Complementary (secondary) metabolites in an octocoral competing with a scleractinian coral: effects of varying nutrient regimes

Competitive interactions between two sessile, epibenthic species were investigated on the Great Barrier Reef (GBR) in the presence and absence of added nutrients, as part of the Enrichment of Nutrients on Coral Reefs Experiment (ENCORE). Sarcophyton ehrenbergi Marenzeller (Octocorallia: Alcyonacea), an alcyonacean soft coral, and Pocillopora damicornis (Linnaeus), a scleractinian coral, were relocated and placed in contact with each other on large plastic grids on each of 12 micro-atolls within the One Tree Island (OTI) lagoon (23°30′S, 152°96′E, GBR). These micro-atolls were allocated in equal-sized groups to three enrichment treatments (addition of nitrogen, N; addition of phosphorus, P; addition of both nitrogen and phosphorus, N+P) and one control. Non-relocated (NR) and relocated colonies were also monitored as controls. After relocation and 1 year of nutrient enrichment, concentrations of a terpenoid complementary metabolite—sarcophytoxide—and wax esters were analyzed in colonies of S. ehrenbergi that had been exposed to elevated concentrations of N, P, N+P and compared with colonies on the non-nutrient-enriched control. Non-relocated control colonies from the natural environment were monitored over a period of 1 year and compared to colonies relocated to the control micro-atolls to assess handling effects. Analyses were performed on non-interacting S. ehrenbergi colonies, S. ehrenbergi colonies in experimental contact with P. damicornis colonies, and on non-interacting S. ehrenbergi colonies from the site of initial collection. Significant differences were found between sarcophytoxide levels in colonies of S. ehrenbergi in contact with P. damicornis vs. control/non-contact colonies; contact colonies had higher levels of this metabolite. Non-relocated control colonies of S. ehrenbergi exhibited significantly higher levels of sarcophytoxide than relocated control colonies. Augmentation of nutrient levels in micro-atolls significantly increased sarcophytoxide levels in S. ehrenbergi colonies relative to colonies on the control micro-atolls, although this response was not strong. Concentrations of fatty esters increased significantly through time in S. ehrenbergi colonies in their natural setting (non-relocated controls). This variability was not observed in relocated colonies in the treatment and control micro-atolls, irrespective of contact with P. damicornis. Concentrations of fatty esters in colonies of S. ehrenbergi in contact with P. damicornis were significantly lower than control/non-contact colonies, indicating that there is a cost in terms of stored energy reserves for the production of additional complementary metabolites when involved in competition for space. Augmentation of P levels in micro-atolls induced significant increases in fatty ester levels within S. ehrenbergi colonies vs. colonies in control micro-atolls, or in micro-atolls treated with added N or N+P together. These findings indicate that interspecific competition for space between a scleractinian coral and an alcyonacean soft coral and/or changes in the environmental nutrient regime can influence concentrations of complementary/secondary metabolites in the alcyonacean coral and the organism's stored energy reserves.     

The ecological and anatomy of a new species of aeolid opisthobranch mollusc; a predator of the scleractinian coral Porites

A new species of aeolid opisthobranch (family Tergipedidae) is described from Tanzania. It lives and feeds on the scleractinian coral Porites somaliensis. Studies on its development show that it can reach sexual maturity three weeks after hatching. The larval stage is extremely abbreviated; the veliger settles ten minutes after hatching, and within ninety minutes of hatching has assumed a slug-like form.     

Gene expression under chronic heat stress in populations of the mustard hill coral (Porites astreoides) from different thermal environments

Recent evidence suggests that corals can acclimatize or adapt to local stress factors through differential regulation of their gene expression. Profiling gene expression in corals from diverse environments can elucidate the physiological processes that may be responsible for maximizing coral fitness in their natural habitat and lead to a better understanding of the coral's capacity to survive the effects of global climate change. In an accompanying paper, we show that Porites astreoides from thermally different reef habitats exhibit distinct physiological responses when exposed to 6 weeks of chronic temperature stress in a common garden experiment. Here, we describe expression profiles obtained from the same corals for a panel of 9 previously reported and 10 novel candidate stress response genes identified in a pilot RNA‐Seq experiment. The strongest expression change was observed in a novel candidate gene potentially involved in calcification, SLC26, a member of the solute carrier family 26 anion exchangers, which was down‐regulated by 92‐fold in bleached corals relative to controls. The most notable signature of divergence between coral populations was constitutive up‐regulation of metabolic genes in corals from the warmer inshore location, including the gluconeogenesis enzymes pyruvate carboxylase and phosphoenolpyruvate carboxykinase and the lipid beta‐oxidation enzyme acyl‐CoA dehydrogenase. Our observations highlight several molecular pathways that were not previously implicated in the coral stress response and suggest that host management of energy budgets might play an adaptive role in holobiont thermotolerance.     

Diversity and dynamics of bacterial communities in early life stages of the Caribbean coral Porites astreoides

In this study, we examine microbial communities of early developmental stages of the coral Porites astreoides by sequence analysis of cloned 16S rRNA genes, terminal restriction fragment length polymorphism (TRFLP), and fluorescence in situ hybridization (FISH) imaging. Bacteria are associated with the ectoderm layer in newly released planula larvae, in 4-day-old planulae, and on the newly forming mesenteries surrounding developing septa in juvenile polyps after settlement. Roseobacter clade-associated (RCA) bacteria and Marinobacter sp. are consistently detected in specimens of P. astreoides spanning three early developmental stages, two locations in the Caribbean and 3 years of collection. Multi-response permutation procedures analysis on the TRFLP results do not support significant variation in the bacterial communities associated with P. astreoides larvae across collection location, collection year or developmental stage. The results are the first evidence of vertical transmission (from parent to offspring) of bacteria in corals. The results also show that at least two groups of bacterial taxa, the RCA bacteria and Marinobacter, are consistently associated with juvenile P. astreoides against a complex background of microbial associations, indicating that some components of the microbial community are long-term associates of the corals and may impact host health and survival.     

Evidence for a host role in thermotolerance divergence between populations of the mustard hill coral (Porites astreoides) from different reef environments

Studying the mechanisms that enable coral populations to inhabit spatially varying thermal environments can help evaluate how they will respond in time to the effects of global climate change and elucidate the evolutionary forces that enable or constrain adaptation. Inshore reefs in the Florida Keys experience higher temperatures than offshore reefs for prolonged periods during the summer. We conducted a common garden experiment with heat stress as our selective agent to test for local thermal adaptation in corals from inshore and offshore reefs. We show that inshore corals are more tolerant of a 6‐week temperature stress than offshore corals. Compared with inshore corals, offshore corals in the 31 °C treatment showed significantly elevated bleaching levels concomitant with a tendency towards reduced growth. In addition, dinoflagellate symbionts (Symbiodinium sp.) of offshore corals exhibited reduced photosynthetic efficiency. We did not detect differences in the frequencies of major (>5%) haplotypes comprising Symbiodinium communities hosted by inshore and offshore corals, nor did we observe frequency shifts (‘shuffling’) in response to thermal stress. Instead, coral host populations showed significant genetic divergence between inshore and offshore reefs, suggesting that in Porites astreoides, the coral host might play a prominent role in holobiont thermotolerance. Our results demonstrate that coral populations inhabiting reefs <10‐km apart can exhibit substantial differences in their physiological response to thermal stress, which could impact their population dynamics under climate change.     

The effect of temperature on the size and population density of dinoflagellates in larvae of the reef coral Porites astreoides

Abstract. Pre-settlement events play an important role in determining larval success in marine invertebrates with bentho-pelagic life histories, yet the consequences of these events typically are not well understood. The purpose of this study was to examine the pre-settlement impacts of different seawater temperatures on the size and population density of dinoflagellate symbionts in brooded larvae of the Caribbean coral Porites astreoides. Larvae were collected from P. astreoides at 14–20 m depth on Conch Reef (Florida) in June 2002, and incubated for 24 h at 15 temperatures spanning the range 25.1°–30.0°C in mean increments of 0.4±0.1°C (±SD). The most striking feature of the larval responses was the magnitude of change in both parameters across this 5°C temperature range within 24 h. In general, larvae were largest and had the highest population densities of Symbiodinium sp. between 26.4°–27.7°C, and were smallest and had the lowest population densities at 25.8°C and 28.8°C. Larval size and symbiont population density were elevated slightly (relative to the minimal values) at the temperature extremes of 25.1°C and 30°C. These data demonstrate that coral larvae are highly sensitive to seawater temperature during their pelagic phase, and respond through changes in size and the population densities of Symbiodinium sp. to ecologically relevant temperature signals within 24 h. The extent to which these changes are biologically meaningful will depend on the duration and frequency of exposure of coral larvae to spatio-temporal variability in seawater temperature, and whether the responses have cascading effects on larval success and their entry to the post-settlement and recruitment phase.     

Genetic diversity and large-scale connectivity of the scleractinian coral Porites lutea in the South China Sea

Coral Reefs - In light of recent declines in scleractinian communities worldwide, research on the genetic structure of and connectivity among coral populations has assumed importance. However, the...     

Physiological responses to short-term sediment exposure in adults of the Caribbean coral Montastraea cavernosa and adults and recruits of Porites astreoides

Coral Reefs - Sedimentation is a common anthropogenic stressor known to reduce coral growth, reproduction, and the photosynthetic capacity of their endosymbiotic algae. This study assessed the...     

Elevated temperature reduces survivorship and settlement of the larvae of the Caribbean scleractinian coral, Favia?fragum (Esper)

The effect of elevated seawater temperatures, such as those plaguing tropical seas during the summers of anomalously warm years, on early life stages of reef corals remains poorly studied. To redress this situation, survivorship of larvae of the brooding coral, Favia fragum, was studied in the laboratory, using both short term (48 h) and long term (156–191 h) exposures to 28, 29, and 31°C. Ability to settle when presented with induction substrates and survival after settlement, at the same exposure temperature and after reciprocal transfers to the other experimental temperatures, were also measured. No significant effect of temperature on survivorship was detected after 48 h of exposure, but larvae incubated for 156 h at the highest temperature (31°C) exhibited a 13% reduced survivorship compared to larvae at 28°C. Induction of settlement further increased mortality at the highest temperature (31°C); survivorship after settlement at 31°C was 27% lower than when larvae were simply maintained at the elevated temperature. These results indicate that elevated temperatures are more detrimental to coral larvae undergoing the developmentally complex settlement process than to the swimming planula stage. This may bode poorly for Caribbean corals with late summer reproductive seasons. Communicated by Ecology Editor Prof. Peter Mumby     

Effects of delayed settlement on post-settlement growth and survival of scleractinian coral larvae

Demographic connectivity requires both the dispersal of individuals between sub-populations, and their subsequent contribution to population dynamics. For planktonic, non-feeding marine larvae, the capacity to delay settlement enables greater dispersal distances, but the energetic cost of delayed settlement has been shown to adversely impact post-settlement fitness in several taxa. Here, we assess whether delayed settlement influences mortality rates or growth rates for the first 6 weeks following settlement of the scleractinian coral, Acropora tenuis. Coral larvae that were settled at 2, 4, and 6 weeks after spawning, and then deployed in the field, showed negligible effects of delayed settlement on post-settlement survival and time to initial budding for colony formation. Between-cohort differences in budding rate appeared to be explained by temporal variation in the post-settlement acquisition of zooxanthellae. The potential for coral larvae to remain in the pelagic zone for increased periods of time with little to no effect on post-settlement survival and growth suggests that the capacity for delayed settlement is likely to have meaningful demographic consequences for broadcast-spawning reef-building corals, and that the predicted trade-off between delayed settlement and post-settlement fitness is less applicable to reef-building scleractinian corals than other taxa with non-feeding larvae.     

Competition between macroalgae and corals: effects of herbivore exclusion and increased algal biomass on coral survivorship and growth

Recent declines in coral abundance accompanied by increases in macroalgal cover on Florida reefs highlight the importance of competition for space between these groups. This paper documents the frequency of coral-algal interactions on the Northern Florida Reef Tract and evaluates the effects of grazer exclusions and experimental algal addition on growth and tissue mortality of three coral species, Siderastrea siderea, Porites astreoides, and Montastraea faveolata. The frequency of interactions between corals and macroalgae was high as more than 50% of the basal perimeter of colonies was in contact with macroalgae; turf forms, Halimeda spp., and Dictyota spp. were the most common groups in contact with corals. Decreased grazing pressure resulted in significant increases in algal biomass within cages, and caged corals showed species-specific susceptibility to increased algal biomass. While no effects were detected for S. siderea, significant decreases in growth rates were documented for caged P. astreoides which had growth rates three to four times lower than uncaged colonies. When an algal addition treatment was included to duplicate maximum algal biomass levels documented for reefs in the area, colonies of P. astreoides in the algal addition treatment had growth rates up to ten times lower than uncaged colonies. High susceptibility to algal overgrowth was also found for the reef-building coral M. faveolata, which experienced significant tissue mortality under both uncaged (5.2% decrease in live tissue area per month) and caged (10.2% per month) conditions. The documented effects of increased algal biomass on coral growth and tissue mortality suggest a potential threat for the long-term survivorship and growth of corals in the Florida Reef Tract if present rates of algal growth and space utilization are maintained.     

Spatial and temporal patterns of scleractinian coral, soft coral, and zoanthid disease on a remote, near-pristine coral reef (Palmyra Atoll, central Pacific)

There is an urgent need for accurate baselines of coral disease prevalence across our oceans in order for sudden or unnatural changes to be recognized. Palmyra Atoll allows us to study disease dynamics under near-pristine, functionally intact conditions. We examined disease prevalence among all known species of scleractinian coral, soft coral and zoanthid (Palythoa) at a variety of coral reef habitats at Palmyra over a 2 yr period. In 2008, overall disease prevalence across the atoll was low (0.33%), but higher on the shallower backreef (0.88%) and reef terrace (0.80%) than on the deeper forereef (0.09%). Scleractinian coral disease prevalence was higher (0.30%) than were soft coral and zoanthid disease (0.03% combined). Growth anomalies (GAs) were the most commonly encountered lesions, with scleractinian species in the genera Astreopora (2.12%), Acropora (1.30%), and Montipora (0.98%) showing the highest prevalence atoll-wide. Discoloration necrosis (DN) was most prevalent in the zoanthid Palythoa tuberculosa (1.18%), although the soft coral Sinulana and Montipora also had a prevalence of 0.44 and 0.01%, respectively. Overall disease prevalence within permanently marked transects increased from 0.65% in 2008 to 0.79% in 2009. Palythoa DN contributed most to this increased prevalence, which coincided with rising temperatures during the 2009 El Ni?o. GAs on the majority of susceptible genera at Palmyra increased in number over time, and led to tissue death. Host distribution and environmental factors (e.g., temperature) appear to be important for determining spatiotemporal patterns of disease at Palmyra. More sophisticated analyses are required to tease apart the likely inter-correlated proximate drivers of disease occurrence on remote, near-pristine reefs.     

Calcification rate and the effect of temperature in a zooxanthellate and an azooxanthellate scleractinian reef coral

Calcification rates, normalized to skeletal mass, in the zooxanthellate Galaxea fascicularis and the azooxanthellate Dendrophyllia sp. were similar over the whole temperature range of 18–29 °C. Calcification was measured by Ca⁴⁵ incorporation in corals that were naturally acclimated to the prevailing seawater temperature. In both species maximum calcification rate occurred at about 25 °C and calcification rates can be fitted to a Gaussian distribution with respect to temperature. The similarity in temperature dependence of the zooxanthellate and azooxanthellate coral suggests that temperature affects some fundamental process of calcification that is independent of light effects. It is shown that two different populations of Galaxea fascicularis have distinctly different ratios of tissue protein to skeletal mass per polyp. This indicates that tissue protein may not be suitable for normalizing calcification rates in individual coral polyps, both within and between species. Intra- and interspecific comparisons of calcification rates may be better made on the basis of skeletal mass when polyps are similar in size and shape.Communicated by Topic Editor C. Barnes     

Effects of predator exclusion on nest and hatchling survival in the gopher tortoise

Gopher tortoise (Gopherus polyphemus) populations are declining throughout the Southeast, and high levels of predation on nests and juveniles have been suggested as a potential contributor to this decline. Therefore, we documented gopher tortoise nest success and hatchling survival relative to mammalian predator control. We used 4, large (approx. 40-ha) fenced, predator exclosures to exclude mid-sized mammalian predators: bobcat (Lynx rufus), raccoon (Procyon lotor), Virginia opossum (Didelphis virginianus), fox (Urocyon cinereoargenteus and Vulpes vulpes), coyote (Canis latrans), nine-banded armadillo (Dasypus novemcinctus), and skunk (Mephitis mephitis); 4 unfenced plots served as controls. We monitored nests for survival through hatching and used radio-telemetry to examine hatchling survival. We radio-tracked 40 hatchlings for up to 329 days, but we were only able to track 8 individuals from a single nest at an unfenced plot because of high nest predation. Mean nest survival was greater at exclosures than at unfenced controls (F_{1, 2} = 45.80, P = 0.0001). Hatchling survival differed (χ² = 5.839, P = 0.016) between unfenced plots (37.5%) and exclosures (74.4%), suggesting that mammals also were significant predators of hatchlings. The number of juvenile (<13 cm in diameter) and subadult tortoise burrows (13–21.9 cm) increased over a 6-year period in exclosures, providing further support for an effect of excluding mammalian predators on nest and juvenile tortoise survival. © 2012 The Wildlife Society.     

Effects of predators and grazers exclusion on early post-settlement coral mortality

Mortality of newly settled individuals is a key factor in shaping adult population size and distribution of many marine invertebrates. Despite this recognized importance, few studies have addressed early post-settlement mortality rates and causes in reef-building corals. To investigate the effects of exclusion of macro-predators and grazers on mortality of Acropora striata (Verrill) recruits, a caging experiment was completed at Moorea, French Polynesia. More than half of the recruits died within 7 days in the field, and although the exclusion of macro-predators and grazers did not significantly reduce nor enhance mortality, it certainly altered their cause. In the presence of macro-predators and grazers, coral recruits faced significant predation-induced mortality (50.0% of dead recruits presented a heavily damaged or missing skeleton). Conversely, in the absence of macro-predators and grazers, dead recruits were mainly intact (91.7%), and most likely suffered from competition with turf algae and associated sediment trapping. These results underline complex interacting effects of predation, competition with turf algae, and sedimentation on coral early post-settlement mortality.     

Intracellular crystal-bearing vesicles in the epidermis of scleractinian corals, Astrangia danae (Agassiz) and Porites porites (Pallas).

Orthorhombic aragonitic crystals, embedded with a granular lipo-protein matrix and surrounded by a trilaminar membrane, are localized in the apical cytoplasm of epidermal cells of Scleractinian corals. Adult specimens of Astrangia danae (Agassiz) and settled planulae of Porites porites (Pallas) contain crystals averaging 0.7 mu by 0.1 mu by 0.3 mu within Golgi-derived vesicles. Short-term labelling with 45Ca reveals distribution of radioactivity amont a basic tissue fraction (92%) an acid tissue fraction (5%) and a skeletal fraction (3%). Identification of the primordial crystal population within membrane-bound visicles provides overwhelming evidence for the intracellular mode of calcification in Scleractinia. Moreover, it permits development of a novel concept of cellular regulation over these dynamic events. The membrane-bound vesicel is a miniature crystal fabrication station and a vehicle responsible for transportation of seed crystals and an organic matrix material to sites of discharge from the cell. The vesicle membrane becomes a probable locus of active transport and enzymatic activity as well as a physical barrier to be penetrated for release of vesicle contents into the extracellular milieu. Contact between the vesicle membrane and the plasmalemma would result in exocytosis and the onset of skeletogenesis. Principles governing crystal growth would prevail from then on. The released crystal becomes a nucleation catalyst and the organic matrix, a supply of ionic calcium for self-limiting crystallization. Crystals are produced by the organism spontaneously and continuously from shortly after larval attachment throughout the life of the polyp. Therefore, these membrane-bound vesicles signal the dynamic process by which initiation, differentiation, growth and limitation of the coral skeleton is regulated.     

Allometric scaling in small colonies of the scleractinian coral Siderastrea siderea (Ellis and Solander)

Although most physiological traits scale allometrically in unitary organisms, it has been hypothesized that modularity allows for isometric scaling in colonial modular taxa. Isometry would allow increases in size without functional constraints, and is thought to be of central importance to the success of a modular design. Yet, despite its potential importance, scaling in these organisms has received little attention. To determine whether scleractinian corals are free of allometric constraints, we quantified metabolic scaling, measured as aerobic respiration, in small colonies (< or =40 mm in diam.) of the scleractinian Siderastrea siderea. We also quantified the scaling of colony surface area with biomass, since the proposed isometry is contingent upon maintaining a constant ratio of surface area to biomass (or volume) with size. Contrary to the predicted isometry, aerobic respiration scaled allometrically on biomass with a slope (b) of 0.176, and colony surface area scaled allometrically on biomass with a slope of 0.730. These findings indicate that small colonies of S. siderea have disproportionately high metabolic rates and SA:B ratios compared to their larger counterparts. The most probable explanations for the allometric scaling of aerobic respiration are (1) a decline in the SA:B ratio with size such that more surface area is available per unit of biomass for mass transfer in the smallest colonies, and (2) the small size, young age, and disproportionately high growth rates of the corals examined. This allometric scaling also demonstrates that modularity, alone, does not allow small colonies of S. siderea to overcome allometric constraints. Further studies are required to determine whether allometric scaling is characteristic of the full size range of colonies of S. siderea.     

New genera of Copepoda (Poecilostomatoida) from the scleractinian coral Psammocora in New Caledonia

Three new monotypic genera of copepods (Poecilostomatoida) are associated with the hermatypic shallow-water coral Psammocora (Stephanaria) logianensis near Noumea, New Caledonia: in the Anchimolgidae, Lipochaetes extrusus (antenna 4-segmented, endopods absent in legs 3 and 4) and Dumbeana undulatipes (antenna 3-segmcntcd, endopod of leg 3 with formula 0 1; 0–2; 1,11,2; leg 4 endopod with 0 1:1); and in the Rhynchomolgidae; Emunoa proknta (leg 4 endopod with 0 1;II, antenna 4-segmented, mandible witli outer pointed process and inner row of spines). Copepoda (primarily Poecilostomatoida and Siphonostomatoida, but also relatively few Cyclopoida and Harpacticoida) are very frequent associates or parasites of Scleractinia. At present 245 species from 48 scleractinian coral genera are known. Species of these copepod associates, their host genera, and localities, described since (and those not included in) previous publications of the author are listed.     

Effects of temperature and UV radiation increases on the photosynthetic efficiency in four scleractinian coral species

Experiments were performed on coral species containing clade A (Stylophora pistillata, Montipora aequituberculata) or clade C (Acropora sp., Pavona cactus) zooxanthellae. The photosynthetic efficiency (F(v)/F(m)) of the corals was first assessed during a short-term increase in temperature (from 27 degrees C to 29 degrees C, 32 degrees C, and 34 degrees C) and acute exposure to UV radiation (20.5 W m(-2) UVA and 1.2 W m(-2) UVB) alone or in combination. Increasing temperature to 34 degrees C significantly decreased the F(v)/F(m) in S. pistillata and M. aequituberculata. Increased UV radiation alone significantly decreased the F(v)/F(m) of all coral species, even at 27 degrees C. There was a combined effect of temperature and UV radiation, which reduced F(v)/F(m) in all corals by 25% to 40%. During a long-term exposure to UV radiation (17 days) the F(v)/F(m) was significantly reduced after 3 days' exposure in all species, which did not recover their initial values, even after 17 days. By this time, all corals had synthesized mycosporine-like amino acids (MAAs). The concentration and diversity of MAAs differed among species, being higher for corals containing clade A zooxanthellae. Prolonged exposure to UV radiation at the nonstressful temperature of 27 degrees C conferred protection against independent, thermally induced photoinhibition in all four species.