Climate Change and the Timing, Magnitude, and Composition of the Phytoplankton Spring Bloom

Global Change Biology (2008) 14, 1–10, doi: 10.1111/j.1365-2486.2008.01571.x

Climate change and the timing, magnitude, and composition of the phytoplankton spring bloom

ULRICH SOMMER andKATHRIN LENGFELLNER Leibniz Institute for Marine Sciences at Kiel University, Du¨sternbrooker Weg 20, 24105 Kiel, Germany

Abstract In this article, we show by mesocosm experiments that winter and spring warming will lead to substantial changes in the spring bloom of phytoplankton. The timing of the spring bloom shows only little response to warming as such, while light appears to play a more important role in its initiation. The daily light dose needed for the start of the phytoplankton spring bloom in our experiments agrees well with a recently published critical light intensity found in a field survey of the North Atlantic (around 1.3 mol photons m2 day1). Experimental temperature elevation had a strong effect on phytoplankton peak biomass (decreasing with temperature), mean cell size (decreasing with temperature) and on the share of microplankton diatoms (decreasing with temperature). All these changes will lead to poorer feeding conditions for copepod zooplankton and, thus, to a less efficient energy transfer from primary to fish production under a warmer climate. Keywords: climate change, phytoplankton, spring bloom, zooplankton

Received 21 September 2007; revised version received 20 December 2007 and accepted 27 December 2007

the North Atlantic Ocean and a surprisingly uniform Introduction 2 1 critical light level (Ic) of 1.3 mol photons m day The spring bloom is one of the dominant features in the (0.96–1.75) without apparent latitudinal variation was seasonal growth patterns of phytoplankton of tempe- found to initiate the spring bloom (Siegel et al., 2002). rate and cold oceans and lakes. In nutrient-poor and Deviating from this focus on light, most of the phy- high-latitude waters, it is even the single seasonal peak toplankton papers related to global change and to of primary production, providing the energy and mat- contemporaneous climate variability put the emphasis ter base for zooplankton and fish production. While the on temperature or on climate indices, like the North timing of the spring bloom is variable from site to site Atlantic Ocean Oscillation Index (Weyhenmeyer et al., and from year to year, already half a century ago, 1999; Wehenmeyer, 2001; Edwards et al., 2002; Stenseth Sverdrup’s (1953) critical depth hypothesis provided a et al., 2002). While usually acknowledging the impor- theoretical framework for a mechanistic explanation tance of thermal stratification for light supply, direct where the onset of thermal stratification in spring seas temperature effects have not been disentangled from acts as a switch from insufficient light to light suffi- light effects. Most field studies have found the expected ciency. At similar water transparency and surface irra- earlier onset of the spring bloom under warming con- diance, phytoplankton circulating through a shallow ditions (Straile, 2000; Straile & Adrian, 2000; Gerten & mixed surface layer experience on an average more Adrian, 2001), which agrees both with the frequently light than phytoplankton circulating through a deeper reported earlier onset of spring events reported from mixed water layer, i.e. the mixing depth has to fall terrestrial ecosystems (e.g. Walther et al., 2002) and below a critical limit (i.e. critical mixing depth) before with commonsense expectation. However, also retarda- phytoplankton growth can start in winter. In a recent tions by warming have been reported (e.g. for the study, the critical mixing depth was related to the shallow German Bight of the North Sea, Wiltshire & average daily light dose in the mixed surface layer of Manly, 2004). Obviously, temperature and stratification- mediated light effects are not easily disentangled in Correspondence: Ulrich Sommer, tel. 149 431 600 4400, field studies, because the onset of thermal stratification fax 149 431 600 4402, e-mail: [email protected] depends on the balance of surface warming and wind r 2008 The Authors Journal compilation r 2008 Blackwell Publishing Ltd 1 2 U. SOMMER & K. LENGFELLNER energy input. On the other hand, temperature has survival experiment (Sommer et al., 2007). During the direct, accelerating effects on the physiological rates first experiment (2005), the 1400 L chamber was connected both of phytoplankton and of herbivorous zooplankton in circular flow to a 300 L ‘benthos’-chamber containing feeding on phytoplankton. In general, production sediment and mussels in order to supply the plankton rates of light-limited phytoplankton appear less community with meroplanktonic larvae and organisms responsive to temperatures (Tilzer et al., 1986) than germinating from benthic resting stages. As no such heterotrophic processes. The temperature indepen- organisms had appeared in the experiment, the benthos dence of light-limited production contrasts with a chamber was abandoned during the following ones. temperature dependence of light-saturated production. Temperature and light were computer controlled and

The classic Q10-value of light-saturated phytoplankton had a late winter/early spring seasonal pattern. Be- growth (1.88; Eppley, 1972) is near the lower margin of cause of technical reasons, the starting dates of the

Q10-values reported for heterotrophic processes: micro- experiments differed somewhat between the years, algal respiration: 2.6–5.2 (Hancke & Glud, 2004); but the temperature and the light program were ad- zooplankton respiration: 1.8–3.0 (Ivleva, 1980; Ikeda justed to a theoretical start on 4 February (Julian et al., 2001); zooplankton filtration rates: 2–3 (Prosser, day 35). There were four temperature regimes (each 1973); bacterial respiration: 3.3 (Sand-Jensen et al., 2007). duplicated), the coldest one (‘baseline’) corresponding In order to disentangle light and temperature effects to the decadal average 1993–2002 in Kiel Bight and on the timing, magnitude, and composition (size struc- three elevated temperature regimes with 1 2, 1 4, ture and higher taxa) of the phytoplankton spring and 1 6 1C temperature elevation above the baseline bloom, we performed indoor mesocosms experiments until the end of February. After this, the temperature with natural plankton communities from the Kiel Bight, difference between the treatments was reduced by Baltic Sea, Germany. Plankton communities were 0.25 1C per month. For the sake of brevity, the initial subject to four temperature regimes, the lowest one temperature difference will be used to characterize the conforming to the 1993–2002 average of local sea sur- temperature treatments throughout this article. face temperatures (SSTs), while the other ones were Light supply and day length were adjusted according elevated by 2, 4, and 6 1C, in order to mimic moderate to the seasonal light patterns calculated from astronomic to drastic climate change scenarios (IPCC, 2007). But equations (Brock, 1981) for above cloud light levels (I0) note that the treatment range from 0 to 6 1C temperature and reduced to a fixed percent level for each experiment elevation does not exceed the present day year-to-year (16%, 32%, 64% of I0), in order to account for different variability of January to March mean temperatures levels of light loss by cloud cover and underwater (Matthaüs & Schinke, 1994). While temperature regimes attenuation. For further details, see Sommer et al. (2007). were uniform between the three experimental runs, While each temperature regime was run in duplicate in light regimes differed between them. The natural day each of the experimental years (2005, 2006, 2007), only length was adjusted to natural conditions and the one light regime could be run per year (Table 1). natural solar irradiances (I0) calculated from astronomic models for each day (Brock, 1981) were reduced to 16%, Sampling and analysis 32%, and 64% to mimic different degrees of cloudiness and underwater light attenuation. Phytoplankton was sampled three times per week (Monday, Wednesday, Friday) from mid-depth of the mesocosms. Phytoplankton 45 mm were counted by the Materials and methods inverted microscope method (Utermo¨hl, 1958) and distinguished at the genus level in most cases. We Experimental design aimed at counting 100 individuals per taxonomic unit Eight mesocosms with a volume of 1400 L and a depth of in order to obtain 95% confidence limits of 20%, but 1 m were set up in temperature-controlled rooms and this standard could not be attained with rare species. filled with natural late winter plankton communities from Small phytoplankton were counted by a flow cytometer Kiel Fjord, Western Baltic Sea. Mesozooplankton was (FACScalibur, Becton Dickinson, San Jose, CA, USA) added within the first week from net catches at typical and distinguished by size and fluorescence of over-wintering concentrations, targeted at 10–20 chlorophyll a, phycoerythrin, and allophycocyanin. individuals L1 and consisted mainly of the copepods When flow cytometer categories could be matched to Pseudocalanus sp. and Oithona similis.Theplanktonwas phytoplankton in the microscopic counts (Teleaulax, gently stirred by a propeller which secured a homoge- Plagioselmis, Chrysochromulina), we used the flow cyt- neous distribution of plankton and did not lead to ometer data. Phytoplankton biomass was estimated as mortality of zooplankton, as tested by a zooplankton carbon calculated from cell volumes (Menden-Deuer &

r 2008 The Authors Journal compilation r 2008 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/j.1365-2486.2008.01571.x CLIMATE CHANGE AND PHYTOPLANKTON SPRING BLOOM 3

Table 1 Experimental light and temperature regimes in the mesocosm experiments

Year I in I0% DT ( 1C) T on Julian day 35 ( 1C) T on Julian day 91 ( 1C)

2005 16 0, 2, 4, 6 2.4, 4.4, 6.4, 8.4 4.7, 6.4, 8.1, 9.8 2006 64 0, 2, 4, 6 2.4, 4.4, 6.4, 8.4 4.7, 6.4, 8.1, 9.8 2007 32 0, 2, 4, 6 2.4, 4.4, 6.4, 8.4 4.7, 6.4, 8.1, 9.8

I, % of natural light intensity above cloud cover (I0); DT, initial temperature elevation relative to the long-term mean (1993–2002, actual temperatures) at Julian day 35 (start of experiments) and at Julian day 91 (last spring peak found in any of the mesocosms.

Lessard, 2000) calculated from linear measurements after approximation to the nearest geometric standard kz 1 Imix ¼ I0ð1 e ÞðkzÞ : ð1Þ solid (Hillebrand et al., 1999). Phytoplankton data were lumped into ‘functional groups’ using the stan- It agreed relatively well between all temperature dard size classification pico-, nano-, and microplankton treatments within the 16% and 32% I0-experiments (Sieburth et al., 1978) and the distinction between dia- and the difference between both experiments was min- toms and flagellates as classification criteria. In addi- or (Fig. 2). Overall, Imix-values at the start of the spring 2 1 tion, bentho-pelagic diatoms (Tabularia fasciculata, bloom ranged from 1.14 to 1.63 mol photons m day 2 1 Navicula) originating from wall growth in the meso- with a mean value of 1.34 mol photons m day . The cosms were treated as a separate category, because their high-light experiment was started at light intensities 2 1 occurrence in the plankton was considered to be artifi- above Ic (2.27 mol photons m day ), which lead to an cially enhanced by the experimental conditions. A immediate start of phytoplankton growth. further separate functional group was defined for the The timing of the spring peak showed a weak depen- silicoflagellate Dictyocha speculum, because this species dence on temperature, with a relatively uniform 1 1 combines functional features of flagellates (motility) acceleration of 1–1.4 days C temperature increase and diatoms (Si demand). relative to the background (Table 2). In the 16% light experiment, this trend was marginally insignificant (P 5 0.0775). This weak temperature effect contrasts with an almost 1.5 months offset between the timing of the spring peak in the low-light and the high-light Results experiments (Fig. 3a).

Timing of the spring bloom Phytoplankton biomass and cell size All experiments showed the typical temporal pattern of a spring bloom with a subsequent decline of phyto- At all light levels tested, the peak biomass of phytoplankton biomass (‘clear water phase’; Sommer et al., plankton declined with increasing temperatures (Fig. 1986), in some cases (low-light, high-temperature ex- 3b, Table 3). The best fit to the data could be obtained by periments) the clear water phase was followed by a the multiplicative regression model according to the b recovery of phytoplankton biomass (Fig. 1). In the low equation y 5 a x . While the magnitude of the tem- and medium-light (16% and 32% of I0) experiments, perature effect was different between the different light there was an initial decline (16%) or stagnation (32%) of levels, the sign of the effect was identical between all phytoplankton biomass before spring growth started, experiments. Similarly, there was a pronounced effect of while phytoplankton growth started without a lag- temperature on the average cell size, with cell size phase in the high-light experiment. The starting date declining with increasing temperature elevation (Fig. of the phytoplankton spring increase was defined by 3c, Table 4). the beginning of exponential growth. It was uncorre- lated to the temperature treatment (16% I : P 5 0.57; 0 Phytoplankton composition 32% I0: P 5 0.19), and occurred over a wide range of temperatures (2.4–8.8 1C). The light level at the start of Initial community composition differed strongly be- the spring bloom was calculated by using the pro- tween years, but was uniform between mesocosms of grammed I0-values and calculating the mean light the same year. In 2005 (16% I0), initial phytoplankton intensity for the mesocosms with a typical attenuation biomass was dominated by microplankton (420 mm cell coefficient for winter water (k 5 0.25 m1, z 5 1m; length) diatoms (61 5.0%, SD) followed by nanofla-

Imix 5 0.885 I0) according to the equation (Riley, 1957): gellates (35.8 4.9%). In 2006 (64% I0), the initial bio- r 2008 The Authors Journal compilation r 2008 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/j.1365-2486.2008.01571.x 4 U. SOMMER & K. LENGFELLNER

(a) 16% Io Start of spring bloom 150 2.5 ) 1

− 120 2

90 1.5

60 1

Daily light dose 0.5 30 0 0 02 46 810 30 50 70 90 110 130 Temperature (°C) Julian day Fig. 2 Temperature and daily light dose (mol photons (b) 32% Io m2 day1) at the onset of the spring bloom. Filled triangles: 600 experiment with 16% I0 ; ﬁlled circles: experiment with 32% I0 ; ) Biomass (µg C L

1 500 horizontal lies: upper and lower margin of Siegel’s et al. (2002) − data for critical light daily light doses. In the 64% I0 experiment, 400 this point could not be identiﬁed because exponential growth 300 started directly at the beginning of the experiment, i.e. at 2.27 mol photons m2 day1. 200

Biomass (µg C L 100 Table 2 Date of the spring bloom (d, in Julian days) in 0 dependence of temperature elevation (DT,in 1C), regression 30 50 70 90 110 130 analysis according to the model: d 5 a 1 bDT Julian day 2 Light (% of I0) ab rP (c) 64% Io 1500 16 90.5 2.4 1.38 0.65 0.430 0.0775 32 82.8 1.1 0.98 0.29 0.646 0.0162 )

1 1250 − 64 47.5 1.1 1.13 0.29 0.714 0.0082 1000

750 In spite of the interannual differences in initial bio- 500 mass composition, the cross-sectional analysis compar-

Biomass (µg C L 250 ing the biomass composition at the peak time of the spring bloom showed several quite consistent trends 0 30 50 70 90 110 between the years. The negative correlation of the Julian day relative biomass of microplankton diatoms with temperature elevation was the most obvious trend in func- Fig. 1 Time course of phytoplankton biomass. Biomass (mg tional group composition (Fig. 4, Table 5). Major CL1) shown for one of the 1 0 1C temperature treatments (open contributors were centric species Rhizosolenia setigera, squares) and one of the 1 6 1C treatments (ﬁlled circles): (a) light Proboscia alata, and Chaetoceros spp., in different propor- level 16% of I0; (b) light level 32% of I0; (c) light level 64% of I0. tions in the different experiments. In the 2007 experi-

ment (32% I0), the silicoflagellate D. speculum, which mass was co-dominated by microplankton diatoms was absent from the other experiments, showed a (45.5 6.8%) and nanoplankton diatoms (38.3 6.2%), similar response pattern as the microplankton diatoms. while nanoflagellates comprised only 13.5 3.8% of the Functionally, it might be considered an intermediate biomass. In 2007 (32% I0), nanoflagellates dominated between the other flagellates (motility) and the diatoms (51.2 7.0%; without Dictyocha). The silicoflagellate (with skeletal Si structures). The nanoplankton formed 12.1 2.3% and microplankton diatoms formed (o20 mm) diatoms, represented mainly by the chain- 11.8 0.6% of the total biomass, respectively. Contrary forming Skeletonema costatum, responded differently to to the big differences in relative biomass, the taxonomic temperature between the different experiments (16% I0: lists showed wide overlap between years, with one no significant response; 32%: negative response; 64% I0: notable exception. D. speculum was missing or at least unimodal response with an optimum 44 1C tempera- below the limit of detection in 2005 and 2006. ture elevation). The total of planktonic diatoms

r 2008 The Authors Journal compilation r 2008 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/j.1365-2486.2008.01571.x CLIMATE CHANGE AND PHYTOPLANKTON SPRING BLOOM 5

(a) Timing Table 3 Maximal phytoplankton biomass (B,inmgCL1) 100 during the spring bloom in dependence of temperature eleva- 16% Io tion (DT,in 1C), regression analysis according to the model: 90 B 5 a(DT 1 1)b 80 2 32% Io Light (% of I0)lnab rP 70 16 4.59 0.15 0.40 0.11 0.694 0.0102

Julian day 60 32 6.81 0.31 1.02 0.23 0.771 0.0041 50 64% Io 64 7.01 0.15 0.37 0.11 0.660 0.0142 40 0246 ∆ ° 1 T ( C) Table 4 Average cell size (C, in pg C cell ) during the spring bloom in dependence of temperature elevation (DT,in 1C), (b) Biomass regression analysis according to the model: C 5 a(DT 1 1)b 1600 Experiment ln ab R2 P 1200

1 16 2.50 0.31 1.47 0.23 0.874 0.0007 − 32 4.11 0.44 1.54 0.32 0.794 0.0030 800 64% Io 64 3.59 0.15 0.52 0.11 0.787 0.0033 µg C L

400 32% Io 16% Io were positively correlated to temperature elevation,

0 except for the 64% I0-experiment, where they were of 0246minor importance only. The relative biomass of pico- ∆T (°C) plankton responded positively to temperature elevation or exhibited a unimodal response with an optimum Cell size (c) near 4 1C warming. 60

50 Discussion 1

− 40 30 Limitations of the mesocosm approach 64% Io pg C cell 20 Mesocosms are frequently criticized of not being perfect 10 16% Io 32% Io images of the real world because of containment arti- facts (e.g. wall growth) and of being unable to catch 0 0246important in situ processes such as advection and im- ∆T (°C) migration of new genotypes and species. While acknowledging this critique as being justified, we Fig. 3 Timing, biomass, and mean cell size of the spring bloom consider mesocosms a necessary tool filling the scale in dependence of the temperature elevation for the three differ- gap between laboratory microcosm studies based on ent light levels (16%: hanging triangles; 32%: circles; 64%: clonal cultures and field studies (Sommer, 2002). In standing triangles): (a) timing (Julian days); (b) biomass comparison to clonal cultures, our mesocosms have 1 1 (mgCL ); (c) cell size (pg C cell ). In some cases, the number the advantage to capture the full genetic diversity of of points appears less than the number of experimental units plankton found at the m3-scale in situ and selecting the because identical results were obtained from parallel treatments. optimally adapted reaction norms to all experimental treatments. Given the high taxonomic variability in responded negatively to temperature elevation, except light requirements of phytoplankton, the identification for the 64% I0-experiment, in which both size classes of of the daily light dose needed for the start of the spring diatoms formed 490% of the total biomass in all bloom would have been entirely dependent on the temperature treatments. choice of the test organisms. In the mesocosms, the best While the microplankton flagellates were negligible adapted among many clones had the chance to build up in all experiments, the relative biomass of picoplankton the spring bloom. This is still not the full range of and the nanoplankton flagellates together formed mir- natural diversity, particularly if one considers the pos- ror images of the diatoms. The nanoplankton flagellates sibility of immigrations from other sea basins. Never- r 2008 The Authors Journal compilation r 2008 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/j.1365-2486.2008.01571.x 6 U. SOMMER & K. LENGFELLNER

(a) 16% Io litatively similar to the continuous loss of nutrients by 150

) sedimentation of particles through a pycnocline in a

1 pico − 120 n-flag stratiﬁed water body, though the quantitative effect dict might be very dissimilar. Bentho-pelagic algae were 90 b-diat n-diat mainly represented by the diatom T. fasciculata in our 60 m-diat experiments. This species is also a regular, but subdo- 30 minant component of spring phytoplankton in the near-

Biomass (µg C L shore regions of the Baltic Sea. Once detached from 0 00224466 solid surfaces, it behaves like a planktonic diatom. It ∆T (°C) was unimportant at the start of the spring bloom but gained some importance in the warmer treatments at (b) 32% Io the low and intermediate light levels. As wall growth 1500 ) develops with time and became visible in our meso- 1 pico − 1250 n-flag cosms just before or after the spring peak, we restrict 1000 dict our analysis to the build-up phase of the spring bloom b-diat 750 n-diat and refrain from interpretation of the decline and the m-diat 500 clear water phase. 250 A further restriction lies in the shallow depth of the mesocosms, which only permits to simulate mean 0 00224466 mixed water column light intensities but not the full ∆T (°C) range of light variability from top to the bottom of a natural mixed layer. It is known that the response to (c) 64% Io highly variable light can deviate from the response to 1500

) Biomass (µg C L less variable light with the same mean intensity if the

1 pico − 1200 n-flag range of variation exceeds the limits of saturation or dict even inhibition (Litchman, 2000). Particularly low-light 900 b-diat n-diat adapted species would suffer from inhibiting light 600 m-diat intensities because of their reduced photoprotective 300 abilities (Dimier et al., 2007; Lavaud et al., 2007). Such

Biomass (µg C L effects are less important if the start of the spring bloom 0 00224466 is initiated by a gradual increase of the light intensity ∆T (°C) across a starting threshold, but they can be important if the spring bloom is initiated by a relatively sudden Fig. 4 Phytoplankton spring bloom biomass for the different onset of stratification under high surface irradiance. 1 functional groups. Biomass (mgCL ) shown as stacked barch- We further want to emphasize that our experiments arts for the different temperature treatments and light levels. were meant to mimic the typical spring bloom of Each mesocosm is shown separately. Abbreviations for func- temperate and boreal waters (Sommer et al., 1986; tional groups: pico, picoplankton; n-flag, nanoplankton flagellates; dict, Dictyocha speculum; b-diat, bentho-pelagic diatoms; Sommer, 1996) but not any other kind of phytoplankton n-diat, nanoplankton diatoms; m-diat, microplankton diatoms: bloom. Phytoplankton blooms are order-of-magnitude

(a) light level 16% of I0; (b) light level 32% of I0; (c) light level 64% increases within days or a few weeks which are seen as of I0. a response of phytoplankton to short-term windows of opportunity when environmental controls keeping phytoplankton biomass cease to operate (‘loopholes’ sensu; theless, we consider the agreement between our daily Bakun & Broad, 2003; Irigoien et al., 2005). The environ- light dose at the start of the spring bloom with the one mental control ceasing last might then be considered the found by Siegel et al. (2002) very reassuring: obviously, trigger of a bloom. Recently published examples are the the natural variability of phytoplankton light require- release from grazing pressure (Irigoien et al., 2005) or ments in a big ocean provides little additional scope for external input of limiting nutrients, such as iron from an earlier start of the spring bloom under less light. aeolian dust (Moore et al., 2006). In contrast to such A further problem of mesocosm lies in the develop- cases, we focus on the release from physical controls ment of a biofilm on the walls. This biofilm binds (light, temperature, stratification) as the widely ac- nutrients that would otherwise be available for the cepted primary trigger for the transition from the pelagic community and provides niches for algae with winter depression of phytoplankton biomass to the a bentho-pelagic life style. The former problem is qua- spring bloom in nutrient-rich seas (Sverdrup, 1953;

r 2008 The Authors Journal compilation r 2008 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/j.1365-2486.2008.01571.x CLIMATE CHANGE AND PHYTOPLANKTON SPRING BLOOM 7

Table 5 Relative biomass (pi 5 Bi/Btot ; expressed in carbon) of phytoplankton at the spring bloom biomass maximum (each mesocosm treated as a separate case) in dependence of temperature elevation (DT,in 1C), regression analysis according to the p model; regression analysis for monotonous response according to the models: monotonous: arcsin pi 5 a 1 bDT. *If this model did p 2 not ﬁt: ln ( pi 1 0.001) 5 a 1 DT. Unimodal: arcsin pi 5 a 1 bDT 1cDT , for this model also calculated optima are given

2 Light (% of I0) abcROptDTP

All plankton diatoms 16 44.0 7.7 5.56 2.05 0.558 0.0331 32* 3.10 0.73 0.52 0.19 0.549 0.0355 64 No correlation Microplankton diatoms 16 37.3 8.0 7.1 2.10 0.609 0.0158 32* 3.90 0.79 0.61 0.21 0.581 0.0260 64 53.0 3.3 3.26 0.88 0.697 0.0099 Nanoplankton diatoms 16 No correlation, always o10% 32 7.10 1.18 0.82 0.31 0.531 0.0404 64 28.5 1.6 10.3 1.31 1.11 0.21 0.945 4.64 0.0030 Bentho-pelagic diatoms 16 No correlation 32 66.5 9.5 4.54 1.64 0.561 0.0404 64 Absent Dictyochales (silicoflagellates) 16 Absent 32 66.5 1 9.5 9.84 2.53 0.717 0.0080 64 Absent Microplankton flagellates 16 Absent 32 Absent 64 Absent Nanoplankton flagellates 16 31.1 3.25 2.61 0.87 0.602 0.0237 32 15.2 3.09 5.11 0.83 0.865 0.0008 64 No correlation, always o10% Picoplankton 16 18.7 3.84 14.1 3.1 1.73 0.49 0.800 4.08 0.0077 32 1.07 2.85 3.71 0.76 0.78 0.0028 64 1.63 0.27 0.79 0.22 0.11 0.04 0.656 3.66 0.0322

Smetacek & Passow, 1990). Only in this context, the light experiments as a strong support, but not as a contrast between the temperature insensitivity of light- proof, for a predominant role of light in the initiation limited production and temperature sensitivity of het- of the spring bloom. The weak temperature effect on the erotrophic processes can play a role anticipated in the advancement of the spring bloom (1–1.4 days 1C1)is concept of our study. by far not sufficient to explain the interannual variability in the timing of the spring bloom in situ. The experimentally obtained temperature effect amounts to Light vs. temperature effects just about 1 week over the entire range of experimental The experiments with the different light levels have temperature treatments, which is just one sampling been performed during different years and, therefore, interval in many routine monitoring programs. The with a different composition of the natural inoculum. interannual differences in the timing of the spring This prevents a statistical analysis of the relative bloom are not only much bigger, their response to strength of light and temperature effects. However, we warming might even show the reverse sign, as in the take the strong difference in the bloom timing between German Bight (Wiltshire & Manly, 2004). Similarly, the the high-light experiments and the low and medium- spring bloom in the Kiel Bight occurred much earlier r 2008 The Authors Journal compilation r 2008 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/j.1365-2486.2008.01571.x 8 U. SOMMER & K. LENGFELLNER during the cold late winter/early spring 2003 (peak ture insensitivity of light-limited phytoplankton pro- time: Julian day 48; mean SST January–March: 2.7 1C) duction (Tilzer et al., 1986). On the other hand, than during the warm late winter/early spring 2004 heterotrophic processes are highly temperature depen- (peak time: Julian day 98; mean SST January–March: dent, with reaction rates increasing by a factor of 1.8–4 6.7 1C). on a temperature increase of 10 1C. This applies for The examples of later spring blooms after warmer example to algal respiration and to grazing rates of winters come from relatively shallow water bodies. In zooplankton, which form one of the major loss pro- such water bodies, the onset of the spring bloom is cesses for phytoplankton. The grazer community in our independent of the onset of thermal stratification. In experiments consisted of substantial over-wintering deep water bodies, there is a close coupling between the populations of the copepods Pseudocalanus sp. and O. temperature regime and the light availability, which is similis, together with protozoans (ciliates and flagel- the cornerstone of Sverdrup’s (1953) critical depth the- lates) which were present in small amounts in the ory. The second term of the numerator of Eqn (1) inoculum but grew in response to the increasing food becomes negligible under realistic field values for k availability (Aberle et al., 2007). Higher grazer activities and z, thus making Imix inversely proportional to mix- in the warmer mesocosms could be a potential explana- ing depth, which can be several hundred meters in the tion of the decreased accumulation of phytoplankton deep, open ocean while it is restricted by a shallow biomass during the spring bloom. This assumption is seafloor in the German Bight or by the halocline (ca. 10– also consistent with the temperature-dependent shifts 12 m) in the Kiel Bight. Siegel et al. (2002) used satellite in size structure. Copepods feed preferentially on phy- data for chlorophyll and SSTs and oceanographic mod- toplankton 4500–1000 mm3 cell volume (Sommer & els for the North Atlantic to calculate the mixed-layer Stibor, 2002; Sommer & Sommer, 2006), while exerting light intensity. The mixed-layer light intensity at the less grazing pressure on smaller ones, except for chain- onset of the spring bloom was defined as the ‘critical forming nanoplankton. Under summer conditions, light intensity’ (Ic). The Ic-values of Siegel et al. ranged most ciliates feed on nanoplankton, which would make from 0.97 to 1.75 mol photons m2 day1, with an aver- the combined impact of copepods and ciliates on phy- age of 1.3 mol photons m2 day1 and no latitudinal toplankton more or less neutral in terms of size struc- trend, which would have been indicative of physiolo- ture. However, grazing experiments during our first gical temperature effects. Overall, the agreement be- experiment (Aberle et al., 2007) have shown that the tween our and Siegel’s data on light intensities at the late winter/early spring ciliate community also feeds start of the spring bloom (Fig. 2) supports the assump- on microplankton diatoms, which can explain the shift tion of a dominant role of light. The importance of light towards smaller phytoplankton at higher temperatures. can be overlooked in deep water bodies, where the While the shift towards smaller sizes is an imprint of dependence of Imix on thermal stratification makes enhanced grazing at higher temperatures, it also re- temperature a light switch. However, also from some duces food quality for the new copepod generation deep water bodies (e.g. Lake Constance) early spring hatching in spring. While some microplankton diatoms blooms before the onset of thermal stratification have appear to have an inhibitory effect on the hatching of been reported. They occur if the absence of wind leads eggs when fed to adult copepod females (Ianora et al., to the stagnation of the water column and permits an 2003), microplankton diatoms are the dominant food undisturbed residence of phytoplankton near the well- base during the rest of the copepod life cycle (Irigoien lit surface (Tirok & Gaedke, 2007). However, such et al., 2002; Sommer et al., 2005). If the large diatoms are stagnation periods without stabilizing density gradients replaced by nanoplankton, an intermediate trophic are ephemeral and do not withstand wind-induced level consisting heterotrophic protists, mainly ciliates, mixing. It follows that the prediction of future spring will lead to losses in the energy transfer to copepods plankton dynamics in a changing climate is contingent (Sommer et al., 2002) which are the main food source for on a prediction of cloud cover and wind patterns. At planktivorous pelagic fish. Taken together, the warm- present, these predictions are much less certain than ing-induced shifts in phytoplankton size structure, the temperature predictions. decrease of phytoplankton peak biomass, and the higher metabolic demand of copepods at higher temperatures are all a disadvantage for the copepods. Implications for higher trophic levels and for ecosystem A warming-induced shift from large diatoms to pico- functions and nanophytoplankton does not only impair the trans- The weak responsiveness of the timing of the phyto- fer efficiency from primary production to copepod and plankton spring bloom to temperature as such is in fish production but also affects the ‘biological carbon agreement with the generally acknowledged tempera- pump’, i.e. the sequestration of photosynthetically fixed

r 2008 The Authors Journal compilation r 2008 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/j.1365-2486.2008.01571.x CLIMATE CHANGE AND PHYTOPLANKTON SPRING BLOOM 9 carbon dioxide by the ocean, adversely. Diatoms are Gerten D, Adrian R (2001) Differences in the persistency of the considered important agents of carbon export to the North Atlantic Oscillation signal among lakes. Limnology and deep water because they have high sinking velocities, Oceanography, 46, 448–455. tend to aggregate towards the end of blooms to even Hancke K, Glud RN (2004) Temperature effects on respiration faster sinking aggregates, and, if eaten by copepods, and photosynthesis in three diatom-dominated benthic com- contribute to carbon export as fast sinking fecal pellets munities. Aquatic Microbial Ecology, 37, 265–281. Ianora A, Poulet SA, Miralto A (2003) The effects of diatoms on (Smayda, 1971; Smetacek, 1999; Dugdale et al., 2002). If copepod reproduction. A review. Phycologia, 42, 351–363. more of the primary production is channeled to the Ikeda T, Kanno Y, Ozaki K, Shinada A (2001) Metabolic rate of pelagic food web because of decreased phytoplankton epipelagic copepods as a function of body mass and tempera- size, more of the carbon is recycled in the surface waters ture. Marine Biology, 139, 587–596. by protist respiration. The disadvantage for diatoms IPCC (International Panel on Climate Change) (2007) Climate does not only apply to the winter–spring transition Change 2007: The Physical Science Basis. IPCC, Geneva. studied in this article but also applies to summer Irigoien X, Flynn KJ, Harris RP (2005) Phytoplankton blooms. A conditions: stronger vertical stratification because of ‘loophole’ in microzooplankton grazing impact. Journal of global warming will enhance silicate limitation in sur- Plankton Research, 27, 313–321. face waters (Bopp et al., 2005). Thus, the taxonomic Irigoien X, Harris RP, Verheye HM et al. (2002) Copepod hatching effect of global warming might become a positive feed- success in marine ecosystems with high diatom concentrations. Nature, 419, 387–389. back loop by reducing the biological CO2-sequestration in the ocean. Ivleva IV (1980) The dependence of crustacean respiration rate on body mass and habitat temperature. Internationale Revue der gesamten Hydrobiologie, 65, 1–47. Hillebrand H, Du¨ rselen CD, Kischtel K, Pollingher U (1999) Acknowledgements Biovolume calculations for pelagic and benthic microalgae. This study is a contribution to the DFG (German Research Journal of Phycology, 35, 403–424. Foundation) funded priority program 1162 ‘AQUASHIFT’. Tech- Lavaud J, Strzepek RF, Kroth PG (2007) Photoprotection nical assistance by T. Hansen and H. Tomanetz is gratefully capacity differs among diatoms: possible consequences on acknowledged. the spatial distribution of diatoms related to fluctuations in underwater light climate. Limnology and Oceanography, 52, 1188–1194. References Litchman E (2000) Growth rates of phytoplankton under fluctu- ating light. Freshwater Biology, 44, 223–235. Aberle N, Lengfellner K, Sommer U (2007) Spring bloom succes- Matthaus W, Schinke H (1994) Mean atmospheric circulation sion, grazing impact and herbivore selectivity of ciliate com- ¨ munities in response to winter warming. Oecologia, 150, 668– patterns associated with major Baltic inflows. Deutsche Hydro- 681. graphische Zeitschrift, 46, 321–338. Bakun A, Broad K (2003) Environmental ‘loopholes’ and fish Menden-Deuer S, Lessard EJ (2000) Carbon to volume relation- population dynamics: comparative pattern recognition with ships for dinoflagellates, diatoms, and of the protist plankton. focus on El Ninˇo effects in the Pacific. Fisheries Oceanography, Limnology and Oceanography, 45, 569–579. 12, 458–473. Moore CM, Mills M, Milne A, Langlois R, Achterberg EP, Lochte Bopp L, Aumont D, Cadule P, Alvain S, Gehlen M (2005) K, Geider RJ, LaRoche J (2006) Iron limits primary productiv- Response of diatoms distribution to global warming and ity during spring bloom development in the central North potential implications: a global model. Geophysical Research Atlantic. Global Change Biology, 12, 626–634. Letter, 32, 19, Art No. L19606. Prosser CL (1973) Comparative Animal Physiology. Saunders, Brock TD (1981) Calculating solar radiation for ecological mod- Philadelphia. els. Ecological Modeling, 14, 1–19. Riley GA (1957) Phytoplankton of the North Central Sargasso Dimier C, Corato F, Tramontano F, Brunet C (2007) Photoprotec- Sea. Limnology and Oceanography, 2, 252–270. tion and xanthophylls-cycle activity in three marine diatoms. Sand-Jensen K, Pedersen NL, Sndergaard M (2007) Bacterial Journal of Phycology, 43, 937–947. metabolism in small temperate streams under contemporary Dugdale RC, Barber RT, Chai F, Peng TH, Wilkerson FP (2002) and future climates. Freshwater Biology, 52, 2340–2353. One-dimensional ecosystem model of the equatorial Pacific Sieburth J, Smetacek V, Lenz J (1978) Pelagic ecosystem struc- upwellig system. Part II: sensitivity analysis and comparison ture: heterotrophic compartments and their relationship to with JGOFS EqPac data. Deep Sea Research Part II, 49, 2747– plankton size fractions. Limnology and Oceanography, 23, 2768. 1256–1263. Edwards M, Beaugrand G, Reid PC, Rowden A, Jones MB (2002) Siegel DA, Doney SC, Yoder JA (2002) The North Atlantic Spring Ocean climate anomalies and the ecology of the North Sea. Phytoplankton Bloom and Sverdrup’s critical depth hypoth- Marine Ecology Progress Series, 239, 1–10. esis. Science, 296, 730–733. Eppley RW (1972) Temperature and phytoplankton growth in Smayda TJ (1971) Normal and accelerated sinking of phyto- the sea. Fisheries Bulletin, 70, 1063–1085. plankton in the sea. Marine Geology, 11, 105–122. r 2008 The Authors Journal compilation r 2008 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/j.1365-2486.2008.01571.x 10 U. SOMMER & K. LENGFELLNER

Smetacek V (1999) Diatoms and the ocean carbon cycle. Protist, Stenseth NC, Mysterud A, Ottersen G, Hurrell JW, Chan KS, 150, 25–32. Lima M (2002) Ecological effects of climate fluctuations. Smetacek V, Passow U (1990) Spring bloom and Sverdrup’s Science, 297, 1292–1296. critical depth model. Limnology and Oceanography, 35, Straile D (2000) Meteorological forcing of plankton dynamics in a 228–234. large and deep continental European lake. Oecologia, 122, Sommer U (1996) Plankton ecology: the last two decades of 44–50. progress. Naturwissenschaften, 83, 293–301. Straile D, Adrian R (2000) The North Atlantic Oscillation and Sommer U (2002) Experimental systems in aquatic ecology. plankton dynamics in two European lakes – two variations on Encyclopedia of Life Sciences. Art. 3180, www.els.net a general theme. Global Change Biology, 6, 663–670. Sommer U, Aberle N, Engel A et al. (2007) An indoor mesocosm Sverdrup HU (1953) On conditions for the vernal blooming of system to study the effect of climate change on the late winter phytoplankton. Journal du ConseilInternational pour l’Exploration and spring succession of Baltic Sea phyto- and zooplankton. de la Mer, 18, 287–295. Oecologia, 150, 655–667. Tilzer MM, Elbra¨chter M, Gieskes W, Beese B (1986) Light– Sommer U, Gliwicz ZM, Lampert W, Duncan A (1986) The PEG- temperature interactions in the control of photosynthesis in model of seasonal succession of planktonic events in fresh Antarctic phytoplankton. Polar Biology, 5, 105–111. waters. Archiv fu¨r Hydrobiologie, 106, 433–471. Tirok K, Gaedke U (2007) The effect of irradiance, vertical mixing Sommer U, Hansen T, Blum O, Holzner N, Vadstein O, Stibor H and temperature on spring phytoplankton dynamics under (2005) Copepod and microzooplankton grazing in mesocosms climate change: long-term observations and model analysis. fertilised with different Si:N ratios: no overlap between food Oecologia, 150, 625–642. spectra and Si:N influence on zooplankton trophic level. Utermo¨hl H (1958) Zur Vervollkommnung der quantitativen Oecologia, 142, 274–283. Phytoplankton Methodik. Mitteilungen der Internationalen Ver- Sommer U, Sommer F (2006) Cladocerans versus copepods: the einigung fu¨r Theoretische und Angewandte Limnoogie, 9, 263–272. cause of contrasting top-down controls on freshwater and Walther GR, Post E, Convey P et al. (2002) Ecological responses to marine phytoplankton. Oecologia, 147, 183–194. recent climate change. Nature, 416, 389–395. Sommer U, Stibor H (2002) Copepoda Tunicata: the role of three Wehenmeyer GA (2001) Warmer winters: are planktonic popula- major mesozooplankton groups in pelagic food webs. Ecologi- tions in Sweden’s largest lake affected? Ambio, 30, 565–571. cal Research, 17, 161–174. Weyhenmeyer GA, Blenckner T, Pettersson K (1999) Changes of Sommer U, Stibor H, Katechakis F, Sommer F, Hansen T (2002) the plankton spring outburst related to the North Atlantic Pelagic food web configurations at different levels of Oscillation. Limnology and Oceanography, 44, 1788–1792. nutrient richness and their implications for the ratio Wiltshire KH, Manly BFJ (2004) The warming trend at Helgoland fish production: primary production. Hydrobiologia, 484, Roads, North Sea: phytoplankton response. Helgoland Marine 11–20. Research, 58, 269–273.

r 2008 The Authors Journal compilation r 2008 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/j.1365-2486.2008.01571.x