Macroalgae Decrease Growth and Alter Microbial Community Structure of the Reef-Building Coral, Porites astreoides

With the continued and unprecedented decline of coral reefs worldwide, evaluating the factors that contribute to coral demise is of critical importance. As coral cover declines, macroalgae are becoming more common on tropical reefs. Interactions between these macroalgae and corals may alter the coral microbiome, which is thought to play an important role in colony health and survival. Together, such changes in benthic macroalgae and in the coral microbiome may result in a feedback mechanism that contributes to additional coral cover loss. To determine if macroalgae alter the coral microbiome, we conducted a field-based experiment in which the coral Porites astreoides was placed in competition with five species of macroalgae. Macroalgal contact increased variance in the coral-associated microbial community, and two algal species significantly altered microbial community composition. All macroalgae caused the disappearance of a γ-proteobacterium previously hypothesized to be an important mutualist of P. astreoides. Macroalgal contact also triggered: 1) increases or 2) decreases in microbial taxa already present in corals, 3) establishment of new taxa to the coral microbiome, and 4) vectoring and growth of microbial taxa from the macroalgae to the coral. Furthermore, macroalgal competition decreased coral growth rates by an average of 36.8%. Overall, this study found that competition between corals and certain species of macroalgae leads to an altered coral microbiome, providing a potential mechanism by which macroalgae-coral interactions reduce coral health and lead to coral loss on impacted reefs.

Acclimatization of the tropical reef coral Acropora millepora to hyperthermal stress

The demise of reef-building corals potentially lies on the horizon, given ongoing climate change amid other anthropogenic environmental stressors. If corals cannot acclimatize or adapt to changing conditions, dramatic declines in the extent and health of the living reefs are expected within the next half century. The primary and proximal global threat to corals is climate change. Reef-building corals are dependent upon a nutritional symbiosis with photosynthetic dinoflagellates belonging to the group Symbiodinium. . The symbiosis between the cnidarian host and algal partner is a stress-sensitive relationship; temperatures just 1°C above normal thermal maxima can result in the breakdown of the symbiosis, resulting in coral bleaching (the loss of Symbiodinium and/or associated photopigments) and ultimately, colony death. As ocean temperatures continue to rise, corals will either acclimatize or adapt to changing conditions, or will perish. By experimentally preconditioning the coral Acropora millepora via sublethal heat treatment, the coral acquired thermal tolerance, resisting bleaching during subsequent hyperthermal stress. The complex nature of the coral holobiont translates to multiple possible explanations for acclimatization: acquired thermal tolerance could potentially originate from the host itself, the Symbiodinium, or from the bacterial community associated with the coral. By examining the type of in hospite Symbiodinium and the bacterial community prior acclimation and after thermal challenge, it is shown that short-term acclimatization is not due to a distinct change in the dinoflagellate or prokaryote community. Though the microbial partnerships remain without considerable flux in preconditioned corals, the host transcriptome is dynamic. One dominant pattern was the apparent tuning of gene expression observed between preconditioned and non-preconditioned treatments, showing a modulated transcriptomic response to stress. Additionally several genes were upregulated in association with thermal tolerance, including antiapoptotic genes, lectins, and oxidative stress response genes. Upstream of two of these thermal tolerance genes, inhibitor of NFκB and mannose-binding lectin, DNA polymorphisms were identified which vary significantly between the northern and southern Great Barrier Reef. The impact of these mutations in putative promoter regions remains to be seen, but variation across thermally-disparate geography serves to generate hypotheses regarding the role of regulatory element evolution in a coral adaptation context.

Physiological and ecological variables measured at the high and low pCO2 reef sections

Experiments have shown that ocean acidification due to rising atmospheric carbon dioxide concentrations has deleterious effects on the performance of many marine organisms. However, few empirical or modelling studies have addressed the long-term consequences of ocean acidification for marine ecosystems. Here we show that as pH declines from 8.1 to 7.8 (the change expected if atmospheric carbon dioxide concentrations increase from 390 to 750 ppm, consistent with some scenarios for the end of this century) some organisms benefit, but many more lose out. We investigated coral reefs, seagrasses and sediments that are acclimatized to low pH at three cool and shallow volcanic carbon dioxide seeps in Papua New Guinea. At reduced pH, we observed reductions in coral diversity, recruitment and abundances of structurally complex framework builders, and shifts in competitive interactions between taxa. However, coral cover remained constant between pH 8.1 and ~7.8, because massive Porites corals established dominance over structural corals, despite low rates of calcification. Reef development ceased below pH 7.7. Our empirical data from this unique field setting confirm model predictions that ocean acidification, together with temperature stress, will probably lead to severely reduced diversity, structural complexity and resilience of Indo-Pacific coral reefs within this century.

Two “pillars” of cold-water coral reefs along Atlantic European margins: Prevalent association of Madrepora oculata with Lophelia pertusa, from reef to colony scale

The scleractinian coral Lophelia pertusa has been the focus of deep-sea research since the recognition of the vast extent of coral reefs in North Atlantic waters two decades ago, long after their existence was mentioned by fishermen. These reefs where shown to provide habitat, concentrate biomass and act as feeding or nursery grounds for many species, including those targeted by commercial fisheries. Thus, the attention given to this cold-water coral (CWC) species from researchers and the wider public has increased. Consequently, new research programs triggered research to determine the full extent of the corals geographic distribution and ecological dynamics of “Lophelia reefs”. The present study is based on a systematic standardised sampling design to analyse the distribution and coverage of CWC reefs along European margins from the Bay of Biscay to Iceland. Based on Remotely Operated Vehicle (ROV) image analysis, we report an almost systematic occurrence of Madrepora oculata in association with L. pertusa with similar abundances of both species within explored reefs, despite a tendency of increased abundance of L. pertusa compared to M. oculata toward higher latitudes. This systematic association occasionally reached the colony scale, with “twin” colonies of both species often observed growing next to each other when isolated structures were occurring off-reefs. Finally, several “false chimaera” were observed within reefs, confirming that colonial structures can be “coral bushes” formed by an accumulation of multiple colonies even at the inter-specific scale, with no need for self-recognition mechanisms. Thus, we underline the importance of the hitherto underexplored M. oculata in the Eastern Atlantic, re-establishing a more balanced view that both species and their yet unknown interactions are required to better elucidate the ecology, dynamics and fate of European CWC reefs in a changing environment.

Sweeper polyps of the coral Goniopora tenuidens (Scleractinia : Poritidae)

The massive coral Goniopora tenuidens can develop elongated sweeper polyps. These are thought to be involved in aggressive interactions with neighbouring benthic organ isms, like the sweeper tentacles of other corals. The cnidoms of sweeper polyps and ordinary polyps of G. tenuidens from the Great Barrier Reef were compared. Sweeper polyps had significantly greater densities of elongate holotrichous isorhizas (34577 +/- 3839/mg; mean +/- SD, n = 6) than ordinary polyps (936 +/- 371/mg; p < 0.05), while ordinary polyps had significantly greater densities of spirocysts (75994 +/- 15992/mg) than sweeper polyps (19469 +/- 7808/mg; p < 0.05). This suggests that sweeper polyps of G. tenuidens, like the sweeper tentacles of other corals, are modified for aggression, and that they probably act through nematocyst discharge. However, the scattered distribution of sweeper polyps observed on colonies of G. tenuidens in the field suggests that sweeper polyps may have other functions.

Effects of cyanide on coral photosynthesis: implications for identifying the cause of coral bleaching and for assessing the environmental effects of cyanide fishing

Modulated chlorophyll fluorescence techniques were used to examine the effects of cyanide (NaCN) from cyanide fishing on photosynthesis of the symbiotic algae (zooxanthellae) located within the tissues of the zooxanthellate hard coral Plesiastrea versipora. Incubating corals for 3 h in a cyanide concentration of >10(-5) M NaCN under a saturating light intensity (photosynthetically active radiation [PAR] intensity of 250 mu mol quanta m(-2) s(-1)) caused a long-term decrease in the ratio of variable to maximal fluorescence (dark-adapted F-v/F-m). The effect of cyanide on dark-adapted F-v/F-m was Light dependent; thus F-v/F-m only decreased in corals exposed to 10(-4) M NaCN for 3 h under PAR of 250 mu mol quanta m(-2) s(-1). In corals where dark-adapted F-v/F-m was significantly lowered by cyanide exposure, we observed significant loss of zooxanthellae from the tissues. causing the corals to discolour (bleach). To further examine the light-dependent effect of cyanide and its relation to loss of zooxanthellae, corals were exposed to 10-4 M NaCN or seawater only (control), either in darkness or under 250 mu mol quanta m(-2) s(-1). ill significant decrease in dark-adapted F-v/F-m and loss of zooxanthellae only occurred in corals exposed to cyanide in the light. These results suggest cyanide causes the dissociation of the symbiosis (bleaching) by affecting photosynthesis of the zooxanthellae. Quenching analysis using the saturation-pulse technique revealed the development of high levels of non-photochemical quenching in cyanide-exposed coral. This result is consistent with the known property of cyanide as an inhibitor of the dark reactions of the Calvin cycle, specifically as an inhibitor of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco). Therefore, chronic photoinhibition and an impairment of photosynthesis of zooxanthellae provides an important 'signal' to examine the environmental effects of cyanide fishing during controlled releases in situ.

Climate change, coral bleaching and the future of the world's coral reefs

Sea temperatures in many tropical regions have increased by almost 1 degrees C over the past 100 years, and are currently increasing at similar to 1-2 degrees C per century. Coral bleaching occurs when the thermal tolerance of corals and their photosynthetic symbionts (zooxanthellae) is exceeded. Mass coral bleaching has occurred in association with episodes of elevated sea temperatures over the past 20 years and involves the loss of the zooxanthellae following chronic photoinhibition. Mass bleaching has resulted in significant losses of live coral in many parts of the world. This paper considers the biochemical, physiological and ecological perspectives of coral bleaching. It also uses the outputs of four runs from three models of global climate change which simulate changes in sea temperature and hence how the frequency and intensity of bleaching events will change over the next 100 years. The results suggest that the thermal tolerances of reef-building corals are likely to be exceeded every year within the next few decades. Events as severe as the 1998 event, the worst on record, are likely to become commonplace within 20 years. Most information suggests that the capacity for acclimation by corals has already been exceeded, and that adaptation will be too slow to avert a decline in the quality of the world's reefs. The rapidity of the changes that are predicted indicates a major problem for tropical marine ecosystems and suggests that unrestrained warming cannot occur without the loss and degradation of coral reefs on a global scale.

Changes in quantum efficiency of Photosystem II of symbiotic dinoflagellates of corals after heat stress, and of bleached corals sampled after the 1998 Great Barrier Reef mass bleaching event Ross J. Jones , Selina Ward, Affendi Yang Amri and Ove Hoegh-Guldberg

Pulse-amplitude-modulation chlorophyll fluorometry was used to examine changes in dark-adapted F-v/F-m of endosymbiotic dinoflagellate microalgae within the tissues of the temperate coral Plesiastrea versipora exposed to elevated seawater temperature. The F-v/F-m was markedly reduced following exposure of corals to 28 degrees C for 48 h. When corals were returned to ambient (24 degrees C) conditions, F-v/F-m increased in an initial rapid and then secondary slower phase. Tissue discolouration (coral bleaching), caused by a significant decrease in the density of algae, was observed during the first 2-3 days of the recovery period. After 14 days, F-v/F-m was still significantly lower than in control corals. The recovery of F-v/F-m is discussed in terms of repair processes within the symbiotic algae, division of healthy algae and also the selective removal of photo-damaged dinoflagellates. Under field conditions, bleached corals sampled at Heron Island Reef during a bleaching event had significantly lower F-v/F-m than non-bleached colonies; four months after the bleaching event, there were no differences in F-v/F-m or algal density in corals marked as having bleached or having shown no signs of colour loss. The results of this laboratory and field study are consistent with the hypothesis that an impairment of photosynthesis occurs during heat-stress, and is the underlying cause of coral bleaching.

Low symbiont diversity in southern Great Barrier Reef corals, relative to those of the Caribbean

The specific identity of endosymbiotic dinoflagellates (Symbiodinium spp.) from most zooxanthellate corals is unknown. In a survey of symbiotic cnidarians from the southern Great Barrier Reef (GBR), 23 symbiont types were identified from 86 host species representing 40 genera. A majority (>85%) of these symbionts belong to a single phylogenetic clade or subgenus (C) composed of closely related (as assessed by sequence data from the internal transcribed spacer region and the ribosomal large subunit gene), yet ecologically and physiologically distinct, types. A few prevalent symbiont types, or generalists, dominate the coral community of the southern GBR, whereas many rare and/or specific symbionts, or specialists, are found uniquely within certain host taxa. The comparison of symbiont diversity between southern GBR and Caribbean reefs shows an inverse relationship between coral diversity and symbiont diversity, perhaps as a consequence of more-rapid diversification of Caribbean symbionts. Among clade C types, generalists C1 and C3 are common to both Caribbean and southern GBR symbiont assemblages, whereas the rest are regionally endemic. Possibly because of environmental changes in the Caribbean after geographic isolation through the Quaternary period, a high proportion of Caribbean fauna associate with symbiont taxa from two other distantly related Symbiodinium clades (A and B) that rarely occur in Pacific hosts. The resilience of Porites spp. and the resistance of Montipora digitata to thermal stress and bleaching are partially explained by their association with a thermally tolerant symbiont type, whereas the indiscriminant widespread bleaching and death among certain Pacific corals, during El Nino Southern Oscillation events, are influenced by associations with symbionts possessing higher sensitivity to thermal stress.

Nutrient-induced perturbations to delta C-13 and delta N-15 in symbiotic dinoilagellates and their coral hosts

Inorganic nutrients play a critical role in determining benthic community structure in tropical seas. This study examined the impact of adding inorganic nutrients (ammonium and phosphate) on the isotopic composition of 2 reef-building corals, Pocillopora damicornis and Heliofungia actiniformis, on the southern Great Barrier Reef. The addition of elevated nutrients to patch reefs that pond at low tide did not perturb the C:N ratio of either species or their symbiotic dinoflagellates. The C:N ratios were significantly higher in material extracted from the skeleton (14.8 +/- 1.50 and 10.8 +/- 1.42) than either host (7.6 +/- 0.87 and 6.0 +/- 0.71) or symbiotic dinoflagellates (5.7 +/- 0.48 and 6.9 +/- 0.66) (P. damicornis and H. actiniformis respectively; 95 confidence intervals). The ratio of acquired N to background N suggests that the added dissolved inorganic nitrogen (DIN) accounted for 50 to 100% of total nitrogen within the tissues of P. damicornis and H. actiniformis at the end of the experiment. The addition of the isotopically depleted nutrients (delta(15) N = 0parts per thousand) to patch reefs significantly decreased delta(15)N from control values of between 3 and 4 to values to below 1 in the case of all compartments, while delta(13)C values were relatively unresponsive to nutrient treatments. These findings suggest that coral delta(15)N has the potential to provide a historical record of the delta(15)N of dissolved nitrogen surrounding reef-building corals and their symbiotic dinoflagellates.

Major colour patterns of reef-building corals are due to a family of GFP-like proteins

Reef-building corals are renowned for their brilliant colours yet the biochemical basis for the pigmentation of corals is unknown. Here, we show that these colours are due to a family of GFP-like proteins that fluoresce under ultraviolet (UV) or visible light. Pigments from ten coral species were almost identical to pocilloporin (Dove et al. 1995) being dimers or trimers with approximately 28-kDa subunits. Degenerative primers made to common N-terminal sequences yielded a complete sequence from reef-building coral cDNA, which had 19.6% amino acid identity with green fluorescent protein (GFP). Molecular modelling revealed a 'beta -can' structure, like GFP, with 11 beta -strands and a completely solvent-inaccessible fluorophore composed of the modified residues Gln-61, Tyr-62 and Gly-63. The molecular properties of pocilloporins indicate a range of functions from the conversion of high-intensity UV radiation into photosynthetically active radiation (PAR) that can be regulated by the dinoflagellate peridinin-chlorophyll-protein (PCP) complex, to the shielding of the Soret and Q(x) bands of chlorophyll a and c from scattered high-intensity light. These properties of pocilloporin support its potential role in protecting the photosynthetic machinery of the symbiotic dinoflagellates of corals under high light conditions and in enhancing the availability of photosynthetic light under shade conditions.

Genetic variability of the symbiotic dinoflagellates from the wide ranging coral species Seriatopora hystrix and Acropora longicyathus in the Indo-West Pacific

The scleractinian coral species, Seriatopora hystrix and Acropora longicyathus, are widely distributed throughout the latitudinal range of the tropical west Pacific. These 2 coral species live in a mutually beneficial relation with symbiotic dinoflagellates (zooxanthellae), which are passed to their progeny by vertical transmission (zooxanthellate eggs or larvae) and horizontal transmission (eggs or larvae that acquire symbionts from the environment), respectively. For S. hystrix, vertical transmission might create biogeographically isolated and genetically differentiated symbiont populations because the extent of its larval migration is known to be limited. On the other hand, horizontal transmission in corals such as A. longicyathus may result in genetically connected symbiont populations, especially if its zooxanthellae taxa are widely distributed. To examine these hypotheses, symbionts were collected from colonies of S. hystrix and A. longicyathus living in the Great Barrier Reef (Australia), South China Sea (Malaysia) and East China Sea (Ryukyus Archipelago, Japan), and were examined using restriction fragment length polymorphism and sequence analysis of large and small subunit rRNA genes. Phylogenetic analysis assigned the symbionts to 1 of 3 taxonomically distinct groups, known as clades. Symbionts from Australian and Japanese S. hystrix were placed in Clade C, and Malaysian S. hystrix symbionts in the newly described Clade D. Seven of 11 Australian and all Japanese and Malaysian colonies of A. longicyathus had symbiotic dinoflagellates that also grouped with Clade C, but symbionts from the remaining Australian colonies of A. longicyathus grouped with Clade A. Analysis of molecular variance of Clade C symbionts found significant genetic variation in 1 or more geographic groups (69.8%) and to a lesser extent among populations within geographic regions (13.6%). All populations of Clade C symbionts from S. hystrix were genetically differentiated according to geographic region. Although Clade C symbionts of A. longicyathus from Japan resolved into a distinct geographic group, those from Australia and Malaysia did not and were genetically connected. We propose that these patterns of genetic connectivity correlate with differences in the dispersal range of the coral or symbiont propagules and are associated with their respective modes of symbiont transmission.

Response of a scleractinian coral, Stylophora pistillata, to iron and nitrate enrichment

The purpose of this study was to determine whether the addition of iron alone or in combination with nitrate affects growth and photosynthesis of the scleractinian coral, Stylophora pistillata, and its symbiotic dinoflagellates. For this purpose, we used three series of two tanks for a 3-week enrichment with iron (Fe), nitrate (N) and nitrate + iron (NFe). Two other tanks were kept as a control (C). Stock solutions of FeCl3 and NaNO3 were diluted to final concentrations of 6 nM Fe and 2 muM N and continuously pumped from batch tanks into the experimental tanks with a peristaltic pump. Results obtained showed that iron addition induced a significant increase in the areal density of zooxanthellae (ANOVA, p = 0.0013; change from 6.3 +/- 0.7 x 10(5) in the control to 8.5 +/- 0.6 x 10(5) with iron). Maximal gross photosynthetic rates normalized per surface area also significantly increased following iron enrichment (ANOVA, p = 0.02; change from 1.23 +/- 0.08 for the control colonies to 1.81 +/- 0.24 mu mol O-2 cm(-2) h(-1) for the iron-enriched colonies). There was, however, no significant difference in the photosynthesis normalized on a per cell basis. Nitrate enrichment alone (2 muM) did not significantly change the zooxanthellae density or the rates of photosynthesis. Nutrient addition (both iron and nitrogen) increased the cell-specific density of the algae (CSD) compared to the control (G-test, p = 0.3 x 10(-9)), with an increase in the number of doublets and triplets. CSD was equal to 1.70 +/- 0.04 in the Fe-enriched colonies, 1.54 +/- 0.12 in the N- and NFe-enriched colonies and 1.37 +/- 0.02 in the control. Growth rates measured after 3 weeks in colonies enriched with Fe, N and NFe were 23%, 34% and 40% lower than those obtained in control colonies (ANOVA. p = 0.011). (C) 2001 Elsevier Science B.V. All rights reserved.

Diurnal changes in the photochemical efficiency of the symbiotic dinoflagellates (Dinophyceae) of corals: photoprotection, photoinactivation and the relationship to coral bleaching

The photochemical efficiency of symbiotic dinoflagellates within the tissues of two reef-building corals in response to normal and excess irradiance at wafer temperatures < 30 C were investigated using pulse amplitude modulated (PAM) chlorophyll fluorescence techniques, Dark-adapted F-v/F-m showed clear diurnal changes, decreasing to a low at solar noon and increasing in the afternoon. However, F-v/F-m also drifted downwards at night or in prolonged darkness, and increased rapidly during the early morning twilight. This parameter also increased when the oxygen concentration of the wafer holding the corals was increased. Such changes have not been described previously, and most probably reflect state transition's associated with PQ pool reduction via chlororespiration. These unusual characteristics may be a feature of an endosymbiotic environment, reflective of the well-documented night-time tissue hypoxia that occurs in corals. F-v/F-m decreased to 0.25 in response to full sunlight in shade-acclimated (shade) colonies of Stylophora pistillata, which is considerably lower than in light-acclimated (sun) colonies. In sun colonies, the reversible decrease in F-v/F-m was caused by a lowering of F-m and F-o suggesting photoprotection and no lasting damage. The decrease in F-v/F-m, however, was caused by a decrease in F-m and an increase in F-o in shade colonies suggesting photoinactivation and long-term cumulative photoinhibition. Shade colonies rapidly lost their symbiotic algae (bleached) during exposure to full sunlight. This study is consistent with the hypothesis that excess light leads to chronic damage of symbiotic dinoflagellates and their eventual removal from reef-building corals. It is significant that this can occur with high light conditions alone.