Long-term change in bioconstruction potential of Maldivian coral reefs following extreme climate anomalies

Global climate change has increased the frequency and intensity of extreme heat anomalies and consequent mass coral bleaching events. Long-term dynamics of hard coral cover, bioconstruction potential, carbonate deposition, and reef accretion was monitored over a 20-year period on Maldivian coral reefs in order to investigate the effects of high-temperature anomalies on coral reef accretion and their recovery potential. Changes experienced by shallow reefs between 1997 and 2017 were evaluated by considering five different bioconstructional guilds and the BioConstruction Potential index (BCP), a proxy for the constructional capacity of reefs. Abnormally high temperatures in 1998 and 2016 led to severe coral bleaching and consequent mortality, especially of the primary builders. Renewed carbonate deposition was not documented until 2\u20133 years after the bleaching, and 6\u20139 years passed until constratal (i.e., low relief) growth was achieved. Finally, 14\u201316 years were required to reach accretion rates high enough to ensure superstratal (i.e., high relief) growth. Coral mortality in the Maldives during the 2016 bleaching event was lower than in 1998, and the initial recovery was faster and occurred via a different trajectory than in 1998. Rising levels of anthropogenic carbon emissions are predicted to accelerate sea level rise and trigger severe coral bleaching events at least twice per decade, a frequency that will (a) prevent coral recovery, (b) nullify reef accretion, and consequently, (c) result in the drowning of Maldivian reefs under the worst climate projections

Influence of Local Pressures on Maldivian Coral Reef Resilience Following Repeated Bleaching Events, and Recovery Perspectives

Two severe heat waves triggered coral bleaching and mass mortality in the Maldives in 1998 and 2016. Analysis of live coral cover data from 1997 to 2019 in shallow (5 m depth) reefs of the Maldives showed that the 1998 heat wave caused more than 90% of coral mortality leaving only 6.8 ± 0.3% of survived corals in all the shallow reefs investigated. No significant difference in coral mortality was observed among atolls with different levels of human pressure. Maldivian reefs needed 16 years to recover to the pre-bleaching hard coral cover values. The 2016 heat wave affected all reefs investigated, but reefs in atolls with higher human pressure showed greater coral mortality than reefs in atolls with lower human pressure. Additionally, exposed (ocean) reefs showed lower coral mortality than those in sheltered (lagoon) reefs. The reduced coral mortality in 2016 as compared to 1998 may provide some support to the Adaptive Bleaching Hypothesis (ABH) in shallow Maldivian reefs, but intensity and duration of the two heat waves were different. Analysis of coral cover data collected along depth profiles on the ocean sides of atolls, from 10 to 50 m, allowed the comparison of coral mortality at different depths to discuss the Deep Refuge Hypothesis (DRH). In the upper mesophotic zone (i.e., between 30 and 50 m), coral mortality after bleaching was negligible. However, live coral cover did not exceed 15%, a value lower than coral survival in shallow reefs. Low cover values of corals surviving in the mesophotic reefs suggest that their role as refuge or seed banks for the future recovery of some species in shallow-water reefs of the Maldives may be small. The repeatedly high coral mortality after bleaching events and the long recovery period, especially in sites with human pressure, suggest that the foreseen increased frequency of bleaching events would jeopardize the future of Maldivian reefs, and ask for reducing local pressures to improve their resilience

Pattern and intensity of human impact on coral reefs depend on depth along the reef profile and on the descriptor adopted

Coral reefs are threatened by multiple global and local disturbances. The Maldives, already heavily hit by the 1998 mass bleaching event, are currently affected also by growing tourism and coastal development that may add to global impacts. Most of the studies investigating effects of local disturbances on coral reefs assessed the response of communities along a horizontal distance from the impact source. This study investigated the status of a Maldivian coral reef around an island where an international touristic airport has been recently (2009-2011) built, at different depths along the reef profile (5-20 m depth) and considering the change in the percentage of cover of five different non-taxonomic descriptors assessed through underwater visual surveys: hard corals, soft corals, other invertebrates, macroalgae and abiotic attributes. Eight reefs in areas not affected by any coastal development were used as controls and showed a reduction of hard coral cover and an increase of abiotic attributes (i.e. sand, rock, coral rubble) at the impacted reef. However, hard coral cover, the most widely used descriptor of coral reef health, was not sufficient on its own to detect subtle indirect effects that occurred down the reef profile. Selecting an array of descriptors and considering different depths, where corals may find a refuge from climate impacts, could guide the efforts of minimising local human pressures on coral reef

The two facets of species sensitivity: stress and disturbance on coralligenous assemblages in space and time.

Marine coastal ecosystems are affected by a vast array of human-induced disturbances and stresses, which are often capable of overwhelming the effects of natural changes. Despite the conceptual and practical difficulty in differentiating between disturbance and stress, which are often used interchangeably, the two terms bear different ecological meanings. Both are external agents, but the former causes mortality or physical damage (subtraction of biomass), whereas the latter causes physiological alteration (reduction in productivity). Sensitivity of marine organisms may thus have a dual connotation, being influenced in different ways by disturbance and by stress following major environmental change. Coralligenous assemblages, which shape unique biogenic formations in the Mediterranean Sea, are considered highly sensitive to change. In this paper, we propose a method to differentiate between disturbance and stress to assess the ecological status of the coralligenous assemblages. Disturbance sensitivity level (DSL) and stress sensitivity level (SSL) of the sessile organisms thriving in the coralligenous assemblages were combined into the integrated sensitivity level of coralligenous assemblages (ISLA) index. Changes in the coralligenous status were assessed in space, along a gradient of stress (human-induced pressures) at several sites of the western Mediterranean, and in time, from a long-term series (1961\u20132008) at Mesco Reef (Ligurian Sea) that encompasses a mass mortality event in the 1990s. The quality of the coralligenous assemblages was lower in highly urbanised sites than that in sites in both marine protected areas and areas with low levels of urbanisation; moreover, the quality of the assemblages at Mesco Reef decreased during the last 50 years. Reduction in quality was mainly due to the increase in stress-tolerant and/or opportunist species (e.g. algal turfs, hydroids and encrusting sponges), the disappearance of the most sensitive macroalgae (e.g. Udoteaceae and erect Rhodophyta) and macro-invertebrates (e.g. Savalia savaglia, Alcyonium coralloides and Smittina cervicornis), and the appearance of invasive alien algal species. Although the specific indices of SSL or DSL well illustrated the changes in the spatial or temporal datasets, respectively, their integration in the ISLA index was more effective in measuring the change experienced by the coralligenous assemblages in both space and time

Impact of a harbour construction on the benthic community of two shallow marine caves

Marine caves are unique and vulnerable habitats, threatened by multiple global and local disturbances. Whilst the effects of climate change on marine caves have already been investigated, no information exists about the effects of local human impacts, such as coastal development, on these habitats. This study investigated the impact of the construction of a touristic harbour on two shallow underwater marine caves in the Ligurian Sea (NW Mediterranean). As a standard methodology for monitoring marine caves does not exist yet, changes over time on the benthic community were assessed adopting two different non-taxonomic descriptors: trophic guilds and growth forms. Harbour construction caused an increase of sediment load within the caves, with a consequent decline of filter feeder organisms. Abundance of small organisms, such as encrusting and flattened sponges, was greatly reduced in comparison to organisms with larger and erect growth forms, such as domed mounds and pedunculated sponges. Our study indicated that growth forms and trophic guilds are effective descriptors for evaluating changes over time in marine caves, and could be easily standardised and applied in monitoring plans. In addition, as the harbour construction impacted differently according to the cave topography, the use of a systematic sampling in different zones of an underwater cave is recommended

Combinando revisión bibliográfica, mapas acústicos y observaciones in situ: sinopsis de las formaciones coralígenas en Liguria (NO del mar Mediterráneo)

A review and update of the existing knowledge on the coralligenous assemblages of Liguria (NW Italy) was conducted as an essential step towards management measures for their conservation according to the EU Marine Strategy Framework Directive. By combining a literature review, acoustic mapping and in situ observations on a geographic information systems platform, we were able to assess the distribution and heterogeneity of coralligenous assemblages and the main pressures affecting them. The reliability of the literature was previously estimated using a dependability index. The coralligenous assemblages cover an area of 130.9 ha and range from 10 to 113 m depth. Twelve different biological facies (five of them not included in the EUNIS list) were identified and four main geomorphotypes (plungingcliffs, paleocliffs, rockfalls and shoals) were recognized. Incident light values influenced the distribution of four facies in Portofino promontory. Pressures were found on 33% of the coralligenous assemblages investigated, mainly due to fishing activities, mass mortality events, invasive species and occasional mucilaginous events. Our results showed a high spatial, geomorphological and biological heterogeneity of coralligenous assemblages in Liguria.Una revisión y actualización del conocimiento existente sobre las formaciones coralígenas en Liguria (NO de Italia) ha sido implementado como paso esencial con vistas a las medidas de gestión para su conservación de acuerdo con la Directiva Marco sobre la Estrategia Marina. Combinando en plataforma SIG revisión bibliográfica, mapas acústicos y observaciones in situ hemos sido capaces de determinar la distribución de las formaciones coralígenas, su heterogeneidad y sus principales presiones. La fiabilidad de la bibliografía fue estimada a través del índice de confianza (DI). Las formaciones coralígenas cubren un área de 130.9 ha en un rango de profundidad que va desde los 10 m a los 113 m. 12 facies biológicas diferentes (5 de ellas no incluidas en la lista EUNIS) fueron identificadas y 4 geomorfotipos principales (acantilado actual, paleoacantilado, cúmulo de rocas y bajos) fueron reconocidos. Los valores de luz incidente influenciaron la distribución de 4 facies en el promontorio de Portofino. Fueron encontradas presiones en el 33% de las formaciones coralígenas inves-tigadas, principalmente debidas a actividades de pesca, episodios de muerte masiva, especies invasoras y proliferación de algas mucilaginosas. Nuestros resultados mostraron una elevada heterogeneidad espacial, geomorfológica y biológica de las formaciones coralígenas en Liguria

Integración de el índice ESCA por medio de los macro-invertebrados sésiles

The ESCA (Ecological Status of Coralligenous Assemblages) index was developed to assess the ecological quality of coralligenous habitat using macroalgae as a biological indicator. The aim of this study was to evaluate the response to human-induced pressures of macroalgae and sessile macro-invertebrates shaping the coralligenous habitat and to integrate their sensitivity into the ESCA index. Coralligenous assemblages were sampled at 15 locations of the NW Mediterranean Sea classified into three groups: i) marine protected areas; ii) low urbanized locations; and iii) highly urbanized locations. A sensitivity level value was assigned to each taxon/group on the basis of its abundance in each environmental condition, the data available in the literature and the results of an expert judgement survey. The index that includes the totality of the assemblages (named ESCA-TA), calculated using both macroalgae and sessile macro-invertebrates, detected the levels of human pressure more precisely than the index calculated with only macroalgae or with only invertebrates. The potential for assessing the ecological quality of marine coastal areas was thus increased with the ESCA-TA index thanks to the use of a higher variety of descriptors

Thirty year ecosystem trajectories in a submerged marine cave under changing pressure regime

Marine caves are unique and vulnerable habitats exhibiting high biodiversity and heterogeneity, but threatened by multiple global and local disturbances. Marine caves, although widely distributed along the Mediterranean coast, suffer for the lack of quantitative data on their structure and function, which hinder their conservation status assessment. Thanks to the availability of a nearly 30-year-long series of data (1986-2013), we evaluated ecosystem change in the Bergeggi marine cave (Ligurian Sea, NW Mediterranean), a cave with a complex shape and high habitat heterogeneity. Non-taxonomic descriptors were adopted, namely growth forms (GF) and trophic guilds (TG), which are informative about ecosystem structure and functioning, respectively. The cave experienced a general trend of change during the last three decades, mainly due to the decline in the cover of sessile organisms (especially 3-dimensional forms) matched by an increase of turf and sediment, thus causing the structural and functional homogenization of the cave community. While change before 2004 had been attributed to climatic factors (especially to the summer heat waves of 1999 and 2003), the most important rate of change was observed between 2009 and 2013, coinciding with recent major beach nourishments and the extension of the neighbouring Vado Ligure harbour, thus providing evidences on the importance of local disturbances deriving from coastal interventions. Monitoring the status of cave ecosystems is urgently needed, and the use of effective indicators, such as the specific traits here adopted (morphology and feeding strategy), could provide effective tools to assist marine cave conservation

Seafloor integrity down the harbor waterfront: the coralligenous shoals off Vado Ligure (NW Mediterranean)

In the last ten years, European Directives stressed the necessity to assess the ecological status of marine habitats by means of ecosystem or landscape indicators, rather than just species or chemical ones. In this paper, the seascape approach to characterise and assess the ecological quality of coralligenous rocky shoals of Vado Ligure (Savona, Italy) is introduced. This approach integrates biological, mesological and geomorphological information collected with a Rapid Visual Assessment technique (RVA). The RVA also optimised underwater operations in deep waters where coralligenous reefs usually develop and provided a sufficient amount of data collected by direct inspection. The seascape approach results are appropriate for the characterisation of the coralligenous shoals studied and for the assessment of their ecological quality. The quality of the assemblages was in general low, mainly due to high sedimentary stress; however, some exceptions showing a high ecological quality indicate that, with proper manage- ment tools, they would still have good potentialities of recovery

Multiple indices on different habitats and descriptors provide consistent assessments of environmental quality in a marine protected area

In the last decades, climate change and human pressures have increasingly and dramatically impacted the ocean worldwide, calling for urgent actions to safeguard coastal marine ecosystems. The European Commission, in particular, has set ambitious targets for member states with two major directives, the Water Framework Directive (WFD) and the Marine Strategy Framework Directive (MSFD), both designed to protect the marine environment in EU waters. Diverse biotic indices have accordingly been developed to assess water and habitat quality. The WFD adopts four Biological Quality Elements (BQEs), whereas the MSFD recommends a set of eleven qualitative descriptors. The borderline between water quality and habitat quality is hard to trace and so far most assessments have involved the use of a few indices and were mainly related to a single BQE or qualitative descriptor. In this study, thanks to the availability of a large dataset encompassing a wide array of descriptors, we compared the performance of 11 biotic indices relative to three habitats/biotic components (reefs, seagrass, and fish) of the Marine Protected Area (MPA) of Capo Carbonara (SE Sardinia, Italy). The aim was to assess whether the indices were consistent in defining the environmental status in the MPA investigated. We used the graphical approach RESQUE (REsilience and QUality of Ecosystem), which enabled us to obtain a single and comprehensive measure of the status of the environment by integrating several metrics. This approach was applied here to different habitats for the first time. All indices were consistent with each other in confirming the good status of Capo Carbonara MPA. The use of RESQUE provided insights to interpret the differences between water quality, defined according to the WFD, and habitat quality, defined according to the MSFD. Differences between the two EU directives, in terms of either requirements or goals, have long been discussed but the present study highlights for the first time that they are congruent in their assessment of the environmental status of marine ecosystems