Macroalgae on shallow tropical reefs reduce the availability of reflected light for use in coral photosynthesis

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. coRAl Reef pApeR BULLETIN OF MARINE SCIENCE. VOL 88, NO 4. 2012 1020 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).