Macroecological analysis of the fish fauna inhabiting Cymodocea nodosa seagrass meadows

In this study, patterns in the taxonomic richness and composition of the fish fauna inhabiting Cymodocea nodosa seagrass meadows were described across their entire distribution range in the Mediterranean Sea and adjacent Atlantic Ocean. Specifically, the study tested whether there are differences in the composition of fish assemblages between those ecoregions encompassed by the distribution range of C. nodosa, and whether these differences in composition are connected with differences in bioclimatic affinities of the fish faunas. A literature review resulted in a total of 19 studies, containing 22 fish assemblages at 18 locations. The ichthyofauna associated with C. nodosa seagrass meadows comprises 59 families and 188 species. The western Mediterranean (WM) Sea has the highest species richness (87 species). Fish assemblages from the Macaronesia–Canary Islands, the Sahelian Upwelling, South European Atlantic Shelf and the WM differ, in terms of assemblage composition, relative to other ecoregions. In contrast, the composition of the fish fauna from the central and eastern Mediterranean overlaps. There is a significant serial correlation in fish assemblage composition between adjacent ecoregions along the distribution range of C. nodosa. Dissimilarities in assemblage composition are connected with the geographical separation between locations, and the mean minimum annual seawater temperature is the environmental factor that explains most variation in fish assemblage composition.     

Isolation and characterization of microsatellite markers for the seagrass Cymodocea nodosa

In order to study the spatial patterns of genetic diversity of a clonal marine angiosperm, the seagrass Cymodocea nodosa, microsatellite markers were obtained by screening a genomic library enriched for the (CT) dinucleotide motif. Of 38 primer pairs defined, 15 amplified polymorphic microsatellites and are described. These loci identified a number of alleles ranging from two to seven, and showed expected heterozygosity ranging from 0.35 to 0.76, when a group of 40 individuals from Cadiz Bay in Spain was analysed. Additionally, we describe here the multiplexing conditions for 12 of these loci.     

Within-population spatial genetic structure, neighbourhood size and clonal subrange in the seagrass Cymodocea nodosa

Abstract The extent of clonality within populations strongly influences their spatial genetic structure (SGS), yet this is hardly ever thoroughly analysed. We employed spatial autocorrelation analysis to study effects of sexual and clonal reproduction on dispersal of the dioecious seagrass Cymodocea nodosa. Analyses were performed both at genet level (i.e. excluding clonal repeats) and at ramet level. Clonal structure was characterized by the clonal subrange, a spatial measure of the linear limits where clonality still affects SGS. We show that the clonal subrange is equivalent to the distance where the probability of clonal identity approaches zero. This combined approach was applied to two meadows with different levels of disturbance, Cadiz (stable) and Alfacs (disturbed). Genotypic richness, the proportion of the sample representing distinct genotypes, was moderate (0.38 Cadiz, 0.46 Alfacs) mostly due to dominance of a few clones. Expected heterozygosities were comparable to those found in other clonal plants. SGS analyses at the genet level revealed extremely restricted gene dispersal in Cadiz (Sp = 0.052, a statistic reflecting the decrease of pairwise kinship with distance), the strongest SGS found for seagrass species, comparable only to values for selfing herbaceous land plants. At Cadiz the clonal subrange extended across shorter distances (20-25 m) than in Alfacs (30-35 m). Comparisons of sexual and vegetative components of gene dispersal suggest that, as a dispersal vector within meadows, clonal spread is at least as important as sexual reproduction. The restricted dispersal and SGS pattern in both meadows indicates that the species follows a repeated seedling recruitment strategy.     

A baseline for prioritizing the conservation of the threatened seagrass Cymodocea nodosa in the oceanic archipelago of Madeira

Seagrasses are experiencing fragmentation and regression globally; thus, protection and recovery of meadows are a preservation priority. However, conservation actions must consider inherent regional conditions, since certain coastal areas are not suitable for the settlement of extensive meadows. Likewise, small oceanic archipelagos are not always able to fulfil the habitat requirements of seagrass habitats but can harbour small patches that in turn provide unique research opportunities. In this study, we focused on the seagrass Cymodocea nodosa in the archipelago of Madeira (NE Atlantic Ocean). Here we compile historical and contemporary records of this species along with characterization of associated communities (fish and invertebrates). A bionomic map with potentially suitable areas for the establishment and settlement of this species is also included. Lastly, we highlight coastal management and restoration actions and future research directions to preserve this species in Madeira Island.     

Genetic differentiation and secondary contact zone in the seagrass Cymodocea nodosa across the Mediterranean–Atlantic transition region

Aim A central question in evolutionary ecology is the nature of environmental barriers that can limit gene flow and induce population genetic divergence, a first step towards speciation. Here we study the geographical barrier constituted by the transition zone between the Atlantic Ocean and the Mediterranean Sea, using as our model Cymodocea nodosa, a seagrass distributed throughout the Mediterranean and in the Atlantic, from central Portugal to Mauritania. We also test predictions about the genetic footprints of Pleistocene glaciations. Location The Atlantic–Mediterranean transition region and adjacent areas in the Atlantic (Mauritania to south‐west Portugal) and the Mediterranean. Methods We used eight microsatellite markers to compare 20 seagrass meadows in the Atlantic and 27 meadows in the Mediterranean, focusing on the transition between these basins. Results Populations from these two regions form coherent groups containing several unique, high‐frequency alleles for the Atlantic and for the Mediterranean, with some admixture west of the Almeria–Oran Front (Portugal, south‐west Spain and Morocco). These are populations where only one or a few genotypes were found, for all but Cadiz, but remarkably still show the footprint of a contact zone. This extremely low genotypic richness at the Atlantic northern edge contrasts with the high values (low clonality) at the Atlantic southern edge and in most of the Mediterranean. The most divergent populations are those at the higher temperature range limits: the southernmost Atlantic populations and the easternmost Mediterranean, both potential footprints of vicariance. Main conclusions A biogeographical transition region occurs close to the Almeria–Oran front. A secondary contact zone in Atlantic Iberia and Morocco results from two distinct dispersal sources: the Mediterranean and southernmost Atlantic populations, possibly during warmer interglacial or post‐glacial periods. The presence of high‐frequency diagnostic alleles in present‐day disjunct populations from the southernmost Atlantic region indicates that their separation from all remaining populations is ancient, and suggests an old, stable rear edge.     

Molecular cloning and functional expression in bacteria of the potassium transporters CnHAK1 and CnHAK2 of the seagrass Cymodocea nodosa

The cDNAs CnHAK1 and CnHAK2, encoding K⁺ transporters, were amplified from the leaves of the seagrass Cymodocea nodosa. None of these transporters suppressed the K⁺ deficiency of a Saccharomyces cerevisiae mutant, but both suppressed the equivalent defect of an Escherichia coli mutant. Overexpression of the transporter CnHAK1, but not CnHAK2, mediated very rapid K⁺ or Rb⁺ influxes in the E. coli mutant. The concentration dependence of these influxes demonstrated that CnHAK1 is a low-affinity K⁺ transporter, which does not discriminate between K⁺ and Rb⁺. CnHAK1 expressed in E. coli worked in reverse when the external K⁺ concentrations were low, and we established the condition of a simple functional test of K⁺ loss for transporters of the Kup-HAK family. In comparison with its homologue barley transporter HvHAK2, CnHAK1 was insensitive to Na⁺.     

Nutrient availability in the sediment and the reciprocal effects between the native seagrass Cymodocea nodosa and the introduced rhizophytic alga Caulerpa taxifolia

Two reciprocal experiments testing for the effects of nutrient addition in the sediment and competitive interactions between the native seagrass Cymodocea nodosa (Ucria) Ascherson and the introduced alga Caulerpa taxifolia (Vahl) C. Agardh were performed. This study was conducted for 13 months (August 1995 until September 1996) in a bay on the south coast of Elba Island (Italy). Each experiment consisted of the manipulation of the level of nutrients (addition vs. control) and the manipulation of the neighbours (presence vs. removal). Response variables were blade density and size for one experiment and shoot density and leaf length of seagrass in the other. Results indicated that the presence of Caulerpa taxifolia did not affect significantly Cymodocea nodosa shoot density and the increased nutrient availability in the sediment did not alter this pattern. Neither the removal of the canopy of the seagrass nor the fertilization of the sediment has influenced significantly the density of the alga. Both species, where co-occurring, show larger size than where the neighbour is removed. Hence, results of this study suggest that the two species on the long term are likely to coexist and that the high nutrient supply of the sediment would not enhance the probability of success neither of the seagrass nor of the alga. Predictions made on the basis of short-term results, that high nutrient loads of the substratum would have represented an even more suitable condition for C. taxifolia to colonize C. nodosa beds and that on the long-term the alga has a high probability of success, did not occur.     

Polymorphic microsatellite loci for the marine angiosperm Cymodocea nodosa

The seagrass Cymodocea nodosa (UCRIA) Ascherson represents a good model to assess the relative contribution of clonal and sexual reproduction to genetic structure in marine plant populations. Seven microsatellite loci with repeat units consisting of one trinucleotide, four simple dinucleotides and two complex dinucleotides are described here. The seven loci are characterized by high number of alleles (from three to 13) and high heterozygosity (H_O ranging from 0.240 to 0.860) in the tested populations. Conditions for multiplex polymerase chain reactions are also described.     

3-Keto steroids from the marine organisms Dendrophyllia cornigera and Cymodocea nodosa

The new (20R)-22E-cholesta-4,22-diene-3,6-dione (1), along with three known 3-keto steroids were isolated from the deep-water Mediterranean scleractinian coral Dendrophyllia cornigera (2-4). Moreover, four known related 3-keto steroids were isolated from the sea grass Cymodocea nodosa (5-8). The structure elucidation of steroid 1 and the full NMR resonance assignments of all isolated metabolites were based on interpretation of their spectral data. All compounds are reported for the first time as metabolites of the investigated organisms. Compounds 2 and 3 showed significant cytotoxicity against lung cancer NSCLC-N6 cell line.     

Cymodocea nodosa metrics as bioindicators of anthropogenic stress in N. Aegean,Greek coastal waters

Anthropogenic derived stressors are known to affect seagrasses. Cymodocea nodosa, a widespread seagrass in the Mediterranean Sea with high phenotypic plasticity, is known to acclimatize rapidly to prevailing environmental conditions. To use this species in the biomonitoring of anthropogenic stress, physiological (effective quantum yield of photosystem II [ΔF/Fm′], maximum quantum yield [Fv/Fm], and maximum fluorescence [Fm]), phenological (leaf length and width, number of leaves per shoot), and biochemical (Chl-a, and Carbon, Nitrogen, Phosphorus contents of leaves) metrics were measured between two meadows under different levels of anthropogenic influence in the Kavala Gulf, North Aegean Sea. To reduce bias and separate seasonality from anthropogenic stress responses the physiological parameters were measured under constant laboratory conditions and a hierarchical sampling design was employed. Two well-described meadows, one pristine (Brasidas) and one under significant anthropogenic stress (Nea Karvali), were sampled on six occasions between June 2007 and March 2009 at three spatial scales ranging from hundreds of meters (area) to kilometer (site) to 10s of kilometers (meadow). Of the twelve metrics measured, N-content and Fm were the most effective at discriminating between the two C. nodosa meadows and, therefore, should be considered as promising bioindicators. Statistically significant differences were identified between the cold and hot periods for almost all metrics measured, suggesting that seasonality is a key driver of the observed responses.     

Three new interstitial dorvilleids (Annelida: Polychaeta) from the Cymodocea nodosa meadows of the Canary Islands

Resource–consumer relationships in Lake Victoria were investigated by use of stable isotope data. ¹³C and ¹⁵N signatures were determined for organisms at a deep (22 m) and a littoral (5 m) site in the Napoleon Gulf near Jinja, Uganda. Results suggest that two food chains operate at the deep site, one leading from a shrimp (Caridina nilotica) to juvenile Nile perch (Lates niloticus), the second leading from zooplankton (copepods and cladocerans) to a cyprinid (Rastrineobola argentea) and lake flies (Chaoborus). Isotopic evidence suggests that shrimp eat suspended particulates and benthos, not crustacean zooplankton or water hyacinth (Eichhornia crassipes). Resource–consumer relationships revealed in this study have implications for understanding future yields of the economically important Nile perch fishery.     

Genetic diversity and structure of the tropical seagrass Cymodocea serrulata spanning its central diversity hotspot and range edge

Aquatic Ecology - Persistence of populations at their distributional ranges relies on local population dynamics and the fitness of species with low dispersal potential. We analyzed the population...     

Comparison of the epifauna spatial distribution in Posidonia oceanica,Cymodocea nodosa and unvegetated bottoms: Importance of meadow edges

In order to detect the influence of seagrass, the most important habitats of shallow soft-bottom along the Mediterranean coast, on spatial distribution of epifauna, four different types of habitat were sampled: Posidonia oceanica, Cymodocea nodosa, edge of Posidonia meadow and sandy bottoms. Sampling was carried out, using the hand net method, in various random sites and at different times (April 95, August 95 and February 96) on the Alicante coast (SE Spain). A double taxonomic approach was used in order to detect spatial and temporal changes in the abundance of the main taxonomic groups and amphipod species. The differences among habitats were detected by non-parametric multidimensional scaling (MDS) for community structure and by analysis of variance for groups and amphipod populations. The community structure defined by the abundance of taxonomic groups was not significantly modified by the habitats. Single abundance of taxonomic groups also had no significant preference for the type of habitat except in the case of Acari, a group linked to Posidonia. However, certain trends of preference, such as mysids on Posidonia edge and isopods on Cymodocea, were detectable. On other hand, the amphipod assemblage showed important differences among habitats. Some species changed significantly in abundance depending on the habitat considered, e.g. Dexamine spiniventris and Perioculodes longimanus. It was possible to conclude that there is an important influence of Posidonia and Cymodocea on epifauna distribution by diversification of habitat structure on sandy bottoms, but it was more important at the species level than when considering taxonomic groups. Furthermore, sandy bottoms and the meadow edges had a relatively high importance on fauna distribution, depending on taxa and the period of the year.     

Composition and structure of the molluscan assemblage associated with a Cymodocea nodosa bed in south-eastern Spain: seasonal and diel variation

The molluscan taxocoenosis associated with a Cymodocea nodosa seagrass bed was studied throughout 1?year in Genoveses Bay, in the MPA “Parque Natural Cabo de Gata-Níjar” (south-eastern Spain). A total of 64,824 individuals were collected and 54 species identified. The molluscan fauna was mainly composed of gastropods (99.56% of individuals, 43 spp.). The families Rissoidae (72.98%, 11 spp.) and Trochidae (16.93%, 7 spp.) were the most abundant and diversified in terms of number of species. Rissoa monodonta (47.1% dominance), Rissoa membranacea (25.1%) and Gibbula leucophaea (11.6%) proved the top dominant species in both diurnal and nocturnal samples. Bivalves (0.41%, 10 species) and cephalopods (0.03%, 1 species) represented only a low percentage of the molluscan taxocoenosis. The molluscan assemblage was mainly composed of species with a wide geographical distribution in Europe, followed by strictly Mediterranean species. The abundance was significantly higher in the cold (December, March) than in the warm months (June, July). Species richness (S) was higher in nocturnal than in diurnal samples, reaching maximal values in diurnal samples of March and June. Shannon–Wiener diversity (H′) values were generally higher in nocturnal samples than in diurnal ones, displaying minimum values in December and June, respectively. Evenness was similar in diurnal and nocturnal samples, with maximum values in July in both groups. S and H′ were also significantly different between diurnal and nocturnal samples. Multivariate analyses based on both qualitative and quantitative data showed a significant seasonal and diel variation. Diel changes revealed to be more distinct than seasonal ones.     

Floral structure in the marine angiosperms Cymodocea serrulata and Thalassodendron ciliatum (Cymodocea ciliata)

Several female flowers were found on plants of Cymodocea serrulata collected in Mida Creek, Kenya, during August 1969. The structure of the female inflorescence of C. serrulata , previously known only from one fragmentary example, is described and shown to be very similar to that of C. angustata Ostenf. but different from that of Thalassodendron ciliatum. The occurrence of small squamulae intravaginales in all leaf and bract axils in both C. serrulata and T. ciliatum is described. Secondary male flowers were observed in the axil of the penultimate bract of about 10% of male inflorescences of T. ciliatum collected on the Kenya coast. The frequency of flowering and the factors affecting flowering in C. serrulata are discussed.     

Grazer diversity affects resistance to multiple stressors in an experimental seagrass ecosystem

When multiple stressors act simultaneously, their effects on ecosystems become more difficult to predict. In the face of multiple stressors, diverse ecosystems may be more stable if species respond differently to stressors or if functionally similar species can compensate for stressor effects on focal species. Many habitats around the globe are threatened by multiple stressors, including highly productive seagrass habitats. For example, in Chesapeake Bay, USA, regional climate change predictions suggest that elevated temperature and freshwater inputs are likely to be increasingly important stressors. Using seagrass mesocosms as a model system, we tested whether species richness of crustacean grazers buffers ecosystem properties against the impacts of elevated temperature and freshwater pulse stressors in a fully factorial experiment. Grazer species responded to pulsed salinity changes differently; abundance of Elasmopus levis responded negatively to freshwater pulses, whereas abundance of Gammarus mucronatus and Erichsonella attenuata responded positively or neutrally. Consistent with the hypothesis that biodiversity provides resistance stability, biomass of epiphytic algae that form the base of the food web was less affected by stressors in species‐rich grazer treatments than in single‐species grazer treatments. Stochastic (among‐replicate) variation of sessile invertebrate biomass within treatments was also reduced in more diverse grazer treatments. Therefore, grazer species richness tended to increase the resistance stability of both major components of the seagrass fouling community, algae and invertebrates, in the face of environmental stressors. Finally, in our model system, multi‐stressor impacts suggested a pattern of antagonism contrary to previous assumptions of synergistic stressor effects. Overall, our results confirm that invertebrate grazer species are functionally diverse in their response to environmental stressors, but are largely functionally redundant in their grazing effects leading to greater resistance stability of certain ecosystem properties in diverse grazer assemblages even when influenced by multiple environmental stressors.     

Biodiversity response to experimental induced hypoxic-anoxic conditions in seagrass sediments

The effects of induced hypoxic-anoxic conditions on the metazoan meiofaunal assemblages and nematode diversity were investigated with an in situ experiment in a Posidonia oceanica meadow. The experiment, of the duration of five months, was performed in three experimental sets of plots. Two of them were enriched with organic matter to induce anoxic conditions (1 set with sucrose and 1 set with sugar plus nutrients, i.e. nitrogen and phosphorus) whereas the last set of plots was kept undisturbed and used as Control. Metazoan meiofauna displayed a fast response to the induced anoxic conditions with an immediate reduction of the richness of taxa (only nematodes and copepods tolerated the hypoxic-anoxic conditions). Nematodes were the most tolerant organisms as their species richness did not change in hypoxic-anoxic conditions, but their species composition and trophic structure displayed significant changes. Some genera (Desmoscolex and Bolbolaimus) were replaced by other (Chromadorella, Sabatiera and Polysigma) more tolerant to the extreme conditions. No significant differences were observed in the Control plots, whereas in treated plots, selective deposit feeders and predators decreased significantly, being replaced by non-selective deposit feeders and epistrate feeders. These results indicate that, events causing a reduction in oxygen availability, can have an impact on the nematode beta-diversity and functional diversity with potential important implications on the benthic food web and functioning of the seagrass systems.     

Isolation and characterization of novel microsatellite markers for Cymodocea serrulata (Cymodoceaceae), a seagrass distributed widely in the Indo‐Pacific region

Cymodocea serrulata is a tropical seagrass species distributed widely in the Indo‐Pacific region. We developed 16 novel microsatellite (simple sequence repeat) markers for C. serrulata using next‐generation sequencing for use in genetic studies. The applicability of these markers was attested by genotyping of 40 individuals collected from a natural population in the Philippines. Of the 16 loci, 15 showed polymorphism. For the 15 polymorphic markers, the number of alleles per locus ranged from two to seven, and the observed and expected heterozygosities ranged from 0.131–1.000 and 0.124–0.788, respectively. These markers are useful tools for elucidating genetic diversity, connectivity, and structure in this foundational coastal species.     

Size matters: variations in seagrass seed size at local scales affects seed performance

Hydrobiologia - Seed size can have an impact on angiosperm reproductive fitness. Ecological theory predicts plants that will produce larger seeds in stressful environments to increase the chances...