Photobehavior of stony corals: responses to light spectra and intensity
Faculty of Life Sciences, Bar-Ilan University, Ramat Gan 52900, Israel
* Author for correspondence (e-mail: levysher{at}netvision.net.il)
Accepted 22 July 2003
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Summary |
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Key words: coral, tentacle contraction, fast repetition rate fluorometer (FRRF), chlorophyll fluorescence, diel expansion
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Introduction |
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Reef-building corals, as well as several other reef organisms, harbour
unicellular endosymbiotic algae (zooxanthellae) that supply much of their
energy needs via daytime photosynthesis. Corals are carnivores and,
since zooplankton is most abundant on coral reefs during the night
(Sorokin, 1990), it has been
suggested that most corals expand their tentacles at night to capture prey
(Lewis and Price, 1975
;
Porter, 1974
). Expansion
behavior may be affected by water flow and availability of prey
(Robbins and Shick, 1980
);
however, the extent to which any one of these factors controls tentacle
behavior is not yet clear (Robbins and
Shick, 1980
).
In zooxanthellate sea anemones, a connection exists between photosynthesis
and the expansion state. Organs with dense endosymbiotic algae (zooxanthellae)
populations expand continuously, whereas tissues with few or without
zooxanthellae contract during the day
(Gladfelter, 1975;
Sebens and Deriemer,
1977
).
Lasker (1977) described the
expansion behavior of the coral Montastrea cavernosa. In shallow
water, large numbers of polyps remain partially expanded during the day; he
named this `diurnal behavior'. `Nocturnal behavior' or tentacle expansion
during the night was observed in water deeper than 20 m, and at such depths
polyp expansion during daytime was seldom, if ever, observed. This behavioral
switch is probably based on zooxanthellae density (Lasker,
1977
,
1979
). It was proposed that
diurnally active colonies have greater zooxanthellae densities than do
nocturnal colonies (Lasker,
1977
,
1979
), but this study did not
suggest any mechanism to explain this relationship.
Corals can flourish in nutrient-poor `blue desert' waters due to their
mutualistic symbiosis with zooxanthellae. Their carbon and energy requirements
are met by different species-specific combinations of algal photosynthetic
products and by predation on zooplankton, supplemented in some cases by minor
contributions derived from dissolved organic carbon compounds and bacteria
(Achituv and Dubinsky,
1990).
On the coral reef at Eilat, in the northern Red Sea, the massive stony corals Favia favus and Plerogyra sinuosa expand their tentacles nocturnally and contract them at sunrise. Goniopora lobata and Stylophora pistillata are expanded continuously (O. Levy, personal observations). Tentacle morphology differs in the four coral species examined. In P. sinuosa and F. favus the tentacles are conical or cylindrical, and when expanded they are erect and well-separated. In S. pistillata tentacles are tiny (up to 2 mm) and extended during both day and night. The tentacles of G. lobata are cylindrical and project sideways from the top of the polyp to form a `flower-like' crown of 24 tentacles. The polyps project several centimeters above the skeleton yet the entire polyp can retract into the coral skeleton.
The light environment is an important component of the productivity,
physiology and ecology of corals (Dustan,
1982; Dubinsky et al.,
1984
; Porter et al.,
1984
; Falkowski et al.,
1990
). Underwater light decreases exponentially with depth,
roughly following the Beer-Lambert law. Underwater light is attenuated by the
water itself, by dissolved and suspended matter and, most importantly, by
phytoplankton. Light attenuation is not uniform over all wavelengths, and the
water column behaves like a monochromator, narrowing the spectrum of the most
penetrating light to a relatively narrow waveband
(Falkowski et al., 1990
). In
the clear oligotrophic waters surrounding reefs, light extinction in the
violet and blue parts of the spectrum is minimal, while its attenuation is
higher at longer wavelengths. However, in such `blue desert' shallow waters
corals can also be exposed to considerable penetration of red wavelengths and
non-visible (UV) wavelengths (Smith and
Baker, 1979
). Recently Gorbunov and Falkowski
(2002
) have shown that
zooxanthellate corals even perceive blue moonlight, which consists of the most
penetrating wavelengths in the area, typical of coral reef environments.
The aim of this study was to find out if the expansion and contraction
behavior of zooxanthellate corals occurs as a direct response to light, or as
an indirect response to it mediated by photosynthetic activity of their
symbiotic algae. We examined the possibility that the expansion/contraction
behavior of tentacles optimizes photosynthesis. We examined expansion and
contraction responses to different light intensities and wavelengths over
different times, including in the azooxanthellate coral Cladopsammia
gracilis. We studied the absorption and the action spectra for
photosynthesis and the distribution of zooxanthellae within the corals. We
also studied the photosynthetic characteristics of the four species using the
SCUBA-based, fast repetition rate fluorometer (FRRF;
Kolber et al., 1998).
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Materials and methods |
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Measurement of the light spectrum
The visible light spectrum was measured at a depth of 5 m at the coral
collection site. Spectral scans between 350 and 750 nm were conducted on
several cloudless days in February 2001 using a Li-Cor LI1800 scanning
spectroradiometer (Lincoln, NE, USA). Scans were made every 30 min at 2 nm
wavelength intervals from 6:00 h to 18:00 h.
Effect of light on tentacle contraction
Colonies were tested at low light intensities, up to 1.5% of the sea
surface light level, which is the lower light intensity of euphotic zone and
the limit of hermatypic coral distribution. F. favus, G. lobata, S.
pistillata and C. gracilis were illuminated at 10 and 30 µmol
quanta m-2 s-1 (N=5 corals for each irradiance
level). Colonies of P. sinuosa were illuminated at 30 µmol quanta
m-2 s-1 (N=3). A Xenon lamp of 450
W(Kratos-Schoeffel Instruments, Doisberg, Germany) acted as a light source and
included a LH-151/2 lamp housing and LPS-255 h power supply. The beam from the
lamp housing was passed through a monochromator (Bausch & Lomb
Instruments, New York, USA) to provide light at wavelengths of 400-700 nm.
Tentacle contraction experiments were conducted in a 25 l recirculating
flow tank (modified from Vogel and
Labarbera, 1978). The tank was 100 cm long x 10 cm wide
x 25 cm high. Water was circulated by a propeller connected to a 12 V
d.c. motor and flow speed was computer-controlled at 5 cm s-1. Flow
speed was calibrated using a video camera with a closeup lens (Sony CCD 2000E,
Hi8 PAL system; Tokyo, Japan) to follow the movement of brightly illuminated
particles along a ruler placed in the tank
(Trager et al., 1990
).
All experiments were conducted at night in a darkroom. Two colonies, an
experimental colony and a control colony, were placed in the flow tank
well-separated from each other to ensure that there would be no interference
to the flow received by each. A recirculating bath at 24±0.1° C,
which is equal to the sea temperature, controlled the water temperature. Water
was replaced every 2 h. F. favus, G. lobata, S. pistillata and C.
gracilis colonies were illuminated at two irradiance levels, 10 and 30
µmol quanta m-2 s-1, and at 16 different wavelengths
between 400 and 700 nm at intervals of 20 nm, while colonies of P.
sinuosa were exposed only to 30 µmol quanta m-2
s-1. Circulation in the tank was stopped when the corals were fully
expanded. After 15 min, the experimental coral was illuminated with all 16
wavelengths in a random order, to prevent a habituation effect. Tentacle
contraction behavior of the coral was scored on a scale of 0-4, where 0 was no
expansion (i.e. full contraction) and 4 was 100% expansion. Final analyses
were performed only on the 0% and 100% expansion scores. The scores referred
to polyps of the entire colony (see
Lasker, 1979)
(Fig. 1). The behavior of the
corals was documented every minute for a total of 30 min for each wavelength.
In each experiment a second, non-illuminated coral was used as a control. We
also conducted these experiments with the corals exposed to the photosynthetic
inhibitor DCMU (3-(3,4-dichlorophenyl)-1,1-dimetheyl urea), at a final
concentration of 10 µmol l-1 (see
Rahav et al., 1989
). DCMU
blocks photosystem II and prevents production of photosynthates. The
experiments were also conducted with the azooxanthellate coral
Cladopsammia gracilis, which expands mostly at night. In addition to
the 10 and 30 µmol quanta m-2 s-1, C.
gracilis was exposed to light intensities between 250 and 400 µmol
quanta m-2 s-1.
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Zooxanthellar density
Zooxanthellar densities were measured in F. favus (N=5),
P. sinuosa (N=4), S. pistillata (N=4) and
G. lobata (N=4). Except for G. lobata, colonies
were placed in an anaesthetizing solution of 7.5% MgCl2 in (1:1
v:v) distilled water and seawater at room temperature
(Sebens and Miles, 1988) for
approximately 3 h. Tentacles (N=30) were removed from different
polyps using tweezers and small scissors. Manipulations were carried out
during the day and anaesthetization was necessary because these colonies are
normally contracted during the day. Tentacles (N=30) were removed
from G. lobata in running seawater and without anesthetization as
this species is normally expanded during the day. Severed tentacles were
photographed using a Nikonos V camera with close-up tubes, and their surface
area was calculated assuming their shape to be a cylinder, according to the
formula:
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Pigment and chlorophyll analysis
Small pieces were collected from F. favus and P. sinuosa
colonies, chlorophyll was extracted in 90% acetone, the absorbance spectrum at
400-700 nm was measured using a Cary spectrophotometer (Varian, Palo Alto, CA,
USA) and the concentration calculated using the equations of Jeffrey and
Humphrey (1975). A tissue
homogenate was prepared from these species for estimates of zooxanthellar
pigments. The homogenate was obtained by removing all tissue with an airbrush
(modification of the Water-Pik method of
Johannes and Wiebe, 1970
). The
homogenate was centrifuged twice in seawater, at 1500 g for 15
min in order to separate the algae from the host tissue. The zooxanthellae
pellet was taken for pigment identification by high-performance liquid
chromatography (HPLC), using the reverse-phase HPLC system after Yacobi et al.
(1996
). Pigments were
identified using ChromaScope (BarSpec, Israel), a spectral peak analyzer. The
pigments were identified by the spectral data of the peaks separated by HPLC
and their retention times, using the data of Rowan
(1989
) and Jeffrey et al.
(1997
). Quantification of
compounds represented by the peaks was obtained by injection of known
concentrations of pigment into the HPLC system. All pigment concentrations
presented here are the means of duplicate measurements. Individual
measurements did not differ by more than 10% between the duplicates.
Fluorometer measurements
A fast repetition rate fluorometer (FRRF) was positioned on a tripod
adjacent to the flow tank. FRRF measurements were taken by aiming the
instrument at a coral in the tank and triggering the instrument. Measurements
were made in the dark on corals with expanded and contracted tentacles. The
action spectrum for photosynthesis was obtained by FRRF taken with corals
illuminated by wavelengths of 400-700 nm. An illumination intensity of 10
µmol quanta m-2 s-1 was obtained using the Xenon lamp
and monochromator. FRRF measurements involve a series of subsaturating
`flashlets' that cumulatively saturate PSII within 100 µs
(Falkowski and Kolber, 1995
;
Kolber et al., 1998
). The FRRF
technique enables non-invasive and rapid measurement of maximum quantum yield
of photochemistry in PSII (Fv/Fm, where Fv is variable fluorescence and Fm is
maximum fluorescence) and the photosynthetic parameter Sigma, which is the
cross section of PSII (
PSII)
(Kolber et al., 1998
).
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Results |
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Tentacles of Favia favus fully contracted within 5-6 min when exposed to low light intensities (10 and 30 µmol quanta m-2 s-1) at wavelengths of 400-520 nm(Fig. 3A,B). At 10 µmol quanta m-2 s-1 (N=5) a significant difference was found between the response time at 400-520 nm and at 540-700 nm to elicit full tentacle contraction (Fig. 3B; one-way analysis of variance, ANOVA, followed by the Student's t-test; P<0.0005). Differences related to response time of tentacle contraction were also significant in F. favus colonies (N=5) at 30 µmol quanta m-2 s-1 between wavelengths of 400-500 nm and >660 nm and the rest of the visible spectrum (540-560 nm) (Fig. 3A; one-way ANOVA followed by the Student's t-test, P=0.0016). Contraction occurred at wavelengths of 660-700 nm when colonies were illuminated at 30 µmol quanta m-2 s-1. Tentacle contraction at 540-640 nm was very slow regardless of illumination intensity. Tentacles did not contract even after 30 min of illumination in some corals. Control colonies, which were not illuminated, remained fully expanded during all the experiments (N=5, for each set of experiments). Goniopora lobata, Stylophora pistillata and Cladopsammia gracilis did not respond to light at any wavelength.
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Colonies of Plerogyra sinuosa, exposed to 30 µmol quanta m-2 s-1, contracted their tentacles at wavelengths of 400-540 nm. A mean period of 1-2 minelapsed after exposure to light until the full response was reached. This coral also responded to light of 660 nm (Fig. 3C). Wavelengths of 400-540 nm had a significantly different effect from wavelengths of 560-700 nm (one-way ANOVA followed by the Student's t-test; P<0.0001).
In the coral species that did respond to the light stimuli the wavelengths that were most efficient in triggering the polyp contraction were correlated with the in vitro absorption spectra of their symbiotic algae (Pearson's correlation, r=-0.8543, P<0.0001, N=5 and r=-0.7557, P<0.0007, N=5 for irradiance levels of 10 µmol quanta m-2 s-1 and 30 µmol quanta m-2 s-1, respectively) (Fig. 3A,B). In P. sinuosa, the correlation between the spectral absorbancy of the zooxanthellae and the action spectrum of tentacle contraction was significant (Pearson's correlation, r=-0.8667, P<0.0001, N=3).
The addition of DCMU did not affect the tentacle contraction response at any of the different wavelengths, however, it did block oxygen production. Tentacle contraction in the azooxanthellate coral Cladopsammia gracilis did not occur in response to illumination at any wavelength, even with light intensities as high as 400 µmol quanta m-2 s-1, regardless of wavelength. The spectral data of the separated peaks revealed that most of the major pigments have considerable absorbance between 400-540 nm, with major peaks between 440-480 nm. The widest absorbancy spectral profiles belong to the accessory carotenoid pigments, such as perdinin, diatoxanthin and diadinoxanthin, which display blue/blue-green absorption bands that partially overlap the chlorophyll absorption bands in that domain (Fig. 4).
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Highest zooxanthellar densities were found in the tentacles of Goniopora lobata (1.78±0.58x106 cells cm-2). Lower densities were found in the tentacles of Plerogyra sinuosa. No zooxanthellae were found in the tentacles of Favia favus or Stylophora pistillata (Table 1), although occasional zooxanthellae were seen when tentacles were examine under the microscope. The ratio of zooxanthellar density in the tentacles to the density in the whole coral was highest in G. lobata (Table 1). Tentacles were nearly devoid of algae in the other zooxanthellate species.
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The surface area of G. lobata was found to be 7.5±0.86
(mean ± S.D.) times higher when the polyps were expanded
than when they were contracted. Calculations of G. lobata surface
area did not take into account the trunk (which was not fully extended all the
time) of the polyps, only their tentacle crown. Measurements of the
fluorescence parameters of corals with expanded and contracted tentacles using
the FRRF instrument in the dark clearly demonstrated that minimum fluorescence
(Fo), variable fluorescence (Fv) and maximum fluorescence (Fm) all increase
when the tentacles are contracted in the two nocturnal corals F.
favus and P. sinuosa. In S. pistillata and G.
lobata no significant change in these parameters was observed when the
corals were manually touched in order to induce tentacle contraction. Of the
photosynthetic parameters, Fv/Fm did not change significantly when the polyps
became contracted in any of the four zooxanthellate species
(Fig. 5A). In F. favus
and P. sinuosa the functional absorption cross section of PSII
(PSII) was significantly lower in the expanded than the
contracted tentacles (t-test, P<0.05, d.f.=146), whereas
in G. lobata and in S. pistillata these changes were not
significant (Fig. 5B).
Measurements of the action spectrum of photosynthesis showed that maximum
chlorophyll fluorescence differences [related to the dark measurements
(
F'/Fm'-Fv/Fm)/Fv/Fm, where
F'/Fm' is
the quantum yield] were highest in the blue zone. In all four species the
lowest values were recorded when corals were illuminated with wavelengths of
540-620 nm (Fig. 6).
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Discussion |
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Expansion of tentacles with low zooxanthellae densities might lead to net
energy loss, since expansion requires energy
(Pearse, 1974;
Robbins and Shick, 1980
;
Lasker, 1981
). In addition
daytime expansion of tentacles with low numbers of zooxanthellae may lead to
an overall decrease in the photosynthetic rate, due to light scattering. Some
zooxanthellate sea anemones contain two types of specialized organs:
pseudotentacles, with a high concentration of zooxanthellae, and true
tentacles with few or no algae. The pseudotentacles expand during daylight and
are photosynthesis active. The true tentacles expand during the night and are
used for zooplankton capture (Lewis,
1984
; Sebens and Deriemer,
1977
; Pearse,
1974
; Gladfelter,
1975
). The coral Montastrea cavernosa, which has two
morphotypes, exhibits a similar type of behavior; colonies containing a dense
zooxanthellae population tend to remain open during the daytime, while
morphotypes with sparse zooxanthellae expand only during the night (Lasker,
1977
,
1979
).
We suggest that differences in algae density and their distribution within
the tissue may lead to differences in the relative contribution of their
energy sources. The relative importance of autotrophy versus
heterotrophy in a given species can be reflected in the diel behavioral
patterns of tentacle expansion and contraction. Levy et al.
(2001) showed that polyps of
Favia favus could be induced to expand under high flow velocity and
low-medium light (below the compensation point), regardless of the presence of
prey. Thus in corals with a low density of zooxanthellae in their tentacles
there is a hierarchy of responses, with light level and flow speed overruling
the presence of prey. These results probably do not apply to corals that
contain high algal densities in their tentacles (such as G. lobata),
which would benefit from expansion whenever light levels are high. Crossland
and Barnes (1977
) claimed that
polyp retraction in Acropora acuminata can be a way of avoiding light
by self-shading. They showed that the light saturation level and the
compensation point were 25% higher when polyps were contracted than when they
were partially expanded. Similarly, when contracted, Xeniids completely
stopped their oxygen evolution (Svoboda,
1978
).
FRRF measurements demonstrate that extended tentacles in nocturnal species
scatter some of the radiation. Thus, less excitation energy reaches the
zooxanthellae. As a consequence, the efficiency of chlorophyll excitation
decreases and fluorescence is reduced (Fo, Fm). PSII, the
functional absorption cross section of PSII, also decreases. The retraction of
tentacles stimulated by specific wavelengths corresponding to the algal
radiation absorbance profile therefore enhances light harvesting, and thus
increases photosynthetic performance. The increase in photosynthetic
efficiency appears to proceed without any change in the efficiency at which
the absorbed quanta are used, as indicated by the constancy of Fv/Fm, in
agreement with general photosynthetic theory; regardless of their
wavelength-dependent probability of absorption, once absorbed, all quanta are
utilized with the same efficiency. However, corals that expand their tentacles
during daylight (G. lobata and S. pistillata) did not
exhibit changes in
PSII and in the Fv/Fm parameter when the
tentacles were contracted or expanded. This may be related to the higher
zooxanthellae density in the tentacles, at least in G. lobata,
compared to the nocturnal corals. Nevertheless, in S. pistillata the
tentacles are so small (1-2 mm) that the scattering effect is minimal and it
may be assumed that this is the reason why S. pistillata colonies are
fully expanded during daytime. Salih et al.
(1995
) suggested an
alternative explanation. Coral expansion and contraction changes the density
of the fluorescence pigment in the chromatophores; at high light levels, polyp
contraction leads to denser concentrations of tissue fluorescent pigments
(FPs), forming a thicker and a quasi-continuous FP layer, which acts as an
effective sunscreen.
Our results on the effect of light spectrum on tentacle contraction
behavior in F. favus and P. sinuosa, and the absence of this
effect in azooxanthellate corals, support the notion that this behavior is
related to the photosynthetic activity of the zooxanthellae. FRRF measurements
indicated that the two species that contract diurnally have a significantly
lower photosynthetic performance when their tentacles are expanded than when
they are contracted. In G. lobata and S. pistillata there is
no such significant change in photosynthetic performance, regardless of their
tentacle state. We assume that the expansion/contraction behavior of the
tentacles acts as a shutter, optimizing the photosynthesis of the coral
colony. Maximum photobehavior response is in the blue/green zone, which
matches the maximum transparency of oligotrophic tropical waters
(Jerlov, 1968). Although clear
sense organs such as photoreceptors are not known in corals, Gorbunov and
Falkowski (2002
) have recently
suggested that corals exhibit the absorption spectra of rhodopsins isolated
from a number of marine invertebrates. It is usually accepted that these
pigments indicate sensitivity to light, which is not mediated by any known
receptor in Anthozoa (Martin,
2002
), but is presumably associated with neurons concentrated just
beneath the translucent surface of the epidermal cells. Our results seems to
point to a causative relationship between the photosynthesis of the
zooxanthellae (or the products thereof) and tentacle behavior in corals, but
cannot totally exclude the possibility that such cells are sensitive to the
same wavelengths as the photosynthesis, and may also play a role in coral
behavior.
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Acknowledgments |
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