Temporal Variation in Photosynthetic Pigments and UV-Absorbing Compounds in Shallow Populations of Two Hawaiian Reef Corals

As we seek to understand the physiological mechanisms of coral bleaching, it is important to understand the background temporal variation in photosynthetic pigments and photoprotective compounds that corals exhibit. In this study, reef flat populations of two hermatypic coral species, Montipora capitata (Dana, 1846) and Porites compressa Dana, 1846, were sampled monthly in Kāne‘ohe Bay, Hawai‘i, from January 1998 to March 1999. Surface ultraviolet radiation (UVR) was measured continually during this time period at the same location. High-performance liquid chromatography (HPLC) analysis of photosynthetic pigments and mycosporine-like amino acids (MAAs) revealed temporal changes in concentrations and proportions of these compounds in tissues of both species of coral. Chlorophyll a (chl a), chlorophyll c2 (chl c2), peridinin, and diadinoxanthin concentrations changed on a skeletal weight (M. capitata) or surface area (P. compressa) basis, significantly correlating with seasonal changes in solar input (number of days from the winter solstice). In P. compressa, diadinoxanthin increased in proportion to the total pigment pool during summer months, suggesting an up-regulation of a xanthophyll cycle. In M. capitata, the ratio of chl a: chl c2 decreased during winter months, suggesting photoacclimation to lower light levels. It is surprising that there was not a clear seasonal pattern in total MAA concentration for either species, with the exception of shinorine in P. compressa. The relative stability of MAA concentrations over the course of the year despite a pronounced seasonal trend in UVR suggests either that MAAs are not performing a photoprotective role in these species or that concentrations are kept at a threshold level in the presence of a dynamic light environment. A clear understanding of the natural variation in coral pigmentation (both light harvesting and photoprotective compounds) is imperative as coral bleaching becomes more frequent and intense due to global climate change (Høegh-Guldberg 1999). Corals and zooxanthellae have evolved a symbiosis in extremely high solar irradiance environments and a narrow range in sea surface temperature. The algal symbionts (zooxanthellae) resident in the gastrodermis of the coral animal require access to photosynthetically active radiation (PAR) (400–750 nm) for diurnal carbon gain, most of which is exported in support of the symbiosis (Muscatine et al. 1984). However, access to PAR comes at a price in the form of exposure to ultraviolet radiation (UVR) (280–400 nm). UVB (280– 320 nm) radiation is absorbed by and causes damage to nucleic acids and proteins (HolmHansen et al. 1993). In addition, the absorption of UVB and UVA (320–400 nm) by other cellular components can cause oxidative damage via the production of active oxygen species including singlet oxygen and oxygen, Pacific Science (2005), vol. 59, no. 4:561–580 : 2005 by University of Hawai‘i Press All rights reserved 1 Funding was provided in part by an Edmondson Grant-in-Aid awarded to I.B.K. Manuscript accepted 21 December 2004. 2 Department of Zoology, University of Hawai‘i, 2538 The Mall, Honolulu, Hawai‘i 96822 and Hawai‘i Institute of Marine Biology, P.O. Box 1346, Kāne‘ohe, Hawai‘i 96744. 3 Current address: U.S. Geological Survey, Center for Coastal and Watershed Studies, 600 4th Street South, St. Petersburg, Florida 33701 (e-mail: [email protected]). hydroperoxyl, and hydroxyl radicals (Dunlap and Yamamoto 1995). UVR can penetrate the water column down to 30 m in clear, oligotrophic waters commonly found in the tropics ( Jerlov 1950, Smith and Baker 1979) and has been shown to play a role in coral bleaching (Gleason and Wellington 1993, Grottoli-Everett and Kuffner 1995). Variability in the amount of photosynthetic pigment in corals has been recognized for a long time. As depth increases, so does the concentration of photosynthetic pigment per unit of coral surface area, manifested as an increase in pigment per algal cell (Chalker and Dunlap 1983, Falkowski et al. 1990, Masuda et al. 1993). Also, shade-acclimated colonies have zooxanthellae containing more pigment per algal cell than do light-acclimated colonies (Porter et al. 1984). Increases in photosynthetic pigment concentration per algal cell as depth increases have traditionally been interpreted as photoacclimation to offset decreases in light availability. Photoacclimation on a seasonal basis, however, has not been as well documented. Recent studies have shown an inverse relationship between zooxanthellae density and solar irradiance in natural populations, revealing a marked seasonal cycle in zooxanthellae densities for several species of coral wherein densities increase in the fall/winter (Stimson 1997, Fagoonee et al. 1999, Fitt et al. 2000). Other studies have documented high zooxanthellae densities during periods of decreased underwater PAR (during monsoon season: Brown et al. 1999b; due to increased turbidity: Cook et al. 2002). Most of those studies also document a wintertime increase in the amount of photosynthetic pigment per algal cell, but they measured only the chlorophylls. Tissue concentrations of chl a are often measured as the sole index of the lightharvesting capacity of the coral-algal symbiosis (see Table 3 in Kaiser et al. 1993), which in turn is often used as an indicator of the physiological state of the symbiosis. The historic trend of measuring only chl a could be misleading because other pigments may also be responsive to changes in the solar irradiance regime (Chang et al. 1983, IglesiasPrieto and Trench 1997). The carotenoids, for example, may perform a photoprotective role by quenching excess irradiance, as demonstrated for the xanthophylls in free-living dinoflagellates (Demers et al. 1991) and recently for coral-algal symbioses (Brown et al. 1999a). In dinoflagellates, the light harvesting is accomplished with chl a and the accessory pigments chl c2 and peridinin (Iglesias-Prieto and Trench 1997). Only recently have the accessory photosynthetic pigments found in the zooxanthellae been considered with respect to coral ecology (Fang et al. 1995, Ambarsari et al. 1997, Helmuth et al. 1997, Myers et al. 1999). A suite of UV-absorbing compounds found in the tissues of corals has been intensively investigated for their sun-screening potential (for reviews see Dunlap and Shick 1998, Gleason 2001, Shick and Dunlap 2002). Known as mycosporine-like amino acids (MAAs), these compounds have been found in orders-ofmagnitude higher concentrations in shallowdwelling corals compared with deep conspecifics (Dunlap et al. 1986, Banaszak et al. 1998). There has been debate over whether these UV-absorbing compounds actually benefit the coral as sunscreens; circumstantial evidence continues to mount in support of this contention, but direct evidence is scarce (Gleason 2001). Several species of coral increase concentrations of MAAs when transplanted from low to high irradiance environments (Scelfo 1986, Gleason and Wellington 1993). The naturally occurring, seasonal variation in MAA concentration in corals has received little attention (except see Drollet et al. 1997, Michalek-Wagner 2001 [soft corals]) but offers a natural experiment by which we can evaluate acclimation potential and the role of MAAs in UVR protection. The aim of this study was to document temporal variability in photosynthetic pigments and photoprotective compounds in two species of corals in Hawai‘i, both of which are major framework builders in the Hawaiian Islands. The two species were chosen based upon their importance in the local coral community, and because both are known to bleach ( Jokiel and Brown 2004). PACIFIC SCIENCE . October 2005 562