Joaquim Garrabou

The Structure of Mediterranean Rocky Reef Ecosystems across Environmental and Human Gradients, and Conservation Implications

Historical exploitation of the Mediterranean Sea and the absence of rigorous baselines makes it difficult to evaluate the current health of the marine ecosystems and the efficacy of conservation actions at the ecosystem level. Here we establish the first current baseline and gradient of ecosystem structure of nearshore rocky reefs at the Mediterranean scale. We conducted underwater surveys in 14 marine protected areas and 18 open access sites across the Mediterranean, and across a 31-fold range of fish biomass (from 3.8 to 118 g m−2). Our data showed remarkable variation in the structure of rocky reef ecosystems. Multivariate analysis showed three alternative community states: (1) large fish biomass and reefs dominated by non-canopy algae, (2) lower fish biomass but abundant native algal canopies and suspension feeders, and (3) low fish biomass and extensive barrens, with areas covered by turf algae. Our results suggest that the healthiest shallow rocky reef ecosystems in the Mediterranean have both large fish and algal biomass. Protection level and primary production were the only variables significantly correlated to community biomass structure. Fish biomass was significantly larger in well-enforced no-take marine reserves, but there were no significant differences between multi-use marine protected areas (which allow some fishing) and open access areas at the regional scale. The gradients reported here represent a trajectory of degradation that can be used to assess the health of any similar habitat in the Mediterranean, and to evaluate the efficacy of marine protected areas.

Global regime shift dynamics of catastrophic sea urchin overgrazing

A pronounced, widespread and persistent regime shift among marine ecosystems is observable on temperate rocky reefs as a result of sea urchin overgrazing. Here, we empirically define regime-shift dynamics for this grazing system which transitions between productive macroalgal beds and impoverished urchin barrens. Catastrophic in nature, urchin overgrazing in a well-studied Australian system demonstrates a discontinuous regime shift, which is of particular management concern as recovery of desirable macroalgal beds requires reducing grazers to well below the initial threshold of overgrazing. Generality of this regime-shift dynamic is explored across 13 rocky reef systems (spanning 11 different regions from both hemispheres) by compiling available survey data (totalling 10 901 quadrats surveyed in situ) plus experimental regime-shift responses (observed during a total of 57 in situ manipulations). The emergent and globally coherent pattern shows urchin grazing to cause a discontinuous ‘catastrophic’ regime shift, with hysteresis effect of approximately one order of magnitude in urchin biomass between critical thresholds of overgrazing and recovery. Different life-history traits appear to create asymmetry in the pace of overgrazing versus recovery. Once shifted, strong feedback mechanisms provide resilience for each alternative state thus defining the catastrophic nature of this regime shift. Importantly, human-derived stressors can act to erode resilience of desirable macroalgal beds while strengthening resilience of urchin barrens, thus exacerbating the risk, spatial extent and irreversibility of an unwanted regime shift for marine ecosystems.

Sponge Mass Mortalities in a Warming Mediterranean Sea: Are Cyanobacteria-Harboring Species Worse Off?

Mass mortality events are increasing dramatically in all coastal marine environments. Determining the underlying causes of mass mortality events has proven difficult in the past because of the lack of prior quantitative data on populations and environmental variables. Four-year surveys of two shallow-water sponge species, Ircinia fasciculata and Sarcotragus spinosulum, were carried out in the western Mediterranean Sea. These surveys provided evidence of two severe sponge die-offs (total mortality ranging from 80 to 95% of specimens) occurring in the summers of 2008 and 2009. These events primarily affected I. fasciculata, which hosts both phototrophic and heterotrophic microsymbionts, while they did not affect S. spinosulum, which harbors only heterotrophic bacteria. We observed a significant positive correlation between the percentage of injured I. fasciculata specimens and exposure time to elevated temperature conditions in all populations, suggesting a key role of temperature in triggering mortality events. A comparative ultrastructural study of injured and healthy I. fasciculata specimens showed that cyanobacteria disappeared from injured specimens, which suggests that cyanobacterial decay could be involved in I. fasciculata mortality. A laboratory experiment confirmed that the cyanobacteria harbored by I. fasciculata displayed a significant reduction in photosynthetic efficiency in the highest temperature treatment. The sponge disease reported here led to a severe decrease in the abundance of the surveyed populations. It represents one of the most dramatic mass mortality events to date in the Mediterranean Sea.

Effects of diver frequentation on Mediterranean sublittoral populations of the bryozoan Pentapora fascialis

The erect, foliaceous bryozoan Pentapora fascialis was selected as an indicator of the abrasive effects of heavy diving activity in Mediterranean coralligenous communities. A comparative survey of bryozoan populations at diver-frequented and unfrequented sites was undertaken in the Medes Islands Protected Area (NW Mediterranean) in 1992. Density, colony diameter, and colony height of P. fascialis populations were significantly lower and colony position was more cryptic at frequented sites than at unfrequented sites. Human frequentation may affect not only the structure of P. fascialis populations, but also that of the coralligenous community as a whole.

Landscape pattern indices applied to Mediterranean subtidal rocky benthic communities

Marine rocky benthic communities present rich contrasts in spatial pattern. Its quantification is a prerequisite for the comparison of spatial pattern across communities, for the evaluation of temporal changes, and for the analysis of the effects of pattern on ecological processes. This study pursues two goals: (1) to evaluate the potential application of landscape pattern indices to the description of spatial pattern in Mediterranean subtidal rocky benthic communities, and (2) to select a minimal set of informative, non-redundant indices for the description of spatial pattern in these communities. Four communities dwelling along a depth gradient were studied, two dominated by algae, and two dominated by clonal animals. The communities differed in species composition, dynamics and structure. Using traditional methods, previous studies had determined that, along this depth gradient, the heterogeneity of community spatial patterns increases, and their seasonal dynamics becomes dampened. We used a series of photographs (310 cm2 each) of permanent sites taken monthly over a one year period to analyze community spatial pattern. We tested a total of 17 landscape pattern indices that quantify different aspects of spatial pattern (patch size and shape characteristics, diversity, contagion and interspersion), for differences among communities, and for differences through time within each community. Results show clear differences in patch characteristics (number, mean size, size variability and shape), diversity, contagion and interspersion indices, among communities. In some cases, significant temporal patterns were also found, and these were consistent with the seasonal dynamics formerly described for each community. Generally, spatial pattern was less heterogeneous, but more variable seasonally, in the shallower, algae-dominated communities, than in deeper communities dominated by clonal animals. These results indicate the existence of community-related characteristic spatial patterns, and characteristic spatial pattern dynamics, in subtidal rocky benthic communities. Moreover, trends found in this study were in agreement with previous studies of spatial pattern in Mediterranean rocky benthic communities. Based on this study, we selected number of patches, mean patch size, standard deviation of patch size, mean shape patch index, and Shannons diversity index as the most suitable set of indices for the description of spatial pattern in Mediterranean subtidal rocky benthic communities.

Genetic survey of shallow populations of the Mediterranean red coral [Corallium rubrum (Linnaeus, 1758)]: new insights into evolutionary processes shaping nuclear diversity and implications for conservation

Combined action from over‐harvesting and recent mass mortality events potentially linked to ongoing climate changes has led to new concerns for the conservation of shallow populations (5–60 m) of Corallium rubrum, an octocorallian that is mainly found in the Mediterranean Sea. The present study was designed to analyse population structure and relationships at different spatial scales (from 10s of meters to 100s of kilometres) with a focus on dispersal pattern. We also performed the first analysis of the distribution of genetic diversity using a comparative approach between regional‐clusters and samples. Forty populations dwelling in four distinct regions between 14 and 60 m in depth were genotyped using 10 microsatellites. Our main results indicate (i) a generalized pair‐sample differentiation combined with a weak structure between regional‐clusters; (ii) the occurrence of isolation by distance at the global scale, but also within two of the three analysed regional‐clusters; (iii) a high level of genetic diversity over the surveyed area with a heterogeneous distribution from regional‐cluster to sample levels. The evolutionary consequences of these results are discussed and their management implications are provided.

Nano to macroscale biomineral architecture of red coral (Corallium rubrum)

Abstract Different techniques have been used to characterize the physical and chemical structure of the red coral calcitic skeleton. A section normal to the axis of the skeleton shows a medullar zone surrounded by a circular domain composed of concentric rings. Growth rings are revealed by the cyclic variation of organic matter (OM) and Mg/Ca ratio. These growth rings are annual; thus, both OM and Mg/Ca ratio can be used to date red coral colonies. Growth rings display wavelets. The internal structure of each wavelet results from the stacking of layers with tortuous interfaces. Tortuosity is due to the presence of microprotuberances. Interfaces between layers may display sharp discontinuities indicative of interruption of the mineralizing process. SEM and TEM studies show that each layer is made of (1) fibers, organized or not in fan-shaped structures; and (2) submicrometer (apparently mono-) crystalline units. Fibers are superstructures made of submicrometer units possibly assembled by an oriented aggregation mechanism. HRTEM studies show that in spite of displaying single-crystal scattering behavior, the submicrometer crystalline units are made of 2-5 nm nanograins again possibly aggregated by a mechanism of oriented attachment. Thus, submicrometer crystalline units and polycrystalline fibers can be both defined as mesocrystals. The red coral skeleton is a hierarchically organized organic-inorganic composite that exhibits porosity and structural and compositional order on length scales from the nanoscale to the macroscale.

Community structure and frond size distribution of a deep water stand of Cystoseira spinosa (Phaeophyta) in the Northwestern Mediterranean

Populations of Cystoseira spinosa, an endemic Mediterranean brown alga, are restricted to deep water at undisturbed sites. The species composition of an old stand in the Scandola Marine Reserve (Corsica) at a depth of 26−29 m reflects the dominance of Cystoseira spinosa over other brown and red algae, with an average biomass of 450 g dw m−2, and a mean density of 28.8 plants m−2. The length of the main axis was chosen as a convenient parameter related to size. The number of secondary axes increases exponentially with the length of the main axis, suggesting the existence of environmental constraints (possibly hydrodynamism), which may impose severe restrictions on the unlimited growth of the main axis. The size pattern of the Cystoseira spinosa plants from the population studied showed a log-normal distribution, with the highest frequency within size classes of 9–15 cm (main axis length), and a maximum size of 44 cm. Areas devoid of adult Cystoseira plants and lacking other erect algae had a significantly ...

Multilevel modular mesocrystalline organization in red coral

Abstract Biominerals can achieve complex shapes as aggregates of crystalline building blocks. In the red coral skeleton, we observe that these building blocks are arranged into eight hierarchical levels of similarly (but not identically) oriented modules. The modules in each hierarchical level assemble into larger units that comprise the next higher level of the hierarchy, and consist themselves of smaller, oriented modules. EBSD and TEM studies show that the degree of crystallographic misorientation between the building blocks decreases with decreasing module size. We observe this organization down to a few nanometers. Thus, the transition from imperfect crystallographic order at millimeter scale to nearly perfect single crystalline domains at nanometer scale is progressive. The concept of “mesocrystal” involves the three-dimensional crystallographic organization of nanoparticles into a highly ordered mesostructure. We add to this concept the notion of “multilevel modularity.” This modularity has potential implications for the origin of complex biomineral shapes in nature. A multilevel modular organization with small intermodular misorientations combines a simple construction scheme, ruled by crystallographic laws, with the possibility of complex shapes. If the observations we have made on red coral extend to other biominerals, long-range crystallographic order and interfaces at all scales may be key to how some biominerals achieve complex shapes adapted to the environment in which they grow.

Growth of Mesophyllum alternans and Lithophyllum frondosum (Corallinales, Rhodophyta) in the northwestern Mediterranean

Growth parameters of Mesophyllum alternans and Lithophyllum frondosum were studied in the northwestern Mediterranean. Growth and shrinkage rates, in terms of area gained or lost per month, were measured for both crustose corallines over a 2 year period by photographic and computer-assisted image analysis. No seasonal pattern in growth or shrinkage was found for either species. M. alternans grew and shrank at significantly higher rates than L. frondosum. Growth rates for both species were over an order of magnitude lower than those previously reported for other Mediterranean and tropical species, and were similar to reports for crustose corallines in Arctic and temperate waters. Almost 50% of monitored M. alternans thalli underwent at least one fission or fusion event over the 2 year monitoring period, while in L. frondosum these events were rarely observed. Interspecific differences in rates of growth, shrinkage, fission and fusion appear to depend on differences in thallus thickness (M. alternans is thin and L. frondosum is thick). These differences were interpreted as distinct biological strategies of persistence and the occupation of primary substratum.