The phytoplankton community of Lake Ontario was assessed during April, July and September 2008 as part of the Cooperative Science and Monitoring Initiative (CSMI) framework. Results were also compared with historic surveys that began in 1970. A total of 320 unique species were identified during 2008, the vast majority being considered ‘rare’ or ‘less common’. The biomass was found to be, on average, 1.6 g m−3 in spring, 3.0 g m−3 in early summer and 2.4 g m−3 in late summer with rare and less common species accounting for 60–80% of the total. Analysis of the size structure of the phytoplankton community combined with size fractionated primary productivity experiments revealed that one picoplankton (<2 μm) species, Chroococcus dispersus var. minor, accounted for up to half of the observed primary productivity, despite contributing 1% or less to total biomass. Our results also showed that the lake was mesotrophic during the summer of 2008 (July and September) and that trophic state has fluctuated between hyper-eutrophic and ultra-oligotrophic since monitoring began in 1970. These findings demonstrate that the Lake Ontario ecosystem is continually changing and more frequent sampling is needed. A high level of taxonomic expertise is required for even the most basic assessments of the phytoplankton community structure and improved taxonomic training and implementation of standardized techniques are necessary.

Introduction

During the recent past, Lake Ontario's ecosystem has been exposed to multiple stressors such as: eutrophication, toxic contamination, phosphorus abatement, invasive species and global climate change (Mills et al., 2003). Assessing the impact of these stressors on the whole system is extremely important for a top-down understanding of its ecology and management. Lake Ontario, the world's 11th largest lake (1,640 km3; Reynolds et al., 2000), forms part of the international border between Canada and the United States and is jointly managed by both countries under the terms of the Great Lakes Water Quality Agreement. In response to widespread public concerns over eutrophication, both countries organized lake wide surveys of the lower trophic levels beginning in 1970 with the aim of developing a phosphorus abatement program (implemented in 1978). While these early surveys represent a baseline in terms of ecosystem health assessments, follow up surveys have been relatively sparse.

The first comprehensive lake wide surveys of Lake Ontario were conducted in 1970 by the Fisheries Research Board of Canada (now Fisheries and Oceans Canada). The results of the earliest lakewide survey in 1970 showed that on an annual basis, phosphorus loads (≈1 g m−2), primary production (≈220 g C m−2) and mean chlorophyll a (≈5 μg l−1) were indicative of mesotrophic conditions based on Vollenweider's eutrophication models (Vollenweider et al., 1974). These surveys were also the first to deploy the Utermöhl (1958) methodology for assessment of the phytoplankton community in the Great Lakes. Phytoplankton biomass in 1970 was extremely high by mid-summer with a lakewide average of 8.6 g m−3 and dominated by larger species of Chlorophyta and Cyanophyta indicating an elevated trophic state (Munawar and Nauwerck, 1971; Munawar and Munawar, 1982). The 1978 survey, which followed the implementation of phosphorous controls earlier that year, revealed a sharp decrease in phytoplankton biomass to 1.2 g m−3 and a shift in species composition towards smaller phytoflagellates (Cryptophyceae) and diatoms (Munawar and Munawar, 1986, 1996, 2003; Munawar et al., 1987). The next round of plankton surveys were carried out 12 years later, in 1990, as part of the Lake Ontario Trophic Transfer (LOTT) study and again revealed a phytoplankton community in a state of flux (Munawar and Munawar, 2003).

The United States Environmental Protection Agency also conducted lake wide offshore surveys of Lake Ontario phytoplankton. Surveys in 1972–1973 highlighted the abundance and distribution of Diatom communities across the lake (Stoermer et al., 1975; Stoermer and Ladeski, 1978). Because of differences in study design, these results were not directly comparable with the Canadian surveys. In later years, the EPA adopted the standard Utermöhl methodology and conducted surveys more or less annually from 1986–1992 (5/6 years) which revealed a phytoplankton community continually adapting to phosphorus abatement (Makarewicz et al., 1995). A further study conducted in 1998 found that phytoplankton species composition in Lake Ontario was unique compared to the other Great Lakes (Barbiero and Tuchman, 2001). There has been a greater attempt to integrate the Canadian and American research efforts in Lake Ontario under the banner of the Cooperative Science and Monitoring Initiative (CSMI) for the most recent surveys during 2003 (Munawar et al., 2010) and 2008 in order to ensure consistency of methods and reduce duplication.

This article deals with the biomass, species and size composition of phytoplankton based on the most recent investigation of Lake Ontario carried out during 2008. We also consider long term trends in the phycology of Lake Ontario and the broader implications relating to trophic state and ecosystem health.

Materials and methods

Lake Ontario covers 19,100 km2 with a mean depth of 86 m, and has a retention time of 8 years (Beeton, 1984). Synoptic surveys were conducted during spring (April), early summer (July) and late summer (September) of 2008. Nine stations distributed across three North-South transects of Lake Ontario were sampled (Figure 1). Water was collected using an integrated sampler (Schroeder, 1969) to a maximum depth of 20 m or 2 m off the bottom at shallower sites. Phytoplankton samples were preserved immediately in Lugol's iodine. Analysis of biomass, species and size composition followed the standard Utermöhl (1958) inverted microscope procedure, a methodology consistent with earlier studies (Vollenweider et al., 1974; Munawar and Munawar, 1996). All species names were verified according to, preferentially, AlgaeBase (Guiry and Guiry, 2014) or the Integrated Taxonomic Information System (www.itis.org) and are listed in Appendix 1 (available in the online supplementary information) and any differences with our historic nomenclature are noted. Phytoplankton species were assigned to the following size classes: picoplankton (<2 μm), nanoplankton (2–20 μm) and net plankton based on the greatest axial linear dimension. Size-fractionated productivity experiments were conducted shipboard using 14Carbon following the standard procedure described by Munawar and Munawar (1996). Chlorophyll a concentrations were determined by acetone pigment extraction (Strickland and Parsons, 1968). The chlorophyll a data has been provided courtesy of the U.S. EPA.

Results

Phytoplankton biomass and composition

Seasonal trends

Phytoplankton biomass was relatively low during April (Figure 2a) showing a lake wide average of 1.6 g m−3 with a range of 1.2 to 2.6 g m−3. The highest biomass concentrations were observed at stations 17 (2.6 g m−3), 41 (2.1 g m−3) and 74 (2.1 g m−3). Taxonomic composition during the spring cruise indicated that the mean lake wide biomass was composed of Dinophyceae (32%), Chlorophyta (28%) and Diatomeae (15%).

Phytoplankton showed higher concentrations during early summer (July) compared to spring and late summer (Figure 2b) with an average of 3.0 g m−3 and a range of 1.5 to 4.7 g m−3. The largest values were recorded in the eastern transect at Stations 71 and 74. The phytoplankton community in July, as a lakewide mean, consisted of Diatomeae (26%), Dinophyceae (22%) and Chrysophyceae (18%).

During the late summer (September) cruise, mean phytoplankton biomass was slightly lower (2.4 g m−3) than July and ranged from 1.6 to 4.6 g m−3 (Figure 2c). The highest biomass concentrations were observed at Stations 80, 71 and 43. The mean composition was Dinophyceae (27%), Chlorophyta (21%) and Cryptophyceae (21%).

Chlorophyll a concentrations are shown in Table 1. The chlorophyll a concentration was low in the spring, with a mean of 1.6 μg l−1ranging from 0.5 to 2.9 μg l−1. The concentration was highest during early summer with a mean of 3.2 μg l−1 (ranging from 1.1 to 6.8 μg l−1). The mean concentration decreased in the late summer cruise, tapering off to 1.9 μg l−1 with a range of 0.9 to 2.7 μg l−1.

Species composition and diversity

The overall species composition identified during 2008 on a lake wide basis is shown Appendix 1. The species were classified as ‘rare’, ‘less common’ and ‘common’ based on their relative contribution to the total biomass from one or more stations (i.e. rare: <1%, less common: 1–5% and common: >5%). Since the distribution of species may vary across the lake, it is possible for the same species to fall into one of the three levels at various stations. The total number of species found in each category is shown in Table 2. A total of 133 species were identified as being rare in April, compared with 211 in July and 218 in September. Substantially fewer species were identified as less common (April: 51; July: 55; September: 74) and even fewer were identified as common (April: 14, July: 8; September: 13). The following taxonomic groups were the main contributors of species by season:

Spring

Rare: Diatomeae, Chrsysophyceae, Chlorophyta

Less common: Diatomeae, Dinophyceae, Cryptophyceae

Common: Dinophyceae, Diatomeae, Chrysophyceae

Early summer

Rare: Chrysophyceae, Chlorophyta, Diatomeae

Less common: Diatomeae, Chrysophyceae, Dinophyceae

Common: Diatomeae, Dinophyceae, Cyanophycta

Late summer

Rare: Chlorophyta, Chrysophyceae, Diatomeae

Less common: Dinophyceae, Chlorophyta, Cryptophyceae

Common: Dinophyceae, Cryptophyceae, Diatomeae

Table 3 shows the number of species for each station, grouped by their contribution to the total phytoplankton biomass. For the three seasons the rare species contributed a mean of 38 (spring), 64 (early summer), and 70 (late summer) species, which contributed 17%, 23% and 25% to the total phytoplankton biomass, respectively. The less common category had a mean of 14, 18 and 18 species for the three surveys (44%, 49% and 52% of the biomass, respectively). Finally common species harboured only 2–3 species in each of the three cruises (contributing 39%, 27% and 22% to the biomass, respectively). The combined rare plus less common species contributed 61% of the total biomass during spring, 72% in the early summer and 77% in the late summer.

Common species

On a lake-wide basis, only a limited number of species were classified as ‘common’:

Spring

Chlorophyta: Spermatozopsis sp.

Chrysophyceae: Chrysochromulina parva, Mallomonas sp., Ochromonas scintillans

Diatomeae: Cyclotella comta, C. glomerata, C. ocellata, Stephanodiscus Hantzschii

Cryptophyceae: Rhodomonas minuta

Dinophyceae: Gymnodinium helveticum, G. uberrimum, Peridinium aciculiferum, P. africanum, P. inconspicuum, Peridinium spp.

Early summer

Cyanophyta: Oscillatoria limnetica, O. minima

Chlorophyta: Tetraedron muticum

Chrysophyceae: Chrysochromulina parva

Diatomeae: Fragilaria crotonensis, Synedra acus var. radians

Cryptophyceae: Cryptomonas ovata, Rhodomonas minuta

Dinophyceae: Gymnodinium uberrimum, Peridinium aciculiferum

Late summer

Cyanophya: Dolichospermum flosaquae

Chlorophyta: Coelastrum sphaericum

Chrysophyceae: Ochromonas globosa

Diatomeae: Fragilaria crotonensis

Cryptophyceae: Cryptomonas tetrapyrenoidosa, Rhodomonas minuta, R. minuta var. nannoplanctica

Dinophyceae: Ceratium hirundinella, Glenodinium sp., Gymnodinium helveticum, Peridinium aciculiferum, P. inconspicuum, P. palatinum

Spatial transects

Biomass and taxonomic composition

Figure 3 shows the distribution and composition of phytoplankton biomass by taxonomic groups at three transects from west to east in the three seasons. The values reported are the arithmetic mean for each transect. In spring, the mean phytoplankton biomass was similar in all the three transects (1.6–1.7 g m−3). Dinophyceae and Chlorophyta were prevalent at all transects. Diatomeae, Chrysophyceae and Cryptophyceae contributed moderately.

In the early summer the biomass showed an increasing gradient from west (2.2 g m−3) to east (4.0 g m−3). Dinophyceae, Chrysophyceae and Chlorophyta contributed significantly at the western transect. Diatomeae were more prevalent in the central and eastern transects, contributing 36% and 30% to total biomass, respectively.

In the late summer, the western and central transects had a similar mean biomass (≈2 g m−3); whereas the biomass was about 50% higher in the eastern transect (3.2 g m−3; Figure 3). In the western transect, Chlorophyta (23%), Cryptophyceae (23%) and Dinophyceae (21%) were the most common groups of phytoplankton. At the central transect Dinophyceae (28%), Chlorophyta (25%) and Diatomeae (15%) were more prevalent. Finally, in the east, Dinophyceae (34%), Cryptophyceae (26%) and Chlorophyta (16%) were the common groups of algae.

Biomass, size and species composition

The size distribution of the phytoplankton community is presented in Figure 4. Picoplankton (<2 μm) biomass was relatively low ranging from 20.9–68.7 mg m−3 or roughly 1–4% of the total biomass at all transects and seasons. The nanoplankton (2–20 μm) fraction ranged from 911.7–1 561.4 mg m−3 and dominated at all transects in the spring as well as the western transect for early and late summer. Net plankton (>20 μm) biomass ranged from 528.0–2 408.5 mg m−3 and was most prevalent in the central and eastern transects during early and late summer.

The top phytoplankton species from each size group is shown in Table 4. The 5 species contributing the most to the total biomass within each size category at each transect were selected. However, only a single species of picoplankton, Chroococcus dispersus var. minor, is reported since on average, it composed 92% of the picoplankton biomass. It was found at all three transects in all seasons, indicating a lake wide distribution.

From the selected top species, the following were recorded at all transects in the three seasons: the picoplankton Chroococcus dispersus var. minor; and the nanoplankton: Chrysochromulina parva, and Rhodomonas minuta. In addition to the above, the following species were recorded at all transects during specific seasons: in spring, Cyclotella glomerata, Gymnodinium helveticum, and Spermatozopsis sp.; in late summer, Peridinium aciculiferum.

Size-fractionated primary productivity

Primary productivity was estimated for three size fractions: picoplankton, nanoplankton and net plankton (Figure 5). During the spring, primary productivity ranged from 0.1–1.0 mg C m−3 h−1. In the western transect, picoplankton contributed most (average of 51%), followed by nanoplankton (38%) to the total productivity. The net plankton contribution was the lowest (11%). No productivity experiments were possible on the early summer cruise; however, experiments were resumed in the late summer (September). Primary productivity was higher in September, ranging from 3.7–9.4 mg C m−3 h−1. Nanoplankton productivity dominated every transect (45–50%) followed by picoplankton (29–35%). The net plankton contribution was the smallest (15–21%) in September.

Discussion

Lake Ontario has experienced significant ecological changes during the past five decades due to the impacts of eutrophication, contaminants, invasive species, climate change, and phosphorus abatement (Mills et al., 2003). During this period, only 5 lake-wide studies of phytoplankton and primary productivity were conducted in 1970, 1978, 1990, 2003 and 2008 by Fisheries and Oceans Canada (or its predecessor agencies). Despite this limitation, these surveys do provide a window of opportunity to assess major spatial and temporal changes in the ecology of phytoplankton. We will begin the discussion by presenting the results of the 2008 survey followed by a detailed examination of the long term changes in the phytoplankton community.

Size distribution, biomass and productivity

Net plankton (>20 μm) dominated the phytoplankton biomass in the eastern transect in early and late summer (Figure 4) with contributions ranging from 61–63%. Average biomass among transects ranged from a low of 528.0 mg m−3 in the spring (west) to a high of 1,552.2 mg m−3 in the late summer (east). There was a high degree of variability in the species composition of the net plankton. However, Gymnodinium helveticum in the spring and Peridinium aciculiferum in the late summer were common across all transects and were significant contributors to the total biomass. Net plankton productivity was very low in the spring, 0.05 mg C m−3 h−1 increasing to 1.1 mg C m−3 h−1 in the late summer and typically the lowest of all size fractions. Generally, the larger organisms were associated with lowest rates of production.

Nanoplankton (2–20 μm) biomass dominated the three transects in the spring and also in the western transect during early and late summer. Biomass for this size group averaged 911.7–1 561.4 mg m−3 across transects in all three cruises and accounted for 55–66% of the total biomass; Chrysochromulina parva and Rhodomonas minuta were reported in every sample. Cyclotella glomerata and Spermatozopsis sp. were also found in each transect during the spring. Nanoplankton was the most photosynthetically active fraction, primary productivity for this group averaged 0.2 mg C m−3 h−1 in April, or just under half of the total. In September, nanoplankton productivity increased to 2.9 mg C m−3 h−1 again contributing about half of the total. Nanoplankton typically had the highest biomass and the highest rates of production of all size groups.

Picoplankton (<2 μm) biomass was low, on average 13.2–90.6 mg m−3 across the 3 transects during the spring, summer and fall surveys (Figure 4) and comprised only 1–4% of total phytoplankton biomass. Within the size class, Chroococcus dispersus var. minor was ubiquitous in all observations (Table 4) contributing on average >90% of the picoplankton biomass and often being the only species identified. Picoplankton primary productivity averaged 0.2 mg C m−3 h−1 in the spring and 1.9 mg C m−3 h−1 in the summer. Despite being categorized as either rare or less common, our results show that C. dispersus minor was responsible for 29–51% of the total primary productivity observed in the April and September cruises. Previous research on Lake Erie and Lake Superior (Munawar et al., 2008, 2009) has also demonstrated the importance of this one species to autochthonous carbon production in the Great Lakes.

Species diversity and the necessity of standard techniques

The 2008 phytoplankton composition data showed high species diversity in all the three cruises (Table 3; Appendix 1). In spring a large number of species (198) were observed with 133 of those species identified as being “rare” (i.e. contributed <1% to the total phytoplankton biomass). The rare species consisted mainly of Diatomeae, Chrysophyceae and Chlorophyta, each contributing from 32 to 38 species. The “less common” category (between 1–5% of the total biomass) contained 51 species. The “common” category (>5% of total biomass) harboured only 14 species. In the early summer cruise, a higher number of species (274) was recorded consisting of 211 rare, 55 less common and 8 common species. Of the rare species observed in early summer, Chrysophyceae (71 species), Chlorophyta (52) and Diatomeae (49) were the main contributors. The number of species was highest during the late summer (305) comprising 218 rare, 74 less common, and 13 common species. Main contributions to the number of species once again came from the rare category and belonged to Chlorophyta, Chrysophyceae and Diatomeae.

Very few species were identified as common at any site during any cruise and collectively these common species represented only 23–40% of the total biomass (Table 4). Put another way, 60–77% of the total phytoplankton biomass of Lake Ontario was composed of rare and less common species. These results demonstrate that even the most rudimentary understanding of the phytoplankton community requires a very high level of taxonomic expertise. Our results show that counting strategies which rely on the identification of only common species are likely to misrepresent the community.

Previous studies have also drawn attention to the high level of biodiversity in Lake Ontario. For example, during surveys conducted by Fisheries and Oceans Canada (DFO) in 1990, more than 200 phytoplankton species were identified from spring, summer and fall samples (Munawar and Munawar, 2003). Similarly, the United States Environmental Protection Agency (EPA) undertook lakewide surveys from 1986–1992 during spring and summer, identifying 379 species (Makarewicz et al., 1995). The EPA also surveyed Lake Ontario in 1998 and identified more than 100 species in each of the spring and summer (Barbiero and Tuchman, 2001). While there may appear to be wide fluctuations in the biodiversity of Lake Ontario, it is difficult to compare the results of these surveys for a variety of reasons which include differences in sample size, study duration and most importantly, the particular expertise of the phytoplankton taxonomist.

The above species diversity data highlights the great need of carrying out proper taxonomic identification and enumeration of phytoplankton by qualified persons using standard methods. For our part, Fisheries and Oceans Canada (DFO) has followed standard sampling, settling and enumeration techniques (Utermöhl, 1958; Lund et al., 1958; Munawar and Munawar, 1996) for over 40 years. At DFO, qualified, experienced phycologists have been responsible for identification and enumeration of samples which has resulted in the development of consistent, comparable data for the all the Great Lakes. The need for improved taxonomic knowledge and training is not unique to our observations of phytoplankton in Lake Ontario. In an opinion piece, Edward Wilson of Harvard University, described the current state of taxonomic knowledge as the “disgrace of the biological sciences” and argued that “no ecosystem under human pressure can be made sustainable indefinitely without knowing all the species that compose it” (Wilson, 2013). Taxonomy is a critical and often overlooked component of ecosystem health.

The taxonomic composition observed during the three surveys provides some interesting clues about the changing ecology of Lake Ontario phytoplankton. Spring phytoplankton biomass was on average 1.6 g m−3 composed of Dinophyceae (33%), Chlorophyta (28%) and Diatomeae (15%). These taxonomic groups contained a large pool of species (122) identified as rare and less common that could be expected to serve as “seeds” for algal growth, subject to the availability of suitable ecological conditions (Table 3; Appendix 1). For example diatoms harboured 38 rare, 12 less common and 4 common species in the spring. Limiting phosphorous concentrations, irradiance and temperature, to name a few possibilities, may not have been conducive for the growth of these “seed” species. Since diatom growth is dependent on silica utilization (Schelske et al., 1986), it could be hypothesized that the growth of the spring pool of diatoms was inhibited, as evidenced by the rising silica concentration which has more than doubled from 0.4 mg l−1 in 1970 to 0.9mg l−1 in 2008 (Table 5). Alternatively, if diatoms were being grazed by dreissenid mussels in this period, we would expect to find some evidence for diatom growth including silica utilization and elevated carbon turnover rates for larger net plankton. Growth inhibition of diatoms therefore seems more likely.

In the early summer, phytoplankton biomass increased (mean 2.9 g m−3) along with temperatures, however total phosphorus remained low (7.2 μg l−1). During this period, Diatomeae (26%) dominated the biomass along with Dinophyceae (22%) with Chrsysophyceae (18%) close behind. A large number of species were identified (274). Of these, diatoms had 49 rare species, 15 less common, and 2 common species (Table 3; Appendix 1). Diatoms appear to have grown well in the summer compared to the spring as revealed by the depletion of silica to a relatively low concentration (0.13 mg m−3). Deep Chlorophyll Maxima (DCMs) are likely to develop in the metalimnion during this period of early stratification. While our study was not designed to test hypotheses regarding the DCM, the topic was covered in detail by Twiss et al (2012) who reported that phytoplankton biomass in the metalimnion/deep chlorophyll layer were in the range of 0.3–1.4 g m−3. So despite the observed increase in chlorophyll a, phytoplankton biomass was considerably lower in the metalimnion than in the epilimnion. More research is needed in order to understand how the distribution of phytoplankton in the water column results in the formation of a DCM.

In the late summer survey (September), algal biomass was slightly lower (2.5 g m−3) than July. However the community structure changed again with the reduction of diatoms to only an average of 12% of the biomass. Instead, Dinophyceae (27%), Chlorophyceae (21%) and Cryptophyceaen phytoflagellates (21%) contributed significantly to the bulk of the biomass. The highest number of species were found in the September cruise (305), consisting of 218 rare, 74 less common and 13 common species.

In summary, the seasonality of phytoplankton revealed a significant change of patterns as given below:

  • emergence of diatoms now occurring in the early summer rather than spring;

  • increase of phytoflagellates (Dinophyceae, Chrysophyceae and Cryptophyceae) in the late summer; and

  • fewer diatoms in the late summer.

These observed changes in phytoplankton seasonality would suggest considerable variability in many of the species—specific growth factors. For example, while point source phosphorous loadings have declined steadily since the 1970s (Dolan and Chapra, 2012), tributary P loadings have been much more variable resulting in periodic but significant increases in P concentrations in localized (nearshore) areas (Makarewicz et al., 2012). Fluorometric analysis of the phytoplankton community has also shown that these nearshore areas have elevated levels of chlorophyll a (Pavlac et al., 2012; Twiss and Marshall, 2012) however the relationship between chlorophyll a, on one hand, and phytoplankton biomass and species composition, on the other, is not consistent. More work is needed to assess the spatial and temporal extent of such localized influences on phytoplankton taxonomy and biomass.

Long term changes

During spring the total phosphorus concentration has radically decreased from an average of 21.4 μg l−1 in 1970 to 16.8 μg l−1 in 1978 following nutrient controls and further declining to 7.8 μg l−1 in 2008 (Table 5). The average nitrate + nitrite concentration showed an increasing trend since 1970 (0.2–0.4 mg l−1) whereas calcium showed a decreasing trend (40.3 mg l−1 in 1978 to 33.8 mg l−1 in 2008). Soluble reactive silica displayed a steadily increasing trend from 0.3 mg l−1 in 1970 to 0.9 mg l−1 in 2008. The mean surface temperature in 1970 was high (6.4°C) whereas the spring of 1978 was cold (1.8°C). Temperatures increased steadily between 1990, 2003 and 2008. This variability in temperature may be attributable to the timing of the spring cruise (i.e. early April–mid May), rather than being a direct consequence of climate change. The Secchi depth was similar from 1970 to 1990 (3.4–5.0 m) but very high values were recorded during 2003 (10.3 m) and 2008 (11.4 m) following the advent and expansion in populations of exotic species (Nicholls, 2001) in addition to reduced phosphorous loads.

Long term changes of spring phytoplankton and its composition is shown in Table 6. During 1970 the biomass was 1.6 g m−3 and increased in 1990 to 5.8 g m−3 before the onslaught of dreissenid mussels, but after the imposition of phosphorus controls. Later, in 2003 phytoplankton biomass declined drastically to 0.1 g m−3, concurrent with a relatively high biomass (0.3 g m−3) of unicellular heterotrophic plankton (Munawar et al., 2010). However, in 2008 phytoplankton biomass increased to 1.6 g m−3 essentially the same as in 1970. Despite the reductions in both total phosphorus and soluble reactive phosphorus since 1970 (Table 5), the observed fluctuations in phytoplankton biomass suggest that P limitation alone is not regulating the size of the algal standing crop during the spring.

Regarding the spring composition, the Cyanophyta contribution (% total biomass) was very low in all the years (0.01–5.9%). Chlorophyta was low in 1970 (9.3%) and 1990 (8.4%) but increased considerably in the later years (53.3% in 2003 and 30.9% in 2008). During 1970 and 1990 diatoms were prevalent with 55% and 69% contributions, respectively. On the other hand, diatoms decreased significantly to a low of 16% in both 2003 and 2008. In 2003, diatoms were replaced by Chlorophyta and in 2008 Chlorophyta and Dinophyceae were most prevalent. Our data is supported by the observations of Dove (2009) who reported steadily decreasing total phosphorus and calcium concentrations for spring 1969–2008, whereas NO3 + NO2 and soluble reactive silica steadily increased indicating that many biotic and abiotic factors are influencing community composition.

For the summer comparison we used surveys of 1970, 1978, 2003 and 2008 since summer phytoplankton data for 1990 was not available. The biomass was very high (6.2 g m−3) in 1970 but decreased to 1.1 g m−3 in 1978 immediately following phosphorus abatement. It reached a very low level (0.2 g m−3) in 2003 but increased considerably in 2008 (3.0 g m−3). Summer phytoplankton composition was quite variable. Cyanophyta biomass was fairly high in 1970 (0.9 g m−3) but was much lower in subsequent years (0.04–0.2 g m−3). Interestingly, the lowest biomass observed for Cyanophyta in 2003 corresponded with the highest % contribution to total biomass (17%). Chlorophyta contributed the most to total biomass (50%) in 1970, but was much lower in later years (7–14%). Chrysophyceae contributed moderately ranging from a mean of 8% to 18% during the four summer surveys. Diatomeae were variable but increased overall, from a mean of 0.4% in 1970 to a rise in 1978 (19%), a drop in 2003 (8%) and finally a peak at 28% in 2008. Cryptophyceae and Dinophyceae phytoflagellates contributed 27–50% (combined) in all years of comparison.

The robust water quality data base available for the spring from Environment Canada is not available for the summer, however the available data indicates that Secchi depths are increasing (2.1 m in 1970 to 7.2 m in 2008) whereas silica concentrations have been highly variable, ranging from a low of 0.06 mg l−1 in 1971 to a peak of 0.3 mg l−1 in 1982 (Dove, 2009). It is difficult to interpret the observed changes in phytoplankton in the summer due to its variable nature. The 10-fold increase of biomass observed in 2008 compared to 2003 is complex and in need of a reasonable explanation. For 2003, we had previously described a foodweb where heterotrophic nanoflagellates were sequestering organic carbon (Munawar et al., 2010) but the mechanisms of trophic transfer appear to be different in the current (2008) survey. Diatoms contributed the most to total biomass during the summer of 2008 (27.6%), but >70% of the biomass was composed of other taxa. There is little evidence that silica depletion is limiting diatom growth since silica concentrations during 2008 (0.1 mg l−1) were in the middle of the historic range.

Based on the phytoplankton biomass index (trophic ladder) of Munawar and Munawar (1982) and Munawar et al. (2012) the trophic state of Lake Ontario fluctuated, as shown below:

Spring

1970: Oligotrophic

1990: Highly eutrophic

2003: Ultra-oligotrophic

2008: Oligotrophic

Summer

1970: Highly eutrophic

1978: Oligotrophic

2003: Ultra-oligotrophic

2008: Mesotrophic

The trophic state of Lake Ontario has shown considerable variability in both the spring and summer seasons over the four years of comparison. The 2003 data set stands out since the lake was ultra-oligotrophic in both the spring and the summer. The lake continued to be oligotrophic in the spring of 2008 but was found to be mesotrophic in the summer. This is a sudden change and needs careful comparing with the nutrient results. Spring TP was low (6.55 μg l−1) in 2003 but increased slightly (7.82 μg l−1) in 2008. Other nutrients such as NO3 + NO2 and SiO2 continued to show increasing trends (Table 5; Dove, 2009). Although the long term trophic state assessment suggests changes in the prevailing general conditions, these data should be used and interpreted carefully due to the long time gaps (currently 5 years) between surveys during which nutrient-plankton dynamics may differ. One thing that is apparent is that the ecology of Lake Ontario has been undergoing alterations due to anthropogenic stressors. The lake has experienced rapid transition from eutrophy to oligotrophy and in 2008, mesotrophy. The next CSMI sampling (2013) will be critical for assessing the foodweb dynamics and ecological and trophic status of the lake however the 5 year interval is bound to miss rapid ecological changes. More frequent sampling is needed to capture the holistic changes occurring in Lake Ontario.

Recommendations

Our study of the phytoplankton community of Lake Ontario during 2008 was designed to be compatible with historic work and make optimum use of existing surveillance programs. However, this approach has also served to highlight some of the major research gaps. We recommend more intensive and frequent research and monitoring. The temporal (diurnal, seasonal, annual) and spatial (horizontal and vertical) variability of phytoplankton communities needs to be assessed and accounted for in future monitoring efforts. It follows that increased sampling efforts will be in vain if we–the Great Lakes research community–do not improve our collective taxonomic skill set. A major capacity building effort to expand the pool of taxonomists is therefore required. These recommendations are not unique to Lake Ontario or the Laurentian Great Lakes and will hopefully foster a better understanding of foodweb dynamics in all aquatic ecosystems.

Conclusions

The phytoplankton community of Lake Ontario was studied extensively during research cruises conducted in April, July and September of 2008. Phytoplankton biomass was relatively high on average (1.6–3.0 g m−3) and very diverse with 200–300 species identified in each cruise. Importantly, rare and less common species, collectively accounted for ≈60–80% of the total biomass. These results demonstrate the need for good taxonomy and show that counting strategies which rely on identifying only common species are likely to be misleading. Equally important is the need to standardize identification and enumeration techniques to generate consistent and reliable data. Furthermore, the size distribution data revealed that one tiny picoplankton species, Chroococcus dispersus var. minor, which seldom accounted for more than 1% of the total biomass, was responsible for ≈30–50% of the primary productivity and therefore has a major impact on autocthonous production. Long term comparisons show considerable variability in phytoplankton biomass and composition between 1970 (pre P abatement) and 2008. The previous lakewide research effort in 2003, following P abatement in the 1970s and the invasion of dreissenid mussels in the 1990s, revealed an ultra-oligotrophic phytoplankton community. Phytoplankton biomass was so low (0.2 g m−3) that concerns were raised about the health and sustainability of the fisheries. In the summer of 2008, however, the lake appeared to be mesotrophic based on its elevated phytoplankton biomass. It does not appear that increases in phosphorus loads are driving this change. Lake Ontario appears to be in continuous state of changing trophic conditions. More frequent and extensive research is needed into the factors regulating the phytoplankton community in order to provide a better understanding of foodweb dynamics. Such assessments will not be possible without a substantial research and training effort directed at improving the collective understanding of phytoplankton taxonomy.

Acknowledgements

The authors thank the crew and technical staff of the CCGS Limnos and the R/V Lake Guardian for assistance with sample collection. We also thank D. Kane (Defiance College), J. Leach (Ontario Ministry of Natural Resources) and E. Mills (Cornell University) for providing constructive reviews. Finally, we thank S. Blunt and R. Rozon (AEHMS) for assisting with the technical editing.

Supplemental Material

Supplemental data for this article can be accessed on the publisher's website.

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Supplementary data