Phytoplankton indicative species of trophic status in temperate lakes in mid-summer, modified from Bellinger and Sigee .
Eutrophication is one of the most widespread problems of inland waters in the world. In many countries from North to South America, eutrophication is due to several impacts resulting from the inefficient or nonexistent wastewater treatment; the agricultural expansion with inadequate soil uses and application of chemical fertilizers; the urbanization of watersheds, the increase of intensive husbandry of cattle, pigs, and chicken; the increase of aquaculture; the construction of reservoirs; and the destruction of natural ecosystems. Basically, the increase in the internal load of nitrogen and phosphorus in lakes and reservoirs produces an increase in the biological productivity of the water bodies. As consequence, phytoplankton community in freshwater systems is mainly dominated by cyanobacteria. Despite differences in continental climate regimes, this seems to be a regular pattern along the Americas, where there are various practices related to the use of lower and upper taxonomic groups of phytoplankton for the indication of the trophic level and water quality status of freshwater systems. As was reported in numerous studies in the Americas, increase in nutrient concentrations mainly due to rich in phosphorus cause larger phytoplankton biomass and predominance of cyanobacteria such as genera Microcystis, Anabaena, Planktothrix, Oscillatoria, and Cylindrospermopsis than ever before.
- cyanobacterial dominance
Eutrophication, defined as the nutrient enrichment process (mainly nitrogen and phosphorus) of any water body which results in an excessive growth of phytoplankton and macrophytes [1, 2, 3], has become a major cause of concern in developing as well as developed countries . Also, it was recognized as a pollution problem in the European and North American lakes and reservoirs in the mid-twentieth century. Since then, it has become more widespread in the whole world.
Eutrophication is due to several impacts resulting from the inefficient or nonexistent wastewater treatment; the agricultural expansion with inadequate soil uses and application of chemical fertilizers; the urbanization of watersheds; the increase of intensive husbandry of cattle, pigs, and chicken; the increase of aquaculture; the construction of reservoirs; and the destruction of natural ecosystems . The eutrophication event describes formation of a set of symptoms in a lake system exposed to excessive nutrient increase . Common symptoms due to eutrophication include excessive algal blooms, tremendous organic and inorganic material accumulation, and lower biodiversity, high turbidity, excessive sedimentation, and high anoxia conditions, particularly in the deeper parts of lakes. The increase in anoxia condition can cause fish deaths in midsummer. One of the first and worst symptoms of eutrophication has been formation of planktonic algal blooms. In freshwaters, former of these algal blooms are mostly nitrogen (N)-fixing cyanobacteria .
Eutrophic water bodies are richly supplied with plant nutrients (N, P, as well other nutrients of less acute demand), and consequences include the increase of biological productivity and turbidity of water because of dense growths of phytoplankton [6, 7]. Thus, phytoplankton community structures and their relevant participants could be used as a biological indicator of negative environmental impacts formed in lakes and reservoirs, as was eutrophication event .
In the Americas, as was reported in previous studies, the increase in nutrient concentrations leads to greater biomass of phytoplankton in freshwater systems. In this new region of the world, there are numerous experiences relating the effect of eutrophication on the phytoplankton community.
In this book chapter, we aimed to provide a short overview based on the sparse and scattered literature sources and fixed practices in the American continent related to the proliferation of certain groups of phytoplankton in lakes and reservoirs in terms of eutrophication. We try to depict some generalizations that have arisen from this review, in relation to dominant phytoplankton in the eutrophic lakes and reservoirs in the Americas.
2. Eutrophication and phytoplankton
Excessive nutrient accumulation in aquatic ecosystems by carrying of anthropogenic sources, mainly rich in phosphorus (P) and nitrogen (N), creates a series of changes in their structure and function in the direction of deterioration of water quality, known as eutrophication . Among the structural changes caused by the eutrophication, there is the dominance of the “r” selective species in the community structure of phytoplankton known as tiny primary pelagic producers, particularly in the predominance of cyanobacteria in the freshwater ecosystems such as lakes and reservoirs.
As were reported by Bellinger and Sigee , the detection of excessive harmful blooms of some algae that are biological indicators of environmental pollution, particularly of nutrient pollution, reveals anthropogenic activities in freshwater systems and a rapid change in their trophic status. It is known that in the mid-twentieth century, some researchers such as Thunmark , Nygaard , and Stockner  developed trophic status indexes by using typical algal groups of oligotrophic (particularly desmids, a group of green algae) or typical algal groups of eutrophic conditions (chlorococcal, cyanobacterial, and euglenoid species). Although these indices provide useful information about trophic status of the lakes, generally they are not enough to indicate a lot of environmental problems since a lot of algal species have been living in both eutrophic and oligotrophic freshwater systems. In the other word, there are a lot of similarities in view of species homogeneity and seasonal succession of species for both systems. The rehabilitation of previous methods on sampling and taxonomic analysis, and development of new methods in this framework have provided the development in indices based on more specific indicator algal species from different taxonomic groups. Thus, Bellinger and Sigee  revealed in their books what the indicator species of the trophic status would be in mid-summer in temperate lakes (Table 1).
|Lake types||Algal indicators|
In the Americas, there are some examples about how phytoplankton groups and species have been used for the determination of the trophic status and quality of surface waters. Some of these experiences will be presented in the following sections.
2.1 North America
|Lake types||Algal indicators|
In the Experimental Lake Area (ELA), located in Ontario, Schindler  and Schindler et al.  showed that water fertilization (N and P) causes quantitative increase of all phytoplankton groups, especially the cyanobacteria species
2.1.2 The United States of America
In 1978, the Environmental Protection Agency (EPA) published a study about eutrophication relating aquatic plant response to nutrient loading to lakes and reservoirs . There was good correlation between phosphorus loading and the average chlorophyll
In several lakes suffering the eutrophication process, green algae and diatoms have been replaced by cyanobacteria, particularly
Cyanobacteria dominance in the eutrophic Lake Chapala is described by de Anda and Shear . The high TN and TP concentrations contained in the large quantities of domestic, agricultural, and industrial sewage that enter to the lake through its main tributary, the Lerma river, increased the phytoplankton biomass and resulted in the dominance of
Tomasini-Ortiz et al.  reported the dominance of
Valle de Bravo reservoir (State of Mexico) provides drinking water to about 2,500,000 inhabitants in Mexico City . This water body also shows frequent cyanobacterial blooms as consequence of the high nutrient load in its waters, posing health risks for human population. The common genera found during blooms are
2.2 Central America
Unregulated land use and lack of wastewater treatment have led to eutrophication in many lakes of Guatemala . Some examples of this situation are the following studies.
Basterrechea  found the prevalence of cyanobacteria in the Lake Amatitlán due to eutrophic conditions. Similarly, Rejmánková et al.  recorded blooms of the
The Lake Yojoa is the largest natural lake in the country and represents an important natural resource for Hondurans . The lake is used extensively for commercial production of tilapia fish; fishes are raised to full maturity in floating cages in the lake, and subsequently, high nutrient load is directly supplied to the water body. Other sources of nutrients are: (a) significant amount of wastewater from the ineffective product of water treatment plant, (b) wastewater from restaurants around the lake, and (c) agricultural practices in the neighboring lands, where fertilizers are commonly used, thus contributing with nutrients to the system, having an impact on water quality .
Because of the high input of nutrients, cyanobacteria are the dominant phytoplankton group that accounted for 59.0% of total phytoplankton in the lake . Dominant species in the lake are
2.2.3 El Salvador
Wastewater effluents and similar runoffs with high nutrient concentrations derived from agricultural fertilizers, which are increased by the susceptibility to erosion, deforestation, and sediment trawling, have induced the eutrophication process and, consequently, produced the proliferation of
The Cerrón Grande reservoir also suffered the eutrophication process, and its waters are classified as hypereutrophic. The dominant cyanobacteria species is
In the eutrophic Lake Xolotlán (Lake Managua), Hooker and Hernández  and Erikson  found high phosphorus concentrations (≈150 μg/L), turbid waters (0.40 m of transparency), and high algal biomass of mainly “blue-greens” (cyanobacteria). Phytoplankton community was dominated by cyanobacteria throughout the entire year , and
Vammen et al.  pointed out that increased eutrophication in Lake Cocibolca (Lake Nicaragua) had resulted in the increase of phytoplankton density and a marked dominance of two cyanobacterial species (
Hernández González et al.  also found that the most representative phytoplankton genera detected during most of the period sampled in the eutrophic lakes Cocibolca, Tiscapa, and Masaya, were cyanobacteria, among which are distinguished
2.2.5 Costa Rica
Umaña et al.  stated that there are few long-term works in lakes in Costa Rica, which have shown a wide annual variation of their characteristics. In the Talamanca region of the province of Limón, Jones et al.  found a gradient of trophic states, varying from high-altitude lakes with a tendency to be oligotrophic, to lower-altitude lakes with a tendency to be eutrophic, despite being located in woodland regions where it is away from any human disturbances. These researchers express that, because they do not have a high burden of anthropic phosphorus, their planktonic communities do not show the classic dominance of cyanobacteria against other planktonic groups, but rather a higher prevalence of green algae, a few dinoflagellates and a few cryptomonadales, all of which suggest a more balanced availability between nitrogen and phosphorus. On the other hand, the Arenal reservoir, the largest water body in Costa Rica, located between the provinces of Guanacaste and Alajuela, has been classified as mesotrophic by Jones et al. , representing varied phytoplanktonic community that is dominated by green algae, some diatoms, and cyanobacteria (
Reservoirs of the Panama channel show a mesotrophic status, with a predominance of diatom populations that are represented by 40.0% of total phytoplankton in Gatún reservoir, 55.1% in Alajuela reservoir, and 58.0% in Miraflores reservoir .
Gómez Luna et al.  identified the phytoplankton communities in three reservoirs which are used for drinking water supply to 80.0% of the inhabitants in the City of Santiago de Cuba. High concentrations of nutrients were detected in Chalóns, Charco Mono, and Paradas reservoirs, where the phytoplankton communities were dominated by the cyanobacterial species
2.2.8 Puerto Rico
Pantoja Agreda  conducted a limnological characterization of Guajataca reservoir, which was classified as mesotrophic. The dominant phytoplankton group were Euglenophyta (43.8% of total phytoplankton), followed by Pyrrhophyta (34.9%) and Chlorophyta (10.7%); cyanobacteria accounted for less than 5.00% of total algal density. This fact is common in water bodies with high content of organic matter.
2.3 South America
According to Roldán  and Roldán and Ramírez , water bodies with more signs of eutrophication (Porce II, El Peñol, Prado, and Tominé) have a predominance of cyanobacteria, especially of the genera
Composition of phytoplankton in the Lake Yahuarcocha is dominated by the following species:
2.3.3 Peru and Bolivia
In the Lake Titicaca, in the corresponding Bolivian basin, Fonturbel and Castaño-Villa  considered nutrient concentrations and phytoplankton groups as a whole to determine that the families Oscillatoriaceae and Nostocaceae (cyanobacteria) respond positively to the increase in pH (alkalinization) and negatively to the increasing nutrients, while the families Naviculaceae (diatoms), Closteriaceae, and partly Zygnemataceae (green algae) showed an inverse tendency with proliferating in acidic water enriched with nutrients. The diatoms seem to respond negatively, both to the acidification of the water and to the excessive nutrient enrichments. Studies revealed that they are the most sensitive groups to the eutrophication of waters.
Between the 1970s and 1990s, both sections of the Lake Titicaca, deep Lago Mayor and large part of shallow Lago Menor, were oligotrophic with high water transparency and strong nitrogen limitation. Chlorophyta and cyanobacteria (particularly
Numerous studies on eutrophication of freshwater ecosystems have been conducted along the Brazilian territory. Prevalence of cyanobacteria under this eutrophic condition has also been reported.
Tundisi  reported blooms of the cyanobacteria
Lake Vaca Brava, in the State of Goiás (Central Western Brazil), is an urban water body that suffers the eutrophication process as a consequence of the human settlement in its neighboring areas . Increased cyanobacterial density accompanies the eutrophication process, where
Likewise, Chellappa et al.  studied the dynamics of phytoplankton in the Armando Ribeiro Gonçalves reservoir, located in the state of Rio Grande do Norte (Northern Brazil), which is used for drinking water supply; this reservoir was classified as eutrophic due to its high nutrient concentrations, and the toxic cyanobacteria dominated the phytoplankton composition, particularly
Due to inadequate treatment, sewage with high levels of P and N reaches to Pampulha and Ibirité reservoirs in South-Eastern Brazil [53, 54], causing changes in the composition and diversity of the plankton community.
Despite resulting in known impacts, such as loss of aquatic biodiversity, the emergence of potentially toxic cyanobacterial blooms, overgrowth of aquatic macrophytes, anoxia and fish mortality, increased eutrophication of Brazilian reservoirs has also, as an additional consequence, the increase of greenhouse gas emission that aggravates the global warming process [55, 56].
In this country, it has also been reported that the increase in the concentration of nitrogen and phosphorus leads to an increase in phytoplankton biomass and to the dominance of cyanobacteria . In lakes which have heavy eutrophication process, the dominant cyanobacteria which occur blooms are usually of
Quirós , analyzing the empirical relationships between nutrient concentrations and biological communities in more than 100 Argentine lakes and reservoirs, found that total phosphorus concentration is the main factor in the control of the phytoplankton biomass. Likewise, he also found that the applied empirical order grouped lakes in two groups which are the lakes located in the lower latitudes which are shallow, warm, and eutrophic where phytoplankton are limited by nitrogen, and the lakes located in higher latitude, temperate-cold, and oligotrophic where phytoplankton are limited by phosphorus . Also, Quirós et al.  found that nutrient enrichment of the Pampa’s surface water and its multiple negative effects on its lagoons have increased the internal phosphorus load allowing the increase in the frequency of cyanobacterial blooms, especially during relatively dry years.
The largest reservoirs (Salto Grande, Bonete, Baygorria, and Palmar) have suffered the process of eutrophication, which has led to an intense growth of phytoplankton . De León and Chalar , Chalar et al. , and Chalar [68, 69] studied the phytoplankton dynamics of the Salto Grande reservoir and recorded the dominance of typical diatoms in eutrophic environments and high densities of cyanobacteria which are predominant with
Vidal et al.  had detected cyanobacterial blooms, mainly supported by
RAP-AL  also detected that in the eutrophic system of Laguna del Sauce which has a predominance of cyanobacteria throughout the year, there was a marked increase in the frequency and duration of microalgae blooms, particularly of
The rapid growth of anthropogenic or human sourced activities has led to the environmental degradation of the Lake Ypacaraí, the most renowned water body in Paraguay . Increasing nutrient concentrations over the last decades have recently resulted in intense cyanobacterial blooms; dominant species in the lake are
González and Quirós , when they considered trends in 16 reservoirs that have different trophic status, found both linear relationship, between total phosphorus (TP) and total nitrogen (TN) with the phytoplankton biomass, and empirical relationship, between total phosphorus concentration and the nitrate/ammonia quotient which determine the dominance of cyanobacteria. According to the authors’ empirical ordination, Venezuelan reservoirs were separated in three groups: group 1 includes reservoirs with low TP (<20 μg/L), while groups 2 and 3 include those reservoirs with moderate to high TP concentrations (>20 μg/L) (Figure 1). In group 1, green algae (chlorophyta) are dominant. Group 2 is composed by those reservoirs where nitrate is the dominant inorganic nitrogen compound over ammonia (high nitrate/ammonia quotient), with short water residence time, and the dominant phytoplankton taxa are different from cyanobacteria, while group 3 is composed by those reservoirs with low nitrate/ammonia quotient, high residence time of their waters, and the dominant phytoplankton is cyanobacteria.
Surveys have shown that more than 40.0% of lakes and reservoirs in the Americas are in eutrophic trophic level [1, 74], and this is a major cause of concern in the developing as well as developed countries.
According to Pratts et al. , one of the main problems that affect lakes and reservoirs is the eutrophication. It induces undesirable ecological consequences for the water bodies [1, 3], such as excessive phytoplankton and macrophyte growth. This reduces light penetration and restricts the reoxygenation of water, therefore generating anoxic conditions in the hypolimnetic layers of lakes and reservoirs, as well as high decomposition rates of organic matter that produces a foul smell and makes the water more turbid. Other negative consequences are the proliferation of algal blooms and toxic phytoplankton, fish mortality by suffocation due to drastic oxygen concentration drop during the overturning of waters, proliferation of adequate habitats for vectors of tropical diseases, and loss of biodiversity. These problems are especially important if the water bodies are used for drinking water supply: if these problems are inadequately treated, they may involve serious health risks for human populations.
Regarding the main primary producers in lakes and reservoirs, phytoplankton communities respond quickly to environmental change (as the fertilization of waters with nitrogen and phosphorus) and are indicators of eutrophication . They also show different community dynamics in ecosystems with contrasting trophic states, where high nutrient levels generally favor species belonging to cyanobacteria group.
In most of the studies on lakes and reservoirs in the Americas discussed in the present work, and despite their regional, latitudinal, altitudinal, and climatic differences, eutrophic conditions have led to be dominated by specific species of cyanobacteria. Then, species from the genera
According to Reynolds et al.  and Bellinger and Sigee , cyanobacteria adapts to all types of freshwater environment, including extreme conditions and frequently have the ability to compete with other phytoplankton groups under eutrophic conditions in surface waters. Shapiro  and Dokulil and Teubner  stated that the ability of “blue-greens” to outcompete other freshwater algae has been attributed to a range of characteristics, including:
increasing trend in temperature due to climate change;
optimum growth at high temperatures not preferred by other phytoplankton groups, as in diatoms;
high survival ability in the water column compared to other species under low light tolerance caused by extensive algal bloom;
tolerance to low N/P ratios, which is the characteristic for eutrophic lakes—allowing continued growth when N becomes limited;
depth regulation by buoyancy—avoiding photoinhibition during the early phase of population increase, and allowing algae to obtain inorganic nutrients from the hypolimnion layer when the nutrients decrease in the epilimnion layer from mid- to late-summer;
resistance to zooplankton grazing by both mechanical and chemical interference;
tolerance to high pH and low CO2 concentrations, allowing continued growth of “blue-greens” (but not other algae) at the lake surface during the extensive bloom formation; and
symbiotic association with aerobic bacteria—bacterial symbionts at the heterocyst surface provide the local reducing atmosphere required for nitrogen fixation that causes inorganic nutrients accumulation in surface waters, poor in nutrients.
The dominance of cyanobacteria in eutrophic water bodies can also be explained according to the main meaningful functional groups proposed by Reynolds [85, 86] and Reynolds et al. , based on nutrient availability and stability of the water column. Thus, cyanobacteria can dominate in the phytoplanktonic community in an array of warm, mixed, and fertilized (mainly phosphorus) water bodies, with low transparency values and limitation in C and N [87, 88].
In most of the eutrophic lakes and reservoirs in the Americas, as were in various researches on freshwater systems in the temperate regions, there are important increases in level of nutrients, mainly in level of phosphorus, which leads to excessive phytoplankton biomass firstly in a predominance of cyanobacteria. Likewise, in most cases, the dominant cyanobacterial species belong to the genera
Authors would like to thank the Inter American Network of Academic of Sciences (IANAS) for all its help in gathering the information.
We also thank Dr. Diego Rodríguez and an anonymous reviewer for improving the language translation.
Conflict of interest
The authors declare no conflict of interest.
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