Armenteros
Maickel
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Maickel
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ArticleThe coral ecosphere: a unique coral reef habitat that fosters coral-microbial interactions(Wiley, 2019-05-21) Weber, Laura ; Gonzalez‐Díaz, Patricia ; Armenteros, Maickel ; Apprill, AmyScleractinian corals are bathed in a sea of planktonic and particle‐associated microorganisms. The metabolic products of corals influence the growth and composition of microorganisms, but interactions between corals and seawater microorganisms are underexplored. We conducted a field‐based survey to compare the biomass, diversity, composition, and functional capacity of microorganisms in small‐volume seawater samples collected adjacent to five coral species with seawater collected > 1 m away from the reef substrate on the same reefs. Seawater collected close to corals generally harbored copiotrophic‐type bacteria and its bacterial and archaeal composition was influenced by coral species as well as the local reef environment. Trends in picoplankton abundances were variable and either increased or decreased away from coral colonies based on coral species and picoplankton functional group. Genes characteristic of surface‐attached and potentially virulent microbial lifestyles were enriched in near‐coral seawater compared to reef seawater. There was a prominent association between the coral Porites astreoides and the coral symbiont Endozoicomonas, suggesting recruitment and/or shedding of these cells into the surrounding seawater. This evidence extends our understanding of potential species‐specific and reef site‐influenced microbial interactions that occur between corals and microorganisms within this near‐coral seawater environment that we propose to call the “coral ecosphere.” Microbial interactions that occur within the coral ecosphere could influence recruitment of coral‐associated microorganisms and facilitate the transfer of coral metabolites into the microbial food web, thus fostering reef biogeochemical cycling and a linkage between corals and the water column.
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ArticleDiscovery and quantification of anaerobic nitrogen metabolisms among oxygenated tropical Cuban stony corals(Springer Nature, 2020-12-20) Babbin, Andrew ; Tamasi, Tyler ; Dumit, Diana ; Weber, Laura ; Rodríguez, María Victoria Iglesias ; Schwartz, Sarah L. ; Armenteros, Maickel ; Wankel, Scott D. ; Apprill, AmyCoral reef health depends on an intricate relationship among the coral animal, photosynthetic algae, and a complex microbial community. The holobiont can impact the nutrient balance of their hosts amid an otherwise oligotrophic environment, including by cycling physiologically important nitrogen compounds. Here we use 15N-tracer experiments to produce the first simultaneous measurements of ammonium oxidation, nitrate reduction, and nitrous oxide (N2O) production among five iconic species of reef-building corals (Acropora palmata, Diploria labyrinthiformis, Orbicella faveolata, Porites astreoides, and Porites porites) in the highly protected Jardines de la Reina reefs of Cuba. Nitrate reduction is present in most species, but ammonium oxidation is low potentially due to photoinhibition and assimilatory competition. Coral-associated rates of N2O production indicate a widespread potential for denitrification, especially among D. labyrinthiformis, at rates of ~1 nmol cm−2 d−1. In contrast, A. palmata displays minimal active nitrogen metabolism. Enhanced rates of nitrate reduction and N2O production are observed coincident with dark net respiration periods. Genomes of bacterial cultures isolated from multiple coral species confirm that microorganisms with the ability to respire nitrate anaerobically to either dinitrogen gas or ammonium exist within the holobiont. This confirmation of anaerobic nitrogen metabolisms by coral-associated microorganisms sheds new light on coral and reef productivity.
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ArticleMicrobial signatures of protected and impacted Northern Caribbean reefs: changes from Cuba to the Florida Keys.(Wiley, 2019-11-19) Weber, Laura ; Gonzalez‐Díaz, Patricia ; Armenteros, Maickel ; Ferrer, Víctor M. ; Bretos, Fernando ; Bartels, Erich ; Santoro, Alyson E. ; Apprill, AmyThere are a few baseline reef‐systems available for understanding the microbiology of healthy coral reefs and their surrounding seawater. Here, we examined the seawater microbial ecology of 25 Northern Caribbean reefs varying in human impact and protection in Cuba and the Florida Keys, USA, by measuring nutrient concentrations, microbial abundances, and respiration rates as well as sequencing bacterial and archaeal amplicons and community functional genes. Overall, seawater microbial composition and biogeochemistry were influenced by reef location and hydrogeography. Seawater from the highly protected ‘crown jewel’ offshore reefs in Jardines de la Reina, Cuba had low concentrations of nutrients and organic carbon, abundant Prochlorococcus, and high microbial community alpha diversity. Seawater from the less protected system of Los Canarreos, Cuba had elevated microbial community beta‐diversity whereas waters from the most impacted nearshore reefs in the Florida Keys contained high organic carbon and nitrogen concentrations and potential microbial functions characteristic of microbialized reefs. Each reef system had distinct microbial signatures and within this context, we propose that the protection and offshore nature of Jardines de la Reina may preserve the oligotrophic paradigm and the metabolic dependence of the community on primary production by picocyanobacteria.
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ArticleCoral reef fish assemblages exhibit signs of depletion in two protected areas from the eastern of Los Canarreos archipelago (Cuba, Caribbean Sea)(PeerJ, 2022-10-04) Navarro-Martínez, Zenaida María ; Armenteros, Maickel ; Espinosa, Leonardo ; González-Díaz, Patricia ; Apprill, AmyUnderstanding the impact of marine protected areas on the distribution and composition of fishes is key to the protection and management of coral reef ecosystems, and especially for fish-based activities such as SCUBA diving and recreational fishing. The aim of this research is to compare the ichthyofauna structure in three areas in the eastern part of Los Canarreos archipelago in Cuba with different management schemes: Cayo Campos-Cayo Rosario Fauna Refuge (CCCR), Cayo Largo Ecological Reserve (CL) and non-protected area (nMPA), and considering habitat differences and depth variation. A total of 131 video transects were conducted using diver operated stereo-video (stereo-DOV) in November, 2015 in backreef and forereef along the CCCR, CL and the adjacent nMPA. We recorded 84 species and 27 functional groups suggesting high complementarity of functions. Several multispecies schools were observed along surveys, which explain the biomass peaks in some sites, mainly for Lutjanidae, Haemulidae and Carangidae. A concerning issue was the bare representation of critical functional groups and threatened species. The effect of sites nested within habitats was significant and the most important driver structuring fish assemblages, while MPA condition was not evident. Favorable habitat features (habitat heterogeneity and surrounding coastal ecosystems) are likely enhancing fish assemblages and counteracting the effects of pouching derived from insufficient management. We recommend immediate actions within a strategy of precautionary management including, but not limited to, the appointment of staff for the administration of CL, frequent monitoring and effective enforcement.
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ArticleExtracellular reef metabolites across the protected Jardines de la Reina, Cuba Reef System(Frontiers Media, 2020-12-14) Weber, Laura ; Armenteros, Maickel ; Kido Soule, Melissa C. ; Longnecker, Krista ; Kujawinski, Elizabeth B. ; Apprill, AmyCoral reef ecosystems are incredibly diverse marine biomes that rely on nutrient cycling by microorganisms to sustain high productivity in generally oligotrophic regions of the ocean. Understanding the composition of extracellular reef metabolites in seawater, the small organic molecules that serve as the currency for microorganisms, may provide insight into benthic-pelagic coupling as well as the complexity of nutrient cycling in coral reef ecosystems. Jardines de la Reina (JR), Cuba is an ideal environment to examine extracellular metabolites across protected and high-quality reefs. Here, we used liquid chromatography mass spectrometry (LC-MS) to quantify specific known metabolites of interest (targeted metabolomics approach) and to survey trends in metabolite feature composition (untargeted metabolomics approach) from surface and reef depth (6 – 14 m) seawater overlying nine forereef sites in JR. We found that untargeted metabolite feature composition was surprisingly similar between reef depth and surface seawater, corresponding with other biogeochemical and physicochemical measurements and suggesting that environmental conditions were largely homogenous across forereefs within JR. Additionally, we quantified 32 of 53 detected metabolites using the targeted approach, including amino acids, nucleosides, vitamins, and other metabolic intermediates. Two of the quantified metabolites, riboflavin and xanthosine, displayed interesting trends by depth. Riboflavin concentrations were higher in reef depth compared to surface seawater, suggesting that riboflavin may be produced by reef organisms at depth and degraded in the surface through photochemical oxidation. Xanthosine concentrations were significantly higher in surface reef seawater. 5′-methylthioadenosine (MTA) concentrations increased significantly within the central region of the archipelago, displaying biogeographic patterns that warrant further investigation. Here we lay the groundwork for future investigations of variations in metabolite composition across reefs, sources and sinks of reef metabolites, and changes in metabolites over environmental, temporal, and reef health gradients.
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ArticleSmall-scale variability dominates benthic coverage and diversity across the Jardines de la Reina, Cuba coral reef system(Frontiers Media, 2019-11-29) Hernández-Fernández, Leslie ; González de Zayas, Roberto ; Weber, Laura ; Apprill, Amy ; Armenteros, MaickelCoral reefs are complex and biodiverse ecosystems that are undergoing significant change. Understanding reef composition and biodiversity at multiple spatial scales is necessary to track both large-scale and more subtle ecosystem changes. The Jardines de la Reina (JR) archipelago, located offshore of the island of Cuba, contains the largest marine protected area (MPA) in the Caribbean Sea but lacks multi-scale studies. In this contribution, we documented the diversity of scleractinian corals, octocorals, algae, and sponges across nested spatial scales spanning four orders of magnitude (101–105 m). In addition, we tested the hypothesis that species diversity followed a gradient along the ca. 200 km of reef tract. Across the archipelago, we examined benthic cover and species diversity within 255 photo-quadrats (25 × 25 cm) at 13 fore reef sites (two sampling locations per site, and 10 photo-quadrats per location). Small-scale (101 m) variability between photo-quadrats characterized the coral reef community structure in JR compared with local- (102 m) and mesoscale (104–105 m) variability. This finding suggests that biological processes (e.g., recruitment, competition) had primacy over hydrodynamics for driving the differences in reef community composition. However, the dominance of algae and low cover and diversity of scleractinian corals suggests the pervasive effects of global change on coral communities despite potential benefits provided by the MPA (e.g., oligotrophy and abundance of herbivores). There was no gradient of benthic community structure along the fore reef tract of JR; instead, a patchy distribution occurred in response to more subtle drivers acting at local scales. Overall, our multi-scale comparison was useful for differentiating the impacts of processes potentially impacting the JR reefs, thus providing important information to understand how reef communities are impacted by different environmental and anthropogenic stressors, and the potential benefits of MPAs.
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ArticleDiversity of cryptofaunal nematode assemblages along the Jardines de La Reina Coral Reef, Southern Cuba(MDPI, 2024-04-29) Marzo-Perez, Diana ; Perez-Garcia, Jose Andres ; Apprill, Amy ; Armenteros, MaickelCryptofaunal nematodes, those living on the hard substrate of the coral reefs, are largely unknown in terms of diversity and assemblage structure. We described nematode assemblages at seven sites spanning about 200 km along Jardines de La Reina, a well-preserved reef system in the Greater Antilles. We identified about 3000 nematodes, mostly of the families Desmodoridae and Chromadoridae; the most abundant species were Croconema cinctum, Desmodora communis, and Euchromadora vulgaris. The regional richness was moderate with 70 observed species (0.95 confidence interval: 65–75 species) and 75 extrapolated species (0.95 CI: 68–83 species). This richness was lower than in other reef biotopes, maybe reflecting evolutionary constraints due to interactions with stony corals. The local expected richness at 100 individuals was similar among sites, with a median of 26 species (0.95 CI: 20–34 species), and likely caused by diversification rate and evolutionary time acting at the same pace on populations. The taxonomic β-diversity was high and without differences among sites (median: 0.85; 0.95 CI: 0.33–1), probably due to significant substrate heterogeneity at 10-cm scale. The prevalence of replacement over richness difference suggests that local processes (e.g., environmental filtering and competition) contribute more to β-diversity than niche availability, which would be largely similar across the reef terraces. Contrary to our expectations, no gradient of assemblage structure occurred, nor significant effect of benthic cover on nematodes. However, nematode functional structure showed a conservative set of biological traits reflecting adaptations to hydrodynamic regime: armed oral cavity/intermediate colonizing capability/ornamented cuticles/conical tail. Our results provide insights about the taxonomic and functional diversity of nematodes and highlight the vast knowledge gaps about the processes ruling the meiofauna community structure in coral reefs.