Consequences of Mediterranean warming events in seagrass (Posidonia oceanica) flowering records

Posidonia oceanica, a seagrass endemic to the Mediterranean forms extended and extremely persistent meadows. It is a clonal plant with an apparently irregular pattern of flowering events. An extensive bibliographic review allowed the reconstruction of past flowering events of this species around the Mediterranean, with a high degree of confidence for the last 30 years. The data series on annual flowering prevalence (FP, flowering records per total records) and flowering intensity (FI, fraction of flowering shoots) produced have been compared with four series on Sea Surface annual Temperature maxima (SST_max) obtained for the NW Mediterranean (averaged from the local data series of l'Estartit and Villefranche: 1957–2005) and for the Eastern, Western basin and the whole Mediterranean sea (extracted from NCEP Reynolds interpolated SST maps: 1982–2005). Significant warming trends are detected in the Mediterranean SST_max series, at a rate of (mean+SE) 0.04±0.01°C yr⁻¹ (R²=0.24, P<0.01, N=24 years), in the Eastern basin series (0.06±0.01°C yr⁻¹, R²=0.43, P<0.001, N=24 years) and in the long SST_max series of the NW Mediterranean (0.02±0.01 C yr⁻¹, R²=0.12, P<0.02, N=49 years). The magnitudes of the SST_max anomalies around the absolute warming trend do not increase with time in any SST_max series. Peaks of FP and FI in the Mediterranean seem to occur each 9–11 years, and coincide with peaks of annual SST_max. Annual FP and FI increase with the residuals of annual SST_max warming trend in all Mediterranean basins (FP_MED: R²=0.27, P<0.01, N=23; FP_NW: R²=0.34, P<0.01, N=31; FP_E: R²=0.20; P<0.10, N=23). An outstanding event of P. oceanica flowering across the Mediterranean has been registered in Autumn 2003; 1 month after the highest annual SST_max recorded in the series. The hypothesis of flowering induction by thermal stress as the possible cause of this relationship is discussed, as well as the potential use of P. oceanica flowering record as early indicator of biological change induced by global sea warming in Mediterranean marine ecosystems.     

Genetic Polymorphism and Transplantation Success in the Mediterranean Seagrass Posidonia oceanica

We studied the role of genetic variability of donor beds in establishing transplantation criteria for the Mediterranean seagrass Posidonia oceanica. Horizontal rhizomes, collected from three geographically distinct populations, were transplanted into a common bed at a highly human‐impacted locality. The transplantation site was located near one of the donor populations. After three years, the shoots collected in the population adjacent to the transplanting site showed the lowest growth performance. Genetic variability, assessed through the analysis of hypervariable microsatellite regions, and growth performance followed a similar trend. The shoots growing and branching at the highest rate were those collected from populations with the highest heterozygosity values, despite greater geographic distance. No genetic differences were found between the transplanted shoots and shoots from donor meadows, as expected due to the low rate of sexual reproduction in P. oceanica and the short time that had passed since the transplants. The problem of affecting the local gene pool by the introduction of foreign genotypes could arise, but introduction of new alleles could balance the degradation of genetic variability caused by human impact. In general our study suggests that the genetic variability of source material is an important aspect to consider in the development of seagrass restoration strategies.     

Genetic structure in the Mediterranean seagrass Posidonia oceanica: disentangling past vicariance events from contemporary patterns of gene flow

The Mediterranean Sea is a two‐basin system, with the boundary zone restricted to the Strait of Sicily and the narrow Strait of Messina. Two main population groups are recognized in the Mediterranean endemic seagrass Posidonia oceanica, corresponding to the Western and the Eastern basins. To address the nature of the East–West cleavage in P. oceanica, the main aims of this study were: (i) to define the genetic structure within the potential contact zone (i.e. the Strait of Sicily) and clarify the extent of gene flow between the two population groups, and (ii) to investigate the role of present water circulation patterns vs. past evolutionary events on the observed genetic pattern. To achieve these goals, we utilized SSR markers and we simulated, with respect to current regime, the possible present‐day dispersal pattern of Posidonia floating fruits using 28‐day numerical Lagrangian trajectories. The results obtained confirm the presence of the two main population groups, without any indices of reproductive isolation, with the break zone located at the level of the Southern tip of Calabria. The populations in the Strait of Sicily showed higher affinity with Western than with Eastern populations. This pattern of genetic structure probably reflects historical avenues of recolonization from relict glacial areas and past vicariance events, but seems to persist as a result of the low connectivity among populations via marine currents, as suggested by our dispersal simulation analysis.     

Vicariance patterns in the Mediterranean Sea: east–west cleavage and low dispersal in the endemic seagrass Posidonia oceanica

Aim The seagrass, Posidonia oceanica is a clonal angiosperm endemic to the Mediterranean Sea. Previous studies have suggested that clonal growth is far greater than sexual recruitment and thus leads to low clonal diversity within meadows. However, recently developed microsatellite markers indicate that there are many different genotypes, and therefore many distinct clones present. The low resolution of markers used in the past limited our ability to estimate clonality and assess the individual level. New high‐resolution dinucleotide microsatellites now allow genetically distinct individuals to be identified, enabling more reliable estimation of population genetic parameters across the Mediterranean Basin. We investigated the biogeography and dispersal of P. oceanica at various spatial scales in order to assess the influence of different evolutionary factors shaping the distribution of genetic diversity in this species. Location The Mediterranean. Methods We used seven hypervariable microsatellite markers, in addition to the five previously existing markers, to describe the spatial distribution of genetic variability in 34 meadows spread throughout the Mediterranean, on the basis of an average of 35.6 (± 6.3) ramets sampled. Results At the scale of the Mediterranean Sea as a whole, a strong east–west cleavage was detected (amova) . These results are in line with those obtained using previous markers. The new results showed the presence of a putative secondary contact zone at the Siculo‐Tunisian Strait, which exhibited high allelic richness and shared alleles absent from the eastern and western basins. F statistics (pairwise θ ranges between 0.09 and 0.71) revealed high genetic structure between meadows, both at a small scale (about 2 to 200 km) and at a medium scale within the eastern and western basins, independent of geographical distance. At the intrameadow scale, significant spatial autocorrelation in six out of 15 locations revealed that dispersal can be restricted to the scale of a few metres. Main conclusions A stochastic pattern of effective migration due to low population size, turnover and seed survival is the most likely explanation for this pattern of highly restricted gene flow, despite the importance of an a priori seed dispersal potential. The east–west cleavage probably represents the outline of vicariance caused by the last Pleistocene ice age and maintained to this day by low gene flow. These results emphasize the diversity of evolutionary processes shaping the genetic structure at different spatial scales.     

Spatial patterns of genetic diversity in Posidonia oceanica, an endemic Mediterranean seagrass

Posidonia oceanica is an endemic seagrass species in the Mediterranean Sea. In order to assess levels of genetic structure in this species, the microsatellite polymorphism was analysed from meadows collected in several localities, along the coasts of the Tyrrhenian Sea (Mediterranean Sea). The existence of single population units and the recruitment of seedlings collected in some localities were investigated. Moreover, genetic structure at different spatial scales and biogeographic relationships among populations were also assessed. Our analysis showed the existence of clear patterns of genetic structure in P. oceanica in the area considered in the analysis. P. oceanica, in fact, is present in separate meadows that represent discrete populations, characterized by low genetic diversity. Comparable levels of genetic variability between mature meadows and seedlings were found. Patterns of genetic relatedness among populations seem to be in accord with direction of dominant current flux in the whole area, separating South Tyrrhenian from North Tyrrhenian populations. Moderate levels of gene flow between populations and genetic substructure within populations, together with the finding of the limited role of sexual reproduction in increasing genetic variability, should be a cause for concern for the persistence of this essential resource in the Mediterranean basin.     

Natural rock roughness as a key parameter for optimizing seedling adhesion and restoration of the seagrass Posidonia oceanica in its native environment

Seagrasses provide various ecosystem functions in coastal areas of the world. In the Mediterranean Sea, Posidonia oceanica is an endemic species threatened by several activities despite being protected by national and international laws. Currently, several transplanting initiatives have been carried out using different methods, among which those including seeds and seedlings are considered the most ecological and low-cost ones. Beach-cast fruits and seeds can be found in spring and their appearance can easily be reported, through a citizen science approach, by the community. One of the obstacles in using these methods is identifying the best substrate in which to place P. oceanica seeds to facilitate root adhesion of the seedlings prior to their transplantation into the sea. In the present study, we analyzed, using a 3D surface optical microscope, the roughness of natural rocks to identify the availability of specific roughness ranges suitable for adhesion and root anchoring of P. oceanica seedlings. Conventional roughness parameters and roughness power spectral density were calculated for the inner and outer surfaces of 9 different rock samples. Among the rock samples examined, the calcarenitic ones and in particular marsala calcarenite, due to the presence of the “ideal roughness for seedlings” can be considered one of the best consolidated substrates to be used for the construction of ad hoc devices on which plantlet of P. oceanica can grow for the purpose of restoration.     

La Posidonia oceanica: problemi di ecologia,di funzionamento e di biologia

Abstract

The functional roles of seagrasses in the economy of coastal waters are to be fully realised and more clearly delineated. The biology, ecology and energetics of seagrasses meadows of the Mediterranean Sea, and in particular of Posidonia oceanica inclusing the stabilization of coastal sediments, this role as a base for major detrital food chains, nutrient resources contributory to general productivity of the open sea and the support of dense epiphytic communities, are discussed.     

Microwave-assisted extraction and pharmacological evaluation of polysaccharides from Posidonia oceanica

Microwave-assisted extraction was employed for the isolation of polysaccharides from Posidonia oceanica (PPO). The extracting parameters were optimized adopting response surface methodology. The highest polysaccharide yield (2.55 ± 0.09%), which is in concordance with the predicted value (2.76%), was obtained under the following conditions: extraction time 60 s, liquid–solid ratio of 50:1 (mL/g) and power of 800 W. This polysaccharide, with molecular weight of 524 KDa, characterized by gas chromatography–mass spectrometry showed that PPO was mainly composed of galactose, glucose, and arabinose with molar percentages 25.38, 24.37, and 21.64%, respectively. The pharmacological evaluation of PPO using animal models at the dose of 100 mg/kg indicated a significant anti-inflammatory activity with a percentage of inhibition of edema of 54.65% and a significant antinociceptive activity with 78.91% inhibition of writhing for peripheral analgesic activity and an increase in the hot plate reaction time for central analgesic activity.     

Microbial colonization in the seagrass Posidonia spp. roots

The pattern of colonization by microorganisms on root surfaces from three species of seagrass belonging to the genus Posidonia was assessed. Microbial abundance on roots was measured by two electronic microscope techniques. Trends in microbial colonization between species and root order were defined. In addition, eutrophication status of the sampling sites and physiological status of Posidonia oceanica (L.) Delile roots have been taken into account. Our results show high microbial abundance in the Mediterranean species P. oceanica, in comparison with the low rates of colonization found in the Australian species P. australis Hook f. and P. sinuosa Cambridge et Kuo. Microbial density tended to decrease as root order increased, and living roots always showed higher microbial abundance than dead ones. Colonization of P. oceanica roots at the three sites with different environmental status follows different trends according to root order. It is suggested that root age influences the rate of microbial colonization of seagrass roots and that colonization of root surface by microorganisms is associated with organic exudates from the roots rather than with decaying root tissues.     

Distribution,structure and phenology of Posidonia oceanica meadows along sicilian coasts

Abstract

Distribution, structure and phenology of Posidonia oceanica meadows along Sicilian coasts are reported. Posidonia beds are frequently found in Sicily, especially along the south-eastern, north-western and western coasts. Leaf surface per shoot is identified as the most important variable among the phenological parameters. The rhizomes annual mean primary production turned out to be among the highest values observed in the Mediterranean Sea. Flowering and fruiting of Posidonia oceanica are frequent and can occur every year.     

New microsatellite markers for the endemic Mediterranean seagrass Posidonia oceanica

The seagrass Posidonia oceanica is endemic to the Mediterranean Sea, where it plays an important role in coastal ecosystem dynamics. Because of this important role and concerns about the observed regression of some meadows, population genetic studies of this species have been promoted. However, the markers used until now were not polymorphic enough to efficiently assess the level and spatial pattern of genetic variability. Hypervariable molecular markers were obtained by screening a genomic library enriched for microsatellite dinucleotide repeats. Among 25 primer pairs defined, eight amplified polymorphic microsatellites with an encouraging level of variability at the two geographical scales sampled.     

Sulfur cycling and seagrass (Posidonia oceanica) status in carbonate sediments

Sulfur cycling was investigated in carbonate-rich and iron-poor sediments vegetated with Posidonia oceanica in oligotrophic Mediterranean around Mallorca Island, Spain, to quantify sulfate reduction and pools of sulfide in seagrass sediments. The oxygen penetration depth was low (< 4.5 mm) and sulfate reduction rates were relatively high (0.7–12 mmol m^–2d^–1). The total pools of reduced sulfides were remarkably low (< 5 mol S m^–2) indicating a fast turnover of reduced sulfides in these iron-poor sediments. The sulfate reduction rates were generally higher in vegetated compared to bare sediments possible due to enhanced sedimentation of sestonic material inside the seagrass meadows. The sulfate reduction rates were positively correlated with the seasonal variation in water temperature and negatively correlated with the shoot density indicating that the microbial activity was controlled by temperature and release of oxygen from the roots. The pools of reduced sulfides were low in these iron-poor sediments leading to high oxygen consumption for reoxidation. The sediments were highly anoxic as shown by relatively low oxygen penetration depths (< 4.5 mm) in these low organic sediments. The net shoot recruitment rate was negative in sediments enriched with organic matter, suggesting that organic matter enrichment may be an important factor for seagrass status in these iron-depleted carbonate sediments.     

Genetic input by Posidonia oceanica (L.) Delile fruits dispersed by currents in the Ligurian Sea

Abstract

An external genetic input of Posidonia oceanica fruits dispersed by currents in the Ligurian Sea (Western Mediterranean) was investigated. During 2003–2004, when a massive fruiting event occurred, fruits were collected from plants at Monterosso al Mare (meadow) and compared with stranded fruits sampled in front of the meadow and downcurrent in Tuscany along 80 km of the coast. After their growth in culture, the plants were analysed using 10 random amplified polymorphic DNA (RAPD) molecular markers. Cluster analysis of similarity showed four distinct genetic populations. One group included parental plants from Monterosso and stranded fruits with the same genetic traits. The second group was formed by fruits stranded in the southern sector (Tuscany), and the third and the fourth groups were samples taken onshore, in front of the meadow, which appeared very different from the other two groups. Results evidenced the probability of the arrival of a new genetic population of nearly 40%, and it seems likely that the stranded fruits of external provenance did not come from the nearest P. oceanica meadows of Tuscany but were probably carried ashore by the Corsica current, as supported by an oceanographic analysis.     

Mediterranean warming triggers seagrass (Posidonia oceanica) shoot mortality

Rapid warming of the Mediterranean Sea threatens marine biodiversity, particularly key ecosystems already stressed by other impacts such as Posidonia oceanica meadows. A 6‐year monitoring of seawater temperature and annual P. oceanica shoot demography at Cabrera Archipelago National Park (Balearic Islands, Western Mediterranean) allowed us to determine if warming influenced shoot mortality and recruitment rates of seagrasses growing in relative pristine environments. The average annual maximum temperature for 2002–2006 was 1 °C above temperatures recorded in 1988–1999 (26.6 °C), two heat waves impacted the region (with seawater warming up to 28.83 °C in 2003 and to 28.54 °C in 2006) and the cumulative temperature anomaly, above the 1988–1999 mean annual maximum temperature, during the growing season (i.e. degree‐days) ranged between 0 °C in 2002 and 70 °C in 2003. Median annual P. oceanica shoot mortality rates varied from 0.067 year^?1 in 2002 to 0.123 year^?1 in 2003, and exceeded recruitment rates in all stations and years except in shallow stations for year 2004. Interannual fluctuations in shoot recruitment were independent of seawater warming (P>0.05). P. oceanica meadows experienced a decline throughout the study period at an average rate of ?0.050±0.020 year^?1. Interannual variability in P. oceanica shoot mortality was coupled (R²>0.40) to seawater warming variability and increasing water depth: shoot mortality rates increased by 0.022 year^?1 (i.e. an additional 2% year^?1) for each additional degree of annual maximum temperature and by 0.001 year^?1 (i.e. 0.1% year^?1) for each accumulated degree water temperature remained above 26.6 °C during the growing season. These results demonstrate that P. oceanica meadows are highly vulnerable to warming, which can induce steep declines in shoot abundance as well indicating that climate change poses a significant threat to this important habitat.     

A meta‐analysis reveals a positive correlation between genetic diversity metrics and environmental status in the long‐lived seagrass Posidonia oceanica

The seagrass Posidonia oceanica is a key engineering species structuring coastal marine systems throughout much of the Mediterranean basin. Its decline is of concern, leading to the search for short‐ and long‐term indicators of seagrass health. Using ArcGIS maps from a recent, high‐resolution (1–4 km) modelling study of 18 disturbance factors affecting coastal marine systems across the Mediterranean (Micheli et al. 2013, http://globalmarine.nceas.ucsb.edu/mediterranean/ ), we tested for correlations with genetic diversity metrics (allelic diversity, genotypic/clonal diversity and heterozygosity) in a meta‐analysis of 56 meadows. Contrary to initial predictions, weak but significantly positive correlations were found for commercial shipping, organic pollution (pesticides) and cumulative impact. This counterintuitive finding suggests greater resistance and resilience of individuals with higher genetic and genotypic diversity under disturbance (at least for a time) and/or increased sexual reproduction under an intermediate disturbance model. We interpret the absence of low and medium levels of genetic variation at impacted locations as probable local extinctions of individuals that already exceeded their resistance capacity. Alternatively, high diversity at high‐impact sites is likely a temporal artefact, reflecting the mismatch with pre‐environmental impact conditions, especially because flowering and sexual recruitment are seldom observed. While genetic diversity metrics are a valuable tool for restoration and mitigation, caution must be exercised in the interpretation of correlative patterns as found in this study, because the exceptional longevity of individuals creates a temporal mismatch that may falsely suggest good meadow health status, while gradual deterioration of allelic diversity might go unnoticed.     

Seed and early plantlet structure of the Mediterranean seagrass Posidonia oceanica

Seeds from mature fruits of the Mediterranean seagrass Posidonia oceanica deposited in the intertidal zone by sea surface currents revealed an advanced state of embryo development. The fruit dehisces by three longitudinal openings, which originate from the base or point of fruit attachment. Within the fruit the seed is positioned with its radical end at the fruit base, and the apical or plumular end protected until the seed is completely released. Structural observations of the collected mature seeds suggest the possible onset of germination. The mature seed is characterized by an enlarged hypocotyl with abundant starch reserves, a well-defined vascular system with a predominant central vascular strand to mobilize those reserves, a well-developed plumule, and root system initials, which will assure anchorage to the sea floor. Thus, within the dispersal unit, the future plant organs and growing points are well established and the carbohydrate-rich endosperm will assure the availability of sufficient nutrient supplies for short-term development of the seedling.     

Comparison of Cocconeis pseudonotata sp. nov. with two closely related species,C. notata and C. diruptoides,from Posidonia oceanica leaves

Three Cocconeis Ehrenberg species, epiphytic on the leaves of Posidonia oceanica (L.) Delile, were studied by light and electron microscopy. A new species, C. pseudonotata, is described which is closely related to C. notata Petit and C. diruptoides Hustedt. Gross morphology and the presence of a sigmoid raphe and sternum are the characters shared by the three species, whereas the central areas of sternum and raphe-sternum valves, and the stria and areola densities are the main distinctive characters for the species when observed by light microscopy. Scanning and transmission electron microscopic observations revealed that the fine structure of areolae must be also considered in order to identify the species. Comparison among the three species has been carried out by observations on material from our samples, as well as on the type material of C. diruptoides and cleaned samples from the Hustedt collection. The study also provides new information on the geographical distribution of these species.     

Detrital stocks and dynamics of the seagrass Posidonia oceanica (L.) Delile in the Spanish Mediterranean

Previous studies have shown that most leaf production (>90%) of the seagrass Posidonia oceanica is shed after senescence and that a substantial percentage (up to 80%) may thereafter be exported off the seagrass meadows by waves and currents. It has also been reported that P. oceanica meadows can accumulate large stocks of belowground detritus due to slow decomposition rates. However, the generality of these results across broad spatial scales is poorly known. In this report, we examine the fate of leaf production and the magnitude and dynamics of belowground detritus in 16 P. oceanica meadows distributed along the Spanish Mediterranean. Herbivores removed a small percentage of leaf production in all the meadows (≤13%), with most leaf production (>85%) being shed after senescence. Most shed leaves (>90%) were exported off the meadows by physical agents, such as waves and currents. The amount of belowground detritus stored within 10–15 cm from the sediment surface varied from ca. 70 to 7500 g DW m⁻² among the meadows examined, and they accumulated at rates ranging from ca. 65 to 650 g DW m⁻² per year. These values are large when compared to other communities of aquatic and terrestrial macrophytes. Our results show that P. oceanica meadows in the Spanish Mediterranean support high values of secondary production in other systems by exporting large amounts of leaf detritus as well as acting as substantial carbon sinks by accumulating large reservoirs of belowground detritus. Therefore, the increasing anthropogenic threats on P. oceanica could entail an important loss of secondary production and carbon storage in Mediterranean coastal ecosystems.