aULLETIN
OF MARINE
SCIENCE.
29(1):
79-95. ]979
CORAL REEF
PAPER
DISTRIBUTION OF ZOOXANTHELLAE AND PHOTOSYNTHETIC
CHLOROPLAST PIGMENTS OF THE REEF-BUILDING CORAL
MONTASTREA ANNULARIS ELLIS AND SOLANDER IN
RELATION TO DEPTH ON A WEST INDIAN CORAL REEF
Phillip Dustan
ABSTRACT
Studies on the distribution and photosynthetic chloroplast pigments of symbiotic zooxanthellae in the reef-building coral MOil/as/rea allllularis Ellis and Solander strongly
suggest that photoadaptation
to decreasing light intensity occurs within a population
inhabiting the fore-reef of a West Indian (Jamaican) coral reef. It is suggested that the
photoadaptation allows for the extension of the depth range of the species.
The responses of M. allllularis and its zooxanthellae to transplantation
suggest that
colonies have a certain capacity for modification when placed at different depths. The
magnitude of these potential changes is small and colonies do not fare well in the transplant habitats. Such sub-optimal conditions are reflected in a decrease in algal density!
Col' living coral tissue, a decrease in zooxanthellar
intracellular photosynthetic pigment
concentration,
and significant decreases in coral skeletal extension rates. Responses
such as these are reasonably clear data in support of ecotypic variation and suggest
that there are sun and shade populations of zooxanthellae in M. allllularis.
maintenance of hermatypic coral colonies
(Wells, 1957).
Reef-building corals primarily live between the ocean's surface and 100 m and are,
therefore, subject to a photic environment
in which there is considerable variation in
both intensity and spectral quality (Jerlov,
1970) . While individual "adult" colonies
are sessile throughout their lives, members
of the same species may inhabit depth
ranges as great as 95 m (Goreau and Wells,
1967) suggesting that the zooxanthellae
within the same species of coral are able to
photosynthesize over a tremendous range of
light intensities and spectral qualities.
Corals that enjoy large vertical depth
distributions exhibit the general, though not
universal, trend of skeletal flattening with
increasing depth and/or in shaded habitats
(Kawaguti, 1937; Goreau, 1963).
The
limits of this general trend are a sphere and
flat plate (Barnes, 1973). This change in
skeletal morphology seems to be the result
of a decreasing calcium carbonate deposition
rate as a direct consequence of decrcasing
zooxanthellar photosynthetic activity (Gor-
Hermatypic scleractinian corals are responsible for the construction of modern
reefs. They provide the framework and a
good deal of the infilling sediments that
form the basic wave-resistant structure
known as a coral reef. It is believed that
the remarkable ecological role played by
hermatypic corals is due to the evolution of
the symbiotic relationship these coelenterates
have with dinoflagellates, commonly referred to as zooxanthellae (Yonge, 1973).
The processes of calcification and zooxanthcllar photosynthesis have been linked to
cnablc corals to deposit skeletal calcium
carbonatc fastcr than environmental erosion
(Goreau and Goreau, 1973). The net resuit is the construction of a geological structure at a rate so fast that it can be measured
within thc lifetime of a human (Land, 1974;
Gorcau and Land, 1974).
The ecological importance of zooxanthcllac is demonstrated by the observation
that thc lower depth distribution of hermatypic corals is above the lower limit of the
photic zone, suggesting that light is of primary importance for the growth and
79
80
BULLETIN OF MARINE SCIENCE, VOL 29, NO. I, 1979
eau, 1959a). The addition and subsequent
growth of new polyps on a sphere requires
an increase in the volume of a colony, which
requires more calcium carbonate per polyp
than does growth as a flat plate with new
polyp addition and most skeletal growth
taking place at the edges (Goreau, 1959a;
Barnes, 1973; Dustan, 1975a).
It is believed that all zooxanthellae from
hermatypic corals are the same species,
Gymnodinium microadriadicum Freudenthal
(Taylor, 1969). However, Trench has
demonstrated that the photosynthetic products of zooxanthellae are different in the
sea anemone Anthopleura elegantissma
Brant and the zooanthid Palythoa townsleyi
Walsh and Bowers, and that each animal
harbors a specific symbiont (Trench, 1971).
Evidence of physiological variability with respect to photoadaptation has been presented
by Lang (1973) and supported by in vIvo
studies (Wethy and Porter, 1976, DavIes,
1977). Soluble protein differences between
zooxanthellae from different species of hermatypic coral and other coelenterates have
been found using electrophoresis (Schoenberg, 1975). It is conceivable that variation
among the zooxanthellae could lead to some
of the differences in skeletal morphology
and behavior that have been used as criteria
for distinguishing "species" of coral (Goreau, 1969; Lang, 1973; Wells, 1973).
Thus, to begin to understand the variation
displayed by reef coral populations, knowledge of the adaptations of zooxanthellae
and the host animal to their respective environments is needed. As selection pressures
change with habitat differences, parameters
giving insight into the adaptations need to
be examined over the habitat range of the
species under scrutiny. Such a study was
undertaken
of the reef-building coral
Montastrea annularis Ellis and Solander and
its symbiotic zooxanthellae over the species
"depth range."
Description of Study Area
The study area was Dancing Lady Reef,
Discovery Bay, Jamaica, West Indies. This
o
55
50
E
45
S
~ 40
(f)
>- 35
z
C
0
6
30
0
u
w 25
(9
«
0
0: 20
w
>
«
15
I
to
~9
I
20
30
DEPTH (m)
I
I
40
50
Figure 1. Jepth distribution of mean colony size
of M. alllwiaris on Dancing Lady Reef, Jamaica.
Each point represents data from a single line transect run parallel to the reef flat across Dancing
Lady Reef. Transect length varied between 23 and
93 m corresponding to the width of the reef. See
Dustan (1975a) for details of methodology.
reef is part of the vast north coast fringing
reef system first described in detail by
Goreau 11959b), and later by Kinzic
(1973) a ld Goreau and Goreau (1973).
It runs al[1ost the whole length of the northern coast of Jamaica with few gaps except
for harbOl's and river mouths. Montastrea
annularis iVaschosen for the study as it is
abundant wer a wide depth range-greater
than 50 ill (Goreau and Wells, 1967; Dustan, 1975a) and is a primary frameworkbuilding oral on most West Indian reefs
(Goreau, 959b; Goreau and Land, 1974).
On DanciIlg Lady Reef M. annularis has a
bimodal depth distribution with peaks in
abundance at 10 and 30 m (Dustan, 1975a).
The specie, exhibits changes in growth form
that are correlated with its habitat (Gareau,
1959a; Milliman, 1969; MacIntyre and
Smith, 1973; Barnes, 1973). The 10-m
peak is comprised mostly of round colonies.
At 30 m and below most of the colonies
assume a flattened form (Barnes, 1973;
Dustan, 1~'75a; 1975b). The distribution
of mean colony size parallels abundance
MATSUI
AND
with the largest colonies occurrmg
ROSENBLATT:
at 8 and
35 ill (Fig. 1).
NEW
SEARSID
lated and converted
surface area.
II/tracellular
MATERIALS
AND METHODS
concerning the distribution of photosynthetic pigments in
the zooxanthellae population of MOlltastrea all1IIII1Iris was gathered during the months of September 1972 through February 1973, during SCUBA
excursions to the study area on Dancing Lady
Reef. Samples of coral colonies were collected
with hammer and chisel and brought to the surface
in individual plastic bags. Once on board the dive
boat, they were placed in a shaded container. Upon
arrival at the laboratory the corals were maintained
in the indoor running seawater aquarium. Samples
were processed within 4 h of collection, usually
within 2 h.
Samplillg of coral colollies.-Tnformation
Dellsity of polyps/cm'.-The
density of polyps/cm'
was determined by photography of colonies in sitlt
on Dancing Lady Reef, Bouy Reef, and Pinnacle
I (all outer reefs within the Discovery Bay area).
A close-up tube with framer attached to a Nikonos
camera was used to photograph an unshaded flat
30 cm' area of each colony. Each area photographed was exposed to full ambient light intensities. Contact prints were made from the negatives
and a mask made to correspond to 6 cm' of coral
surface. The number of polyps within each mask
were recorded for each colony.
Isolatioll alld determillation of zooxalltlrellae pOplIlatioll size.-Samples
of coral were rinsed with
fresh water to wash off any surface material and
algae on the undersides of the coral. A circular
mask was made by cutting a 22-mm diameter circle
in a polyethelene sheet which was then carefully
placed and fastened, so as not to distort the shape,
over the surface of the living coral with rubberbands. The area inside the circle was "waterpicked" clean of all tissue with filtered seawater
(Millipore .45 p. [MFSW]) which was then collected in a clean plastic bag (Johannes and Wiebe,
1970). The "blastate" was gently ground in a
loose-fitting glass tissue grinder (10 ml volume) to
break up the mucus released during waterpicking.
Light microscopic examination indicated that no
observable damage to the zooxanthellae occurred
during this step. The processed blastate was centrifuged to collect the algal cells (4080 g, 10 min,
5°C). The supernatant was collected, its volume
determined, and a subsample centrifuged (12,100
g, 10 min, 5°C) to collect any algae not coIlected
on the first run. The main peIlet was resuspended
in 5 ml MFSW, and cell number determined by
four replicate hemocytometer
counts. The pellet
from the supernatant was estimated with two replicate counts. The total number of algae was calcu-
FISHES
81
to algal cells/cm'
photoSYllthetic
pigmell t
living coral
cOl/tel/t.-
Zooxanthellae photosynthetic pigments were analyzed from colonies of M. 1I111/IIlllriscollected from
Dancing Lady Reef by SCU BA divers and brought
to the laboratory as previously described. After
waterpicking, zooxanthellae were washed twice by
centrifugation
(4080 g, 5 min, 5°C) in a large
volume of MFSW. The pellet was then resuspended in a small volume of MFSW thoroughly
mixed, and a small aliquot taken for hemocytometer counts. Four counts were made for each sample. Two to 10 ml of the suspension were collected
by centrifugation
(12,000 g, 10 min, 5°C), the
pellet dispersed and extracted in 90% acetone buffered with MgC03 at -5°C under nitrogen gas for
24 h. Samples were then vortex-mixed again and
centrifuged (12,100 g, 10 min, 5°C). Three ml
of extract were placed in a glass cuvette and the
optical densities at 665, 645, 630, and 480 nm
determined.
Measurements
were initiaIly taken
with a Beckman DU spectrophotometer
(battery
powered) which was later replaced with a Beckman DU-2. There were no differences in the accuracy between these two machines. These data
were then converted to pigment concentrations using the equations of Jeffrey (Strickland and Parsons, 1965).
experimel/ts.-Reciprocal
transplantation experiments were carried out on Dancing Lady Reef with M. wlll/daris to determine the
effect of transplantation
on growth rate, zooxanlhellae population density and pigmentation,
and colony growth form. Colonies were transplanted from 10m to 15, 25, and 45 m and colonies from 45 m were transplanted to 25 and 15 m.
Colonies were not moved into shaIlower reef environments because of potential damage by severe
storms that pound the reef during the winter
months.
Colonies were transplanted to a site and then
stained with Alizarin Red-S for determination of
skeletal extension rate (Dustan, 1975a). Transplanted colonies were placed on the reef at their
transplant stations in positions such that if a
change in growth form did occur, it could be
picked out as not being correlated with colony
placement. Flat colonies were placed in approximate growth position and also at right angles to
their normal growth position. Round colonies were
positioned with their tops facing up and horizontaIly. Small pieces were collected from colonies
after both I and 2 years had elapsed. The zooxanthellae were isolated, their pigment concentrations determined, and the coral skeletons sliced for
determination of skeletal extension rate. At the
end of 2 years small pieces of colonies were examTrallsplal/tatioll
BULLETIN
82
Depth
(m)
6
13
17.5
27
30
35
45
80
C\J
E 70
u
U)
"-
(f)
0....
OF MAR]NE
SCIENCE,
Mean polyp
N Number
12 80.6
82.3
8
21 67.8
14 49.6
.28 43.5
22 35.6
15 31.5
-.J
ORIGIN
o
o
"'0
)( 9
IN-SITU
10M (2yrs)
~ 8
lJ 10 M ( 7mo)
• 30M (7mo)
"
•• 45M
.lO
~
~ 7
(2yrs)
tj
~6
N
E 5
~
~4
...J
60
d
3
~
2
I
>-
a
0....
VOL 29, NO. I, ]979
<:(
61
50
20
40
30
I
I
I
I
I
,
10
20
30
40
50
60
DEPTH(m)
10
20
30
40
50
DEPTH(m)
Figure 2. Depth distribution of polyp density/cm'
in M. alllll/laris,
Dancing Lady Reef, Pinnacle 1,
and Bouy Reef, Jamaica. Vertical bars equal one
standard deviation unit.
ined carefully for any changes in growth forms
which had occurred.
In addition, very small colonies were collected
from two depths: 17 m on the escarpment of the
fore-reef terrace, and 45 m on the fore-reef slope.
These colonies were between 1 and 15 em in
diameter and presumed to be juveniles. They were
all brought into the laboratory, stained with Alizarin Red-S, fastened to artificial substrates, and
placed back on Dancing Lady Reef. One group
consisting of colonies from 17 and 45 m was affixed to aM. alll/I/laris colony at 15 m and another
similar group placed at 45 m. Two years later the
survivors were collected and examined for changes
in growth form.
Transplantation
experiments of shorter duration
were carried out to determine the degree of specificity of colonies of M. allllularis to their respective light regimes. Colonies were moved from 45
m to 28 and 15 m, from 10 01 to 15, 28, and 45 01,
and from 30 01 to outdoor running seawater
aquaria exposed to full sunlight filtered through
0.25-in clear plexiglass to absorb radiation.
In a further experiment a colony from 40 m
was placed in an outdoor aquaria with running
seawater and parts of it were exposed to bright
sun filtered through 0.25-in clear plexiglass, shade,
red filtered light (Wratten #29 gel encased in
plexiglass), and dark blue plexiglass (Rohm and
Haas #2264).
The colony was then illuminated
Figure 3. Depth distribution of mean zooxanthellae density,'cm' living coral tissue of M. alllll/laris,
Dancing Lady Reef, Jamaica. Vertical bars equal
one standard deviation unit. Legend in upper right
of the figu'e indicates colony depth of origin and
time of sanpling after transplantation.
by natural i unlight for a total of 20 h over a 2-day
period. Tte zooxanthellae
from the centers of
each differ :nt part were isolated and examined
optically wi th a Wilde light microscope (400 X)
for presence or absence of pigment.
Bleached
zooxanthellae
appear colorless while unbleached
cells are yellow-brown.
RESULTS
Density of Polyps/cm2
The density of polyps/cm2 of living
tissue surface decreases non-linearly as
water dept 1 increases (Fig. 2). Chalice size
does not vary with depth; the polyps become spaced farther apart (1. W. Wells,
personal c )mmunication).
Zooxanthellae Density
The demity of zooxanthellae/cm2 of living coral t ssue surface area decreases with
increasing ';vater depth to about 45 m, then
increases slightly to the lower depth limit
of M. annu'aris (Fig. 3). Algal density/cm2
is negative.y correlated with depth (r
-0.83) and positively correlated with decrease in d\:nsity of polyps/cm2 (r
0.91)
(Table 1).
=
=
MATSUI
AND
ROSENBLATT:
NEW
Table I. Correlation analysis between density of
zooxanthellae/cm' li\·ing coral tissue and density of
living coral pol)'ps/cm' for M. amwlaris, Dancing
Lady Reef, Jamaica
Depth class
(m)
Zooxanthellae/cm'
(X 10')
Coral
polyps/cm'
Zooxanthellae/polyp
(X 10')
8.76
5.61
5.24
4.38
2.65
4.06
Correlation
coefficient
(r)
Variables
Zooxanthellae/cm'
& depth (m)
Polyps/cm' &
depth (m)
Zooxanthellac/cm"
po1yps/ cm'
..
_~- ._------------
13.67
13.92
10.83
7.83
6.42
5.50
&
64.1
40.0
48.4
55.9
41.3
73.8
FISHES
83
o IN· SITU
D. 10m
a 45m
o 30m
I Standard deviation
3
-!
-!'"
w02
u, )(
01
1-5
9-13
15-17
30
40-42
45-50
SEARSID
0>
-.i ::l..
:r:
I
u
o
/0
20
30
40
50
10
20
30
40
50
10
20
30
40
DEPTH (m)
50
3
-!
Significance
level
-0.83
< .01
-0.95
< .01
+0.91
< .01
-!'"
W
o
u,
2
)(
ul 0>
-.i ::l.. I
:r:
u
o
-------------
Intracellular Photosynthetic Pigment
Content
5
-!
-!
W
,,,,
4
U
00
The concentrations of intracellular photosynthetic pigments of zooxanthellae varied
with depth. A graphic representation (Fig.
4) shows that the mean concentration of
pigment/cell increases slightly between the
surface and 15 m. At 28 m (the next
sample point, due to sparse coverage in
between), the start of the deep reef habitat,
pigmcnt conccntration/cells shows a further
increase, then decreases rapidly with depth
to 35 m. Below 35 m there is a slight increase once more. Analysis of variance
with regression on depth performed separatcly for Chlorophyll a, c, and carotinoids
showed that in each case there was a significant diffcrence between depths (P > .05),
a non-significant linear regression, and
significant deviations from linearity (P >
.05).
Pigment concentration/cm~ of living coral
tissue was calculated by multiplying pigment
concentration/cell by the mean number of
zooxanthellae/cm~. Pigment concentration/
cm~ decreases slightly with depth bctween
O~3
Z
~
0>
::l..
o
~
2
u
Figure 4. Depth distribution of intracellular photosynthetic pigment content of zooxanthellae from
M. {///111/1aris,
Dancing Lady Reef, Jamaica. Vertical bars equal one standard deviation unit. Legend
in upper right indicates depth of origin of colonies.
the surface and 15 m (Fig. 5). Below 28 m
the trend established in the pigment/cell
data holds for the pigment/cm2 data.
Transplantation Experiments
The pigment concentration/zooxanthellae
and per cm2 of surface area for transplanted
colonies differed from the values established
in in situ colonies at both original and
transplant depths. In all cases, except a
BULLETIN
84
OF MARINE
SCIENCE,
610m
o 45m
<>30m
--------Depth
ts~
10
-1
~' N
20
30
Origin
40
20 ~
o
0>
O:::::i..
:36
"---
_
0
~
'
I
10
<>~
,
20
~\,,~
30
40
-
50
..
---
Mean
(m)
..~rans)Iant
50
~ 13
Cl... -.... 10
29, NO. I, 1979
Table 2. Growth rate (mm/yr) of colonies transplanted ar.d allowed to grow for 1 year as determined by Alizarin Red-S staining technique
ORIGIN
o IN-SITU
\
VOL
N
growth
rate
(mm/yr)
SD
Axis of polyp addition
10
3
IS
5
28
45
28
45
6
2
15
7
6
4
10
10
10
10
28
45
45
45
10
10
10
10
28
45
45
45
10
15
28
45
28
45
15
28
15
28
6.68*
5.49
2.74
1.46
4.82*
4.83*
2.31
2.00
1.33
2.29
0.76
2.00
1.20
1.04
1.39
1.39
Axis of IIpll'ard growth
~
20
ONE
z u
W-....
f-
0>
1E::i..
10
c:(
u
o
10
20
30
40
50
DEPTH(m)
Figure 5. Depth distribution of intracellular zooxanthellae photosynthetic pigment content/cm2 living coral tissue of M. alllll/laris, Dancing Lady
Reef, Jamaica. Vertical bars equal one standard
deviation unit. Pigment/em" calculated from pigment/algal cell and zooxanthellae/cm2
data. Legend in upper right indicates depth of origin of colonies.
10-m individual at 45 m, concentrations
were lower in transplanted colonies than
in situ colonies from depths of origin or
transplantation.
Pigment concentrations/
zooxanthellae for all transplant groups
(10-, 25-, 45-m origins) are very similar
for chlorophylls and carotinoids at the 15and 25-m sites. The pigment content of
10-m colonies increases with depth.
The skeletal extensions rates (SER) of
all transplanted corals were less than, or
the same as, the mean in situ growth rate
of colonies at the depth of origin. The mean
SER for both axes of growth [polyp addition and upward growth (Dustan, 1975a)]
for colonies of 10-m origin display a decrease in SER with increasing transplantation depth (Table 2). The SER of these
3
6
6
3
16
7
7
4
6.68*
4.17
1.67
1.00
1.70*
1.63 *
1.30
0.92
2.00
2.22
0.59
0.24
0.40
1.20
0.63
0.36
• ill sir" groI\ th rate of resident population.
colonies LIang the axis of upward growth
comes very close to the mean in situ rate of
colonies at the transplant depths of 28 and
45 m (Dtstan, 1975a). Ten meter colonies
allowed tc grow for 2 years at the transplant
stations ('fable 3) show a decrease in SER
at 15 ane 28 m and an increase at 45 m
(n
1, h(lwever).
The SER of colonies of 45-m origin was
greatly reduced in both axes of growth for
the I-year transplants (Table 2) at their
transplant stations as compared to 45 m or
transplant depth in situ rates. The 2-year
transplant~ (Table 3) show a slight increase
in growth rate over the I-year transplants.
The growth rate of the corals at the 28 m
station is higher than at the 15-m station.
However, small sample sizes do not allow
for a rigor )Us statistical test.
Transplanted colonies were harvested
after 2 years of residence at their respective
transplant
stations and examined for
changes in growth form. Whatever changes
may have occurred were expected to be
=
DUSTAN:
PHOTODAPTATION
Table 3. Growth rate (mm/yr)
of transplanted
colonies of M. alllllliaris over a 2-year period as
determined by Alizarin Red-S staining
-
Depth
------
Mean
growth
(01)
Origin
Trans·
plant
10
10
10
10
28
45
45
45
10
15
28
45
28
45
15
28
10
10
10
10
10
15
28
45
28
45
15
28
IN ZOOXANTHELLAE
85
1
rate
N
(mm/yr)
SD
Axis of polyp addition
3
5
2
1
16
7
4
1
6.68*
4.00
1.70
1.82
4.82*
4.83*
3.00
3.70
2.00
4.47
0.32
2.00
1.20
2.10
2
Axis of upward growth
28
45
45
45
• ;11 sirll
3
5
3
1
16
7
4
1
6.68*
2.26
0.97
1.65
1.70';'
1.63*
1.79
2.07
2.00
1.79
0.52
0.4
1.2
1.2
one-year growth rate.
small as the growth rate of transplanted
colonies was found to be much less than
resident colonies at the transplant stations.
Colonies from the shallow reef grew at
reduced skeletal extension rates on the deep
reef (25 and 45 m), but did not change
their axis of growth. They did show some
slight flattening in that growth at their edges
increased but the axis of maximum polyp
addition did not seem to change. Large
colonies showed much less tendency towards
flattening but this may reflect the amount of
growth necessary to change a small colony.
Neither large nor small colonies developed
an epitheca which is used as a base for
edgewise addition of polyps (Barnes, 1972).
Colonies from 45 m at 25 and 15 m
suffered high mortality and survivors exhibited changes in growth form at their
edges. Not all colonies changed. Those
that changed form did not all change the
same amount. The edges of flat colonies
grew down, away from the living surface at
an angle of approximately 90°. This angle
3
Figure 6. X-rays of M. alllllliaris showing patterns
of skeletal growth in the flat form: (1) Normal
ill sitll pattern.
30 m; (2) Colony transplanted
from 45 m to 15 m 2 years after transplantation;
(3) Colony from Pinnacle 1 dynamite blast site
showing reorientation of polyp surface after the
colony was shifted. 35 m, Pinnacle 1 Reef, Jamaica.
was independent of colony placement and
seems to be the result of a failure of the
small corallites at the edge to turn up as
they normaly do just before a new corallite
buds at the edge.
X-radiographs of M. annularis show that
the flat form is the result of corallites being
added at the growing edge of the colony.
As the corallite grows larger its axis of
growth rotates so that the polyp grows upwards at an angle of approximately 30° to
the surface of the colony. This outwardly
angled growth occurs for about 1 year then
the corallite turns upwards, budding off a
new corallite at the colony's edge as it does.
In transplanted colonies the corallites do not
turn upwards (Fig. 6) and the lip formed is
the result of this failure.
If a colony is moved at its depth of
origin, the corallites added to the colony
after that time will reorient and grow
86
BULLETIN
OF MARINE
SCIENCE,
VOL.
29, NO.
I, 1979
Figure 7. Photo of large flattened M. allllularis colony showin! reorientation of polyp surface to plane
of water's surface after falling over some years before. 35 m, .)ancing Lady Reef, Jamaica. Photo by
author.
parallel to the water's surface. This was
observed in colonies displaced by excavation
operations at Pinnacle 1 in 1969 (35 m)
and on Dancing Lady Reef (35 m) where
a large colony fell to one side possibly as
a result of storm damage (Fig. 7). The
response of the transplanted colonies is,
therefore, not a natural "repair response"
as the new corallites grew at 90 to the
living surface, independent of its orientation
to the water's surface.
Transplant experiments conducted on the
reef showed that within this population the
rate of bleaching is related to the increment
of upward movement, therefore presumably
to higher light intensity (Table 4). Colonies
transplanted and placed in the shade or in
the indoor running seawater aquarium did
not bleach within the time span of the experiment.
Short duration transplant experiments
suggest that bleaching is a response of the
zooxanthellae to high light intensities and
results from a loss of photosynthetic pig0
ment from thc algae before they are expelled frem the coral colony. The colony
brought f'om 40 m to an outside aquarium
showed distinct differences in the proportion of colJrless and yellow-brown pigmented
zooxanthellae between the exposed areas
and shad<:d control area (Table 5). The
difference:; seen between different light
quality treatments are interesting, and one
would like to speculate on their significance,
however critical comparisons might be confused sine the filters were not adjusted so
as to pass light of similar intensities.
The number of zooxanthellacjcm3
in
transplant<:d colonies did not show trends
similar to in situ colonies (Fig. 3). After
2 years zcoxanthellaejcm3 in colonies from
10 m dec'eased at 15 m to less than half
the in sitl! 15-m density and one-third the
in situ 10 -m density. At 25 m the 10-m
colonies hld half the estimated density of
in situ 25-m colonies but, at 45 m thcir
density m~tched the 45-m estimated in situ
density (st II half of the 10-m in situ value).
DUSTAN:
Table 4. Transplant
Origin
depth
(m)
Transplant
depth
(m)
-------
PHOTODAPTATION
experiments with M.
N
Time
from
trans
plant
(days)
Degree of
bleachingt
4
*
none
none
rounded
flat
","
none
flat
none
flat
19
*
10
17.5
13
24
none
10
30
45
0.5
4
5
45
17.5
30
.~Rate
of bleaching:
21
16
19
25
26
15
• very slight,
•• noticeable,
Growth
form
rounded
12
8
1.5
Mortality
(colonial)
small pts.
of colony
one
17.5
26
87
{llllllllaris
10
45
IN ZOOXANTHELLAE
*****
Comments
lots of
sed. scour
lots of
sed. scour
low light
outdoor tank
expt. in
running
seawater
angle of
colony not
significant
rounded
**
***
....;.-.,...•.
.,.
•••
moderate,
Colonies from 10 m transplanted in the
winter of 1972 to 15 m and harvested in
the summer of 1973 (7 months later) had
zooxanthellae
population
densities approaching 60% of the mean population
density of IO-m residents and 75% of the
I5-m residents. It is not known if the
colonies sampled after 2 years have reached
a stable zooxanthellae density.
Zooxanthellae/cm~ increased by one-third
in the 45 to 25-m transplants and matched
the estimated density/cm~ of the 25-m
residents. Zooxanthellae density of 45-m
colonies at 15 m remained the same as 45-m
resident colonies, approximately half the
density of lS-m residents.
DISCUSSION
•
$ ••
heavy,
•••••
angle of
colony not
significant
severe.
of zooxanthellae population density. As a
first approximation, disregarding polyp fine
structure, a layer of zooxanthellae one-cell
thick will cover the surface of a coral at cell
densities of approximately 1.5 X 106 algal
cells/cm~ (Drew, 1972). The zooxanthellae
in M. annularis range in mean cell density
from 8.76 X 10G/cm~ at a depth of 1 m to
2.65 x IOG/cm~ at 42 m and thus go from
a multilayered arrangement in shallow water
towards a more monolayered arrangement
in deep water. Similar changes in structure
have been noticed in the organization of
chloroplasts in sun and shade leaves (Busgen and Munch, 1929; Bjorkman et al.,
1972), the geometry of leaf structure
(Horn, 1971), and the overall geometry of
forest canopy and understory vegetation
Algal Density
Drew (1972) presented data that showed
algal cell numbers are correlated with the
area of coral polyp and not ambient illumination or depth which led him to suggest
that zooxanthellae cell densities are regulated by the coral host. In M. annularis,
however, ambient illumination appears to
play an important role in the maintenance
Table 5. Results of bleaching experiment
%
Filter
Shade (control)
Exposed to full
sunlight
Blue
Red
Cell counts/field
(Bleached cells/non-bleached)
Bleached
cells
0/25,
0/59,
0/27
0.0
7/0,
0/30,
1/11,
18/0,
0/41,
0/7,
9/0
0/26
4/55
100.0
0.0
6.8
88
BULLETIN OF MARINE SCIENCE, VOL. 29, NO, 1, 1979
(Horn, 1971). At high light intensities the
multilayered arrangement is selected for as it
presents a greater surface area for light capture. As light intensities approach the compensation point intensity for photosynthesis,
shading reduces the efficiency of the multilayered geometry (Horn, 1971).
The
reduction in the density of zooxanthellael
cm~ with increasing water depth suggests
an analogous response that optimizes light
capture by the remaining zooxanthellae. The
increase in zooxanthellae density below 45 m
is puzzling. The population of M. annularis
is sparse below 45 m so that only a very
small percentage of the population exhibits
this increase in zooxanthellae. It may be
that the increase represents a subtle change
in the symbiotic relationship that may allow
for a further extension in the depth range
of the species.
Polyp Density
The compensation point light intensity of
a coral colony is related to the photosynthetic capacity of the zooxanthellae, their
respiration rate, and the respiration rate of
the animal tissue. Species of reef-building
coral with large polyps respire less
oxygen/ cm2 living tissue than do corals with
small polyps (Kawaguti, 1937; Mayor,
1917; 1924) . The observed decrease in
polyps/cm2 with increasing water depth in
M. annularis may be a mechanism whereby
the volume of living coral tissue/cm2 is
reduced, thus lowering the metabolic demands of the coral animal on its symbiont
and resulting in a lowering of the colony's
compensation point light intensity. As light
intensity decreases with depth this may enable the species to extend its depth range
into regions of lower light intensities, an
adaptive response paralleling adaptations of
terrestrial shade plants (Raven and Goodchild, 1975). Thus it would appear that
the coral colony, zooxanthellae and animal
host together, parallel the adaptations of
higher plants with respect to changes in
light intensity. The density of zooxanthellae
per area decreases as a function of light
intensity and the animal host appears to
accommc·date by changes in its tissue surface area to volume ratio.
Zooxanthellae Photosynthetic Pigments
Chang ~s in photosynthetic pigment content in t1e zooxanthellae of M. annlllaris
suggest that the algae photoadapt to the
changes in light intensity that occur between
the surface and 55 m. The changes in
photosyn' hetic pigment content are similar
to the patterns described in higher plants
(Bjorkm,n et aI., 1972; Bjorkman and
Holmgrer., 1963), green and red algae
(Broady and Emmerson, 1959; Reger and
Krauss, 1970; bQuist, 1974; Anderson
et aI., 1573; Beardall and Morris, 1976),
and dino'lagellates (Prezelin, 1976). The
increase in pigment content in response to
decreasing light intensity in chlorophyll
b-containing green plants is due to an increase in relative concentration of light
harvestin& antennae chlorophyll alb protein (Brewn et aI., 1974; Alberte et aI.,
1976). In some dinoflagellates the lightharvesting peridinin-chlorophyll a protein
complex (PCP), a caroteno-protein, may be
analogous to the chlorophyll alb protein
(Thornbe' et aI., 1976). In the dinoflagellate Glenodinium sp. thc intracellular concentration of PCP increases five-fold in
response ta a change of light intensity from
2000 uW Icm2 to 250 uWIcm2 (Prczclin,
1976) which corresponds to thc light levcls
estimated betwecn 35 and 60 m (Lang and
Dustan, field observations). Purified PCP
has a bread absorption maximum around
480 nm 'vhich corresponds to the wavelengths of light that penetrate deepest into
tropical seas (Prezelin et aL, 1976). Thus
the concentration of PCP could be of
adaptive significance in populations of
photosyntt etic dinoflagellates that occur in
deep water (Prezelin et al., 1976). The
zooxanthellae of M. annlllaris possess PCP
(Haxo, personal communication) and the observed increase in intracellular carotenoid
concentrat:on (OD at 480 nm) with depth
between 0 and 28 m and 35-50 m, hints at
DUSTAN:
PHOTODAPTATION
the possibility that PCP may be of photoadaptive significance in the symbionts of
rcef-building corals.
The patterns of the distribution of intracellular photosynthetic pigment contents
suggest that there are "sun" and "shade"
zooxanthellae corresponding to the ambient
lighting conditions on the fore-reef terrace
and forc-reef slope respectively. Included
here in the fore-reef terrace population are
the reef flat populations which are classified
as sun-adapted as they receive more light
energy than does the deeper fore-reef
slope.
Colonies of M. annularis exhibit changes
in growth form with depth that parallel
observed changes in zooxanthellae pigment
composition. Shallow colonies, above 1520 m, are predominantly rounded in their
morphologies while deeper colonies are
flattened. This presumably is a direct consequence in the amount of light energy
available to support light-enhanced calcification (Goreau, 1963; Barnes and Taylor,
1973; Dustan, 1975b).
The variations in pigment contents seen
within the depth ranges of sun and shade
populations indicate that photo adaptation
on a finer scale may occur within these sun
and shade algal populations. Within the sun
population the intracellular photosynthetic
pigment content increases with depth between 1 and 15 m (decreasing light intensity). The shade zooxanthellae at 28 m,
ncar the top of the fore-reef slope, possess
almost twice as much chlorophyll a and c
as the fore-reef terrace algae. This tremendous increase in pigment content would seem
to be in response to decreased light intensity
(Brody and Emmerson, 1959). The decrease in intracellular pigment content between 28 and 35 ill suggests that the shade
algae arc adapted to a very narrow range
of light intensity and when light intensity
decreases further, pigment content decreases
(Brody and Emmerson,
1959).
The
greatest proportion of the fore-reef slope
population lives above 35 m (Dustan,
1975a) implying that optimal conditions
IN ZOOXANTHELLAE
89
exists above this depth (Brody and Emmerson, 1959). The decrease in photosynthetic
pigment content may have real ecological
significance, and implies that zooxanthellar
contribution to the coral colony may decrease significantly below 35 m. This in
turn may limit the depth to which most of
the M. annularis can successfully extend.
The small increase in pigment content between 35 and 50 m may reflect another type
of photoadaptation, which is also reflected
in the increase of zooxanthellae/cm2 at
these depths.
Transplanation Experiments
Lang (1970; 1973) demonstrated, through
transplanation of coral colonies from the
deeper habitats of the reef to shallow water,
that the zooxanthellae of Jamaican reef
corals have restricted abilities to adapt to
sudden increases in light intensity. Controls, transplanted and placed in the shade,
did not undergo the severe bleaching seen
in experimental colonies. The results of her
experiments (Lang, 1970; Table 11, p. 61)
show that the response to transplantation
differs between species and that the rate of
bleaching was proportional to the increment
of increase
in light intensity.
Thus
the
zooxanthellae of deep water corals are unable to rapidly change their photophysiological machinery to adapt to sudden increases
in light intensity. The results of my study
are in agreement with these findings and
further suggest that the algal photophysiology within a species may vary with
changes in habitat depth.
Conclusions
The bimodal vertical distribution of M.
combined with its responses to
transplantation (bleaching, reduced skeletal
extensions rate, and changes in the photosynthetic pigment content) suggest the
existence of two ecotypic races of zooxanthellae in the M. annularis population on
Dancing Lady Reef. One is adapted to the
high light conditions above 15-20 m, and the
annularis
90
BULLETIN
OF MARINE
SCIENCE,
other to the lower intensity light conditions
below 20 m. The two populations overlap to
the extent that flat colonies are sometimes
found in shallow shaded habitats. The depth
range of the separation (10-20 m) is the
limit of red light penetration into the sea
and where the exponential decrease in light
intensity begins to approach its asymptote.
Changes in water clarity, sea state (with
the exception of large storms), and seasonal
position of the sun will not affect the shape
of the light attenuation curve greatly but
may shift the curve horizontally on its
depth axis. Colonies above 15-20 mare
exposed to a highly variable, high light
intensity environment containing many elements of the visible spectrum, while
organisms below 20 m are exposed to a less
variable light environment of lower light
energy composed almost exclusively of bluegreen light. The 15 to 20 m region marks
the overlap region of these two light climates. The range and variance in light
intensity and spectral quality in this overlap
region may be such that colonies of M.
annularis may not be able to photosynthesize and calcify as vigorously in this light
climate as they can at the population
peaks at 10 and 30 m. Light-enhanced
calcification in corals appear to require a
translation of the light energy trapped by
zooxanthellar photosynthesis into cellular
metabolic energy (Chalker and Taylor,
1975). As speculation, there may not be
enough radiant energy over a long term to
sustain the shallow water rounded morphology, and the high intensities experienced
occasionally may select against the low
light adapted algae. The observation that
mean colony size decreases in the overlap
zone (Fig. 1) lends circumstancial support
to this hypothesis. Furthermore, other environmental conditions in this region seem
close to ideal for profuse coral growth:
wave action is present but not severe and
light intensities are reasonably high.
On the eastern side of Discovery Bay the
slope of the reef is almost constant between
5- and 25-m depths. The region between
VOL. 29, NO, 1, 1979
15 and W m is similar in sparse coral
coverage and species composition to the
overlap rl:gion on Dancing Lady Reef. On
these twc reefs at the 15 to 20 m depth
range alITost all of the reef-building corals,
with the exception of Madracis mirahilis
Duchassa ng and Michelotti, arc smallcr and
seemingly less vigorous than individuals of
the samc species living deeper or more
shallow I Dustan and Lang, unpublished
field obs,:rvation).
Observations on the
discontinuous distribution of reef-building
corals in lhe Gulf of Aqaba (Loya, 1972),
Bonair (~catterday, 1974), Acklin Islands
(Dahl et a1., 1974), Mexico (Rannefield,
1972), C,yman (Roberts et a1., 1975), and
Jamaica (Goreau and Goreau, 1973) suggest that coral communities can often be
divided in:o shallow and deep assembluges.
These spf'cies assemblages are frequently
separated by a zone of sparse coral coverage. There is considerable variation in the
absolute depth of the separation and it is
often complicated by geomorphological
changes ir the slope of the reef. In clear
water situations (Jamaica, Gulf of Aqaba)
the 15 to 20 m depth range is the region
that make s the separation of deep and
shallow reef populations. Some investigators have presented data that suggest the
adaptation of corals to specific light intensities may prevent a deep water coral from
invading s 1allow, brightly lit reef hubituts
(Lang, 1973; Loya, 1972; Scatterday,
1974; Jauhert and Vasseur, 1974; Wethey
and Portel, 1976). Analysis of the coral
community structure of Eilat (Red Sea)
clearly shewed a region of reduced coral
coverage and diversity between 13 and
17 m. Light intensity measurements showed
that the rqion occurs at the asymptote of
the decre, se in light intensity (Loya,
1972).
H:wer than 50% of the species
found bela'", 20 m are found in the more
shallow depths of the reef (Loya, 1972).
There ule some data from studies with
terrestrial green plants that demonstrate the
inability of individuals of some plant species to photosynthesize efficiently in both
DUSTAN:
PHOTODAPTATION
high and low light conditions. Heritable
differences in leaf morphology between sun
and shade populations of the same species
have been demonstrated (Bjorkman and
Holmgren, 1963; Heslop-Harrison, 1956;
Bjorkman et al., 1972). Shade ecotypes of
Solidago viragallrea are more capable of
efficient use of weak light than are high
light ecotypes, and sun ecotypes are more
efficient at using high light intensities
(Bjorkman and Holmgren, 1963). High
light clones can adapt to low light intensities when grown under low light intensities
but plants from low light habitats cannot
acclimate to high light conditions. Examination of the leaf structure of S.
viragallrea showed that the chloroplasts of
the shade plants were partially destroyed
when grown under high light conditions
(Bjorkman and Holmgren, 1963).
The
authors concluded that the photosynthetic
apparatus of S. viragaurea is not adaptable
enough to permit this single genotype to
perform adequately in both open and shaded
habitats.
Investigations have shown that cultured
clones of the alga Chlorella vulgaris can
adapt to both high and low light intensities
independently (Neilson et aI., 1962). At
low light (300 uW/cm~) C. vulgaris contains more chlorophyll and has a lower light
saturation intensity for oxygen production
than when grown at high light intensities
(3000 uW/ em~). Cultures placed in the
reciprocal light regime take 24-36 h to
photoadapt (Neilson et aI., 1962). If the
zooxanthellae from M. annularis possess
the ability to photoadapt, the time lag and
metabolic energy requirements needed for
frequent photoadaptation might prevent efficient acclimation of a coral colony to the
irregular light regime in the 15- to 20-m
region. This alone might help to explain
the break in abundance between the shallow
and deep populations and could select for
specialization to either habitat but not to
the overlap region. It is possible, then that
the variations in ambient lighting conditions,
in addition to light intensity and spectral
IN ZOOXANTHELLAE
91
quality, may limit the distribution of reefbuilding corals.
The systematic variations of zooxanthellae
density and photosynthetic pigments suggest
that as water depth increases the zooxanthellae become more efficient at absorbing the available light energy. Between 9
and 42 m the ratio of zooxanthellae/cm~ to
polyps/cm~ is relatively constant and
significantly lower than the ratio below
45 m or above 5 m (Table 1). Perhaps
this may reflect a stoichiometric optimization which remains constant as long as
efficient photosynthetic output and transfer
to the coral by the zooxanthellae is maintained. Colonies outside this depth range
comprise a small percentage of the total
M. annularis population on Dancing Lady
Reef. Zooxanthellae in colonies shallower
than 9 m may experience light inhibition of
photosynthesis at the high light intensities
experienced near the surface while colonies
deeper than 42 m may photoadapt in yet
another manner that allows for a slight
increase in photosynthetic efficiency of the
colony. However efficient the energy capture becomes, though, it appears that
eventually the coral becomes light-limited.
Recently it has been suggested that
growth of an alga at low light levels results
in an enhancement of its ability to photosynthesis at "sub-optimal light levels and
reduces its ability to utilize saturating levels"
(Beardall and Morris, 1976). However, the
enhanced ability at low light levels does not
result in enhanced algal growth rates
(Beardall and Morris, 1976). Sessile algae
adapted to low light intensities may therefore grow at a slower rate than their high
light counterparts but the adaptation to low
light permits some growth, however slow,
to occur. If skeletal extension growth rates
of hermatypic corals may be taken as an
indication of zooxanthellae "output" or
efficiency, it has been shown that M. annularis growth rate decreases with depth
(Dustan, 1975 a). Thus it would seem that
photoadaptation of the zooxanthellae may
permit the coral to extend its depth range.
92
BULLETIN OF MARINE SCIENCE, VOL. 29, NO. ], ]979
Furthermore M. annularis is more abundant
in deep water suggesting that growth rate
per se may not be the overriding governing
ecological factor in the "success" of coral
populations.
The experimental demonstrations that
calcification is enhanced by photosynthesis
(Kawaguti and Sakumoto, 1948; Goreau,
1959a) laid the foundation for suggestings
that the zooxanthellae may have an effect
on the morphology of the coral's skeleton
(Goreau, 1963). Goreau's hypothesis suggests that the flattening of coral skeletons
in dimly lit environments is in response to
a decrease in algal photosynthetic rate. At
other times he suggested that flattening was
adaptive in a variety of other ways, such as
increase in competitive ability when competing with ramous corals, resistance to
downslope travel after being bored by
sponges, and a combination of these factors
(Goreau, 1959; Goreau, 1963; Goreau and
Hartman, 1963; 1966).
Roos (1967)
suggested that Porites astroides Lamarck
flattens so as to have light striking all parts
of the tisue maximally, thus enabling the
zooxanthellae to maximize their photosynthetic rate. It is important to note that
the flattening of corals with depth is a
general trend found in hermatypic scleractinians only. Many species that flatten
with depth may also be found flattened in
shallow-shaded habitats implying flattening
is not solely a consequence of depth. Parallel morphological changes are not seen in
ahermatypes (aposymbiotic corals) (Yonge,
1973) .
Much of the speculation concerning the
variability of reef corals has centered on
the possibility of zooxanthellar influences
on the growth form and behavior of corals.
Coral planulae containing zooxanthellae
show phototactic responses which may vary
with the ambient light intensity of the
habitat occupied by the parent coral
(Kawaguti, 1937; Atoda, 1951a; 1951b).
Zahl and McLaughlin (1959) experimented
with the phototactic behavior of the Caribbean sea anemone Condylactis sp., and were
able to show that individuals contammg
zooxanthdlae moved out of direct sunlight
into a :nore indirectly lit environment.
Aposymbiotic anemones showed no preference for shade or direct sunlight. These
experiments led them to the suggestion that
different species containing zooxanthellae
may have very different specific light needs,
and may, therefore, show different habitat
preferenc1:s on the reef.
The population of M. annularis on Dancing Lady Reef has a biomodal distribution
with peaks in abundance at 10 and 30 m.
Colonies Lbove 15 to 20 m arc rounded and
colonies .lssume a flattened form deeper
(Dustan, 1975a). Thus, the distribution of
growth fo 'ms coincides with that of the two
ecotypes of zooxanthellae-sun
and shade.
This correlation implicates the zooxanthellae
as a factor in the distribution and possibly
the differentiation of M. annularis, as selective pressures thought to limit light-enhanced
calcificatic n rates appear to involve zooxanthellar photosynthesis. Each component
of the symbiotic association is subject to
different J'ressures of natural selection and
it is suggested that co-evolution of the two
may allo~ for the diversity of forms, and
possibly, diversity of species that inhabit
coral reefs.
ACKNOWLEDGMENTS
I thank 'l". Copland, M. Chang, and E. G.
Graham of .he Discovery Bay Marine Laboratory
and J. C. Lang of the University of Texas for their
help in the f eld. Discussions with H. Lyman. 1. C.
Lang, and 1. S. Land aided in the formulation of
the research project. X-radiographs were provided
by 1. MacIntyre of the Smithsonian Institute. A.
Ley and J. Johnston read the manuscript critically
and made nany useful suggestions. The Kaiser
Bauxite Co. provided technical support, and 1. P.
Thornber and C. A. Richardson provided clerical
support. Th s research was carried out at the Discovery Bay Marine Laboratory
and funded by
Smithsonian Research Award No. 43001 to J. C.
Land and National Science Foundation Grant No.
31-589A to '). F. Squires. This work formed part
of a Ph.D. t lesis submitted to State University of
New York at Stony Brook and comprises Contribution No. 310 of the Department of Ecology and
Evolution ar d Contribution No. ISO of the Discovery Bay ]\[arine Laboratory.
DUSTAN:
LITERATURE
PHOTODAPTATION
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DATE: ACCEPTED: August
inverte-
16, 1977.
Marine Biology, A-002, Scripps Institution of Oceanography, University of California,
San Diego, La Jolla, California 92093.
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