Monika Winder

CLIMATE CHANGE UNCOUPLES TROPHIC INTERACTIONS IN AN AQUATIC ECOSYSTEM

The largest uncertainty in forecasting the effects of climate change on eco- systems is in understanding how it will affect the nature of interactions among species. Climate change may have unexpected consequences because different species show unique responses to changes in environmental temperatures. Here we show that increasingly warmer springs since 1962 have disrupted the trophic linkages between phytoplankton and zoo- plankton in a large temperate lake because of differing sensitivity to vernal warming. The timing of thermal stratification and the spring diatom bloom have advanced by more than 20 days during this time period. A long-term decline in Daphnia populations, the keystone herbivore, is associated with an expanding temporal mismatch with the spring diatom bloom and may have severe consequences for resource flow to upper trophic levels.

The annual cycles of phytoplankton biomass

Terrestrial plants are powerful climate sentinels because their annual cycles of growth, reproduction and senescence are finely tuned to the annual climate cycle having a period of one year. Consistency in the seasonal phasing of terrestrial plant activity provides a relatively low-noise background from which phenological shifts can be detected and attributed to climate change. Here, we ask whether phytoplankton biomass also fluctuates over a consistent annual cycle in lake, estuarine–coastal and ocean ecosystems and whether there is a characteristic phenology of phytoplankton as a consistent phase and amplitude of variability. We compiled 125 time series of phytoplankton biomass (chlorophyll a concentration) from temperate and subtropical zones and used wavelet analysis to extract their dominant periods of variability and the recurrence strength at those periods. Fewer than half (48%) of the series had a dominant 12-month period of variability, commonly expressed as the canonical spring-bloom pattern. About 20 per cent had a dominant six-month period of variability, commonly expressed as the spring and autumn or winter and summer blooms of temperate lakes and oceans. These annual patterns varied in recurrence strength across sites, and did not persist over the full series duration at some sites. About a third of the series had no component of variability at either the six- or 12-month period, reflecting a series of irregular pulses of biomass. These findings show that there is high variability of annual phytoplankton cycles across ecosystems, and that climate-driven annual cycles can be obscured by other drivers of population variability, including human disturbance, aperiodic weather events and strong trophic coupling between phytoplankton and their consumers. Regulation of phytoplankton biomass by multiple processes operating at multiple time scales adds complexity to the challenge of detecting climate-driven trends in aquatic ecosystems where the noise to signal ratio is high.

Temporal organization of phytoplankton communities linked to physical forcing

The performance of individual phytoplankton species is strongly governed by the thermal stratification’s impact on vertical mixing within the water column, which alters the position of phytoplankton relative to nutrients and light. The present study documents shifts in phytoplankton structure and vertical positioning that have accompanied intensified long-term stratification in a natural ecosystem. Ordination analysis is used to extract gradients in phytoplankton composition in Lake Tahoe, an extremely nutrient-poor lake, over a 23-year period of records. Community structure in the 1980s was associated most strongly with resource availability (low nitrogen to phosphorus ratios, deeper euphotic zone depth), while intensified stratification dominated the phytoplankton structure since the late 1990s. Within diatoms, small-sized cells increased with reduced mixing, suggesting that suppressed turbulence provides them with a competitive advantage over large-sized cells. Among the morphologically diverse chlorophytes, filamentous and coenobial forms were favored under intensified stratification. The selection for small-sized diatoms is accompanied by a shoaling trend in their vertical position in the water column. In contrast, the motile flagellates displayed a deeper vertical positioning in recent years, indicating that optimal growth conditions shifted likely due to reduced upwelling of nutrients. As the thermal stratification of lakes and oceans is strongly linked to climate variables, the present study confirms that climate warming will alter phytoplankton structure and dynamics largely through effects on nutrient availability and sinking velocities. Intensified stratification should favor the expansion of small-sized species and species with the capability of buoyancy regulation, which may alter primary productivity, nutrient recycling, and higher trophic productivity.

Environmental stability and lake zooplankton diversity – contrasting effects of chemical and thermal variability

Environmental variability in space and time is a primary mechanism allowing species that share resources to coexist. Fluctuating conditions are a double edged sword for diversity, either promoting coexistence through temporal niche partitioning or excluding species by stochastic extinctions. The net effect of environmental variation on diversity is largely unknown. We examined the association between zooplankton species richness in lakes and environmental variability on interannual, seasonal and shorter time scales, as well as long-term average conditions. We analyzed data on physical, chemical and biological limnology in 53 temperate zone lakes in North America and Europe sampled over a combined 1042 years. Large fluctuations in pH, phosphorus and dissolved organic carbon concentration on different time scales were associated with reduced zooplankton species richness. More species were found in lakes that showed greater temperature variation on all time scales. Environmental variability on different time scales showed similar or, in some cases, stronger associations with zooplankton species richness compared with long-term average conditions. Our results suggest that temporal fluctuations in the chemical environment tend to exclude zooplankton species while temperature variability promotes greater richness. The results indicate that anthropogenic increases in temporal variability of future climates may have profound effects on biodiversity.

Biological communities in San Francisco Bay track large-scale climate forcing over the North Pacific.

Long-term observations show that fish and plankton populations in the ocean fluctuate in synchrony with large-scale climate patterns, but similar evidence is lacking for estuaries because of shorter observational records. Marine fish and invertebrates have been sampled in San Francisco Bay since 1980 and exhibit large, unexplained population changes including record-high abundances of common species after 1999. Our analysis shows that populations of demersal fish, crabs and shrimp covary with the Pacific Decadal Oscillation (PDO) and North Pacific Gyre Oscillation (NPGO), both of which reversed signs in 1999. A time series model forced by the atmospheric driver of NPGO accounts for two-thirds of the variability in the first principal component of species abundances, and generalized linear models forced by PDO and NPGO account for most of the annual variability of individual species. We infer that synchronous shifts in climate patterns and community variability in San Francisco Bay are related to changes in oceanic wind forcing that modify coastal currents, upwelling intensity, surface temperature, and their influence on recruitment of marine species that utilize estuaries as nursery habitat. Ecological forecasts of estuarine responses to climate change must therefore consider how altered patterns of atmospheric forcing across ocean basins influence coastal oceanography as well as watershed hydrology.

Partitioning the Relative Importance of Phylogeny and Environmental Conditions on Phytoplankton Fatty Acids

Essential fatty acids (EFA), which are primarily generated by phytoplankton, limit growth and reproduction in diverse heterotrophs. The biochemical composition of phytoplankton is well-known to be governed both by phylogeny and environmental conditions. Nutrients, light, salinity, and temperature all affect both phytoplankton growth and fatty acid composition. However, the relative importance of taxonomy and environment on algal fatty acid content has yet to be comparatively quantified, thus inhibiting predictions of changes to phytoplankton food quality in response to global environmental change. We compiled 1145 published marine and freshwater phytoplankton fatty acid profiles, consisting of 208 species from six major taxonomic groups, cultured in a wide range of environmental conditions, and used a multivariate distance-based linear model to quantify the total variation explained by each variable. Our results show that taxonomic group accounts for 3-4 times more variation in phytoplankton fatty acids than the most important growth condition variables. The results underscore that environmental conditions clearly affect phytoplankton fatty acid profiles, but also show that conditions account for relatively low variation compared to phylogeny. This suggests that the underlying mechanism determining basal food quality in aquatic habitats is primarily phytoplankton community composition, and allows for prediction of environmental-scale EFA dynamics based on phytoplankton community data. We used the compiled dataset to calculate seasonal dynamics of long-chain EFA (LCEFA; ≥C20 ɷ-3 and ɷ-6 polyunsaturated fatty acid) concentrations and ɷ-3:ɷ-6 EFA ratios in Lake Washington using a multi-decadal phytoplankton community time series. These analyses quantify temporal dynamics of algal-derived LCEFA and food quality in a freshwater ecosystem that has undergone large community changes as a result of shifting resource management practices, highlighting diatoms, cryptophytes and dinoflagellates as key sources of LCEFA. Moreover, the analyses indicate that future shifts towards cyanobacteria-dominated communities will result in lower LCEFA content in aquatic ecosystems.

Trade-offs in Daphnia habitat selection

Diel vertical migration (DVM) is a dynamic behavioral pattern found ex- tensively in the worlds oceans and lakes, yet the role of food and temperature distribution on DVM is still unclear. While DVM has been mostly studied in systems with surface food maxima, deep-water food maxima are quite common in lakes and oceans. In such ecosys- tems, optimal conditions of temperature and food are uncoupled. In a Swiss high-mountain lake (Oberer Arosasee) with a deep-water food maximum, we found that Daphnia galeata adults and juveniles exhibit DVM behavior almost throughout the year and migrated up- wards, out of food-rich environments, at night. In a large indoor mesocosm experiment, we were able to show that Daphnia respond to fish-mediated cues by migrating into deeper water layers. In the presence of fish and using natural vertical food and temperature dis- tributions in the mesocosms, we could reproduce the vertical distribution of adult Daphnia observed in the field. The indoor experiments show that food and temperature modulate the actual depth at which the animals stop migrating, whereas fish and ultraviolet radiation likely determine the timing of migration (its synchronization with dawn and dusk). Overall, our results show that the nighttime movement into the surface waters contributes to the fitness ofDaphnia, given the costs and benefits associated with the trade-off between food and temperature.

Patterns of spatial and temporal variability of UV transparency in Lake Tahoe, California‐Nevada

Lake Tahoe is an ultra-oligotrophic subalpine lake that is renowned for its clarity. The region experiences little cloud cover and is one of the most UV transparent lakes in the world. As such, it is an ideal environment to study the role of UV radiation in aquatic ecosystems. Long-term trends in Secchi depths showed that water transparency to visible light has decreased in recent decades, but limited data are available on the UV transparency of the lake. Here we examine how ultraviolet radiation varies relative to longer-wavelength photosynthetically active radiation (PAR, 400-700 nm, visible wavelengths) horizontally along inshore-offshore transects in the lake and vertically within the water column as well as temporally throughout 2007. UV transparency was more variable than PAR transparency horizontally across the lake and throughout the year. Seasonal patterns of Secchi transparency differed from both UV and PAR, indicating that different substances may be responsible for controlling transparency to UV, PAR, and Secchi. In surface waters, UVA (380 nm) often attenuated more slowly than PAR, a pattern visible in only exceptionally transparent waters with very low dissolved organic carbon. On many sampling dates, UV transparency decreased progressively with depth suggesting surface photobleaching, reductions in particulate matter, increasing chlorophyll a, or some combination of these increased during summer months. Combining these patterns of UV transparency with data on visible light provides a more comprehensive understanding of ecosystem structure, function, and effects of environmental change in highly transparent alpine and subalpine lakes such as Tahoe.

Seasonal vertical distribution of phytoplankton and copepod species in a high-mountain lake

Many zooplankton species migrate to deeper water layers during the day to reduce light-dependent mortality risk at the surface layers. Theories explaining diel vertical migration (DVM) of zooplankters share the assumption that the surface waters are more food-rich compared to the deep-water layers and that zooplankters return at night to the surface to profit from the warmer, food-rich environment. However, evidence suggests that the resources in deep-water layers can be as profitable as in the upper water layers for zooplankton. Those deep-water food maxima have often been overlooked in freshwater. In this study we investigated the vertical distribution of phytoplankton together with the vertical day and night distribution of copepod species in a high-mountain lake with a deep-water phytoplankton maximum dominated by cryptophytes and blue-greens. All copepod species, including the small-sized individuals avoided the upper strata during daytime. Adult Cyclops abyssorum migrated almost throughout the entire year. In contrast, the Eudiaptomus gracilis and copepodites of C. abyssorum and nauplia of both species did not migrate but remained in the same water layers day and night. Secchi depth transparency significantly correlated with daytime depth of adult copepods. Daytime depths are usually associated with high concentration of algal biovolume and moderate temperature. Although food conditions are better in deeper strata, for some species the warmer temperatures in the surface waters may be the reason why they migrate to shallower depths during the night.

Have Human Impacts Changed Alpine Zooplankton Diversity over the Past 100 Years

Anthropogenic stress and fish introduction generally are thought to have eliminated vulnerable and sensitive zooplankton species from many alpine lakes, creating impoverished communities. To investigate this hypothesis we resampled lakes studied in the early 20th century and compared past and present zooplankton composition and taxa richness. We also studied how human induced changes may influence genetic diversity of present-day populations of the widespread cladoceran, Daphnia. Resampling did not show a drastic overall change in planktonic crustacean composition. Taxa richness significantly decreased with increasing lake altitude, but no other environmental factor correlated with richness. Large zooplankton taxa were found in lakes both with and without fish. Therefore we conclude that the presence of fish can be excluded as the general factor explaining the occurrence or absence of large zooplankton in alpine lakes. Levels of chlorophyll a and POC best distinguished lakes with Daphnia from lakes without Daphnia. In 8 out of 12 lakes sexual Daphnia were more abundant than asexual individuals. Clonal diversity ranged from 0.01 to 1.3 but was not related to the proportion of sexual individuals. The ability to create resting stages may be an essential factor for the maintenance of genetic diversity and the long-term persistence of Daphnia and other zooplankton taxa.