Seagrass ecosystem multifunctionality under the rise of a flagship marine megaherbivore

Large grazers (megaherbivores) have a profound impact on ecosystem functioning. However, how ecosystem multifunctionality is affected by changes in megaherbivore populations remains poorly understood. Understanding the total impact on ecosystem multifunctionality requires an integrative ecosystem approach, which is especially challenging to obtain in marine systems. We assessed the effects of experimentally simulated grazing intensity scenarios on ecosystem functions and multifunctionality in a tropical Caribbean seagrass ecosystem. As a model, we selected a key marine megaherbivore, the green turtle, whose ecological role is rapidly unfolding in numerous foraging areas where populations are recovering through conservation after centuries of decline, with an increase in recorded overgrazing episodes. To quantify the effects, we employed a novel integrated index of seagrass ecosystem multifunctionality based upon multiple, well-recognized measures of seagrass ecosystem functions that reflect ecosystem services. Experiments revealed that intermediate turtle grazing resulted in the highest rates of nutrient cycling and carbon storage, while sediment stabilization, decomposition rates, epifauna richness, and fish biomass are highest in the absence of turtle grazing. In contrast, intense grazing resulted in disproportionally large effects on ecosystem functions and a collapse of multifunctionality. These results imply that (i) the return of a megaherbivore can exert strong effects on coastal ecosystem functions and multifunctionality, (ii) conservation efforts that are skewed toward megaherbivores, but ignore their key drivers like predators or habitat, will likely result in overgrazing-induced loss of multifunctionality, and (iii) the multifunctionality index shows great potential as a quantitative tool to assess ecosystem performance. Considerable and rapid alterations in megaherbivore abundance (both through extinction and conservation) cause an imbalance in ecosystem functioning and substantially alter or even compromise ecosystem services that help to negate global change effects. An integrative ecosystem approach in environmental management is urgently required to protect and enhance ecosystem multifunctionality.     

Leaf photoacclimatory responses of the tropical seagrass Thalassia testudinum under mesocosm conditions: a mechanistic scaling-up study

Here, the leaf photoacclimatory plasticity and efficiency of the tropical seagrass Thalassia testudinum were examined. Mesocosms were used to compare the variability induced by three light conditions, two leaf sections and the variability observed at the collection site. The study revealed an efficient photosynthetic light use at low irradiances, but limited photoacclimatory plasticity to increase maximum photosynthetic rates (P(max)) and saturation (E(k)) and compensation (E(c)) irradiances under high light irradiance. A strong, positive and linear association between the percentage of daylight hours above saturation and the relative maximum photochemical efficiency (F(V)/F(M)) reduction observed between basal and apical leaf sections was also found. The results indicate that T. testudinum leaves have a shade-adapted physiology. However, the large amount of heterotrophic biomass that this seagrass maintains may considerably increase plant respiratory demands and their minimum quantum requirements for growth (MQR). Although the MQR still needs to be quantified, it is hypothesized that the ecological success of this climax species in the oligotrophic and highly illuminated waters of the Caribbean may rely on the ability of the canopy to regulate the optimal leaf light environment and the morphological plasticity of the whole plant to enhance total leaf area and to reduce carbon respiratory losses.     

Synergistic effects of high temperature and sulfide on tropical seagrass

To examine the synergism of high temperature and sulfide on two dominant tropical seagrass species, a large-scale mesocosm experiment was conducted in which sulfide accumulation rates (SAR) were increased by adding labile carbon (glucose) to intact seagrass sediment cores across a range of temperatures. During the initial 10 d of the 38 d experiment, porewater SAR in cores increased 2- to 3-fold from 44 and 136 μmol L^− 1 d^− 1 at 28-29 °C to 80 and 308 μmol L^− 1 d^− 1 at 34-35 °C in Halodule wrightii and Thalassia testudinum cores, respectively. Labile C additions to the sediment resulted in SAR of 443 and 601 μmol L^− 1 d^− 1 at 28-29 °C and 758 to 1,557 μmol L^− 1 d^− 1 at 34-35 °C in H. wrightii and T. testudinum cores, respectively. Both T. testudinum and H. wrightii were highly thermal tolerant, demonstrating their tropical affinities and potential to adapt to high temperatures. While plants survived the 38 d temperature treatments, there was a clear thermal threshold above 33 °C where T. testudinum growth declined and leaf quantum efficiencies (Fv/Fm) fell below 0.7. At this threshold temperature, H. wrightii maintained shoot densities and leaf quantum efficiencies. Although H. wrightii showed a greater tolerance to high temperature, T. testudinum had a greater capacity to sustain biomass and short shoots under thermal stress with labile C enrichment, regardless of the fact that sulfide levels in the T. testudinum cores were 2 times higher than in the H. wrightii cores. Tropical seagrass tolerance to elevated temperatures, predicted in the future with global warming, should be considered in the context of the sediment-plant complex which incorporates the synergism of plant physiological responses and shifts in sulfur biogeochemistry leading to increased plant exposure to sulfides, a known toxin.     

Thalassia testudinum seedling responses to changes in salinity and nitrogen levels

The dominant seagrass in Florida Bay, Thalassia testudinum Banks ex König, is a stenohaline species with optimum growth around marine salinity (30-40 PSU). Previous studies have examined the responses of mature short shoots of T. testudinum to environmental stresses. Our goal was to assess responses of seedlings to changes in water chemistry in Florida Bay that might occur as part of the Comprehensive Everglades Restoration Plan (CERP). Specifically, we examined seedling survival, growth, photosynthesis, respiration and osmolality in response to hypo- and hyper-salinity conditions, as well as possible synergistic effects of depleted and elevated ammonium concentrations. The study was conducted in mesocosms on T. testudinum seedlings collected during August 2003 near Florida Bay. Hyper- and hypo-saline conditions were detrimental to the fitness of T. testudinum seedlings. Plants at 0 and 70 PSU exhibited 100% mortality and a significant decrease in survival was observed in the 10, 50 and 60 PSU treatments. Increased levels of ammonium further decreased growth in the lower salinity treatments. Seedlings in 30 and 40 PSU had the greatest growth. Quantum yield and relative electron transport rate, measured using PAM fluorometry, showed a decrease in photosynthetic performance on either side of the 30-40 PSU optimum. Tissue osmolality decreased significantly with decreased salinity but tissue remained consistently hyperosmotic to the media across all salinity treatments. Maintaining negative water potential and allocating more energy to osmoregulation may decrease the productivity of this species in salinity-stress conditions. Our results suggest that the salinity-tolerance limits of this seagrass at the seedling stage are not as broad as those reported for mature plants. Increased fresh water inflow, especially if co-occurring with an increase in water-column ammonium, could negatively affect successful recruitment of T. testudinum seedlings in northern regions of Florida Bay.     

Spatial and temporal patterns of aboveground net primary productivity (ANPP) along two freshwater-estuarine transects in the Florida Coastal Everglades

We present here a 4-year dataset (2001–2004) on the spatial and temporal patterns of aboveground net primary production (ANPP) by dominant primary producers (sawgrass, periphyton, mangroves, and seagrasses) along two transects in the oligotrophic Florida Everglades coastal landscape. The 17 sites of the Florida Coastal Everglades Long Term Ecological Research (FCE LTER) program are located along fresh-estuarine gradients in Shark River Slough (SRS) and Taylor River/C-111/Florida Bay (TS/Ph) basins that drain the western and southern Everglades, respectively. Within the SRS basin, sawgrass and periphyton ANPP did not differ significantly among sites but mangrove ANPP was highest at the site nearest the Gulf of Mexico. In the southern Everglades transect, there was a productivity peak in sawgrass and periphyton at the upper estuarine ecotone within Taylor River but no trends were observed in the C-111 Basin for either primary producer. Over the 4 years, average sawgrass ANPP in both basins ranged from 255 to 606 g m⁻² year⁻¹. Average periphyton productivity at SRS and TS/Ph was 17–68 g C m⁻² year⁻¹ and 342–10371 g C m⁻² year⁻¹, respectively. Mangrove productivity ranged from 340 g m⁻² year⁻¹ at Taylor River to 2208 g m⁻² year⁻¹ at the lower estuarine Shark River site. Average Thalassia testudinum productivity ranged from 91 to 396 g m⁻² year⁻¹ and was 4-fold greater at the site nearest the Gulf of Mexico than in eastern Florida Bay. There were no differences in periphyton productivity at Florida Bay. Interannual comparisons revealed no significant differences within each primary producer at either SRS or TS/Ph with the exception of sawgrass at SRS and the C−111 Basin. Future research will address difficulties in assessing and comparing ANPP of different primary producers along gradients as well as the significance of belowground production to the total productivity of this ecosystem.     

Assessment of turtle grass (Thalassia testudinum ex Banks Konig) community structure in a UNESCO Biosphere Reserve

Tropical turtle grass beds (Thalassia testudinum) were investigated in an UNESCO Biosphere Reserve in St. Johns Island, United States Virgin Islands. Four coastal bays were studied to assess floral characteristics, benthic invertebrate density and secondary production. These bays varied with respect to oceanic exposure and anthropogenic stresses. Results indicate that Coral Bay Harbor, the most anthropogenetically impacted site, had the highest T. testudinum biomass, but the lowest floral diversity. Its faunal community was dominated by small polychaetes with significantly lower secondary production. The most protected site (Hurricane Hole) maintained the highest floral and faunal species richness, faunal density, faunal diversity, and secondary production. The other two bays, Great Lameshur and Little Lameshur, demonstrated intermediate plant biomass and species richness, faunal density and secondary production. Each of these bays, however, had high oceanic exposure due to their orientation which also demonstrated a sediment size shift to larger particles compared to the other sites. One unique finding was a significant increase in the shoot:root ratio in Little Lameshur where green turtle (Chelonia mydas) grazing was frequently observed, suggesting a potential top-down structuring force in this bay.     

Rhythmic plant morphogenesis: Recurrent patterns of idioblast cell production

Most plants are constructed from repeating modular units such as phytomers, merophytes, and cell packets. Even an organism as simple as the filamentous cyanobacterium Anabaena shows recurrent patterns of differentiated cellular structures, notably with respect to its heterocysts. These examples reflect the inherent rhythms established within developmental processes of living organisms. In the present article, attention is paid to repetitious production of idioblasts—isolated cells, or clusters of cells, with an identity different to that of neighbouring cells from which they are derived. In higher plant root tissues, idioblasts are contained within cell packets that grow up from mother cells during the course of a number of cycles of cell production. The heterocysts of Anabaena are also discussed; they, too, are a type of idioblast. The idioblasts of root tissues originate as small cells which result from unequal cell divisions. Such divisions are usually the final ones within a cell packet which has already undergone a number of division cycles and are characteristically located at one or both ends of a packet. The packet end walls are suggested to have a role in regulating division asymmetry. Idioblastic systems discussed are root cortical trichosclereids and diaphragm cells; in their earliest stage, the cells from which lateral root primordia arise are also considered as clusters of idioblasts because they, too, are the products of asymmetric divisions of pericyclic mother cells. The division patterns of all these idioblastic systems were modelled in a consistent way using L-systems, with the assumption that the age of a cell-packet end wall plays a special role in cell determination. This article is dedicated to Vsevelod Ya. Brodsky, doyen of Russian studies of rhythms in cell division and development, who celebrates his 80th birthday on August 4, 2008 This article was presented in original.     

Diurnal light curves and landscape-scale variation in photosynthetic characteristics of Thalassia testudinum in Florida Bay

When using pulse-amplitude modulated (PAM) fluorometry to measure landscape-scale photosynthetic characteristics, diurnal variations in fluorescence during sampling may confound the assessment of the physiological condition. In this study, two photophysiological assessment techniques: Diurnal Yield and Diurnal Rapid Light Curve (RLC) were investigated in an attempt to incorporate the temporal and spatial scales of sampling into a physiological assessment of Thalassia testudinum in Florida Bay. Photosynthesis–irradiance (P–E) curves were calculated using both methods and the ability of each to predict the relationship between relative electron transport rates and irradiance was assessed. Both methods had limitations in providing consistent estimates of photosynthetic efficiency or capacity. The Diurnal Yield method produced unrealistically high predictions of photosynthetic capacity (relative electron transport rate (rETR_max), 417–1715) and saturation irradiance (I_k, 1045–4681 μmol photons m⁻² s⁻¹). In contrast, the Diurnal RLC method generally produced predictions of rETR_max (100–200) and I_k (300–500 μmol photons m⁻² s⁻¹) which were similar to average values calculated from each day's RLCs. The Diurnal RLC method was unable to predict photosynthetic efficiency () only when ambient irradiances were continuously >I_k during the sampling period. We believe that with sampling modifications in high-light or shallow environments, such as starting sampling earlier in the morning, extending sampling later in the day, or using the average from each day's RLCs, that the Diurnal RLC method can produce representative estimates of rETR_max, , and I_k, providing a method to characterize seagrass photosynthesis at the landscape-level. The Diurnal RLC method does not negate Diurnal variation but it produces a curve that incorporates the changing ambient light environment into the assessment of seagrass physiological status.     

Effects of simultaneous changes in light, nutrients, and herbivory levels, on the structure and function of a subtropical turtlegrass meadow

The interactive effects of light, nutrients, and simulated herbivory on the structure and functioning of a subtropical turtlegrass bed were analyzed monthly from May to October 2001 in Perdido Bay, FL. For each of the three factors, two levels were evaluated in a factorial design with four replicates per treatment. The variables included: light, at ambient and 40% reduction; nutrients, at ambient and 2× ambient concentrations; and herbivory, with no herbivory and simulated effects of a density of 15 sea urchins/m². In practice, light levels turned out to be 40% of surface PAR for ambient conditions, and 16% for shaded plots. Biomass removed as herbivory represented, on average, slightly less than 20% of the above-ground biomass. Separate three-way ANOVAs found no significant three-way interactions for any of the response variables, and few two-way interactions. There were no significant nutrient effects on turtlegrass above-ground biomass, although nutrient additions produced significant decreases in epibiont biomass, and net above-ground primary production (NAPP); significant increases in below-ground biomass during the peak of the growing season. Shoot density and average number of leaves per shoot increased significantly, while the C/N ratio of the oldest leaf in the enriched plots decreased significantly. Light reduction significantly negatively affected all response variables, except below-ground biomass, shoot density and leaf length. Herbivory had isolated and inconsistent significant effects on below-ground biomass, shoot density, average number of leaves per shoot, and leaf length and width. Overall, our results indicate that nutrients are not limiting in Perdido Bay, and that nutrient additions had mostly detrimental effects. Light appeared to be the most important variable limiting seagrasses growth and abundance, and as with terrestrial plants, seagrasses seemed to respond more to light and nutrients than to herbivory. However, it is essential that additional tests of the single and interactive effects of the three key factors of light, nutrients and herbivory be done to evaluate the generality of our work, since our study is the first of its kind in seagrass meadows.