skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Removal of detritivore sea cucumbers from reefs increases coral disease
Abstract Coral reefs are in global decline with coral diseases playing a significant role. This is especially true for Acroporid corals that represent ~25% of all Pacific coral species and generate much of the topographic complexity supporting reef biodiversity. Coral diseases are commonly sediment-associated and could be exacerbated by overharvest of sea cucumber detritivores that clean reef sediments and may suppress microbial pathogens as they feed. Here we show, via field manipulations in both French Polynesia and Palmyra Atoll, that historically overharvested sea cucumbers strongly suppress disease among corals in contact with benthic sediments. Sea cucumber removal increased tissue mortality ofAcropora pulchraby ~370% and colony mortality by ~1500%. Additionally, farmerfish that killAcropora pulchrabases to culture their algal gardens further suppress disease by separating corals from contact with the disease-causing sediment—functioning as mutualists rather than parasites despite killing coral bases. Historic overharvesting of sea cucumbers increases coral disease and threatens the persistence of tropical reefs. Enhancing sea cucumbers may enhance reef resilience by suppressing disease.  more » « less
Award ID(s):
1947522 2224354
PAR ID:
10492577
Author(s) / Creator(s):
; ; ;
Publisher / Repository:
Nature Publishing Group
Date Published:
Journal Name:
Nature Communications
Volume:
15
Issue:
1
ISSN:
2041-1723
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Sea cucumbers have been overharvested world-wide, making assessments of their ecological effects challenging, but recent research demonstrated that sea cucumbers increase coral survival via disease suppression and were therefore important for facilitating reef health. The mechanisms underpinning the sea cucumber-coral interaction therefore are not well understood but are likely mediated through sea cucumber grazing of microbes from reef sediments. We explored how sea cucumber grazing alters the sediment microbiome by leveraging a healthy sea cucumber population on a reef in French Polynesia. We used quantitative PCR, 16S rRNA gene sequencing, and shotgun metagenomics to compare the sediment microbiome in cages placed in situ with or without sea cucumbers. We hypothesized that grazing would lower microbial biomass, change sediment microbiome composition, and deplete sediment metagenomes of anaerobic metabolisms, likely due to aeration of the sediments. Sea cucumber grazing resulted in a 75% reduction in 16S rRNA gene abundances and reshaped microbiome composition, causing a significant decrease of cyanobacteria and other phototrophs relative to ungrazed sediments. Grazing also resulted in a depletion of genes associated with cyanotoxin synthesis, suggesting a potential link to coral health. In contrast to expectations, grazed sediment metagenomes were enriched with marker genes of diverse anaerobic or microaerophilic metabolisms, including those encoding high oxygen affinity cytochrome oxidases. This enrichment differs from patterns linked to other bioturbating invertebrates. We hypothesize that grazing enriches anaerobic processes in sediment microbiomes through removal of oxygen-producing autotrophs, fecal deposition of sea cucumber gut-associated anaerobes, or modification of sediment diffusibility. These results suggest that sea cucumber harvesting influences biogeochemical processes in reef sediments, potentially mediating coral survival by altering the sediment microbiome and its production of coral-influencing metabolites. 
    more » « less
  2. As coral reefs face accelerating threats at global scales, examining how different coral species respond to local disruption from top-down and bottom-up forces can inform management at local scales. This may provide additional time for reducing global stressors. We conducted a full factorial experiment examining the effects of corallivory, herbivory, and fertilizer addition on 2 corals:Acropora pulchraandPorites rus, the former of which is faster-growing but more susceptible to predation, disease, and heat-induced mortality. Fertilizer addition enhanced corallivory but did not affect net coral growth. Consumer exclusion enhanced the net growth ofA. pulchraby 18.1 times regardless of fertilizer treatment, while the net growth ofP. rusdid not differ among caging and fertilizer treatments.A. pulchrawas rarely overgrown by algae regardless of treatment, while herbivore exclusion and fertilizer enrichment produced opposing effects on overgrowth ofP. rus. In uncaged treatments, fertilizer enrichment led to greater herbivory but also 1.8 times greater algal overgrowth ofP. rusrelative to unfertilized treatments. However, in caged treatments, algal overgrowth ofP. ruswas 1.9 times higher in unfertilized versus fertilized treatments. Our results suggest that interactions between corallivory, herbivory, and fertilizer enrichment can have alternative effects on different coral species, with a hardier coral experiencing more negative impacts of fertilizer enrichment than a more sensitive coral, which was, in turn, more strongly suppressed by predation. Local stressors that disrupt top-down and bottom-up processes may increase the vulnerability of even the most robust corals, and it is these corals that have been predicted to become more common under future ocean scenarios. 
    more » « less
  3. Reef-building corals are integral ecosystem engineers of tropical reefs but face threats from climate change. Investigating genetic, epigenetic, and environmental factors influencing their adaptation is critical. Genomic resources are essential for understanding coral biology and guiding conservation efforts. However, genomes of the coral genus Acropora are limited to highly-studied species. Here, we present the assembly and annotation of the genome and DNA methylome of Acropora pulchra from Mo’orea, French Polynesia. Using long-read PacBio HiFi and Illumina RNASeq, we generated the most complete Acropora genome to date (BUSCO completeness of 96.7% metazoan genes). The assembly size is 518 Mbp, with 174 scaffolds, and a scaffold N50 of 17 Mbp. We predicted 40,518 protein-coding genes and 16.74% of the genome in repeats. DNA methylation in the CpG context is 14.6%. This assembly of the A. pulchra genome and DNA methylome will support studies of coastal corals in French Polynesia, aiding conservation and comparative studies of Acropora and cnidarians. 
    more » « less
  4. Abstract For many long‐lived taxa, such as trees and corals, older, and larger individuals often have the lowest mortality and highest fecundity. However, climate change‐driven disturbances such as droughts and heatwaves may fundamentally alter typical size‐dependent patterns of mortality and reproduction in these important foundation taxa. Working in Moorea, French Polynesia, we investigated how a marine heatwave in 2019, one of the most intense marine heatwaves at our sites over the past 30 years, drove patterns of coral bleaching and mortality. The marine heatwave drove island‐wide mass coral bleaching that killed up to 76% and 65% of the largest individuals of the two dominant coral genera,PocilloporaandAcropora, respectively. Colonies ofPocilloporaandAcropora≥30 cm diameter were ~3.5× and ~1.3×, respectively, more likely to die than colonies <30‐cm diameter. Typically, annual mortality in these corals is concentrated on the smallest size classes. Yet, this heatwave dramatically reshaped this pattern, with heat stress disproportionately killing larger coral colonies and equalizing annual mortality rates across the size spectrum. This shift in the size‐mortality relationship reduced the overall fecundity of these genera by >60% because big corals are disproportionately important for reproduction on reefs. Additionally, the survivorship of microscopic coral recruits, critical for the recovery of corals following disturbances, declined to 2%, over an order of magnitude lower compared to a year without elevated thermal stress, where 33% of coral recruits survived. While other research has shown that larger corals can bleach more frequently than smaller corals, we show the severe impact this phenomenon can have at the reef‐wide scale. As marine heatwaves become more frequent and intense, disproportionate mortality of the largest, most fecund corals and near‐complete loss of entire cohorts of newly‐settled coral recruits will likely reduce the recovery capacity of these iconic ecosystems. 
    more » « less
  5. Abstract Reef-building corals are integral ecosystem engineers in tropical coral reefs worldwide but are increasingly threatened by climate change and rising ocean temperatures. Consequently, there is an urgency to identify genetic, epigenetic, and environmental factors, and how they interact, for species acclimatization and adaptation. The availability of genomic resources is essential for understanding the biology of these organisms and informing future research needs for management and and conservation. The highly diverse coral genusAcroporaboasts the largest number of high-quality coral genomes, but these remain limited to a few geographic regions and highly studied species. Here we present the assembly and annotation of the genome and DNA methylome ofAcropora pulchrafrom Mo’orea, French Polynesia. The genome assembly was created from a combination of long-read PacBio HiFi data, from which DNA methylation data were also called and quantified, and additional Illumina RNASeq data forab initiogene predictions. The work presented here resulted in the most completeAcroporagenome to date, with a BUSCO completeness of 96.7% metazoan genes. The assembly size is 518 Mbp, with 174 scaffolds, and a scaffold N50 of 17 Mbp. Structural and functional annotation resulted in the prediction of a total of 40,518 protein-coding genes, and 16.74% of the genome in repeats. DNA methylation in the CpG context was 14.6% and predominantly found in flanking and gene body regions (61.7%). This reference assembly of theA. pulchragenome and DNA methylome will provide the capacity for further mechanistic studies of a common coastal coral in French Polynesia of great relevance for restoration and improve our capacity for comparative genomics inAcroporaand cnidarians more broadly. 
    more » « less