Increased mortality and photoinhibition in the symbiotic dinoflagellates of the Indo–Pacific coral Stylophora pistillata (Esper) after summer bleaching

Coral bleaching (the loss of symbiotic dinoflagellates from reef-building corals) is most frequently caused by high-light and temperature conditions. We exposed the explants of the hermatypic coral Stylophora pistillata to four combinations of light and temperature in late spring and also in late summer. During mid-summer, two NOAA bleaching warnings were issued for Heron Island reef (Southern Great Barrier Reef, Australia) when sea temperature exceeded the NOAA bleaching threshold, and a ‘mild’ (in terms of the whole coral community) bleaching event occurred, resulting in widespread S. pistillata bleaching and mortality. Symbiotic dinoflagellate biomass decreased by more than half from late spring to late summer (from 2.5×10⁶ to 0.8×10⁶ dinoflagellates cm² coral tissue), and those dinoflagellates that remained after summer became photoinhibited more readily (dark-adapted F _V : F _M decreased to (0.3 compared with 0.4 in spring), and died in greater numbers (up to 17% dinoflagellate mortality compared with 5% in the spring) when exposed to artificially elevated light and temperature. Adding exogenous antioxidants (d-mannitol and l-ascorbic acid) to the water surrounding the coral had no clear effect on either photoinhibition or symbiont mortality. These data show that light and temperature stress cause mortality of the dinoflagellate symbionts within the coral, and that susceptibility to light and temperature stress is strongly related to coral condition. Photoinhibitory mechanisms are clearly involved, and will increase through a positive feedback mechanism: symbiont loss promotes further symbiont loss as the light microenvironment becomes progressively harsher.     

Photoinhibition of Symbiodinium spp. within the reef corals Montastraea faveolata and Porites astreoides: implications for coral bleaching

It is speculated that differences in coral bleaching susceptibility may be influenced by the genotype of in hospite Symbiodinium and their differential responses to bleaching stressors. Photoinhibition of photosystem II (PSII), damage to the D1 (psbA) PSII reaction centre protein and production of reactive oxygen species by in hospite Symbiodinium are likely precursors of coral bleaching. In order to assess whether photorepair rates of in hospite Symbiodinium underlie the bleaching susceptibility of their hosts, photoinhibition (net and gross), photoprotection and photorepair rates were assessed in a bleaching-‘tolerant’ coral (P. astreoides) and a bleaching-‘sensitive’ coral (M. faveolata) using non-invasive fluorometric techniques and by blocking de novo synthesis of psbA. Previous studies using such techniques have demonstrated that in vitro Symbiodinium types ‘sensitive’ to bleaching stressors had reduced rates of photorepair relative to ‘tolerant’ Symbiodinum types. Our measurements demonstrated that Symbiodinium in the more bleaching tolerant P. astreoides had higher photorepair rates than Symbiodinium in M. faveolata. Higher repair rates in P. astreoides resulted in lower net photoinhibition relative to M. faveolata, where both corals exhibited similar susceptibility to photodamage (gross photoinhibition). Photoprotective mechanisms were observed in both corals; M. faveolata exhibited higher antennae-bed quenching than P. astreoides at low-light intensities, but at and above light-saturating intensities, which are different for each coral species, P. astreoides displayed more efficient non-photochemical quenching (Stern–Volmer quenching) of chlorophyll fluorescence than M. faveolata. Increased NPQ by P. astreoides at E/E _k ≥ 1 was not driven by antennae-bed quenching. The ability of in hospite Symbiodinium in P. astreoides to mitigate the effects of photoinhibition under high light conditions compared with Symbiodinium in M. faveolata, and their high repair capacity following photoinhibition, may be a key factor to consider in future bleaching studies and may underlie the relative bleaching tolerance of P. astreoides compared to M. faveolata.     

PSII activity and pigment dynamics of Symbiodinium in two Indo-Pacific corals exposed to short-term high-light stress

This study examined the capacity for photoprotection and repair of photo-inactivated photosystem II in the same Symbiodinium clade associated with two coexisting coral species during high-light stress in order to test for the modulation of the symbiont’s photobiological response by the coral host. After 4 days exposure to in situ irradiance, symbionts of the bleaching-sensitive Pocillopora damicornis showed rapid synthesis of photoprotective pigments (by 44 %) and strongly enhanced rates of xanthophyll cycling (by 446 %) while being insufficient to prevent photoinhibition (sustained loss in F _v/F _m at night) and loss of symbionts after 4 days. By contrast, Pavona decussata showed no significant changes in F _v/F _m, symbiont density or xanthophyll cycling. Given the association with the same Symbiodinium clade in both coral species, our findings suggest that symbionts in the two species examined may experience different in hospite light conditions as a result of different biometric properties of the coral host.     

Symbiont specificity and bleaching susceptibility among soft corals in the 1998 Great Barrier Reef mass coral bleaching event

Considerable variability in bleaching was observed within and among soft coral taxa in the order Alcyonacea (Octocorallia: Cnidaria) on the central Great Barrier Reef (GBR, latitude 18.2°–19.0°S, longitude 146.4°–147.3°E) during the 1998 mass coral bleaching event. In April 1998, during a period of high sea surface temperatures, tissue samples were taken from bleached and unbleached colonies representative of 17 soft coral genera. The genetic identities of intracellular dinoflagellates (Symbiodinium spp.) in these samples were analyzed using PCR-denaturing gradient gel electrophoresis fingerprinting analysis of the internal transcribed spacer regions 1 and 2. Alcyonaceans from the GBR exhibited a high level of symbiont specificity for Symbiodinium types mostly in clade C. A rare clade D type (D3) was associated only with Clavularia koellikeri, while Nephthea sp. hosted symbionts in clade B (B1n and B36). Homogenous Symbiodinium clade populations were detected in all but one colony. Colonies that appeared bleached possessed symbiont types that were genetically indistinguishable from those in nonbleached conspecifics. These data suggest that parameters other than the resident endosymbionts such as host identity and colony acclimatization are important in determining bleaching susceptibility among soft corals. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

The effects of an abnormal decrease in temperature on the Eastern Pacific reef-building coral Pocillopora verrucosa

Coral bleaching events are associated with abnormal increases in temperature, such as those produced during El Niño. Recently, a breakdown in the coral–dinoflagellate (genus Symbiodinium) endosymbiosis has been documented in corals exposed to anomalously cold-water temperatures associated with La Niña events. Given the ecological significance of such events, as well as the threat of global climate change, surprisingly little is known about the physiological response of corals to cold stress. This study evaluated some physiological effects of continuous temperature decline in colonies of the eastern Pacific reef-building coral Pocillopora verrucosa. Twenty days of incubation at 18.5–19.0 °C resulted in a substantial decrease in holobiont lipid and Chla content, as well as an increase in Symbiodinium density. These observations suggest a combination of symbiont acclimation due to the temperature decline and reallocation of carbon toward algal growth as opposed to translocation to the host coral. With a decreased availability of symbiont-derived carbon, the coral likely catabolized storage lipids in order to survive the stress event. Despite this stress and some tissue necrosis, no mortality was noted and corals recovered quickly when returned to the ambient temperature. As these results are in marked contrast to similar studies investigating elevated temperature on this coral from this same location, Pocillopora in the Mexican Central Pacific may be more prone to long-term damage and mortality during periods of ocean warming as opposed to ocean cooling.     

Comparing environmental influences on coral bleaching across and within species using clustered binomial regression

Differential susceptibility among reef-building coral species can lead to community shifts and loss of diversity as a result of temperature-induced mass bleaching events. We evaluate environmental influences on coral colony bleaching over an 8-year period in the Florida Keys, USA. Clustered binomial regression is used to develop models incorporating taxon-specific responses to the environment in order to identify conditions and species for which bleaching is likely to be severe. By building three separate models incorporating environment, community composition, and taxon-specific responses to environment, we show observed prevalence of bleaching reflects an interaction between community composition and local environmental conditions. Environmental variables, including elevated sea temperature, solar radiation, and reef depth, explained 90% and 78% of variability in colony bleaching across space and time, respectively. The effects of environmental variables were only partially explained (33% of variability) by corresponding differences in community composition. Taxon-specific models indicated individual coral species responded differently to local environmental conditions and had different sensitivities to temperature-induced bleaching. For many coral species, but not all, bleaching was exacerbated by high solar radiation. A 25% reduction in the probability of bleaching in shallow locations for one species may reflect an ability to acclimatize to local conditions. Overall, model results indicate predictions of coral bleaching require knowledge of not just the environmental conditions or community composition, but the responses of individual species to the environment. Model development provides a useful tool for coral reef management by quantifying the influence of the local environment on individual species bleaching sensitivities, identifying susceptible species, and predicting the likelihood of mass bleaching events with changing environmental conditions.     

Seasonal fluctuations in the photosynthetic capacity of photosystem II in symbiotic dinoflagellates in the Caribbean reef-building coral <Emphasis Type="Italic">Montastraea</Emphasis>

The photosynthetic capacity of photosystem II (PS II) in symbiotic dinoflagellates (Symbiodinium sp.), as measured by analysis of chlorophyll fluorescence, was investigated in the primary Caribbean reef-building corals, Montastraea annularis and Montastraea faveolata, for 5 years and Montastraea franksi over 2 years in the Bahamas. Significant seasonal fluctuations in the quantum yield of charge separation (F_v/F_m) of PS II were found in all species at all depths, with the highest photosynthetic capacity consistently recorded between mid-winter and early spring and the lowest photosynthetic capacity occurring in the mid to late summer. Corals residing in shallow depths of 1-2 m showed the greatest fluctuations in F_v/F_m, whereas deeper corals (3-4 and 14 m depths) had consistently higher values of F_v/F_m. Densities of symbiotic dinoflagellates and photosynthetic pigments followed a similar pattern. Fluctuations of photosynthetic capacity showed a strong correlation with seasonal patterns of water temperature and light. Such seasonal shifts in photosynthetic capacity are most likely due to several biochemical processes in the algae that lead to alterations of both photoprotection and photodamage. While symbiont density changed significantly on a seasonal basis, visual signs of coral bleaching were noted only in the fall of 1995 and the spring and summer of 1998. Comparisons of photosynthetic capacity and the decrease in the number of symbionts and their subsequent recovery indicated that symbiont populations in this study had the ability to recover quickly following bleaching events, as long as continued physical perturbation (e.g. thermal stress) did not shorten the recovery phase. Large-scale bleaching events are best viewed as the end points of seasonal physiological variation in which photosynthetic capacity and density of symbiotic dinoflagellates are reduced to a lower level than during "non-bleaching" years.     

Symbiont shuffling during thermal bleaching and recovery in the sea anemone Entacmaea quadricolor

The sea anemone Entacmaea quadricolor simultaneously harbours multiple symbiont types from the genus Symbiodinium, while providing essential habitat for anemonefish. This anemone lives close to its upper thermal threshold and experiences bleaching under elevated temperature and light stress. Here, we determine whether E. quadricolor experienced a shuffling in the abundance of two genetically distinct symbiont types (Symbiodinium C25 and C3.25) during bleaching and recovery. Anemones were exposed to control (22.9 °C) or elevated temperature (28.5 °C) for 42 days, whereas for the following 75 days, all anemones were exposed to 22.9 °C. By day 47, a more pronounced bleaching occurred via symbiont expulsion in the elevated temperature treatment than the control, and the proportion of C25 to C25 + C3.25 increased by 6.2 and 13.2 % in the control and bleached anemones, respectively. The increased relative abundance of C25 to C3.25 after exposure to thermal stress may indicate that C3.25 performs poorly when temperature is elevated. Although no significant recovery in symbiont density was detected, a revival of the C3.25 genotype was found at day 117, which may indicate that it is either more competitive or has qualities that are beneficial to the symbiosis when thermal stress is no longer apparent. This work demonstrates the potential for this anemone species to shuffle its symbiont types in response to environmental change and could provide resilience during times of stress.     

Lipids and stable carbon isotopes in two species of Hawaiian corals,<Emphasis Type="Italic"> Porites compressa</Emphasis> and<Emphasis Type="Italic"> Montipora verrucosa</Emphasis>, following a bleaching event

Mass coral bleaching events have occurred on a global scale throughout the worlds tropical oceans and can result in large-scale coral mortality and degradation of coral reef communities. Coral bleaching has often been attributed to periods of above normal seawater temperatures and/or calm conditions with high levels of ultraviolet radiation. Unusually high shallow-water temperature (>29°C) in Kaneohe Bay, Hawaii, USA, in late summer (20 August–9 September) and fall (1–7 October) of 1996 produced visible bleaching of two dominant corals, Porites compressa Dana, 1864 and Montipora verrucosa Dana, 1864. The present study examined chlorophyll a (chl a), total lipid concentrations, and lipid class composition in corals of both species in which the entire colony was non-bleached, moderately bleached, or bleached. Skeletal, host tissue, and algal symbiont ¹³C values were also measured in non-bleached and bleached colonies. In additional unevenly bleached colonies, paired samples were collected from bleached upper surfaces and non-bleached sides. Samples were collected on 20 November 1996 during the coral recovery phase, a time when seawater temperatures had been back to normal for over a month. Chl a levels were significantly lower in bleached colonies of both species compared with non-bleached specimens, and in bleached areas of unevenly bleached single colonies. Total lipid concentrations were significantly lower in bleached P. compressa compared with non-bleached colonies, whereas total lipid concentrations were the same in bleached and non-bleached M. verrucosa colonies. The proportion of triacylglycerols and wax esters was lower in bleached colonies of both species. Both bleached and non-bleached M. verrucosa had from ~17% to 35% of their lipids in the form of diacylglycerol, while this class was absent in P. compressa. ¹³C was not significantly different in the host tissue and algal symbiont fractions in non-bleached and bleached samples of either species. This suggests that the ratio of carbon acquired heterotrophically versus photosynthetically was the same regardless of condition. Skeletal ¹³C was significantly lower in bleached than in non-bleached corals. This is consistent with previous findings that lower rates of photosynthesis during bleaching results in lower skeletal ¹³C values. The two species in this study displayed different lipid class compositions and total lipid depletions following bleaching, suggesting that there is a difference in their metabolism of lipid reserves and/or in their temporal responses to bleaching and recovery.Communicated by J.P. Grassle, New Brunswick     

High genetic diversity of the symbiotic dinoflagellates in the coral Pocillopora meandrina from the South Pacific

Symbioses between dinoflagellates in the genus Symbiodinium (commonly referred to as zooxanthellae) and scleractinian corals are an essential feature for the maintenance of coral reefs. The fine-scale diversity and population structure of the zooxanthellae inhabiting the coral Pocillopora meandrina, a major reef building species in Polynesia, was examined. We used two polymorphic microsatellites to study seven populations from the South Pacific, whose host structuring has been previously investigated. The symbionts of P. meandrina showed high levels of diversity, with more than one zooxanthella genotype being identified in most of the host individuals. Genetic differentiation between symbiont populations was detected at a large scale (2,000 km) between the Tonga and the Society Archipelagos. Within the Society Archipelago, the two most remote populations (Tahiti and Bora-Bora; 200 km apart) were only weakly differentiated from each other. Statistical tests demonstrated that the symbiont genetic structure was not correlated with that of its host, suggesting that dispersal of the symbionts, whether they are transported within a host larva or free in the water, depends mainly on distance and water currents. In addition, the data suggests that hosts may acquire new symbionts after maternal transmission, possibly following a disturbance event. Lastly, the weak differentiation between symbiont populations of P. verrucosa and P. meandrina, both from Moorea, indicated that there was some host-symbiont fine-scale specificity detectable at the genetic resolution offered by microsatellites.     

There are many ways to be a mutualist: endophytic fungus reduces plant survival but increases population growth

One of the challenges to quantifying the costs and benefits of symbiosis is that symbionts can influence different components of host fitness. To improve understanding of the ecology of inherited symbionts, we developed general theory for a perennial host-hereditary symbiont interaction, in which symbionts can have independent and potentially opposing effects on host regeneration and survival. The model showed that negative effects on one component of fitness may be outweighed by positive effects on another, leading to a net positive impact of symbiosis on population growth. Model predictions depended on the availability of suitable patches, which influenced the relative contributions of survival vs. regeneration to host fitness. We then used experimental symbiont removal to quantify effects of a hereditary, fungal endophyte on a grass host. Endophyte presence strongly reduced host survival but increased regeneration. Application of the model revealed that negative effects on plant survival were overwhelmed by beneficial effects on regeneration, resulting in stable endophyte persistence at 100% frequency, consistent with field observations. Our work demonstrates the utility of a demographic perspective for predicting the dynamics of symbioses and supports the hypothesis that symbionts function as mutualists when host and symbiont fitness are coupled through vertical transmission.     

Lipogenesis in the intact coral Pocillopora capitata and its isolated zooxanthellae: Evidence for a light-driven carbon cycle between symbiont and host

Surface tissue of the reef coral Pocillopora capitata contained approximately 34% lipid on a dry weight basis. Of this, 75% was storage lipid (wax ester and triglyceride) and 25% structural (phospholipid, galactolipid, etc.). Based on chlorophyll a: lipid ratios of intact coral and isolated zooxanthellae, it was determined that over 90% of the storage lipid resided in the host tissue. One half of the structural lipids was found in the host and the other in the symbiotic algae. Gentle fractionation of coral tissue indicated that zooxanthellae possessed less than 14% of the total coral protein. Coral tips and isolated zooxanthellae were incubated with sodium acetate-1-¹⁴C in light and dark to obtain lipogenic rates and proportions of fatty acids and lipid classes synthesized. The rate of lipid synthesis from acetate-1-¹⁴C by intact coral was stimulated three-fold in the light (1200 lux), which indicated that the majority of coral lipogenesis occurred in the zooxanthellae. Intact coral triglycerides contained ca. 68% of the ¹⁴C-activity and wax esters ca. 21%. Zooxanthellae isolated by the Water Pik technique synthesized negligible amounts of wax ester, which implied that wax ester synthesis was a property of the animal tissue. Isolated zooxanthellae and intact coral synthesized identical triglyceride fatty acids from acetate-1-¹⁴C. This study provides evidence for a carbon cycle between host and symbiont whereby the zooxanthellae take up host-derived carbon (probably in the form of acetate), synthesize fatty acids using their photosynthetically derived energy, and return the lipid to the host where it appears as wax ester and triglyceride.     

Bleaching response of corals and their <Emphasis Type="Italic">Symbiodinium</Emphasis> communities in southern Africa

The high-latitude coral communities of southern Africa suffered minimal impacts during past mass bleaching events. Recent reports indicate an increase in bleaching frequency during the last decade, yet the actual levels of thermal stress and contributing factors in these bleaching events, and the degree of acclimatisation or adaptation on these reefs are poorly understood. During the 2005 warm-water anomaly in the southern Indian Ocean we conducted bleaching surveys and collected samples for genotyping of the algal symbiont communities at 21 sites in southern Mozambique and South Africa. Coral bleaching reached unprecedented levels and was negatively correlated with both latitude and water depths. Stylophora pistillata and Montipora were the most susceptible taxa, whereas three common branching corals had significantly different bleaching responses (Stylophora > Acropora > Pocillopora). Temperature records indicated that localised strong upwelling events coupled with persistent above-average seawater temperatures may result in accumulated thermal stress leading to bleaching. Symbiodinium in 139 scleractinian corals belonged almost exclusively to clade C, with clade D symbionts present in only 3% of the colonies. Two atypical C subclades were present in Stylophora and Pocillopora colonies and these were more abundant in shallow than deeper sites. Taxon-specific differences in bleaching responses were unrelated to different clades of algal symbionts and suggest that Symbiodinium C subtypes with diverse thermal tolerance, coupled with acclimatisation and morphology of the host colony influence the bleaching response. Additionally, the predominance of putatively thermal-sensitive Symbiodinium in southern African corals may reflect a limited experience of bleaching and emphasises the vulnerability of these reefs to moderate levels of thermal stress.     

Lag Effects in the Impacts of Mass Coral Bleaching on Coral Reef Fish, Fisheries, and Ecosystems

Abstract:  Recent episodes of coral bleaching have led to wide-scale loss of reef corals and raised concerns over the effectiveness of existing conservation and management efforts. The 1998 bleaching event was most severe in the western Indian Ocean, where coral declined by up to 90% in some locations. Using fisheries-independent data, we assessed the long-term impacts of this event on fishery target species in the Seychelles, the overall size structure of the fish assemblage, and the effectiveness of two marine protected areas (MPAs) in protecting fish communities. The biomass of fished species above the size retained in fish traps changed little between 1994 and 2005, indicating no current effect on fishery yields. Biomass remained higher in MPAs, indicating they were effective in protecting fish stocks. Nevertheless, the size structure of the fish communities, as described with size-spectra analysis, changed in both fished areas and MPAs, with a decline in smaller fish (<30 cm) and an increase in larger fish (>45 cm). We believe this represents a time-lag response to a reduction in reef structural complexity brought about because fishes are being lost through natural mortality and fishing, and are not being replaced by juveniles. This effect is expected to be greater in terms of fisheries productivity and, because congruent patterns are observed for herbivores, suggests that MPAs do not offer coral reefs long-term resilience to bleaching events. Corallivores and planktivores declined strikingly in abundance, particularly in MPAs, and this decline was associated with a similar pattern of decline in their preferred corals. We suggest that climate-mediated disturbances, such as coral bleaching, be at the fore of conservation planning for coral reefs.     

Assessing the effects of disease and bleaching on Florida Keys corals by fitting population models to data

Coral diseases have increased in frequency over the past few decades and have important influences on the structure and composition of coral reef communities. However, there is limited information on the etiologies of many coral diseases, and pathways through which coral diseases are acquired and transmitted are still in question. Furthermore, it is difficult to assess the impacts of disease on coral populations because outbreaks often co-occur with temperature-induced bleaching and anthropogenic stressors. We developed spatially explicit population models of coral disease and bleaching dynamics to quantify the impact of six common diseases on Florida Keys corals, including aspergillosis, dark spots, white band, white plague, white patch, and Caribbean yellow band. Models were fit to an 8-year data set of coral abundance, disease prevalence, and bleaching prevalence. Model selection was used to assess alternative pathways for disease transmission, and the influence of environmental stressors, including sea temperature and human population density, on disease prevalence and coral mortality. Classic disease transmission from contagious to susceptible colonies provided the best-fit model only for aspergillosis. For other diseases, external disease forcing, such as through a vector or directly from pathogens in the environment, provided the best fit to observed data. Estimates of disease reproductive ratio values (R₀) were less than one for each disease, indicating coral colonies were below densities required for diseases to become established through contagious spread alone. Incidences of white band and white patch disease were associated with greater susceptibility or slower recovery of bleached colonies, and no disease outbreaks were associated with periods of elevated sea temperatures alone. Projections of best-fit models indicated that, atleast during the period of this study, disease and bleaching did not have substantial impacts on populations and impaired rates of population growth appeared to be attributable to other stressors. By applying epidemiological models to field data, our study gives qualitative insights into the dynamics of coral diseases, relative stressor impacts, and directions for future research.     

DNA damage induced by ultraviolet radiation in coral-reef microbial communities

Ultraviolet radiation (UVR) has been implicated in coral-bleaching processes and UVR may create stress to marine organisms by damage to DNA. Absorption of energy from UVB (280 to 320 nm) induces direct damage to DNA via cyclobutane pyrimidine dimer photoproduct-formation. We examined the extent of DNA damage created by UVR in coral reef microbial communities and whether the coral-surface microlayer (CSM) provides protection from UVR to the microorganisms found there. Diel patterns and depth profiles of UVR effects were examined in coral mucus (coral-surface microlayer, CSM) from Montastraea faveolata and Colpophyllia natans, and water-column samples of similar depths. UV-induced photodamage was determined using a radioimmunoassay specific for cyclobutane pyrimidine dimers (thymine dimers). Significant photodamage was detected in water-column and CSM samples, although the level of damage in CSM samples was consistently lower than in water-column samples collected from the same depth, suggesting the presence of photoprotective mechanisms within the CSM. Diel patterns of photodamage were detected in both water-column and CSM samples, but peak damage occurred earlier in the day for the CSM samples, suggesting differences in damage and repair kinetics between the water column and CSM. The results suggest that microorganisms within the CSM are afforded some protection from UVR stress and that changes in the amount of DNA damage in these organisms may be an indicator of changing UVR stress to corals. Received: 10 January 1997 / Accepted: 15 September 1997     

A multi-mutualist simulation: Applying biological market models to diverse mycorrhizal communities

We present a cellular automaton that simulates the interaction between a host tree and multiple potential mycorrhizal symbionts and generates testable hypotheses of how processes at the scale of individual root tips may explain mycorrhizal community composition. Existing theoretical biological market models imply that a single host is able to interact with and select from multiple symbionts to organize an optimal symbiont community. When evaluating the tree–symbiont interaction, two scales must be considered simultaneously: the scale of the entire host plant at which carbon utilization and nutrient demands operate, and the scale of the individual root tip, at which colonization and carbon-nutrient trade occurs. Three strategies that may be employed by the host tree for optimizing carbon use and nutrient acquisition through mycorrhizal symbiont communities are simulated: (1) carbon pool adjustment, in which the plant controls only the total amount of carbon to be distributed uniformly throughout the root system, (2) symbiont selection, wherein the plant opts either for or against the interaction at each fine root tip, and (3) selective carbon allocation, wherein the plant adjusts the amount of carbon allocated to each root tip based on the cost of nutrients. Strategies were tested over various nutrient availabilities (the amount of inorganically and organically bound nutrients). Success was defined on the basis of minimizing carbon expended for nutrient acquisition because this would allow more carbon to be utilized for growth and reproduction. In all cases, the symbiont selection and selective carbon allocation strategies were able to meet the nutritional requirements of the plant, but did not necessarily optimize carbon use. The carbon pool adjustment strategy is the only strategy that does not operate at the individual root tip scale, and the strategy was not successful when inorganic nutrients were scarce since there is no mechanism to exclude suboptimal symbionts. The combination of the symbiont selection strategy and the carbon pool adjustment resulted in optimal carbon use and nutrient acquisition under all environmental conditions but result in monospecific symbiont assemblages. On the other hand, the selective carbon allocation strategy is the only strategy that maintained successful, multi-symbiont communities. The simulations presented here thus imply clear hypotheses about the effect of nutrient availability on symbiont selection and mycorrhizal community richness and composition.     

Coefficient of variation of sea surface temperature (SST) as an indicator of coral bleaching

Coral bleaching has become a major problem on reefs around the world in recent decades. It is believed that mean temperature alone is the primary force driving this ecological phenomenon. We propose that variance in temperature in the short term is just as important as the mean. Thirty years of daily sea surface temperature (SST) data have been collected by the University of Puerto Rico at Mayaguez Marine Laboratory in La Parguera, PR. These data were collated and analyzed initially (by Amos Winter) for their relationship to coral bleaching in this area. We found that the data fell into three categories: high mean temperatures associated with severe bleaching, cooler mean temperatures associated with no bleaching, and years of high SSTs but with no coral bleaching. Here, we examined the relationship between mean temperature during those months in which bleaching occurred, temperature variance (as measured by standard deviation), and coefficient of variation (CV; i.e., SD standardized by the mean). We also derived a critical threshold temperature and level of resolution in time for calculating these statistics to clearly describe the circumstances of bleaching versus non-bleaching events, particularly at marginal bleaching temperatures. These characteristics were compared for the four warmest months of the year (July–October) for four warm bleaching years (1969, 1987, 1990, and 1995), four cool non-bleaching years (1984, 1985, 1986, and 1988), and two warm non-bleaching years (1994 and 2000). No relationship was found between the mean SST and SD in terms of predicting bleaching. The two primary statistics which, in concert, did indicate bleaching, however, were the short-term, biweekly mean temperature and its the associated CV. Bleaching occurs in association with both high temperatures and a high CV. The CV becomes a critical determinant of bleaching only when temperatures are ∼29.1–29.8°C. The warm, non-bleaching years were generally characterized by a CV of < 1.9 and a temperature range between 28.5 and 29.9°C. We conclude that increased mean SSTs alone are not sufficient to induce coral bleaching; a high variance in SST at marginal, lower bleaching temperatures can induce bleaching, and likewise, a low variance of such will not induce bleaching. This variance is most clearly described by the CV.     

The effects of antifoulant-paint-contaminated sediments on coral recruits and branchlets

The 184-m cargo ship "Bunga Teratai Satu" ran aground on Sudbury Reef, within the Great Barrier Reef Marine Park, on 2 November 2000. Although no cargo or fuel was lost, the ship remained aground for 12 days and a large quantity of antifoulant paint containing tributyltin (TBT), zinc, and copper was scraped from the hull during the grounding and subsequent refloating operation. This resulted in extensive contamination of the reef sediments for up to 250 m surrounding the grounding site. Two laboratory-based experiments assessed the impact of contaminated sediments on the survival of both newly settled corals of Acropora microphthalma and branchlets of A. formosa. Newly settled corals exposed to sediments containing 8.0 mg kg^–1 TBT, 72 mg kg^–1 Cu, and 92 mg kg^–1 Zn or greater suffered significantly higher mortality after 72 h, compared to control or low-concentration treatments. Coral recruits exposed to 40 mg kg^–1 TBT (Sn), 306 mg kg^–1 Cu, and 403 mg kg^–1 Zn were all killed within 38 h. Branchlets from adult corals exposed to sediments with a high concentration of contaminants (TBT 160 mg kg^–1, Cu 1,180 mg kg^–1, and Zn 1,570 mg kg^–1) suffered significant mortality (38%), whereas branchlets placed in treatments with lower levels of contaminants suffered no mortality. Visual bleaching of the branchlets was observed at high contaminant levels, but an overall reduction in the symbiotic zooxanthellae populations was not observed in surviving corals. The photosynthetic yields of light-adapted zooxanthellae remained constant in live branchlets, indicating that the TBT-contaminated sediment may be more toxic to the host than the symbiont. Our results show that antifoulant contamination at ship-grounding sites has the potential to cause major mortality of resident coral communities and can have a negative impact on the recovery of adult populations.Communicated by P.W. Sammarco, Chauvin     

Recovery of corals a decade after a bleaching event in Dubai, United Arab Emirates

Elevated sea surface temperatures in the late 1990s were associated with widespread coral mortality in the Arabian Gulf, particularly in Acropora dominated areas. This study investigates the composition, condition, and recruitment patterns of coral communities in Saih Al-Shaib, Dubai, United Arab Emirates, a decade after mass bleaching. Five statistically distinct communities were identified by cluster analysis, with grouping optimized from 17 significant indicator species. Overall, 25 species of scleractinian coral were observed, representing 35 ± 1.6% coral cover. Densities of recruits were low (0.8 ± 0.2 m⁻²), and composition generally reflected that of the surrounding adult community. Ten years after mass mortality, Acropora dominated assemblages were observed in three of the six sites examined and coral cover (41.9 ± 2.5%) was double post-bleaching cover. One shallow near-shore site appears to have had recovery of Acropora reset by a further bleaching event in 2002. However, the prevalence of young Acropora colonies here indicates that recovery may recur in several years. One area formerly dominated by Acropora is now dominated by faviids and poritids, with adult and juvenile composition suggesting this dominance shift is likely to persist. Porites lutea and Porites harrisoni dominated communities were negligibly impacted by the bleaching events, and the limited change in coral cover and composition in intervening years likely results from slow growth and low recruitment. Despite strong recovery of several dominant Acropora species, five formerly common species from this area were not observed suggesting local extinction. Dubai coral communities exhibit both resistance and resilience to elevated sea temperatures. The conservation of these patch reefs is warranted given the predicted increase in bleaching events, and the role that these communities may play in regional recovery.