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- Population-level effects of clam harvesting on the seagrass Zostera noltiiPublication . Cabaço, Susana; Alexandre, Ana; Santos, RuiSeagrass declines have been reported worldwide, mostly as a consequence of anthropogenic disturbance. In Ria Formosa lagoon, southern Portugal, the intertidal meadows of Zostera noltii are highly disturbed by clam harvesters. The most common technique used to collect the clams consists of digging and tilling the sediment with a modified knife with a large blade. Here we present both descriptive and experimental evidence of the negative effects of clam harvest on the Z. noltii populations of Ria Formosa. A comparison between disturbed and undisturbed meadows suggests that clam harvesting activities change the species population structure by significantly reducing shoot density and total biomass, particularly during August, when the harvest effort is higher. Experimental harvest revealed a short-term impact on shoot density, which rapidly recovered to control levels during the following month. An experimental manipulation of rhizome fragmentation revealed that plant survival is reduced only when fragmented rhizomes are left with 1 intact internode. Shoot production and rhizome elongation and production of fragmented rhizomes having 2 to 5 internodes were not significantly affected, even though growth and production were lower when only 2 internodes were left. Experimental shoot damage at different positions along the rhizome had a significant effect on plant survival, rhizome elongation, and production only when the apical shoot was removed. Our results show that clam harvest can adversely affect Z. noltii meadows of Ria Formosa while revealing a low modular integration that allows the species to rapidly recover from physical damage.
- Effects of clam harvesting on sexual reproduction of the seagrass Zostera noltiiPublication . Alexandre, Ana; Santos, Rui; Serrão, EsterThe sexual reproduction of Zostera noltii in the Ria Formosa lagoon (southern Portugal) was assessed by quantifying the variation in both flowering effort and evolution of maturation stages during the fertile season. The effects of clam harvesting on the sexual reproduction of Z. noltii were investigated using both descriptive and experimental approaches. Meadows disturbed by clam harvesting were compared with undisturbed meadows in 2 sectors of the lagoon. In both sectors, disturbed meadows showed significantly lower vegetative shoot density and significantly higher reproductive effort. The reproductive effort in the western disturbed meadows was 2-fold higher than in undisturbed meadows, whereas in eastern disturbed meadows it was 4-fold higher. In disturbed meadows, early maturation stages were found until the end of the flowering season and higher seed production was observed. Both the negative effect of clam harvesting on Z. noltii density and the positive effect on its reproductive effort were confirmed by manipulative field experiments. Plots that were experimentally harvested during the fertile season showed significantly lower vegetative shoot density and higher reproductive effort than unharvested plots. Results suggest that Z. noltii responds to clam harvesting disturbance by both increasing its reproductive effort and extending its fertile season.
- Nutrition of the seagrass Cymodocea nodosa: pulses of ammonium but not of phosphate are crucial to sustain the species growthPublication . Alexandre, Ana; Santos, RuiWe investigated the nutrient acquisition of the seagrass Cymodocea nodosa and the importance of sediment to water column nutrient pulses, which regularly occur in coastal lagoons forced by incoming flood tides. Ammonium was preferentially taken up and accounted for 60-90% of the total daily N acquisition, whereas amino acid acquisition through belowground plant parts represented the second most important source of N, accounting 8-34%. The uptake of ammonium pulses increased dramatically the daily N acquisition from 9.5 mmol m-2 day-1 to 1.33 mmol m-2 day-1 at ambient nutrient concentrations, enabling the species to meet its N demand. Roots accounted for 96% of the total phosphate acquisition, with no evidence for P limitation. The ability of seagrasses to adapt to nutrient pulses may be an overlooked nutrition strategy common to many ecosystems where nutrient availability in the water column is low but nutrient pulses occur.
- Light is more important than nutrient ratios of fertilization for cymodocea nodosa seedling developmentPublication . Alexandre, Ana; Silva, João; Santos, RuiRestoration 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.
- Timing and success of reproductive stages in the seagrass Zostera noltiiPublication . Alexandre, Ana; Cabaço, Susana; Santos, Rui; Serrão, EsterThe timing and success of sexual reproduction of the seagrass Zostera noltii was investigated at the Ria Formosa lagoon, Portugal. Thirty plants were tagged and monitored individually through time to determine in situ the development time of each maturation stage, from the emergence of the flowers to the production of seeds. The overall process of flowering and fruiting lasted 47 ± 4 days, during which formation and maturation of the fruits was the most time-consuming stage (27 ± 2 days). Spathe success, i.e. the percentage of spathes that produced seeds, was 22 ± 4% while spathe mortality was 34 ± 6%. A considerable percentage of spathes (37 ± 7%) was lost through leaf detachment, but some of these may still add to the reproductive success of the species by contributing to the species recruitment within the source meadow or elsewhere. Meadow seed production (MSP) of Z. noltii was estimated to be 312 ± 66 seeds m−2, whereas the potential seed production of the studied meadow was 2623 seeds m−2. Under laboratory conditions, 70% of Z. noltii seeds germinated within 26 days, but only 10% reached the seedling stage due to the high mortality of germlings. Fertility, defined as the probability of a seed to originate a new plant, was estimated to be 14 × 10−4, which is higher than what is expected for most seagrasses.
- Nitrogen uptake in light versus darkness of the seagrass Zostera noltei: integration with carbon metabolismPublication . Alexandre, Ana; Silva, João; Santos, RuiWe 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 bedPublication . Khan, Faisal; Alexandre, Ana; Ullah, Hadayet; Santos, RuiWe 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 noltiiPublication . Alexandre, Ana; Santos, RuiNitrogen 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 oceanicaPublication . Costa, Monya; Silva, João; Olivé, Irene; Barrote, Isabel; Alexandre, Ana; Albano, Sílvia; Santos, RuiPosidonia 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.
- The tropical seagrass halophila stipulacea: reviewing what we know from its native and invasive habitats, alongside identifying knowledge gapsPublication . Winters, Gidon; Beer, Sven; Willette, Demian A.; Viana, Inés G.; Chiquillo, Kelcie L.; Beca-Carretero, Pedro; Villamayor, Betty; Azcárate-García, Tomás; Shem-Tov, Rachamim; Mwabvu, Bridget; Migliore, Luciana; Rotini, Alice; Oscar, Michelle A.; Belmaker, Jonathan; Gamliel, Inbal; Alexandre, Ana; Engelen, Aschwin; Procaccini, Gabriele; Rilov, GilHalophila stipulacea is a small tropical seagrass, native to the Red Sea, Persian Gulf, and the Indian Ocean. It invaded the Mediterranean Sea 150 years ago as a Lessepsian migrant, but so far has remained in insulated, small populations across this basin. Surprisingly, in 2002 it was reported in the Caribbean Sea, where within less than two decades it spread to most of the Caribbean Island nations and reaching the South American continent. Unlike its invasion of Mediterranean, in the Caribbean H. stipulacea creates large, continuous populations in many areas. Reports from the Caribbean demonstrated the invasiveness of H. stipulacea by showing that it displaces local Caribbean seagrass species. The motivation for this review comes from the necessity to unify the existing knowledge on several aspects of this species in its native and invasive habitats, identify knowledge gaps and develop a critical strategy to understand its invasive capacity and implement an effective monitoring and conservation plan to mitigate its potential spread outside its native ranges. We systematically reviewed 164 studies related to H. stipulacea to create the "Halophila stipulacea database." This allowed us to evaluate the current biological, ecological, physiological, biochemical, and molecular knowledge of H. stipulacea in its native and invasive ranges. Here we (i) discuss the possible environmental conditions and plant mechanisms involved in its invasiveness, (ii) assess the impact of H. stipulacea on native seagrasses and ecosystem functions in the invaded regions, (iii) predict the ability of this species to invade European and transoceanic coastal waters, (iv) identify knowledge gaps that should be addressed to better understand the biology and ecology of this species both in its native and non-native habitats, which would improve our ability to predict H. stipulacea's potential to expand into new areas in the future. Considering the predicted climate change scenarios and exponential human pressures on coastal areas, we stress the need for coordinated global monitoring and mapping efforts that will record changes in H. stipulacea and its associated communities over time, across its native, invasive and prospective distributional ranges. This will require the involvement of biologists, ecologists, economists, modelers, managers, and local stakeholders.
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