Vulnerability of Rotifers and Copepod Nauplii to Predation by Cyclops Kolensis (Crustacea, Copepoda) Under Varying Temperatures in Lake Baikal, Siberia

Hydrobiologia DOI 10.1007/s10750-016-3005-2

ROTIFERA XIV

Vulnerability of rotifers and copepod nauplii to predation by Cyclops kolensis (Crustacea, Copepoda) under varying temperatures in Lake Baikal, Siberia

Michael F. Meyer . Stephanie E. Hampton . Tedy Ozersky . Olga O. Rusanovskaya . Kara H. Woo

Received: 22 March 2016 / Revised: 24 September 2016 / Accepted: 1 October 2016 Ó Springer International Publishing Switzerland 2016

Abstract As lakes warm worldwide, temperature that the less evasive Gastropus and Keratella would be may alter plankton community structure and abun- more susceptible to predation than nauplii. We dance by affecting not only metabolism but also exposed a starved predator to individuals of each prey trophic interactions. Siberia’s Lake Baikal presents type and observed encounters, ingestions, and escapes. special opportunity for studying shifting trophic Contrary to our hypothesis, Keratella were consumed interactions among cryophilic zooplankton species in at lower rates than nauplii, due to higher probability of a rapidly warming lake. To understand how warming ingestion after encounter with nauplii. In a second may affect trophic interactions among plankton, we experiment, we assessed how predation varied across a studied predator–prey relationships of a copepod thermal gradient, conﬁning all three prey types and predator (Cyclops kolensis) with three prey types: one starved predator at 5° temperature increments two rotifer species (Gastropus stylifer and Keratella (5–20°C). Predation outcomes mirrored observational cochlearis) and copepod nauplii. We hypothesized feeding trials, and predation outcomes were independent of temperature. Rotifers’ relatively high repro- ductive rate may present a mechanism to withstand Guest editors: M. Devetter, D. Fontaneto, C. D. Jersabek, predation should copepod’s preferred nauplii prey D. B. Mark Welch, L. May & E. J. Walsh / Evolving rotifers, become less abundant in a warmer Baikal. evolving science

M. F. Meyer (&) Keywords Freshwater food webs Á Rotifera Á School of the Environment, Washington State University, Coldwater stenotherms Á Zooplankton Pullman, WA, USA e-mail: [email protected]

S. E. Hampton Á K. H. Woo Introduction Center for Environmental Research, Education, and Outreach, Washington State University, Pullman, WA, As lakes warm worldwide (O’Reilly et al., 2015), USA aquatic communities are likely to shift in composition T. Ozersky and interactions (Moore et al., 1996), both as a result Large Lakes Observatory, University of Minnesota- of direct effects on metabolism (Huey, 1991; Dell Duluth, Duluth, MN, USA et al., 2011) and indirect effects mediated through trophic pathways (Dell et al., 2014). The variety of O. O. Rusanovskaya Biological Research Institute, Irkutsk State University, responses to warming magnifies potential for relation- Irkutsk, Russian Federation ships, such as competition and predation, to change 123 Hydrobiologia under warmer or more variable temperature regimes with warm-adapted, cosmopolitan species (Kozhov, (Huey, 1991; Seifert et al., 2015), but these changes 1963; Kozhova & Izmest’eva, 1998; Hampton et al., may be difficult to predict. Temperature-induced 2008, 2014; Izmest’eva et al., 2016). Warming in changes in planktonic composition and activity have Siberia has occurred nearly twice as fast as global air important implications for ecosystem functioning temperatures, and Lake Baikal has warmed approxi- (e.g., Elliott et al., 2006), determining carbon flow to mately twice as fast as ambient air temperature, with higher trophic levels (Schabetsberger et al., 2009; average surface temperatures increasing by 0.2°C Schmidt et al., 2009), nutrient cycling (Lehman, 1980; decade-1 since 1946 (Shimaraev et al., 2002; Hamp- Higgins et al., 2006; Hambright et al., 2007), occur- ton et al., 2008). Furthermore, increases in cosmopoli- rence of nuisance algal blooms (Rigosi et al., 2015), tan plankton abundances during summer have been and greenhouse gas production (Tadonle´ke´ et al., observed, such as the 12-fold increase of Cyclops 2012). Furthermore, temperature-mediated changes kolensis Lilljeborg, 1901 over the past six decades can alter plankton assemblage composition and abun- (Izmest’eva et al., 2016). Concurrent with this warm- dance, as well as interactions among planktonic ing, endemic plankton species abundance has either species, which can eventually contribute to temporal not changed or has declined in summer months mismatching of consumers with their resources (Hampton et al., 2008; Izmest’eva et al., 2016). The (Thackeray et al., 2010). These effects of temperature extent, to which these changes may have occurred change on communities can become even more through direct effects on metabolism, or indirectly complex when metabolic rate and overall activity of through food web changes, is unknown. aquatic organisms differ across taxa (Dell et al., 2014). Here we experimentally explored the potential for For example, a rotifer trophic web comprised of trophic interactions between rotifers and their preda- predatory Asplanchna brightwellii Gosse, 1850, her- tors to change with shifting temperature. While the bivorous Brachionus calyciflorus Pallas, 1766, and a Baikal plankton is dominated by herbivorous Epis- green alga, ingestion rates increased for both of the chura baikalensis Sars, 1900, predatory C. kolensis consumers, but the greatest increases occurred at and a variety of herbivorous rotifers can occasionally different temperature ranges; thus, outcomes of their become more numerous (Kozhov, 1963; Pomazkova interactions would differ depending on the range and & Kuzevanova, 1989). Perhaps because the pelagic rates of temperature change (Seifert et al., 2015). waters are frequently a near monoculture of Epischura Plankton community structure and function may (Izmest’eva et al., 2016), the ecology of rotifers in respond to warming most strongly in cold lakes that Baikal, including interactions with their prospective have been historically dominated by coldwater taxa, predators such as Cyclops, is not well documented in such as Lake Baikal in Siberia (Moore et al., 2009). In the international scientific literature. Cyclopoid–ro- addition to being the world’s deepest and most tifer interactions can be highly species-specific due to voluminous lake, Lake Baikal is also the oldest and the many predator avoidance strategies that rotifers most biodiverse lake, and exhibits exceptionally high exhibit as well as variation in recruitment–temperature occurrences of endemism (Kozhov, 1963; Kozhova & relationships among zooplankton species (Brandl, Izmest’eva, 1998). The endemic Baikalian plankton 2005; Zhang et al., 2015). Increasing surface temper- tend to be coldwater stenotherms. They are well atures in Lake Baikal in conjunction with increasing adapted to life under ice for half the year where predatory cyclopoid abundance likewise could inten- average temperatures are about 1°C (e.g., Bondarenko sify cyclopoid predation pressure on rotifers. The et al., 2006; Melnik et al., 2006; Hampton et al., 2008), relative paucity of knowledge on ecology of Baikal’s with optimal growth rates at temperatures below 10°C rotifers and the potential for characteristics of Baikal for prominent endemic plankton species (Kozhov, populations to have diverged from those found 1963; Richardson et al., 2000). However, the highest elsewhere together heighten the need to focus on annual diversity of rotifer assemblages occurs in the interactions for these species under changing temper- late-summer and fall months (Pomazkova & Kuze- atures. We exposed Gastropus stylifer Imhof, 1891 vanova, 1989) when surface temperatures average and Keratella cochlearis Gosse, 1851 to predation by about 8°C and can occasionally exceed 16°C (Hamp- co-occurring cyclopoid copepods (C. kolensis), and ton et al., 2008), and cold-tolerant endemics co-occur compared these interactions with cyclopoid response 123 Hydrobiologia to copepod nauplii. The two central objectives of our different location. These samples for plankton enu- experiments were (1) to measure outcomes of preda- meration and community description data were col- tor–prey interactions for each prey type, and (2) to lected from the long-term plankton monitoring site determine whether these outcomes changed in ‘‘Point No. 1’’ (51°5204800 N, 105°0500200 E) on August response to temperature. We hypothesized that the 19, 2015, where a team of researchers from the Irkutsk less evasive rotifers would be consumed at higher rates State University’s Biological Research Institute has than nauplii by C. kolensis and that the results of sampled plankton every 7–10 days for more than predator–prey interactions may change across a tem- seven decades (Silow et al., 2016). Zooplankton perature gradient as movement rates of predators and samples in this long-term program are collected using prey change in a taxon-specific manner. a 100 lm zooplankton net, which can allow smaller rotifers to pass through the mesh. Samples were collected between 0 m (15.0°C) and 10 m (14.5°C) Methods and immediately preserved with formalin. Samples were then concentrated over a period of 5 days. Our overarching approach was to collect experimental Analysis of the sample consisted of accounting for the animals in the field, starve individual cyclopoid presence and abundance of each species within one- predators, and expose them to rotifer and nauplii prey unit volume for that sample collection. Systematic in both an observational experimental arena and one in identification of each species was conducted by a which temperature could be manipulated. counting method according to the standard protocols (Kozhova et al., 1978). Experimental animals Predator–prey behavioral observations On August 19, 2015, plankton were collected with a 64 lm net approximately 50–100 m offshore from In order to address our first objective of measuring Bolshie Koty (51°54021.804600 N, 105°3059.04300 E), outcomes of predator–prey interactions for the focal where water column depth ranged from 10 to 50 m, by prey species, we directly observed predator–prey inter- towing the net behind a rowboat at a depth approxi- actions for each combination of potential predator and mately 1–2 m below the surface. G. stylifer, K. prey type. Individual predators were isolated in GF/F- cochlearis, and copepod nauplii were chosen as prey filtered water without prey at 15°C for 7–24 h before the because they were in high availability relative to other start of the experiment. We incubated the prey with prey. Predators (C. kolensis) and prey were sorted in 64 lm filtered water to remove other animals but to the laboratory under 910–30 magnification. We chose provide some potential food for them, and held them at only gravid (showing well-developed, dark ovaries) 15°C for 18–24 h before the start of the experiment. female C. kolensis for experiments, in order to reduce To initiate the experiment, we placed 30 individuals variation that can occur with predator size, stage, and of a single prey species into 2 ml of 0.7 lm GF/F- sex (Allan, 1976; George, 1976; Gilbert & Williamson, filtered lake water in a well plate under 910 magni- 1983). Before each of the two experiments, prey were fication. We made no effort to include or exclude food sorted into separate containers, targeting prey without for prey. A single predator was added to each predator eggs but recognizing that many of them would later treatment. Interactions were observed for 15 min or a produce eggs at various times during the experiment. total of three prey ingestions, whichever occurred first. We noted encounters, attacks, and ingestions, follow- Plankton enumeration and community description ing the methods of Gilbert & Williamson (1978). Cross-observer comparisons indicated that subjective Although three samples were collected for enumera- interpretation of attacks among observers compro- tion on August 19, 2015 at the same time and location mised data quality; consequently, we focus our as the experimental animals, problems with preserva- analyses on encounters and ingestions. A total of nine tion necessitated using data from Irkutsk State replicates were executed for each of the three prey University’s Biological Research Institute’s regular species, at room temperature of approximately 20°C. sampling to characterize the plankton community at a Data were analyzed with a Type 1 one-way ANOVA 123 Hydrobiologia

(lm in R; R Core Team, 2016) to determine whether was not present. The plankton at that site were prey type significantly influenced encounters, inges- dominated by E. baikalensis, as expected, and Cy- tions, and ingestions per encounter. A post hoc Tukey clops, as well as a variety of rotifers, including K. HSD test was then performed for significant ANOVA cochlearis, were present (Table 1). models. Predator–prey behavioral observations Temperature–predator incubation experiment Our results did not support the hypothesis that rotifers To address our second objective, determining whether would be more susceptible to predation than nauplii; predator–prey interactions were affected by warming, rather, nauplii were more readily ingested once we incubated predators with prey at varying temper- encountered (Fig. 1). The number of encounters atures, and assessed whether the outcomes of preda- differed significantly among prey types (ANOVA; tor–prey interactions changed in response to DF = 2; F = 24.32; P \ 0.01), with Keratella temperature. Individual predators were isolated and encountering predators more frequently than both held in GF/F-filtered Baikal water without prey at nauplii and Gastropus (Tukey HSD; P \ 0.01). 15°C for 24 h before the start of the experiment. We Ingestion did not differ significantly among the prey incubated the prey with 64 lm filtered water to (ANOVA; DF = 2; F = 1.37; P = 0.27). Ingestions remove other animals but to provide some potential per encounter, which includes both the predator’s food for them and held them at 15°C for 24 h before probability of attacking and the prey’s ability to evade the start of the experiment. an attack, did differ with prey type (ANOVA; DF = 2; To initiate the experiment, we placed five individ- F = 5.52; P = 0.01). There was no difference uals of each prey species into 20 ml of 0.7 lm GF/F- between the two rotifers (Tukey HSD; P = 0.08), filtered lake water for a total of 15 prey per container. but nauplii were more likely to be ingested after Again, no effort was made to include or exclude food encounter than Keratella (Tukey HSD; P \ 0.01). for prey. A single copepod adult was added to each predator treatment, and no predator was added to Temperature–predator incubation experiment control treatments. Ten replicates of the predator treatment and five replicates of the control treatment For Keratella, temperature significantly affected abun- were incubated at 5, 10, 15, and 20°C under low- dance (ANOVA; DF = 3; F = 17.29; P \ 0.01), but intensity fluorescent light for 10 h. The control predator (ANOVA; DF = 1; F = 0.31; P = 0.58) and treatment at 10°C had two replicates due to a lack of its interaction with temperature (ANOVA; DF = 3; adequate prey. At the end of the experiment, we F = 0.24; P = 0.87) did not have an observable effect preserved the contents of each dish with Lugol’s and (Fig. 2). Tukey HSD tests revealed that Keratella remaining prey were counted. Data were analyzed abundance at the end of the treatment was significantly using a Type 3 two-way ANOVA (lm in R; R Core higher in 15°C treatments than for any other temper- Team, 2016), to accommodate the design imbalance ature (P \ 0.01). Gastropus was not significantly (Shaw & Mitchell-Olds, 1993) created by the lower affected by predator presence (ANOVA; DF = 1; replication of the 10°C control, with treatment (i.e., F = 0.76; P = 0.39), temperature changes (ANOVA; with or without predator) and temperature (i.e., 5, 10, DF = 3; F = 1.99; P = 0.13), and their interaction 15, and 20°C) as factors. A post hoc Tukey HSD test (ANOVA; DF = 3; F = 1.14; P = 0.34). Predator was performed for significant ANOVA models. presence significantly reduced nauplii (ANOVA; DF = 1; F = 16.13; P \ 0.01), but no effects were evident for temperature (ANOVA; DF = 3; F = 1.32; Results P = 0.28) nor the interaction of predator and temperature (ANOVA; DF = 3; F = 0.52; P = 0.67). At the Plankton enumeration and community description conclusion of this experiment, we noticed that rotifers frequently were smaller or carrying eggs, indicating At the location offshore where the samples for that reproduction occurred in both predator and control community description were collected, G. stylifer treatments, and likely to a level that helped replace 123 Hydrobiologia 00 48 0 rotifers that might have been eaten. Visually, it 52

° appeared that both rotifers may have reproduced the most in the 15°C treatment (Fig. 2b, c), though only 0.45 51.8 33.75 11.71 Keratella’s increase was signiﬁcant. Individuals per Liter Individuals

Discussion

e from ‘‘Point No. 1’’ (51 Keratella (Rotifera) Contrary to our expectations, the rotifer was less vulnerable to predation than copepod nauplii, due Imhof, 1891 Imhof, Ehrenberg, 1830Ehrenberg, Carlin, 1943 36 Gosse, 1851Kellicot, 1879 19.8 23.63 Hudson, 1885Hudson, 9 Plate, 1886 19.13 Müller, 1786 1786 Müller, O.F. Müller, 1776 Müller, O.F.

Chlorophyta to Keratella’s low probability of ingestion after Rotifers Rotifers Total Rotifer: 149.85 Rotifer: Total encounter, with more variable results for the rotifer Species , and Gastropus. Nauplii were highly susceptible to preda-

) from a single sample were used from a different tion, as demonstrated by both their relatively high 1 - Filinia terminalis Filinia Bipalpus hudsoni probability of ingestion after encounter and the Keratella quadrata quadrata Keratella Keratella cochlearis Collotheca mutabilis Collotheca Bosmina longirostris Kellicottia longispina Polyarthra vulguaris Cyanophyta reduction of naupliar survivorship in predator treat- ,

Euchlanis dilatata dilatata dilatata Euchlanis dilatata ments across a temperature gradient. Since Epischura nauplii were nearly three times more abundant than Cyclops nauplii (Table 1), the majority of nauplii consumed were almost certainly Epischura, though Bacillariophyta 1.35 3.82

, we did not screen for a speciﬁc taxon of nauplii. Contrary to our results, many studies have shown that

Copepodites nauplii are better defended against cyclopoid preda- Lilljeborg, 1901) Lilljeborg,

Dinophyta tion than are the rotifers due to effective escape I + II I + , Total responses and sometimes due to larger size (Wil- liamson, 1980). Copepods usually prefer smaller prey between 150 and 200 lm (Plassmann et al., 1997), Total Cyclops: 9.67 Cyclops: Total 1.58 3.15 1.13 Cyclops kolensis 5.85 Chrysophyta (

Total 195.31 Zooplankton: such as rotifers, although physical defenses such as

Nauplii those of Keratella, can deter predation (Gilbert &

Cyclops Williamson, 1978; Gilbert & Stemberger, 1984; Stemberger & Gilbert, 1984; Devetter & Sed’a, I + II I + V + VI III + IV III + 2006; Sarma et al., 2011; Nandini et al., 2014). Rotifers’ swimming patterns also can affect probability of detection by predators (Williamson, 1980).

4.95 Total When defenses are lacking, some rotifer species are less preferred prey presumably due to their inability to satiate the predator for proportional energy expendi-

Sars, 1900) ture (Stemberger, 1985). Altogether, literature demon- Copepodites strates that larger size, physical defenses, and behavior I0.9 are frequently, but not always, effective defenses against copepod predators, but the outcomes of predator–prey interactions can be highly species-

Epischura baikalensis speciﬁc and difﬁcult to predict, in spite of these Total Epischura: 24.08 ( generalities (e.g., Stemberger, 1985; Brandl, 2005). 0 E) for a depth from 0 to 10 m on the same day as experimental animals were collected Temperature did not appear to alter predation rates 00 02 Epischura

0 across these taxa, although the rotifers appeared to Nauplii Due to problems with preservation of our original samples, zooplankton community enumerations (individuals l 05

° reproduce more in the 15°C treatment, suggesting that I

IIV 0.68 7.88 II V 0.68 life history 0.68 can play a strong role V in determining 1.13 IIIIVVI 3.38 4.95 2.25 III IV 2.25 1.35 III IV 0.9 0.45 Total 19.13 Total Stage per Liter Individuals Stage per Liter Individuals Stage per Liter Individuals Stage per Liter Individuals location on the same day, collected as part of the long-term plankton monitoring project at Irkutsk State University’s Biological Research Institut Table 1 N, 105 Phytoplankton taxa noted though not included in this characterization were population-level outcomes of predator–prey dynamics. 123 Hydrobiologia

temperature and population growth in rotifers can result in changes that occur on short time scales of hours and days (Edmondson, 1946; Halbach, 1973), there is likely some range of temperature in which rotifers may replace themselves more rapidly than they are removed by Cyclops. Beyond rotifer replacement, temperature may have more complex effects on predator–prey outcomes at the level of populations through shifts in timing and magnitude of Cyclops recruitment (Ekvall & Hansson, 2012) or through increases in top-down predation pressures by larger consumers (Gyllstro¨m et al., 2005). When considering the inter-generational effects of temperature change on community structure, Pavoń-Meza et al. (2007) demonstrated in Brachionus that temperature and food availability can influence body size and spine length, factors which can affect predation. Although Dell et al. (2014) demonstrated that predator–prey interactions are likely to shift in tandem with gradually changing temperatures, long-term changes in temperature at Baikal do not appear to be synchronous across species. Temperature increases in Lake Baikal have been correlated with 12-fold increases in cyclopoid abundance, while the endemic, herbivorous Epischura have not shown significant population changes despite increase in their algal food source (Izmest’eva et al., 2011, 2016). Considering the large increase in C. kolensis over the past 60 years, it is conceivable that the rotifers may experience an increased predation pressure even if they do not elicit as strong a predatory response from C. kolensis as do nauplii. In the context of our experiments, temperature could play a critical role for zooplankton community dynamics between generations, but within the short time span of our experiments, predation at different temperatures did not alter outcomes of predator–prey interactions. While much work has already explored the predation patterns of copepods on rotifers, patterns tend to be species-specific, whereas rotifers avoid predation Fig. 1 Average (±1 SE) a number of encounters, b number of ingestions, and c proportion of ingestions per encounter for each through a host of defense mechanisms and behavioral prey type in observational feeding trials patterns (Brandl, 2005). In a review of cyclopoid predation on rotifer prey, Brandl (2005) compiled Rotifers have generally shown increased reproduction extensive information of known cyclopoid predation at temperatures greater than 15°C (Halbach, 1973; on rotifer species, as well as synthesized general trends Pourriot & Clement, 1981; Pourriot & Rougier, 1997), among cyclopoid and rotifer species. Community and the egg development time for some rotifers can be composition, predator satiation, and prey density can on the order of 6 h (Kostopoulou & Vadstein, 2007). play major roles in prey selection, in addition to Since strong, species-specific relationships between species-specific defenses.

123 Hydrobiologia

Fig. 2 Average (±1 SE) Nauplii Remaining (a) number of remaining a nauplii, b Gastropus, and 5ºC 10ºC 15ºC 20ºC c Keratella after incubated 6 predation trials by temperature and predator presence 4

0 Control Predator Control Predator Control Predator Control Predator

Gastropus Remaining (b) 5ºC 10ºC 15ºC 20ºC

Control Predator Control Predator Control Predator Control Predator

Keratella Remaining (c) 5ºC 10ºC 15ºC 20ºC

Control Predator Control Predator Control Predator Control Predator

Significance in the context of a changing climate at somewhat higher temperatures in spite of predation, due to their ability to rapidly reproduce with increas- Located in the heart of Siberia, Lake Baikal remains a ing average temperatures (Halbach, 1973; Pourriot & hotspot for endemic biodiversity of coldwater ste- Rougier, 1997; Pourriot & Clement, 1981). However, notherms (Moore et al., 2009). With increasing water while the patterns we observed here were independent temperatures in lakes worldwide, it is unclear how of temperature, the dominant herbivore in Lake coldwater-adapted species will respond and alter Baikal, E. baikalensis, is known to be intolerant of plankton communities. In the case of these Lake temperatures above 15°C (Kozhov, 1963; Afanasyeva, Baikal rotifers, we did not see evidence that their 1977), which could precipitate major plankton com- abundance might be reduced through changes in munity changes. With Baikal’s average water temper- Cyclops predation. If anything, rotifers may prosper atures increasing rapidly (Hampton et al., 2008)in 123 Hydrobiologia concert with climate change, it is possible that Gilbert, J. J. & C. E. Williamson, 1983. Sexual dimorphism in copepod nauplii, typically the most abundant prey zooplankton (Copepoda, Cladocera, and Rotifera). Annual Review of Ecology and Systematics 14: 1–33. type, might become less abundant and prompt C. Gilbert, J. J. & R. S. Stemberger, 1984. Asplanchna-induced kolensis to prey more heavily on rotifer prey. polymorphism in the rotifer Keratella slacki. Limnology and Oceanography 29: 1309–1316. Acknowledgments We would like to thank the faculty, Gyllstro¨m, M., L. A. Hansson, E. Jeppesen, F. G. Criado, E. students, staff, and mariners of the Irkutsk State University’s Gross, K. Irvine, T. Kairesalo, R. Kornijo´w, M. R. Miracle, Biological Research Institute Biostation for expert field and M. Nyka¨nen, & others, 2005. The role of climate in shaping laboratory support, Marianne Moore, Bart De Stasio, and zooplankton communities of shallow lakes. Limnology and Eugene Silow for helpful advice; Dick Keefe for translation Oceanography 50: 2008–2021. assistance; and Steve Powers, Stephanie Labou, and Steve Katz Halbach, U., 1973. Life table data and population dynamics of for diverse technical and statistical assistance. Funding was the rotifer Brachionus calyciflorus Pallas as influenced by provided by the National Science Foundation (NSF-DEB- periodically oscillating temperature. In Effects of Tem- 1136637) to S.E.H., a Fulbright Fellowship to M.F.M., and the perature on Ectothermic Organisms. Springer, Berlin: Russian Ministry of Education and Science Research Project 217–228. (No. GR 01201461929; 1354-2014/51). Hambright, K. D., T. Zohary & H. Gu¨de, 2007. Microzoo- plankton dominate carbon flow and nutrient cycling in a warm subtropical freshwater lake. Limnology and Oceanography 52: 1018–1025. 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