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JOURNAL OF PLANKTON RESEARCH j VOLUME 31 j NUMBER 5 j PAGES 489 – 502 j 2009 Warm spring and summer water temperatures in small eutrophic lakes of the Canadian prairies: potential implications for phytoplankton and zooplankton ALAIN P. DUPUIS*† AND BRENDA J. HANN DEPARTMENT OF BIOLOGICAL SCIENCES, UNIVERSITY OF MANITOBA, Z320 DUFF ROBLIN BLDG, WINNIPEG, MB, CANADA R3T † PRESENT ADDRESS: FISHERIES AND OCEANS CANADA, FRESHWATER INSTITUTE, 2N2 501 UNIVERSITY CRESCENT, WINNIPEG, MB, CANADA R3T 2N6 *CORRESPONDING AUTHOR: [email protected] Received February 11, 2008; accepted in principle December 15, 2008; accepted for publication January 1, 2009; published online 24 January, 2009 Corresponding editor: Mark J. Gibbons Shallow, polymictic lakes with low heat storage capacity are especially susceptible to warmer spring conditions, predicted for a changing climate. In these lakes, atmosphere to water mass heat transfer is efficient as a result of high wind exposures and large surface areas relative to volumes. We examined effects of warmer water temperatures on phytoplankton and zooplankton abundance and species composition in three small eutrophic lakes (5.2 – 14.9 ha) of the Canadian prairies in Winnipeg, Manitoba, Canada, over two open-water seasons with contrasting spring weather conditions, i.e. 2005-a “normal” spring and 2006-a warm spring. Warmer spring and summer water temperatures were associated with decreased water transparency, increased phytoplankton biomass, increased relative filamentous cyanobacteria biomass and shifts in dominant genera from Aphanizomenon to Anabaena and Planktothrix. Zooplankton responded strongly; abundance of Daphnia (D. pulicaria, D. ambigua and D. parvula) decreased while rotifers, Skistodiaptomus oregonensis and Bosmina longirostris increased in abundance. Of several factors influencing phytoplankton dynamics, total dissolved nutrients [nitrogen (N), phosphorus (P) and N:P] and water column stability did not show important changes between years. In contrast, water temperature [described as the metric degree-days (8C day)] was related to changes in phytoplankton and % cyanobacteria biovolume. Daphniid abundance showed a significant negative relationship with an increase in filamentous cyanobacteria biomass and, thus we suggest, was indirectly associated with increased water temperatures. I N T RO D U C T I O N Warming air temperatures and changing climatic conditions have been linked to plankton population variability in both marine (Edwards and Richardson, 2004) and freshwater (George and Taylor, 1995; Straile, 2000; Winder and Schindler, 2004) ecosystems. Small shallow lakes, in contrast to deep water-bodies, are especially susceptible to warmer air temperatures (Adrian et al., 1999; Gerten and Adrian, 2000). The seasonal period at which changes occur may affect the magnitude of impact on freshwater food webs. During spring, lakes with small volume to surface area ratios efficiently transfer heat across the atmosphere – water interface leading to water temperatures closely matching those of ambient air (Carpenter et al., 1992). Downing et al. (Downing et al., 2006) showed that small water-bodies doi:10.1093/plankt/fbp001, available online at www.plankt.oxfordjournals.org # The Author 2009. Published by Oxford University Press. All rights reserved. For permissions, please email: [email protected] JOURNAL OF PLANKTON RESEARCH j 31 VOLUME (,1 km2) predominate by surface area in a recent survey of the world’s lakes and this may suggest that a changing climate would have broad-ranging consequences for freshwater systems. Long-term studies on shallow eutrophic lakes have shown correlations between spring water temperatures and the dynamics of phytoplankton and zooplankton (Adrian et al., 1999; Gerten and Adrian, 2000; Benndorf et al., 2001). For example, in Müggelsee, Germany, a shallow eutrophic lake, warmer water temperatures in late April and early May caused an earlier onset of the spring daphniid peak and the clear-water phase (Gerten and Adrian, 2000). Further, George and Hewitt (George and Hewitt, 2006) demonstrated that interannual variations in temperature and wind speed not only correlated with daphniid abundance but also with an increased abundance of filamentous cyanobacteria. Increased water temperatures have led to longer periods of dominance of cyanobacteria in some eutrophic lakes; hence, further research is needed to elucidate what impact this might have on zooplankton populations, particularly at the species level (Adrian and Deneke, 1996). Few studies have investigated impacts of warming on small grazers such as rotifers that may be important food-web components in years when larger daphniids are lacking (Tirok and Gaedke, 2006). This study examines the implications of a warm spring and summer on plankton dynamics in three small eutrophic lakes in the Canadian prairies (the Fort Whyte lakes in Winnipeg, Manitoba, Canada). An increase in cyanobacteria biomass and a decline in large herbivorous zooplankton coincided with warmer spring temperatures in 2006 (+2.98C above the 30-year average) relative to that experienced in 2005 (+0.98C above the 30-year average). With conditions of warmer water temperatures we expected an increase in phytoplankton and zooplankton biomass however, alternative dynamics were possible. Other factors associated with cyanobacterial prevalence include high nitrogen (N) and phosphorus (P) concentrations (Downing et al., 2001), low N:P ratios (Schindler, 1977; Smith, 1983) and high water column stability (Reynolds and Walsby, 1975) and may be more important than the influence of relatively small increases in water temperatures (+28C). For large herbivorous zooplankton, warmer water temperatures could alter the importance of bottom-up (food quality) and/or top-down (planktivory) mechanisms. Our approach was to use commonly collected limnological variables (temperature profiles, nitrogen and phosphorus concentrations and plankton) sampled at a high frequency over both a cooler (2005) and a warmer (2006) open-water season to examine potential implications for phytoplankton and zooplankton dynamics. Using our data, we addressed the following objectives. (i) To identify j NUMBER j 5 PAGES 489 – 502 j 2009 and contrast changes in the plankton community between a cooler and a warmer thermal regime. (ii) To present potential explanations for the documented changes. METHOD Study site The Fort Whyte lakes (498 49.0200 N, 978 13.4400 W) situated in Winnipeg, Manitoba, Canada are a set of five man-made lakes, constructed at 20-year intervals starting in 1920 (Loadman, 1980). Inflows to the lakes are restricted to spring runoff draining from adjacent agricultural fields, mixed-grass bison pasture, deciduous forest and urban developments. They are presently used as an environmental education centre (www.fortwhyte. org) and receive nutrient inputs from the on-site primary treatment lagoon and from migrating Canada geese in the fall. For the purpose of this study, Lakes 2, 3 and 4 were selected as suitable models for small eutrophic lakes representative of many prairie waterbodies such as small lakes, large ponds, impoundments and dugouts. These lakes have small surface areas (5.2– 14.9 ha), intermediate mean depths (4.5– 5.0 m) and a gradient in nutrient concentrations, although they are interconnected via narrow channels (Table I). Spring conditions (April and May) in 2006 were 2.98C warmer compared to average conditions from 1971 to 2000 (Environment Canada, 2004). While ice-off occurred on April 14 in both 2005 and 2006, air Table I: Morphological and chemical characteristics of the Fort Whyte lakes, Winnipeg, Manitoba, Canada Parameter Lake 2 Lake 3 Morphometry Surface area 5.18 9.38 (ha) 23.45 43.47 Total volume (104 m3) Mean depth (m) 4.5 4.6 Maximum 8.4 7.5 depth (m) Chemistry 30.87 (22.39) 54.32 Chlorophyll a (+SD) (mg L21) Total nitrogen 95.44 (23.35) 142.50 (+SD) (mM) Total 3.70 (1.57) 5.64 phosphorus (+SD) (mM) Alkalinity (+SD) 4768.75 (171.67) 4393.75 (meq L21) Lake 4 14.91 74.14 5.0 8.3 (39.47) 84.88 (50.79) (54.52) 171.31 (52.14) (2.70) 6.97 (2.74) (226.96) 4488.75 (185.51) Chemistry data reported as mean (+SD) May–August values for 2005 – 06. 490 A. P. DUPUIS AND B. J. HANN j WARM TEMPERATURES AND PLANKTON DYNAMICS temperatures in April and May remained on average 28C higher in 2006 compared to 2005. As a result, spring and summer thermal profiles were altered substantially (Fig. 1). Across Lakes 2, 3 and 4, mean May temperatures of the epilimnion increased from 10.3 to 11.48C in 2005 compared with 13.1 to 13.88C in 2006, an average increase of 2.58C (Fig. 1). Summer (June– August) water temperatures also increased in Lakes 2, 3 and 4 in 2006 increasing from a mean epilimnetic temperature of 20.28C in 2005 compared with 21.4– 21.88C in 2006. Data collection All three lakes were sampled weekly in 2005 and twice weekly in 2006, weather permitting, at the deepest point of each lake. On each sampling date, water transparencies were measured with a Secchi disc and temperature profiles were collected at 1-m intervals with an YSI multi-probe meter (Model 55). Water chemistry samples were taken from just below the surface and analysed for total dissolved nitrogen and total dissolved phosphorus (TDN and TDP), total nitrogen and total Fig. 1. Contour plots of temperature profiles (8C) from May to August at the Fort Whyte lakes 2 (A and B), 3 (C and D) and 4 (E and F) during the years 2005 and 2006. 491 JOURNAL OF PLANKTON RESEARCH j phosphorus (TN and TP) as well as chlorophyll a (chl a). Analyses were completed in the water analysis lab at the Freshwater Institute, Department of Fisheries and Ocean in Winnipeg, MB using standard methods (Stainton et al., 1977). Phytoplankton samples were collected just below the surface using glass scintillation vials (20 mL) and were preserved with Lugol’s solution and stored in the dark. In 2006, an integrated epilimnetic phytoplankton sample was also collected by combining water samples taken at 1-m intervals throughout the epilimnion for comparison with the subsurface samples. Our analysis showed that, on average, the estimation of the phytoplankton biomass in subsurface samples was within 13% of that estimated for the integrated epilimnion samples. To maintain consistent methods between years, only the subsurface samples were further analysed. On each sampling date, integrated zooplankton samples were taken through the epilimnion to the surface using a 25 cm diameter Wisconsin zooplankton net with a 73 mm mesh size at similar periods during the day, i.e. between 9:00 and 11:00 am. A 73 mm mesh size was used in an effort to maximize net efficiency (to prevent clogging under conditions of high algal biomass) and minimize loss of small zooplankton passing through the net. As a result, the abundance of small rotifers (,73 mm) was likely underestimated. Zooplankton samples were preserved with 95% ethanol. In our study, we define the epilimnion as the upper layer with ,18C difference per meter. A change of .18C per meter was defined as the thermocline and the hypolimnion is the layer from the thermocline to the bottom. When the water-column was isothermal, a 3-m integrated depth was sampled. Data processing Two water-column stability estimates were calculated for each sampling date in 2005 and 2006, the Schmidt stability index (S) and the density gradient between the epilimnion and the hypolimnion. This was estimated to test the possibility that changes in water-column stability were related to the observed dynamics in cyanobacteria biomass. S (g cm21) describes the amount of work required to mix the entire water column to a uniform density (Robertson and Imberger, 1994). S ¼ A1 o X ðz zÞðrz r ÞAz Dz r ¼ V1 X 31 VOLUME ðVz rz Þ where Az is the lake area (m2) and rz is the density (g cm23), both at depth z (m). z* represents the depth j NUMBER 5 j PAGES 489 – 502 j 2009 where the mean density is found, and r* is that density. V represents volume (m3). One-meter depth intervals (Dz) were used for the calculations. The second measure of water-column stability was determined by calculating the difference in mean density between the epilimnion and the hypolimnion. This was calculated to determine the possibility of mixing between the layers. Water density values were based on theoretical relationships between water temperature (8C) and density of water (g mL21). A measure of cumulative daily temperatures, degreedays (DD, 8C day) was estimated for each day during the open-water season (May – August) above a given threshold temperature (TTh) (Neuheimer and Taggart, 2007). Within an appropriate physiological range, ectotherm growth and development are temperaturedependent. Therefore, degree-days can be used to relate temperature to organism developmental time. Degree-days are calculated using the formula: DDðnÞ ¼ X ðTi TTh Þ†Dd; Ti TTh Relevant threshold temperature (TTh) is given as 48C, found during isothermal conditions following ice-off. Ti is the mean daily temperature and Dd is a day. Average daily epilimnetic water temperatures were estimated based on linear interpolations of local air temperatures on measured water temperatures for each lake. A dynamic linear model was used to estimate daily epilimnetic temperatures (Kjellman et al., 2003): WTt ¼ a þ WTt1 þ b ðATt1 WTt1 Þ Daily water temperatures (WTt) were estimated based on air temperatures (ATt) recorded at time t from a nearby Environment Canada weather station (Richardson International Airport, 498 55.2000 N, 978 13.8000 W). The minimum sum of squares between measured and estimated water temperature were used to estimate parameters a and b. Linear regressions were performed relating predicted values to observed values to determine the suitability of the model in estimating daily epilimnetic temperatures. As a result, the dynamic model gave reasonably good estimates of daily epilimnetic temperatures (linear regressions: Lake 2, observed ¼ (22.532 1027) +1.000(predicted), F1,43 ¼ 55.757, P , 0.001, r 2 ¼ 0.565; Lake 3, observed=(22.162 1027) + 1.000(predicted), F1,43 ¼ 38.523, P , 0.001, r 2 ¼ 0.571; Lake 4, observed ¼ (22.057 1028) + 1.000(predicted), F1,43 ¼ 77.949, P , 0.001, r 2 ¼ 0.644). Zooplankton were identified to species using taxonomic keys developed for Daphnia (Hebert, 1995) and 492 A. P. DUPUIS AND B. J. HANN j WARM TEMPERATURES AND PLANKTON DYNAMICS for other cladocerans and copepods (Pennak, 1989). Rotifers were counted only as a group; however, dominant species were identified (Chengalath et al., 1971). For zooplankton, a minimum of 100 animals per subsample were counted. Phytoplankton were classified by cell size based on longest linear dimensions. Filamentous cyanobacteria were identified to genus (Findlay and Kling, 1979). Phytoplankton cell counts were made using the Utermöhl inverted-microscope technique. For phytoplankton, a single subsample was counted. Biovolumes were estimated by approximating cell dimensions to nearest geometrical shapes (Rott, 1981). Data analysis Statistical analyses are separated into two parts: (i) assessment of possible factors driving a shift towards cyanobacteria dominance, and (ii) the effects of temperature on plankton abundance and composition. In the first part, univariate paired t-tests were used to test whether monthly means (May – August) of water column stabilities, nutrient concentration (both TDN and TDP) and TDN:TDP ratios differed between 2005 and 2006. Dissolved forms of N and P were selected for analysis because they were assumed to be more readily available for assimilation over the short-term (within a month) in comparison to suspended forms. The second part of the analysis investigated the relationships between water temperature and plankton abundance and composition using the metric, degreedays (DD, 8C day). Degree-day was related to phytoplankton biovolume estimates, to relative cyanobacteria biovolume estimates and to daphniid abundance. These relationships were examined by dividing the field season into monthly intervals (May, June, July and August). Lake-years were used as independent data points for the analysis (3 lakes 2 years ¼ 6 data points). Mean monthly values of biological parameters were regressed by monthly degree-day values. In addition, simple linear regressions were used to investigate effects of water temperature on daphniid abundance by relating a measure of food quality, % cyanobacteria, to daphniid abundance. Unfortunately, the absence of planktivorous fish data prevented us from investigating possible relationships with zooplankton abundances. Normality and homogeneity of residuals were verified using a Shapiro – Wilk’s test for normality and visual checks of residuals by predicted values plots for homogeneity. Chlorophyll a and total phytoplankton biovolume were log-transformed to normalize and homogenize residuals. All statistical tests were performed in SAS 9.1.2. R E S U LT S Phytoplankton and zooplankton dynamics Phytoplankton abundance and species composition changed markedly between 2005 and 2006. Both measures of phytoplankton biomass, chlorophyll a (mg L21) and biovolume estimates (mm3 L21), indicate large increases in 2006. In the present study, only biovolume estimates were analysed in further detail as log(chl a) and log(biovolume) estimates were strongly correlated (Pearson: Lake 2, n ¼ 15, r ¼ 0.700, P ¼ 0.004; Lake 3, n ¼ 8, r ¼ 0.809, P ¼ 0.015; Lake 4, n ¼ 15, r ¼ 0.693, P ¼ 0.004). Across Lakes 2, 3 and 4, May– August mean phytoplankton biovolume estimates ranged from 1.7 to 3.1 mm3 L21 in 2005 compared with 4.3 to 7.3 mm3 L21 in 2006 (Fig. 2). As a result, water transparency measured by Secchi disc declined substantially from 2.9– 2.2 m to 0.6– 0.3 m between 2005 and 2006 (Fig. 2). Total phytoplankton biomass was negatively correlated with Secchi depth (Pearson: Lake 2, n ¼ 22, r ¼ 20.622, P ¼ 0.002; Lake 3, n ¼ 19, r ¼ 20.482, P ¼ 0.037; Lake 4, n ¼ 15, r ¼ 20.770, P , 0.001). Relative biomass of filamentous cyanobacteria increased substantially from maximum open-water values of 28.2, 46.7 and 90.9% in 2005, increasing to 77.7, 90.1, 95.0% in 2006, for Lakes 2, 3 and 4, respectively (Fig. 2). In addition, phytoplankton succession progressed earlier in 2006. By mid-May in 2006, cyanobacteria already represented 11–15% of the total phytoplankton biomass. In comparison, in 2005, cyanobacteria accounted for only 0.2–3% of the mid-May phytoplankton biomass (Fig. 2). Dominant cyanobacteria taxa shifted from Aphanizomenon spp. in 2005 to Anabaena spp. and Planktothrix spp. in 2006, particularly from June to August (Fig. 3). Between 2005 and 2006, the relative importance of other phytoplankton (omitting filamentous cyanobacteria) based on our size classification did not change significantly (paired t-tests, P . 0.2). Major changes were observed in zooplankton communities between years. Across Lakes 2, 3 and 4, mean May – August daphniid abundance decreased from 10.6 – 20.3 ind. L21 in 2005 to 0.5– 7.3 ind. L21 in 2006 (Fig. 4A – F). In 2005, Daphnia pulicaria and D. ambigua dominated while D. parvula were observed nearly exclusively in 2006. Mean May – August rotifer (.73 mm in size) abundance increased to very high values in all lakes ranging from 62.3 to 474.8 ind. L21 in 2005 compared with 3693.0 to 4112.5 ind. L21 in 2006 (Fig. 4). Populations that also increased between 2005 and 2006 are the calanoid copepod Skistodiaptomus oregonensis (7.9 – 12.7 to 15.5– 41.7 ind. L21) and the small cladoceran Bosmina longirostris (0 – 1.2 to 6.5– 21.0 493 JOURNAL OF PLANKTON RESEARCH j 31 VOLUME j NUMBER 5 j PAGES 489 – 502 j 2009 Fig. 2. Two-year (2005 and 2006) comparison of phytoplankton biovolume estimates (mm3 L21) and water transparency indicated in Secchi depth (vertical bars, m) from May to August in Lakes 2, 3 and 4. Phytoplankton are classified by cell size except for filamentous cyanobacteria. ind. L21) (Fig. 4). Cyclopoid copepods, dominated by Diacyclops thomasi showed inconsistent changes between years with a spring peak in 2005 but not in 2006 except for Lake 4 (data not shown). Also, zooplankton predators, instars III and IV of Chaoborus flavicans, peaked in summer except for Lake 2 in 2006. A single winter sample taken February 15 in 2006, along with sampling conducted continuously from 1977 to 1978 (Loadman, 1980), suggested that no cladocerans over-winter as adults during the ice-covered conditions (data not shown). Relationships between water temperature and phytoplankton Response of plankton abundance and composition to changes in water temperature, observed from 2005 to 2006, was investigated using simple linear regression models with degree-days as an explanatory variable. Significant relationships were found between water temperature and total phytoplankton biomass during May and June, prior to cyanobacteria dominance (Fig. 5A and B). Degree-days (8C day) explained 72 and 88% of the variability in total biovolume for the months of May and June (Fig. 5A and B). July water temperatures were also significantly related to total phytoplankton biomass; however, this was primarily driven by increasing prevalence of cyanobacteria. Warmer water temperatures in 2006, indicated by degree-days, were associated with greater relative cyanobacteria biomass in all lakes compared to 2005 (Fig. 5C and D). Relative cyanobacteria biomass increased quickly with degree-days, increasing by 36 and 26% in July and August, respectively, for each 100 degree-days (Fig. 5C and D). Degree-day explains 96 and 75% of the variation in % cyanobacteria in July and August. 494 A. P. DUPUIS AND B. J. HANN j WARM TEMPERATURES AND PLANKTON DYNAMICS Fig. 3. Two-year (2005 and 2006) comparison of relative abundances of dominant filamentous cyanobacteria genus, i.e. representing .95% of total biomass, (Aphanizomenon spp., Planktothrix spp., Anabaena spp. and Limnothrix sp.) from biovolume estimates from May to August in Lakes 2, 3 and 4. A star indicates no filamentous cyanobacteria in sample. Alternative factors regulating cyanobacteria Univariate paired t-tests were conducted to test for difference in nutrient concentrations and water-column stability between 2005 and 2006. Mean monthly nutrient concentrations were not significantly different between years in the Fort Whyte lakes (Fig. 6D– I and Table II). Thus, from 2005 to 2006, no important influx of nutrients occurred that was common to all three lakes at the same time. Several authors have associated low N to P ratios with cyanobacteria dominance (Schindler, 1977; Smith, 1983). Between years, only July and August showed significant differences in TDN:TDP (Fig. 6J – L and Table II). Similarly, high water-column stability can potentially favour dominance of buoyancy-controlling cyanobacteria (Reynolds and Walsby, 1975). Schmidt stability index (S, g cm21) did not significantly vary between 2005 and 2006 (Fig. 6A– C and Table II). We also calculated the density gradient between the epilimnion and the hypolimnion in both years. In July and August, the density gradient was significantly greater in 2006 compared to 2005 (Table II). Relationships between water temperature and daphniids Monthly linear regressions between degree-days and daphniid abundance were not significant (P . 0.05). However, negative relationships between relative cyanobacteria biomass and daphniid abundance were significant for June and July (Fig. 7). In 2006, lower daphniid abundance was associated with higher filamentous cyanobacteria biomass compared to 2005. Percent 495 JOURNAL OF PLANKTON RESEARCH j 31 VOLUME j NUMBER 5 j PAGES 489 – 502 j 2009 Fig. 4. Two-year (2005 and 2006) comparison of mean Daphnia spp. (ind. L21), Skistodiaptomus oregonensis (ind. L21), Bosmina longirostris (ind. L21) and rotifer (103 ind. L21) population dynamics from May to August in Lakes 2, 3 and 4. Note the y-axis break for Lake 2 zooplankton (A and B). cyanobacteria explained most of the variation in daphniid abundance in both June (r 2 ¼ 0.66) and July (r 2 ¼ 0.71). DISCUSSION In the Fort Whyte lakes, changes in phytoplankton and zooplankton population dynamics could have resulted from a number of possible direct and indirect effects. Some of the proposed factors explaining large increases in cyanobacteria could be related to increased water temperatures (Robarts and Zohary, 1987), grazing of small phytoplankton species by herbivorous zooplankton (Lampert et al., 1986), increased nutrient concentrations (Downing et al., 2001), decreased nitrogen to phosphorus ratios (Schindler, 1977; Smith, 1983) and disruption of water-column stability (Reynolds and Walsby, 1975). In addition, possible factors influencing a decline in Daphnia and an increase in S. oregonensis, B. longirostris and rotifers also include increased water temperature, degrading food quality (e.g. increasing prevalence of cyanobacteria), changes in planktivory pressures and changes in vertical distribution. Although many other mechanisms are possible and complex interactions are likely, we focus our presentation on parameters that were measured using basic limnological sampling methods (e.g. thermal profiles, Secchi transparency, zooplankton and phytoplankton abundance). A full analysis of factors explaining patterns in planktonic succession and their relative importance has been more thoroughly discussed in Sommer et al. (Sommer et al., 1986) and Sommer (Sommer, 1989). In this study, it remains impossible to isolate any given factor; however, we believe there is enough evidence to discuss 496 A. P. DUPUIS AND B. J. HANN j WARM TEMPERATURES AND PLANKTON DYNAMICS Fig. 5. Monthly relationships between degree-days (8C day) and phytoplankton biomass estimated as biovolume (mm3 m23) for May (A) and June (B). (C) and (D) describe the monthly relationships between degree-days (8C day) and % filamentous cyanobacteria for July (C) and August (D). In all figures, the dashed lines represent the 95% confidence interval. the potential influence of some of the factors that were monitored in this study. Water temperature and phytoplankton Water temperature is an important factor regulating phytoplankton physiological rates (Rhee and Gotham, 1981). In 2006, a warm spring and summer in the Fort Whyte lakes was correlated with increased total phytoplankton and relative cyanobacteria biomass. This is consistent with long-term (.30 years) patterns observed in several North American and European lakes where a warming climate has been linked to earlier phytoplankton blooms (Weyhenmeyer et al., 1999; Gerten and Adrian, 2000; Winder and Schindler, 2004), increased total biomass (Schindler et al., 1990) and, in eutrophic lakes, dominance of cyanobacteria (Adrian and Deneke, 1996). In nutrient-rich systems, empirical and experimental results suggest that increasing water temperatures are directly linked to changes in phytoplankton species composition, showing an increasing proportion of cyanobacteria taxa (Zhang and Prepas, 1996; De Senerpont Domis et al., 2007). In fact, in some years, warming temperatures have led to year-round cyanobacteria dominance (Adrian and Deneke, 1996). In the Fort Whyte lakes, higher temperatures in June – August were also associated with shifts in the dominant cyanobacteria taxa, from Aphanizomenon in 2005 to Anabaena and Planktothrix in 2006. This may be attributed to differences in competitive abilities among species under different environmental conditions. We suggest that direct effects of increased temperature did not drive a taxonomic shift as A. flos-aquae growth rates are greater than those of P. agardhii and P. redekei over a range of temperatures (6 – 158C) without light limitation (Gibson, 1985). Instead, decreased water transparency associated with greater phytoplankton biomass and elevated water temperatures in 2006 may have facilitated dominance of Planktothrix over Aphanizomenon. Under conditions of lowered light intensities, several laboratory experiments suggested greater photosynthetic efficiency and growth rates in P. agardhii relative to A. flos-aquae (Foy et al., 1976; Foy and Gibson, 1982) resulting in superiority of the former in low-light environments. Importantly, these shifts in cyanobacteria species could have negative implications especially when replacement taxa produce toxins and/or are of poorer nutritional quality for zooplankton. Alternative factors driving cyanobacteria dominance In the literature, increased nutrient loading and lowered N:P ratios are often identified as the most important 497 JOURNAL OF PLANKTON RESEARCH j 31 VOLUME j NUMBER 5 j PAGES 489 – 502 j 2009 Fig. 6. Two-year comparison (2005 and 2006) of physical and chemical dynamics from May to August in Lakes 2, 3 and 4. reason for increased cyanobacteria biomass (Downing et al., 2001; Schindler et al., 2008). Between 2005 and 2006, we found no evidence that nitrogen or phosphorus concentrations differed and only in late summer did we find significant difference in TDN:TDP ratios. In this study, we do not believe that cyanobacteria dynamics were related to TDN:TDP ratios as we observed higher ratios in 2006 occurring after the major changes in the phytoplankton community. Another factor influencing the prevalence of cyanobacteria is water-column stability. Gas-vacuolation produced by some cyanobacteria could allow a competitive advantage over other non-buoyant phytoplankton under conditions of low mixing intensity (Reynolds and Walsby, 1975; Visser et al., 1996). Overall water column stabilities in the Fort Whyte lakes, measured by the Schmidt stability index, did not change significantly between years. In contrast, when comparing density differences between epilimnetic and hypolimnetic water volumes, density gradients were significantly greater in July and August of 2006 compared to 2005. This may suggest a partial explanation for greater cyanobacteria biomass in 2006; however, important increases in cyanobacteria prevalence began prior to July in 2006 and we did not observe changes in gas vacuolation in cyanobacteria between years. An alternative explanation to consider is the potential for zooplankton to control cyanobacteria biomass. In the Fort Whyte lakes, it is also possible that grazing pressures from large herbivorous zooplankton (i.e. Daphnia) was stronger in 2005 leading to lower overall biomass of total phytoplankton and cyanobacteria biomass. This would then suggest that high cyanobacteria biomass in 2006 was an effect rather than a cause 498 A. P. DUPUIS AND B. J. HANN j WARM TEMPERATURES AND PLANKTON DYNAMICS of low Daphnia abundance. Some experiments have shown that even cyanobacterial filaments can be grazed by large Daphnia (Epp, 1996). Water temperature and shifts in zooplankton community Warmer water temperatures in the Fort Whyte lakes in 2006 did not lead to paralleled increase between Table II: Results of univariate paired t-test testing for differences between 2005 and 2006 monthly means for chemistry parameters (TDN, TDP and TDN:TDP) and water column stability estimates (Schmidt stability index and density gradient between epilimnion and hypolimnion), n ¼ 3 Month Variable T P May TDN TDP TDN:TDP Schmidt index Epi.-Hypo. density TDN TDP TDN:TDP Schmidt index Epi.-Hypo. density TDN TDP TDN:TDP Schmidt index Epi.-Hypo. density TDN TDP TDN:TDP Schmidt index Epi.-Hypo. density 2.25 0.90 20.12 20.23 22.45 2.09 4.06 20.70 22.87 23.39 20.34 1.84 212.70 0.12 25.80 1.08 2.25 212.13 20.37 26.02 0.15 0.46 0.92 0.84 0.13 0.17 0.056 0.56 0.10 0.08 0.77 0.21 0.006 0.92 0.03 0.39 0.15 0.007 0.74 0.03 June July August gradient gradient gradient gradient Significant results (P , 0.05) are indicated in bold. phytoplankton biomass and daphniid abundance. Relationships between water temperature and daphniid abundance were not significant. This is contrary to some studies linking climate warming to changes in plankton seasonal dynamics and abundance. In European lakes, warming temperatures coincident with the North Atlantic oscillation (NAO) were associated with an earlier peak of both phytoplankton and Daphnia (Straile, 2002). In some cases, higher water temperatures were also linked to higher daphniid biomass (Straile, 2000). Long-term studies of climate-related impacts on plankton show a trend towards smaller zooplankton species. In Heiligensee, Germany, a warming temperature trend was associated with a shift from D. galeata to the smaller D. cucullata (Adrian and Deneke, 1996). Similarly, in the Fort Whyte lakes, increased water temperatures in 2006 were associated with small-bodied D. parvula (adult size 1.0 mm) compared to high abundances of large-bodied D. pulicaria (adult size 2.2 mm) and small-bodied D. ambigua (adult size 1.0 mm) in 2005. Concurrently in the Fort Whyte lakes, other small zooplankton such as rotifers (albeit, species ,73 mm are probably underestimated) and B. longirostris increased to high densities in 2006. There have been several examples of highly eutrophic lakes associated with small size spectra in zooplankton community structure (Gliwicz, 1977; Finlay et al., 2007). Our study further suggests that warming temperatures could promote shifts in zooplankton size spectra in moderately eutrophic lakes such as the Fort Whyte lakes. This supports the arguments that climate change effects will probably resemble symptoms of eutrophication in shallow lakes (Mooij et al., 2005). While increasing water temperatures may enhance bottom-up and top-down factors in affecting the zooplankton community, we are unable to provide direct Fig. 7. Monthly relationships between % filamentous cyanobacteria and daphniid abundance (ind. L21) for June (A) and July (B) with the 95% confidence interval (dashed lines). 499 JOURNAL OF PLANKTON RESEARCH j 31 VOLUME support for either mechanism. In the Fort Whyte lakes, daphniid food quality in 2006, expressed as % filamentous cyanobacteria, deteriorated with increasing temperatures and was negatively related to daphniid abundance for the months of June and July. In accordance with this relationship, several authors have suggested that the presence of filamentous cyanobacteria is generally associated with smaller species of daphniid, i.e. ,1 mm body length (DeMott et al., 2001; Ghadouani et al., 2003). Laboratory experiments have shown that larger-sized daphniids are more negatively affected by the presence of cyanobacterial filaments than smaller-sized ones causing interference with feeding appendages, high rejection rates, lowered filtering rates and decreased reproduction (Gliwicz, 1977; Fulton and Paerl, 1987; Gliwicz, 1990). Furthermore, recent studies have shown that changes in water viscosity, as a result of changing water temperature, can negatively affect daphniid feeding efficiency (Abrusán, 2004; Bednarska and Dawidowicz, 2007). For D. pulicaria, decreasing water viscosity with increasing water temperatures may allow greater water flow through intersetular gaps of feeding appendages and thus, increase the potential for clogging in the presence of filaments (Abrusán, 2004). Our study, however, does not rule out the alternative that increasing water temperatures resulted in increased planktivory. In spring, warming water temperatures are directly related to larval fish growth to sizes capable of feeding on large cladocerans and increasing predation rate of adult planktivorous fish (Mehner, 2000; Hansson et al., 2007). Also, feeding behaviour measured by attack rate and swimming speed is positively related to water temperature in some zooplanktivorous fishes (e.g. juvenile brook trout, Salvelinus fontinalis; Marchand et al., 2002). Such studies suggest that warming water temperatures can increase the magnitude of and advance the onset of planktivory by fish resulting in more intense size-selective predation (Brooks and Dodson, 1965) and declines in the abundance of large herbivorous zooplankton. These studies raise the possibility that warmer conditions in the Fort Whyte lakes in 2006 resulted in positive changes in zooplanktivory and caused a restrained response in the spring development of a population of large zooplankton grazers. Fish populations were not monitored during our study; therefore, we cannot make clear conclusions about the impact of planktivory. Invertebrate planktivory can also impart important top-down pressures on the zooplankton community. In Bautzen Reservoir, Germany, Wagner and Benndorf (Wagner and Benndorf, 2007) demonstrated that warmer spring temperatures were related to an earlier j NUMBER 5 j PAGES 489 – 502 j 2009 onset of both young-of-the-year percid and Leptodora kindtii predation on D. galeata. In another study, fishless enclosures with Chaoborus resulted in decreased abundance of small-sized (Bosmina and rotifers) and mediumsized (Ceriodaphnia) zooplankton species (Lynch, 1979). In contrast, Lynch (Lynch, 1979) showed that the presence of planktivorous fishes was associated with a decreased abundance of the midge larvae. In Fort Whyte lakes, a qualitative measure of Chaoborus flavicans (daytime sampling and relatively small diameter net) did not show changes in density of predatory instars III and IV between 2005 and 2006 (data not shown). However, without more data, we cannot exclude the alternative explanation that changes in Chaoborus abundance were related to inter-annual changes in zooplankton abundance and species composition. Further studies on the potential impacts of climate change on plankton dynamics will be needed to isolate the relative impacts of bottom-up and top-down factors in the regulation of zooplankton population and community composition. It is also possible that the changes in zooplankton community structure observed between years are related to altered vertical migration behaviour. In zooplankton, diel vertical migration has been shown to be related to fish planktivory and light transparency (Lampert, 1993), factors that could potentially be affected by warming temperatures (De Stasio et al., 1996). In our study, zooplankton were only sampled within the epilimnion. As a result, there is a possibility that some zooplankton were not sampled if daytime habitat was deeper in 2006 compared to 2005. However, we believe that the changes between years are so strong that they are unlikely to be an artefact of the sampling procedures. In other words, we believe the patterns are valid, but that the true whole water-column abundance of zooplankton may have been underestimated in both years. In summary, the present study suggests that a warmer spring and summer could potentially trigger some important changes in plankton population dynamics in small eutrophic lakes. In the Fort Whyte lakes, warming temperatures were related to substantial increases in total phytoplankton biomass and relative importance of filamentous cyanobacteria. As a result, water transparency decreased substantially and was related to shifts in cyanobacteria species better adapted to low light conditions. Warmer spring and summer conditions were also associated with strong responses in the zooplankton community showing declines in daphniids and increases in small-bodied zooplankton and a dominant calanoid copepod. Taken together, our study suggests that warming temperatures can have important implications for phytoplankton– zooplankton interactions in small eutrophic lakes. 500 A. P. DUPUIS AND B. J. HANN j WARM TEMPERATURES AND PLANKTON DYNAMICS AC K N OW L E D G E M E N T S Downing, J. A., Watson, S. B. and McCauley, E. (2001) Predicting cyanobacteria dominance in lakes. Can. J. Fish. Aquat. Sci., 58, 1905–1908. We thank Michael Paterson and Mark Abrahams for constructive comments and encouragement throughout this study; Hedy Kling for providing guidance in phytoplankton taxonomy; Lynn Frazer for assistance with zooplankton collection and identification and Fort Whyte Alive for use of study site. Downing, J. A., Prairie, Y. T., Cole, J. J. et al. (2006) The global abundance and size distribution of lakes, ponds, and impoundments. Limnol. Oceanogr., 51, 2388– 2397. Edwards, M. and Richardson, A. J. (2004) Impact of climate change on marine pelagic phenology and trophic mismatch. Nature, 430, 881 –884. Environment Canada. (2004) Canadian Climate Normals 1971–2000 for Winnipeg Richardson International Airport, Manitoba, Canada. Environment Canada, National Climate Archive. Data Archives: http://climate.weatheroffice.ec.gc.ca. 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