Néstor Mazzeo

Restoration of shallow lakes by nutrient control and biomanipulation—the successful strategy varies with lake size and climate

Major efforts have been made world-wide to improve the ecological quality of shallow lakes by reducing external nutrient loading. These have often resulted in lower in-lake total phosphorus (TP) and decreased chlorophyll a levels in surface water, reduced phytoplankton biomass and higher Secchi depth. Internal loading delays recovery, but in north temperate lakes a new equilibrium with respect to TP often is reached after <10–15 years. In comparison, the response time to reduced nitrogen (N) loading is typically <5 years. Also increased top-down control may be important. Fish biomass often declines, and the percentage of piscivores, the zooplankton:phytoplankton biomass ratio, the contribution of Daphnia to zooplankton biomass and the cladoceran size all tend to increase. This holds for both small and relatively large lakes, for example, the largest lake in Denmark (40 km2), shallow Lake Arreso, has responded relatively rapidly to a ca. 76% loading reduction arising from nutrient reduction and top-down control. Some lakes, however, have proven resistant to loading reductions. To accelerate recovery several physico-chemical and biological restoration methods have been developed for north temperate lakes and used with varying degrees of success. Biological measures, such as selective removal of planktivorous fish, stocking of piscivorous fish and implantation or protection of submerged plants, often are cheap versus traditional physico-chemical methods and are therefore attractive. However, their long-term effectiveness is uncertain. It is argued that additional measures beyond loading reduction are less cost-efficient and often not needed in very large lakes. Although fewer data are available on tropical lakes these seem to respond to external loading reductions, an example being Lake Paranoa, Brazil (38 km2). However, differences in biological interactions between cold temperate versus warm temperate-subtropical-tropical lakes make transfer of existing biological restoration methods to warm lakes difficult. Warm lakes often have prolonged growth seasons with a higher risk of long-lasting algal blooms and dense floating plant communities, smaller fish, higher aggregation of fish in vegetation (leading to loss of zooplankton refuge), more annual fish cohorts, more omnivorous feeding by fish and less specialist piscivory. The trophic structures of warm lakes vary markedly, depending on precipitation, continental or coastal regions locations, lake age and temperature. Unfortunately, little is known about trophic dynamics and the role of fish in warm lakes. Since many warm lakes suffer from eutrophication, new insights are needed into trophic interactions and potential lake restoration methods, especially since eutrophication is expected to increase in the future owing to economic development and global warming.

Impacts of climate warming on lake fish community structure and potential effects on ecosystem function

Fish play a key role in the trophic dynamics of lakes, not least in shallow systems. With climate warming, complex changes in fish community structure may be expected owing to the direct and indirect effects of temperature, and indirect effects of eutrophication, water-level changes and salinisation on fish metabolism, biotic interactions and geographical distribution. We review published and new data supporting the hypotheses that, with a warming climate, there will be changes in: fish community structure (e.g. higher or lower richness depending on local conditions); life history traits (e.g. smaller body size, shorter life span, earlier and less synchronised reproduction); feeding mode (i.e. increased omnivory and herbivory); behaviour (i.e. stronger association with littoral areas and a greater proportion of benthivores); and winter survival. All these changes imply higher predation on zooplankton and macroinvertebrates with increasing temperatures, suggesting that the changes in the fish communities partly resemble, and may intensify, the effects triggered by eutrophication. Modulating factors identified in cold and temperate systems, such as the presence of submerged plants and winter ice cover, seem to be weaker or non-existent in warm(ing) lakes. Consequently, in the future lower nutrient thresholds may be needed to obtain clear-water conditions and good ecological status in the future in currently cold or temperate lakes. Although examples are still scarce and more research is needed, we foresee biomanipulation to be a less successful restoration tool in warm(ing) lakes without a strong reduction of the nutrient load.

The structuring role of free-floating versus submerged plants in a subtropical shallow lake

In shallow temperate lakes many ecological processes depend on submerged macrophytes. In subtropical and tropical lakes, free-floating macrophytes may be equally or more important. We tested the hypothesis that different macrophyte growth forms would be linked with different bottom-up and top-down mechanisms in out-competing phytoplankton. We compared experimentally the effects of submerged and free-floating plants on water chemistry, phytoplankton biomass, zooplankton and fish community structure in a shallow hypertrophic lake (Lake Rodó, 34°55′S 56°10′W, Uruguay). Except for the retention of suspended solids, we found no other significant bottom-up process connected with either Eichhornia crassipes or Potamogeton pectinatus. Free-floating plants had a lower abundance of medium-sized zooplankton than any other microhabitat and submerged plants were apparently preferred by microcrustaceans. Fish showed a differential habitat use according to species, size-class and feeding habits. Dominant omnivore-planktivores, particularly the smallest size classes, preferred submerged plants. In contrast, omnivore-piscivores were significantly associated with free-floating plants. The density of omnivorous-planktivorous fish, by size class, significantly explained the distribution of medium-sized zooplankton, the high number of size 0 fish being the main factor. The abiotic environment and the structure of the zooplankton community explained little of the fish distribution pattern. Our results suggest that bottom-up effects of free-floating plants are weak when cover is low or intermediate. Top-down effects are complex, as effects on zooplankton and fish communities seem contradictory. The low piscivores:planktivores ratio in all microhabitats suggests, however, that cascading effects on phytoplankton through free-floating plant impacts on piscivorous fish are unlikely to be strong.

Biomanipulation as a Restoration Tool to Combat Eutrophication: Recent Advances and Future Challenges

Eutrophication resulting from high nutrient loading has been the paramount environmental problem for lakes world-wide for the past four decades. Efforts are being made in many parts of the world to reduce external nutrient loading via improved wastewater treatment or diversion of nutrient-rich inflows. However, even after a reduction of the external phosphorus loading, the effects obtained may be unsatisfactory. This may reflect an insufficient reduction in the external nutrient loading to effectively limit phytoplankton growth. However, the lack of success may also be due to chemical or biological within-lake inertia preventing or delaying improvements. To overcome the resilience and thereby reinforce recovery, a number of physico-chemical and biological restoration methods have been developed. In this chapter, we describe recent developments of biological restoration methods related to eutrophication, their short-term and long-term effects, and discuss the possibility of using combined physico-chemical and biological methods to improve the long-term stability of restoration and to reduce restoration costs. As comprehensive reviews of the effect of fish manipulation in cold temperate lakes are numerous, for these waterbodies, we highlight recent results, including effects on biodiversity and metabolism, and present new approaches of biomanipulation. Our particular focus is, however, directed at biomanipulation in warm lakes and on combined treatments which are far less well described in the literature.

Lake and watershed characteristics rather than climate influence nutrient limitation in shallow lakes

Both nitrogen (N) and phosphorus (P) can limit primary production in shallow lakes, but it is still debated how the importance of N and P varies in time and space. We sampled 83 shallow lakes along a latitudinal gradient (5 degrees 55 degrees S) in South America and assessed the potential nutrient limitation using different methods including nutrient ratios in sediment, water, and seston, dissolved nutrient concentrations, and occurrence of N-fixing cyanobacteria. We found that local characteristics such as soil type and associated land use in the catchment, hydrology, and also the presence of abundant submerged macrophyte growth influenced N and P limitation. We found neither a consistent variation in nutrient limitation nor indications for a steady change in denitrification along the latitudinal gradient. Contrary to findings in other regions, we did not find a relationship between the occurrence of (N-fixing and non-N-fixing) cyanobacteria and the TN:TP ratio. We found N-fixing cyanobacteria (those with heterocysts) exclusively in lakes with dissolved inorganic nitrogen (DIN) concentrations of < 100 microg/L, but notably they were also often absent in lakes with low DIN concentrations. We argue that local factors such as land use and hydrology have a stronger influence on which nutrient is limiting than climate. Furthermore, our data show that in a wide range of climates N limitation does not necessarily lead to cyanobacterial dominance.

Horizontal dynamics of zooplankton in subtropical Lake Blanca (Uruguay) hosting multiple zooplankton predators and aquatic plant refuges

In the subtropics, the effects of macrophytes on trophic interactions are more complex than in temperate lakes. Fish, particularly the smallest species and individuals, aggregate in high numbers in the vegetation, and a strong predation pressure on Zooplankton by shrimps and invertebrates, such as Chaoborus, can occur in these systems. We studied seasonal and diel changes in Zooplankton and their potential predators (both fish and invertebrates) and physical and chemical characteristics among open water and vegetated habitats (emergent and submerged plants (SP)), in the subtropical Lake Bianca (34°54’ S; 54°50’ W), a shallow system with an extensive and complex littoral area and high abundance of vertebrate and invertebrate predators on Zooplankton. We found differential horizontal distribution of some zooplankton species under the scenario of high abundance of small omnivorous-planktivorous fish and Chaoborus, especially in the seasons with intermediate catch per unit effort of fish. We found indications of a diel horizontal migration (DHM) opposite than described for temperate systems, as the two main cladocerans Bosmina longirostris and Diaphanosoma birgei were found in higher densities in the submerged plant beds during night, in spring and autumn respectively. Although we need experiments to prove DHM, Chaoborus seemed to be the main trigger of the apparent DHM, followed by small omnivorous fish. During summer no spatial differences were found likely because of high densities of fish in all habitats. In absence of piscivorous fish, the distribution of fish Jenynsia multidentata seemed to be conditioned by food availability and by predation risk of waterfowl. The refuge capacity of aquatic plants for Zooplankton in subtropical systems seems weak and with consequent weak or no cascading effects on water transparency, as under very high fish and invertebrate densities (summer) the refuge for Zooplankton was lost.

Environmental Warming in Shallow Lakes: A Review of Potential Changes in Community Structure as Evidenced from Space-for-Time Substitution Approaches

Abstract Shallow lakes, one of the most widespread water bodies in the world landscape, are very sensitive to climate change. Several theories predict changes in community traits, relevant for ecosystem functioning, with higher temperature. The space-for-time substitution approach (SFTS) provides one of the most plausible empirical evaluations for these theories, helping to elucidate the long-term consequences of changes in climate. Here, we reviewed the changes at the community level for the main freshwater taxa and assemblages (i.e. fishes, macroinvertebrates, zooplankton, macrophytes, phytoplankton, periphyton and bacterioplankton), under different climates. We analyzed data obtained from latitudinal and altitudinal gradients and cross-comparison (i.e. SFTS) studies, supplemented by an analysis of published geographically dispersed data for those communities or traits not covered in the SFTS literature. We found only partial empirical evidence supporting the theoretical predictions. The prediction of higher richness at warmer locations was supported for fishes, phytoplankton and periphyton, while the opposite was true for macroinvertebrates and zooplankton. With decreasing latitude, the biomass of cladoceran zooplankton and periphyton and the density of zooplankton and macroinvertebrates declined (opposite for fishes for both biomass and density variables). Fishes and cladoceran zooplankton showed the expected reduction in body size with higher temperature. Life history changes in fish and zooplankton and stronger trophic interactions at intermediate positions in the food web (fish predation on zooplankton and macroinvertebrates) were evident, but also a weaker grazing pressure of zooplankton on phytoplankton occurred with increasing temperatures. The potential impacts of lake productivity, fish predation and other factors, such as salinity, were often stronger than those of temperature itself. Additionally, shallow lakes may shift between alternative states, complicating theoretical predictions of warming effects. SFTS and meta-analyses approaches have their shortcomings, but in combination with experimental and model studies that help reveal mechanisms, the “field situation” is indispensable to understand the potential effects of warming.

Effects of Submerged Vegetation on Water Clarity Across Climates

A positive feedback between submerged vegetation and water clarity forms the backbone of the alternative state theory in shallow lakes. The water clearing effect of aquatic vegetation may be caused by different physical, chemical, and biological mechanisms and has been studied mainly in temperate lakes. Recent work suggests differences in biotic interactions between (sub)tropical and cooler lakes might result in a less pronounced clearing effect in the (sub)tropics. To assess whether the effect of submerged vegetation changes with climate, we sampled 83 lakes over a gradient ranging from the tundra to the tropics in South America. Judged from a comparison of water clarity inside and outside vegetation beds, the vegetation appeared to have a similar positive effect on the water clarity across all climatic regions studied. However, the local clearing effect of vegetation decreased steeply with the contribution of humic substances to the underwater light attenuation. Looking at turbidity on a whole-lake scale, results were more difficult to interpret. Although lakes with abundant vegetation (>30%) were generally clear, sparsely vegetated lakes differed widely in clarity. Overall, the effect of vegetation on water clarity in our lakes appears to be smaller than that found in various Northern hemisphere studies. This might be explained by differences in fish communities and their relation to vegetation. For instance, unlike in Northern hemisphere studies, we find no clear relation between vegetation coverage and fish abundance or their diet preference. High densities of omnivorous fish and coinciding low grazing pressures on phytoplankton in the (sub)tropics may, furthermore, weaken the effect of vegetation on water clarity.

Dual thinking for scientists

Recent studies provide compelling evidence for the idea that creative thinking draws upon two kinds of processes linked to distinct physiological features, and stimulated under different conditions. In short, the fast system-I produces intuition whereas the slow and deliberate system-II produces reasoning. System-I can help see novel solutions and associations instantaneously, but is prone to error. System-II has other biases, but can help checking and modifying the system-I results. Although thinking is the core business of science, the accepted ways of doing our work focus almost entirely on facilitating system-II. We discuss the role of system-I thinking in past scientific breakthroughs, and argue that scientific progress may be catalyzed by creating conditions for such associative intuitive thinking in our academic lives and in education. Unstructured socializing time, education for daring exploration, and cooperation with the arts are among the potential elements. Because such activities may be looked upon as procrastination rather than work, deliberate effort is needed to counteract our systematic bias.

Bimodality in stable isotope composition facilitates the tracing of carbon transfer from macrophytes to higher trophic levels

Even though the suitability of macrophytes to act as a carbon source to food webs has been questioned by some studies, some others indicate that macrophyte-derived carbon may play an important role in the trophic transfer of organic matter in the food web of shallow lakes. To evaluate the importance of macrophytes to food webs, we collected primary producers—macrophytes and periphyton—and consumers from 19 South American shallow lakes and analyzed their carbon stable isotopes composition (δ13C). Despite the diversity of inorganic carbon sources available in our study lakes, the macrophytes’ δ13C signatures showed a clear bimodal distribution: 13C-depleted and 13C-enriched, averaging at −27.2 and −13.5‰, respectively. We argue that the use of either CO2 or HCO3− by the macrophytes largely caused the bimodal pattern in δ13C signals. The contribution of carbon from macrophytes to the lake’s food webs was not straightforward in most of the lakes because the macrophytes’ isotopic composition was quite similar to the isotopic composition of periphyton, phytoplankton, and terrestrial carbon. However, in some lakes where the macrophytes had a distinct isotopic signature, our data suggest that macrophytes can represent an important carbon source to shallow lake food webs.