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First published online February 13, 2009
Journal of Experimental Biology 212, 662-667 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.022624
Phototropic growth in a reef flat acroporid branching coral species
1 ARC Centre of Excellence, The University of Queensland, Centre for Marine
Studies, St Lucia, QLD 4072, Australia
2 Queensland Department of Primary Industries and Fisheries, Horticulture and
Forestry Science, Indooropilly Research Centre, QLD 4068, Australia
3 Faculty of Life Sciences, Bar-Ilan University, The Interuniversity Institute
for Marine Science, Eilat, POB 469, Eilat 88103, Israel
* Author for correspondence (e-mail: p.kaniewska{at}uq.edu.au)
Accepted 9 December 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: axial polyp differentiation, coral morphology, light quantity, light quality, Acropora pulchra
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Pigliucci, 2005). In plants,
variations in crown architecture as a response to uneven light environments
results in maximizing light capture and photosynthesis in shaded habitats and
minimizing photoinhibition in high light habitats
(Pearcy et al., 2005). Many
scleractinian corals have highly variable colony morphologies (e.g.
Willis, 1985;
Bruno and Edmunds, 1997;
Muko et al., 2000) with
branching corals showing morphological plasticity in response to differing
environmental conditions, such as water motion
(Kaandorp et al., 2005) and
ambient light levels (Muko et al.,
2000). Changes in colony geometry of branching corals are
influenced by the frequency, location and direction of new branch initiation
and growth. Most acroporid branching species have specialized corallite
structures, axial corallites, which are formed as a consequence of polyp
differentiation at the branch tip, and are an area where linear branch
extension occurs (Oliver et al.,
1983; Oliver,
1984; Veron,
2000). The differentiation of an existing radial polyp into an
axial polyp and the resulting axial corallite formation leads to the
initiation of a new branch and therefore a new direction of growth
(Oliver, 1984). The
developmental signals of axial corallite formation and possible environmental
cues involved in this axial corallite development are unknown.
Corals form a symbiosis with photosynthetic dinoflagellates (genus
Symbiodinium), which may be a critical factor in the success of
scleractinian corals in the nutrient-poor tropical oceans
(Muscatine and Porter, 1977).
Given the central role of photosynthesis in supplying the energetic needs of
corals and their symbionts, light plays a key role in the biology and
development of corals. Similar to plants, corals need sufficient external
light intensities to have enough energy for survival, growth and reproduction
(Chalker et al., 1983;
Anthony, 1999) while minimizing
the chances of photoinhibition and photodamage
(Jones and Hoegh-Guldberg,
2001). It is common for terrestrial plants to use plant geometry
and physiology to optimize their photosynthetic response (reviewed by
Herbert, 1996). Similarly,
scleractinian corals can manage the availability of light to their symbiotic
dinoflagellate through a range of mechanisms, such as polyp contraction
(Brown et al., 2002;
Levy et al., 2003), use of
antioxidant enzymes (Brown et al.,
2002) and light absorption by fluorescent and non-fluorescent
pigments (Salih et al., 2000;
Dove, 2004). With changing
light levels, the symbiotic dinoflagellates can change in density within the
host and change the amount of photosynthetic pigments they contain (e.g.
Falkowski and Dubinsky, 1981;
Iglesias-Prieto and Trench,
1997). Colony morphology is also important for maintaining optimal
light levels within the colony (Anthony et
al., 2005), and fine-scale changes in mesostructure (e.g. septa,
columella and dissepiments) can have major influences on the amplification of
low light levels (Enriquez et al.,
2005). Colony morphology of branching coral species can be highly
complex (Kaandorp et al.,
2005) and branching corals may use their colony morphology to
optimize within-colony irradiance levels
(Kaniewska et al., 2008).
As colony morphology represents a strategy for manipulating within-colony
light levels, light may be an important environmental cue in axial corallite
development, as it would influence the direction of new branch growth.
Phototropism, where an organism will alter growth patterns in response to
light direction, is common among plants
(Iino, 1990). Terrestrial
plants also have differing responses to various wavelengths of light.
Phytochrome photoreceptors in green plants respond to far red light and
initiate stem elongation in response to low light levels
(Khattak et al., 2004). Plants
also have blue light receptors, cryptochromes, which elicit a directional
growth response towards light (Ahmad et
al., 1998). In corals, changes in light quality and intensity
result in changes in photosynthesis
(Kinzie and Hunter, 1987),
Symbiodinium growth rates (Kinzie
et al., 1984), GFP-like protein concentrations
(D'Angelo et al., 2008) and
coral settlement behaviour (Petersen et
al., 2005).
The underwater light environment for corals is different from that of
terrestrial plants, as light attenuates with depth as a result of absorption
and scattering by dissolved and suspended material, as well as phytoplankton
(Kirk, 1994). Light
attenuation in the water column is not uniform across the spectrum, the blue
part of the spectrum experiences the least attenuation whereas longer
wavelengths attenuate quickly with depth. The spectral attenuation is affected
by water type, as attenuation will occur more rapidly in turbid waters
(Kirk, 1994). The
coral–algal complex contains pigments that absorb in the blue and red
region for light harvesting
(Iglesias-Prieto and Trench,
1997) and there are also host pigments that absorb in the green
spectrum (Dove, 2001). In
order for the coral to respond to a possible light cue and change growth
morphology, it must be able to detect changes in light by possessing
light-sensing photoreceptors. To date only blue-light-sensing photoreceptors,
cryptochromes that are also found in plants, have been found in corals
(Gorbunov and Falkowski, 2002;
Levy et al., 2007). In
addition, physiological and biochemical responses to blue light have been
documented (Levy et al.,
2006). Given that the underwater environment is dominated by the
blue part of the light spectrum, it can be expected that if a light cue exists
for axial corallite development, and therefore branch initiation in acroporid
branching corals, it will operate in the blue part of the light spectrum.
Acropora pulchra Brook 1891, is a complex branching coral common in shallow waters. It develops distinct axial polyps which deposit axial corallites, a corallite structure from which branch extension occurs, at the tip of the branches. The aim of this study was to determine if light serves as a cue for axial corallite development, and to understand the role of light intensity and quality in this development.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Branches were left to grow in aquaria for 8 weeks. A pilot study demonstrated that this was enough time for A. pulchra branches to develop axial corallites (data not shown). After 8 weeks, branch lengths were measured and branches were re-photographed to record direction of axial corallite development (proximal or distal or both), lateral branch growth and overall branch health. The amount of axial corallite growth at the cut surfaces at both ends of a branch was calculated from the photographs.
Effect of light quantity and quality on axial corallite development
To test the influence of light quantity and quality on axial corallite
development, light intensity and quality were manipulated in a field
experiment. Branches (288x7 cm to 8 cm) were collected from 16 healthy
Acropora pulchra colonies on Heron Island reef flat
(23°33'S, 151°54'E), Great Barrier Reef, Australia. The
axial corallites were removed from the branches by cutting with side cutters
approximately 1 cm from the branch tip. Two branches were placed 1 cm (distal
end down) into underwater cement in diagonally opposite cells, of 12
cmx12 cm four-cell seedling trays. A replicate consisted of one seedling
tray (two branches; Fig. 1).
The branches were photographed and initial branch lengths were recorded. The
seedling trays were attached to one of four underwater frames
(Fig. 1) for exposure to a
range of light treatments. Each frame had four replicates of light quantity
treatments of 0, 30, 50, 80 and 100% light reduction (using shade cloth or
opaque black plastic), and four replicates of light quality treatments of
clear (acetate sheet), blue (408–508 nm), red (618–700 nm) and
green (482–554 nm) filters (nos 132, 124 and 026, respectively, from LEE
Filters, Burbank, CA, USA; Fig.
2). Each of the 36 treatments per frame were widely spaced and
randomly assigned, to minimize effects of potential differences in flow among
positions. The materials used for the various treatments were made into open
bottomed boxes approximately 15 cm square with sides of approximately 3 cm.
These were fixed to wire mesh (10 cm square) and suspended above the seedling
trays to leave approximately 3 cm of the coral branch bases exposed to light
and water movement (Fig. 1).
This would minimize water flow differences among positions within the frame
and allow some light for branches in dark treatments, to avoid branch
mortality.
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Coral branches were left to grow for 8 weeks, after which branch lengths were recorded and the amount of vertical axial corallite growth at the cut surfaces was determined by calculating the difference between initial and final branch lengths. Branches were also photographed as a record of the potential lateral encrusting growth at the base, new lateral branch formation and overall branch health (including recovery from handling effects).
Ambient downwelling irradiance (photosynthetically active radiation, PAR)
next to the frames was recorded underwater in situ using underwater
light loggers (Odyssey, Z412, Christchurch, New Zealand). The logger, a 2
cosine-corrected light sensor was calibrated against a manufacturer-calibrated
sensor (Li-cor, LI-192S). In addition, a spectral scan was performed
underwater at 4 m at the site of the experiment, on a cloudless day at noon,
using a USB2000 spectrometer (Ocean Optics, Dunedin, FL, USA; bandwidth of
200–850 nm in a custom-made underwater housing) via an attached
optic fibre.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Effect of light quantity and quality on axial corallite development
During this study the mean daily ambient irradiance level was
225.9±5.8 µmol m–2 s–1 (mean
± s.e.m.), whereas the mean maximum daily irradiance was
409.2±10.2 µmol m–2 s–1 (mean
± s.e.m.). A spectral scan at the site of the experiment together with
the spectral characteristics of the filters showed that there was 15% less PAR
under the red filter than under the blue and green filters. This was confirmed
by PAR measurements performed in situ under the three coloured
filters at 4 m. The transmission rate of the clear filter was 95% in the PAR
region.
Differences in axial corallite growth among light reduction treatments were detected (nested ANOVA, F52,42=2.78, P<0.001). Assuming the mean daily ambient irradiance during the length of the experiment reported above, light reduction treatments of 0, 30, 50, 80 and 100% would equate to a mean daily ambient irradiance of 226, 158, 113, 45 and 0 µmol m–2 s–1, respectively. The greatest axial corallite growth was found in the control treatment, where there was a threefold increase in axial corallite growth compared to the 30% and 50% light reduction treatments. There was a twofold increase in axial corallite growth between the 30% and 50% light reduction treatments and the 80% and 100% light reduction treatments (Fig. 5A). The values reported for the 80% and 100% light reduction treatments corresponded to growth associated with live tissue and polyp regeneration over the exposed skeleton, but no axial corallite development.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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).
Here we found a similar response for the reef-building coral Acropora
pulchra, where the growth of axial corallites towards available light
provides evidence that light is an important cue for the development of this
coral structure and is therefore similar to plant directional morphogenesis.
This confirms previous findings that axial corallites in Acropora
formosa, which were exposed to shaded environments, did not grow and
eventually reverted back to radial corallites
(Oliver, 1984). In addition,
in the current study there was development of axial corallites at the distal
end of a branch, where previous axial corallites were not present. This shows
that this is not just regeneration of an axial corallite, but a developmental
response towards light. There were no differences in growth rates between
axial corallites regenerated at the proximal end and newly developed ones at
the distal end of the branch (data not shown).
In most acroporid coral species branch extension only occurs in axial
corallites (Oliver et al.,
1983; Oliver,
1984), where the highest growth rate is present
(Fang et al., 1989), therefore
the position where a radial corallite differentiates into an axial corallite
will determine the direction of the new branch growth. Growth towards light
(positive phototropism) is advantageous for photosynthetic organisms such as
corals and their symbionts (Porter et al.,
1984). In terrestrial plants, shade avoidance is well known, with
a complex set of physiological behaviours triggered by specific wavelengths of
light resulting in an increased likelihood of light availability
(Iino, 1990). The underwater
light environment experienced by corals is different from the terrestrial
light environment that many plants are exposed to. One of these differences is
that in water the light field as a function of depth, becomes more diffuse and
omni directional (Kirk, 1994).
However, the acroporid species investigated in this study grows on reef flats
and shallow reef slopes and is therefore exposed to more directional light,
with exposure to almost direct sunlight at low tide. Therefore the directional
light environment for this branching coral may be comparable to that of
terrestrial plants. The directional growth towards light found in this study
is similar to the terrestrial plant shade-avoidance strategy. As linear branch
extension occurs in the axial corallite for most acroporid coral species, it
can be argued that branch extension and secondary branch development in a
colony is towards the light, as shaded parts of the A. pulchra colony
and branches do not develop axial corallites.
In the field experiment, variability in light intensity influenced the
axial corallite regeneration. The existence of a threshold, above which an
axial corallite is regenerated, may represent a minimum light level, below
which is considered as potential shade areas, and therefore the coral does not
develop an axial corallite, to preclude growth in the direction of low light.
It has been suggested that photosynthetic organisms acclimate to a mean
irradiance as opposed to instantaneous irradiances
(Chabot et al., 1979;
Falkowski and Raven, 1997).
The threshold here was found to be <80% light reduction, which at 4 m at
Harry's Bommie represents a mean daily light level of <45µmol
m–2 s–1. An optimal irradiance level for
corals is where the light harvested equals the turnover rate of photosystems,
quantified by the subsaturating irradiance of the
photosynthesis–irradiance relationship
(Falkowski and Raven, 1997).
This has been estimated for foliose corals to be between 150–370µmol
m–2 s–1
(Anthony et al., 2005), whereas
a hypothetical lower limit for reef distribution has been suggested to be
50µmol m–2 s–1
(Kleypas et al., 1999). The
threshold for axial corallite development seems to adhere to the latter value.
Acropora pulchra is a shallow-water species, which is most abundant
between 0–5 m (Wallace,
1999; Veron, 2000)
and has therefore adapted to higher irradiance levels. Values below 45µmol
m–2 s–1 could be considered as potential
shade areas by this species, although this threshold value may not be optimal
for many coral species with a larger depth range.
A spectral scan at the site of the field experiment
(Fig. 2) revealed that there
was still a substantial amount of red light present at the site. Light
attenuation will vary across water types where the depth of the ocean floor is
greater than the depth of the light penetration, and water types where the
ocean floor depth is less than the light penetration potential
(Mobley, 1994; Ackelson,
2003). In such optically shallow waters the inherent optical property of the
water column will be affected by the benthic substrate
(Boss and Zanevald, 2003). This
could explain the spectral scan in Fig.
2, as the site has a large percentage cover of sand, and so the
light is highly reflected and less attenuation occurs at that depth compared
to attenuation across wavelengths that might occur in other water types such
as oceanic waters (e.g. Maritorena et al.,
1994; Boss and Zanevald,
2003; Voss et al.,
2003; Zanevald and Boss,
2003).
In higher plants, phototropism – the directional growth and bending
towards light – is triggered by blue light
(Iino, 1990) and is mediated
by cryptochrome photoreceptors (Ahmad et
al., 1998). In the current study, a similar phototropic behaviour
was found in reef-building corals, where axial corallite growth was only
initiated by blue light (408–508 nm), adding to the similarities between
the two photosynthetic organisms. The difference between axial corallite
growth under the clear filter compared to the 0% light reduction treatment
(Fig. 5) is probably due to
minor fouling of the clear filter, which occurred despite regular cleaning of
the filters. Considering that blue wavelengths of light are dominant in the
water column (Kirk, 1994), and
evidence of the same blue photoreceptors (cryptochromes) in corals
(Gorbunov and Falkowski, 2002;
Levy et al., 2007) as in
terrestrial plants, it is understandable that the axial corallite development
occurred in the blue light treatment. Apart from phototropism, plants have
many behavioural responses to blue light, including leaf and cotyledon
expansion, petiole elongation, promotion of flowering and inhibition of
hypocotyl elongation (Ahmad et al.,
1998). Similarly corals have many reported physiological responses
to blue light and this study adds another blue light response. Other studies
have shown that coral polyp tentacle behaviour responded to the blue zone of
the spectrum (Levy et al.,
2006), coral larvae can have settlement preferences for areas
treated with blue light (Petersen et al.,
2005), coral respiration rates can increase in response to the
blue part of the spectrum (Kinzie and
Hunter, 1987), symbiotic dinoflagellates can have higher growth
rates under blue light (Kinzie et al.,
1984) and blue light can regulate GFP-like protein concentrations
(D'Angelo et al., 2008). The
species used in this study, however, is a reef flat species, living high up in
the water column where the smallest attenuation of red and green light occurs.
If any coral were to respond to red or green wavelengths, it should be a reef
flat species. It is expected that if coral species migrated down the water
column during evolution, then basic responses such as phototropic growth,
should still be sensitive to the red and green parts of the spectrum. This was
not the case for Acropora pulchra, which perhaps reflects the fact
that this coral species, has over time evolved to migrate up the water column
to the reef flat, instead of, from the reef flat down the water column.
Overall, the growth of Acropora pulchra branches over an 8 week
period in this field study was comparable to that reported for Acropora
formosa transplantation experiments. For A. formosa at 5 m, the
mean yearly extension rate was 8 cm per year
(Oliver et al., 1983), which
for 2 months, would be 1.3 cm assuming a constant light regime. In another
study, extension rates of white axial corallite tips in A. formosa
were on average 0.75 cm over 30 days
(Oliver, 1984) which for 8
weeks would be 1.5 cm. The current study measured regeneration growth of axial
corallites and linear extension from these cut surfaces. Axial corallite
extension in full light conditions was, on average, 1.2 cm over 8 weeks
(Fig. 5). Considering that
branches in this study had to invest energy to repair the cut surfaces at the
top and redevelop axial corallites, these are comparable values.
In the field experiment, light was available to the middle part of the branch, but not the proximal and distal end of the branch. Overall, the available energy should have been sufficient to support regeneration at the cut surface and further growth of the branch if the treatment conditions stimulated tip growth. This was the case, for even in the 100% light reduction treatment there was regeneration and repair of tissue at the cut surface, but no axial corallite development was induced. In light-reduction treatments in the field experiment, parts of the branch near the base exposed to light grew and extended towards the light, either as a new secondary branch or lateral encrusting growth over the base of the cement.
This study showed that axial corallite development and therefore branch initiation in Acropora pulchra, shows a directional growth response towards light, reminiscent of the phototropic response in terrestrial plants. Similar to plants this growth response was triggered by the blue part of the spectrum, which also is the dominant light environment for corals. These results indicate that perhaps light is one of the critical factors structuring coral colony architecture in A. pulchra, which may also be true for many shallow water acroporid coral species.
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Footnotes |
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