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.     

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.     

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.     

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.     

Food sources of two detritivore amphipods associated with the seagrass Posidonia oceanica leaf litter

This study focused on the ingestion and assimilation of Posidonia oceanica (L.) Delile litter by Gammarella fucicola Leach and Gammarus aequicauda Martynov, two dominant detritivore amphipods of the P. oceanica leaf litter. Scanning electron microscope observations indicated that leaf litter is highly colonized by diverse diatoms, bacteria and fungi, which may constitute a potential food source for the litter fauna. Gut content observations demonstrated that these species eat P. oceanica litter, and that this item is an important part of their ingested diet. Stable isotope analyses showed that the species do not experience the same gains from the ingested Posidonia. Gammarella fucicola displayed isotopic values, suggesting a major contribution of algal material (micro- and macro-epiphytes or drift macro-algae). On the other hand, the observed isotopic values of G. aequicauda indicated a more important contribution of P. oceanica carbon. The mixing model used agreed with this view, with a mean contribution of P. oceanica to approximately 50% (range 40-55%) of the assimilated biomass of G. aequicauda. This demonstrated that the two species, suspected to be detritus feeders, display in reality relatively different diets, showing that a certain degree of trophic diversity may exist among the detritivore community of the seagrass litter.     

Variations in the concentration of phenolic compounds in the seagrass Posidonia oceanica under conditions of competition

The concentration of phenolic compound was measured in the seagrass Posidonia oceanica when interacting with two Bryopsidophyceae, Caulerpa taxifolia and Caulerpa racemosa, between May 1999 and May 2000. These measurements were performed on adult and intermediate leaves and in sheaths of the seagrass. Sampling was carried out at three stations subject to increasing levels of interaction with Caulerpa. The number of tannin cells was also analysed. Five phenolic compounds were identified in P. oceanica, with a predominance of caffeic acid in the adult and intermediate leaves. For a given level of interaction (and for both caulerpa sp.), a significant seasonal variation in phenolic compounds was shown in the adult leaves (higher in November and lower in September and March for example for the interaction with C. taxifolia). Only for two compounds (corresponding to a mixture containing ferulic acid and the ester methyl 12-acetoxyricinoleate) were significant differences observed as a function of the level of interaction with C. taxifblia, and only in the adult leaves: higher concentrations of phenols were observed with increasing level of interaction. Thus,adult leaves gave values of 55.5 +/- 14.1 microg g(-1) dm without interaction (OCt) and 94.9 +/- 23.4 microg g(-l) dm with high interaction (2Ct),corresponding to an increase of 70%. No significant difference was observed with intermediate leaves and sheaths, or for interaction with C. racemosa. The number of tannin cells (supposed to produce the phenolic compounds) largely increased in the adult and intermediate leaves when the degree of interaction with C. taxifolia increased: 90 mm above the base of the sheath (in adult leaves), 16.7 +/- 10.6 tannin cells cm(-2) were found without interaction (OCt), and 57.8 + 21.2 tannin cells cm(-2) with high interaction (2Ct). No significant difference was found for C. racemosa interaction. It thus appears that when the seagrass P. oceanica is in interaction with C. taxifolia, it accelerates its production of secondary metabolites so as to limit invasion of the beds.     

C, N, P concentrations and requirements of flowering Posidonia oceanica

The carbon, nitrogen and phosphorus contents in flowering and nonflowering shoots were compared after an important flowering event occurred in the Posidonia meadow of the Bay of Calvi. The flower formation caused a significant increase of C and a significant decrease of N concentrations in intermediate and adult leaves. Minimum daily requirements in mgshoot^-1day^-1 of 3.4 and 4.8 of C, 0.09 and 0.09 N, 0.01 and 0.02 of P respectively for nonflowering and flowering shoots were calculated. It shows that additional quantities of C and P are required for the inflorescence elaboration. The unchanged quantity of N required by the shoot for the inflorescence elaboration and the significant modification of N concentration in intermediate and adult leaves suggests that N is limited in the environment and that an efficient resorption of N occurs from leaves to ensure the inflorescence formation.     

Random amplified polymorphic DNA assessment of diversity in western Mediterranean populations of the seagrass Posidonia oceanica

Posidonia oceanica is an endemic Mediterranean seagrass species that has often been assumed to contain low levels of genetic diversity. Random amplified polymorfic DNA (RAPD) markers were used to assess genetic diversity among five populations from three geographical regions (north, central, and south) of the western Mediterranean Sea. Stranded germinating seeds from one of the central populations were also included in the analysis. Forty-one putative genets were identified among 76 ramets based on 28 RAPD markers. Genotypic diversity strongly depended on the spatial structure, age, and maturity of the meadows. The lowest clonal diversity was found in the less structured and youngest prairies. Conversely, a high genotypic diversity was found in the highly structured meadows. The genotypic diversity in these meadows was at the same level as in P. australis and higher than previously reported data for P. oceanica populations in the Tyrrhenian Sea near the coast of Italy.     

Unexpected response of the seagrass Posidonia oceanica to a warm-water episode in the north western Mediterranean Sea

The response of Posidonia oceanica (Linnaeus) Delile to the warm-water episode of summer 1999 was studied by means of the technique of lepidochronology. Study sites include three sites affected by the mass mortality event of benthic invertebrates and one not affected. The results showed a significant decline in some parameters (number of leaves and/or rhizome growth) for the three sites affected by the mass mortality event for the year following the warm-water episode (1999-2000). A similar decline was not observed for the unaffected site. The fact that high temperatures could have a negative impact on deep Posidonia oceanica near its cold limit of distribution is an unexpected result.     

Molecular level responses to chronic versus pulse nutrient loading in the seagrass Posidonia oceanica undergoing herbivore pressure

Oecologia - Seagrasses are key marine foundation species, currently declining due to the compounded action of global and regional anthropogenic stressors. Eutrophication has been associated with...     

Implications of extreme life span in clonal organisms: millenary clones in meadows of the threatened seagrass Posidonia oceanica

The maximum size and age that clonal organisms can reach remains poorly known, although we do know that the largest natural clones can extend over hundreds or thousands of metres and potentially live for centuries. We made a review of findings to date, which reveal that the maximum clone age and size estimates reported in the literature are typically limited by the scale of sampling, and may grossly underestimate the maximum age and size of clonal organisms. A case study presented here shows the occurrence of clones of slow-growing marine angiosperm Posidonia oceanica at spatial scales ranging from metres to hundreds of kilometres, using microsatellites on 1544 sampling units from a total of 40 locations across the Mediterranean Sea. This analysis revealed the presence, with a prevalence of 3.5 to 8.9%, of very large clones spreading over one to several (up to 15) kilometres at the different locations. Using estimates from field studies and models of the clonal growth of P. oceanica, we estimated these large clones to be hundreds to thousands of years old, suggesting the evolution of general purpose genotypes with large phenotypic plasticity in this species. These results, obtained combining genetics, demography and model-based calculations, question present knowledge and understanding of the spreading capacity and life span of plant clones. These findings call for further research on these life history traits associated with clonality, considering their possible ecological and evolutionary implications.     

The seagrass Posidonia oceanica as indicator of coastal water quality: Experimental intercalibration of classification systems

The pervasive use of ecological indices is increasingly requiring actions of harmonisation. Specifically, within the EU Water Framework Directive, an important effort in methods intercalibration is being done. However, a significant limitation in comparability assessment arises from the datasets used, which have different geographic origins. The purpose of our study was to perform an experimental intercalibration, where data were collected specifically on a set of common sites and following all the requirements of the methods being assessed. Three indices based on the marine angiosperm Posidonia oceanica, the POMI, the BiPo and the PoSte, were applied to sites in three different geographical areas of the western Mediterranean: Catalonia, Corsica and Southern Italy (Ischia), distant between hundreds and more than thousands of kilometers. Two indices, POMI and BiPo, showed not only a very good relationship with human pressures (measured on a common scale for all sites) but also a high comparability, in all aspects investigated. The differences found for the third one (PoSte) are hypothesised as being due to a different rationale used to define reference conditions, the different metrics used in the index, and in particular to a different definition of ecological status in relation to the time scale of the response to anthropogenic pressures. Our study demonstrates that indices with very different approaches can provide fully reliable and comparable results.     

A biotic index using the seagrass Posidonia oceanica (BiPo), to evaluate ecological status of coastal waters

The development of ecologically based indices that respond to disturbances in a predictable manner has been stressed by the EU Water Framework Directive. The seagrass Posidonia oceanica, given its ecological indicator characteristics, has been identified as one of the elements to determine ecological status under the EU Water Framework Directive. The purpose of this study is therefore to develop a biotic index based on P. oceanica (BiPo), focussing on: (i) the necessity of an index that may be applied over the largest geographical extent possible, (ii) the necessity of a tool for a baseline evaluation of P. oceanica status in the Mediterranean, (iii) the compliance with WFD requirements, (iv) the efficiency of the method in terms of reliability and cost. The BiPo index is developed on the basis of all P. oceanica monitoring data available in the western Mediterranean and on a standard assessment of anthropogenic pressures. The index metrics are selected and evaluated on the basis of this pressures assessment, and are subsequently integrated for the evaluation of ecological status. The index is then tested on 15 sites around Corsica (France). The results show that the BiPo well reflects meadow health status and ecological status. Furthermore it is reliable, standard and cost-effective, and can be applied to a wide array of management and conservation purposes.     

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.     

The growth and degeneration of the hydroid Sertularia perpusilla,an obligate epiphyte of leaves of the seagrass Posidonia oceanica

The hydrorhizae of Sertularia perpusilla colonies that originate from stolon attachments initially grow up and down Posidonia leaves. After a short time the distal hydroid tissue degenerates concurrently with the downward growth of the proximal hydrorhiza onto younger sections of the leaves. Consequently the hydroids move down the leaves which grow upward from a basal meristem. In situ inversion of leaves had no effect on either the orientation or the rates of growth and degeneration. This indicates that orientation may be in response to age related features of leaf tissue rather than to light, gravity or water movement, the directions of which were reversed by inverting the leaves. However, orientation of growth of new hydroids from attached stolons is immediate, probably before the hydroid colony is long enough to be able to detect an age gradient. This paradox could be explained if initial orientation were based on the direction of gravity or light but subsequent growth were directed along the age gradient. For hydroids in the size range studied there was a relation between growth rate and number of hydranths. Thus growth rate may be limited by food rather than by there being only one growing tip of the hydrorhizae.     

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.