Patterns of change in coral reef communities of a remote Maldivian atoll revisited after eleven years.

Coral reefs are exposed worldwide to several global and local human pressures including climate change and coastal development. Assessing the effects of such pressures on coral reef communities and the changes they undergo over time is mandatory to understand their possible future trends. Nonetheless, some coral reefs receive no or little scientific attention, as in the case of Huvadhoo Atoll that is an under-studied region in the southernmost area of the Maldives (Indian Ocean). This study analyzes the changes occurring over time in eight coral reefs (four inner reefs within the atoll lagoon and four outer reefs on the ocean side) at Huvadhoo Atoll, firstly surveyed in 2009 and revisited in 2020 using the same field methods. The cover of 23 morphological benthic descriptors (including different growth forms of Acropora) was taken into account and then grouped into three categories (i.e., hard coral, other benthic taxa and abiotic descriptors) to analyze the change in the composition of the coral reef community. Significant changes (e.g., increase in hard coral cover and decrease in abiotic descriptors) were observed in the inner reefs as compared to the outer reefs, which showed less variability. A significant decrease in tabular Acropora cover was observed in both inner and outer reefs, with possible negative effects on reef complexity and functioning. By comparing two time periods and two reef types, this study provides novel information on the change over time in the community composition of Maldivian coral reefs.

Unexpected slow recovery of seagrass leaf epiphytes after the impact of a summer heat wave and concomitant mucilage bloom.

The epiphytes of seagrass leaves constitute a peculiar community, comprised of a number of species specialized for this living substrate. Several studies report on the response of epiphytes to different pressures but no information exists about the effects of summer heatwaves, which have become frequent events in the last decades. This paper represents the first attempt to investigate the change in the leaf epiphyte community of the Mediterranean seagrass Posidonia oceanica due to the heatwave occurred in summer 2003. Thanks to a series of data collected seasonally between 2002 and 2006, and punctual data in the summers of 2014 and 2019, we assessed the change over time in the leaf epiphyte community. Temperature data trends were analysed through linear regression, while multivariate analyses (i.e., nMDS and SIMPER) were applied to cover data in order to assess changes over time in the epiphyte community. As a whole, the two most abundant taxa were the crustose coralline alga Hydrolithon and the encrusting bryozoan Electra posidoniae, which displayed the highest average cover values in summer (around 19%) and spring (around 9%), respectively. Epiphytes proved to be sensitive to temperature highs, displaying different effects on cover, biomass, diversity and community composition. Cover and biomass exhibited a dramatic reduction (more than 60%) after the disturbance. In particular, Hydrolithon more than halved, while E. posidoniae dropped sevenfold during summer 2003. While the former recovered comparatively quickly, the latter, as well as the whole community composition, apparently required 16 years to return to a condition similar to that of 2002.

Serpulid reefs and their role in aquatic ecosystems: A global review.

The Serpulidae are a large family of sedentary polychaetes, characterized by a calcareous habitation tube, which they cannot leave. The calcium carbonate tube is in the form of both aragonite and calcite, in fairly constant ratio for each taxon. Tubes are cemented firmly to any hard substrate (in only few species tubes are free). Although in the majority of the species the tubes encrust the substrate for all their length, the distal part may eventually detach and grow erectly. Certain species in dense populations build tubes vertical to the substrate in clumps and cement the tubes to each other. This gives serpulids the capability of forming reef-life structures when densely settling. Despite the relative smallness of the individual tubes (rarely longer than 15cm and wider than 1cm), such reef-like structures may cover tens of m2, with a layer more than 1m thick. Serpulid reefs can be divided roughly into seven groups, according to the building modality and the type of habitat they occupy: (i) pseudocolonies; (ii) littoral belts; (iii) subtidal to deep-water reefs; (iv) reefs in coastal lakes and harbours; (v) brackish water reefs; (vi) tapestries in freshwater caves; (vii) biostalactites inside marine caves. The role of serpulid reefs in the ecosystems they inhabit is multifarious and may be distinguished in functions (biomass and production, benthic pelagic coupling, resistance and resilience, reproductive and survivorship strategies, trophodynamics, bioconstruction, living space and refuge, nursery, sediment formation and retention, food for other species, carbonate deposition and storage) and services (water clearance, reef associated fishery, cultural benefits). On the other hand, many serpulids are important constituents of biological fouling, and their calcareous masses damage submerged artefacts, causing huge economic costs. Positive and negative roles of serpulid reefs need to be compared with common metrics; the overall balance, however, is still to be assessed.

Variability between observers does not hamper detecting change over time in a temperate reef.

Marine ecosystems are subject to global and local impacts, both contributing to dramatic changes in coastal communities. Assessing such changes requires time series or the revisitation of sites first surveyed in the past. In both cases, data are not necessarily collected by the same observers, which could lead to a bias in the results. In the Marine Protected Area (MPA) of Capo Carbonara (Sardinia, Italy), established in 1998, rocky reef communities were first assessed in 2000 by two diving scientists. Twenty years later, the same rocky reefs were resurveyed using the same method by two other diving scientists. In both surveys, semi-quantitative data on conspicuous species were collected at five sites in four depth zones, providing the possibility of assessing change over time. To explore the influence of climate and local pressures, existing data on sea surface temperature, resident population, tourism and diving activities were analysed. The reef communities of the Capo Carbonara MPA have distinctly changed over time, mostly under the effect of seawater warming, as highlighted by the occurrence of thermophilic species and by other climate-related indicators. On the other side, species vulnerable to local human pressures have increased over time, demonstrating the effectiveness of the protection measures undertaken by the MPA. Comparing data collected by four different observers in the two periods demonstrated that change over time was significantly greater than variability between the observers.

Benthic diversity patterns and predictors: A study case with inferences for conservation.

Understanding which drivers cause diversity patterns is a key issue in conservation. Here we applied a spatially explicit model to predict marine benthic diversity patterns according to environmental factors in the NW Mediterranean Sea. While most conservation-oriented diversity studies consider species richness only and neglect equitability, we measured separately species richness, equitability, and 'overall' diversity (i.e., the Shannon-Wiener H' function) on a dataset of 890 benthic species × 209 samples. Diversity values were predicted by means of Random Forest regression, on the basis of 10 factors: depth, distance from the coast, distance from the shelf break, latitude, sea-floor slope, sediment grain size, sediment sorting, distance from harbours and marinas, distance from rivers, and sampling gear. Predictions by Random Forests were accurate, the main predictors being latitude, sediment grain size, depth and distance from the coast. Based on predicted values, diversity hotspots were identified as those localities where indices were in the 15% top segment of ranked values. Only a minority of the diversity hotspots was included within the boundaries of the protection institutes established in the region. Marine protected areas are often created in sites harbouring important coastal habitats, which risks neglecting the diversity hidden in the sedimentary seafloor. We suggest that marine protected areas should accommodate portions of sedimentary habitat within their boundaries to improve diversity conservation.

Eavesdropping on dolphins: Investigating the habits of bottlenose dolphins (Tursiops truncatus) through fixed acoustic stations.

This study investigates the bottlenose dolphin (Tursiops truncatus, Montagu 1821) habitat use in the Portofino marine protected area (NW Italy) and adjacent waters, a core area for the dolphins and a highly touristic area in the Mediterranean Sea. A permanent automated real-time passive acoustic monitoring system, able to detect and track dolphins continuously, was tested in the area within the activities of the Life+ Nature project ARION. The habits of bottlenose dolphins was investigated considering the resident rate inside the area, which quantifies the amount of time dolphins spent in these waters, by means of random forest regression. The dependency of dolphin resident rate was analyzed in relation to four explanatory variables: sea surface temperature, season, time of day, and proximity to the coast. Dolphins spent more time in the area during spring and when sea surface temperature ranged between 15-16°C. Summer resulted the season with lower dolphin residency with significant difference between working day and weekend, in the last the lowest residency was recorded. Main findings provide important information to properly manage the area in order to protect bottlenose dolphins.

Organization Science improves management effectiveness of Marine Protected Areas.

The ecological management effectiveness (EME) of Marine Protected Areas (MPAs) is the degree to which MPAs reach their ecological goals. The significant variability of EME among MPAs has been partly explained by MPA design, management and implementation features (e.g. surface area, enforcement, age of protection). We investigated EME variability by employing, for the first time, Organization Science. Eight Mediterranean MPAs were taken into account as case studies to explore the relationships between EME and MPA features, such as: 1) organizational size (i.e. the ratio between the number of full-time employees and the total MPA surface area), 2) management performance (i.e. the level of effort exerted to enhance and sustain the MPA management, including enforcement), 3) total surface area, and 4) MPA age. The log-response ratios of fish biomass and density in protected vs unprotected (control) areas were used as a proxy of EME. Management performance, organizational size and, to a lesser extent, MPA age were positively correlated with the log-response ratio of fish biomass, whereas total surface area did not display a significant role. None of the four features considered was significantly correlated with the log-response ratio of fish density. Based on our findings, we argue that the employment of Organization Science in the management effectiveness assessment can assist MPA managers to reach MPAs goals more effectively, with a more efficient use of available resources.

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 2-3 years after the bleaching, and 6-9 years passed until constratal (i.e., low relief) growth was achieved. Finally, 14-16 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.

Mediterranean Bioconstructions Along the Italian Coast.

Marine bioconstructions are biodiversity-rich, three-dimensional biogenic structures, regulating key ecological functions of benthic ecosystems worldwide. Tropical coral reefs are outstanding for their beauty, diversity and complexity, but analogous types of bioconstructions are also present in temperate seas. The main bioconstructions in the Mediterranean Sea are represented by coralligenous formations, vermetid reefs, deep-sea cold-water corals, Lithophyllum byssoides trottoirs, coral banks formed by the shallow-water corals Cladocora caespitosa or Astroides calycularis, and sabellariid or serpulid worm reefs. Bioconstructions change the morphological and chemicophysical features of primary substrates and create new habitats for a large variety of organisms, playing pivotal roles in ecosystem functioning. In spite of their importance, Mediterranean bioconstructions have not received the same attention that tropical coral reefs have, and the knowledge of their biology, ecology and distribution is still fragmentary. All existing data about the spatial distribution of Italian bioconstructions have been collected, together with information about their growth patterns, dynamics and connectivity. The degradation of these habitats as a consequence of anthropogenic pressures (pollution, organic enrichment, fishery, coastal development, direct physical disturbance), climate change and the spread of invasive species was also investigated. The study of bioconstructions requires a holistic approach leading to a better understanding of their ecology and the application of more insightful management and conservation measures at basin scale, within ecologically coherent units based on connectivity: the cells of ecosystem functioning.

A predictive approach to benthic marine habitat mapping: Efficacy and management implications.

The availability of marine habitats maps remains limited due to difficulty and cost of working at sea. Reduced light penetration in the water hampers the use of optical imagery, and acoustic methods require extensive sea-truth activities. Predictive spatial modelling may offer an alternative to produce benthic habitat maps based on complete acoustic coverage of the seafloor together with a comparatively low number of sea truths. This approach was applied to the coralligenous reefs of the Marine Protected Area of Tavolara - Punta Coda Cavallo (NE Sardinia, Italy). Fuzzy clustering, applied to a set of observations made by scuba diving and used as sea truth, allowed recognising five coralligenous habitats, all but one existing within EUNIS (European Nature Information System) types. Variable importance plots showed that the distribution of habitats was driven by distance from coast, depth, and lithotype, and allowed mapping their distribution over the MPA. Congruence between observed and predicted distributions and accuracy of the classification was high. Results allowed calculating the occurrence of the distinct coralligenous habitats in zones with different protection level. The five habitats are unequally protected since the protection regime was established when detailed marine habitat maps were not available. A SWOT (Strengths-Weaknesses-Opportunities-Threats) analysis was performed to identify critical points and potentialities of the method. The method developed proved to be reliable and the results obtained will be useful when modulating on-going and future management actions in the studied area and in other Mediterranean MPAs to develop conservation efforts at basin scale.

Applying organization science to assess the management performance of Marine Protected Areas: An exploratory study.

Marine Protected Areas (MPAs) are important tools to achieve marine conservation and resources management goals. The management effectiveness of MPAs (the degree to which MPAs achieve their goals) is highly variable and can be affected by many MPA attributes, for example their design, enforcement and age. Another key factor possibly affecting MPA management effectiveness is the management performance, here conceived according to Horigue et al. definition (2014) as the "level of effort exerted to enhance and sustain management of MPAs". Organization Science (OS), the discipline that studies organizations, can offer a useful framework to assess and interpret MPA management performance. Using an exploratory multiple case study approach, we applied OS principles to 11 Mediterranean MPAs in order to: i) characterize several MPA organizational features; ii) assess MPA management performance (evaluated as the effort deployed in, for example, planning the future, formalizing measurable goals, and implementing specific strategies). Results show that a number of organizational features and networking attributes are highly variable among the MPAs we have studied. For instance, goals are seldom measurable and the strategy to achieve goals is not systematically pursued. Two relevant outcomes emerge from this exploratory study: i) the management performance of the MPAs considered needs considerable improvements; ii) the methods and the approach proposed could help MPAs' managers and policy makers to understand how to improve their management performance and, consequently, their effectiveness.

Fish mitigate trophic depletion in marine cave ecosystems.

Dark marine habitats are often characterized by a food-limited condition. Peculiar dark habitats include marine caves, characterized by the absence of light and limited water flow, which lead to reduced fluxes of organic matter for cave-dwelling organisms. We investigated whether the most abundant and common cave-dwelling fish Apogon imberbis has the potential to play the role of trophic vector in Mediterranean marine caves. We first analysed stomach contents to check whether repletion changes according to a nycthemeral cycle. We then identified the prey items, to see whether they belong to species associated with cave habitats or not. Finally, we assessed whether A. imberbis moves outside marine caves at night to feed, by collecting visual census data on A. imberbis density both inside and outside caves, by day and by night. The stomach repletion of individuals sampled early in the morning was significantly higher than later in the day. Most prey were typical of habitats other than caves. A. imberbis was on average more abundant within caves during the day and outside during the night. Our study supports the hypothesis regarding the crucial trophic role of A. imberbis in connecting Mediterranean marine caves with external habitats.

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.

An integrated method to evaluate and monitor the conservation state of coralligenous habitats: The INDEX-COR approach.

A new method based on photographic sampling coupled with in situ observations was applied to 53 stations along the French Mediterranean coast, to assess the integrity of coralligenous reefs affected by different levels of anthropogenic pressure. The conservation state of the assemblages characterizing these habitats was then assessed by an index - the INDEX-COR - that integrates three metrics: (i) the sensitivity of the taxa to organic matter and sediment deposition, (ii) the observable taxonomic richness, and (iii) the structural complexity of the assemblages. The sensitivity of INDEX-COR was tested and showed good correlation with the Level of Pressure calculated for each station according to expert judgment and field observations.

An ecosystem-based approach to assess the status of Mediterranean algae-dominated shallow rocky reefs.

A conceptual model was constructed for the functioning the algae-dominated rocky reef ecosystem of the Mediterranean Sea. The Ecosystem-Based Quality Index (reef-EBQI) is based upon this model. This index meets the objectives of the EU Marine Strategy Framework Directive. It is based upon (i) the weighting of each compartment, according to its importance in the functioning of the ecosystem; (ii) biological parameters assessing the state of each compartment; (iii) the aggregation of these parameters, assessing the quality of the ecosystem functioning, for each site; (iv) and a Confidence Index measuring the reliability of the index, for each site. The reef-EBQI was used at 40 sites in the northwestern Mediterranean. It constitutes an efficient tool, because it is based upon a wide set of functional compartments, rather than upon just a few species; it is easy and inexpensive to implement, robust and not redundant with regard to already existing indices.

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 (1961-2008) 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 50years. 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.

Observational information on a temperate reef community helps understanding the marine climate and ecosystem shift of the 1980-90s.

The dearth of long-time series hampers the measurement of the ecosystem change that followed the global marine climate shift of the 1980-90s. The sessile communities of Portofino Promontory reefs (Ligurian Sea, NW Mediterranean) have been discontinuously studied since the 1950s. Collating information from various sources, three periods of investigations have been distinguished: 1) 1950-70s; 2) 1980-90s; 3) 2000-10s. A cooler phase in time 1 was followed by a rapid warming in time 2, to stabilize at about 0.5°C higher in time 3. Human pressure grew impressively, especially after the establishment of a MPA in 1999. Multivariate analyses evidenced a major change of community composition in time 2. Some species disappeared or got rarer, many found refuge at depth, and among the newcomers there were recently introduced alien species. This study demonstrated the importance of descriptive historical data to understand magnitude and pattern of change in the long term evolution of marine ecosystems.

A Permanent Automated Real-Time Passive Acoustic Monitoring System for Bottlenose Dolphin Conservation in the Mediterranean Sea.

Within the framework of the EU Life+ project named LIFE09 NAT/IT/000190 ARION, a permanent automated real-time passive acoustic monitoring system for the improvement of the conservation status of the transient and resident population of bottlenose dolphin (Tursiops truncatus) has been implemented and installed in the Portofino Marine Protected Area (MPA), Ligurian Sea. The system is able to detect the simultaneous presence of dolphins and boats in the area and to give their position in real time. This information is used to prevent collisions by diffusing warning messages to all the categories involved (tourists, professional fishermen and so on). The system consists of two gps-synchronized acoustic units, based on a particular type of marine buoy (elastic beacon), deployed about 1 km off the Portofino headland. Each one is equipped with a four-hydrophone array and an onboard acquisition system which can record the typical social communication whistles emitted by the dolphins and the sound emitted by boat engines. Signals are pre-filtered, digitized and then broadcast to the ground station via wi-fi. The raw data are elaborated to get the direction of the acoustic target to each unit, and hence the position of dolphins and boats in real time by triangulation.

Through bleaching and tsunami: Coral reef recovery in the Maldives.

Coral reefs are degrading worldwide, but little information exists on their previous conditions for most regions of the world. Since 1989, we have been studying the Maldives, collecting data before, during and after the bleaching and mass mortality event of 1998. As early as 1999, many newly settled colonies were recorded. Recruits shifted from a dominance of massive and encrusting corals in the early stages of recolonisation towards a dominance of Acropora and Pocillopora by 2009. Coral cover, which dropped to less than 10% after the bleaching, returned to pre-bleaching values of around 50% by 2013. The 2004 tsunami had comparatively little effect. In 2014, the coral community was similar to that existing before the bleaching. According to descriptors and metrics adopted, recovery of Maldivian coral reefs took between 6 and 15years, or may even be considered unachieved, as there are species that had not come back yet.