Temporal variation in macroalgal removal: insights from an impacted equatorial coral reef system

Macroalgal removal is a critical ecosystem function yet few studies have considered its temporal variability, especially on impacted reefs with limited herbivorous fish biodiversity. To address this, we quantified macroalgal removal and mass-standardised bite rates of herbivorous fishes monthly from July 2016 to June 2017 using a series of transplanted Sargassum ilicifolium assays and underwater video cameras on three degraded coral reefs in Singapore: Pulau Satumu, Kusu Island, and Terumbu Pempang Tengah. Our results revealed a distinct temporal pattern in macroalgal herbivory (proportion of biomass removed and mass-standardised bite rates) rates across all sites, increasing from July and decreasing from January, with the highest rates recorded in December (28.10 ± 3.05 g 3.5 h−1; 208.24 ± 29.99 mass-standardised bites 3.5 h−1) and the lowest in May (0.86 ± 0.17 g 3.5 h−1; 9.55 ± 3.19 mass-standardised bites 3.5 h−1). These coincided with the S. ilicifolium growth cycle, confirming previous evidence that herbivory rates are closely linked to macroalgal condition. Video analyses revealed nine species feeding over a year (31,839 bites; 8702.89 mass-standardised bites), with Siganus virgatus responsible for ∼ 80% of the total mass-standardised bites. Siganus virgatus took the largest proportion of bites monthly, except between April and June, when Scarus rivulatus was dominant, suggesting temporal constraints in functional roles

Macroalgal browsing on a heavily degraded, urbanized equatorial reef system

The removal of macroalgal biomass is critical to the health of coral reef ecosystems. Previous studies on relatively intact reefs with diverse and abundant fish communities have quantified rapid removal of macroalgae by herbivorous fishes, yet how these findings rel ate to degraded reef systems where fish diversity and abundance are markedly lower and algal biomass substantially higher, is unclear. We surveyed roving herbivorous fish communities and quantified their capacity to remove the dominant macroalga Sargassum ilicifolium on seven reefs in Singapore; a heavily degraded urbanized reef system. The diversity and abundance of herbivorous fishes was extremely low, with eight species and a mean abundance ~1.1 individuals 60 m -2 recorded across reefs. Consumption of S. ilicifolium varied with distance from Singapore's main port with consumption being 3- to 17-fold higher on reefs furthest from the port (Pulau Satumu: 4.18 g h -1 ; Kusu Island: 2.38 g h -1 ) than reefs closer to the port (0.35-0.78 g h -1 ). Video observations revealed a single species, Siganus virgatus, was almost solely responsible for removing S. ilicifolium biomass, accounting for 83% of the mass-standardized bites. Despite low herbivore diversity and intense urbanization, macroalgal removal by fishes on some Singaporean reefs was directly comparable to rates reported for other inshore Indo-Pacific reefs

Fear effects and group size interact to shape herbivory on coral reefs

Fear of predators (‘fear effects’) is an important determinant of foraging decisions by consumers across a range of ecosystems. Group size is one of the main behavioural mechanisms for mitigating fear effects while also providing foraging benefits to group members. Within coral reef ecosystems, fear effects have been shown to influence the feeding rates of herbivorous fishes, a key functional group that prevents macroalgal overgrowth. Yet, how fear effects and group size interact to shape macroalgal removal on coral reefs remains unclear. Here, we conducted field-based experiments using models of a common piscivorous fish, the leopard coral grouper Plectropomus leopardus and a series of macroalgal Sargassum ilicifolium assays positioned at increasing distances from the models (1, 2, 3 and 4 m) on two coral reefs in Singapore to investigate how acute fear effects shape the intensity of herbivory, and whether these effects were influenced by variation in the group size of herbivorous fishes feeding on the assays. We found acute fear effects strongly influenced the foraging behaviour of herbivorous fishes over small spatial scales. Rates of Sargassum biomass removal, feeding rates and the total number of individual feeding events were all lower near the predator model. These effects dissipated rapidly with increasing distance from the predator model and were undetectable at a distance of 4 m. We also found generally larger group sizes of herbivorous fishes further from the predator model, presumably reflecting decreased risk. Furthermore, the number of individual bites/event increased significantly with increasing group size for two common browsing fishes, Siganus virgatus and Siganus javus. Our findings highlight that acute fear effects influence the distribution and intensity of herbivory over small spatial scales. Fear effects also interacted with herbivore group size resulting in changes in the number of individual feeding events and bite rates that collectively shape the realized ecosystem function of macroalgal removal on coral reefs. Group size is an important context-dependent factor that should be considered when examining fear effects on coral reefs. A free Plain Language Summary can be found within the Supporting Information of this article

Latitudinal variation in monthly-scale reproductive synchrony among Acropora coral assemblages in the Indo-Pacific

Early research into coral reproductive biology suggested that spawning synchrony was driven by variations in the amplitude of environmental variables that are correlated with latitude, with synchrony predicted to break down at lower latitudes. More recent research has revealed that synchronous spawning, both within and among species, is a feature of all speciose coral assemblages, including equatorial reefs. Nonetheless, considerable variation in reproductive synchrony exists among locations and the hypothesis that the extent of spawning synchrony is correlated with latitude has not been formally tested on a large scale. Here, we use data from 90 sites throughout the Indo-Pacific and a quantitative index of reproductive synchrony applied at a monthly scale to demonstrate that, despite considerable spatial and temporal variation, there is no correlation between latitude and reproductive synchrony. Considering the critical role that successful reproduction plays in the persistence and recovery of coral reefs, research is urgently needed to understand the drivers underpinning variation in reproductive synchrony

MinION-in-ARMS: Nanopore Sequencing to Expedite Barcoding of Specimen-Rich Macrofaunal Samples From Autonomous Reef Monitoring Structures

Autonomous Reef Monitoring Structure (ARMS) are standardized devices for sampling biodiversity in complex marine benthic habitats such as coral reefs. When coupled with DNA sequencing, these devices greatly expand our ability to document marine biodiversity. Unfortunately, the existing workflow for processing macrofaunal samples (\u3e2-mm) in the ARMS pipeline—which involves Sanger sequencing—is expensive, laborious, and thus prohibitive for ARMS researchers. Here, we propose a faster, more cost-effective alternative by demonstrating a successful application of the MinION-based barcoding approach on the \u3e2 mm-size fraction of ARMS samples. All data were available within 3.5–4 h, and sequencing costs relatively low at approximately US$3 per MinION barcode. We sequenced the 313-bp fragment of the cytochrome c oxidase subunit I (COI) for 725 samples on both MinION and Illumina platforms, and retrieved 507–584 overlapping barcodes. MinION barcodes were highly accurate (∼99.9%) when compared with Illumina reference barcodes. Molecular operational taxonomic units inferred between MinION and Illumina barcodes were consistently stable, and match ratios demonstrated highly congruent clustering patterns (≥0.96). Our method would make ARMS more accessible to researchers, and greatly expedite the processing of macrofaunal samples; it can also be easily applied to other small-to-moderate DNA barcoding projects (\u3c10,000 specimens) for rapid species identification and discovery

Seasonal variation of Sargassum ilicifolium (Phaeophyceae) growth on equatorial coral reefs

Temporal and spatial variations in Sargassum ilicifolium thallus density and length were investigated on equatorial coral reefs in Singapore from November 2011 to October 2012. Thalli density varied little throughout the year, however, we found strong seasonal patterns in thallus length and identified temperature as the significant driver. Sargassum ilicifolium reached maximum length in December (110.39 ± 2.37 cm) during periods of cooler water temperatures, and minimum length in May (9.88 ± 0.48 cm) during periods of warmer water temperatures. Significant spatial variation was also observed for both thallus density and length of S. ilicifolium among reefs. Within reefs, densities of S. ilicifolium were higher on reef flats (20.40 ± 0.40 individuals · 0.25 m−2) compared to upper reef slopes (5.66 ± 0.23 individuals · 0.25 m−2). Our findings highlight that marked seasonality in the growth of canopy-forming macroalgae can occur within equatorial reef systems where temperature ranges are restricted (\u3c3°C)

Corals in the hottest reefs in the world exhibit symbiont fidelity not flexibility

Reef-building corals are at risk of extinction from ocean warming. While some corals can enhance their thermal limits by associating with dinoflagellate photosymbionts of superior stress tolerance, the extent to which symbiont communities will reorganize under increased warming pressure remains unclear. Here we show that corals in the hottest reefs in the world in the Persian Gulf maintain associations with the same symbionts across 1.5 years despite extreme seasonal warming and acute heat stress (≥35°C). Persian Gulf corals predominantly associated with Cladocopium (clade C) and most also hosted Symbiodinium (clade A) and/or Durusdinium (clade D). This is in contrast to the neighbouring and milder Oman Sea, where corals associated with Durusdinium and only a minority hosted background levels of Cladocopium. During acute heat stress, the higher prevalence of Symbiodinium and Durusdinium in bleached versus nonbleached Persian Gulf corals indicates that genotypes of these background genera did not confer bleaching resistance. Within symbiont genera, the majority of ITS2 rDNA type profiles were unique to their respective coral species, confirming the existence of host-specific symbiont lineages. Notably, further differentiation among Persian Gulf sites demonstrates that symbiont populations are either isolated or specialized over tens to hundreds of kilometres. Thermal tolerance across coral species was associated with the prevalence of a single ITS2 intragenomic sequence variant (C3gulf), definitive of the Cladocopium thermophilum group. The abundance of C3gulf was highest in bleaching-resistant corals and at warmer sites, potentially indicating a specific symbiont genotype (or set of genotypes) that may play a role in thermal tolerance that warrants further investigation. Together, our findings indicate that co-evolution of host–Symbiodiniaceae partnerships favours fidelity rather than flexibility in extreme environments and under future warming