Diversity in skeletal architecture influences biological heterogeneity and Symbiodinium habitat in corals

Scleractinian corals vary in response to rapid shifts in the marine environment and changes in reef community structure post-disturbance reveal a clear relationship between coral performance and morphology. With exceptions, massive corals are thought to be more tolerant and branching corals more vulnerable to changing environmental conditions, notably thermal stress. The typical responses of massive and branching coral taxa, respectively, are well documented; however, the biological and functional characteristics that underpin this variation are not well understood. We address this gap by comparing multiple biological attributes that are correlated with skeletal architecture in two perforate (having porous skeletal matrices with intercalating tissues) and two imperforate coral species (Montipora aequituberculata, Porites lobata, Pocillopora damicornis, and Seriatopora hystrix) representing three morphotypes. Our results reveal inherent biological heterogeneity among corals and the potential for perforate skeletons to create complex, three-dimensional internal habitats that impact the dynamics of the symbiosis. Patterns of tissue thickness are correlated with the concentration of symbionts within narrow regions of tissue in imperforate corals versus broad distribution throughout the larger tissue area in perforate corals. Attributes of the perforate and environmentally tolerant P. lobata were notable, with tissues ～5 times thicker than in the sensitive, imperforate species P. damicornis and S. hystrix. Additionally, P. lobata had the lowest baseline levels of superoxide and Symbiodinium that provisioned high levels of energy. Given our observations, we hypothesize that the complexity of the visually obscured internal environment has an impact on host–symbiont dynamics and ultimately on survival, warranting further scientific investigation.     

Temperature-Regulated Bleaching and Lysis of the Coral Pocillopora damicornis by the Novel Pathogen Vibrio coralliilyticus

Coral bleaching is the disruption of symbioses between coral animals and their photosynthetic microalgal endosymbionts (zooxanthellae). It has been suggested that large-scale bleaching episodes are linked to global warming. The data presented here demonstrate that Vibrio coralliilyticus is an etiological agent of bleaching of the coral Pocillopora damicornis. This bacterium was present at high levels in bleached P. damicornis but absent from healthy corals. The bacterium was isolated in pure culture, characterized microbiologically, and shown to cause bleaching when it was inoculated onto healthy corals at 25°C. The pathogen was reisolated from the diseased tissues of the infected corals. The zooxanthella concentration in the bacterium-bleached corals was less than 12% of the zooxanthella concentration in healthy corals. When P. damicornis was infected with V. coralliilyticus at higher temperatures (27 and 29°C), the corals lysed within 2 weeks, indicating that the seawater temperature is a critical environmental parameter in determining the outcome of infection. A large increase in the level of the extracellular protease activity of V. coralliilyticus occurred at the same temperature range (24 to 28°C) as the transition from bleaching to lysis of the corals. We suggest that bleaching of P. damicornis results from an attack on the algae, whereas bacterium-induced lysis and death are promoted by bacterial extracellular proteases. The data presented here support the bacterial hypothesis of coral bleaching.     

Temporal patterns in effective quantum yield of individual zooxanthellae expelled during bleaching

Bleaching is a worldwide phenomenon affecting coral reefs. During elevated temperature and light conditions (bleaching), expelled zooxanthellae show distinct patterns in photosynthetic health. An innovative new device was used to collect individual expelled zooxanthellae, when a coral was exposed to bleaching conditions. This has provided new insight into the photosynthetic condition and abundance of expelled zooxanthellae. It has been assumed that expelled zooxanthellae were dead or moribund; however, we have found individual cells can have healthy effective quantum yields (?_PSII) >0.65 after 8 h of bleaching conditions (500 μmol photons m⁻² s⁻¹, 33 °C). The population of expelled zooxanthellae from Cyphastrea serailia and Pocillopora damicornis showed distinct patterns in the frequency distribution of ?_PSII over time and between locations (sun versus shade) within a colony. During the first 4 h of exposure to bleaching conditions, only 5% of expelled individual cells from P. damicornis were photosynthetically inactive (?_PSII<0.05), whereas for C. serailia, this was 30%. The overall photosynthetic health of expelled zooxanthellae from C. serailia was better than P. damicornis (0.53±0.13 and 0.38±0.13 after 8 h, respectively). This was generally reflected by the in hospite measurement of the coral, yet, the in hospite cells always had a higher ?_PSII than expelled cells, suggesting that host tissue provided added photoprotection for the zooxanthellae.     

Unrecognized coral species diversity masks differences in functional ecology

Porites corals are foundation species on Pacific reefs but a confused taxonomy hinders understanding of their ecosystem function and responses to climate change. Here, we show that what has been considered a single species in the eastern tropical Pacific, Porites lobata, includes a morphologically similar yet ecologically distinct species, Porites evermanni. While P. lobata reproduces mainly sexually, P. evermanni dominates in areas where triggerfish prey on bioeroding mussels living within the coral skeleton, thereby generating asexual coral fragments. These fragments proliferate in marginal habitat not colonized by P. lobata. The two Porites species also show a differential bleaching response despite hosting the same dominant symbiont subclade. Thus, hidden diversity within these reef-builders has until now obscured differences in trophic interactions, reproductive dynamics and bleaching susceptibility, indicative of differential responses when confronted with future climate change.     

A method for determining the surface area of corals

Although there are several techniques available that can accurately determine the surface area of simple branching corals, there is an absence of techniques that can be applied to finely branching species like Pocillopora damicornis. This paper describes a rapid, spectrophotometer-based technique that can accurately determine the surface area of a range of coral species, including P. damicornis. The technique involves dipping corals coated with plastic varnish into a solution that contains a small amount of detergent and the dye Methylene Blue. The amount of dye solution clinging to the surfaces (as a thinlayer) is proportional to the total surface area.     

Effect of naturally changing zooplankton concentrations on feeding rates of two coral species in the Eastern Pacific

Zooplankton concentrations are known to vary by as much as an order of magnitude over a lunar cycle. Here, we conducted an experiment to determine the effect of ambient zooplankton concentrations over a lunar cycle on feeding rates of the corals Pavona gigantea (Verrill) (mounding coral, 3.0 mm diameter polyps) and Pocillopora damicornis (Linnaeus) (branching coral, 1.0 mm diameter polyps) in situ on a shallow reef at Isla Contadora, Gulf of Panamá (Pacific), Panamá. Coral fragments exposed to either enhanced or ambient zooplankton concentrations were allowed to feed for 1 h, collected, and their gut contents dissected. The number of zooplankton captured was counted, feeding rates calculated per cm², and the species composition of captured zooplankton assemblages determined. Although both species captured the same zooplankton assemblage, feeding rates were always significantly higher for P. gigantea than for P. damicornis. Under ambient flow and zooplankton concentrations, feeding rates were highly correlated with zooplankton concentration in the 200-400 μm size class. Under constantly enhanced zooplankton concentrations in the control fragments, feeding rates did not vary significantly over the lunar cycle. As such, coral feeding rates vary not as a result of lunar phase per se, but with changes in zooplankton abundance over the lunar cycle. Coral feeding rates are directly proportional to ambient zooplankton concentrations and may vary by as much as 50% over a lunar cycle, suggesting that corals must cope with major swings in sources of fixed carbon and nutrients over relatively short timescales.     

Regulation and control of intracellular algae (= zooxanthellae) in hard corals

To examine algal (= zooxanthellae) regulation and control, and the factors determining algal densities in hard corals, the zooxanthellae mitotic index and release rates were regularly determined in branch tips from a colony of a staghorn coral, Acropora formosa, recovering from a coral ''bleaching'' event (the stress-related dissociation of the coral–algal symbiosis). Mathematical models based upon density-dependent decreases in the algal division frequency and increases in algal release rates during the post-bleaching recovery period accurately predict the observed recovery period (ca. 20 weeks). The models suggest that (i) the colony recovered its algal population from the division of the remaining zooxanthellae, and (ii) the continual loss of zooxanthellae significantly slowed the recovery of the coral. Possible reasons for the ''paradoxical'' loss of healthy zooxanthellae from the bleached coral are discussed in terms of endodermal processes occurring in the recovering coral and the redistribution of newly formed zooxanthellae to aposymbiotic host cells. At a steady-state algal density of 2.1 x 10⁶ zooxanthellae cm^-2 at the end of the recovery period, the zooxanthellae would have to form a double layer of cells in the coral tissues, consistent with microscopic observations. Neighbouring colonies of A. formosa with inherently higher algal densities possess proportionately smaller zooxanthellae. Results suggest that space availability and the size of the algal symbionts determines the algal densities in the coral colonies. The large increases in the algal densities reported in corals exposed to elevated nutrient concentrations (i.e between a two- and five-fold increase in the algal standing stock) are not consistent with this theory. We suggest that increases of this magnitude are a product of the experimental conditions: reasons for this statement are discussed. We propose that the stability of the coral–algal symbiosis under non-stress conditions, and the constancy of zooxanthellae densities in corals reported across growth form, depth and geographic range, are related to space availability limiting algal densities. However, at these densities, zooxanthellae have attributes consistent with nutrient limitation.     

Differential nitric oxide synthesis and host apoptotic events correlate with bleaching susceptibility in reef corals

Coral bleaching poses a threat to coral reefs worldwide. As a consequence of the temperature-induced breakdown in coral–dinoflagellate symbiosis, bleaching can have extensive effects on reef communities. However, our understanding of bleaching at a cellular level is limited, and this is particularly true regarding differential susceptibility among coral species. Recent work suggests that bleaching may represent a host innate immune-like response to symbiont dysfunction that involves synthesis of the signalling compound nitric oxide (NO) and the induction of host apoptotic-like cell death. In this study, we examined the activity of apoptosis-regulating enzymes alongside oxidised NO accumulation (a proxy for NO synthesis) in the reef corals Acropora millepora, Montipora digitata, and Pocillopora damicornis during experimental thermal stress. P. damicornis was the most sensitive species, suffering mortality (tissue sloughing) after 5 days at 33 °C but non-lethal bleaching after 9 days at 31.5 °C. A. millepora bleached at 33 °C but remained structurally intact, while M. digitata showed little evidence of bleaching. P. damicornis and A. millepora both exhibited evidence of temperature-induced NO synthesis and, after 5 days of heating, levels of oxidised NO in both species were fivefold higher than in controls maintained at 28.5 °C. These responses preceded bleaching by a number of days and may have occurred before symbiont dysfunction (measured as chlorophyll a degradation and oxidised NO accumulation). In A. millepora, apparent NO synthesis correlated with the induction of host apoptotic-like pathways, while in P. damicornis, the upregulation of apoptotic pathways occurred later. No evidence of elevated NO production or apoptosis was observed in M. digitata at 33 °C and baseline activity of apoptosis-regulating enzymes was negligible in this species. These findings provide important physiological data in the context of the responses of corals to global change and suggest that early events in the host may be important in the collapse of the coral–dinoflagellate symbiosis.     

Spatio-Temporal Analyses of Symbiodinium Physiology of the Coral Pocillopora verrucosa along Large-Scale Nutrient and Temperature Gradients in the Red Sea

Algal symbionts (zooxanthellae, genus Symbiodinium) of scleractinian corals respond strongly to temperature, nutrient and light changes. These factors vary greatly along the north-south gradient in the Red Sea and include conditions, which are outside of those typically considered optimal for coral growth. Nevertheless, coral communities thrive throughout the Red Sea, suggesting that zooxanthellae have successfully acclimatized or adapted to the harsh conditions they experience particularly in the south (high temperatures and high nutrient supply). As such, the Red Sea is a region, which may help to better understand how zooxanthellae and their coral hosts successfully acclimatize or adapt to environmental change (e.g. increased temperatures and localized eutrophication). To gain further insight into the physiology of coral symbionts in the Red Sea, we examined the abundance of dominant Symbiodinium types associated with the coral Pocillopora verrucosa, and measured Symbiodinium physiological characteristics (i.e. photosynthetic processes, cell density, pigmentation, and protein composition) along the latitudinal gradient of the Red Sea in summer and winter. Despite the strong environmental gradients from north to south, our results demonstrate that Symbiodinium microadriaticum (type A1) was the predominant species in P. verrucosa along the latitudinal gradient. Furthermore, measured physiological characteristics were found to vary more with prevailing seasonal environmental conditions than with region-specific differences, although the measured environmental parameters displayed much higher spatial than temporal variability. We conclude that our findings might present the result of long-term acclimatization or adaptation of S. microadriaticum to regionally specific conditions within the Red Sea. Of additional note, high nutrients in the South correlated with high zooxanthellae density indicating a compensation for a temperature-driven loss of photosynthetic performance, which may prove promising for the resilience of these corals under increase of temperature increase and eutrophication.     

Holocene growth history of an eastern Pacific fringing reef,Punta Islotes,Costa Rica

Rock and sediment cores reveal that a well-developed fringing reef in Golfo Dulce, Pacific Costa Rica, up to 9 m thick was established on Cretaceous basalt about 5500 y BP. It is presently being smothered with fine sediments and is almost completely dead. This reef is made up of three main facies that are represented by comparable extant reef zones: reef-flat branching coral, fore-reef slope massive coral, and fore-reef talus sediment facies. Reef growth began with the establishment of small patch reefs dominantly formed by the branching coral Pocillopora damicornis. P. damicornis spread across the basalt bench and massive colonies of Porites lobata grew on the outer slopes, eventually blocking the seaward transport of Pocillopora fragments to the fore-reef talus sediments. The reef flourished until 500 years ago. Lower accumulation rates during the past 500 years may be due to deteriorating environmental conditions rather than slower growth after the reef reached sea level. Present-day reef communities are severely degraded with less than 2% living coral cover. The increased turbidity associated with the final stage of degradation of this reef is probably related to human activity on the adjacent shores, including deforestation, mining, and road construction.     

Interspecific comparison of the symbiotic relationship in corals with high and low rates of bleaching-induced mortality

Some coral species are more resistant than others to environmental factors that cause bleaching and bleaching-related mortality. This study compared aspects of the coral/zooxanthellae symbiosis in species and genera that suffered either high or low mortality during a bleaching event. These characteristics were assessed in Okinawa between March and June 1999, 5-10 months after the bleaching event there in August-September 1998. Species with low mortality rates generally had higher densities of zooxanthellae per square centimeter and a very low rate of release of degraded zooxanthellae. Low-mortality species also had more total coral tissue per square centimeter of coral surface area. The size of zooxanthellae varied little among species. The differences in these characteristics among coral species suggest that the symbiotic relationship operates very differently among coral species.     

Differential susceptibility to oxidative stress of two scleractinian corals: antioxidant functioning of mycosporine-glycine

This study examined the importance of mycosporine-glycine (Myc-Gly) as a functional antioxidant in the thermal-stress susceptibility of two scleractinian corals, Platygyra ryukyuensis and Stylophora pistillata. Photochemical efficiency of PSII (F_v/F_m), activity of antioxidant enzymes, superoxide dismutase (SOD) and catalase (CAT), and composition and abundance of mycosporine-like amino acids (MAAs) in the coral tissue and in symbiotic zooxanthellae were analyzed during 12-h exposure to high temperature (33 °C). After 6- and 12-h exposures at 33 °C, S. pistillata showed a significantly more pronounced decline in F_v/F_m compared to P. ryukyuensis. A 6-h exposure at 33 °C induced a significant increase in the activities of SOD and CAT in both host and zooxanthellae components of S. pistillata while in P. ryukyuensis a significant increase was observed only in the CAT activity of zooxanthellae. After 12-h exposure, the SOD activity of P. ryukyuensis was unaffected in the coral tissue but slightly increased in zooxanthellae, whereas the CAT activity in the coral tissue showed a 2.5-fold increase. The total activity of antioxidant enzymes was significantly higher in S. pistillata than in P. ryukyuensis, suggesting that P. ryukyuensis is less sensitive to oxidative stress than S. pistillata. This differential susceptibility of the corals is consistent with a 20-fold higher initial concentration of Myc-Gly in P. ryukyuensis compared to S. pistillata. In the coral tissue and zooxanthellae of both species investigated, the first 6 h of exposure to thermal stress induced a pronounced reduction in the abundance of Myc-Gly but not in other MAAs. When exposure was prolonged to 12 h, the Myc-Gly pool continued to decrease in P. ryukyuensis and was completely depleted in S. pistillata. The delay in the onset of oxidative stress in P. ryukyuensis and the dramatic increase in the activities of the antioxidant enzymes in S. pistillata, which contains low concentrations of Myc-Gly suggest that Myc-Gly provides rapid protection against oxidative stress before the antioxidant enzymes are induced. These findings strongly suggest that Myc-Gly is functioning as a biological antioxidant in the coral tissue and zooxanthellae and demonstrate its importance in the survival of reef-building corals under thermal stress.     

Intergenerational Transfer of Specific Bacteria in Corals and Possible Implications for Offspring Fitness

Diverse and abundant bacterial populations play important functional roles in the multi-partite association of the coral holobiont. The specificity of coral-associated assemblages remains unclear, and little is known about the inheritance of specific bacteria from the parent colony to their offspring. This study investigated if broadcast spawning and brooding corals release specific and potentially beneficial bacteria with their offspring to secure maintenance across generations. Two coral species, Acropora tenuis and Pocillopora damicornis, were maintained in 0.2 μm filtered seawater during the release of their gametes and planulae, respectively. Water samples, excluding gametes and planulae, were subsequently collected, and bacterial diversity was assessed through a pyrosequencing approach amplifying a 470-bp region of the 16S rRNA gene including the variable regions 1–3. Compared to the high bacterial diversity harboured by corals, only a few taxa of bacteria were released by adult corals. Both A. tenuis and P. damicornis released similar bacteria, and the genera Alteromonas and Roseobacter were abundant in large proportions in the seawater of both species after reproduction. This study suggests that adult corals may release bacteria with their offspring to benefit the fitness in early coral life stages.     

Development of coral and zooxanthella‐specific microsatellites in three species of Pocillopora (Cnidaria,Scleractinia) from French Polynesia

Since the building of coral reefs results from the association of corals and zooxanthellae, their intracellular algal symbionts, genetic markers for both organisms are essential for studying the contribution of their respective dispersal to the resilience of endangered reef ecosystems. Very few microsatellites have been obtained in corals thus far. Here we report the successful cloning of six polymorphic microsatellites (allele number: 5–15) from Pocillopora verrucosa, P. meandrina and P. damicornis. Four of them amplified coral, and two amplified zooxanthella DNA.     

Light Respiratory Processes and Gross Photosynthesis in Two Scleractinian Corals

The light dependency of respiratory activity of two scleractinian corals was examined using O₂ microsensors and CO₂ exchange measurements. Light respiration increased strongly but asymptotically with elevated irradiance in both species. Light respiration in Pocillopora damicornis was higher than in Pavona decussata under low irradiance, indicating species-specific differences in light-dependent metabolic processes. Overall, the coral P. decussata exhibited higher CO₂ uptake rates than P. damicornis over the experimental irradiance range. P. decussata also harboured twice as many algal symbionts and higher total protein biomass compared to P. damicornis, possibly resulting in self-shading of the symbionts and/or changes in host tissue specific light distribution. Differences in light respiration and CO₂ availability could be due to host-specific characteristics that modulate the symbiont microenvironment, its photosynthesis, and hence the overall performance of the coral holobiont.     

Molecular identification of symbiotic dinoflagellates in Pacific corals in the genus <Emphasis Type="Italic">Pocillopora</Emphasis>

This study focused on the association between corals of the genus Pocillopora, a major constituent of Pacific reefs, and their zooxanthellae. Samples of P. meandrina, P. verrucosa, P. damicornis, P. eydouxi, P. ligulata and P. molokensis were collected from French Polynesia, Tonga, Okinawa and Hawaii. Symbiodinium diversity was explored by looking at the 28S and ITS1 regions of the ribosomal DNA. Most zooxanthellae were found to belong to clade C, sub-clade C1, with little differentiation between populations. Interestingly, individuals of P. damicornis harbored sub-clade C1, clade D and clade A, depending on location. The symbiotic association of P. damicornis with its zooxanthellae may be somewhat more flexible than those of other Pocillopora species.     

Large fluctuations but constant mean temperatures allow corals to persist in intertidal rock pools on the east coast of South Africa

Intertidal corals have been under-studied yet they provide scope for understanding adaptation and acclimatisation of corals to marginal conditions. Corals in intertidal rock pools along the east coast of South Africa withstand large temperature fluctuations, and marginal conditions for survival and growth. Four sites along the KwaZulu-Natal (KZN) coastline were sampled to determine latitudinal differences in coral communities, from 27°S to 31°S. Water temperature of rock pools at each site was monitored to see if temperature determined coral diversity in intertidal pools. Sixteen coral species were present in rock pools overall. Each of three sites in northern and central KZN hosted 12 coral taxa whereas only six taxa occurred at the most southern site. Anomastrea irregularis was the most abundant species at all sites, followed by Pocillopora verrucosa and P. damicornis. Unexpectedly, rock pool temperatures did not show a trend with latitude and thus cannot explain this decline in coral diversity. Temperatures in isolated rock pools showed large summer day time fluctuations of more than 10 °C at spring tide. However, temperatures drop substantially at high tide, lowering the mean rock pool temperature and possibly allowing these coral communities to persist in the marginal conditions of rock pools in South Africa.     

Temperature-dependent performance of competitive native and alien invasive plant species

To assess the likely impacts of environmental change, the responses of two well-known invasive plant species, native Pueraria lobata and alien Humulus japonicus, to differences in growth temperature were studied in South Korea. Habitat preferences, physiological responses such as photosynthetic rates and chlorophyll contents, growth rates, and nutrient contents were quantified for each species. A competition experiment was conducted to evaluate the temperature preferences of the two species. All results indicated that the alien species H. japonicus can take advantage of elevated temperatures (35 °C) to enhance its competitive advantage against the native species P. lobata. While H. japonicus took advantage of elevated temperatures and preferred high-temperature areas, P. lobata showed reduced performance and dominance in high-temperature areas. Therefore, in future, due to global warming and urbanization, there are possibilities that H. japonicus takes advantage of elevated temperature against P. lobata that could lead to increased H. japonicus coverage over time. Therefore, consistent monitoring of both species especially where P. lobata is dominated are required because both species are found in every continents in the world. Controlling P. lobata requires thorough inspection of H. japonicus presence of the habitat in advance to prevent post P. lobata management invasion of H. japonicus.     

Experimental responses to elevated water temperature in genotypes of the reef coral<Emphasis Type="Italic"> Pocillopora damicornis</Emphasis> from upwelling and non-upwelling environments in Panama

The authors investigated the response to experimentally elevated water temperature in genotypes of Pocillopora damicornis from three coral reefs in the upwelling Gulf of Panama and four coral reefs in the non-upwelling Gulf of Chiriquí, Panamanian Pacific. Sea-surface temperature in the Gulf of Panama declines below 20 °C during seasonal upwelling, while in the thermally stable Gulf of Chiriquí, the temperature ranges from 27 to 29 °C. Genotypes of P. damicornis from the seven locations were determined by allozyme electrophoresis. The most abundant genotype at each location was selected for a thermal tolerance experiment where corals were exposed to water temperature of 30 °C (1 °C above ambient) for 43 days. Four site coral genotypes can be uniquely differentiated by the GPI locus, two by the LGG-2 locus, and two by a combination of the MDH-1, LGG-2, and LTY-3 loci. A visual assessment of the coral condition after exposure to an elevated temperature showed that corals from localities in the non-upwelling environment retained a normal to slightly pale appearance, while corals from the upwelling environment bleached and their polyps were mostly retracted. A two-way ANOVA confirmed that corals were significantly affected by water temperature and locality. The zooxanthellae were also significantly affected by the interaction of elevated temperature and locality of the corals. Mean zooxanthellae density decreased by 25 and 55%, respectively, in experimentally heated corals from the non-upwelling and upwelling environments. Low concentrations of photosynthetic pigments per live area of the corals were the norm in corals under elevated temperature. The mean concentration of chlorophyll a per live area of the corals was reduced by 17 and 49%, respectively, in heated corals from the non-upwelling and upwelling sites. Coral genotypes from the upwelling Gulf of Panama demonstrated higher vulnerability to thermal stress than coral genotypes from the non-upwelling Gulf of Chiriquí. However, the latter showed greater differences in their responses. Thus, even at small geographic scales, corals can display different levels of tolerance to thermal stress. The difference in thermal tolerance between corals from upwelling and non-upwelling environments is concomitant with greater genetic differences in experimental corals from the thermally stable Gulf of Chiriquí compared with corals from the upwelling Gulf of Panama.Communicated by K.S. Sealey