (absorption maxima 332 nm) (Dunlap and Chalker 1986). Their 
absorption spectra (figure 13) do partially overlap and together com-
prise a broad-band filter that absorbs and blocks MUV from 285 nm to 
350 nm. These absorbing agents are mycosporine amino acids (MAA's) and 
were first discovered as UV absorbing metabolites in 1965. Their con-
centrations do decrease in corals found in deeper reef locations 
(figure 14) but remain at a constant level from 20 meters on down to 
45 meters (Dunlap et al. 1988). Antarctic marine organisms were 
studied for the existence of MAA's and a total of 8 different types
were found (table 3). Similar but unidentified UV absorbing com-
pounds have also been found in the mucus of _Fungia fungites_. A study
exposed the solitary corals to air, which promoted the generation of
mucus, and found a peak UV absorption of 332 nm (Drollet et al. 1993). 

     Table 3 Extracted from (Karentz et. al. 1991)(Dunlop et. al. 1986)

 A field experiment (Gleason and Wellington 1993) was performed based 
on the previous anectodal evidence suggesting a link between UV and
Zooxanthellae Expulsion Bleaching. At the Bahamas the common reef
building species _Montastrea annularis_ was transplanted from 24 meter
depth to 18 and 12 meters. An acrylic cover that was transparent to
irradiance at or above 405 nm, allowed ~ 50 % of 400 nm irradiance
through and blocked all UV irradiance at 385 nm and lower was utilized
to remove UV from some transplanted corals. Corals moved to 12 m began
to show signs of Expulsion Bleaching at 7 days and were visibly more 
pale 21 days after transplantation. UV-B irradiance in the range 300-
320 nm was monitored at the various depths used in the experiment. It 
was assumed that UV-B in the 280-300 nm range was not a factor due to 
the northern tropical latitude and high attenuation coefficient for 
those wavelengths in water. This study determined that the UV-B inten-
sity during the time of the experiment was 6.4 times as intense at 
12 m than it was at 24 m, while at 18 m it was only 2.4 times as in-
tense. Since corals only showed signs of bleaching at 12 m after 7 
days and did not bleach at 18 m, it can be assumed that UV-B intensi-
ties need to be ~ 6.4 times as intense as normal for UV-B induced 
bleaching to occur. This may be very difficult to achieve in a shallow 
captive reef system. UV-A was 2 times as intense at 12 m than it was 
at 24 m, while at 18 m it was only 1.3 times as intense. Zooxanthellae 
Pigmentation Bleaching was not observed and that seems odd since trans-
planting a coral from 24 m to 12 m should have induced some degree of 
photoadaptation. Additionally, coral UV-A Pigmentation was not analyzed
during this field study. The observed UV levels were compared to 
average UV values during the peak time of year which happened to be
higher than those measured during the experiment. The result of that
comparison was that only a 3.2 times increase in UV-B induced bleach-
ing. This 3.2 value was based on normal values and not those that 
actually occured during the experiment which resulted in a 6.4 times 
increase in UV-B. The author did speculate that any increase in UV-B 
that might have induced Expulsion Bleaching in the Caribbean is pro-
bably not due to ozone layer thinning because of its normally minimal 
thickness at the low latitudes. They speculated that calm weather con-
ditions and exceptionally clear water were to blame (Gleason and 
Wellington 1993).





 



 We know how these hermatypic corals shield themselves from UV-B and 
we also know that in nature UV-C never reaches sea level. Unnatural or
man made lights can emit UV-A and UV-B and have a slight potential to
emit some UV-C. Typical metal halide lamps that have a quartz outer 
envelope do cut off 50 % of the UV-C light emited at 200 nm but are
transparent to UV light greater than 300 nm. This author has just
recently seen a preliminary UV spectral density chart for a typical 
10,000 K metal halide lamp. The UV-A, UV-B and PAR emissions were very
similar to that which occurs on a typical coral reef. There was some
UV-C light that was very low from 240 to 280 nm (quartz transmits 75 %
of this UV). This irradiance level appeared to be low enough to not
be much of a concern, however there was a sharp increase in UV-C at
around 200 nm that was sharply cutoff at ~190 nm due to the decreased
transmission capability of quartz bulb in that area. The source of this
SPD data has not been verified but the emission of some low wavelength
UV-C is theoretically possible and the use of a UV blocking material 
that prevents light in the UV-C range from transmitting might be appli-
cable to captive systems but this author has yet to verify any UV 
related bleaching events in his own captive systems. UV light in this 
wavelength never reaches sea level and is actually the UV light that 
combines with oxygen to form ozone in the stratosphere. The affects 
that this kind of light would have on captive corals is completely 
unpredictable due to a lack of scientific research concerned with UV-C
irradiance since it never reaches the ground.



 The authors current theory with respect to keeping these animals in
captivity is to only reproduce the natural environmental conditions 
that these animals normally receive that are not detrimental to their 
life history in captivity. A shallow water reef in nature receives no 
UV-C but does receive UV-B and UV-A. Corals that are found in deep or
turbid water that is low in UV-B irradiance, will lower their S-320 
absorption concentration and if kept in captivity under similar con-
ditions, might become more prone to UV-B damage when relocated to a
different captive light environment. Since a minimum concentration
of MAA's is kept even in deep water corals (figure 14), captive 
corals should probably be maintained with minimal or no UV-B. If the
captive animal was ever moved back into nature or relocated to a 
different captive reef with intense UV-B irradiance, a reacclimation 
period would be required to allow for the increase in S-320 MAA con-
centrations. If the captive reef engineer was installing a UV shield
to block any potential UV-C emission near the quartz glass cutoff
area (~200 nm), a shield that also blocks any MUV (280-340 nm) could
be used. The author believes that the typical UV-B from metal halides
is low enough to not be too concerned. 



 That brings us to the topic of UV-A wavelengths. In nature, shallow 
water reefs receive a substantial amount of UV-A. While MUV can cause 
DNA damage in wavelengths up to 340 nm, UV-A only appears to affect 
the photoinhibition of photosynthesis (Cullen and Neale 1994). Photo-
inhibition refers to a reduction in photosynthetic capacity and can be
caused by damage due to wavelengths in the UV range, by light in the 
visible part of the spectrum and by interactions between UV light and 
visible light (Powles 1984). The symbiosis of coral animal and plant 
does allow some adaptation to the changing environment that may have 
induced photoinhibition of the symbiont algae. The algae themselves can 
reactivate UV DNA damage to the photosynthesis centers during the night
or when UV is not present, change their concentration of S-320 MAA's 
and they can also change light collection pigment sizes to decrease the
amount of irradiance absorbed. The coral animal might also have the 
ability to expel algae that are photoinhibited and not producing 
carbon. Add these adaption capabilities to the complex interactions 
between UV-B, UV-A, MUV and PAR light and the difficulty in separating 
them into well defined wavelengths (as described in Middleton and 
Teramura 1994) and a common inability to demonstrate repeatable 
exposure-dependent response becomes apparent.

 The coral animal also has the ability to create UV-A reflecting and 
fluoresceing pigmentation that can also make researching the affects that
UV-A has on photoinhibition difficult. In addition, some scientist have
speculated that these reflecting and fluoresceing pigments might actually
be modifying the spectrum of UV-A light into a wavelength that is 
absorbed via photosynthesis in the symbiont plant algae (Kawaguti 1969)
(Schlichter et al. 1985)(Schlichter et al. 1986). They have been a few
studies undertaken that examined these UV-A pigments but most of the 
research to date has concerned UV-B absorbing substances due to the DNA
damaging affects of exposure to UV-B. Catala-Stucki (1959) found green,
orange, silver-blue, beige, brown and grey fluorescence when corals held
in captivity were exposed to UV light. Kawaguti (1969) found a green
fluorescent pigment in reef corals. Shibata (1969) found red, pink, 
muave, violet and yellow pigmentation in addition to the S-320 absorp-
tion substances. In the Caribbean some UV excitation fluorescence was 
found in certain species but all emitted green colored light (Logan
et al. 1990). A recent study (Mazel 1995) found fluorescence emission
in quite a few colors (figures 15 and 16). In Image 22 a purple _Acro-
pora austera_ ? with intense UV-A pigments can be seen. Intense blue
pigments can be seen in the _Acropora millepora_ in Image 21. New growth 
areas will lack zooxanthellae and have intense UV-A pigments as can be
seen in Image 23. 

 The exact role that these pigments have in the symbiosis has not been
determined to date. While studying these corals in captivity the author
has noted that when not exposed to UV-A, these fluorescent pigments fade
very quickly. They also fade whenever the colony is stressed. From 1991
to 1994 captive reefs maintained by this author have been illuminated
with metal halide lamps (5500 K to 6500 K) in conjunction with Phillips
Actinic 03 fluorescent bulbs. The intensity of the corals UV pigmenta-
tion would always fade whenever the actinic bulbs attained 4 months of 
operation. The bulbs were also visibly weaker in intensity. Upon replac-
ing these old and weak bulbs with new ones, the UV pigments would in-
crease intensity for at least a period of a month and then level off. 
Mazel (1995) found that excitation wavelengths of 365 nm or 405 nm 
induced fluorescence. Kawaguti (1969) found that green fluorescence was 
excited by UV-A light at 380 nm. Earlier this year some new bluer metal 
halides became available to captive reef system aquarist. These bluer 
bulbs do emit a larger quantity of mid to upper UV-A light and they have 
been maintaining or increasing the fluorescent UV-A pigmentation in many
corals from Fiji and Jakarta. The corals from Jakarta that are import-
ed generally lack these colorful pigments but will eventually UV Pig-
mentation Color (intensify their UV pigments). Scientist have studied
the Jakarta area and have noted the increasing siltation and urban
pollution (Robinson et al. 1981)(Moll and Suharsono 1986)(Purwanto 1987)
(Sukarno 1987). Fiji corals from shallow water are initially intensely
colored with UV fluorecence and reflectance pigmentation. This author 
has also noticed that some Coral UV Pigmentation intensity appears to 
increase during the photoperiod and reaches a maximum intensity by
early evening. This has occurred in a captive reef system that utilizes
3-175 watt metal halides for a normal daytime photoperiod and has 2-400
watt metal halides for the midday photoperiod.




 A study undertaken on a symbiotic coral found at an extraordinary depth
range in the Red Sea, hypothesized that the coral animal might be pro-
viding the symbiont with additional light. They speculated that host 
pigments may be transforming light of short wavelengths (UV-A 380-400 
nm) into wavelengths suitable for photosynthesis (Schlichter et al. 
1986). The same researchers found a similar pigment system in the deep-
water hermatypic coral _Leptoseris fragilis_. It was speculated that 
host pigments may transform the violet portion of the incident light 
into longer wavelengths. thus increasing the photosynthetic efficiency 
of the zooxanthellae (Schlichter et al. 1985).






 The author believes that the reflecting pigments can be identified by
their ability to change apearence depending on the color of light that
is illuminating the coral. For example, many blue appearing acropora
appear pink when illuminated with red/yellow irradiance that a typical
flashlight gives off. The fluoresing pigments may lack this ability
and always fluoresce a specific color when excited by a certain irra-
diance wavelength in the mid to upper UV-A range. One may ask why corals
would be reflecting or fluorescing this upper UV light into light 
usable to photosynthesis. Why not just absorb the upper UV-A and adapt
to the existing PAR light? It is possibly that reflected or fluoresced
light might offer advantages to direct solar light. The angle of re-
flection or fluorescing might allow the light to travel to surfaces
of the colony not receiving direct solar illumination. Many times in
captivity corals have photoadapted to the non-moving man made light
sources and have distinctly darker undersides. The different effects
of UV-A and UV-B light are illustrated in figure 17. DNA damage is
stopped at ~ 340 nm but some other studies noted that unshielded DNA
can be damaged by light up to 360 nm. The author recommends exposing
the corals to upper UV-A due to the previous mentioned reasons but not
exposing the coral to UV-B or lower UV-A.

------------------------------------------------------------------------
 Synergistic Environmental Parameters that Induce Bleaching
------------------------------------------------------------------------


 The synergistic (or combined) effects of irradiance, ultraviolet radia-
tion (UV-A and UV-B) and tempertaure on the activities of protective
enzymes against active oxygen were studied in Lesser et al. (1990).
It was speculated that exposure to high irradiance and UV combined with
the additional exposure to sublethal temperature perturbations could
result in photoinhibition and irreversible injury to the photosynthetic
apparatus of zooxanthellae. Photoinhibition occurs at high temperatures
as a result of reduction in photosynthetic electron transport (Osmond 
1981). Reduced electron transport, combined with the continued absorp-
tion of excitation energy in the presence of molecular oxygen, will lead
to the production of active oxygen species for which many components
of the photosynthetic apparatus are targets (Allen 1977)(Asada and 
Takahashi 1987). Lesser and Shick (1989) suggested that oxygen toxicity
is a physiological stress that could mediate the expulsion of zooxan-
thellae. In Lesser et al. (1990), they reached the conclusion that Zoo-
xanthellae Expulsion Bleaching occurred with increasing temperature 
combined with UV exposure and did not occur with increasing PAR irra-
diance combined with increasing temperature. After examining this study,
it appears that increasing irradiance actually refers to High Light 
which was equivalent to the light the corals had received originally in 
nature. That might explain why no expulsion was observed with the same 
high irradiance the corals had originally received. Expulsion did occur
due to increasing temperature. Another factor that was not considered 
was Coral UV-A Pigmentation levels and how they were affected by trans-
porting the corals from nature to the captive study. The author has seen
numerous Coral UV-A Pigmentation Bleaching events occur when corals are 
moved or stressed. The study did examine the UV-B absorption substance
levels S-320. It is also possible that the UV-A Pigmentation was reduced
by the high temperature stress that was induced in the study. Either of 
these events could have induced the corals Zooxanthelale Expulsion 
Bleaching under high temperature and high UV but not high temperature 
and high PAR irradiance. Which led the researchers to conclude that 
although they currently lack direct measurements of active forms of 
oxygen, their experimental results are consistent with the proposition
that the production of active forms of oxygen is significantly affected 
by temperature and may be an important factor mediating recent bleaching
events (Lesser et al. 1990).


========================================================================
 Coral Photoadaptation in Captivity
========================================================================

------------------------------------------------------------------------
 Photoadaptation and Ecomorphology in Captivity
------------------------------------------------------------------------




  If Scleractinian Stony corals are positioned in an captive environment
where water current, light intensity, light spectrum and water tempera-
ture are identical to those that the coral experienced on the natural
reef, natural growth rates will occur as soon as the coral recovers from 
transportation stress. It is very rare for this to occur but it occa-
sionally will. What usually happens is that one of the before mentioned 
parameters will be different and the coral must not only recover from 
transportation stress and become acclimated to the new environment, but 
also ecomorph or physically adapt. The coral pigments and zooxanthellae 
pigments can successfully adapt to this new environment if the differ-
ence is not too great and the transportation stress was minimal.

 Zooxanthellae pigments can photoadapt to a light environment. In cap-
tive systems with non-moving light sources, self shading can become a 
problem. Image 28 is a white _Stylophora pistillata_ that was recently 
imported. After being in a captive reef for a month, the undersides
of the coral that were receiving less light, darkened as Image 29 shows.
The author speculates that either zooxanthellae pigments increased in
size or the symbiotic population increased. Sometimes corals in cap-
tivity can bleach the opposite way. Image 24 illustrates Zooxanthellae
Expulsion that had occurred in the low light areas of the colony.

 An unplanned experiment occurred in the authors tranship and fragment
grow-out reef. Two juvenile _Pocillopora damicornis_ corals that had
settled on the upper side glass wall of the reef, had to be removed
due to coralline algae flaking. There were mounted to glass microscope
slides via epoxy putty as shown in Image 25. A closeup of one of the
coral spats (Image 26) displays a large population of zooxanthellae
(brown dots in coral polyps). After being relocated to a much more 
intense light field, the spat lightened in color considerably. Image
27 is an extreme closeup that appears to not have photocopied well
but the original clearly displays a lowered zooxanthellae density.
the difference in light environments was measured with a LUX meter
and the stronger light environment was greater by a factor of 4. It
should also be noted that coral species vary in their ability to
adapt to environmental changes.

 When growth occurs, the new areas may take on a different form. Thick 
branched corals prefer stronger currents and if they are placed in weaker 
water flows, new growth on the branch ends will be thinner. Thin branch-
ed coral colonies prefer weaker currents and new growth will be thicker 
if the current is too strong. Buddemeier (1994) noted that the shallow 
reef region is a very high energy region. In fact, it may be nearly 
impossible for captive system engineers to provide the same water 
movement energy without blowing out a tank wall or tipping the reef over.
We can partially simulate this region with random timers, underwater 
powerheads and even the new rotating powerheads. A dump bucket can also 
be utilized to create wave rhythms. Almost all Scleractinian stony 
corals will do better in a moderate varying water current that carries 
waste products away and helps respiration. Some thinly branched delicate 
species might prefer weaker currents. The water flow can also assist the 
coral colony in preventing a buildup of particulate matter in the lower 
regions of the colony. This author will occasionally assist large 
colonies by sending short bursts of current into areas where particulate
matter has collected.

 
 How do you know (before the coral has grown into its captive environ-
ment) that the water current is the correct magnitude for each coral? 
The polyp extension rate seems to be a good indicator. If the coral is 
heavily stressed in its environment, the individual polyps will not 
extend at night for feeding. If slightly stressed, the polyps will stay 
in during the day and partially extend at night. When the environment 
is not stressing the coral, full polyp extension will occur during the 
night and partial polyp extension will occur during the day. What makes 
this difficult to use as a coral vitality indicator, is that each 
species and ecomorph has different lengths considered partial extension. 
For example, Acropora millepora (Image 21) has polyps nearly fully 
extended during the day. Once you learn how each species behaves, this 
indicator can work very well. In fact, the healthier the coral gets the 
greater the polyp extension will occur during the day.

 These corals might be extending their polyps during the day to pri-
marily assist photosynthesis since zooxanthellae inhabit their ten-
tacles, and during the night to feed on plankton. You can add newly 
hatched brine shrimp at night for the extremelly small polyped corals 
(_Pocillopora_, _Porites_), etc.) and adult brine shrimp for the larger
polyped acropora. It is best to add the shrimp a couple of hours after 
the twilight light has ended when full tentacle extension occurs. These 
polyps are able to eat items much larger then themselves. Some reef-
keepers have speculated that calcium can be transferred to the coral 
via a live food that might contain calcium in its structure. A coral 
food paste can be created from shrimp, clam, scallop and crab meat 
purchased from a local grocery store. Add a product containing fatty 
acids and spray the food over a colony with extended tentacles. This 
could greatly enhance vitality and growth.


========================================================================
 Future Research
========================================================================


 Collecting applied research on corals in captivity, is somewhat similar
to researching isolated coral reefs in nature. The nature and status of
natural biological communities at any particular location and time may 
reflect regional or local characteristics, including consequences of 
human activities (e.g. change of sediment or nutrient discharge into 
reef waters). Many academic inferences about reef processes rely on 
isolated (in space and time) collections or observations which need to 
be interpreted against the background of natural variability of the 
physical environment. Information about many physical variables impor-
tant to reef ecology is not, however, readily accessible to coral reef 
researchers (Lough 1994). This same problem with the variability of 
physical parameters also affects collecting data from various separate 
captive systems.


 One area that could use further investigation from applied researchers
is Coral UV-A Pigments. Determining how to identify reflecting pigments
from fluorescing pigments and how to stimulate the production of either
is an interesting topic. The author currently believes that the typical
fluorescent green stimulated by ~385 nm is a common fluorescent pig-
ment in many corals. _Acropora loripes_ in some captive systems have
slowly changed from bright blue to actinic green. How to stimulate
the production of reflecting pigments could open up a rainbow of colors
and allow captive systems to preserve the coloration of corals from
very clear and shallow reefs such as Fiji.

 As more and more fragments are made by captive coral reef farmers
the art and science of fragmentation could eventually become rather 
extensive. For example, Image 30 is of three _Acropora sp._ table 
fragments that were raffled away at Macna VI in Cleveland. Staghorn 
corals seem to need a minimum size before asexually produced fragments 
survive. Recently, a _Pocillopora sp._ (probably woodjensi) imported
from Fiji has demonstrated an ability to encrust very quickly. This
is unusual for a _Pocillopora sp._. The ability to encrust greatly 
enhances the survivability and production rate for fragments. The
author has noted that many species do not fragment well and/or need
special care in handling. Some of the more delicate corals just
barely survive importation but improving techniques are advancing
the science of coral transportation.

 
 Stimulating natural growth rates brings a whole host of long term
problems for corals in captivity. As these corals begin growing into
each other frequent pruning might be necessary. Keeping a data
base of corals that are compatable enough to grow next to and into
each other would be a valuable tool in the future. The area of coral
sexual reproduction contains numerous opportunities for captive
data collection.  





========================================================================
 Errata
========================================================================


 To say this paper was completed in panic mode would be an understate-
ment. It is highly possibly that errors have found their way into this
manuscript. Additionally, this paper could be redone in the future with 
new applied research data or new scientific findings. Scientific papers
on photoadaptation in nature could be integrated more completely. The
Breeder's Registry (Stanley Brown) has agreed to be an informational ex-
change between the author and the readers of this paper. Anyone reading
this is encouraged to submit corrections, comments, additional datum or
copies of hard to find references to The Breeder's Registry. Stanley 
will relay the request and/or information to the author.

  The Breeder's Registry
  P.O. Box 255373
  Sacramento, Ca. 95865-5373 


========================================================================
 Acknowledgements
========================================================================


 Most of the scientific references used in this paper were obtained from 
the UCLA Biomedical Library. Thanks to Paul Miller of Alt Systems for 
the presentation slide graphics, chart scanning and printing. Additional 
thanks to Les Dittert of Alt Systems for scanning 35 mm images and 
printing the originals used for the color photographs included with this
paper. Special thanks to Kevin Gaines for the photo of the Solomons 
_Acropora austera_ ? that highlights the UV pigmentation. A cordial
thank you to the Macare family at H2O Tropicals for assisting with
the measurement of lux values in the authors reefs and for providing
a spectral chart for the 20,000 K metal halides from Germany. A special
thanks to Perry Tishgart of Champion Lighting for providing a spectral
chart of the 175 watt 10,000 K bulbs from Corallife. A friendly thank
you to Dustin and Teresa for providing quartz UV filtering charts. A 
final thanks to Greg Meeker for keeping an eye on the authors captive 
reefs while presenting this paper to Macna VII.


========================================================================
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  Spec. Publi., Bogor 29:111-121

Trench, R.K., 1979. The Cell Biology of Plant-Animal Synbiosis. Ann. 
  Rev. Plant. Physiol. 30:485-531

*Vaughan, T.W., 1911. Recent Madreporaria of southern Florida. Carnegie
  Inst. Washington Year Book 8:135-144.

*Vaughan, T.W., 1914. Reef corals of the Bahamas and of southern   
  Florida. Carnegie Inst. Washington Yearb., No. 13:222-226

*Yonge, C.M., and A.G. Nicholls. 1931a. Studies on the physiology of 
  corals. IV. The structure, distribution and physiology of the zooxan-
  thellae. Sci. Rep. Great Barrier Reef Exped. 1928-1929 1:135-176

*Yonge, C.M., and A.G. Nicholls. 1931b. Studies on the physiology of 
  corals. V. The effect of starvation in light and in darkness on the
  relationship between corals and zooxanthellae. Sci. Rep. Great Barrier
  Reef Exped. 1928-1929 1:177-211

Symbol Definition * = Papers that the author has not acquired complete
                     printings of. The author has complete printings
                     of any paper not marked with an *. Anyone who has
                     printings of the * papers, please contact the 
                     author via the errata section.
                            
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 Using this paper as a reference
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Tyree, S. 1995. Scleractinian Corals in Nature and Captivity. Part I -
  Coral Bleaching and Photoadaptation Dynamics in Nature and Captivity
  including a Recent Captive System Description. Unpublished report pre- 
  sented at the Marine Aquarium Conference of North America [MACNA VII],
  Sept. 17th-19th, 1995 in Louisville, Kentucky.

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