Dispersal mitigates bacterial dominance over microalgal competitor in metacommunities.

Ecological theory suggests that a combination of local and regional factors regulate biodiversity and community functioning in metacommunities. The relative importance of different factors structuring communities likely changes over successional time, but to date this concept is scarcely documented. In addition, the few studies describing successional dynamics in metacommunity regulation have only focused on a single group of organisms. Here, we report results of an experimental study testing the effect size of initial local community composition and dispersal between local patches on community dynamics of benthic microalgae and their associated bacteria over community succession. Our results show that over time dispersal outweighed initial effects of community composition on microalgal evenness and biomass, microalgal ß-diversity, and the ratio of bacteria to microalgae. At the end of the experiment (ca. 20 microalgae generations), dispersal significantly decreased microalgal evenness and ß-diversity by promoting one regionally superior competitor. Dispersal also decreased the ratio of bacteria to microalgae, while it significantly increased microalgal biomass. These results suggest that the dispersal-mediated establishment of a dominant and superior microalgae species prevented bacteria from gaining competitive advantage over the autotrophs in these metacommunities, ultimately maintaining the provision of autotrophic biomass. Our study emphasizes the importance of time for dispersal to be a relevant community-structuring mechanism. Moreover, we highlight the need for considering multiple competitors in complex metacommunity systems to properly pinpoint the consequences of local change in dominance through dispersal for metacommunity function.

Inter- and intraspecific phenotypic plasticity of three phytoplankton species in response to ocean acidification.

Phenotypic plasticity describes the phenotypic adjustment of the same genotype to different environmental conditions and is best described by a reaction norm. We focus on the effect of ocean acidification on inter- and intraspecific reaction norms of three globally important phytoplankton species (Emiliania huxleyi, Gephyrocapsa oceanica and Chaetoceros affinis). Despite significant differences in growth rates between the species, they all showed a high potential for phenotypic buffering (similar growth rates between ambient and high CO2 conditions). Only three coccolithophore genotypes showed a reduced growth in high CO2 Diverging responses to high CO2 of single coccolithophore genotypes compared with the respective mean species responses, however, raise the question of whether an extrapolation to the population level is possible from single-genotype experiments. We therefore compared the mean response of all tested genotypes with a total species response comprising the same genotypes, which was not significantly different in the coccolithophores. Assessing species reaction norms to different environmental conditions on short time scale in a genotype-mix could thus reduce sampling effort while increasing predictive power.

Temperature effects on seaweed-sustaining top-down control vary with season.

Rising seawater temperature and CO2 concentrations (ocean acidification) represent two of the most influential factors impacting marine ecosystems in the face of global climate change. In ecological climate change research, full-factorial experiments performed across seasons in multispecies, cross-trophic-level settings are essential as they permit a more realistic estimation of direct and indirect effects as well as the relative importance of the effects of both major environmental stressors on ecosystems. In benthic mesocosm experiments, we tested the responses of coastal Baltic Sea Fucus vesiculosus communities to elevated seawater temperature and CO2 concentrations across four seasons of one year. While increasing [CO2] levels had only minor effects, warming had strong and persistent effects on grazers, and the resulting effects on the Fucus community were found to be season dependent. In late summer, a temperature-driven collapse of grazers caused a cascading effect from the consumers to the foundation species, resulting in overgrowth of Fucus thalli by epiphytes. In fall/winter (outside the growing season of epiphytes), intensified grazing under warming resulted in a significant reduction in Fucus biomass. Thus, we were able to confirm the prediction that future increases in water temperatures will influence marine food-web processes by altering top-down control, but we were also able to show that specific consequences for food-web structure depend on the season. Since F. vesiculosus is the dominant habitat-forming brown algal system in the Baltic Sea, its potential decline under global warming implies a loss of key functions and services such as provision of nutrient storage, substrate, food, shelter, and nursery grounds for a diverse community of marine invertebrates and fish in Baltic Sea coastal waters.

Effects of sea surface warming on marine plankton.

Ocean warming has been implicated in the observed decline of oceanic phytoplankton biomass. Some studies suggest a physical pathway of warming via stratification and nutrient flux, and others a biological effect on plankton metabolic rates; yet the relative strength and possible interaction of these mechanisms remains unknown. Here, we implement projections from a global circulation model in a mesocosm experiment to examine both mechanisms in a multi-trophic plankton community. Warming treatments had positive direct effects on phytoplankton biomass, but these were overcompensated by the negative effects of decreased nutrient flux. Zooplankton switched from phytoplankton to grazing on ciliates. These results contrast with previous experiments under nutrient-replete conditions, where warming indirectly reduced phytoplankton biomass via increased zooplankton grazing. We conclude that the effect of ocean warming on marine plankton depends on the nutrient regime, and provide a mechanistic basis for understanding global change in marine ecosystems.

Community composition has greater impact on the functioning of marine phytoplankton communities than ocean acidification.

Ecosystem functioning is simultaneously affected by changes in community composition and environmental change such as increasing atmospheric carbon dioxide (CO2 ) and subsequent ocean acidification. However, it largely remains uncertain how the effects of these factors compare to each other. Addressing this question, we experimentally tested the hypothesis that initial community composition and elevated CO2 are equally important to the regulation of phytoplankton biomass. We full-factorially exposed three compositionally different marine phytoplankton communities to two different CO2 levels and examined the effects and relative importance (ω(2) ) of the two factors and their interaction on phytoplankton biomass at bloom peak. The results showed that initial community composition had a significantly greater impact than elevated CO2 on phytoplankton biomass, which varied largely among communities. We suggest that the different initial ratios between cyanobacteria, diatoms, and dinoflagellates might be the key for the varying competitive and thus functional outcome among communities. Furthermore, the results showed that depending on initial community composition elevated CO2 selected for larger sized diatoms, which led to increased total phytoplankton biomass. This study highlights the relevance of initial community composition, which strongly drives the functional outcome, when assessing impacts of climate change on ecosystem functioning. In particular, the increase in phytoplankton biomass driven by the gain of larger sized diatoms in response to elevated CO2 potentially has strong implications for nutrient cycling and carbon export in future oceans.

Maintenance of Intraspecific Diversity in Response to Species Competition and Nutrient Fluctuations.

Intraspecific diversity is a substantial part of biodiversity, yet little is known about its maintenance. Understanding mechanisms of intraspecific diversity shifts provides realistic detail about how phytoplankton communities evolve to new environmental conditions, a process especially important in times of climate change. Here, we aimed to identify factors that maintain genotype diversity and link the observed diversity change to measured phytoplankton morpho-functional traits Vmax and cell size of the species and genotypes. In an experimental setup, the two phytoplankton species Emiliania huxleyi and Chaetoceros affinis, each consisting of nine genotypes, were cultivated separately and together under different fluctuation and nutrient regimes. Their genotype composition was assessed after 49 and 91 days, and Shannon's diversity index was calculated on the genotype level. We found that a higher intraspecific diversity can be maintained in the presence of a competitor, provided it has a substantial proportion to total biovolume. Both fluctuation and nutrient regime showed species-specific effects and especially structured genotype sorting of C. affinis. While we could relate species sorting with the measured traits, genotype diversity shifts could only be partly explained. The observed context dependency of genotype maintenance suggests that the evolutionary potential could be better understood, if studied in more natural settings including fluctuations and competition.

Composition and Dominance of Edible and Inedible Phytoplankton Predict Responses of Baltic Sea Summer Communities to Elevated Temperature and CO2.

Previous studies with Baltic Sea phytoplankton combining elevated seawater temperature with CO2 revealed the importance of size trait-based analyses, in particular dividing the plankton into edible (>5 and <100 µm) and inedible (<5 and >100 µm) size classes for mesozoopankton grazers. While the edible phytoplankton responded predominantly negative to warming and the inedible group stayed unaffected or increased, independent from edibility most phytoplankton groups gained from CO2. Because the ratio between edible and inedible taxa changes profoundly over seasons, we investigated if community responses can be predicted according to the prevailing composition of edible and inedible groups. We experimentally explored the combined effects of elevated temperatures and CO2 concentrations on a late-summer Baltic Sea community. Total phytoplankton significantly increased in response to elevated CO2 in particular in combination with temperature, driven by a significant gain of the inedible <5 µm fraction and large filamentous cyanobacteria. Large flagellates disappeared. The edible group was low as usual in summer and decreased with both factors due to enhanced copepod grazing and overall decline of small flagellates. Our results emphasize that the responses of summer communities are complex, but can be predicted by the composition and dominance of size classes and groups.

Grazing Induced Shifts in Phytoplankton Cell Size Explain the Community Response to Nutrient Supply.

Phytoplankton cell size is important for a multitude of functional traits such as growth rates, storage capabilities, and resistance to grazing. Because these response traits are correlated, selective effects on mean community cell size of one environmental factor should impact the ability of phytoplankton to cope with other factors. Here, we experimentally apply expectations on the functional importance of phytoplankton cell size to the community level. We used a natural marine plankton community, and first altered the community's cell size structure by exposing it to six different grazer densities. The size-shifted communities were then treated with a saturated nutrient pulse to test how the changes in community size structure influenced the mean community growth rate in the short-term (day 1-3) and nutrient storage capacity in the postbloom phase. Copepod grazing reduced the medium-sized phytoplankton and increased the share of the smallest (<10 µm3) and the largest (>100,000 µm3). Communities composed of on average small cells grew faster in response to the nutrient pulse, and thus confirmed the previously suggested growth advantage of small cells for the community level. In contrast, larger phytoplankton showed better storage capabilities, reflected in a slower post-bloom decline of communities that were on average composed of larger cells. Our findings underline that the easily measurable mean cell size of a taxonomically complex phytoplankton community can be used as an indicator trait to predict phytoplankton responses to sequential environmental changes.

Dispersal decreases diversity in heterogeneous metacommunities by enhancing regional competition.

Experiments and models reveal that moderate dispersal rates between local communities can increase diversity by alleviating local competitive exclusion; in contrast, high dispersal rates can decrease diversity by amplifying regional competition. However, hitherto experimental tests on how dispersal affects diversity in the presence and absence of environmental heterogeneity are largely missing, although it is known that environmental heterogeneity influences diversity. For the first time we experimentally show that the interaction between dispersal rate and the presence of an environmental gradient with on-average lower resource availability than the homogeneous control treatment affects diversity. In metacommunities of nine co-occurring species of marine benthic microalgae we factorially manipulated dispersal rate and the presence and absence of a light intensity gradient across local patches to test effects on local, regional, and beta diversity and to compare results to predictions from monoculture experiments. Although species in this experiment did not show resource partitioning along the light gradient as assumed by source-sink models, dispersal limitation maintained diversity in metacommunities with light gradients but not without. Local diversity and evenness were high under low light intensities when dispersal was limited and decreased with both increasing light intensities and dispersal rates. These diversity changes can be explained by the reduction of growth of the regional superior competitor at low light intensities alleviating its competitive strength. Increasing dispersal rate in turn compensated for the superior competitor's slow growth in those local patches with rather unfavorable light conditions and thus led to decreasing diversity and evenness. In contrast, diversity in the metacommunities without a light gradient was constantly low. Here, the superior competitor contributed 90% to total community biomass in all patches. High dominance, however, likely resulted from on-average higher resource availability (i.e., higher light intensities) compared to metacommunities with light gradient and not from patch homogeneity in itself.

Biodiversity in a complex world: consolidation and progress in functional biodiversity research.

The global decline of biodiversity caused by human domination of ecosystems worldwide is supposed to alter important process rates and state variables in these ecosystems. However, there is considerable debate on the prevalence and importance of biodiversity effects on ecosystem function (BDEF). Here, we argue that much of the debate stems from two major shortcomings. First, most studies do not directly link the traits leading to increased or decreased function to the traits needed for species coexistence and dominance. We argue that implementing a trait-based approach and broadening the perception of diversity to include trait dissimilarity or trait divergence will result in more realistic predictions on the consequences of altered biodiversity. Second, the empirical and theoretical studies do not reflect the complexity of natural ecosystems, which makes it difficult to transfer the results to natural situations of species loss. We review how different aspects of complexity (trophic structure, multifunctionality, spatial or temporal heterogeneity, and spatial population dynamics) alter our perception of BDEF. We propose future research avenues concisely testing whether acknowledging this complexity will strengthen the observed biodiversity effects. Finally, we propose that a major future task is to disentangle biodiversity effects on ecosystem function from direct changes in function due to human alterations of abiotic constraints.

Effects of grazer richness and composition on algal biomass in a closed and open marine system.

Most natural local systems exchange organisms with a regional pool of species through migration and dispersal. Such metacommunity processes of interconnected multispecies assemblages are likely to affect local dynamics of both species and processes. We present results from an artificial marine outdoor rock pool system in which we investigated the factors of (1) local grazer richness and composition, and (2) connectivity of local patches to a regional species pool, and their effects on algal biomass. Local species richness of six grazers was manipulated in both open and closed pools, which were embedded in a regional species pool containing all six grazers. Grazer richness showed significant net biodiversity effects on grazing in the closed, but not in the open, system. Grazer composition, on the other hand, showed significant effects on grazing in both open and closed systems, depending on which species were initially present. The two most efficient grazers were able to compensate for less efficient grazers in species mixtures, hence ensuring the function of grazing. The efficiency of top-down control of algal biomass in open systems thus depends on which particular species are lost. Further, differences in grazing between the open and closed system changed over time due to temporal dynamics in grazer composition. The results emphasize the importance of including system connectivity in experimental designs to allow an extrapolation of biodiversity ecosystem-functioning relationships to natural systems.

Warming has stronger direct than indirect effects on benthic microalgae in a seaweed system in spring.

Using outdoor mesocosms we investigated the relative importance of the direct and indirect (here: altered grazing) effects of seawater warming on benthic microalgae in a Baltic Sea Fucus vesiculosus (Phaeophyceae) system during the spring season. Seawater warming had a positive main effect on microalgal total biomass accrual and growth rate and on total mesograzer abundance and biomass. Moreover, under the existing resource-replete conditions in spring the direct positive effect of warming on microalgae was stronger than its indirect negative effect through enhanced grazing. The outcome of this study contrasts previous observations from the summer and winter season, where indirect effects of warming mediated by altered grazing were identified as an important driver of primary biomass in the Fucus system. In this context, the results from the spring season add mechanistic information to the overall understanding of the seasonal variability of climate change effects. They suggest that the relative importance of the underlying direct and indirect effective pathways of warming and the overall effect on the balance between production and consumption are influenced by the trophic state of the system, which in temperate regions is related to season.

Dispersal frequency affects local biomass production by controlling local diversity.

Dispersal is a major factor regulating the number of coexisting species, but the relationship between species diversity and ecosystem processes has mainly been analysed for communities closed to dispersal. We experimentally investigated how initial local diversity and dispersal frequency affect local diversity and biomass production in open benthic microalgal metacommunities. Final local species richness and local biomass production were strongly influenced by dispersal frequency but not by initial local diversity. Both final local richness and final local biomass showed a hump-shaped pattern with increasing dispersal frequency, with a maximum at intermediate dispersal frequencies. Consequently, final local biomass increased linearly with increasing final richness. We conclude that the general relationship between richness and ecosystem functioning remains valid in open systems, but the maintenance of ecosystem processes significantly depends on the effects of dispersal on species richness and local interactions.

Extinction debt in source-sink metacommunities.

In an increasingly modified world, understanding and predicting the consequences of landscape alteration on biodiversity is a challenge for ecologists. To this end, metacommunity theory has developed to better understand the complexity of local and regional interactions that occur across larger landscapes. While metacommunity ecology has now provided several alternative models of species coexistence at different spatial scales, predictions regarding the consequences of landscape alteration have been done exclusively for the competition-colonization trade off model (CC). In this paper we investigate the effects of landscape perturbation on source-sink metacommunities. We show that habitat destruction perturbs the equilibria among species competitive effects within the metacommunity, driving both direct extinctions and an indirect extinction debt. As in CC models, we found a time lag for extinction following habitat destruction that varied in length depending upon the relative importance of direct and indirect effects. However, in contrast to CC models, we found that the less competitive species are more affected by habitat destruction. The best competitors can sometimes even be positively affected by habitat destruction, which corresponds well with the results of field studies. Our results are complementary to those results found in CC models of metacommunity dynamics. From a conservation perspective, our results illustrate that landscape alteration jeopardizes species coexistence in patchy landscapes through complex indirect effects and delayed extinctions patterns.