Análise da variação espaço-temporal em diferentes escalas sobre a distribuição ecológica das comunidades de macroalgas de duas bacias de drenagem da região centro-sul do estado do Paraná

Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)

Estrutura das comunidades de macroalgas da bacia de drenagem do rio Cascavel, Estado do Paraná, Brasil

The drainage basin of Cascavel River is almost entirely within the urban perimeter of Guarapuava, Paraná State, Brazil. Seven stream segments were sampled in two seasons (summer and winter). We found 12 taxa of macroalgae with a dominance of Chlorophyta (seven taxa) followed by Cyanophyta (three taxa), Heterokontophyta and Rhodophyta (one taxon each). Richness, diversity, and evenness were higher during the winter while the abundance and dominance were higher in the summer. Among the microenvironmental characteristics, the current velocity was the only one that differed significantly between the periods. The regression analysis revealed that the richness of the substrate was responsible for the variation in richness, diversity, evenness, and dominance during the summer period. During the winter the current velocity was responsible for the variation of species diversity. A cluster analysis of macroalgal communities did not group points in the same temporal period. The Canonical Correspondence Analysis (CCA) showed that the segments were close to each other because of the occurrence of one or a few species in common. The patterns of spatial and temporal distribution of stream macroalgae seem to be strongly influenced by microhabitat characteristics at different scales.However, they aresupported by regional variables.

Riqueza, abundância e sazonalidade de comunidades de macroalgas em diferentes escalas espaciais em riachos da região centr-sul do estado do Paraná

Conselho Nacional de Desenvolvimento Cientifico e Tecnológico (CNPq)

Distribution of stream macroalgae in the northwest region of Sao Paulo State, southeastern Brazil

Forty-four stream segments were sampled from May to October in 1992 and 1993 in the northwest region of São Paulo State, southeastern Brazil (19 degrees 45'-21 degrees 25'S, 49 degrees 05'-51 degrees 30'S). Thirty-six macroalgal subgeneric taxa were found and Chlorophyta was the dominant algal group (47% species), followed by Cyanophyta (33.5%), Rhodophyta (14%) and Chrysophyta (5.5%). The most widespread species were Stigeoclonium helveticum (25% sites), Batrachospermum delicatulum and Compsopogon coeruleus (20.5%). Distribution was patchy, with species number per sampling site ranging from 0 to six (3.1 +/- 1.7) and correlated positively with species abundance. Species cover ranged from 0 to 61% of the stream bottom (19.1 +/- 19.7%). Most sites (57%) were dominated by one or two macroalgae species. No significant difference was found between the frequency distribution of variables measured for streams and for total macroalgae, but the most widespread species differed for most parameters and occurred over wider ranges of environmental conditions. Mean species number and abundance were close to values found in distinct regions or biomes of North America. Higher conductance and lower oxygen values, as well as rocky substrata, generally constituted the most favourable combination of conditions for the development of macroalgae in the region. The pattern of strong dominance of few species was considered to be typical for stream macroalgal communities in general.

Spatial competition induces the mobilization of morula cells in the colonial ascidian Didemnum perlucidum (Tunicata: Didemnidae)

The effects of spatial competition among colonial marine organisms are often evident in the contact zones between colonies. These effects are especially pronounced when the interaction results in overgrowth or necrosis of one of the competitors. Ascidians, one of the dominant taxonomic groups in subtidal sessile communities, have specialized morula cells that provide a defense against microbial infections. Injuries resulting from interspecific competitive interactions might also act as a stimulus for this defensive mechanism. Therefore, we expected to see the recruitment of morula cells in tissues near competitor contact zones. To test the hypothesis that spatial competition elicits this immune response, we placed colonies of the ascidian Didemnum perlucidum from southeastern Brazil in four different types of competitive situations: (1) overgrowth of the competitor, (2) stand-off interactions, (3) overgrowth by the competitor, and (4) free of competitors. Our results indicate that competitive interactions increase the population of morula cells in contact zones, as more cells were observed in interactions that resulted in the overgrowth of individuals of D. perlucidum, and fewer cells were observed in colonies that were free of competitors. We identified the defensive function of the morula cells by showing the presence of the enzyme phenoloxidase within its vacuoles. Phenoloxidase is a widespread enzyme among animals and plants, and is frequently used in defense by synthesizing toxic quinones from polyphenol substrates. This is the first study to document the presence of morula cells in didemnid ascidians and the mobilization of these cells by spatial competition by heterospecifics, and one of the first studies to identify phenoloxidase activity in morula cells.

(Table 1) Presence of sublittoral macroalgae in the investigated profiles in Potter Cove, King George Island, Antarctica

The vegetation of a small fjord and its adjacent open shore was documented by subaquatic video. The distribution of individual species of macroalgae and the composition of assemblages were compared with gradients of light availability, hydrography, slope inclination, substratum, and exposition to turbulence and ice. The sublittoral fringe is usually abraded by winterly ice floes and devoid of large, perennial algae. Below this zone, the upper sublittoral is dominated by Desmarestia menziesii on steep rock faces, where water movements become irregular, or by Ascoseira mirabilis and Palmaria decipiens on weakly inclined slopes with steady rolling water movements. In the central sublittoral above 15 m, where turbulence is still active, Desmarestia anceps is outcompeting all other species on solid substratum, However, the species is not able to persist on loose material under these conditions. Instead, Himantothallus grandifolius may occur. Deeper, where turbulence usually is negligible, Desmarestia anceps also covers loose material. The change of dominance to Himantothallus grandifolius in the deep sublittoral cannot completely be explained at present. Himantothallus grandifolius also prevails in a mixed assemblage under the influence of grounding icebergs. Most of the smaller algae are opportunists with different degrees of tolerance for turbulence, but some apparently need more stable microhabitats and thus are dependent from continuing suppression of competitive large phaeophytes.

Spatial community shift from hard to soft corals in acidified water

Anthropogenic increases in the partial pressure of CO2 (pCO2) cause ocean acidification, declining calcium carbonate saturation states, reduced coral reef calcification and changes in the compositions of marine communities. Most projected community changes due to ocean acidification describe transitions from hard coral to non-calcifying macroalgal communities; other organisms have received less attention, despite the biotic diversity of coral reef communities. We show that the spatial distributions of both hard and soft coral communities in volcanically acidified, semi-enclosed waters off Iwotorishima Island, Japan, are related to pCO2 levels. Hard corals are restricted to non-acidified low- pCO2 (225 µatm) zones, dense populations of the soft coral Sarcophyton elegans dominate medium- pCO2 (831 µatm) zones, and both hard and soft corals are absent from the highest- pCO2 (1,465 µatm) zone. In CO2-enriched culture experiments, high- pCO2 conditions benefited Sarcophyton elegans by enhancing photosynthesis rates and did not affect light calcification, but dark decalcification (negative net calcification) increased with increasing pCO2. These results suggest that reef communities may shift from reef-building hard corals to non-reef-building soft corals under pCO2 levels (550-970 µatm) predicted by the end of this century, and that higher pCO2 levels would challenge the survival of some reef organisms.

Experiment: Elevated CO2 levels affect the activity of nitrate reductase and carbonic anhydrase in the calcifying rhodophyte Corallina officinalis

The concentration of CO2 in global surface ocean waters is increasing due to rising atmospheric CO2 emissions, resulting in lower pH and a lower saturation state of carbonate ions. Such changes in seawater chemistry are expected to impact calcification in calcifying marine organisms. However, other physiological processes related to calcification might also be affected, including enzyme activity. In a mesocosm experiment, macroalgal communities were exposed to three CO2 concentrations (380, 665, and 1486 µatm) to determine how the activity of two enzymes related to inorganic carbon uptake and nutrient assimilation in Corallina officinalis, an abundant calcifying rhodophyte, will be affected by elevated CO2 concentrations. The activity of external carbonic anhydrase, an important enzyme functioning in macroalgal carbon-concentrating mechanisms, was inversely related to CO2 concentration after long-term exposure (12 weeks). Nitrate reductase, the enzyme responsible for reduction of nitrate to nitrite, was stimulated by CO2 and was highest in algae grown at 665 µatm CO2. Nitrate and phosphate uptake rates were inversely related to CO2, while ammonium uptake was unaffected, and the percentage of inorganic carbon in the algal skeleton decreased with increasing CO2. The results indicate that the processes of inorganic carbon and nutrient uptake and assimilation are affected by elevated CO2 due to changes in enzyme activity, which change the energy balance and physiological status of C. officinalis, therefore affecting its competitive interactions with other macroalgae. The ecological implications of the physiological changes in C. officinalis in response to elevated CO2 are discussed.

Biogenic and environmental fluctuations of temperature and pH in a novel mesocosm concept ("Kiel Outdoor Benthocosms") April 2013 to September 2014

The Kiel Outdoor Benthocosm infrastructure (Kiel, Germany,N 54°19.8'; E 010°09.0') allows combining natural in-situ fluctuations on all environmental variables with the controlled manipulation of treatment factors. The environmental fluctuations are admitted by a continuous flow-through of fjord water. The treatment is applied by delta-treatments which shift the mean of target variables (temperature and pH in this case) while maintaining the frequency and amplitude of natural fluctuations. The data presented here show the treatment levels and the continuously logged temperature and pH conditions in the experimental tanks. The dynamics of temperature and pH are driven by (i) in situ variability, (ii) the treatments imposed and (iii) the biology of the biota in the tanks. These contained macroalgal communities with associated mesograzers, mussels, and sea stars. The data set comprised 5 experimental runs: spring experiment (4.4.-19.6.2013), summer experiment 1 (4.7.-17.9.2013), autumn experiment (10.10-17.12.2013), winter experiment (16.1. - 1.4.2014), summer experiment 2 (10.7. - 26.9.2014).

Spatial and temporal variation in algal-assemblage structure in isolated dryland river waterholes, Cooper Creek and Warrego River, Australia

The scale at which algal biodiversity is partitioned across the landscape, and the biophysical processes and biotic interactions which shape these communities in dryland river refugia was studied on two occasions from 30 sites in two Australian dryland rivers. Despite the waterholes studied having characteristically high levels of abiogenic turbidity, a total of 186 planktonic microalgae, 253 benthic diatom and 62 macroalgal species were recorded. The phytoplankton communities were dominated by flagellated cryptophytes, euglenophytes and chlorophytes, the diatom communities by cosmopolitan taxa known to tolerate wide environmental conditions, and the macroalgal communities by filamentous cyanobacteria. All algal communities showed significant differences between catchments and sampling times, with a suite of between 5 and 12 taxa responsible for similar to 50% of the observed change. In general, algal assemblage patterns were poorly correlated with the measured environmental variables. Phytoplankton and diatom assemblage patterns were weakly correlated with several waterhole geomorphic measures, whereas macroalgal assemblage patterns showed some association with variability in ionic concentration.

Herbivores strongly influence algal recruitment in both coral- and algal-dominated coral reef habitats

Coral reefs can exist as coral- and macroalgae-dominated habitats often separated by only a few hundred metres. While herbivorous fish are known to depress the abundance of algae and help maintain the function of coral-dominated habitats, less is known about their influence in algae-dominated habitats. Here, we quantified herbivorous fish and benthic algal communities over a 6 mo period in coral-dominated (back-reef) and algal-dominated (lagoon) habitats in a relatively undisturbed fringing coral reef (Ningaloo, Western Australia). Simulta - neously, we tested the effects of herbivorous fish on algal recruitment in both habitats using recruitment tiles and fish exclusion cages. The composition of established algal communities differed consistently between habitats, with the back-reef hosting a more diverse community than the Sargassum-dominated lagoon. However, total algal biomass and cover only differed between habitats in autumn, coinciding with maximum Sargassum biomass. The back-reef hosted high coral cover and a diverse herbivorous fish community, with herbivore biomass an order of magnitude greater than the lagoon. Despite these differences in herbivore composition, exclusion of large herbivores had a similar positive effect to foliose macroalgae recruitment on experimental tiles in both back-reef and lagoon habitats. Additionally, territorial damselfish found in the backreef increased turf algae cover and decreased crustose coralline algae cover on recruitment tiles. Collectively, our results show that disparate herbivorous fish communities in coral- and algaedominated habitats are similarly able to limit the recruitment of foliose macroalgae, but suggest that when herbivorous fish biomass and diversity are relatively low, macroalgal communities are able to escape herbivore control through increased growth.

Dynamic ecosystems under anthropogenic stress : how does macrotidal sandy fauna respond to green tides?

Highly dynamic systems, often considered as resilient systems, are characterised by abiotic and biotic processes under continuous and strong changes in space and time. Because of this variability, the detection of overlapping anthropogenic stress is challenging. Coastal areas harbour dynamic ecosystems in the form of open sandy beaches, which cover the vast majority of the world’s ice-free coastline. These ecosystems are currently threatened by increasing human-induced pressure, among which mass-development of opportunistic macroalgae (mainly composed of Chlorophyta, so called green tides), resulting from the eutrophication of coastal waters. The ecological impact of opportunistic macroalgal blooms (green tides, and blooms formed by other opportunistic taxa), has long been evaluated within sheltered and non-tidal ecosystems. Little is known, however, on how more dynamic ecosystems, such as open macrotidal sandy beaches, respond to such stress. This thesis assesses the effects of anthropogenic stress on the structure and the functioning of highly dynamic ecosystems using sandy beaches impacted by green tides as a study case. The thesis is based on four field studies, which analyse natural sandy sediment benthic community dynamics over several temporal (from month to multi-year) and spatial (from local to regional) scales. In this thesis, I report long-lasting responses of sandy beach benthic invertebrate communities to green tides, across thousands of kilometres and over seven years; and highlight more pronounced responses of zoobenthos living in exposed sandy beaches compared to semi-exposed sands. Within exposed sandy sediments, and across a vertical scale (from inshore to nearshore sandy habitats), I also demonstrate that the effects of the presence of algal mats on intertidal benthic invertebrate communities is more pronounced than that on subtidal benthic invertebrate assemblages, but also than on flatfish communities. Focussing on small-scale variations in the most affected faunal group (i.e. benthic invertebrates living at low shore), this thesis reveals a decrease in overall beta-diversity along a eutrophication-gradient manifested in the form of green tides, as well as the increasing importance of biological variables in explaining ecological variability of sandy beach macrobenthic assemblages along the same gradient. To illustrate the processes associated with the structural shifts observed where green tides occurred, I investigated the effects of high biomasses of opportunistic macroalgae (Ulva spp.) on the trophic structure and functioning of sandy beaches. This work reveals a progressive simplification of sandy beach food web structure and a modification of energy pathways over time, through direct and indirect effects of Ulva mats on several trophic levels. Through this thesis I demonstrate that highly dynamic systems respond differently (e.g. shift in δ13C, not in δ15N) and more subtly (e.g. no mass-mortality in benthos was found) to anthropogenic stress compared to what has been previously shown within more sheltered and non-tidal systems. Obtaining these results would not have been possible without the approach used through this work; I thus present a framework coupling field investigations with analytical approaches to describe shifts in highly variable ecosystems under human-induced stress.

Macroalgal Defenses Against Herbivory: Causes and Consequences of Intraspecific Variation

In marine benthic communities, herbivores consume a considerable proportion of primary producer biomass and, thus, generate selection for the evolution of resistance traits. According to the theory of plant defenses, resistance traits are costly to produce and, consequently, inducible resistance traits are adaptive in conditions of variable herbivory, while in conditions of constant/strong herbivory constitutive resistance traits are selected for. The evolution of resistance plasticity may be constrained by the costs of resistance or lack of genetic variation in resistance. Furthermore, resource allocation to induced resistance may be affected by higher trophic levels preying on herbivores. I studied the resistance to herbivory of a foundation species, the brown alga Fucus vesiculosus. By using factorial field experiments, I explored the effects of herbivores and fish predators on growth and resistance of the alga in two seasons. I explored genetic variation in and allocation costs of resistance traits as well as their chemical basis and their effects on herbivore performance. Using a field experiment I tested if induced resistance spreads via water-borne cues from one individual to another in relevant ecological conditions. I found that in the northern Baltic Sea F. vesiculosus communities, strength of three trophic interactions strongly vary among seasons. The highly synchronized summer reproduction of herbivores promoted their escape from the top-down control of fish predators in autumn. This resulted into large grazing losses in algal stands. In spring, herbivore densities were low and regulated by fish, which, thus,enhanced algal growth. The resistance of algae to herbivory increased with an increase in constitutive phlorotannin content. Furthermore, individuals adopted induced resistance when grazed and when exposed to water-borne cues originating from grazing of conspecific algae both in the laboratory and in field conditions. Induced resistance was adopted to a lesser extent in the presence of fish predators. The results in this thesis indicate that inducible resistance in F. vesiculosus is an adaptation to varying herbivory in the northern Baltic Sea. The costs of resistance and strong seasonality of herbivory have likely contributed to the evolution of this defense strategy. My findings also show that fish predators have positive cascading effects on F. vesiculosus which arise via reduced herbivory but possibly also through reduced resource allocation to resistance. I further found evidence that the spread of resistance via water-borne cues also occurs in ecologically realistic conditions in natural marine sublittoral. Thus, water-borne induction may enable macroalgae to cope with the strong grazing pressure characteristic of marine benthic communities. The results presented here show that seasonality can have pronounced effects on the biotic interactions in marine benthic communities and thereafter influence the evolution of resistance traits in primary producers.

Influence of occupant microhabitat on the composition of encrusting communities on gastropod shells

The exploitation of microhabitats is widely considered to increase biodiversity in marine ecosystems. Although intertidal hermit crabs and gastropods may inhabit the same shell type and shore level, their microhabitat may differ depending on the state of the tide. On the south coast of Wales the hermit crab Pagurus bernhardus mainly inhabits the shells of Nucella lapillus (84%). Hermit crab shells had a significantly different encrusting community compared with live N. lapillus shells. At low tide the live gastropods were found on exposed rock surfaces whereas hermit crabs were restricted to tidal pools. Communities encrusting live gastropod shells were characterised by lower species richness and abundance compared with shells inhabited by hermit crabs (12 species found in total). A greater abundance and richness of epibionts was recorded from both shell types during the summer compared with winter. Differences in community composition between shell occupant types were attributed to microhabitats used by gastropods and hermit crabs and the associated desiccation pressures, rather than competitive interactions or shell characteristics. This contradicts earlier studies of subtidal shells where biological processes were considered more important than physical factors in controlling species abundance and richness patterns. The use of rockpool microhabitats by hermit crabs increases the biodiversity of rocky shores, as some species commonly found on hermit-crab-inhabited shells were rare in other local habitats.

Species name, classification (WORMS), abundance and biomass of the megabenthic communities of the Algarve

The present study analysed the megabenthic diversity in subtidal soft bottoms and assessed the main environmental drivers of megabenthic community organisation along the Algarve coast (southern Portugal). We tested the hypothesis that megabenthic communities respond to the same environmental drivers than macrofauna. We found that similar to macrofauna, megafaunal communities were organised in relation to the depth of closure, light reaching the bottom, and the hydrodynamic conditions related with exposure within the shallower areas. The influence of the main river outflow prevailed over other drivers, but only up to 9 m depth. We found that seven different spatial units should be considered, each characterised by different indicator species. Additionally, among a total of 412 taxa collected between 4 and 50 m depth, we provide the characteristics of the 64 commonest species in terms of occurrence, frequency, distribution, abundance, bathymetric and sedimentary preferences, which constitutes most valuable information for ecosystem modelling. Megabenthic alpha diversity decreased with depth, contrary to evenness and was higher in the proximity of the river Guadiana and in highly exposed shores. We conclude that the megafauna, which is significantly quicker to collect and analyse, can provide an accurate alternative to macrofauna sampling, as their communities are shaped by the same drivers.