Impact of excess and harmful radiation on energy budgets in scleractinian corals

Using dynamic energy budget (DEB) theory, this paper explores the potential of excess and harmful radiation, notably UV, to cause changes in performance and, ultimately, bleaching in scleractinian corals for a range of ambient nitrogen and (beneficial) photosynthetically active radiation levels. Two negative impacts of radiation are considered: a reduction in the capacity of the symbiont to generate energy through photosynthesis (defined in this paper as photoinhibition); an increase in the costs for the symbiont to remain viable due to repair of damage (defined in this paper as photodamage). Model predictions indicate that although both types of impact reduce the growth potential of host and symbiont, photoinhibition predominantly affects host features, except at very low ambient nitrogen levels, under which conditions the severity of nitrogen limitation is so strong that a reduction in photosynthetic rates due to photoinhibition has minimal impact. In steady state, photoinhibition leads to a reduction in host biomass, and an increase in symbiont density, implying that photoinhibition (as defined in this paper) is unlikely to cause bleaching. In contrast, the impact of photodamage is mostly affecting symbiont features, including a decline in symbiont density. Thus, photodamage may contribute to coral bleaching. Furthermore, the model predicts that, with both photoinhibition and photodamage, an increasing ratio of harmful to beneficial radiation accelerates the suppression of growth rates of symbiont and host, implying that coral health deteriorates progressively faster with increasing harmful radiation, such as UVb.     

Diel fluctuations of mycosporine-like amino acids in shallow-water scleractinian corals

Reports of bathymetric decrease in the total mycosporine-like amino acid (MAA) concentration of benthic invertebrates suggest that light gradients may be important determinants of MAA content. With the pronounced diel light changes, distinct temporal variations in MAA concentrations might also be expected. We examined the changes in the abundance of MAA in three shallow-water scleractinian corals, Pavona divaricata, Galaxea fascicularis and Montipora digitata from Okinawa, Japan, in relation to daily cycles in solar radiation and tested whether the species have different capabilities for protection against UVR depending on their MAA composition. The results show that symbiotic algae freshly isolated from the investigated coral species do not contain MAAs and that distribution of these compounds resided only within the animal tissue. Total MAA content in the tissue of P. divaricata, G. fascicularis and M. digitata rose rapidly at midday and significantly dropped at night. The observed variations were by a factor of two and, thus, very dramatic. For all the investigated coral species, total MAA concentrations were significantly correlated with the diurnal cycle in solar radiation, during both winter and summer seasons. Seawater temperature was significantly correlated with MAA levels only in the June experiment, but represented no more than 20% of the MAA variation in all three coral species, whereas solar radiation explained 60–70% of the MAA fluctuations. This suggests that MAAs are an integral component of the hard corals biochemical defense system against high solar irradiance stress. The diurnal increase in total MAA concentrations was due to an increase in the concentration of imino-MAA species of up to 2–2.5-fold of their pre-dawn values. In contrast, the oxocarbonyl-MAA mycosporine-glycine (Myc-Gly) showed the lowest (Tukey–Kramer HSD test: P<0.05) values at midday, compared to afternoon and night hours. Analysis of diel changes in chlorophyll fluorescence and chlorophyll a content of the investigated species revealed that P. divaricata and G. fascicularis were less sensitive to the high levels of ambient irradiance compared to M. digitata. In P. divaricata and G. fascicularis, Myc-Gly, an MAA with an antioxidant function, is the most abundant MAA, contributing about 70% to the total MAA pool, whereas the major MAA factions in M. digitata were represented by oxidatively robust imino-MAAs. We speculate that MAAs furnish scleractinian corals with protection from biologically damaging ultraviolet radiation through both the direct sunscreening activity of imino-MAAs and the antioxidant properties of oxocarbonyl-MAAs and suggest that the predominance, in the host tissue, of MAA species with an antioxidant ability may render corals more tolerant to high photosynthetically active and ultraviolet radiation.Communicated by T. Ikeda, Hakodate     

Risk-averse foraging by bananaquits on negative energy budgets

Summary Adult bananaquits on negative energy budgets were presented with a patch containing two flower types with identical mean rewards, but different variances. The flower patch contained a random array of 85 yellow and 85 red artificial flowers. Flowers of one color were filled with the same quantity of nectar (constant flowers); flowers of the other color were filled with variable quantities of nectar (variable flowers). In the first series of experiments the birds were given three presentations, followed by three more presentations with the flower colors reversed, to control for color preferences. Some individuals were occasionally indifferent during a presentation, but overall the birds significantly preferred the constant flowers. In the second series of experiments two birds were give five presentations of the floral patch during a day at a rate less than minimally required to meet all 24-h energy costs. In all experiments, bananaquits on negative energy budgets were either indifferent or risk-averse, but never risk-prone. The absence of risk-prone foraging might be attributed to resource dispersion pattern, reward skew, or a species characteristic.     

Comparative studies on the metabolism of shallow-water and deep-sea marine fishes. I. White-muscle metabolism in shallow-water fishes

Maximal rates of oxygen consumption in vitro have been measured under standardized conditions at three test temperatures (5°, 15°, and 25°C) on minced preparations of white muscle from 39 species of shallow-water marine teleost fishes. These fishes came from four different geographic areas, two with cool average water-temperatures (near 15°C: coastal southern California, Galápagos Islands) and two with warm average water-temperatures (near 25°C: Hawaiian Islands; Bermuda). The group includes species covering much of the range of variation to be found among the teleosts with respect to five additional variables: phylogenetic position, type of environment, body weight, activity level, and growth stage. The purpose of the work is to provide part of a base line of tissue-metabolism data on shallow-water fishes for comparison with similar results from deep-sea species. Major conclusions from statistical analyses of the results are: four groups of shapes of oxygen-uptake rate versus temperature curves exist: normal, flat, dipped and peaked. Over 50% of curves are normal. Intra-group differences, contributing significantly to the total variance of the results at given test temperatures, are: cool versus warm average environmental temperatures primarily for epipelagic species; epipelagic versus non-epipelagic environments; very active species versus all others; juvenile stages versus adults. In each case, the subgroup first mentioned shows higher muscle oxygen-uptake rates than the other subgroup. Variables not contributing significantly to the total variance are phylogenetic position and body weight. Physiological and ecological implications of these results are discussed.     

Comparative studies on the metabolism of shallow-water and deep-sea marine fishes. II. Red-muscle metabolism in shallow-water fishes

Maximal rates of oxygen consumption in vitro have been measured under standardized conditions at three test temperatures (5°, 15°, 25°C) on minced preparations of red muscle from 10 species of shallow-water marine teleost fishes. These fishes came from three different geographic areas, two with cool average water temperatures (near 15°C: coastal southern California, Galápagos Islands) and one with warm average water temperatures (near 25°C: Hawaiian Islands). The group is made up of post-juvenile or adult epipelagic fishes, which are moderately or very active in terms of their locomotor activities. A large part of the range of phylogenetic diversity among the teleosts is represented, as is the body weight range from a few grams to several kilograms. The purpose of the work is to provide part of a set of tissue-metabolism data on shallow-water fishes for future comparison with similar results from deep-sea species. Of 8 complete curves for oxygen uptake rate versus temperature (R-T curves), 6 are normal in shape (Q₁₀1.5), 1 is normal but with a low Q₁₀, and 1 is partly flat, partly normal. The differences between the species in terms of both absolute positions and slopes of the R-T curves are not related in any consistent way to any of the three testable variables: phylogenetic position, long-term adaptation temperature, and body size. The red muscles of a variety of adult epipelagic fishes, at ecologically realistic temperatures, are shown to be exceptions to the general rule that tissues of ectothermous lower vertebrates have lower metabolic rates than comparable tissues of non-torpid endothermous higher vertebrates. This circumstance probably is a major factor in the great capacities for sustained high-speed swimming shown by most epipelagic fishes. Other physiological and ecological implications of the results are discussed.     

Effects of eutrophication on reef-building corals

Seven fringing reef complexes were chosen along the leeward coast (west) of Barbados to study the effects of eutrophication processes upon the scleractinian coral assemblages. The structure of scleractinian coral communities was studied along an eutrophication gradient with a quantitative sampling method (line transect) in terms of species composition, zonation and diversity patterns. On the basis of these data the fringing reefs were divided into three ecological zones: back reef, reef flat, and spur and groove. Statistically discernible and biologically significant differences in scleractinian coral community structure, benthic algal cover and Diadema antillarum Philippi densities were recorded among the seven fringing reefs. High correlations between environmental variables and biotic patterns indicate that the effects of eutrophication processes (nutrient enrichment, sedimentation, turbidity, toxicity and bacterial activity) were directly and/or indirectly affecting the community structure of scleractinian coral assemblages. In general, species diversity was most sensitive in delineating among-reef, and among-zone, differences, which were attributed to intensification of eutrophication processes. Porites astreoides Lamarck, P. porites (Pallas), Siderastrea radians (Pallas), and Agaricia agaricites (Linnaeus) were the most abundant coral species in the polluted southern reefs. The absence and/or low abundance of coral species previously characterized as well adapted to high turbidity and sedimentation [i.e. Montastrea cavernosa Linnaeus, Meandrina meandrites (Linnaeus)] indicate that eutrophication processes may adversely affect these species. It is suggested that sediment rejection abilities, combined with feeding and reproductive strategies, are the primary biological processes of scleractinian corals through which eutrophication processes directly and/or indirectly affect the structure of coral communities.     

Effects of eutrophication on reef-building corals

Fourteen environmental variables were monitored at seven locations along the west coast of Barbados on a weekly basis over a one-year period, 1981 to 1982. The physicochemical and biological data indicate that an environmental gradient exists as a result of increased eutrophication of coastal waters. Growth rates (linear extension) of Montastrea annularis (Ellis and Solander), measured along the environmental gradient, exhibit high correlation with a number of water quality variables. Concentration of suspended particulate matter is the best univariate estimator of M. annularis skeletal extension rates (r ²=0.79, P<0.0001). The results suggest that suspended particulate matter may be an energy source for reef corals, increasing growth up to a certain maximum concentration. After this, reduction of growth occurs due to smothering, reduced light levels and reduced zooxanthellae photosynthesis.     

Seasonal and sex-specific variations in levels of photo-protecting mycosporine-like amino acids (MAAs) in soft corals

This study focusses on the nature and extent of variation in mycosporine-like amino acids (MAAs) in relation to annual cycles in solar radiation, seawater temperature, and reproduction in reef-flat populations of two soft coral species. The results show MAA tissue concentrations in shallow water colonies of Lobophytum compactum and Sinularia flexibilis to be significantly correlated to annual cycles in solar radiation (P<0.0006 and P<0.0005, respectively) and seawater temperature (P<0.0006 and P<0.0004, respectively). Evidence of seasonal cycles in MAA levels in the tissues of shallow-reef invertebrates positively correlating with annual cycles in solar radiation and temperature suggests that they are an integral component of the soft corals' biochemical defence system against high irradiance and/or temperature stress and thus bleaching. This is further corroborated by the higher production of MAAs in females than males prior to spawning (up to 67% and 56% for L. compactum and S. flexibilis, respectively), presumably to provide a high level of protection against irradiance stress for progeny.     

Effect of epibionts on the microdistribution of chlorophyll in corals and its detection by fluorescence spectral imaging

The spatial distribution of chlorophyll in three coral species carrying invertebrate symbionts was determined using spectral imaging techniques. From each pixel of the image, full fluorescence spectral data was obtained as well as comparative ratios of fluorescence. The multipixel fluorescence map and the relative-intensity fluorescence ratios demonstrated a high concentration of chlorophyll a next to the pits of Cryptochirus coralliodytes in Favites halicora. Spectral similarity maps of Goniastrea retiformis infested with Lithophaga lessepsiana and of Millepora dichotoma infested with Savignium milleporum revealed relatively higher chlorophyll concentrations in these two corals next to the symbionts. We hypothesize that the invertebrate symbionts fertilize their immediate surroundings with their excreta, enhancing algal growth. The spectral analysis system used in this study made it possible to distinguish such changes by spatial quantitation of the fluorescence emitted from small surface areas.     

Effect of acclimatization to low temperature and reduced light on the response of reef corals to elevated temperature

This study tested the effects of acclimatization on the response of corals to elevated temperature, using juvenile massive Porites spp. and branching P. irregularis from Moorea (W149°50′, S17°30′). During April and May 2006, corals were acclimatized for 15 days to cool (25.7°C) or ambient (27.7°C) temperature, under shaded (352 μmol photons m⁻² s⁻¹) or ambient (554 μmol photons m⁻² s⁻¹) natural light, and then incubated for 7 days at ambient or high temperature (31.1°C), under ambient light (659 μmol photons m⁻² s⁻¹). The response to acclimatization was assessed as biomass, maximum dark-adapted quantum yield of PSII (F _v/F _m), and growth, and the effect of the subsequent treatment was assessed as F _v/F _m and growth. Relative to the controls (i.e., ambient temperature/ambient light), massive Porites spp. responded to acclimatization through increases in biomass under ambient temperature/shade, and low temperature/ambient light, whereas P. irregularis responded through reduced growth under ambient temperature/shade, and low temperature/ambient light. Acclimatization affected the response to thermal stress for massive Porites spp. (but not P. irregularis), with an interaction between the acclimatization and subsequent treatments for growth. This interaction resulted from a lessening of the negative effects of high temperature after acclimatizing to ambient temperature/shade, but an accentuation of the effect after acclimatizing to low temperature/shade. It is possible that changes in biomass for massive Porites spp. are important in modulating the response to high temperature, with the taxonomic variation in this effect potentially resulting from differences in morphology. These results demonstrate that corals can acclimatize during short exposures to downward excursions in temperature and light, which subsequently affects their response to thermal stress. Moreover, even con-generic taxa differ in this capacity, which could affect coral community structure. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

The effects of temperature on the growth of juvenile scleractinian corals

Tropical reef corals are well known for their sensitivity to rising temperature, yet surprisingly little is known of the mechanisms through which temperature acts on intact coral colonies. One such mechanism recently has been suggested by the association between the growth of juvenile corals and seawater temperature in the Caribbean, which suggests that temperature causes a transition between isometric and allometric growth scaling in warmer versus cooler years, respectively (Edmunds in Proc R Soc B 273:2275–2281, 2006). Here, this correlative association is tested experimentally for a cause-and-effect relationship. During April and May 2006, juvenile colonies (8–35 mm diameter) of massive Porites spp. from Moorea, French Polynesia, were incubated at warm (27.8°C) and cool (25.7°C) temperatures for 15 days, and their response assessed through the scaling of growth (change in weight) with colony size. The results reveal that the scaling of colony-specific growth (mg colony⁻¹ day⁻¹) was unaffected by temperature, although growth absolutely was greater at the cool compared to the warm temperature, regardless of colony size. This outcome was caused by contrasting scaling relationships for area-specific growth (mg cm⁻² day⁻¹) that were negatively allometric under warm conditions, but independent of size under cool conditions. In April 2007, a 22 days field experiment confirmed that the scaling of area-specific growth in juvenile Porites spp. is negatively allometric at a warm temperature of 29.5°C. Based on strong allometry for tissue thickness, biomass, and Symbiodinium density in freshly collected Porites spp., it is hypothesized that the temperature-dependency of growth scaling in these small corals is mediated by the interaction of temperature with biomass.     

Effects of eutrophication and sedimentation on juvenile corals

Settlement of juvenile scleractinian corals was investigated from 1987 to 1990 on eutrophic and less eutrophic fringing reefs on the west coast of Barbados, West Indies. The number of coral recruits and number of recruiting coral species on cement blocks decreased with increasing eutrophication of the reefs. This may suggest lower settlement rates on eutrophic reefs, but could also liave resulted from higher post-settlement mortality, since blocks were examined only once after 3 yr of immersion. Coral settlement rates to artificial plates that were checked monthly were also lower on the more eutrophic reefs. This could result from lower local availability of larvae caused by fewer adult corals and/or lower reproductive rates of corals on eutrophic reefs. However, the ratio of coral recruits to adult coral abundance was considerably lower on eutrophic reefs, suggesting that local coral abundance alone can not explain lower settlement rates on eutrophic reefs. The lower rates on eutrophic reefs may result from a lower probability of coral larvae settlin when present, perhaps because of a limited availability of suitable settlement substrate. Colonization of settlement plates by non-coralline organisms was heavier on eutrophic reefs, and unoccupied space was lower, supporting the suggestion that suitable coral settlement substrate may be limiting on eutrophic reefs. Moreover, coralline algae, which facilitate metamorphosis and settlement of coral larvae, were less abundant on settlement plates on eutrophic reefs.     

Effects of sand deposition on scleractinian and alcyonacean corals

The ability of corals to withstand experimental sand deposition was investigated for two experimental periods (17 h and 6 wk) in eight scleractinia (Favia favus, Favites pentagona, Platygyra daedalea, Gyrosmilia interrupta, Galaxea fascicularis, Cyphastrea chalcidicum, Favites abdita, Goniopora dijboutensis) and five alcyonacea (Lobophytum depressum, L. venustum, Sinularia dura, S. leptoclados, Sarcophyton glaucum) collected in 1992 from Natal, South Africa. Scleractinia were active sediment shedders, alcyonacea passive, relying on water motion and gravity. Short-term sand clearing efficiency was primarily dependent on corallum shape. Sand application led to hydrostatic inflation of polyps in scleractinia and the entire colony in alcyonacea as well as to increased tentacular action in the scleractinian Gyrosmilia interrupta. Under continuous sand application, inflation remained while other activities, such as tentacular motion, ceased completely. In scleractinia and alcyonacea, tissue necroses appeared after the first week of continuous sand application. Death of entire colonies and partial bleaching of continually sandcovered areas were observed in alcyonacea only. Different grain sizes of sand had no influence on clearing reaction or efficiencies.     

Effects of temperature on the mortality and growth of Hawaiian reef corals

Three common species of Hawaiian reef corals, Pocillopora damicornis (L.), Montipora verrucosa (Lamarck) and Fungia scutaria Lamarck, were grown in a temperature-regulated, continuous-flow sea water system. The skeletal growth optimum occurred near 26°C, coinciding with the natural summer ambient temperature in Hawaii, and was lowest at 21° to 22°C, representing Hawaiian winter ambient. Levels of approximately 32°C produced mortality within days. Prolonged exposure to temperatures of approximately 30°C eventually caused loss of photosynthetic pigment, increased mortality, and reduced calcification. Corals lived only 1 to 2 weeks at 18°C. The corals showed greater initial resistance at the lower lethal limit, but ultimately low temperature was more deleterious than high temperature. Results suggest that a decrease in the natural water temperature of Hawaiian reefs would be more harmful to corals than a temperature increase of the same magnitude.Contribution No. 504 of the Hawaii Institute of Marine Biology.     

Influence of UV radiation on the survival of larvae from broadcast-spawning reef corals

Effects of ambient ultraviolet light on the survivorship of eggs and planulae larvae was investigated for three species of broadcast-spawning reef corals, Acropora palmata, Montastraea annularis, and M. franksi. Eggs and larvae from these corals contain high concentrations of lipids (60–70% by weight) and float in surface waters for 3–4 days following spawning. Larvae originating from colonies living at deeper sites on the reef exhibited significantly lower survivorship than conspecifics originating from parents in shallow water when experimentally exposed for up to 4 days to ambient surface levels of ultraviolet radiation (UVR). Concentrations of the UVR-protective compounds correlated positively with survival and matched concentrations found in parent colonies, implying that higher concentrations of ultraviolet B protective compounds are responsible for greater survival of eggs and larvae from shallow compared to deeper-dwelling parents. Ultraviolet B appears to be responsible for most of the observed differences in larval survivorship with ultraviolet A playing a minor or insignificant role. Data presented here indicate that coral recruits on Caribbean reefs and elsewhere may originate primarily from adult colonies dwelling in shallow water.Communicated by P.W. Sammarco, Chauvin     

Effects of sheltering fish on growth of their host corals

Stony corals are the foundation species of tropical reefs, and their structures can harbor a diverse range of mutualist taxa that can confer important benefits, including provision of nutrients. Prominent among the associates of branching coral in the genus Pocillopora are groups of zooplanktivorous damselfishes that take refuge in the coral to avoid their predators. In field and laboratory experiments, we explored the effects of colonies of resident damselfishes on growth of their host corals. Laboratory studies revealed a positive relationship between biomass of fish and output of ammonium. In the field, levels of ammonium were significantly elevated in the water surrounding the branches of Pocillopora occupied by colonies of damselfish, particularly in time periods following active feeding by the fish. Experimental manipulation of the presence of fish on host corals during a month-long field experiment revealed that corals hosting fish grew significantly more than those that lacked fish, and coral growth was positively correlated with the biomass of resident fish. The Pocillopora colonies in the field experiment varied in the degree of openness of their branching structure, and dye studies indicated that this affected their ability to retain waterborne nutrients. Together with biomass of resident fish, colony openness explained 76% of the variation in coral growth rate during the experiment. Corals can exhibit considerable morphological variability, and mutualistic fish respond to colony architecture during habitat selection, with some species preferring more open-branched forms. This makes it likely that corals may face tradeoffs in attracting resident fish and in retaining the nutrients they provide.     

Possible effects of water pollution on the community structure of Red Sea corals

The community structure and species diversity of hermatypic corals was studied during 1969–1973, in two reef flats in the northern Gulf of Eilat, Red Sea: the reef flat of the nature reserve at Eilat, which is chronically polluted by oil and minerals, and a control reef, located 5 km further south, which is free from oil pollution. In 1969, the nature reserve and the control reef had similar coral community structure. In September, 1970, both reefs suffered approximately 90% mortality of corals, as a result of an unexpected and extremely low tide. In 1973 the control reef was “blooming” with a highly diverse coral community, while almost no signs of coral recolonization have been observed at the nature reserve, and it is significantly lower in diversity. It is suggested that phosphate eutrophication and chronic oil pollution are the major man-made disturbances that interfere with coral colonization of the reef flat at the nature reserve. Although no direct evidence is provided that oil damages hermatypic corals, the data strongly suggest that chronic oil spills prevent normal settlement and/or development of coral larvae. It is possible that chronic oil, pollution results in either one or a combination of the following: (1) damage to the reproductive system of corals; (2) decreased viability of coral larvae; (3) changes in some physical properties of the reef flat which interfere with normal settlement of coral larvae.     

Effects of photoacclimation on the light niche of corals: a process-based approach

The ecology of photosynthetic organisms is influenced by the need to adjust the photosynthetic apparatus to variable light environments (photoacclimation). In this study, we quantified different components of the photoacclimation process for a reef-building coral (Turbinaria mesenterina, Lamarck, 1816): including, variation in absorption cross-section, size of photosynthetic units, turnover time, chlorophyll content, and colony respiration. We used these calibrations to characterize this species’ light niche, and to determine the sensitivity of the niche boundaries to different processes of photoacclimation. Results showed that the breadth of the light niche was most sensitive to the size of the photosynthetic unit, absorption cross-section, and rates of respiration. Habitats with the highest light availability did not lead to maximal energy acquisition. This was because, although corals acclimated to high light have high rates of photosynthesis per unit chlorophyll, their chlorophyll content was strongly reduced. This suggests that potential energetic benefits that could be achieved through increased light harvesting (i.e., increased chlorophyll content) in high-light habitats are outweighed by costs associated with photoprotection. Such costs appear to place an upper bound on the habitat distributions of coral species. Our approach reveals how the photophysiological processes involved in photoacclimation interact to determine the light niche.