Epiphyte Overgrowth Research Articles

Ex-situ restoration of the Mediterranean forest-forming macroalga Ericaria amentacea: optimizing growth in culture may not be the key to growth in the field

Evidence of local and regional declines in the canopy-forming alga Ericaria amentacea, a foundation species of diverse marine forest communities on exposed Mediterranean coasts, have spurred restoration efforts focused on sustainable ex-situ techniques. The need to balance the costs of culture maintenance and the susceptibility of early life stages to stressors in the native habitat, including rapid, often extreme shifts in temperature, hydrodynamics and nutrient availability, have driven current efforts to create a culture environment that primes seedlings for outplant, increasing their resilience rather than maximizing growth. We tested the effects of 1) higher culture temperature (25°C) combined with wave simulation and 2) reduced nutrient loads (10% of standard protocol) with wave simulation on post-culture and outplant outcomes relative to optimal growth conditions in established protocols (20°C, no waves, high-nutrient culture medium). While increased temperature and water motion negatively affected seedling growth in culture, and higher nutrients caused oxidative stress likely associated with enhanced epiphyte overgrowth, these effects were not clearly translated into patterns of long-term growth in the field. Instead, survival in the initial days post-outplant appeared to be the bottleneck for restoration potential, where substrates with persisting seedlings at one month were generally found with flourishing juveniles at four months. Larger clumps of seedlings, in turn, were strongly associated with both initial survival and future growth. These results underscore the importance of the zygote settlement phase to establish high seedling densities, which may be optimized by phenological monitoring of the donor population. They also suggest that less-controlled, more environmentally-realistic culture conditions involving the introduction of mild stress may enhance the survival of early life stages of E. amentacea during the transition to the native environment, simultaneously providing a means to reduce human resource costs in culture and move toward scaling up.

Controlling Light to Optimize Growth and Added Value of the Green Macroalga Codium tomentosum

Codium tomentosumis a recently domesticated green macroalga, being currently cultured as an extractive species in integrated multi-trophic aquaculture (IMTA). Optimization of light requirements in outdoor systems must be achieved to increase the market value of cultivated algal biomass. The present study addresses the seasonal effects of light intensity and wavelength on productivity, pigment composition and epiphyte overgrowth inC. tomentosumcultured in a land-based IMTA system. Exposure to high light (non-filtered sun light) lead to higher net productivities in spring. However, non-filtered sun light caused significantly reduced productivities during summer when compared to filtered sun light (~ 4x lower irradiance levels). Furthermore, lower photosynthetic capacity (Fv/Fm) was observed in macroalgae cultured under high light during summer, indicating photoinhibition. Treatments with filtered sun light (low and red light) showed intermediate and more stable productivities. Epiphyte biomass was higher under high light and the lowest epiphyte overgrowth was recorded under red light. Concentrations of light-harvesting pigments were lower in summer than in spring, indicating a seasonal photoacclimation of macroalgae. An opposite seasonal trend was observed for accessory xanthophylls, as the main role of these pigments is photoprotection. Higher all-trans-neoxanthin and violaxanthin concentrations were found in high light than in low or red light treatments, confirming the important role of these biomolecules in the photoprotection ofC. tomentosum. This study underlines the importance of controlling light to optimize algal growth outdoors and enhance the production of high-value compounds (i.e., pigments). Additionally, this practice can also reduce epiphyte overgrowth, thus enhancing the valorization of macroalgal biomass derived fromC. tomentosumaquaculture.

Temperature Effects on Leaf and Epiphyte Photosynthesis, Bicarbonate Use and Diel O2 Budgets of the Seagrass Zostera marina L.

Ocean warming along with nutrient enrichment are major stressors causing global seagrass decline. While the effects of global warming on metabolic parameters in seagrasses are well described, the effect of increasing temperature on the epiphytic overgrowth of seagrass leaves and the consequences for the seagrass plant are poorly understood. Here, we investigated the effects of elevating temperature on the photosynthetic efficiency of the seagrass species Zostera marina L. and its associated epiphytes, to explore how ocean warming might affect epiphytism in seagrasses. Gas exchange and final pH measurements on bare seagrass leaves, leaves with epiphytes, and epiphytes separated from seagrass leaves were used to quantify photosynthesis and respiration rates, and the inorganic carbon extraction capacity of leaves and epiphytes as a function of photon scalar irradiance and temperature (12, 17, 22, and 27°C). Seagrass without epiphytic biofilm had a high ability to exploit the incoming irradiance regardless of the light intensity and temperature, shown as continuously high light use efficiency and maximum net photosynthesis rates. The presence of epiphytic biofilm on the seagrass leaves impaired plant photosynthesis by increasing light requirements and reducing the photosynthetic efficiency (especially at 27°C). Epiphytes showed the lowest respiration rates in darkness and had the highest oxygen surplus over diel cycles up to 22°C, whereas bare leaves had the highest diel oxygen surplus at 27°C. Both bare leaves and epiphytes lost the ability to utilize bicarbonate at 27°C, and epiphytes also did not show use of bicarbonate at 12°C. Our results indicate a competitive advantage for epiphytes in cold CO2-rich environments, whereas seagrass with bare leaves could be less affected under elevated seawater temperatures.

Low Light Availability Reduces the Subsurface Sediment Carbon Content in Halophila beccarii From the South China Sea.

Eutrophication, dredging, agricultural and urban runoffs, and epiphyte overgrowth could reduce light availability for seagrass. This may affect “blue carbon” stocks in seagrass beds. However, little research is available on the effect of light intensities on carbon sequestration capacity in seagrass beds, especially small-bodied seagrasses. The dominant seagrass Halophila beccarii, a vulnerable species on the IUCN Red List, was cultured in different light intensities to examine the response of vegetation and sediment carbon in seagrass beds. The results showed that low light significantly reduced leaf length and above-ground biomass, while carbon content in both above-ground and below-ground tissues were not affected. Low light reduced both the above-ground biomass carbon and the total biomass carbon. Interestingly, while under saturating light conditions, the subsurface and surface carbon content was similar, under low light conditions, subsurface sediment carbon was significantly lower than the surface content. The reduction of subsurface sediment carbon might be caused by less release flux of dissolved organic carbon from roots in low light. Taken together, these results indicate that reduced light intensities, to which these meadows are exposed to, will reduce carbon sequestration capacity in seagrass beds. Measures should be taken to eliminate the input of nutrients on seagrass meadows and dredging activities to maintain the “blue carbon” storage service by enhancing light penetration into seagrass.

Imaging O2 dynamics and microenvironments in the seagrass leaf phyllosphere with magnetic optical sensor nanoparticles.

Eutrophication leads to epiphyte blooms on seagrass leaves that strongly affect plant health, yet the actual mechanisms of such epiphyte-induced plant stress remain poorly understood. We used magnetic optical sensor nanoparticles in combination with luminescence lifetime imaging to map the O2 concentration and dynamics in the heterogeneous seagrass phyllosphere under changing light conditions. By incorporating magnetite into the sensor nanoparticles, it was possible to image the spatial O2 distribution under flow over seagrass leaf segments in the presence of a strong magnetic field. Local microniches with low leaf surface O2 concentrations were found under thick epiphytic biofilms, often leading to anoxic microhabitats in darkness. High irradiance led to O2 supersaturation across most of the seagrass phyllosphere, whereas leaf microenvironments with reduced O2 conditions were found under epiphytic biofilms at low irradiance, probably driven by self-shading. Horizontal micro-profiles extracted from the O2 images revealed pronounced heterogeneities in local O2 concentration over the base of the epiphytic biofilm, with up to 52% reduction in O2 concentrations in areas with relatively thick (>2mm), compared with thin (≤1mm), epiphyte layers in darkness. We also present evidence of enhanced relative internal O2 transport within leaves with epiphyte overgrowth, compared with bare seagrass leaves, in light as a result of limited mass transfer across thick outward diffusion pathways. The local availability of O2 was still markedly reduced in the epiphyte-covered leaves, however. The leaf phyllosphere is thus characterized by a complex microlandscape of O2 availability that strongly affects microbial processes occurring within the epiphytic biofilm, which may have implications for seagrass health, as anoxic microhabitats have been shown to promote the microbiological production of reduced toxic compounds, such as nitric oxide.

Temporal variations of Halodule wrightii meadows and associated fauna near their southern distribution limit in the southwestern Atlantic

AbstractHalodule wrightiimeadows in Southern Brazil have been regressing in an unsheltered area of the subtropical Paranaguá Bay, near their southern limit in the SW Atlantic, since 2006. To identify early indicators of regression events, we assessed variations in plant and macrobenthic structure in two local meadows under unsheltered and protected conditions. Differences between sites increased after an epiphytic overgrowth of the algaHincksia mitchelliaeat the unsheltered site. Seagrass growth was suppressed and the numbers of burrowing and opportunistic benthic species increased with the increase of algal biomass. In the protected meadow, seagrass biomass and number of leaves changed seasonally, but macrobenthic abundance and species richness remained stable. Ecosystem changes were evident when the unsheltered meadow was already collapsing. The number of leaves per shoot, the horizontal internode length, the abundance and structure of the macrofaunal associations, and the host-epiphyte surface interactions, were the first variables to reflect the early stages of seagrass regression. Our results suggest that the persistence ofH. wrightiimeadows at their southern distribution limit in the SW Atlantic will be affected by local hydrodynamics and their ability to compete with ephemeral macroalgal species under stress conditions.

Strong leaf surface basification and CO2limitation of seagrass induced by epiphytic biofilm microenvironments

Coastal eutrophication is a growing problem worldwide, leading to increased epiphyte overgrowth of seagrass leaves. Yet little is known about how epiphytes affect key biogeochemical conditions and processes in the seagrass phyllosphere. We used electrochemical microsensors to measure microgradients of O2 , pH, and CO2 at the bare and epiphyte-covered leaf surface of seagrass (Zostera marina L.) to determine effects of epiphytes on the leaf chemical microenvironment. Epiphytes result in extreme daily fluctuations in pH, O2 , and inorganic carbon concentrations at the seagrass leaf surface severely hampering the plant's performance. In light, leaf epiphyte biofilms and their diffusive boundary layer lead to strong basification, markedly reducing the CO2 and HCO3 - availability at the leaf surface, leading to reduced photosynthetic efficiency as a result of carbon limitation and enhanced photorespiration. With epiphytes, leaf surface pH increased to >10, thereby exceeding final pH levels (~9.62) and CO2 compensation points for active photosynthesis. In darkness, epiphyte biofilms resulted in increased CO2 and hypoxia at the leaf surface. Epiphytes can lead to severe carbon limitation in seagrasses owing to strong phyllosphere basification leading to CO2 depletion and costly, yet limiting, HCO3 - utilization, increasing the risk of plant starvation.

Low recruitment, high tissue loss, and juvenile mortality limit recovery of kelp following large-scale defoliation

Low recruitment due to limitations of propagule supply or post-settlement survival reinforces dominance of turf algal assemblages that replace canopy algae following large-scale losses. However, post-recruitment processes that hinder juvenile growth and survival (epiphytic overgrowth, grazing, physical stress) also could impede recovery. To evaluate the contribution of recruitment, growth, and survival of young sporophytes to recovery of degraded kelp populations and key factors driving post-recruitment tissue loss and mortality, we followed cohorts of juvenile kelp Saccharina latissima at two defoliated sites in Nova Scotia. We also monitored kelp recruitment, abundance, size structure, and macroalgal composition for 5.5 years. Recruit densities were an order of magnitude lower compared to previous studies in the region. Large decreases in blade area of juveniles were related to cover by the invasive bryozoan Membranipora membranacea, grazing by small snails Lacuna vincta, and warm seawater temperatures. Cohort survival was low (time to 50% mortality 2.5–5.5 months) and increased risk of death was directly related to bryozoan encrustation. Modest seasonal or interannual gains in kelp abundance were lost during periods of peak temperature, which showed a warming trend during the study, favouring persistence of widespread turf-forming, opportunistic and invasive algae. We conclude that low recruitment success, high rate of tissue loss relative to growth, and high mortality, inhibited kelp recovery. Impacts of epiphytic overgrowth, grazing, and warm temperatures on these processes highlight the need to protect intact kelp populations, growing in favourable conditions, to maintain positive interactions that increase resilience to undesirable regime shifts.

CO<sub>2</sub> and nutrient-driven changes across multiple levels of organization in <i>Zostera noltii</i> ecosystems

Abstract. Increasing evidence emphasizes that the effects of human impacts on ecosystems must be investigated using designs that incorporate the responses across levels of biological organization as well as the effects of multiple stressors. Here we implemented a mesocosm experiment to investigate how the individual and interactive effects of CO2 enrichment and eutrophication scale-up from changes in primary producers at the individual (biochemistry) or population level (production, reproduction, and/or abundance) to higher levels of community (macroalgae abundance, herbivory, and global metabolism), and ecosystem organization (detritus release and carbon sink capacity). The responses of Zostera noltii seagrass meadows growing in low- and high-nutrient field conditions were compared. In both meadows, the expected CO2 benefits on Z. noltii leaf production were suppressed by epiphyte overgrowth, with no direct CO2 effect on plant biochemistry or population-level traits. Multi-level meadow response to nutrients was faster and stronger than to CO2. Nutrient enrichment promoted the nutritional quality of Z. noltii (high N, low C : N and phenolics), the growth of epiphytic pennate diatoms and purple bacteria, and shoot mortality. In the low-nutrient meadow, individual effects of CO2 and nutrients separately resulted in reduced carbon storage in the sediment, probably due to enhanced microbial degradation of more labile organic matter. These changes, however, had no effect on herbivory or on community metabolism. Interestingly, individual effects of CO2 or nutrient addition on epiphytes, shoot mortality, and carbon storage were attenuated when nutrients and CO2 acted simultaneously. This suggests CO2-induced benefits on eutrophic meadows. In the high-nutrient meadow, a striking shoot decline caused by amphipod overgrazing masked the response to CO2 and nutrient additions. Our results reveal that under future scenarios of CO2, the responses of seagrass ecosystems will be complex and context-dependent, being mediated by epiphyte overgrowth rather than by direct effects on plant biochemistry. Overall, we found that the responses of seagrass meadows to individual and interactive effects of CO2 and nutrient enrichment varied depending on interactions among species and connections between organization levels.

Leaf vs. epiphyte nitrogen uptake in a nutrient enriched Mediterranean seagrass ( Posidonia oceanica) meadow

In situ nitrogen uptake by leaves and epiphytes was studied in a Mediterranean seagrass ( Posidonia oceanica) meadow impacted from a fish farm and a pristine meadow, using 15NH 4 and 15NO 3 as tracers. In the impacted meadow both leaves and epiphytes yielded higher N concentrations and showed higher specific N uptake, suggesting a linkage between N uptake and its accumulation. Epiphytes took up N faster than leaves in relation to their corresponding biomass, but when assessed per unit area, N uptake was higher in leaves. Leaf N uptake was negatively correlated with epiphyte N uptake. With increasing epiphyte load on leaves, N leaf uptake decreased while N epiphyte uptake increased, indicating that epiphyte overgrowth hinders N uptake by P. oceanica leaves. Epiphyte contribution to total N uptake increased, while that of leaves decreased at the impacted meadow. However, 2–3 times less N was transferred daily from the water column to the benthic compartment, through seagrass and epiphyte uptake on total, at the impacted meadow. Therefore, it is probably still the loss of the key species – the seagrass – which plays the most important role in N cycling in seagrass ecosystems.

Long-Term Effects of Adding Nutrients to an Oligotrophic Coastal Environment

Management of ecological disturbances requires an understanding of the time scale and dynamics of community responses to disturbance events. To characterize long-term seagrass bed responses to nutrient enrichment, we established six study sites in Florida Bay, USA. In 24 plots (0.25 m2) at each site, we regularly added nitrogen (N) and phosphorus (P) in a factorial design for 7 years. Five of the six sites exhibited strong P limitation. Over the first 2 years, P enrichment increased Thalassia testudinum cover in the three most P-limited sites. After 3 years, Halodule wrightii began to colonize many of the P-addition plots, but the degree of colonization was variable among sites, possibly due to differences in the supply of viable propagules. Thalassia increased its allocation to aboveground tissue in response to P enrichment; Halodule increased in total biomass but did not appear to change its aboveground: belowground tissue allocation. Nutrient enrichment did not cause macroalgal or epiphytic overgrowth of the seagrass. Nitrogen retention in the study plots was variable but relatively low, whereas phosphorus retention was very high, often exceeding 100% of the P added as fertilizer over the course of our experiments. Phosphorus retentions exceeding 100% may have been facilitated by increases in Thalassia aboveground biomass, which promoted the settlement of suspended particulate matter containing phosphorus. Our study demonstrated that low-intensity press disturbance events such as phosphorus enrichment can initiate a slow, ramped successional process that may alter community structure over many years.

CONSUMERS AFFECT PREY BIOMASS AND DIVERSITY THROUGH RESOURCE PARTITIONING

Consumer presence and nutrient availability can have contrasting and interactive effects on plant diversity. In a factorial experiment, we manipulated two levels of nutrient supply and the presence of two moderately specialized grazers in different combinations (no grazers, two species in monoculture, and both in combination). We tested how nutrients and grazers regulated the biomass of marine coastal epiphytes and the diversity of algal assemblages, based on the prediction that the effect of consumers on prey diversity depends on productivity and consumer specialization. Nutrient enrichment increased the epiphytic load, while monocultures of single grazer species partly prevented epiphyte growth. However, only the presence of two species with complementary feeding preferences effectively prevented epiphyte overgrowth. The epiphytes comprised micro- and macroalgal species, and the diversity of these algal assemblages differed, depending on grazer identity. For the microalgae, diversity was reduced by nutrient addition when grazer control was inefficient, but not when specialist microalgal grazers were present. Macroalgal diversity was reduced in ambient water with specialist macroalgal grazers compared to the treatment with inefficient ones. These results indicate that grazer composition and productivity are crucial in determining whether consumer pressure will have a positive or negative effect on algal diversity.

Field biology of Halimeda tuna (Bryopsidales, Chlorophyta) across a depth gradient: comparative growth, survivorship, recruitment, and reproduction

Growth, survivorship, recruitment, and reproduction of Halimeda tuna, a dominant green alga in many reef systems of the Florida Keys, were monitored at a shallow back reef (4–7m) and deep reef slope (15–22 m) on Conch Reef. Despite lower light intensities and similar grazing pressures, amphipod infestations, and epiphyte loads at both sites, the deeper site exhibited significantly higher growth rates in summer months over a 4-year period than found for the shallow population, possibly because of higher nutrient levels at depth and photoinhibition of shallow plants. Sexual reproductive events occurred simultaneously across the entire reef, with up to 5% of the population at both sites developing gametangia. New upright axes formed from zygotes, asexual fragmentation, or vegetative runners. Plants appear to have persistent basal stumps that survive harsh environmental conditions, even if upright, photosynthetic axes are removed. Sexual reproduction and ‘smothering’ by epiphyte overgrowth are hypothesized to be two causes of death for individuals.

Effects of Fish Farm Loadings on Seagrass (Posidonia oceanica) Distribution, Growth and Photosynthesis

The spatial extent and timing of the impact of fish farms on the distribution and performance of a Posidonia oceanica meadow were examined in an embayment of the south-eastern coast of Spain (Hornillo Bay, Murcia). Changes in seagrass distribution were determined using available seagrass mapping (from 1988, i.e., before the onset of aquaculture activities and 1998) and by successive sampling in 1994 and 1998. Environmental variables (light attenuation coefficient, water-column dissolved nutrients and organic content of sediments) together with plant performance (shoot biomass, leaf growth rate, photosynthetic activity, carbohydrate reserves, the number of leaves per shoot, epiphyte loads and herbivore pressure) were measured in plants affected by organic discharges, and were compared with those found in reference healthy plants over an annual growth cycle. Since the onset of fish farm activity, 11.29 ha of P. oceanica meadow has been completely lost and 9.86 ha significantly degraded, thus resulting in a total affected area which accounts for about 53% of the former meadow, or 7-fold the fish farming area. Unequal propagation of seagrass die-off or degradation reflects the relevance of local factors such as depth and hydrodynamism on the true extent of fish farm impact. Water transparency decreases and dissolved nutrient and organic content of sediments increases in the vicinity of cages compared to distant reference stations, thus supporting the notion of environmental gradients caused by the organic release from cages, which spreads outwards. Shoot size, leaf growth rate and the number of leaves per shoot in plants close to the fish farm decreased. Moreover, low leaf growth and low rhizome carbohydrate concentration (always relative to that found in an undisturbed area) indicated carbon budget imbalances. Since light reduction in the affected area was only modest (31% of light reaching the sea surface, while at the same depth this figure was 39% at the reference site), and light availability was well above the minimum requirement estimated for this species, neither this factor nor epiphyte overgrowth (epiphyte load was lower in the affected area) seem to explain such carbon imbalances or the observed meadow regression. Alternatively, the high herbivore pressure found in the affected zone suggests that overgrazing is one of the main causes of decreasing shoot sizes and hence of carbon imbalance, reduced growth and shoot mortality. The impact of fish farms on seagrasses, therefore, seems to be highly variable and depends on complex interactions between a large number of processes.

Epiphytic Overgrowth of Charophyte Thalli by Stromatolite-like Structures and Fungi in the Lower Cretaceous of the Iberian Ranges (Spain)

The Lower Cretaceous (113 million years old) lacustrine deposits of Las Hoyas(Iberian Ranges, Cuenca, Spain) yield an epiphytic assemblage formed by thecharophyte species Clavatoraxis diaz-romeraliiMartín-Closas & Diéguez overgrown by a muddy, laminatedstromatolite-like structure. Fossil charophyte thalli coated with biogeniclaminations were previously unknown from the fossil record. Within thisstromatolite-like structure, filaments are found which correspond to thalli ofanother charophyte, Palaeonitella vermicularisMartín-Closas & Diéguez, and to septate hyphae of fungi(Ascomycetes). The distribution pattern of the biogenic lamination and itsselective growth only on the strongest thalli ofClavatoraxis diaz-romeralii suggests that it occurredwhen these macrophytes were still alive, standing upright on the lake bottom.From this point of view the stromatolite-like structures are reminiscent ofextant overgrowths of charophyte thalli by epiphytic, filamentouscyanobacteria, eucaryotic algae and fungi. These assemblages appear to developafter eutrophication of nutrient-poor environments, which are more suitablefor charophyte growth.

Preliminary Data on Alkaline Phosphatase Activity Associated with Mediterranean Seagrasses

Alkaline phosphatase activity (APA) was measured in two species of Mediterranean seagrasses, Posidonia oceanica (L.) Delile and Cymodocea nodosa (Ucria) Ascherson, under different nutritional conditions, both natural and experimental. The levels of APA were higher in old leaves, partially due to massive epiphytic overgrowth, and low but detectable in roots; APA decreased with increasing nutrient levels, and a good correlation was found between the rise of P content in vegetative tissues following nutrient addition and the concomitant decrease in APA values. We conclude that APA may be a good indicator of seagrass nutritional status

STUDIES OF MESOHERBIVORY IN AQUARIA AND IN AN UNBARRICADED MARICULTURE FARM ON THE CHINESE COAST1

ABSTRACTThe effects upon macrophytic and epiphytic algae of caprellid amphipods, including Caprella irregularis Mayer, and of gammarid amphipods, including Ampithoe lacertosa Bate, Jassa falcata (Montagu) and Pontogeneia rostrata Gurjanova, were studied in aquaria and in a coastal mariculture farm near Qingdao, People's Republic of China. The macrophytic species studied included Enteromorpha linza (L.) J. Agardh, Gracilaria asiatica Zhang & Xia, Gracilaria lemaneiformis (Bory) Weber‐van Bosse and Scytosiphon lomentaria (Lyngbye) C. Agardh. These algae and amphipods were selected for study because of their local abundances. Aquarium experiments demonstrated that C. irregularis, J. falcata and P. rostrata feed on ephemeral/epiphytic algae. A. lacertosa (adults and juveniles) ate Gracilaria but preferred E. linza. The different species of amphipods had substantially different patterns of daily activity.Caprellids prevented epiphytic overgrowth of G. asiatica when added to plants in an experimental, openocean, mariculture farm, despite the presence of numerous amphipod predators (e.g. the fishes Hexagrammos otakii Jordan & Starks and Sebastes thompsoni Jordan & Hubbs). Periodic removals of all (naturally colonizing) amphipods from another group of plants in the farm resulted in heavy epiphytic overgrowth. Since these results were obtained in an unbarricaded mariculture farm, we conclude that mesoherbivores may have large effects upon algal community structure in temperate intertidal and subtidal habitats.