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.     

Biogeographic partitioning and host specialization among foraminiferan dinoflagellate symbionts (<Emphasis Type="Italic">Symbiodinium</Emphasis>; Dinophyta)

Large discoidal soritid foraminiferans (Soritinae) are abundant in coral reef ecosystems. As with the many cnidarian invertebrates that inhabit these systems, they also depend on symbiotic dinoflagellates (Symbiodinium) for their growth and survival. Several particular Symbiodinium sub-genera or clades inhabit these soritids. One of these groups, referred to as clade C, dominates corals and their relatives throughout the tropical Indo-Pacific. In contrast, the distributions of Symbiodinium spp. from clades A, B, and C are more evenly apportioned across Caribbean invertebrate communities. To explore the possibility that a similar biogeographic break exists in the symbionts harbored by soritids, we surveyed the Symbiodinium spp. from the soritid genus Sorites, collected from the Pacific and Caribbean coasts of Panama as well as from Florida. Characterization of Symbiodinium obtained from foraminiferal and cnidarian samples was conducted using restriction fragment length polymorphism and phylogenetic analyses of the nuclear internal transcribed spacer region 2 (ITS 2) and a portion of the large subunit ribosomal DNA sequences. A distinctive biogeographic break between the kinds of symbionts found in Sorites from the East Pacific and Caribbean was clearly evident. Differences between cnidarian and foraminferan symbioses in each ocean may be explained by the subjection of Caribbean communities to severer environmental conditions during the early Quarternary. Caribbean Sorites spp. harbored symbionts described from clade F (specifically sub-clade Fr4) and clade H (formally referred to as Fr1), while Sorites spp. from the eastern Pacific were dominated by a single Symbiodinium haplotype in clade C. An ITS 2 phylogeny determined that most clade C types recovered from Indo-Pacific soritids form a monophyletic sub-lineage with other clade C symbionts typically found in Pacific corals from the genus Porites. The existence of multiple Symbiodinium lineages at various taxonomic levels associated specifically with soritids indicates that symbioses with these hosts are important in driving Symbiodinium spp. evolution.Electronic Supplementary Material Supplementary material is available in the online version of this article at .Communicated by O. Kinne, Oldendorf/Luhe     

Latitudinal symbiont zonation in <Emphasis Type="Italic">Stylophora pistillata</Emphasis> from southeast Africa

Studies on latitudinal gradients in Symbiodinium diversity on scleractinian corals are largely restricted to warm-water low latitude locations, and it appears that there is a shift in symbiont distributions with increasing latitude. The Symbiodinium assemblages of high latitude coral communities have largely been undocumented despite occupying an important transitional zone between tropical and temperate regions. Using a combination of the internal transcribed spacer region 2 (ITS2) and denaturing gradient gel electrophoresis (DGGE), we assessed the cladal and subcladal variability of Symbiodinium in the widely distributed species Stylophora pistillata along a latitudinal transect in southeast African waters which extended into high latitude locations. All colonies examined belonged to clade C. Six unique ITS2-DGGE banding profiles (designated C_spa to C_spf) were observed, which showed a latitudinal distribution from north to south, most likely a result of a gradient in water temperature and irradiance driven by riverine input in the southern regions. Sequence analysis revealed that all sequences except one did not match previously identified clade C sub-types, probably due to the lack of regional information in the Western Indian Ocean when compared to the Caribbean and Pacific. This study further supports the applicability of ITS2-DGGE in studies on Symbiodinium diversity, and highlights that potentially ecologically informative biogeographic patterns may be overlooked when only cladal designations are employed.     

<Emphasis Type="Italic">Symbiodinium</Emphasis> sp. associations in the gorgonian<Emphasis Type="Italic"> Pseudopterogorgia elisabethae</Emphasis> in the Bahamas: high levels of genetic variability and population structure in symbiotic dinoflagellates

Little is known concerning the fine-scale diversity, population structure, and biogeography for Symbiodinium spp. populations inhabiting particular invertebrate species, including the gorgonian corals, which are prevalent members of reef communities in the Gulf of Mexico, the Caribbean, and the western Atlantic. This study examined the Symbiodinium sp. clade B symbionts hosted by the Caribbean gorgonian Pseudopterogorgia elisabethae (Bayer). A total of 575 colonies of P. elisabethae were sampled in 1995 and 1998–2000 from 12 populations lying along an ~450 km transect in the Bahamas and their Symbiodinium sp. clade B symbionts genotyped at two polymorphic dinucleotide microsatellite loci. Twenty-three unique, two-locus genotypes were identified in association with these P. elisabethae colonies. Most colonies hosted only a single Symbiodinium sp. clade B genotype; however, in some instances ( n=25), two genotypes were harbored simultaneously. For 10 of the 12 populations, 66–100% of the P. elisabethae colonies hosted the same symbiont genotype. Added to this, in 9 of the 12 populations, a Symbiodinium sp. clade B genotype was either unique to a population or found infrequently in other populations. This distribution of Symbiodinium sp. clade B genotypes resulted in statistically significant ( P<0.05 or <0.001) differentiation in 62 of 66 pairwise comparisons of P. elisabethae populations. Tests of linkage disequilibrium suggested that a combination of clonal propagation of the haploid phase and recombination is responsible for maintaining these distinct Symbiodinium sp. clade B populations.     

Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion

This report documents the extent to which coral colonies show fluctuations in their associations with different endosymbiotic dinoflagellates. The genetic identity of Symbiodinium from six coral species [Acropora palmata (Lamarck), A. cervicornis (Lamarck), Siderastrea siderea (Ellis and Solander), Montastrea faveolata (Ellis and Solander), M. annularis (Ellis and Solander), and M. franksi (Gregory)] was examined seasonally over five years (1998 and 2000–2004) in the Bahamas and Florida Keys at shallow (1 to 4 m) fore-reef/patch reef sites and at deeper fore-reef (12–15 m) locations. Symbionts were identified genetically using denaturing gradient gel electrophoresis (DGGE) fingerprinting of the internal transcribed spacer region 2 (ITS2) of ribosomal RNA gene loci. Repetitive sampling from most labeled colonies from the Bahamas and the Florida Keys showed little to no change in their dominant symbiont. In contrast, certain colonies of M. annularis and M. franksi from the Florida Keys exhibited shifts in their associations attributed to recovery from the stresses of the 1997–1998 El Niño southern oscillation (ENSO) event. Over several years, a putatively stress-tolerant clade D type of Symbiodinium was progressively replaced in these colonies by symbionts typically found in M. annularis and M. franksi in Florida and at other Caribbean locations. Greater environmental fluctuations in Florida may explain the observed changes among some of the symbioses. Furthermore, symbiotic associations were more heterogeneous at shallow sites, relative to deep sites. The exposure to greater environmental variability near the surface may explain the higher symbiont diversity found within and between host colonies.     

Do corals select zooxanthellae by alternative discharge?

Loss of zooxanthellae (dinoflagellate Symbiodinium) from corals will sometimes lead to mass mortality of corals. To detect and quantify Symbiodinium released from corals, we developed a zooxanthellae “trap” and a quantitative PCR (qPCR) system with Symbiodinium clades A–F-specific primer sets. The trap was attached to a branch or the surface of several wild stony corals, and the water samples within the traps, including released Symbiodinium, were subjected to qPCR. All tested corals released clade C Symbiodinium at estimates of ~5,900 cells h⁻¹ cm⁻² of coral surface. Although all tested Pocillopora eydouxi harboured both clades C and D, some of these colonies released only clade C or released a lesser amount of clade D than that in the tissues. Our Symbiodinium quantification system revealed that wild hermatypic corals constantly release Symbiodinium to the environment. Our result suggests that some corals may discharge certain clades of Symbiodinium alternatively.     

Three party symbiosis: acoelomorph worms,corals and unicellular algal symbionts in Eilat (Red Sea)

Epizoic worms were found to occur on certain coral colonies from reefs off the coast of Eilat (Red Sea). We identified 14 coral species infested by acoelomorph worms at a depth range of 2–50 m. The host corals were all zooxanthellate and included both massive and branching stony corals and a soft coral. Worms from all hosts were identified as belonging to the genus Waminoa and contained two distinct algal symbionts differing in size. The smaller one was identified as Symbiodinium sp. and the larger one is presumed to belong to the genus Amphidinium. Worm-infested colonies of the soft coral, Stereonephthya cundabiluensis, lacked a mucus layer and exhibited distinct cell microvilli, a phenotype not present in colonies lacking Waminoa sp. In most cases, both cnidarian and Acoelomorph hosts displayed high specificity for genetically distinctive Symbiodinium spp. These observations show that the epizoic worms do not acquire their symbionts from the “host” coral.     

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.     

Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs

A community ecology approach to the study of the most common group of zooxanthellae, dinoflagellates in the genus Symbiodinium, was applied to symbiotic invertebrate assemblages on coral reefs in the western Caribbean, off the Yucatan peninsula (Puerto Morelos, Mexico) and over 1000 km away in the northeastern Caribbean, at Lee Stocking Island, Bahamas. Sequence differences and intragenomic variation, as determined by denaturing gradient gel electrophoresis and sequencing of the internal transcribed spacer 2 (ITS 2) region, were used to classify these symbionts. Twenty-eight genetically distinct Symbiodinium types were identified, eleven of which were found in hosts from both Caribbean locations. A single symbiont population was detected in 72% of hosts from the Yucatan and 92% of hosts from the Bahamas. The reef-wide community distribution of these symbionts is dominated by a few types found in many different host taxa, while numerous rare types appear to have high specificity for a particular host species or genus. Clade or lineage A Symbiodinium spp. was restricted to compatible hosts located within 3-4 m of the surface, while Symbiodinium spp. types from other lineages displayed differences in vertical zonation correlated with ITS type but were independent of clade designation. A comparison of the symbiont types found in field-collected hosts with types previously cultured from these hosts indicates the existence of low density or "background"-symbiont populations and cryptic, potentially non-mutualistic types in some hosts.     

Predominance of clade D <Emphasis Type="Italic">Symbiodinium</Emphasis> in shallow-water reef-building corals off Kish and Larak Islands (Persian Gulf,Iran)

Scleractinian coral species harbour communities of photosynthetic taxa of the genus Symbiodinium. As many as eight genetic clades (A, B, C, D, E, F, G and H) of Symbiodinium have been discovered using molecular biology. These clades may differ from each other in their physiology, and thus influence the ecological distribution and resilience of their host corals to environmental stresses. Corals of the Persian Gulf are normally subject to extreme environmental conditions including high salinity and seasonal variation in temperature. This study is the first to use molecular techniques to identify the Symbiodinium of the Iranian coral reefs to the level of phylogenetic clades. Samples of eight coral species were collected at two different depths from the eastern part of Kish Island in the northern Persian Gulf, and Larak Island in the Strait of Hormuz. Partial 28S nuclear ribosomal (nr) DNA of Symbiodinium (D1/D2 domains) were amplified by polymerase chain reaction (PCR). PCR products were analyzed using single stranded conformational polymorphism and phylogenetic analyses of the LSU DNA sequences from a subset of the samples. The results showed that Symbiodinium populations were generally uniform among and within the populations of eight coral species studied, and there are at least two clades of Symbiodinium from Kish and Larak islands. Clade D was detected from eight of the coral species while clade C was found in two of species only (one species hosted two clades simultaneously). The dominance of clade D might be explained by high temperatures or the extreme temperature variation, typical of the Persian Gulf. Publication of this article was held up owing to technical problems. The publisher apologizes sincerely for this lengthy delay.     

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.     

Phylogenetic analyses of potentially free-living <Emphasis Type="Italic">Symbiodinium</Emphasis> spp. isolated from coral reef sand in Okinawa,Japan

The existence of “free-living” Symbiodinium that can form symbioses with hosts is implied by the presence of hosts that produce Symbiodinium-free gametes and expulsion and/or expelled symbiotic algae from host. However, it is still unclear if potentially symbiotic Symbiodinium are found “free-living” in the coral reef environment. Sixteen Symbiodinium strains were established from samples taken from three sampling locations of coral reef sand in Okinawa, Japan. Phylogenetic analyses of the partial large subunit ribosomal DNA (28S-rDNA) and the internal transcribed spacer of ribosomal DNA (ITS-rDNA) conclusively showed that all 16 isolates belonged to Symbiodinium clade A sensu Rowan and Powers (1991). The lack of other Symbiodinium clades besides clade A in this study may be due to other clades not being readily culturable under culture conditions used here. The new isolates could be phylogenetically divided into four groups, though no sequences were identical to previously reported Symbiodinium. Two of the four groups were closely related to symbiotic Symbiodinium clade A isolated from a variety of host species. One isolate group formed a highly supported monophyly with Symbiodinium types that have previously been characterized as “free-living”. The remaining isolate group, although within clade A, was quite divergent from other clade A Symbiodinium. These results indicate that novel diversity of free-living Symbiodinium exists in coral sand.     

Vertical zonation of endosymbiotic zooxanthellae within a population of the intertidal sea anemone,Anthopleura uchidai

Intertidal organisms commonly form zonation bands along the shore. Environmental stressors often determine the vertical position of each zonation band. These stressors may similarly affect the distribution pattern of endogenous species in their intertidal hosts. To evaluate this possibility, we investigated the distribution pattern of endosymbiotic zooxanthellae in the genus Symbiodinium in a population of the intertidal sea anemone Anthopleura uchidai. We used molecular genetics to identify the Symbiodinium clades and found that A. uchidai has two clades of Symbiodinium, clades A and F. These Symbiodinium clades were disproportionally distributed along the vertical gradient of the intertidal shore. Anemones on the upper shore exclusively possessed clade F Symbiodinium while clade A Symbiodinium became dominant in the sea anemones on the lower shore. Photosynthesis activity assays showed that these Symbiodinium clades had similar net productivities at 23.3 and 31.8 °C at all irradiance levels. At 35 °C, however, clade A Symbiodinium exhibited substantially lower net productivities than clade F Symbiodinium, demonstrating that these Symbiodinium clades have distinct tolerances to thermal stress. These results suggest that the thermal gradient across tidal height is a major factor shaping the zonation pattern of Symbiodinium clades in A. uchidai.     

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.     

Mode of zooxanthella transmission does not affect zooxanthella diversity in acroporid corals

Two distinct modes of algal endosymbiont acquisition exist in corals, a direct transmission from the parental colony to the eggs and a larval or post-larval uptake from the environment. The former, maternal-transmission mode is expected to be a more closed system, while the latter is believed to be an open system. Here we test the hypothesis that the diversity of symbionts in closed systems is lower than that in open systems. We examine the identity and diversity of the algal endosymbionts (zooxanthellae) in 25 Montipora species sampled from Irian Jaya (Indonesia) and Magnetic Island (central Great Barrier Reef) and compare the results with those previously obtained from Acropora species, which belong to the same family. All Montipora colonies examined harbour clade C zooxanthellae, with two colonies harbouring both clade C and D zooxanthellae simultaneously. Two algal strains (named C· and D· in this study) present in Montipora have not been observed in Acropora, and may have co-evolved with Montipora. Symbiodinium C· shows approximately 5% sequence divergence from C strains observed in Acropora spp. and occurs in 76% of the colonies examined. Nevertheless, several other C strains commonly found in other corals occur in some of the Montipora colonies. Montipora species transmit their algal endosymbionts directly to the eggs, while Acropora species have to acquire zooxanthellae from the environment every generation. Contrary to our expectations, the diversity of zooxanthellae is similar for the two genera, indicating that the mode of symbiont transmission (i.e. maternal versus horizontal) does not affect symbiont diversity in acroporid corals.Communicated by M.S. Johnson, Crawley     

Elevated temperature impairs onset of symbiosis and reduces survivorship in larvae of the Hawaiian coral, <Emphasis Type="Italic">Fungia scutaria</Emphasis>

Many corals obtain their obligate intracellular dinoflagellate symbionts from the environment as larvae or juveniles. The process of symbiont acquisition remains largely unexplored, especially under stress. This study addressed both the ability of Fungia scutaria (Lamarck 1801) larvae to establish symbiosis with Symbiodinium sp. C1f while exposed to elevated temperature and the survivorship of aposymbiotic and newly symbiotic larvae under these conditions. Larvae were exposed to 27, 29, or 31°C for 1 h prior to infection, throughout a 3-h infection period, and up to 72 h following infection. Exposure to elevated temperatures impaired the ability of coral larvae to establish symbiosis and reduced larval survivorship. At 31°C, the presence of symbionts further reduced larval survivorship. As sea surface temperatures rise, coral larvae exposed to elevated temperatures during symbiosis onset will likely be negatively impacted, which in turn could affect the establishment of future generations of corals.     

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.     

Temporal and spatial infection dynamics indicate recognition events in the early hours of a dinoflagellate/coral symbiosis

The obligate symbiotic relationship between dinoflagellates, Symbiodinium spp. and reef building corals is re-established each host generation. The solitary coral Fungia scutaria Lamarck 1801 harbors a single algal strain, Symbiodinium ITS2 type C1f (homologous strain) during adulthood. Previous studies have shown that distinct algal ITS2 types in clade C correlate with F. scutaria—Symbiodinium specificity during the onset of symbiosis in the larval stage. The present study examined the early specificity events in the onset of symbiosis between F. scutaria larvae and Symbiodinium spp., by looking at the temporal and spatial infection dynamics of larvae challenged with different symbiont types. The results show that specificity at the onset of symbiosis was mediated by recognition events during the initial symbiont—host physical contact before phagocytosis, and by subsequent cellular events after the symbionts were incorporated into host cells. Moreover, homologous and heterologous Symbiodinium sp. strains did not exhibit the same pattern of localization within larvae. When larvae were infected with homologous symbionts (C1f), ~70% of the total acquired algae were found in the equatorial area of the larvae, between the oral and aboral ends, 21 h after inoculation. In contrast, no spatial difference in algal localization was observed in larvae infected with heterologous symbionts. This result provides evidence of functional differences among gastrodermal cells, during development of the larvae. The cells in the larval equator function as nutritive phagocytes, and also appear to function as a region of enhanced symbiont acquisition in F. scutaria.     

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.     

Onset of symbiosis and distribution patterns of symbiotic dinoflagellates in the larvae of scleractinian corals

The establishment of symbiosis in early developmental stages is important for reef-building corals because of the need for photosynthetically derived nutrition. Corals spawn eggs and sperm, or brood planula larvae and shed them into the water. Some coral eggs or planulae directly inherit symbiotic dinoflagellates (Symbiodinium spp.) from their parents, while others acquire them at each generation. In most species examined to date, the larvae without dinoflagellates (aposymbiotic larvae) can acquire symbionts during the larval stage, but little is known regarding the timing and detailed process of the onset of symbiosis. We examined larval uptake of symbiotic dinoflagellates in nine species of scleractinian corals, the onset of symbiosis through the early larval stages, and the distribution pattern of symbionts within the larval host, while living and with histology, of two acroporid corals under laboratory conditions. The larvae acquired symbiotic dinoflagellates during the planktonic phase in all corals examined which included Acropora digitifera, A. florida, A. intermedia, A. tenuis, Isopora palifera, Favia pallida, F. lizardensis, Pseudosiderastrea tayamai, and Ctenactis echinata. The larvae of A. digitifera and A. tenuis first acquired symbionts 6 and 5 days after fertilization, respectively. In A. digitifera larvae, this coincided with the formation of an oral pore and coelenteron. The number of symbiotic dinoflagellates increased over the experimental periods in both species. To test the hypothesis that nutrients promotes symbiotic uptake, the number of incorporated dinoflagellates was compared in the presence and absence of homogenized Artemia sp. A likelihood ratio test assuming a log-linear model indicated that Artemia sp. had a significantly positive effect on symbiont acquisition. These results suggest that the acquisition of symbiotic dinoflagellates during larval stages is in common with many coral species, and that the development of both a mouth and coelenteron play important roles in symbiont acquisition.