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  • Light is more important than nutrient ratios of fertilization for cymodocea nodosa seedling development
    Publication . Alexandre, Ana; Silva, João; Santos, Rui
    Restoration of seagrass beds through seedlings is an alternative to the transplantation of adult plants that reduces the impact over donor areas and increases the genetic variability of restored meadows. To improve the use of Cymodocea nodosa seedlings, obtained from seeds germinated in vitro, in restoration programs, we investigated the ammonium and phosphate uptake rates of seedlings, and the synergistic effects of light levels (20 and 200 mu mol quanta m(-2) s(-1)) and different nitrogen to phosphorus molar ratios (40 mu M N:10 mu M P, 25 mu M N:25 mu M P, and 10 mu N:40 mu M P) on the photosynthetic activity and growth of seedlings. The nutrient content of seedlings was also compared to the seed nutrient reserves to assess the relative importance of external nutrient uptake for seedling development. Eighty two percent of the seeds germinated after 48 days at a mean rate of 1.5 seeds per day. All seedlings under all treatments survived and grew during the 4 weeks of the experiment. Seedlings of C. nodosa acquired ammonium and phosphate from the incubation media while still attached to the seed, at rates of about twice of adult plants. The relevance of external nutrient uptake was further highlighted by the observation that seedlings' tissues were richer in nitrogen and phosphorus than non-germinated seeds. The uptake of ammonium followed saturation kinetics with a half saturation constant of 32 mu M whereas the uptake of phosphate increased linearly with nutrient concentration within the range tested (5 - 100 mu M). Light was more important than the nutrient ratio of fertilization for the successful development of the young seedlings. The seedlings' photosynthetic and growth rates were about 20% higher in the high light treatment, whereas different nitrogen to phosphorus ratios did not significantly affect growth. The photosynthetic responses of the seedlings to changes in the light level and their capacity to use external nutrient sources showed that seedlings of C. nodosa have the ability to rapidly acclimate to the surrounding light and nutrient environment while still attached to the seeds. C. nodosa seedlings experiencing fertilization under low light levels showed slightly enhanced growth if nourished with a balanced formulation, whereas a slight increase in growth was also observed with unbalanced formulations under a higher light level. Our results highlight the importance of high light availability at the seedling restoration sites.
  • Nitrogen uptake in light versus darkness of the seagrass Zostera noltei: integration with carbon metabolism
    Publication . Alexandre, Ana; Silva, João; Santos, Rui
    We conducted a study that shows that light and dark conditions do not affect the uptake rates of ammonium and nitrate by the seagrass Zostera noltei. This is an important advantage over some seaweed species in which these rates are severely reduced at night. In the light, the ammonium uptake rates were initially higher (15 and 20molg(-1)h(-1)) and stabilized at a rate of 5molg(-1)h(-1) after 1h, whereas in the dark the rates remained constant at a rate of 10molg(-1)h(-1) over the first 180min of incubation. The rates of nitrate uptake in the light were high within the first 120min of incubation(7.2-11.1molg(-1)h(-1)) and decreased afterwards to lower values (0.8-3.9molg(-1)h(-1)), whereas in the dark the rates fluctuated around 0.0-11.1molg(-1)h(-1) throughout the whole incubation time (7h). The soluble sugar content of Z.noltei leaves increased significantly with both ammonium and nitrate incubations in the light, indicating the metabolic outcome of photosynthesis. In the dark, there was no significant variation in either the soluble sugar or in the starch content of leaves, rhizomes or roots in either the ammonium or nitrate incubations. However, the total starch content of plants decreased at night whereas the total soluble sugars increased, suggesting a process of starch catabolism to generate energy with the consequent production of smaller monosaccharide products. The starch content of rhizomes decreased significantly during the light incubations with nitrate but not with ammonium. These results suggest that carbohydrate mobilization is necessary for Z.noltei to account for extra energetic costs needed for the uptake and assimilation of nitrate. Furthermore, our results suggest that nitrate uptake, at least during the day, requires the mobilization of starch whereas the uptake of ammonium does not.
  • Effects of elevated CO2 and nutrients on the community metabolism of a Cymodocea nodosa bed
    Publication . Khan, Faisal; Alexandre, Ana; Ullah, Hadayet; Santos, Rui
    We assessed the combined effects of elevated CO2 and nutrients on the metabolism of a benthic community dominated by the seagrass Cymodocea nodosa (Ucria) Ascherson in a mesocosm experiment. C. nodosa plants and their associated community were exposed to two CO2 levels simulating future (700 ppm, pH 7.84) and current (360 ppm, pH 8.12) conditions, and two nutrient levels (enriched and ambient concentration) in a total of four treatments (-C-N, -C+N, +C-N, +C+N). Net community production (NCP) was estimated from changes in the concentration of dissolved inorganic carbon in the seawater in light incubations using benthic chambers. The variation pattern of NCP with the ordinance was consistent for all treatments. Although differences among treatments were not statistically significant, average NCP values were lowest under CO2 enrichment conditions. NCP was lower at a high CO2 level and ambient nitrogen concentration compared to when nutrient availability was higher, suggesting that the low nutrient availability may modulate the community response to CO2 enrichment. The results obtained suggest that the stimulation of the net community production of C. nodosa by elevated CO2 concentrations may be curtailed by low nutrient availability.
  • Nitrogen metabolism in the seagrass Zostera noltii
    Publication . Alexandre, Ana; Santos, Rui
    Nitrogen metabolism is a vital component in plant’s life. The main purpose of this thesis was to investigate the ecophysiology of nitrogen metabolism of the seagrass Zostera noltii in Ria Formosa lagoon. In the global change scenario, the effects of CO2 enrichment on photosynthesis, growth and nitrogen metabolism of Z. noltii were also investigated. Ammonium was identified as the preferential Ni source for Z. noltii, although nitrate uptake rates were considerable in the absence of ammonium. The ammonium uptake rates through the leaves were one order of magnitude higher than through the roots. Leaves were also identified as the main site for the reduction of ammonium and nitrate, as revealed by the much higher activity of the enzymes nitrate reductase and glutamine synthetase in the leaves than in the roots. The simultaneous supply of both Ni forms to Z. noltii enhanced the ammonium uptake rates and decreased the rates of nitrate uptake comparatively to the rates obtained when Ni forms were supplied separately. The uptake of ammonium or nitrate by one plant part (e.g. leaves) did not affect the uptake rate of the other plant part (e.g. roots), and no internal translocation of incorporated nitrogen was detected. The estimated whole-plant nitrogen budget of Z. noltii in the peak production season (spring) was slightly lower than the total nitrogen requirement for growth, which indicates that the growth of Z. noltii in the lagoon is only slightly limited by nitrogen. Z. noltii took up ammonium and nitrate at similar rates in the light and in the dark. In both light conditions, the nitrogen uptake displayed a temporal pattern of enhanced initial rates followed by lower but relatively constant rates. The uptake of nitrogen in the dark represented an additional use and mobilization of carbohydrate reserves. Z. noltii plants exposed to CO2-enriched conditions enhanced the photosynthetic rates while growth and ammonium uptake rates were not affected, suggesting that Z. noltii may benefit from future increases in seawater CO2 concentrations.
  • The effects of epiphytes on light harvesting and antioxidant responses in the seagrass posidonia oceanica
    Publication . Costa, Monya; Silva, João; Olivé, Irene; Barrote, Isabel; Alexandre, Ana; Albano, Sílvia; Santos, Rui
    Posidonia oceanica (L.) Delile is a subtidal seagrass whose leaves are commonly colonized by epiphytes. Epiphytes pose physical barriers to light penetration within the leaves, with possible significant impacts on photosynthesis. Furthermore, epiphytes can indirectly be responsible for leaf chlorosis, necrosis and senescence which are known to be related with the increase of oxygen reactive species (ROS) levels, potentially leading to oxidative stress. The aim of this work was to investigate in situ (i) the effect of epiphytes on the composition and balance of light harvesting pigments in leaves of the naturally growing seagrass P. oceanica, and (ii) evaluate differences in antioxidant responses. Epiphytized and non-epiphytized plants were analyzed to establish potential photosynthetic pigment roleshift between light harvesting and photoprotection functions. The experiments were carried out in Cabo de Gata Natural Park, southern Spain, where epiphytized and non-epiphytized plants can be found at identical depths and light exposure. The results showed that both O2 evolution rate along the day and chlorophyll a/b ratio were higher in non-epiphytized plants, indicating a negative effect of epiphytes on photosynthesis and light harvesting. Although under high irradiance (at solar noon) the xanthophyll cycle was activated in both epiphytized and non-epiphytized leaves, the de-epoxidation-ratio (AZ/VAZ) was lower in epiphytized leaves, due to light attenuation by epiphytes. The antioxidant capacity (TEAC and ORAC essays) and the activity of the antioxidant enzymes ascorbate peroxidase and dehydroascorbate were higher in epiphytized plants, showing that epiphytes can also be a potential source of oxidative stress to P. oceanica. Our results show that despite the light attenuation effect, leaf colonization by epiphytes can also be potentially stressful and reduces plant productivity.
  • First description of seagrass distribution and abundance in Sao Tome and Principe
    Publication . Alexandre, Ana; Silva, João; Ferreira, Rogério; Paulo, Diogo; Serrao, Ester; Santos, Rui
    Seagrass meadows in Sao Tome and Principe, eastern Atlantic Ocean, are described here for the first time. Specifically, we quantified the biomass and density of seagrasses, characterized the plant morphology and measure their nutrient content as a proxy of the nutrient environmental conditions where the meadows develop. The seagrass Halodule wrightii was found in two locations of the northeastern coast of the island of Sao Tome: 1) developing throughout an estimated area of 1500 ha surrounding Cabras islet, at a depth range of 4-10 m, on sandy bottom; and 2) at Santana bay with an area of 1500 m(2) at 5-10 m depth, on sandy bottom. A highly morphologically different population of Halodule wrightii was found on the northeastern coast of the island of Principe, off Abade beach, covering an area of 135 m2 at 4 m depth. Further research is needed to assess if this is a different species. Shoot biomass and density was 10 and 4-fold higher in Sao Tome than in Principe, respectively. CN ratios of above and belowground tissues of plants collected in Sao Tome were also significantly higher than in Principe. The carbon content of Halodule leaves from Sao Tome and Principe (41%) was much higher than that reported for other Halodule species, suggesting that meadows may have an important ecological role for carbon fixation. The presence of H. wrightii in Sao Tome and Principe raises ecological and evolutionary questions that warrant further research.
  • Nitrogen uptake and internal recycling in Zostera marina exposed to oyster farming: eelgrass potential as a natural biofilter
    Publication . Sandoval-Gil, José; Alexandre, Ana; Santos, Rui; Camacho-Ibar, Victor F.
    Oyster farming in estuaries and coastal lagoons frequently overlaps with the distribution of seagrass meadows, yet there are few studies on how this aquaculture practice affects seagrass physiology. We compared in situ nitrogen uptake and the productivity of Zostera marina shoots growing near off-bottom longlines and at a site not affected by oyster farming in San Quintin Bay, a coastal lagoon in Baja California, Mexico. We used benthic chambers to measure leaf NH4 (+) uptake capacities by pulse labeling with (NH4)-N-15 (+) and plant photosynthesis and respiration. The internal N-15 resorption/recycling was measured in shoots 2 weeks after incubations. The natural isotopic composition of eelgrass tissues and vegetative descriptors were also examined. Plants growing at the oyster farming site showed a higher leaf NH4 (+) uptake rate (33.1 mmol NH4 (+) m(-2) day(-1)) relative to those not exposed to oyster cultures (25.6 mmol NH4 (+) m(-2) day(-1)). We calculated that an eelgrass meadow of 15-16 ha (which represents only about 3-4 % of the subtidal eelgrass meadow cover in the western arm of the lagoon) can potentially incorporate the total amount of NH4 (+) excreted by oysters (similar to 5.2 x 10(6) mmol NH4 (+) day(-1)). This highlights the potential of eelgrass to act as a natural biofilter for the NH4 (+) produced by oyster farming. Shoots exposed to oysters were more efficient in re-utilizing the internal N-15 into the growth of new leaf tissues or to translocate it to belowground tissues. Photosynthetic rates were greater in shoots exposed to oysters, which is consistent with higher NH4 (+) uptake and less negative delta C-13 values. Vegetative production (shoot size, leaf growth) was also higher in these shoots. Aboveground/belowground biomass ratio was lower in eelgrass beds not directly influenced by oyster farms, likely related to the higher investment in belowground biomass to incorporate sedimentary nutrients.
  • Temperature is not a limiting factor for the expansion of Halophila stipulacea throughout the Mediterranean Sea
    Publication . Georgiou, Dimos; Alexandre, Ana; Luis, Joaquim; Santos, Rui
    The seagrass Halophila stipulacea is a Lessepsian migrant that has spread from the Red Sea into the Mediterranean Sea where some authors consider it invasive. It has been suggested that the range of expansion of the species in the Mediterranean will be limited by the 15 degrees C sea surface isotherm. Here we tested the effects of temperature on survival, photosynthesis, leaf growth and clonal growth of H. stipulacea. We analysed the temporal and spatial variation of sea surface temperature (SST) in the Mediterranean Sea and the species' spread rate since its introduction to forecast its future expansion and potential changes in the spread rate due to increased SST. We estimated that the species has been spreading throughout the Mediterranean with a variable rate averaging 12 km yr(-1). Despite being a species native to the tropics, it was able to survive, photosynthesise and grow within a broad range of temperatures (10 to 30 degrees C). At 10 degrees C, a temperature colder than the winter's lowest isotherm for most of the Mediterranean Sea, the clonal growth ceased but plants did not die and continued to photosynthesise and produce new leaf biomass. The maximum photosynthetic rate peaked at 30 degrees C but the optimal leaf growth rate was within the range of temperatures for temperate seagrass species (11.5 to 26 degrees C). Based on the present spread rate and on the non-limiting effect of temperature, we estimate that in the next 100 yr H. stipulacea will be present throughout the whole Mediterranean Sea (but perhaps not the north Adriatic), potentially spreading into the Atlantic.
  • Interactions between seagrasses and seaweeds during surge nitrogen acquisition determine interspecific competition
    Publication . Alexandre, Ana; Baeta, Alexandra; Engelen, Aschwin H.; Santos, Rui
    Seagrasses dominate shallow coastal environments where nitrogen (N) availability in the water column is often sporadic and mainly in the form of pulses. We investigated the N uptake competition between seagrasses and seaweeds through a series of N-15 surge uptake experiments combining single-species and mixed incubations across ammonium concentrations. N surge uptake rates of seagrasses were 2 to 14-fold higher than those of seaweeds in the majority of combinations, showing that seagrasses are generally in a competitive advantage over seaweeds in N-poor environments with N-pulses. No threshold concentration of ammonium was found beyond which seaweeds performed better than seagrasses. Mixed incubations revealed interspecific interactions that affected rates positively and negatively. Uptake rates obtained in single-species incubations, therefore, cannot always be used to predict the outcome of uptake competition. Only two (Zostera marina vs. Ulva rotundata and Zostera marina vs. Codium decorticatum) of the nine combinations tested (Z. marina, Z. noltei and Cymodocea nodosa vs. U. rotundata, C. decorticatum and Dictyota dichotoma) were found to enhance macroalgal uptake. Our results showed that the surge uptake capacity of seagrasses represents an important mechanism in their N acquisition strategy that justifies their dominance in shallow oligotrophic environments.
  • Effects of CO2 enrichment on photosynthesis, growth, and nitrogen metabolism of the seagrass Zostera noltii
    Publication . Alexandre, Ana; Silva, Joao; Buapet, Pimchanok; Bjork, Mats; Santos, Rui
    Seagrass ecosystems are expected to benefit from the global increase in CO2 in the ocean because the photosynthetic rate of these plants may be C-i-limited at the current CO2 level. As well, it is expected that lower external pH will facilitate the nitrate uptake of seagrasses if nitrate is cotransported with H+ across the membrane as in terrestrial plants. Here, we investigate the effects of CO2 enrichment on both carbon and nitrogen metabolism of the seagrass Zostera noltii in a mesocosm experiment where plants were exposed for 5 months to two experimental CO2 concentrations (360 and 700 ppm). Both the maximum photosynthetic rate (Pm) and photosynthetic efficiency (alpha) were higher (1.3- and 4.1-fold, respectively) in plants exposed to CO2-enriched conditions. On the other hand, no significant effects of CO2 enrichment on leaf growth rates were observed, probably due to nitrogen limitation as revealed by the low nitrogen content of leaves. The leaf ammonium uptake rate and glutamine synthetase activity were not significantly affected by increased CO2 concentrations. On the other hand, the leaf nitrate uptake rate of plants exposed to CO2-enriched conditions was fourfold lower than the uptake of plants exposed to current CO2 level, suggesting that in the seagrass Z. noltii nitrate is not cotransported with H+ as in terrestrial plants. In contrast, the activity of nitrate reductase was threefold higher in plant leaves grown at high-CO2 concentrations. Our results suggest that the global effects of CO2 on seagrass production may be spatially heterogeneous and depend on the specific nitrogen availability of each system. Under a CO2 increase scenario, the natural levels of nutrients will probably become limiting for Z. noltii. This potential limitation becomes more relevant because the expected positive effect of CO2 increase on nitrate uptake rate was not confirmed.