Ecological Complexity of Coral Recruitment Processes: Effects of Invertebrate Herbivores on Coral Recruitment and Growth Depends Upon Substratum Properties and Coral Species

Sarah W. Davies, Mikhail V. Matz, Integrative Biology Section, The University of Texas at Austin, Austin, Texas, United States of AmericaSarah W. Davies, Peter D. Vize, Department of Biological Sciences, University of Calgary, Calgary, Alberta, CanadaBackground: The transition from planktonic planula to sessile adult corals occurs at low frequencies and post settlement mortality is extremely high. Herbivores promote settlement by reducing algal competition. This study investigates whether invertebrate herbivory might be modulated by other ecological factors such as substrata variations and coral species identity. Methodology/Principal Findings: The experiment was conducted at the Flower Garden Banks, one of the few Atlantic reefs not experiencing considerable degradation. Tiles of differing texture and orientation were kept in bins surrounded by reef (24 m). Controls contained no herbivores while treatment bins contained urchins (Diadema antillarum) or herbivorous gastropods (Cerithium litteratum). Juvenile corals settling naturally were monitored by photography for 14 months to evaluate the effects of invertebrate herbivory and substratum properties. Herbivory reduced algae cover in urchin treatments. Two genera of brooding coral juveniles were observed, Agaricia and Porites, both of which are common but not dominant on adjacent reef. No broadcast spawning corals were observed on tiles. Overall, juveniles were more abundant in urchin treatments and on vertical, rough textured surfaces. Although more abundant, Agaricia juveniles were smaller in urchin treatments, presumably due to destructive overgrazing. Still, Agaricia growth increased with herbivory and substrata texture-orientation interactions were observed with reduced growth on rough tiles in control treatments and increased growth on vertical tiles in herbivore treatments. In contrast to Agaricia, Porites juveniles were larger on horizontal tiles, irrespective of herbivore treatment. Mortality was affected by substrata orientation with vertical surfaces increasing coral survival. Conclusions/Significance: We further substantiate that invertebrate herbivores play major roles in early settlement processes of corals and highlight the need for deeper understanding of ecological interactions modulating these effects. The absence of broadcast-spawning corals, even on a reef with consistently high coral cover, continues to expose the recruitment failure of these reef-building corals throughout the Caribbean.Natural Sciences and Engineering Research Council of Canada (NSERC) PGS-M to SWD; ACCESS Funding from the University of Calgary to SWD; National Science Foundation grant DEB-1054766 to MVM. Boat time provided by FGBNMS under permit# FGBNMS-2007-006. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.Biological Sciences, School ofIntegrative BiologyEmail: [email protected]

Gene expression of endangered coral (Orbicella spp.) in flower garden banks National Marine Sanctuary after Hurricane Harvey

About 190 km south of the Texas–Louisiana border, the East and West Flower Garden Banks (FGB) have maintained > 50% coral cover with infrequent and minor incidents of disease or bleaching since monitoring began in the 1970s. However, a mortality event, affecting 5.6 ha (2.6% of the area) of the East FGB, occurred in late July 2016 and coincided with storm-generated freshwater runoff extending offshore and over the reef system. To capture the immediate effects of storm-driven freshwater runoff on coral and symbiont physiology, we leveraged the heavy rainfall associated with Hurricane Harvey in late August 2017 by sampling FGB corals at two time points: September 2017, when surface water salinity was reduced (∼34 ppt); and 1 month later when salinity had returned to typical levels (∼36 ppt in October 2017). Tissue samples (N = 47) collected midday were immediately preserved for gene expression profiling from two congeneric coral species (Orbicella faveolata and Orbicella franksi) from the East and West FGB to determine the physiological consequences of storm-derived runoff. In the coral, differences between host species and sampling time points accounted for the majority of differentially expressed genes. Gene ontology enrichment for genes differentially expressed immediately after Hurricane Harvey indicated increases in cellular oxidative stress responses. Although tissue loss was not observed on FGB reefs following Hurricane Harvey, our results suggest that poor water quality following this storm caused FGB corals to experience sub-lethal stress. We also found dramatic expression differences across sampling time points in the coral’s algal symbiont, Breviolum minutum. Some of these differentially expressed genes may be involved in the symbionts’ response to changing environments, including a group of differentially expressed post-transcriptional RNA modification genes. In this study, we cannot disentangle the effects of reduced salinity from the collection time point, so these expression patterns could also be related to seasonality. These findings highlight the urgent need for continued monitoring of these reef systems to establish a baseline for gene expression of healthy corals in the FGB system across seasons, as well as the need for integrated solutions to manage stormwater runoff in the Gulf of Mexico.https://www.frontiersin.org/articles/10.3389/fmars.2019.00672/fullPublished versionPublished versio

A Cross-Ocean Comparison of Responses to Settlement Cues in Reef-Building Corals

View the peer-reviewed version (peerj.com/articles/333), which is the preferred citable publication unless you specifically need to cite this preprint. Davies SW, Meyer E, Guermond SM, Matz MV. 2014. A cross-ocean comparison of responses to settlement cues in reef-building corals. PeerJ 2:e333 https://doi.org/10.7717/peerj.333 A cross-ocean comparison of responses to settlement cues in reef-building corals Caribbean coral reefs have deteriorated substantially over the past 30 years, which is broadly attributable to the effects of global climate change. In the same time, Indo-Pacific reefs maintain higher coral cover and typically recover rapidly after disturbances. This difference in reef resilience is largely due to much higher coral recruitment rates in the Pacific. We hypothesized that the lack of Caribbean coral recruitment might be explained by diminishing quality of settlement cues and/or impaired sensitivity of Caribbean coral larvae to those cues, relative to the Pacific. To evaluate this hypothesis, we assembled a collection of bulk samples of reef encrusting communities, mostly consisting of crustose coralline algae (CCA), from various reefs around the world and tested them as settlement cues for several coral species originating from different ocean provinces. Cue samples were meta-barcoded to evaluate their taxonomic diversity. We observed no systematic differences either in cue potency or in strength of larval responses depending on the ocean province, and no preference of coral larvae towards cues from the same ocean. Instead, we detected significant differences in cue preferences among coral species, even for corals originating from the same reef. We conclude that the region-wide disruption of the settlement process is unlikely to be the major cause of Caribbean reef loss. However, due to their high sensitivity to the effects of climate change, shifts in the composition of CCA-associated communities, combined with pronounced differences in cue preferences among coral species, could substantially influence future coral community structure. PeerJ PrePrint

Population genetic structure between Yap and Palau for the coral Acropora hyacinthus

Information on connectivity is becoming increasingly in demand as marine protected areas are being designed as an integral part of a network to protect marine resources at the ecosystem level. Larval dispersal and population structure, however, remain very difficult to assess. Here, we tested the predictions of a detailed oceanographic connectivity model of larval dispersal and coral recruitment within Palau and between Palau and Yap, which was developed to support the review of the existing network of marine protected areas in Palau. We used high throughput microsatellite genotyping of the coral Acropora hyacinthus to characterize population genetic structure. Pairwise F ′ ST values between Palau and Yap (0.10), Palau and Ngulu (0.09) and Yap and Ngulu (0.09) were all significant and similar to pairwise F ′ ST values of sites within Palau (0.02–0.12) and within Yap (0.02–0.09) highlighting structure at island scale and indicating that recruitment may be even more localized than previously anticipated. A bottleneck test did not reveal any signs of a founder effect between Yap and Palau. Overall, the data supports the idea that recovery of A. hyacinthus in Palau did not come exclusively from a single source but most likely came from a combination of areas, including sites within Palau. In light of these results there seems to be very little connectivity around the barrier reef and management recommendation would be to increase the number or the size of MPAs within Palau

EPICOG-SCH: A brief battery to screen cognitive impact of schizophrenia in stable outpatients

Brief batteries in schizophrenia, are needed to screen for the cognitive impact of schizophrenia. We aimed to validate and co-norm the Epidemiological Study of Cognitive Impairment in Schizophrenia (EPICOG-SCH) derived brief cognitive battery. A cross-sectional outpatient evaluation was conducted of six-hundred-seventy-two patients recruited from 234 centers. The brief battery included well-known subtests available worldwide that cover cognitive domains related to functional outcomes: WAIS-III-Letter-Number-Sequencing-LNS, Category Fluency Test-CFT, Logical-Memory Immediate Recall-LM, and Digit-Symbol-Coding-DSC. CGI-SCH Severity and WHO-DAS-S were used to assess clinical severity and functional impairment, respectively. Unit Composite Score (UCS) and functional regression-weighted Composite Scores (FWCS) were obtained; discriminant properties of FWCS to identify patients with different levels of functional disability were analyzed using receiver-operating characteristic (ROC) technique. The battery showed good internal consistency, Cronbach's alpha = 0.78. The differences between cognitive performance across CGI-SCH severity level subscales ranged from 0.5 to 1 SD. Discriminant capacity of the battery in identifying patients with up to moderate disability levels showed fair discriminant accuracy with areas under the curve (AUC) > 0.70, p < 0.0001. An FWCS mean cut-off score ≥ 100 showed likelihood ratios (LR) up to 4.7, with an LR+ of 2.3 and a LR− of 0.5. An FWCS cut-off ≥ 96 provided the best balance between sensitivity (0.74) and specificity (0.62). The EPICOG-SCH proved to be a useful brief tool to screen for the cognitive impact of schizophrenia, and its regression-weighted Composite Score was an efficient complement to clinical interviews for confirming patients' potential functional outcomes and can be useful for monitoring cognition during routine outpatient follow-up visits

Fetal liver blood flow distribution: role in human developmental strategy to prioritize fat deposition versus brain development

Among primates, human neonates have the largest brains but also the highest proportion of body fat. If placental nutrient supply is limited, the fetus faces a dilemma: should resources be allocated to brain growth, or to fat deposition for use as a potential postnatal energy reserve? We hypothesised that resolving this dilemma operates at the level of umbilical blood distribution entering the fetal liver. In 381 uncomplicated pregnancies in third trimester, we measured blood flow perfusing the fetal liver, or bypassing it via the ductus venosus to supply the brain and heart using ultrasound techniques. Across the range of fetal growth and independent of the mother's adiposity and parity, greater liver blood flow was associated with greater offspring fat mass measured by dual-energy X-ray absorptiometry, both in the infant at birth (r = 0.43, P&lt;0.001) and at age 4 years (r = 0.16, P = 0.02). In contrast, smaller placentas less able to meet fetal demand for essential nutrients were associated with a brain-sparing flow pattern (r = 0.17, p = 0.02). This flow pattern was also associated with a higher degree of shunting through ductus venosus (P = 0.04). We propose that humans evolved a developmental strategy to prioritize nutrient allocation for prenatal fat deposition when the supply of conditionally essential nutrients requiring hepatic inter-conversion is limited, switching resource allocation to favour the brain if the supply of essential nutrients is limited. Facilitated placental transfer mechanisms for glucose and other nutrients evolved in environments less affluent than those now prevalent in developed populations, and we propose that in circumstances of maternal adiposity and nutrient excess these mechanisms now also lead to prenatal fat deposition. Prenatal developmental influences play important roles in the human propensity to deposit fa

To What Extent is Blood a Reasonable Surrogate for Brain in Gene Expression Studies: Estimation from Mouse Hippocampus and Spleen

Microarrays are designed to measure genome-wide differences in gene expression. In cases where a tissue is not accessible for analysis (e.g. human brain), it is of interest to determine whether a second, accessible tissue could be used as a surrogate for transcription profiling. Surrogacy has applications in the study of behavioural and neurodegenerative disorders. Comparison between hippocampus and spleen mRNA obtained from a mouse recombinant inbred panel indicates a high degree of correlation between the tissues for genes that display a high heritability of expression level. This correlation is not limited to apparent expression differences caused by sequence polymorphisms in the target sequences and includes both cis and trans genetic effects. A tissue such as blood could therefore give surrogate information on expression in brain for a subset of genes, in particular those co-expressed between the two tissues, which have heritably varying expression

Varied effects of algal symbionts on transcription factor NF-κB in a sea anemone and a coral: possible roles in symbiosis and thermotolerance

Many cnidarians, including the reef-building corals, undergo symbiotic mutualisms with photosynthetic dinoflagellate algae of the family Symbiodiniaceae. These partnerships are sensitive to temperature extremes, which cause symbiont loss and increased coral mortality. Previous studies have implicated host immunity and specifically immunity transcription factor NF-κB as having a role in the maintenance of the cnidarian-algal symbiosis. Here we have further investigated a possible role for NF-κB in establishment and loss of symbiosis in various strains of the anemone Exaiptasia (Aiptasia) and in the coral Pocillopora damicornis. Our results show that NF-κB expression is reduced in Aiptasia larvae and adults that host certain algae strains. Treatment of Aiptasia larvae with a known symbiosis-promoting cytokine, transforming growth factor β, also led to decreased NF-κB expression. We also show that aposymbiotic Aiptasia (with high NF-κB expression) have increased survival following infection with the pathogenic bacterium Serratia marcescens as compared to symbiotic Aiptasia (low NF-κB expression). Furthermore, a P. damicornis coral colony hosting Durusdinium spp. (formerly clade D) symbionts had higher basal NF-κB expression and decreased heat-induced bleaching as compared to two individuals hosting Cladocopium spp. (formerly clade C) symbionts. Lastly, genome-wide gene expression profiling and genomic promoter analysis identified putative NF-κB target genes that may be involved in thermal bleaching, symbiont maintenance, and/or immune protection in P. damicornis. Our results provide further support for the hypothesis that modulation of NF-κB and immunity plays a role in some, but perhaps not all, cnidarian-Symbiodiniaceae partnerships as well as in resistance to pathogens and bleaching.Accepted manuscrip

A cross-ocean comparison of responses to settlement cues in reef-building corals

Caribbean coral reefs have deteriorated substantially over the past 30 years, which is broadly attributable to the effects of global climate change. In the same time, Indo-Pacific reefs maintain higher coral cover and typically recover rapidly after disturbances. This difference in reef resilience is largely due to much higher coral recruitment rates in the Pacific. We hypothesized that the lack of Caribbean recruitment might be explained by diminishing quality of settlement cues and/or impaired sensitivity of Caribbean coral larvae to those cues, relative to the Pacific. To evaluate this hypothesis, we assembled a collection of bulk samples of reef encrusting communities, mostly consisting of crustose coralline algae (CCA), from various reefs around the world and tested them as settlement cues for several coral species originating from different ocean provinces. Cue samples were meta-barcoded to evaluate their taxonomic diversity. We observed no systematic differences either in cue potency or in strength of larval responses depending on the ocean province, and no preference of coral larvae towards cues from the same ocean. Instead, we detected significant differences in cue preferences among coral species, even for corals originating from the same reef. We conclude that the region-wide disruption of the settlement process is unlikely to be the major cause of Caribbean reef loss. However, due to their high sensitivity to the effects of climate change, shifts in the composition of CCA-associated communities, combined with pronounced differences in cue preferences among coral species, could substantially influence future coral community structure.This is the publisher’s final pdf. The published article is copyrighted by the author(s) and published by PeerJ. The published article can be found at: https://peerj.com/.Keywords: Settlement cues, Meta-barcoding, OTU, Ecology, Coral recruitment, Crustose coralline algae, Marine Biology, 18S rRN

Eukaryotic Plankton Communities Across Reef Environments in Bocas del Toro Archipelago, Panamá

Variation in light and temperature can influence the genetic diversity and structure of marine plankton communities. While open-ocean plankton communities receive much scientific attention, little is known about how environmental variation affects plankton communities on tropical coral reefs. Here, we characterize eukaryotic plankton communities on coral reefs across the Bocas del Toro Archipelago, Panama´. Temperature loggers were deployed, and midday light levels were measured to quantify environmental differences across reefs at four inshore and four offshore sites (Inshore = Punta Donato, Smithsonian Tropical Research Institute (STRI) Point, Cristobal, Punta Laurel and Offshore = Drago Mar, Bastimentos North, Bastimentos South, and Cayo de Agua). Triplicate vertical plankton tows were collected midday, and high-throughput 18S ribosomal DNA metabarcoding was leveraged to investigate the relationship between eukaryotic plankton community structure and inshore/offshore reef environments. Plankton communities from STRI Point were additionally characterized in the morning (* 08:00), midday (* 12:00), and late-day (* 16:00) to quantify temporal variation within a single site. We found that inshore reefs experienced higher average seawater temperatures, while offshore sites offered higher light levels, presumably associated with reduced water turbidity on reefs further from shore. These significant environmental differences between inshore and offshore reefs corresponded with overall plankton community differences. We also found that temporal variation played a structuring role within these plankton communities, and conclude that time of community sampling is an important consideration for future studies. Follow-up studies focusing on more intensive sampling efforts across space and time, coupled with techniques that can detect more subtle genetic differences between and within communities will more fully capture plankton dynamics in this region and beyond