Yvonne Vadeboncoeur

FISHES AS INTEGRATORS OF BENTHIC AND PELAGIC FOOD WEBS IN LAKES

Studies of lake ecosystems generally focus on pelagic food chains and processes. Recently, there has been an emerging recognition of the importance of benthic production and processes to whole-lake ecosystems. To examine the extent to which zoobenthos contribute to higher trophic level production in lakes, we synthesized diet data from 470 fish populations (15 species) and stable isotope data from 90 fish populations (11 species), all of which are common inhabitants of north-temperate lakes. Across all species considered, zoobenthos averaged 50% of total prey consumption. Indirect consumption of zoobenthos (i.e., feeding on zoobenthos-supported fishes) contributed another 15%, for a total of 65% reliance on benthic secondary production. Stable isotopes provided estimates of mean zoobenthivory ranging from 43% to 59%. For most fish species, consumption of zoobenthos was highly variable among populations. The overwhelming concern of ecologists with pelagic food chains and processes contrasts sharply with our finding that benthic secondary production plays a central role in supporting higher trophic level production. This extensive zoobenthivory can subsidize fish populations, leading to apparent competition and otherwise altering trophic dynamics and ecosystem processes in the pelagic zone. We argue for a more integrated view of lake ecosystems that recognizes the duality of benthic and pelagic production pathways. Food web models that explicitly consider energy flow from pelagic and benthic sources will provide a more realistic energy flow template for understanding the regulation of lake ecosystem functioning.

BENTHIC ALGAL PRODUCTION ACROSS LAKE SIZE GRADIENTS: INTERACTIONS AMONG MORPHOMETRY, NUTRIENTS, AND LIGHT

Attached algae play a minor role in conceptual and empirical models of lake ecosystem function but paradoxically form the energetic base of food webs that support a wide variety of fishes. To explore the apparent mismatch between perceived limits on contributions of periphyton to whole-lake primary production and its importance to consumers, we modeled the contribution of periphyton to whole-ecosystem primary production across lake size, shape, and nutrient gradients. The distribution of available benthic habitat for periphyton is influenced by the ratio of mean depth to maximum depth (DR = z/ z(max)). We modeled total phytoplankton production from water-column nutrient availability, z, and light. Periphyton production was a function of light-saturated photosynthesis (BPmax) and light availability at depth. The model demonstrated that depth ratio (DR) and light attenuation strongly determined the maximum possible contribution of benthic algae to lake production, and the benthic proportion of whole-lake primary production (BPf) declined with increasing nutrients. Shallow lakes (z < or =5 m) were insensitive to DR and were dominated by either benthic or pelagic primary productivity depending on trophic status. Moderately deep oligotrophic lakes had substantial contributions by benthic primary productivity at low depth ratios and when maximum benthic photosynthesis was moderate or high. Extremely large, deep lakes always had low fractional contributions of benthic primary production. An analysis of the worlds largest lakes showed that the shapes of natural lakes shift increasingly toward lower depth ratios with increasing depth, maximizing the potential importance of littoral primary production in large-lake food webs. The repeatedly demonstrated importance of periphyton to lake food webs may reflect the combination of low depth ratios and high light penetration characteristic of large, oligotrophic lakes that in turn lead to substantial contributions of periphyton to autochthonous production.

Periphyton Function in Lake Ecosystems

Periphyton communities have received relatively little attention in lake ecosystems. However, evidence is increasing that they play a key role in primary productivity, nutrient cycling, and food web interactions. This review summarizes those findings and places them in a conceptual framework to evaluate the functional importance of periphyton in lakes. The role of periphyton is conceptualized based on a spatial hierarchy. At the coarsest scale, landscape properties such as lake morphometry, influence the amount of available habitat for periphyton growth. Watershed-related properties, such as loading of dissolved organic matter, nutrients, and sediments influence light availability and hence periphyton productivity. At the finer scale of within the lake, both habitat availability and habitat type affect periphyton growth and abundance. In addition, periphyton and phytoplankton compete for available resources at the within-lake scale. Our review indicates that periphyton plays an important functional role in lake nutrient cycles and food webs, especially under such conditions as relatively shallow depths, nutrient-poor conditions, or high water-column transparency. We recommend more studies assessing periphyton function across a spectrum of lake morphometry and trophic conditions.

Benthic-Pelagic Links: Responses of Benthos to Water-Column Nutrient Enrichment

Although the responses of pelagic algae and invertebrates to gradients of nutrient enrichment are well known, less is known about the responses of benthos to such gradients or how benthic and pelagic responses may interact. We performed a 9-wk experiment in 2000-L mesocosms in the field to test for the effect of water-column nutrient enrichment on phytoplankton, algae on sediments (epipelon) and hard surfaces (plastic strips), as well as pelagic and benthic primary consumers. The experimental design consisted of 4 nutrient enrichment rates (0, 0.5, 1.0 and 2.0 μg P L-1 d-1, together with N to yield an N:P ratio of 20:1 by weight). Nutrient enrichment induced significant increases in chlorophyll a in phytoplankton and attached algae, but not epipelon. Zooplankton biomass was significantly higher in enriched mesocosms than in controls over the initial 4 wk of enrichment, but the effect was not sustained over the course of the experiment. Densities of sediment-dwelling, and hard-substrata-associated invertebrates were higher in enriched treatments relative to controls. Emergence of benthic insects also increased with enrichment. Size and species composition of benthic macroinvertebrates differed between enriched treatments and controls. Our results suggest that nutrients added to the water column were quickly converted into benthic biomass, likely reducing pelagic responses to enrichment.

Morphometry and average temperature affect lake stratification responses to climate change

Climate change is affecting lake stratification with consequences for water quality and the benefits that lakes provide to society. Here we use long-term temperature data (1970–2010) from 26 lakes around the world to show that climate change has altered lake stratification globally and that the magnitudes of lake stratification changes are primarily controlled by lake morphometry (mean depth, surface area, and volume) and mean lake temperature. Deep lakes and lakes with high average temperatures have experienced the largest changes in lake stratification even though their surface temperatures tend to be warming more slowly. These results confirm that the nonlinear relationship between water density and water temperature and the strong dependence of lake stratification on lake morphometry makes lake temperature trends relatively poor predictors of lake stratification trends.

Borders of Biodiversity: Life at the Edge of the World's Large Lakes

The great lakes of the world represent a global heritage of surface freshwater and aquatic biodiversity. Species lists for 14 of the worlds largest lakes reveal that 15% of the global diversity (the total number of species) of freshwater fishes, 9% of noninsect freshwater invertebrate diversity, and 2% of aquatic insect diversity live in this handful of lakes. The vast majority (more than 93%) of species inhabit the shallow, nearshore littoral zone, and 72% are completely restricted to the littoral zone, even though littoral habitats are a small fraction of total lake areas. Most fish species exploit benthic resources, which increases food web complexity. Moreover, littoral zones are both more negatively affected by human activity and less intensively studied than offshore waters. Conservation of the remarkable biodiversity and biotic integrity of large lakes will require better integration of littoral zones into our understanding of lake ecosystem functioning and focused efforts to alleviate human impacts along the shoreline.

Effects of Multi-chain Omnivory on the Strength of Trophic Control in Lakes

Omnivory has been implicated in both diffusing and intensifying the effects of consumer control in food chains. Some have postulated that the strong, community level, top-down control apparent in lakes is not expressed in terrestrial systems because terrestrial food webs are reticulate, with high degrees of omnivory and diverse plant communities. In contrast, lake food webs are depicted as simple linear chains based on phytoplankton-derived energy. Here, we explore the dynamic implications of recent evidence showing that attached algal (periphyton) carbon contributes substantially to lake primary and secondary productivity, including fish production. Periphyton production represents a cryptic energy source in oligotrophic and mesotrophic lakes that is overlooked by previous theoretical treatment of trophic control in lakes. Literature data demonstrate that many fish are multi-chain omnivores, exploiting food chains based on both littoral and pelagic primary producers. Using consumer-resource models, we examine how multiple food chains affect fourth-level trophic control across nutrient gradients in lakes. The models predict that the stabilizing effects of linked food chains are strongest in lakes where both phytoplankton and periphyton contribute substantially to production of higher trophic levels. This stabilization enables a strong and persistent top down control on the pelagic food chain in mesotrophic lakes. The extension of classical trophic cascade theory to incorporate more complex food web structures driven by multi-chain predators provides a conceptual framework for analysis of reticulate food webs in ecosystems.

Periphyton production on wood and sediment: substratum-specific response to laboratory and whole-lake nutrient manipulations

Substratum heterogeneity is a large source of variability in periphyton production, but the influence of substratum on periphyton response to experimental manipulations is rarely measured. Using laboratory and whole-lake experiments, we compared area-specific primary production of periphyton on wood (epixylon) and sediment (epipelon), and tested whether periphyton on the 2 substrata responded differently to water-column fertilization. In the laboratory, natural periphyton assemblages on wood or sediment were exposed to 1 of 6 treatments in a fully factorial (light [250, 70, or 10 μmol m−2 s−1] × nutrient [control or + N and P]) experiment. We measured 14C primary production on both substrata after 25 to 30 d. We also measured epipelic and epixylic production in a reference and an experimentally fertilized lake. We constructed photosynthesis-irradiance curves for epipelon from 3 depths in each lake, and used the curves to predict primary production at average in situ light intensities for each lake and depth. Production response to fertilization was substratum-specific, and area-specific epipelic production was 10× that of epixylon at both experimental scales. Both epixylon (ANOVA, p < 0.0001) and epipelon (ANOVA, p < 0.0001) production increased significantly with increasing light. Epixylon production was significantly higher in fertilized treatments than in controls (ANOVA, p < 0.01), but epipelon did not respond to fertilization (ANOVA, p = 0.69). Epixylon production was also significantly higher in the fertilized lake than in the reference lake (ANOVA, p < 0.05). Maximum epipelic production rates decreased with water depth in both lakes, and average epipelic production from both lakes was positively and similarly related to average in situ light intensities (linear regression, R2 = 0.94, p = 0.001). Both substratum-specific response to fertilization and substratum-specific periphyton production may be critical in determining fertilization-induced changes in periphyton production in lakes.

Substratum as a driver of variation in periphyton chlorophyll and productivity in lakes

Abstract Quantifying periphyton (attached algal) contributions to autotrophic production in lakes is confounded by properties of substratum that affect community biomass (as chlorophyll content) and productivity. We compared chlorophyll content and productivity of natural algal communities (phytoplankton, epipelon, epilithon, epixylon, and epiphyton) experiencing high (>10%) incident radiation in lakes in the US, Greenland, and Quebec, Canada. Chlorophyll content and productivity differed significantly among regions, but they also differed consistently among communities independent of region. Chlorophyll content of periphyton on hard substrata (rocks and wood) was positively related to water-column total P (TP), whereas chlorophyll content of algae on sediment (epipelon) and TP were not significantly related. Chlorophyll content was up to 100× higher on sediments than on hard substrata. Within regions, chlorophyll-specific primary productivity was highest for phytoplankton and lowest for epipelon. Periphyton on hard substrata and on macrophytes (epiphyton) had similar rates of chlorophyll-specific productivity that were intermediate to those of epipelon and phytoplankton. Area-specific productivity of epipelon was 5 to 10× higher than area-specific productivity of periphyton on hard substrata. This broad geographic comparison indicates that, in low to moderately productive lakes under high-light conditions, algal communities have predictable differences in area-specific and chlorophyll-specific productivity based on substratum. As such, chlorophyll alone is an inadequate predictor of the relative contributions of different algal communities to total primary production. Our results highlight the importance of the relative abundance and spatial distributions of substrata in determining the role of the littoral zones in nutrient and energy cycles in lakes.

Benthic–planktonic coupling, regime shifts, and whole‐lake primary production in shallow lakes

Alternative stable states in shallow lakes are typically characterized by submerged macrophyte (clear-water state) or phytoplankton (turbid state) dominance. However, a clear-water state may occur in eutrophic lakes even when macrophytes are absent. To test whether sediment algae could cause a regime shift in the absence of macrophytes, we developed a model of benthic (periphyton) and planktonic (phytoplankton) primary production using parameters derived from a shallow macrophyte-free lake that shifted from a turbid to a clear-water state following fish removal (biomanipulation). The model includes a negative feedback effect of periphyton on phosphorus (P) release from sediments. This in turn induces a positive feedback between phytoplankton production and P release. Scenarios incorporating a gradient of external P loading rates revealed that (1) periphyton and phytoplankton both contributed substantially to whole-lake production over a broad range of external P loading in a clear-water state; (2) during the clear-water state, the loss of benthic production was gradually replaced by phytoplankton production, leaving whole-lake production largely unchanged; (3) the responses of lakes to biomanipulation and increased external P loading were both dependent on lake morphometry; and (4) the capacity of periphyton to buffer the effects of increased external P loading and maintain a clear-water state was highly sensitive to relationships between light availability at the sediment surface and the of P release. Our model suggests a mechanism for the persistence of alternative states in shallow macrophyte-free lakes and demonstrates that regime shifts may trigger profound changes in ecosystem structure and function.