A decade of population genetics studies of scleractinian corals: A systematic review.

Coral reefs are the most diverse marine ecosystems. However, coral cover has decreased worldwide due to natural disturbances, climate change, and local anthropogenic drivers. In recent decades, various genetic methods and molecular markers have been developed to assess genetic diversity, structure, and connectivity in different coral species to determine the vulnerability of their populations. This review aims to identify population genetic studies of scleractinian corals in the last decade (2010-2020), and the techniques and molecular markers used. Bibliometric analysis was conducted to identify journals and authors working in this field. We then calculated the number of genetic studies by species and ecoregion based on data obtained from 178 studies found in Scopus and Web of Science. Coral Reefs and Molecular Ecology were the main journals published population genetics studies, and microsatellites are the most widely used molecular markers. The Caribbean, Australian Barrier Reef, and South Kuroshio in Japan are among the ecoregions with the most population genetics data. In contrast, we found limited information about the Coral Triangle, a region with the highest biodiversity and key to coral reef conservation. Notably, only 117 (out of 1500 described) scleractinian coral species have genetic studies. This review emphasizes which coral species have been studied and highlights remaining gaps and locations where such data is critical for coral conservation.

Drivers of coral bleaching in a Marine Protected Area of the Southern Gulf of Mexico during the 2015 event.

Here we report the bleached coral cover and its drivers observed at Alacranes Reef in 2015. Our results show that 2015 was an unprecedented heat stress event. However, we observed low coral bleaching, with the most substantial impact on sites with a 10-20% of coral cover with bleaching. Depth was the most relevant variable related to coral bleaching and the bleaching severity index, with deeper reefs being most affected. Further, our results show that reefs with higher structural complexity based on species composition were among the most affected. We identified that accumulated heat stress and thermal variation in the last 28 days were relevant drivers of coral bleaching. This work highlights the importance of multidimensional frameworks in assessing the spatial variation of coral bleaching, demonstrating the importance of structural habitat variables such as depth in high heat stress events and at a reef scale.

Assessing and genotyping threatened staghorn coral Acropora cervicornis nurseries during restoration in southeast Dominican Republic.

Acropora cervicornis is a structurally and functionally important Caribbean coral species. Since the 1980s, it has suffered drastic population losses with no signs of recovery and has been classified as a critically endangered species. Its rapid growth rate makes it an excellent candidate for coral restoration programs. In 2011, the Fundación Dominicana de Estudios Marinos (Dominican Marine Studies Foundation, FUNDEMAR) began an A. cervicornis restoration program in Bayahibe, southeast Dominican Republic. In this study, we present the methodology and results of this program from its conception through 2017, a preliminary analysis of the strong 2016 and 2017 cyclonic seasons in the greater Caribbean, and a genetic characterization of the "main nursery". The mean survival of the fragments over 12 months was 87.45 ± 4.85% and the mean productivity was 4.01 ± 1.88 cm year-1 for the eight nurseries. The mean survival of six outplanted sites over 12 months was 71.55 ± 10.4%, and the mean productivity was 3.03 ± 1.30 cm year-1. The most common cause of mortality during the first 12 months, in both nurseries and outplanted sites, was predation by the fireworm, Hermodice carunculata. We identified 32 multilocus genotypes from 145 total analyzed individuals. The results and techniques described here will aid in the development of current and future nursery and outplanted site restoration programs.

Three decades of heat stress exposure in Caribbean coral reefs: a new regional delineation to enhance conservation.

Increasing heat stress due to global climate change is causing coral reef decline, and the Caribbean has been one of the most vulnerable regions. Here, we assessed three decades (1985-2017) of heat stress exposure in the wider Caribbean at ecoregional and local scales using remote sensing. We found a high spatial and temporal variability of heat stress, emphasizing an observed increase in heat exposure over time in most ecoregions, especially from 2003 identified as a temporal change point in heat stress. A spatiotemporal analysis classified the Caribbean into eight heat-stress regions offering a new regionalization scheme based on historical heat exposure patterns. The temporal analysis confirmed the years 1998, 2005, 2010-2011, 2015 and 2017 as severe and widespread Caribbean heat-stress events and recognized a change point in 2002-2004, after which heat exposure has been frequent in most subsequent years. Major heat-stress events may be associated with El Niño Southern Oscillation (ENSO), but we highlight the relevance of the long-term increase in heat exposure in most ecoregions and in all ENSO phases. This work produced a new baseline and regionalization of heat stress in the basin that will enhance conservation and planning efforts underway.

A coral-algal phase shift in Mesoamerica not driven by changes in herbivorous fish abundance.

Coral-algal phase shifts in which coral cover declines to low levels and is replaced by algae have often been documented on coral reefs worldwide. This has motivated coral reef management responses that include restriction and regulation of fishing, e.g. herbivorous fish species. However, there is evidence that eutrophication and sedimentation can be at least as important as a reduction in herbivory in causing phase shifts. These threats arise from coastal development leading to increased nutrient and sediment loads, which stimulate algal growth and negatively impact corals respectively. Here, we first present results of a dynamic process-based model demonstrating that in addition to overharvesting of herbivorous fish, bottom-up processes have the potential to precipitate coral-algal phase shifts on Mesoamerican reefs. We then provide an empirical example that exemplifies this on coral reefs off Mahahual in Mexico, where a shift from coral to algal dominance occurred over 14 years, during which there was little change in herbivore biomass but considerable development of tourist infrastructure. Our results indicate that coastal development can compromise the resilience of coral reefs and that watershed and coastal zone management together with the maintenance of functional levels of fish herbivory are critical for the persistence of coral reefs in Mesoamerica.

Distribución y abundancia del pez león Pterois volitans (Scorpaeniformes: Scorpaenidae) y especies nativas asociadas en el Parque Marino Cayos de San Felipe, Cuba / Distribution and abundance of the lionfish Pterois volitans (Scorpaeniformes: Scorpaenidae) and associated native species in Parque Marino Cayos de San Felipe, Cuba

ResumenEl primer avistamiento del pez león en el Parque Nacional "Cayos de San Felipe" en el 2009 podría amenazar la diversidad de sus ecosistemas marinos y la capacidad de brindar servicios. Para analizar la incidencia de la invasión del pez león en el área, se realizó un muestreo anual entre 2013 y 2015. La abundancia y la talla del pez león se estudió en manglares a través de censos visuales en diez transectos de 30x2 m/estación y en arrecifes (15 y 25 m de profundidad) con estéreo video en seis transectos de 50x2 m/estación. En arrecifes también se estimó incidencia de posibles competidores y depredadores nativos. En los tres años de estudio, la densidad promedio del pez león varió entre 0.0-1.3 indiv./100 m2 por estación de muestreo y no fue significativamente diferente entre hábitats (mangle - 0.6 indiv./100 m2, arrecifes a 15 m - 0.4 indiv./100 m2 y arrecifes a 25 m - 0.3 indiv./100 m2). La densidad de pez león fue igual o menor que la de competidores e igual o mayor que la de depredadores en ambas profundidades. La densidad del pez león en manglares y arrecifes a 25 m se mantuvo temporalmente estable, mientras que en arrecifes a 15 m disminuyó. Se observó que el incremento temporal de la abundancia de competidores y la densidad de depredadores no cambió durante el monitoreo. La talla del pez león varió entre 5 y 39 cm, siendo su promedio en manglares (12.6 cm) menor que en arrecifes (25.2 cm) y no mostró variaciones entre años. La talla de pez león en arrecifes fue más alta que la de competidores y menor que la de depredadores. Los resultados mostraron que en el parque: 1) los manglares son zonas de cría del pez león, 2) la incidencia del pez león en arrecifes no es tan alta como en otras áreas de Cuba y el Caribe y 3) la abundancia del pez león en arrecifes tendió a disminuir en el tiempo sin intervención de acciones extractivas o presencia de abundancia alta de meros nativos de tallas grandes. Considerando los resultados, se hacen recomendaciones para continuar el monitoreo e investigar los efectos del pez león y los factores que estan regulando su incidencia en el parque.

Abstract:The first lionfish sighting at the National Park "Cayos de San Felipe" was in 2009 and could be a threat to its marine ecosystem diversity and their capacity to generate services. To analyze the incidence of the lionfish invasion in the area, an annual sampling was conducted between 2013 and 2015. Lionfish abundance and size was investigated on mangroves through visual census on ten transects of 30x2 m/station, and on coral reefs (15 and 25 m deep) with stereo video on six transects of 50x2 m/station. Additionally, incidence of potential native competitors and predators on coral reefs were also estimated. Over the three years, the average density of lionfish varied between 0.0-1.3 indiv./100 m2 per sample stations and it was not significantly different among habitats (mangroves with 0.6 indiv./100 m2, reefs at 15 m - 0.4 indiv./100 m2 and reef at 25 m with 0.3 indiv./100 m2). Lionfish's density was equal to or lower than competitors' density, and was equal to or higher than predator's density in both depths. While lionfish density on mangroves and on reefs at 25 m remained temporally stable, it decreased on reefs at 15 m. Temporary increase in the competitor's density was observed and the predator´s density did not change during the monitored time. Lionfish size varied between 5 and 39 cm; the average fish size from mangroves (12.6 cm) was consistently lower than from reefs (25.2 cm) and showed no variations among years. Lionfish size in reefs was higher than competitor's size and lower than that of predator. Results showed that in the park: 1) mangroves represent lionfish nursery areas; 2) incidence of reef lionfish was not as high as in other areas of Cuba and the Caribbean; and 3) lionfish abundance in reefs tended to decrease over the years, without the intervention of extractive activities or high abundance of large size native groupers. In this sense, recommendations are made to continue monitoring and to investigate lionfish effects and factors that are regulating its incidence in the park. Rev. Biol. Trop. 65 (1): 117-125. Epub 2017 March 01.

[Distribution and abundance of the lionfish Pterois volitans (Scorpaeniformes: Scorpaenidae) and associated native species in Parque Marino Cayos de San Felipe, Cuba]. / Distribución y abundancia del pez león (Pterois volitans (Scorpaeniformes: Scorpaenidae) y especies nativas asociadas en el Parque Marino Cayos de San Felipe, Cuba.

The first lionfish sighting at the National Park "Cayos de San Felipe" was in 2009 and could be a threat to its marine ecosystem diversity and their capacity to generate services. To analyze the incidence of the lionfish invasion in the area, an annual sampling was conducted between 2013 and 2015. Lionfish abundance and size was investigated on mangroves through visual census on ten transects of 30x2 m/station, and on coral reefs (15 and 25 m deep) with stereo video on six transects of 50x2 m/station. Additionally, incidence of potential native competitors and predators on coral reefs were also estimated. Over the three years, the average density of lionfish varied between 0.0-1.3 indiv./100 m2 per sample stations and it was not significantly different among habitats (mangroves with 0.6 indiv./100 m2, reefs at 15 m - 0.4 indiv./100 m2 and reef at 25 m with 0.3 indiv./100 m2). Lionfish's density was equal to or lower than competitors' density, and was equal to or higher than predator's density in both depths. While lionfish density on mangroves and on reefs at 25 m remained temporally stable, it decreased on reefs at 15 m. Temporary increase in the competitor's density was observed and the predator´s density did not change during the monitored time. Lionfish size varied between 5 and 39 cm; the average fish size from mangroves (12.6 cm) was consistently lower than from reefs (25.2 cm) and showed no variations among years. Lionfish size in reefs was higher than competitor's size and lower than that of predator. Results showed that in the park: 1) mangroves represent lionfish nursery areas; 2) incidence of reef lionfish was not as high as in other areas of Cuba and the Caribbean; and 3) lionfish abundance in reefs tended to decrease over the years, without the intervention of extractive activities or high abundance of large size native groupers. In this sense, recommendations are made to continue monitoring and to investigate lionfish effects and factors that are regulating its incidence in the park.

Functional over-redundancy and high functional vulnerability in global fish faunas on tropical reefs.

When tropical systems lose species, they are often assumed to be buffered against declines in functional diversity by the ability of the species-rich biota to display high functional redundancy: i.e., a high number of species performing similar functions. We tested this hypothesis using a ninefold richness gradient in global fish faunas on tropical reefs encompassing 6,316 species distributed among 646 functional entities (FEs): i.e., unique combinations of functional traits. We found that the highest functional redundancy is located in the Central Indo-Pacific with a mean of 7.9 species per FE. However, this overall level of redundancy is disproportionately packed into few FEs, a pattern termed functional over-redundancy (FOR). For instance, the most speciose FE in the Central Indo-Pacific contains 222 species (out of 3,689) whereas 38% of FEs (180 out of 468) have no functional insurance with only one species. Surprisingly, the level of FOR is consistent across the six fish faunas, meaning that, whatever the richness, over a third of the species may still be in overrepresented FEs whereas more than one third of the FEs are left without insurance, these levels all being significantly higher than expected by chance. Thus, our study shows that, even in high-diversity systems, such as tropical reefs, functional diversity remains highly vulnerable to species loss. Although further investigations are needed to specifically address the influence of redundant vs. vulnerable FEs on ecosystem functioning, our results suggest that the promised benefits from tropical biodiversity may not be as strong as previously thought.

Global mismatch between species richness and vulnerability of reef fish assemblages.

The impact of anthropogenic activity on ecosystems has highlighted the need to move beyond the biogeographical delineation of species richness patterns to understanding the vulnerability of species assemblages, including the functional components that are linked to the processes they support. We developed a decision theory framework to quantitatively assess the global taxonomic and functional vulnerability of fish assemblages on tropical reefs using a combination of sensitivity to species loss, exposure to threats and extent of protection. Fish assemblages with high taxonomic and functional sensitivity are often exposed to threats but are largely missed by the global network of marine protected areas. We found that areas of high species richness spatially mismatch areas of high taxonomic and functional vulnerability. Nevertheless, there is strong spatial match between taxonomic and functional vulnerabilities suggesting a potential win-win conservation-ecosystem service strategy if more protection is set in these locations.

Additive partitioning of coral reef fish diversity across hierarchical spatial scales throughout the Caribbean.

There is an increasing need to examine regional patterns of diversity in coral-reef systems since their biodiversity is declining globally. In this sense, additive partitioning might be useful since it quantifies the contribution of alpha and beta to total diversity across different scales. We applied this approach using an unbalanced design across four hierarchical scales (80 sites, 22 subregions, six ecoregions, and the Caribbean basin). Reef-fish species were compiled from the Reef Environmental Education Foundation (REEF) database and distributions were confirmed with published data. Permutation tests were used to compare observed values to those expected by chance. The primary objective was to identify patterns of reef-fish diversity across multiple spatial scales under different scenarios, examining factors such as fisheries and demographic connectivity. Total diversity at the Caribbean scale was attributed to ß-diversity (nearly 62% of the species), with the highest ß-diversity at the site scale. [Formula: see text]-diversity was higher than expected by chance in all scenarios and at all studied scales. This suggests that fish assemblages are more homogenous than expected, particularly at the ecoregion scale. Within each ecoregion, diversity was mainly attributed to alpha, except for the Southern ecoregion where there was a greater difference in species among sites. ß-components were lower than expected in all ecoregions, indicating that fishes within each ecoregion are a subsample of the same species pool. The scenario involving the effects of fisheries showed a shift in dominance for ß-diversity from regions to subregions, with no major changes to the diversity patterns. In contrast, demographic connectivity partially explained the diversity pattern. ß-components were low within connectivity regions and higher than expected by chance when comparing between them. Our results highlight the importance of ecoregions as a spatial scale to conserve local and regional coral reef-fish diversity.

Predicted impact of the invasive lionfish Pterois volitans on the food web of a Caribbean coral reef.

The invasion of lionfish in the Caribbean is causing grave concern because of its deleterious impacts on coral reef food-webs. We have used an Ecopath-with-Ecosim model to predict the impacts of lionfish invasion on a coral reef community based on pre-invasion fish community data. Forty-six groups were defined, and an initial Ecopath model was balanced with a near-zero biomass of lionfish. In Ecosim, the near-zero biomass was eradicated by applying a very high fishing pressure in the first year of simulation. We subsequently (re-)introduced lionfish with a very low biomass, and allowed them to increase to very high abundance. With a near-zero lionfish biomass, the great majority of mesocarnivorous/omnivorous coral reef fish were predicted to be dominant while sharks were predicted to be the apex predators. Different management scenarios were established in the ecosystem to explore the eradication and resilience of lionfish. The management scenarios showed that if all adult lionfish were exploitable it will in theory be possible to fish the lionfish to a very low level, but the fishing pressure will have to be maintained, or the lionfish will recover. If the largest individuals are unexploitable it will be much more difficult to control the lionfish population.