BULLETIN OF MARINE SCIENCE. 88(4):1019–1033. 2012
http://dx.doi.org/10.5343/bms.2011.1084
coral reef paper
Macroalgae on shallow tropical reefs
reduce the availability of reflected light
for use in coral photosynthesis
Nicholas B Colvard and Peter J Edmunds
Abstract
We tested the hypothesis that light reflected from dense growths of macroalgae
[i.e., a low reflectance (LR) surface] vs heavily grazed surfaces [i.e., a high reflectance
(HR) surface] has no effect on the photophysiology of scleractinian corals on the
shallow (3-m depth) back reef of Moorea, French Polynesia. Underwater light was
measured using a cosine-corrected sensor that detected photosynthetically active
radiation (PAR, between 400 and 700 nm), and an underwater spectrophotometer
that measured spectral reflectance, R(λ), with nanometer wavelength resolution.
The effect of reflected light on corals was assessed by incubating small colonies of
massive Porites spp. and Pocillopora verrucosa (Ellis and Solander, 1786) for 27 d on
artificial HR and LR surfaces, and measuring the effective photochemical efficiency
(ΔF⁄ Fm') of Symbiodinium on the sides of colonies adjacent to the benthos. At noon
on a cloudless day, upwelling photon irradiance (Eu) from the benthos was reduced
20% over LR vs HR surfaces, and LR surfaces reduced R(λ) 50%–60% for PAR. For
massive Porites spp., ΔF⁄ Fm' did not differ between HR and LR surfaces, but for P.
verrucosa, ΔF⁄ Fm' increased 60% on LR compared to HR surfaces. The increase in
ΔF⁄ Fm' suggests that P. verrucosa modifies its photophysiological performance in
tissue adjacent to LR surfaces to increase the efficiency with which light can be
utilized in photochemical pathways.
One striking change affecting coral reefs over the last half century has been the
widespread decline in cover of scleractinian corals (Gardner et al. 2003, Bellwood et
al. 2004, Hughes et al. 2011), and a shift to dominance by alternate taxa (Bruno et al.
2009, Norström et al. 2009), typically macroalgae (McManus and Polsenberg 2004,
Aronson and Precht 2006). While documentation of these trends has featured prominently in coral reef literature (Pandolfi et al. 2005, Kuffner et al. 2006, Norström et
al. 2009), these efforts have overlooked the significance of alternate taxa in altering
the color (i.e., the reflective properties) of the benthos relative to reefs that are heavily
grazed (e.g., fig. 5 in Hoegh-Guldberg et al. 2007).
On reefs dominated by scleractinians, space on hard substrata that is not occupied
by coral is typically exploited by algal turf (Carpenter 1986, Tanner 1995), crustose
coralline algae (CCA; Klumpp and McKinnon 1992), or sessile invertebrates
(Chadwick and Morrow 2011, Colvard and Edmunds 2011). The benthos on such
reefs is generally distinguished by pastel-colored corals, pale branch apices and
coral colony margins (Fabricius 2006), and pink CCA. In contrast, a reef dominated
by macroalgae has dense growths of a variety of algae that can include Amansia,
Dictyota, Halimeda, and Sargassum (Connor and Adey 1977, Adjeroud and Salvat
1996, Adjeroud 1997, McClanahan et al. 1999) that are dark as a result of brown
(Phaeophycea) and green algae (Chlorophycea) pigments.
Bulletin of Marine Science
© 2012 Rosenstiel School of Marine & Atmospheric Science of
the University of Miami
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Remote sensing of coral reefs has enabled the description of regional-scale differences in the benthic community structure based on the reflective characteristics of
the benthos (Dickey et al. 2006, Lesser and Mobley 2007, Hochberg 2011). In contrast, in situ analysis of underwater light using spectrometry equipment has allowed
underwater light microenvironments to be quantified on a submeter scale (Lesser
2000, Joyce and Phinn 2003). At this scale, light microenvironments are created by
the attenuation and reflectance of sunlight at the air-water interface (Wilkinson
2004), the optical properties of seawater (Smith and Mobley 2008), the topographic
complexity of the reef surface (Dove et al. 2008), and differences in the reflectance
of benthic organisms (Adjeroud and Salvat 1996, Hochberg et al. 2003, Werdell and
Roesler 2003, Hochberg 2011, Kaniewska et al. 2011). Although reflectance of benthic surfaces is likely to have a strong effect on the ambient light regime of shallow
marine environments, these effects pose challenges for measurement because underwater reflectance is subject to high variability attributed to a diversity of biological agents and physical principles (Maritorena et al. 1994, Joyce and Phinn 2003).
Thus, empirical measurements of underwater reflectance are valuable in describing
relative differences among treatments, but they do not provide absolute measures
that can be extrapolated directly to other systems.
Brakel (1979) was among the first to describe depth-dependent light attenuation on
a coral reef, and his analysis revealed the potential for variation in the angular distribution of irradiance to affect coral photosynthesis. Though the acclimatization of
corals to different irradiances has been studied for decades (Redalje 1976, Falkowski
and Dubinsky 1981), the response of corals to varying light regimes continues to
be a rich field for investigation (Ulstrup et al. 2006, Mass et al. 2010, Dubinsky and
Falkowski 2011). However, recent changes in the community structure of coral reefs
may provide a new context for such studies because the declines in coral cover that
have taken place over the last few decades (McCook 1999, Bruno et al. 2009) lead to
changes that affect the way light interacts with the benthos. For instance, the loss of
coral favors a reduction in three-dimensional structure (McManus and Polsenberg
2004, Alvarez-Filip et al. 2009) that reduces the availability of light microenvironments, and often leads to an increased abundance of macroalgae that alters the light
available to corals beneath their canopy (Birrell et al. 2008). Changes in the community structure of coral reefs also are likely to affect the reflectance of the benthos,
yet this topic has not been investigated in detail (but see Maritorena et al. 1994, Joyce
and Phinn 2003). Given the importance of light to tropical corals (Dubinsky and
Falkowski 2011), it is likely that changes in the underwater light regime attributed to
benthic reflectance will influence coral performance.
The goals of the present study were to test the effects of benthic macroalgae in
altering the light regime on a coral reef, and to determine whether these effects influence the photophysiology of reef corals. First, light reflected from benthic surfaces
on a shallow reef was characterized through a contrast of areas at a single depth
that were dominated either by macroalgae [hereafter, defined as a low reflectance
(LR) surface] or coral, CCA, and carbonate pavement [hereafter, defined as a high
reflectance (HR) surface]. Second, the effect of LR and HR surfaces on the effective
photochemical efficiency of PSII (ΔF⁄ Fm') of Symbiodinium within corals was quantified with the objective of evaluating how differences in irradiance (the radiant flux
density emanating from a surface per unit solid angle, after Campbell and Norman
1998) and spectral reflectance (the ratio of reflected radiant flux to incident radiant
colvard and edmunds: change in spectral composition of reef from macroalgae
1021
flux; Hochberg et al. 2003, Kaniewska et al. 2011) affect coral photophysiology. We
define light microenvironments on a scale of centimeters-to-meters for both downwelling and upwelling photon irradiance (i.e., reflected) from the substratum, and do
not address large-scale (i.e., over kilometers) processes that are typically described by
remote sensing techniques (Lesser and Mobley 2007, Hochberg 2011).
Methods
Study Sites and Environment.—Downwelling photon irradiance, Ed, upwelling photon
irradiance, Eu, and relative spectral reflectance, R(λ) (Mobley 1994, Mobley and Sundman
2003), from benthic surfaces were measured on a shallow (3-m depth) back reef on the north
shore of Moorea, French Polynesia (17°30´S, 149°50´W). Between 2005 and 2007—just before
the present analysis was conducted—this habitat was characterized by low-profile carbonate
pavement where 6%–68% of the benthos was sand, 14%–39% a combination of CCA and
bare space (that often cannot be distinguished reliably in digital images), <17% turf, and <2%
macroalgae (Edmunds et al. 2010). Coral bommies are spread throughout this habitat, and on
these surfaces coral cover reaches 8%–43% (Edmunds et al. 2010) and is composed mostly of
Porites spp. (6%–30% cover), Montipora spp. (0%–27% cover), and Pocillopora spp. (0%–6%
cover; Adjeroud 1997, Edmunds et al. 2010). Dense aggregates of the macroalgae Amansia
rhodantha (J. Agardh, 1841), Sargassum spp., and Turbinaria ornata (J. Agardh, 1848) are
scattered among the coral colonies (Adjeroud and Salvat 1996, Adjeroud 1997).
Downwelling and Upwelling Photon Irradiance.—We defined Ed as the rate of incident radiant energy received in quanta m−2 s−1, and Eu as the energy reflected per unit per
time (quanta m−2 s−1) from a given surface (e.g., light reflected from the substratum; Mobley
1994). The underwater light regime was recorded at 3-m depth using a cosine-corrected photosynthetically active radiation (PAR) sensor fitted to a pulse amplitude modulation fluorometer (Diving PAM, Waltz, GmbH) and calibrated against an underwater quantum sensor
(LI-192, LI-COR, Lincoln, Nebraska, USA). The light sensor on the Diving PAM was used to
measure the Ed (μmol quanta m−2 s−1) in the PAR range. PAR was recorded from 12:00 to 13:00
hrs on nine cloudless days from 23 April to 20 May, 2009, with the cosine-corrected sensor
oriented first, at 0° from vertical to record Ed, and second, at 135° from vertical to quantify Eu.
To complete these measurements, the PAR sensor was held approximately 10 cm above the
benthos, and recordings were made from locations selected at random on benthic surfaces.
Twenty such recordings were made for both the 0° and 135° orientations and were made above
a contiguous area of reef extending over approximately 20 m 2. Using this procedure, for each
day that measurements were made (n = 9 d), there were approximately 20 recordings of Ed and
Eu collected for each orientation of the sensor. These measurements were used to characterize
Ed as well as the light reflected from each substratum type (e.g., HR and LR surfaces) and were
used to characterize the underwater regime of PAR levels within the back reef. Multiple recordings every day were necessary to reduce the variability in the measured underwater irradiance due to light scattering and attenuation from the water column (Maritorena et al. 1994).
Underwater Relative Spectral Reflectance.—To evaluate R(λ) (radiance integrated
over unit wavelength; Campbell and Norman 1998, Kaniewska et al. 2011) of benthic surfaces
at 3-m depth, a spectrophotometer (USB2000, Ocean Optics, Dunedin, FL, USA) was operated from a laptop computer (Asus Eee, Taipei, Taiwan), running OOIBase32 software (Ocean
Optics, Dunedin, FL, USA). This instrument was contained in a custom underwater housing
and connected using a vacuum feed-through (Ocean Optics, Dunedin, FL, USA) to a 2-m
long, 400-µm diameter fiber optic cable. This cable was used to sample light reflected from
HR and LR surfaces with 0.33 nm wavelength resolution between 400 and 700 nm (i.e., PAR).
The spectrophotometer used a 2048-element linear silicon CCD array detector to quantify
photons of light separated by wavelength, and was configured to integrate light over 4 ms. The
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manufacturers settings were used to generate a single spectrum from the average of five consecutive discrete spectral acquisitions, with each spectrum smoothed using a moving average
derived from the intensities at six wavelengths. R(λ) was measured using the “scope mode” of
the instrument, which displays the spectral irradiance in raw arbitrary counts for each pixel
in the array, scaled from 0 to 4000. To account for changes in sunlight intensity, the spectrophotometer signal was adjusted to the current light condition using both a dark reference (a
spectrum taken with the light path blocked) and a white reference (a diffuse reflectance standard of matte white plastic) prior to all R(λ) measurements.
To quantify R(λ), the fiber optic cable was positioned in a holder that supported the tip of
the sensor 1.0 cm above the substratum and at 135° from vertical (Fig. 1), so that measurements were not affected by the shadow of the operator (Mazel 1997). The collection angle of
the sensor was 26.5°, and thus light intercepted by the downward-pointing sensor was reflected entirely off the benthos. The light sensitive tip of this sensor was not fitted with a cosine-corrected filter, as is customary for measurements of reflectance in bio-optical literature
(Dickey et al. 2006, Smith and Mobley 2008) because we sought to use the narrow collection
angle of the instrument to sample small areas (0.80 cm2) of benthos. This was advantageous
because it ensured that the sensor measured light emitted from the surface at which it was
pointed, rather than harvesting light over a larger collection angle and surfaces other than
that of interest.
One limitation of measuring light using a sensor with a narrow collection angle is that it
samples light from a small area, particularly when it is close to the surface of interest. On
surfaces with a high degree of reflectance heterogeneity, a small sampling area could result
in measurements of R(λ) having a high variance. However, in our application, preliminary
experiments revealed that the reflectance of reef surface were relatively homogeneous on the
scale investigated, with measurements of R(λ) differing by <15% for multiple placement of the
sensor over substrata that were selected to represent a single benthic category.
R(λ) of HR and LR surfaces was quantified on 13 and 15 May, 2009, with measurements
taken between 11:00 and 14:00 hrs to reduce the solar zenith angle and lessen the possibility
of shading from adjacent objects. Six replicate scans of reflected light from each substratum
were generated daily, with each replicate composed of five sequential smoothed scans (each
lasting 5–7 s) that were averaged by wavelength. Averaging at this stage reduced the variability in underwater irradiance caused by light flecking, surface ripples, and probe placement
(Barron et al. 2000, Devlin et al. 2008, Smith and Mobley 2008). R(λ) (dimensionless) was
calculated following Kaniewska et al. (2011) using:
R(λ) = (I − Id) ⁄ (I0 − Id) (Eq. 1)
where I = sample measurement, and Id = dark reference standard, and I0 = white reference
standard. This calculation of R(λ) accounted for variability in the ambient light environment,
and relies on measurements of in arbitrary units. R(λ) is presented as percent reflectance,
calculated as R(λ) × 100% (Chittka et al. 1994). R(λ) was measured with sequential determinations of (I − Id) and (I0 − Id), which was dictated by instrument limitations; all spectral measurements were recorded <5 s apart.
Manipulative Experiment.—Juvenile colonies (≤40-mm diameter) of massive Porites
spp. (as described in Edmunds 2008) and small branches (50–80 mm long) of Pocillopora
verrucosa (Ellis and Solander, 1786) were used to test the photophysiological response of
corals to HR and LR surfaces. Massive Porites spp. and P. verrucosa were chosen because they
are common in the back reef of Moorea (N Colvard, pers obs).
Juvenile massive Porites spp. and branch tips of P. verrucosa were collected from 3-m depth
in the back reef on 20 April, 2009, and prepared as nubbins (Birkeland 1976). Colonies of
massive Porites spp. were assumed to be genetically unique as they originated from the settlement of planula larvae of sexual origin; genetic independence of P. verrucosa branches was
sought by collecting one branch per colony. Twenty massive Porites spp. and 20 branches of
colvard and edmunds: change in spectral composition of reef from macroalgae
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Figure 1. Diagram showing the sources of light affecting small corals, and the position of the sensors used in the analysis of light and photophysiological performance. In the shallow back reef of
Moorea, small corals receive light from (A) downwelling and (B) reflective sources, both of which
were quantified with a cosine-corrected quantum sensor. To analyze the spectral composition of
light, the tip of the sampling cable of the spectrophotometer was positioned at 135° from the vertical axis to sample light reflected off the benthos (C). To measure photophysiological performance,
the sensor of the Diving PAM was positioned approximately 2 cm above the benthos on the side
of corals [i.e., on marginal tissue (D)] to measure effective photochemical efficiency of PSII of
Symbiodinium (ΔF⁄ Fm’). The high reflective surface is representative of a sandy or carbonate reef
rock substratum, whereas the low reflective surface is representative of a substratum dominated
by macroalgae.
P. verrucosa were prepared as nubbins and assigned haphazardly to one of two treatments
contrasting the effects of LR and HR surfaces. Immediately following collection, corals were
placed in a shaded aquarium at the UC Berkeley Richard B Gump South Pacific Research
Station to prevent photophysiological stress attributed to exposure to surface light intensities. Corals were fastened to 100-cm2 acrylic plates (one per plate) painted with matte paint
to mimic the light reflected from natural LR and HR surfaces in the back reef. LR plates were
painted brown to mimic Turbinaria ornata (J. Agardh, 1848), one of the dominant macroalgae in the back reef of Moorea (Adjeroud and Salvat 1996, Adjeroud 1997; RC Carpenter, CSU
Northridge, pers comm), and HR plates were painted light beige to mimic heavily grazed
reef surfaces and carbonate pavement. To evaluate the effectiveness of these mimics, R(λ) of
painted plates was compared to the corresponding natural surfaces by a randomized block
ANOVA, with sampling days treated as a block, and surfaces a fixed factor.
On 23 April, 2009, the acrylic plates and attached corals were nailed in positions selected
haphazardly in a 20-m2 area of carbonate pavement at 3-m depth in the back reef of Moorea.
On 20 May, 2009 (after 27 d of treatment), ΔF⁄ Fm' of the coral nubbins on each surface was
evaluated. ΔF⁄ Fm' is calculated from (Fm' − F') ⁄ Fm', where Fm' is the maximal fluorescence yield
in actinic light, and F' is the fluorescence yield in actinic light (Cosgrove and Borowitzka
2010). ΔF⁄ Fm' measures the efficiency of light energy utilization by PSII in a light-adapted state,
and it was measured using a Diving PAM (Walz, GmbH), fitted with a fiber optic probe (5.5mm diameter) supported by an aluminum clip that held the sensor tip 1.0 cm above the coral
tissue and at 60° to the sample plane. The settings of the Diving PAM were held constant
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at a gain of 6 and a measuring intensity of 6 for all recordings, and all measurements were
completed on a single day between 12:00 and 13:00 hrs to reduce the effect of variation in
short-term light history prior to sampling (Brown et al. 1999, Kaniewska et al. 2008). To standardize the measurements of ΔF⁄ Fm' with regard to treatments, measurements were taken on
the sides of the nubbins, approximately 2 cm above the acrylic plate (hereafter described as
“marginal” tissue). This position was selected to detect a photophysiological response of the
Symbiodinium to the light reflected from the adjacent substrata. Downwelling irradiance, as
well as Symbiodinium genotypes, can vary across the surface of coral colonies (Rowan and
Knowlton 1995, Iglesias-Prieto et al. 2004, Dove et al. 2008), and therefore the results of the
present analysis are likely to apply only to coral tissue on the margins of the colony.
Statistical Analysis.—To describe the light reflected from natural surfaces, R(λ) for HR
and LR surfaces was integrated within five wavelength bins selected to characterize the absorptivity of the photosynthetically active pigment chlorophyll a (420–440 and 650–670 nm),
as well as the accessory pigments of Symbiodinium (Jeffrey and Haxo 1968): xanthophylls
(440–460 nm), carotenoids (520–540 nm), and phycobilins (570–590 nm). This analytical
approach is similar to that used to quantify the color of flowers through R(λ) (Chittka et al.
1994, McEwen and Vamosi 2010). For the purposes of the present study we used three wavelength bins to detect variation in R(λ) that was biologically meaningful to Symbiodinium.
R(λ) was compared between HR and LR surfaces using a randomized block ANOVA, in which
sampling day was treated as a block, and surfaces a fixed factor. The same statistical model
was used in the manipulative experiment to compare the R(λ) of the HR and LR acrylic tiles.
A one-way ANOVA was used to compare ΔF⁄ Fm' of corals on HR vs LR surfaces. All statistical
analyses were completed with SYSTAT versions 11 and 12, and the statistical assumptions
of normality and homoscedasticity were evaluated through graphical analyses of residuals.
Results
Downwelling and Upwelling Photon Irradiance.—The cosine-corrected
PAR sensor demonstrated that the underwater Ed did not differ in intensity over HR
and LR surfaces (ANOVA: P > 0.05). However, underwater Eu differed between surfaces (ANOVA: P < 0.001), with a mean intensity of 687 (SE 20) μmol quanta m−2 s−1
reflected from HR, and 609 (SE 19) μmol quanta m−2 s−1 reflected from LR surfaces (n
= 9 d, Fig. 2). Overall, when R(λ) was quantified with a cosine corrected sensor, LR
surfaces reflected 11% less light than HR surfaces.
Underwater Spectral Reflectance.—R(λ) of HR surfaces [mean R(λ) = 0.76]
differed significantly from that of LR surfaces [mean R(λ) = 0.36; ANOVA: F1,13 =
11.17, P = 0.005]. When light was measured with the underwater spectrophotometer, mean R(λ) was about 52% lower for LR compared to HR surfaces. There were
also significant differences between HR and LR surfaces for the select wavelength
ranges (i.e., bins). For wavelengths corresponding to the two absorption peaks for
chlorophyll a, the integrated intensity of light between 420 nm and 440 nm differed
between HR and LR surfaces (ANOVA: F1,13 = 21.46, P < 0.001) as it did between 650
nm and 670 nm (F1,13 = 32.46, P < 0.001); in both cases, >60% more light was reflected
from HR compared to LR surfaces. For the wavelength bins corresponding to the
absorption of chlorophyll accessory pigments, integrated light intensity differed between HR and LR surfaces for the wavelengths 440–460 nm (ANOVA: F1,13 = 28.72,
P < 0.001), 520–540 nm (F1,13 = 29.71, P < 0.001), and 570–590 nm (F1,13 = 26.39, P <
0.001; Fig. 2).
colvard and edmunds: change in spectral composition of reef from macroalgae
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Figure 2. Spectral composition of light reflected from the benthos at 3-m depth in Moorea on
13 and 15 May, 2009, for high reflective (HR) and low reflective (LR) surfaces. Mean relative
spectral reflectance [R(λ)] from the substrata is displayed (solid lines; SE = dashed lines, n = 17
replicate scans) for the two substrata. There was a significant difference between the spectral
reflectance integrated between 400 and 700 nm over HR vs LR surfaces, and also for the five
wavelength bins selected to evaluate absorbance of light by chlorophyll a and accessory pigments
(shown as vertical lines).
Manipulative Experiment.—The mean midday Eu measured for colored acrylic
plates using a cosine-corrected PAR sensor was 705 (SE 25) µmol quanta m−2 s−1 for
HR plates, and 488 (SE 28) µmol quanta m−2 s−1 for LR plates (n = 9 d), and these
intensities differed significantly (P < 0.001). Photon irradiance differed between HR
and LR plates (ANOVA: P < 0.05; Fig. 3), and was similar to that recorded on the
natural surfaces they mimicked (Fig. 2).
R(λ) of benthic surfaces, as measured with the spectrophotometer, differed between 400 and 700 nm over HR compared to LR plates (ANOVA: F1,15 = 18.55, P <
0.001). Similar to the natural surfaces, the painted acrylic plates mimicking HR surfaces had a greater relative R(λ) [mean R(λ) = 0.87] than the acrylic plates mimicking
LR surfaces [mean R(λ) = 0.37]. R(λ) differed three-fold between HR and LR surfaces
for the wavelength ranges 420–440 nm (ANOVA: F1,14 = 44.19, P < 0.001), 440–460
nm (F1,14 = 40.97, P < 0.001), 520–540 nm (F1,14 = 36.14, P < 0.001), 570–590 nm (F1,14
= 32.40, P < 0.001), and 650–670 nm (F1,14 = 27.62, P < 0.001; Fig. 3).
All 20 massive Porites spp. appeared healthy throughout the study, however two P.
verrucosa (10%) bleached and died. Symbiodinium within the marginal tissue of massive Porites spp. and P. verrucosa responded to light reflected from the substratum.
ΔF⁄ Fm' differed between corals incubated on HR and LR surfaces in a pattern that
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Figure 3. The spectral composition of acrylic plates painted to create surfaces simulating natural
high reflective (HR) and low reflective (LR) surfaces. The mean relative spectral reflectance
[R(λ)] from the substrata is displayed as solid lines (SE = dashed lines, n = 18) for HR and LR
surface. The relative spectral reflectance integrated between 400 and 700 nm differed between
HR and LR surfaces. The five wavelength bins selected to evaluate absorbance of light by chlorophyll a and accessory pigments are shown as vertical lines.
differed between taxa (i.e., there was a taxon × surface interaction; ANOVA: F1,34 =
9.245, P = 0.005). Exploration of this interaction through post-hoc analyses showed
that ΔF⁄ Fm' differed between surfaces for P. verrucosa, with a 60% increase on LR
compared to HR surface, but not for massive Porites spp. (Fig. 4). In addition to the
interaction, the main effect of surface was also significant (ANOVA: F1,34 = 13.15, P
= 0.001), although there was no difference between taxa (ANOVA: F1,34 = 0.036, P >
0.05; Fig. 4).
Discussion
Our results from a shallow back reef in Moorea show that the R(λ) of the benthos differs between substrata occupied by macroalgae vs coral, turf, and CCA. A
fine-resolution tool (a fiber optic spectrophotometer) demonstrated that macroalgae
reflected about 65% less light than surfaces dominated by CCA and coral, whereas a
coarse tool (a cosine-corrected PAR sensor) showed that Eu was reduced 11% for LR
compared to HR surfaces. While it is well known that the spectral composition and
attenuation of light underwater changes with depth (Schenck 1957, Ramus et al. 1976,
Gernez et al. 2011) and seawater quality (Smith 1974, Devlin et al. 2008, Hieronymi
and Macke 2010), the present study contributes to what is still a sparse literature
colvard and edmunds: change in spectral composition of reef from macroalgae
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Figure 4. Effective photochemical efficiency of PSII (ΔF⁄ Fm') of Porites spp. (n = 10 for each treatment) and Pocillopora verrucosa (n = 9 for each treatment) after 27 d on acrylic plates painted to
mimic high reflective (HR) and low reflective (LR) surfaces. Incubations were completed at 3-m
depth in the back reef, and all measurements were obtained between 12:00 and 13:00 hrs. ΔF⁄ Fm’
was affected significantly by a taxon × surface interaction, as well as surface type.
describing how the underwater light regime on shallow coral reefs is affected by the
reflective properties of the benthos (but see Maritorena et al. 1994, Joyce and Phinn
2003, Mobley and Sundman 2003, Hedley et al. 2004).
Additionally, we show the potential for benthos-mediated variation in Eu and R(λ)
to affect the performance of reef corals. As R(λ) is reduced by macroalgae compared
to coral, turf, and CCA, the temporal trend for rising macroalgal cover on coral reefs
(McManus and Polsenberg 2004, Kuffner et al. 2006, Norström et al. 2009) is likely
to be associated with reduced near-bottom light intensities. While the light-related
implications of this trend are unclear, the reductions in reflected light motivate at
least two predictions regarding the effects on corals. First, corals might have a selective advantage on surfaces dominated by macroalgae if they can maintain high rates
of photosynthesis at low irradiances. Second, it is possible that macroalgal dominated areas of reef could serve as a spatial refuge for corals that are sensitive to damage
at high light intensities.
Based on the aforementioned predictions and the present results for ΔF⁄ Fm', it is
unlikely that small colonies of massive Porites spp. and P. verrucosa on shallow reefs
will be negatively affected by the impacts of macroalgae on reflected light. Not only
was ΔF⁄ Fm' in the marginal tissues of both taxa resistant to the negative effects of
reduced reflected light intensities over LR surfaces, but for P. verrucosa, ΔF⁄ Fm' increased on LR compared to HR surfaces. Therefore Symbiodinium in P. verrucosa
may benefit from LR surfaces where they lose less light energy to non-photosynthetic
pathways (i.e., non-photosynthetic quenching, NPQ; Cosgrove and Borowitzka 2010)
compared to conspecifics on HR surfaces. While this pattern cannot be interpreted
as evidence that photosynthetic carbon fixation is higher in marginal tissues of small
P. verrucosa on LR compared to HR surfaces (Enriquez and Borowitzka 2010), nevertheless, it demonstrates that the reductions in light reflected from macroalgae can
have functional implications for coral photophysiology.
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In the context of the well-known capacity for acclimatization to shade in corals
that involves changes in pigment concentration, thylakoid structures, and symbiont
densities (Falkowski and Dubinsky 1981, Iglesias-Prieto and Trench 1994, Dubinsky
and Falkowski 2011), it is intriguing that Symbiodinium in the marginal tissue of
massive Porites spp. were unresponsive to reduced intensities of Eu. However, this
finding may not be without precedent because at least one other poritid [Porites cylindrica (Dana, 1846)], has a limited capacity to acclimate to shade (Anthony and
Fabricius 2000). Moreover, because there are indications that massive Porites spp.
is functionally unequal to other corals (Loya et al. 2001, Fabricius 2011), it may not
respond to shade in similar ways to other corals. The Symbiodinium offer one reason
why massive Porites spp. and P. verrucosa might differ in their response to reflected
light, because massive Porites spp. in Moorea contain C15 Symbiodinium (Edmunds
et al. in press), whereas P. verrucosa contain C1c Symbiodinium throughout the
Pacific (LaJeunesse et al. 2004). The response of Symbiodinium to varying light regimes differs among genetic variants of this taxon (Hennige et al. 2009), although to
our knowledge, the phenotypes of C1c and C15 have not been compared.
By analyzing the light regime by wavelength bins corresponding to the peak absorptivity of chlorophyll a and its accessory pigments, we sought to explore the
mechanisms through which variation in R(λ) could affect coral photophysiology. The
contrast of light reflected from HR and LR surfaces revealed a two-fold difference
in the light intensity for the wavelength bins corresponding to the absorptivity of
chlorophyll a, with HR surfaces reflecting more light than LR surfaces. There were
also differences between HR and LR surfaces for the wavelength bins corresponding
to the chlorophyll accessory pigments, with HR surfaces reflecting three- to four-fold
more light within these bins than LR surfaces. These differences between HR and LR
surfaces are likely to be a function of the absorption of light for photosynthesis by
macroalgae (McCook et al. 2001, Birrell et al. 2008). By analyzing reflected light in
discrete wavelength bins, our results suggest that light reflected from HR substrata
may have the potential to affect the photophysiology of the Symbiodinium in two
ways: (1) by providing a greater amount of light, and (2) providing a greater proportion of wavelengths that excite chlorophyll a as well as the accessory pigments within
these algae.
As many coral reefs are experiencing a decline in scleractinian cover (Gardner et
al. 2003, Bellwood et al. 2004, Hughes et al. 2011) and an increase in abundance of
macroalgae (Tanner 1995, Aronson and Precht 2006, Norström et al. 2009), evaluating the consequences of these changes is an important priority to understand the
functional implications of algal dominance on tropical reefs (McCook et al. 2001).
The present analysis shows that macroalgae can affect the near-bottom light regime
on coral reefs in ways that have not previously been emphasized (McCook et al. 2001,
Birrell et al. 2008), and demonstrate that these effects can influence the photophysiology of coral tissue located close to these benthic surfaces. It is important to note,
however, that our study utilized small corals that were either juvenile colonies or
branch fragments, and therefore it is unknown to what extent our findings can be
extrapolated to other corals or to other reefs. To elucidate the ecological relevance
of the aforementioned patterns, it will be necessary to conduct similar studies with
larger colonies, to evaluate the impacts of adjacent surfaces to whole colonies (not just
the marginal tissue), and to evaluate the extent to which the reflectance properties
of meter-scale areas of reef can impact the reflectance properties of centimeter-scale
colvard and edmunds: change in spectral composition of reef from macroalgae
1029
areas of reef (as investigated in the present study), and the light regime within the
tissue where the Symbiodinium are located (Kaniewska et al. 2011).
Acknowledgments
This material is based upon work supported by the US National Science Foundation through
the Moorea Coral Reef, Long-Term Ecological Research program (grants OCE 04-17412 and
10-26851), and gifts from the Gordon and Betty Moore Foundation; it was completed under a
research permit issued by the French Polynesian Ministry of Research. We are grateful to N
Davies and the staff of the UC Berkeley, Richard B Gump South Pacific Research Station for
making our visits to Moorea productive and enjoyable, and C Cameron, W Goldenheim, V
Moriarty, M Johnson, and S Swanson for field assistance. We would also like to thank three
anonymous reviewers as well as B Helmuth for providing comments that improved an earlier
draft of this paper. This manuscript was submitted in partial fulfillment for the MS degree at
California State University, Northridge. This is contribution number 183 of the CSUN Marine
Biology Program.
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date suBmitted: 1 august, 2011.
date accepted: 30 July, 2012.
availaBle online: 23 august, 2012.
addresses: (nbc) Department of Biological Sciences, University of South Carolina, 715
Sumter St. Columbia, South Carolina 29208. (pJe) Department of Biology, California
State University, Northridge, 18111 Nordhoff Street, Northridge, California 91330-8303.
corresponding author: (nbc) Email: <[email protected]>.