Interactions between morphological and physiological plasticity optimize energy acquisition in corals

Morphological plasticity in response to environmental heterogeneity may be performance enhancing or may simply result from an intrinsic instability in morphology during development. Although patterns of morphological change are well documented for numerous taxa, it is often unclear whether this plasticity enhances the performance of organisms in the habitat to which they have acclimatized. Reef-building corals are an ideal model system in which to investigate this question. We here develop a three-dimensional geometric model and present a comprehensive photosynthesis data set with experimentally calibrated photosynthesis models that predicts energy acquisition by foliose corals as a function of colony shape. This allows us to assess the extent to which changes in colony morphology along an environmental gradient track the predicted optimal colony morphologies. Our results provide strong evidence that phenotypic plasticity in foliose corals optimizes photosynthetic energy acquisition and is not simply a mechanism to increase light capture. We show that the optimal morphology is constrained at the boundaries of the environmental gradient, with non-optimal morphologies in these habitats having greatly reduced energy acquisition. However, at the center of the environmental gradient, flexibility in photophysiology allows energy acquisition to be very similar for multiple morphologies. Our results highlight the importance of phenotypic plasticity at multiple scales. Variation in overall morphology is important at niche boundaries at which conditions are consistently more stressful, whereas physiological flexibility is important in intermediate and less predictable habitats in which a rapid and reversible response to environmental fluctuations is required.     

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.     

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 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.     

Effects of temperature on morphological landmarks critical to growth and survival in larval Atlantic cod (Gadus morhua)

The morphology and function of structures important to energy acquisition were studied from spawning to the stage of transformation of larva to pelagic juvenile in Atlantic cod, Gadus morhua L., from December 1991 to July 1992. Fertilized eggs produced by adult fish from two genetically discrete populations (Newfoundland and Scotian Shelf) were raised under similar conditions in the laboratory at temperatures of 5 and 10°C. Subsamples of larvae were removed from cultures daily for 10 d, and then less frequently, and fixed for light microscopy and scanning electron microscopy. Nine functional morphological landmarks important to feeding, respiration and locomotion were chosen from observation of 280 ind. These landmarks defined 12 major developmental stages, from hatching to the pelagic juvenile stage. One of the feeding landmarks, intestinal stage, varied as a function of age and size and the variance in development was higher at 10°C than at 5°C; Newfoundland larvae developed more complex intestines than did Scotian Shelf larvae. In addition, Newfoundland larvae had significantly higher growth rates than those of Scotian Shelf larvae. Despite the higher growth rates and greater structural complexity of the intestine in Newfoundland larvae, the rate of yolk utilization was not significantly different between Newfoundland and Scotian Shelf larvae. Staging of respiratory landmarks showed that the gill arches were probably used preferentially in feeding while respiration was cutaneous. The gills, operculum and gill rakers developed late in larval life and accompanied the transition from cutaneous to branchial respiration. In the yolk-sac period, development of feeding and respiratory structures may be largely genetically controlled. During exogenous feeding, extrinsic factors also become important, as shown by the size and age-independent variation in intestinal development of larval cod raised at different temperatures.     

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.     

Chemical changes accompanying maturation of the connective tissue skeletons of gorgonian and antipatharian corals

The skeletons of 3 gorgonian and 2 antipatharian corals were subjected to quantitative chemical analysis. Protein values ranged from 70.4 to 93.6%; ash from 3.0 to 19.4%; lipid from 0 to 8.4%; carbohydrate from 1.24 to 3.94% and halogen from 4.2 to 24.9% of the dry skeletal weight. Hydroxyproline and phenolic values were 0 to 3.0% and 11.6 to 25.0% of the protein, respectively. Lipid, present in 2 gorgonian species and 1 antipatharian, significantly decreased with age in all three cases. Glucose and galactose accounted for over 90%, and sialic acids for an additional 1 to 10%, of the carbohydrate in the gorgonian skeletons studied; the glucose content of the gorgonian skeleton decreased with age. The antipatharian skeletons possessed no glucose or galactose, but contained significant levels of amino sugars; the presence of chitin is confirmed. In the gorgonians, bromine and iodine, the predominant halogens, increased with skeletal age and were present in nearly equal amounts. Small amounts of bromine were found in the antipatharian skeletons, but very large amounts of iodine were found in older parts of the skeleton. The basal regions of both antipatharian species contained >23% by weight of iodine, the highest content of iodine yet recorded for any organism.     

Short-term growth measurements of corals using an accurate buoyant weighing technique

An accurate method for determining the growth rates of the skeleton of isolated branch tips (nubbins) of corals over intervals of less than 24 h is described. The skeletal weight of the coral was estimated from its buoyant weight in seawater whose density had been accurately determined. The coral tissues accounted for between 1 and 5% of the total buoyant weight in Pocillopora verrucosa and Acropora humilis with differing relative tissue biomass. After correcting for tissue buoyant weight, predictions of skeletal weight were accurate to within 1%. The method was used to estimate the growth of sample nubbins of Porites porites of similar diameter, in 2 m of water at Discovery Bay, Jamaica. Since growth of these branch tips is apical, growth rate could be expressed without correction for the size. The mean 24 h skeletal growth rate ranged between 40 and 47 mg. Differences could be measured between day-time and night-time growth, the day: night ratio being 3.7. The method also showed that P. porites virtually ceases calcification during the 4 to 5 d periods that it becomes enclosed in a mucus tunic. Nubbins of P. porites attached to the reef at different locations showed clear differences in growth rate with depth, and between clear and turbid water sites. The growth rate of nubbins was compared with that of branch tips of whole corals by measuring the linear extension after staining with Alizarin Red S. After 3 1/2 mo, the mean linear extension was 4.1 mm in each case, indicating that the growth rate of nubbins is the same as that of branch tips of the whole colony. It is suggested that this buoyant weighing technique will find applications in laboratory experiments with calcification mechanisms and as a bioassay on reefs exposed to environmental stress.Contribution No. 464 of the Discovery Bay Marine Laboratory     

Elevated temperature and light enhance progression and spread of black band disease on staghorn corals of the Great Barrier Reef

Rates of progression and transmission of black band disease (BBD) on the staghorn coral, Acropora muricata, were compared between months for seasonal in situ studies and between temperature treatments in experimental aquaria manipulations at Lizard Island on the Great Barrier Reef (GBR). In situ field experiments demonstrated that BBD progressed along branches approximately twice as fast (1.7–2.4 times) during the austral summer month of January (0.99 ± 0.04 cm/day) than in the cooler months of July (0.58 ± 0.04 cm/day) and May (0.41 ± 0.07 cm/day). Transmission of BBD between colonies was also accelerated in warmer months, with signs of infection becoming visible 1.2 days earlier in January compared to May. The greater seawater temperatures by ∼2 to 3°C and light intensities by up to 650 μE/m²/s in January, suggest that rates of progression and transmission of BBD are linked to one or both of these parameters. Manipulative experiments in summer provide corroborative evidence that elevated temperatures increase rates of BBD progression, with the disease progressing 1.3 times more rapidly in the 32°C elevated temperature treatment than in the 30°C ambient treatment (1.17 ± 0.06 cm/day versus 0.92 ± 0.07 cm/day; F _2,6 = 7.66, P = 0.022). In contrast, although a trend for greatest BBD progression was measured in elevated temperature treatments of 29°C (0.46 ± 0.07 cm/day) and 31°C (0.52 ± 0.06 cm/day) in winter, these rates did not differ significantly (F _3,7 = 1.72, P = 0.249) from those measured for the ambient 27°C treatment (0.37 ± 0.06 cm/day) or the field controls (0.41 ± 0.09 cm/day). The lower rates of BBD progression in the 31°C winter treatment (0.52 ± 0.06 cm/day) than in the 30°C (0.92 ± 0.07 cm/day) summer treatment, may have been a response to 28-fold decreased light irradiance in the former, suggesting that high irradiance in combination with elevated temperatures may promote progression of BBD. Results from this study indicate that the impact of elevated temperature on BBD progression is complex with a combination of environmental factors including temperature and light playing key roles in progression and transmission of the disease.     

Shoreline morphological changes and the human factor. Case study of Accra Ghana

The interface between the sea and land is a very dynamic system that is always migrating landward or seaward. The landward migration results in the shoreline threatening coastal infrastructure and destroying the coastal environment. Coastal erosion has resulted in both social and economic problems. Coastal cities have also experienced increasing infrastructure development and population growth. This has resulted in a land “squeeze situation” in which both the shoreline and the “humanline” are competing for space along the coast. This struggle for space could result in serious environmental disaster as a result of the dynamics of the oceanic system, which could impact the immediate environs severely. The aim of this study was to determine if the rate of human encroachment of coastal lands for development exceed the rate at which the shoreline is moving inland as part of its natural cyclic behaviour. This study used 1985 aerial photographs and 2005 orthophoto map of the Accra western coast. Major land cover was identified, classified and overlayed in GIS environment. This enabled changes to be estimated. The shorelines were also digitised and the rate of change computed using the DSAS software. The results indicate that the estimated total area of land lost by human encroachment on the coastal land within the period under study is about 242,139.7 m2. However, the rate of land lost to human development is about 8,349.64 m2/year, which is relatively high. The historic rate of erosion computed for the period under study is about 1.92 m/year. Comparing the two rates indicates that human activities are moving closer to the shoreline as compared to the rate at which the shoreline is moving inland. This study recommends that setback lines should be put in place to protect lands for the shoreline’s cyclic activities.     

Self- and cross-fertilization in scleractinian corals

The mating patterns of four species of hermaphroditic scleractinian coral were investigated in November 1984 at Orpheus Island on the Great Barrier Reef, Australia. Each of the species shed eggs and sperm into the water, with subsequent external development of larvae. Studies of gamete viability indicated that cross-fertilizations were possible until at least 6 h after spawning.Montipora digitata cross-fertilized exclusively,Acropora tenuis, Goniastrea aspera andG. favulus were capable of self-fertilization, but to varying extents. In all species, cross-fertilization was the dominant mating pattern.     

Antimicrobial activity of Red Sea corals

Scleractinian corals and alcyonacean soft corals are the two most dominant groups of benthic marine organisms inhabiting the coral reefs of the Gulf of Eilat, northern Red Sea. Antimicrobial assays performed with extracts of six dominant Red Sea stony corals and six dominant soft corals against marine bacteria isolated from the seawater surrounding the corals revealed considerable variability in antimicrobial activity. The results demonstrated that, while the majority (83%) of Red Sea alcyonacean soft corals exhibited appreciable antimicrobial activity against marine bacteria isolated from the seawater surrounding the corals, the stony corals had little or no antimicrobial activity. From the active soft coral species examined, Xenia macrospiculata exhibited the highest and most potent antimicrobial activity. Bioassay-directed fractionation indicated that the antimicrobial activity was due to the presence of a range of compounds of different polarities. One of these antibiotic compounds was isolated and identified as desoxyhavannahine, with a minimum inhibitory concentration (MIC) of 48 μg ml⁻¹ against a marine bacterium. The results of the current study suggest that soft and hard corals have developed different means to combat potential microbial infections. Alcyonacean soft corals use chemical defense through the production of antibiotic compounds to combat microbial attack, whereas stony corals seem to rely on other means.     

Studies on reef corals. III. Fine structural changes of calicoblast cells in Pocillopora damicornis during settling and calcification

The site of reef-coral calcification has been studied in the branching coral Pocillopora damicornis Lamarck. Electron microscopy and X-ray microprobe analysis were performed on the calicoblast epidermis of newly settled larval stages and of adult coral. During settling, the heterogeneous columnar cell composition of the planktonic larva epidermis is replaced by a simple epithelium consisting of a single cell type, the calicoblast cell. Metamorphosis appears tightly linked to settling, with cell changes occurring within hours after attachment, and is marked by the appearance of a new secretory cell. The calicoblast cell of the adult coral is extremely flattened, and interdigitates extensively with adjacent calicoblast cells. This cell possesses a featureless plasma membrane lacking microvilli or flagella. It characteristically contains large membrane-bound vesicles with homogeneously fine granular contents. Preliminary microprobe analysis indicated a higher calcium content in these vesicles than in surrounding tissue; however, not in concentrations suggesting calcium-carbonate precipitation. They may represent sites of organic matrix synthesis. The calicoblast epidermis is separated from the underlying coral skeleton by a narrow gap. This gap appeared devoid of substructure, either organic or inorganic. The coral soft tissues are attached to the skeleton by mesogleal attachment processes, the desmoidal processes. These consist of a complex fibrous network originating in the mesoglea, and inserting onto the skeleton via specialized attachment regions consisting of electron-opaque membranous plaques. Skeletogenesis in reef-corals probably occurs extra-cellularly, external to the calicoblast epidermis, by simple overgrowth of the skeleton.     

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.     

Algal overgrowth of alcyonacean soft corals

Colonies of the soft coral Lobophytum pauciflorum (Ehrenberg, 1834) (Coelenterata: Octocorallia: Alcyonacea: Alcyoniidae), some of which were heavily overgrown by the algae Ceranium flaccidum (Kuetzing) Ardissone and Enteromorpha sp., and other minor epizoites, were collected at Taylor Reef (17°50S; 146°35E) in the Great Barrier Reef. Overgrown colonies contained the diterpene 2-epi-sarcophytoxide as the major secondary metabolite, while conspecific colonies with clean polyparies contained two diterpenes in approximately equal amounts: 14-hydroxycembra-1,3,7,11-tetraene and 15-hydroxycembra-1,3,7,11-tetraene. By contrast, twenty conspecific pairs of overgrown and clean colonies of other alcyoniid soft corals collected from Pelorus Channel, Palm Island Group (18°34S; 146°29E), showed no chemical differences within in the pairs. Cultures of a common species of Ceramium [C. codii (Richards) Mazoyer] were incubated with different concentrations of nine soft-coral-derived diterpenes and significant algal growth inhibition was observed in many cases. It appears that terpenoids from soft coral may contribute to the lack of epizoic organisms on soft-coral polyparies.     

Distribution,abundance and survival of juvenile hermatypic corals (Scleractinia) and the importance of life history strategies in the parent coral community

The distribution and abundance of juvenile corals were examined at depths from 3 to 37 m on the reefs of Curaçao and Bonaire (Netherlands Antilles). Juveniles of Agaricia agaricites were most abundant (60.6%), followed by Helioseris cucullata (8.3%). The large massive corals such as Montastrea annularis, M. cavernosa and branched species such as Madracis mirabilis and Acropora palmata had few juveniles. This, combined with species characteristics, shows that these species employ very different life history strategies. In some species the abundance of juveniles over the reef paralleled that of larger colonies, but not for example in Agaricia agaricites. The composition of the coral community was apparently no direct function of juvenile abundance. A change in angle of settlement of A. agaricites juveniles with increasing depth, from vertical to horizontal surfaces, seems to reflect the preferred light intensity. We studied the survival of juvenile corals during a half-year period. One-third remained unharmed, one-third died or disappeared, and one-third was limited in growth by factors such as spatial competition. This was the same for all depths, but factors influencing survival varied with depth.     

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.     

Patterns of Oil-Sediment rejection in corals

The patterns of oil-sediment rejection of 19 Caribbean hermatypic corals are identical to theri patterns of rejection of clean sediments. The rejection pattern is typical for coral species, and displays maximum and minimum rates dependent on the size and density of the oil-sediment particles. The viscosity of the oil determines the size of the oil-sediment particles. A coral's efficiency of rejection of sediment depends on the size and amount of the sediment particles. Oil drops 0.06 mm are removed by the coral's tissues. Physical contact with oil-sediment particles appears to be less harmful to corals than the toxic effects of oils.     

Proximity to competitors changes secondary metabolites of non-indigenous cup corals, Tubastraea spp., in the southwest Atlantic

Competition for space changes species’ distributions and community organization on tropical rocky shores, and the presence of secondary metabolites in the tissues of non-indigenous species may aid them in establishing and expanding their range through negative competitive interactions. The aim of this study was to describe the range of chemical substances produced by the non-indigenous cup corals Tubastraea coccinea and T. tagusensis and to test whether they varied in the field when the corals were placed in proximity to two local competitors. Cholest-5-en-3β-ol and 9-octadecanoic acid were two common secondary metabolites found in the tissues of Tubastraea. In the competition interaction experiment, necrosis was detected on the tissues of the coral Mussismilia hispida, and this species induced variation in sterol, alkaloid, and fatty acid production in Tubastraea tissues. In contrast, a sponge overgrew Tubastraea colonies. These results indicate that chemical defense may contribute to the ability of these non-indigenous corals to invade native communities.