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Nat Commun
2024 Feb 26;151:1338. doi: 10.1038/s41467-024-45730-0.
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Removal of detritivore sea cucumbers from reefs increases coral disease.
Clements CS
,
Pratte ZA
,
Stewart FJ
,
Hay ME
.
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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 of Acropora pulchra by ~370% and colony mortality by ~1500%. Additionally, farmerfish that kill Acropora pulchra bases 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.
Fig. 1. Effects of sea cucumber removal on coral tissue death and mortality.a Aerial view of a sand patch in the field with feeding sea cucumbers (Holothuria atra, pink circles denote example individuals) and a thicket of Acropora pulchra coral (bottom left). b A typical sand patch in the field, with H. atra and A. pulchra coral with turf algae at the base of the coral thicket. c
A. pulchra percent tissue death (mean ± SE) with an inset picture of an A. pulchra outplant experiencing the typical pattern of tissue mortality from the base up. Total numbers of coral outplants assessed per treatment are indicated below each violin plot (n = 10 sand patches, each holding 5 coral outplants for a total of 50 outplants per treatment). P value derived from a one-way, permutation-based linear mixed-effects (LME) model. d
A. pulchra probability of survival through time as a function of sea cucumber presence or removal. Ratio of surviving coral outplants at 45 days to total number of outplants are indicated to the right of survival curves (n = 10 sand patches, each holding 5 coral outplants for a total of 50 outplants per treatment). Survival curves and p value derived from two-tailed, random-effects Weibull regression. e
Acropora nasuta percent tissue death (mean ± SE) as a function of sea cucumber (Stichopus chloronotus) presence or absence and outplant contact with sediment. Total numbers of coral outplants assessed per treatment are indicated below each violin plot (n = 15 outplants per treatment). P values derived from a two-way, permutation-based linear mixed-effects (LME) model. Letters indicate significant groupings via a post hoc permutation test for multiple comparisons. The inset image is of an A. nasuta colony exhibiting partial mortality where in contact with the sediment. Source data are provided as a Source Data file.
Fig. 2. Acropora pulchra percent tissue death (mean ± SE) as a function of presence or absence of sea cucumbers and coral outplant type.Outplants with no turf and buried turf were planted in such a way that living coral tissue directly contacted the sediment, while turf samples reflect living coral tissue that was separated from the sediment by farmerfish turf algae on the base of the outplant. Total numbers of corals assessed per treatment are indicated below each violin plot. P values derived from a two-way, permutation-based linear mixed-effects (LME) model (n = 15 per treatment). Letters indicate significant groupings via a post hoc permutation test for multiple comparisons. Source data are provided as a Source Data file.
Fig. 3. Effects of coral (Acropora pulchra) outplant type, sea cucumber (Holothuria atra) density, and basal versus distal samples on coral and sediment microbiomes.a PCoA (Bray-Curtis dissimilarity index) and one-way PERMANOVA analysis of microbiome composition (beta diversity) of basal coral samples as a function of outplant type. Outplants with no turf and buried turf were planted so that living coral tissue directly contacted the sediment, while turf treatments had coral tissue separated from the sediment by basal turf algae. Letters within legend indicate significant groupings via a post hoc permutation test for multiple comparisons. Total numbers of samples assessed per treatment are indicated to the right of the letter report. b PCoA (Bray-Curtis dissimilarity index) and one-way PERMANOVA analysis of microbiome composition (beta diversity) of basal and distal samples from coral outplants within experimental enclosures. Basal samples derived from living tissue immediately adjacent to dead or dying tissue at the outplant’s base and distal samples from living tissue ~1 cm from the branch tip of the outplant. The total numbers of samples assessed per treatment are indicated within the legend. c, d PCoA (Bray-Curtis dissimilarity index) and one-way PERMANOVA analysis of microbiome composition (beta diversity) from surficial sediment within cages containing two, one, or zero sea cucumbers after c seven days of sea cucumber feeding and d immediately prior to sampling corals within cages (ranging from 7 to 36 days of coral exposure). Letters within legends indicate significant groupings via post hoc permutation tests for multiple comparisons. Total numbers of samples assessed per treatment are indicated to the right of the letter reports. Source data are provided as a Source Data file.
