skip to main content


This content will become publicly available on March 5, 2025

Title: Severe hurricanes increase recruitment and gene flow in the clonal sponge Aplysina cauliformis
Abstract

Upright branching sponges, such asAplysina cauliformis, provide critical three‐dimensional habitat for other organisms and assist in stabilizing coral reef substrata, but are highly susceptible to breakage during storms. Breakage can increase sponge fragmentation, contributing to population clonality and inbreeding. Conversely, storms could provide opportunities for new genotypes to enter populations via larval recruitment, resulting in greater genetic diversity in locations with frequent storms. The unprecedented occurrence of two Category 5 hurricanes in close succession during 2017 in the U.S. Virgin Islands (USVI) provided a unique opportunity to evaluate whether recolonization of newly available substrata on coral reefs was due to local (e.g. re‐growth of remnants, fragmentation, larval recruitment) or remote (e.g. larval transport and immigration) sponge genotypes. We sampledA. cauliformisadults and juveniles from four reefs around St. Thomas and two in St. Croix (USVI). Using a 2bRAD protocol, all samples were genotyped for single‐nucleotide polymorphisms (SNPs). Results showed that these major storm events favoured sponge larval recruitment but did not increase the genetic diversity ofA. cauliformispopulations. Recolonization of substratum post‐storms via clonality was lower (15%) than expected and instead was mainly due to sexual reproduction (85%) via local larval recruitment. Storms did enhance gene flow among and within reef sites located south of St. Thomas and north of St. Croix. Therefore, populations of clonal marine species with low pelagic dispersion, such asA. cauliformis, may benefit from increased frequency and magnitude of hurricanes for the maintenance of genetic diversity and to combat inbreeding, enhancing the resilience of Caribbean sponge communities to extreme storm events.

 
more » « less
NSF-PAR ID:
10494375
Author(s) / Creator(s):
 ;  ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Molecular Ecology
Volume:
33
Issue:
7
ISSN:
0962-1083
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Stony coral tissue loss disease (SCTLD) was first observed in St. Thomas, U.S. Virgin Islands (USVI) in January 2019. This disease affects at least 20 scleractinian coral species; however, it is not well understood how reef diversity affects its spread or its impacts on reef ecosystems. With a large number of susceptible species, SCTLD may not follow the diversity-disease hypothesis, which proposes that high species diversity is negatively correlated with disease prevalence. Instead, SCTLD may have a higher prevalence and a greater impact on reefs with higher coral diversity. To test this, in 2020 we resampled 54 sites around St. Thomas previously surveyed in 2017 or 2019 by the National Oceanic and Atmospheric Administration National Coral Reef Monitoring Program. These sites represented a variety of species diversity values [categorized into poor (<12 spp. rich.) and rich (12 spp. rich.)] in multiple disease zones (Endemic: disease present  9 months; Epidemic: disease present 2–6 months; Control and Emergent: disease present no disease/<2 months). We hypothesized that, contrary to the diversity-disease hypothesis, sites with high species diversity (as measured by species richness or Simpson’s index) would have higher disease prevalence within the epidemic zone, and that high species diversity sites would have a greater impact from disease within the endemic zone. Results indicated a significant positive relationship between disease prevalence and diversity in the epidemic zone, and a similar trend in the endemic zones. Additionally, a negative relationship was seen between pre-outbreak diversity and loss of diversity and coral cover within the endemic zone. This supports the hypothesis that higher diversity predicts greater disease impact and suggests that SCTLD does not follow the diversity-disease hypothesis. Within the epidemic zone, the species with the highest SCTLD prevalence were Dendrogyra cylindrus, Colpophyllia natans, and Meandrina meandrites, while in the endemic zone, Diploria labyrinthiformis, Pseudodiploria strigosa, Montastraea cavernosa, and Siderastrea siderea had the highest SCTLD prevalence. Understanding the relationship between species diversity and SCTLD will help managers predict the most vulnerable reefs, which should be prioritized within the USVI and greater Caribbean region. 
    more » « less
  2. Abstract

    Sponges are a diverse phylum of sessile filter‐feeding invertebrates that are abundant on Caribbean reefs and provide essential ecological services, including nutrient cycling, reef stabilization, habitat, and food for a variety of fishes and invertebrates. As prominent members of the benthic community, and thus potential food resources, factors determining the biochemical and energetic content of sponges will affect their trophic contributions to coral reef ecosystems. In order to evaluate the influence of geographic variation on biochemical composition and energetic content in the tissue of sponges, we collected several common and widespread species (Agelas conifera,Agelas tubulata,Amphimedon compressa,Aplysina cauliformis,Niphates amorpha,Niphates erecta, andXestospongia muta) from multiple shallow reefs in four countries across the Caribbean Basin, including Belize, Curaçao, Grand Cayman, and St. Croix, U.S. Virgin Islands. In addition, we correlated inherent species‐level traits, including the production of antipredator chemical defenses and the relative abundance of microbial symbionts, with biochemical and energetic content. We found that energetic content was higher in sponges with antipredator chemical defenses, and was significantly correlated with the concentration of chemical extracts from these sponges. We also noted that sponges with high microbial abundance contained significantly more soluble protein than sponges with low microbial abundance. Finally, both biochemical and energetic content varied significantly among sponges from different locations; sponges from Grand Cayman had the highest lipid and energetic content, whereas sponges from Belize had the highest carbohydrate content but lowest energetic content. Despite similar environmental conditions at these sites, our results demonstrate that biochemical and energetic content of sponges exhibits geographic variability, with potential implications for the trophic ecology of sponges throughout the Caribbean Basin.

     
    more » « less
  3. Abstract

    On most tropical coral reefs, decades of disturbances have ratcheted down coral cover to create low abundance communities. In such a state, the reefs of St. John,USVirgin Islands, were hit by two Category 5 hurricanes in September 2017, yet the effects on two sites dominated byOrbicella annulariswere minor in terms of coral cover. To explore the implications of this outcome, the fates ofO. annulariscolonies were determined from photoquadrats and used to prepare size‐based matrix models for the year preceding the storms and the four months bracketing the storms. The populations displayed contrasting dynamics from 1988 to July 2017, with coral cover declining from 43% to 5% at Yawzi Point but remaining at ~30% at Tektite. Over this period, colony sizes declined, with ≥82% having planar areas ≤50 cm2(i.e., the smallest size class) by July 2017, and while densities declined from 47 to 8 colonies/m2at Yawzi Point, they increased from 36 to 51 colonies/m2at Tektite. Hurricanes Irma and Maria depressed coral cover by 1–4%, transitioned colonies into the smallest size class (>87% by November), killed 27% and 5% of the colonies in the smallest size class at Yawzi Point and Tektite, respectively, and depressed the 5‐yr intrinsic rate of population growth (λ) to 0.53–0.87. Twenty‐year projections suggested these demographic effects will not have ecologically meaningful impacts on population size, at least compared to projections initiated assuming Hurricanes Irma and Maria had not occurred. With low cover ofO. annularisdistributed among many small colonies, future disturbances may play more important roles in winnowing the few remaining host genotypes rather than further depressing coral cover.

     
    more » « less
  4. Abstract

    Major tropical storms are destructive phenomena with large effects on the community dynamics of multiple biomes. On coral reefs, their impacts have been described for decades, leading to the expectation that future storms should have effects similar to those recorded in the past. This expectation relies on the assumption that storm intensities will remain unchanged, and the impacted coral reef communities are similar to those of the recent past; neither assumption is correct. This study quantified the effects of two category five hurricanes on the reefs of St. John,U.S.Virgin Islands, where 31 yr of time‐series analyses reveal chronic coral mortality, increasing macroalgal abundance, and five major hurricanes that caused acute coral mortality. Contextualized by these trends, the effects of the most recent storms, Hurricanes Irma and Maria (September 2017), on coral cover were modest. While mean absolute coral cover declined 1–4% depending on site, these effects were not statistically discernable. Following decades of increasing abundance of macroalgae, this functional group responded to the recent hurricanes with large increases in abundance on both absolute and relative scales. Decades of chronic mortality have changed the coral assemblages of St. John to create degraded communities that are resistant to severe storms.

     
    more » « less
  5. null (Ed.)
    Stony coral tissue loss disease (SCTLD) was initially documented in Florida in 2014 and outbreaks with similar characteristics have since appeared in disparate areas throughout the northern Caribbean, causing significant declines in coral communities. SCTLD is characterized by focal or multifocal lesions of denuded skeleton caused by rapid tissue loss and affects at least 22 reef-building species of Caribbean corals. A tissue-loss disease consistent with the case definition of SCTLD was first observed in the U.S. Virgin Islands (USVI) in January of 2019 off the south shore of St. Thomas at Flat Cay. The objective of the present study was to characterize species susceptibility to the disease present in St. Thomas in a controlled laboratory transmission experiment. Fragments of six species of corals ( Colpophyllia natans , Montastraea cavernosa , Orbicella annularis , Porites astreoides , Pseudodiploria strigosa , and Siderastrea siderea ) were simultaneously incubated with (but did not physically contact) SCTLD-affected colonies of Diploria labyrinthiformis and monitored for lesion appearance over an 8 day experimental period. Paired fragments from each corresponding coral genotype were equivalently exposed to apparently healthy colonies of D. labyrinthiformis to serve as controls; none of these fragments developed lesions throughout the experiment. When tissue-loss lesions appeared and progressed in a disease treatment, the affected coral fragment, and its corresponding control genet, were removed and preserved for future analysis. Based on measures including disease prevalence and incidence, relative risk of lesion development, and lesion progression rates, O. annularis, C. natans , and S. siderea showed the greatest susceptibility to SCTLD in the USVI. These species exhibited earlier average development of lesions, higher relative risk of lesion development, greater lesion prevalence, and faster lesion progression rates compared with the other species, some of which are considered to be more susceptible based on field observations (e.g., P. strigosa ). The average transmission rate in the present study was comparable to tank studies in Florida, even though disease donor species differed. Our findings suggest that the tissue loss disease affecting reefs of the USVI has a similar epizootiology to that observed in other regions, particularly Florida. 
    more » « less