skip to main content


Title: Three competitors in three dimensions: photogrammetry reveals rapid overgrowth of coral during multispecies competition with sponges and algae
Competition for limited space is an important driver of benthic community structure on coral reefs. Studies of coral-algae and coral-sponge interactions often show competitive dominance of algae and sponges over corals, but little is known about the outcomes when these groups compete in a multispecies context. Multispecies competition is increasingly common on Caribbean coral reefs as environmental degradation drives loss of reef-building corals and proliferation of alternative organisms such as algae and sponges. New methods are needed to understand multispecies competition, whose outcomes can differ widely from pairwise competition and range from coexistence to exclusion. In this study, we used 3D photogrammetry and image analyses to compare pairwise and multispecies competition on reefs in the US Virgin Islands. Sponges ( Desmapsamma anchorata, Aplysina cauliformis ) and macroalgae ( Lobophora variegata ) were attached to coral ( Porites astreoides ) and arranged to simulate multispecies (coral-sponge-algae) and pairwise (coral-sponge, coral-algae) competition. Photogrammetric 3D models were produced to measure surface area change of coral and sponges, and photographs were analyzed to measure sponge-coral, algae-coral, and algae-sponge overgrowth. Coral lost more surface area and was overgrown more rapidly by the sponge D. anchorata in multispecies treatments, when the sponge was also in contact with algae. Algae contact may confer a competitive advantage to the sponge D. anchorata, but not to A. cauliformis , underscoring the species-specificity of these interactions. This first application of photogrammetry to study competition showed meaningful losses of living coral that, combined with significant overgrowths by competitors detected from image analyses, exposed a novel outcome of multispecies competition.  more » « less
Award ID(s):
1946412
NSF-PAR ID:
10231960
Author(s) / Creator(s):
; ; ;
Date Published:
Journal Name:
Marine Ecology Progress Series
Volume:
657
ISSN:
0171-8630
Page Range / eLocation ID:
109 to 121
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Reef-building corals are ecosystem engineers that compete with other benthic organisms for space and resources. Corals harvest energy through their surface by photosynthesis and heterotrophic feeding, and they divert part of this energy to defend their outer colony perimeter against competitors. Here, we hypothesized that corals with a larger space-filling surface and smaller perimeters increase energy gain while reducing the exposure to competitors. This predicted an association between these two geometric properties of corals and the competitive outcome against other benthic organisms. To test the prediction, fifty coral colonies from the Caribbean island of Curaçao were rendered using digital 3D and 2D reconstructions. The surface areas, perimeters, box-counting dimensions (as a proxy of surface and perimeter space-filling), and other geometric properties were extracted and analyzed with respect to the percentage of the perimeter losing or winning against competitors based on the coral tissue apparent growth or damage. The increase in surface space-filling dimension was the only significant single indicator of coral winning outcomes, but the combination of surface space-filling dimension with perimeter length increased the statistical prediction of coral competition outcomes. Corals with larger surface space-filling dimensions (Ds> 2) and smaller perimeters displayed more winning outcomes, confirming the initial hypothesis. We propose that the space-filling property of coral surfaces complemented with other proxies of coral competitiveness, such as life history traits, will provide a more accurate quantitative characterization of coral competition outcomes on coral reefs. This framework also applies to other organisms or ecological systems that rely on complex surfaces to obtain energy for competition.

     
    more » « less
  2. Abstract

    Sponges are increasingly recognized as an ecologically important taxon on coral reefs, representing significant biomass and biodiversity where sponges have replaced scleractinian corals. Most sponge species can be divided into two symbiotic states based on symbiont community structure and abundance (i.e., the microbiome), and are characterized as high microbial abundance (HMA) or low microbial abundance (LMA) sponges. Across the Caribbean, sponge species of the HMA or LMA symbiotic states differ in metabolic capacity, as well as their trophic ecology. A metagenetic analysis of symbiont 16 S rRNA and metagenomes showed that HMA sponge microbiomes are more functionally diverse than LMA microbiomes, offer greater metabolic functional capacity and redundancy, and encode for the biosynthesis of secondary metabolites. Stable isotope analyses showed that HMA and LMA sponges primarily consume dissolved organic matter (DOM) derived from external autotrophic sources, or live particulate organic matter (POM) in the form of bacterioplankton, respectively, resulting in a low degree of resource competition between these symbiont states. As many coral reefs have undergone phase shifts from coral- to macroalgal-dominated reefs, the role of DOM, and the potential for future declines in POM due to decreased picoplankton productivity, may result in an increased abundance of chemically defended HMA sponges on tropical coral reefs.

     
    more » « less
  3. Abstract from the article associated with the dataset: George, Mullinix, et al PeerJ 2021. Reef-building corals are ecosystem engineers that compete with other benthic or- ganisms for space and resources. Corals harvest energy through their surface by photosynthesis and heterotrophic feeding, and they divert part of this energy to defend their outer colony perimeter against competitors. Here, we hypothesized that corals with a larger space-filling surface and smaller perimeters increase energy gain while reducing the exposure to competitors. This predicted an association between these two geometric properties of corals and the competitive outcome against other benthic organisms. To test the prediction, fifty coral colonies from the Caribbean island of Curac ̧ao were rendered using digital 3D and 2D reconstructions. The surface areas, perimeters, box-counting dimensions (as a proxy of space-filling property), and other geometric properties were extracted and analyzed with respect to the percentage of the perimeter losing or winning against competitors based on the coral tissue apparent growth or damage. The increase in surface space-filling dimension was the only significant single indicator of coral winning outcomes, but the combination of surface space-filling dimension with perimeter length increased the statistical prediction of coral competition outcomes. Corals with larger surface space-filling dimensions (Ds > 2) and smaller perimeters displayed more winning outcomes, confirming the initial hypothesis. We propose that the space-filling property of coral surfaces complemented with other proxies of coral competitiveness, such as life history traits, will provide a more accurate quantitative characterization of coral competition outcomes on coral reefs. This framework also applies to other organisms or ecological systems that rely on complex surfaces to obtain energy for competition. For the compressed files: - Reconstruction of the split file can be accomplished by issuing the command cat *.tar.bz2*part-a* > 3D_model_stl_data.tar.bz2 - Unzipping the compressed files can be accomplished by issuing the command tar -jxvf *.tar.bz2 
    more » « less
  4. 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
  5. ABSTRACT

    Aplysina cauliformis, the Caribbean purple rope sponge, is commonly affected by Aplysina Red Band Syndrome (ARBS). This transmissible disease manifests as circular lesions with red margins and results in bare spongin fibers. Leptolyngbya spp. appear to be responsible for the characteristic red coloration but transmission studies with a sponge-derived isolate failed to establish disease, leaving the etiology of ARBS unknown. To investigate the cause of ARBS, contact transmission experiments were performed between healthy and diseased sponges separated by filters with varying pore sizes. Transmission occurred when sponges were separated by filters with pore sizes ≥ 2.5 μm, suggesting a prokaryotic pathogen(s) but not completely eliminating eukaryotic pathogen(s). Using 16S rRNA gene sequencing methods, 38 prokaryotic taxa were significantly enriched in diseased sponges, including Leptolyngbya, whereas seven taxa were only found in some, but not all, of the ARBS-affected sponges. These results do not implicate a single taxon, but rather a suite of taxa that changed in relative abundance with disease, suggesting a polymicrobial etiology as well as dysbiosis. As a better understanding of dysbiosis is gained, changes in the composition of associated prokaryotic communities may have increasing importance for evaluating and maintaining the health of individuals and imperiled coral reef ecosystems.

     
    more » « less