Interplay of management and environmental drivers shifts size structure of reef fish communities.

Countries are expanding marine protected area (MPA) networks to mitigate fisheries declines and support marine biodiversity. However, MPA impact evaluations typically assess total fish biomass. Here, we examine how fish biomass disaggregated by adult and juvenile life stages responds to environmental drivers, including sea surface temperature (SST) anomalies and human footprint, and multiple management types at 139 reef sites in the Mesoamerican Reef (MAR) region. We found that total fish biomass generally appears stable across the region from 2006 to 2018, with limited rebuilding of fish stocks in MPAs. However, the metric of total fish biomass masked changes in fish community structure, with lower adult than juvenile fish biomass at northern sites, and adult:juvenile ratios closer to 1:1 at southern sites. These shifts were associated with different responses of juvenile and adult fish to environmental drivers and management. Juvenile fish biomass increased at sites with high larval connectivity and coral cover, whereas adult fish biomass decreased at sites with greater human footprint and SST anomalies. Adult fish biomass decreased primarily in Honduran general use zones, which suggests insufficient protection for adult fish in the southern MAR. There was a north-south gradient in management and environmental drivers, with lower coverage of fully protected areas and higher SST anomalies and coastal development in the south that together may undermine the maintenance of adult fish biomass in the southern MAR. Accounting for the interplay between environmental drivers and management in the design of MPAs is critical for increasing fish biomass across life history stages.

Los países están ampliando las redes de áreas marinas protegidas (AMP) para mitigar la disminución de las pesquerías y apoyar la biodiversidad marina. Sin embargo, las evaluaciones de impacto de las AMP típicamente estudian la biomasa total de peces. Aquí, examinamos cómo la biomasa de peces desagregada por etapas de vida adultas y juveniles responde a factores ambientales como anomalías de la temperatura superficial del mar (SST) e impacto humano, y múltiples tipos de manejo en 139 sitios de arrecifes en el sistema arrecifal mesoamericano (SAM). Encontramos que la biomasa total de peces en general parece estable en toda la región entre 2006 y 2018, con una recuperación limitada de las poblaciones de peces en las AMP. Sin embargo, la métrica de biomasa total de peces enmascaró los cambios en la estructura de la comunidad de peces, con una biomasa de peces adultos más baja que juveniles en los sitios del norte, y proporciones adulto:juvenil más cercana a 1:1 en los sitios del sur. Estos cambios fueron asociados con diferentes respuestas de peces juveniles y adultos a variables ambientales y de manejo. La biomasa de peces juveniles aumentó en sitios con alta conectividad larvaria y cobertura coralina, mientras que la biomasa de peces adultos disminuyó en sitios con mayor impacto humano y anomalías en la SST. La biomasa de peces adultos disminuyó principalmente en las zonas de uso general (GUZ) hondureñas, lo cual sugiere una protección insuficiente para peces adultos en el sur del SAM. Hubo un gradiente norte­sur en el manejo y los factores ambientales, con menor cobertura de áreas totalmente protegidas y mayores anomalías de SST y desarrollo costero en el sur. En conjunto esto puede degradar el mantenimiento de la biomasa de peces adultos en el sur del SAM. La interacción entre factores ambientales y el manejo en el diseño de las AMP es fundamental para aumentar la biomasa de peces en todas las etapas del ciclo de vida.

Stony coral tissue loss disease induces transcriptional signatures of in situ degradation of dysfunctional Symbiodiniaceae.

Stony coral tissue loss disease (SCTLD), one of the most pervasive and virulent coral diseases on record, affects over 22 species of reef-building coral and is decimating reefs throughout the Caribbean. To understand how different coral species and their algal symbionts (family Symbiodiniaceae) respond to this disease, we examine the gene expression profiles of colonies of five species of coral from a SCTLD transmission experiment. The included species vary in their purported susceptibilities to SCTLD, and we use this to inform gene expression analyses of both the coral animal and their Symbiodiniaceae. We identify orthologous coral genes exhibiting lineage-specific differences in expression that correlate to disease susceptibility, as well as genes that are differentially expressed in all coral species in response to SCTLD infection. We find that SCTLD infection induces increased expression of rab7, an established marker of in situ degradation of dysfunctional Symbiodiniaceae, in all coral species accompanied by genus-level shifts in Symbiodiniaceae photosystem and metabolism gene expression. Overall, our results indicate that SCTLD infection induces symbiophagy across coral species and that the severity of disease is influenced by Symbiodiniaceae identity.

Transmission of stony coral tissue loss disease (SCTLD) in simulated ballast water confirms the potential for ship-born spread.

Stony coral tissue loss disease (SCTLD) remains an unprecedented epizootic disease, representing a substantial threat to the persistence and health of coral reef ecosystems in the Tropical Western Atlantic since its first observation near Miami, Florida in 2014. In addition to transport between adjacent reefs indicative of waterborne pathogen(s) dispersing on ocean currents, it has spread throughout the Caribbean to geographically- and oceanographically-isolated reefs, in a manner suggestive of ship and ballast water transmission. Here we evaluate the potential for waterborne transmission of SCTLD including via simulated ballast water, and test the efficacy of commonly-used UV radiation treatment of ballast water. Two species of reef-building corals (Orbicella faveolata and Pseudodiploria strigosa) were subjected to (1) disease-exposed or UV-treated disease-exposed water, and (2) a ballast hold time series of disease-exposed water in two carefully-controlled experiments to evaluate transmission. Our experiments demonstrated transmission of SCTLD through water, rather than direct contact between diseased and healthy corals. While UV treatment of disease-exposed water led to a 50% reduction in the number of corals exhibiting disease signs in both species, the statistical risk of transmission and volume of water needed to elicit SCTLD lesions remained similar to untreated disease-exposed water. The ballast hold time (24 h vs. 120 h) did not have a significant effect on the onset of visible disease signs for either species, though there appeared to be some evidence of a concentration effect for P. strigosa as lesions were only observed after the 120 h ballast hold time. Results from both experiments suggest that the SCTLD pathogens can persist in both untreated and UV-treated ballast water and remain pathogenic. Ballast water may indeed pose a threat to the continued spread and persistence of SCTLD, warranting further investigation of additional ballast water treatments and pathogen detection methods.

Experimental transmission of Stony Coral Tissue Loss Disease results in differential microbial responses within coral mucus and tissue.

Stony coral tissue loss disease (SCTLD) is a widespread and deadly disease that affects nearly half of Caribbean coral species. To understand the microbial community response to this disease, we performed a disease transmission experiment on US Virgin Island (USVI) corals, exposing six species of coral with varying susceptibility to SCTLD. The microbial community of the surface mucus and tissue layers were examined separately using a small subunit ribosomal RNA gene-based sequencing approach, and data were analyzed to identify microbial community shifts following disease acquisition, potential causative pathogens, as well as compare microbiota composition to field-based corals from the USVI and Florida outbreaks. While all species displayed similar microbiome composition with disease acquisition, microbiome similarity patterns differed by both species and mucus or tissue microhabitat. Further, disease exposed but not lesioned corals harbored a mucus microbial community similar to those showing disease signs, suggesting that mucus may serve as an early warning detection for the onset of SCTLD. Like other SCTLD studies in Florida, Rhodobacteraceae, Arcobacteraceae, Desulfovibrionaceae, Peptostreptococcaceae, Fusibacter, Marinifilaceae, and Vibrionaceae dominated diseased corals. This study demonstrates the differential response of the mucus and tissue microorganisms to SCTLD and suggests that mucus microorganisms may be diagnostic for early disease exposure.

Energetic and reproductive costs of coral recovery in divergent bleaching responses.

Mass thermal bleaching events are a primary threat to coral reefs, yet the sublethal impacts, particularly on energetics and reproduction, are poorly characterized. Given that the persistence of coral populations is contingent upon the reproduction of individuals that survive disturbances, there is an urgent need to understand the sublethal effects of bleaching on reproductive output to accurately predict coral recovery rates. In 2019, the French Polynesian island of Mo'orea experienced a severe mass bleaching event accompanied by widespread coral mortality. At the most heavily impacted sites, we observed Acropora hyacinthus individuals that were resistant to bleaching, alongside colonies that bleached but showed signs of symbiont recovery shortly after the bleaching event. We collected fragments from A. hyacinthus colonies five months post-bleaching and, using energetic assays and histological measurements, examined the physiological and reproductive consequences of these two distinct heat stress responses. Despite healthy appearances in both resistant and recovered corals, we found that recovered colonies had significantly reduced energy reserves compared to resistant colonies. In addition, we detected compound effects of stress on reproduction: recovered colonies displayed both a lower probability of containing gametes and lower fecundity per polyp. Our results indicate that bleaching inflicts an energetic constraint on the concurrent re-accumulation of energy reserves and development of reproductive material, with decreased reproductive potential of survivors possibly hampering overall reef resilience. These findings highlight the presence of intraspecific responses to bleaching and the importance of considering multiple trajectories for individual species when predicting population recovery following disturbance.

Lethal and sublethal impacts of a micropredator on post-settlement Caribbean reef fishes.

The transition from a planktonic larval stage to a benthic or demersal juvenile stage, "recruitment", is a crucial event in the life history of coral reef fishes, and has a strong influence on population size. Predation by piscivorous fishes is thought to be the main determinant of recruitment success, and has received the most attention. However, recent studies suggest that recently settled reef fishes are also an important target of micropredation from blood-feeding ectoparasites which may have significant lethal and sublethal effects. In this study, we quantified the relationship between levels of infestation by gnathiid isopods and mortality rates among juveniles of three species of reef fishes as a function of body mass both within and among species. We found that a single gnathiid isopod larva could kill fish of all three species shortly after settlement, up to 0.116 g [18 mm fork length (FL)] in French grunt (Haemulon flavolineatum), 0.027 g (15 mm FL) in masked goby (Coryphopterus personatus) and 0.01 g (9 mm FL) in beaugregory damselfish (Stegastes leucostictus). For juvenile S. leucostictus, we also compared the ability of fish to defend a territory when infested with a sublethal number of gnathiids versus uninfected individuals. Uninfected fish were significantly more likely to win-pairwise contests versus infected fish. These findings suggest that gnathiids can significantly impact juvenile coral reef fish survival, and affect population dynamics well past the settlement stage.

Depth-Independent Reproduction in the Reef Coral Porites astreoides from Shallow to Mesophotic Zones.

Mesophotic coral ecosystems between 30-150 m may be important refugia habitat for coral reefs and associated benthic communities from climate change and coastal development. However, reduced light at mesophotic depths may present an energetic challenge to the successful reproduction of light-dependent coral organisms, and limit this refugia potential. Here, the relationship of depth and fecundity was investigated in a brooding depth-generalist scleractinian coral, Porites astreoides from 5-37 m in the U.S. Virgin Islands (USVI) using paraffin tissue histology. Despite a trend of increasing planulae production with depth, no significant differences were found in mean peak planulae density between shallow, mid-depth and mesophotic sites. Differential planulae production over depth is thus controlled by P. astreoides coral cover, which peaks at 10 m and ~35 m in the USVI. These results suggest that mesophotic ecosystems are reproductive refuge for P. astreoides in the USVI, and may behave as refugia for P. astreoides metapopulations providing that vertical larval exchanges are viable.

Fertile fathoms: Deep reproductive refugia for threatened shallow corals.

The persistence of natural metapopulations may depend on subpopulations that exist at the edges of species ranges, removed from anthropogenic stress. Mesophotic coral ecosystems (30-150 m) are buffered from disturbance by depth and distance, and are potentially massive reservoirs of coral diversity and fecundity; yet we know little about the reproductive capabilities of their constituent species and the potential for these marginal environments to influence patterns of coral reef persistence. We investigated the reproductive performance of the threatened depth-generalist coral Orbicella faveolata over the extent of its vertical range to assess mesophotic contributions to regional larval pools. Over equal habitat area, mesophotic coral populations were found to produce over an order of magnitude more eggs than nearby shallow populations. Positive changes with depth in both population abundance and polyp fecundity contributed to this discrepancy. Relative larval pool contributions of deeper living corals will likely increase as shallow habitats further degrade due to climate change and local habitat degradation. This is a compelling example of the potential for marginal habitat to be critical to metapopulation persistence as reproductive refugia.