Progress in Oceanography 137 (2015) 456–469
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Progress in Oceanography
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Drivers and effects of Karenia mikimotoi blooms in the western English Channel ⇑ Morvan K. Barnes a,1, Gavin H. Tilstone a, , Timothy J. Smyth a, Claire E. Widdicombe a, Johanna Gloël a,b, Carol Robinson b, Jan Kaiser b, David J. Suggett c a Plymouth Marine Laboratory, Prospect Place, West Hoe, Plymouth PL1 3DH, UK b Centre for Ocean and Atmospheric Sciences, School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich NR4 7TJ, UK c Functional Plant Biology & Climate Change Cluster, University of Technology Sydney, PO Box 123, Broadway, NSW 2007, Australia article info abstract
Article history: Naturally occurring red tides and harmful algal blooms (HABs) are of increasing importance in the coastal Available online 9 May 2015 environment and can have dramatic effects on coastal benthic and epipelagic communities worldwide. Such blooms are often unpredictable, irregular or of short duration, and thus determining the underlying driving factors is problematic. The dinoflagellate Karenia mikimotoi is an HAB, commonly found in the western English Channel and thought to be responsible for occasional mass finfish and benthic mortali- ties. We analysed a 19-year coastal time series of phytoplankton biomass to examine the seasonality and interannual variability of K. mikimotoi in the western English Channel and determine both the primary environmental drivers of these blooms as well as the effects on phytoplankton productivity and oxygen conditions. We observed high variability in timing and magnitude of K. mikimotoi blooms, with abun- dances reaching >1000 cells mL 1 at 10 m depth, inducing up to a 12-fold increase in the phytoplankton carbon content of the water column. No long-term trends in the timing or magnitude of K. mikimotoi abundance were evident from the data. Key driving factors were identified as persistent summertime rainfall and the resultant input of low-salinity high-nutrient river water. The largest bloom in 2009 was associated with highest annual primary production and led to considerable oxygen depletion at depth, most likely as a result of enhanced biological breakdown of bloom material; however, this oxygen depletion may not affect zooplankton. Our data suggests that K. mikimotoi blooms are not only a key and consistent feature of western English Channel productivity, but importantly can potentially be predicted from knowledge of rainfall or river discharge. Crown Copyright Ó 2015 Published by Elsevier Ltd. All rights reserved.
1. Introduction is found within temperate coastal waters of the Pacific (Faust and Gulledge, 2002), the north-west Atlantic (Mahoney et al., Algal blooms involving toxic or otherwise harmful phytoplank- 1990) and the north-east Atlantic off the coasts of Norway (Dahl ton have occurred in many coastal and shelf ecosystems for cen- and Tangen, 1993), Scotland (Davidson et al., 2009), and the Irish turies and can persist as regular predictable or stochastic events Sea (Evans, 1975). It is particularly common in the western (Smayda, 1997). Close to 100 algal species are now considered English Channel where cells usually peak in abundance between ‘harmful’ due to the detrimental effects of large monospecific June and September (Pingree et al., 1975; Holligan et al., 1984; blooms on the marine ecosystem and consequently, human society Garcia and Purdie, 1994). Extensive blooms have been reported (Sournia, 1995); harmful effects can include toxicity (via biotox- in offshore United Kingdom (U.K.) waters in recent years including ins), ichthyotoxicity (via ROS, PUFA & gymnocin which can kill fish the western English Channel in 2003 (Vanhoutte-Brunier et al., but are not dangerous to humans), physical damage, anoxia or 2008), the west coast of Ireland in 2005 (Silke et al., 2005) and in even irradiance reduction. Among these species are many mem- northern Scottish waters in 2006 (Davidson et al., 2009). K. mikimo- bers of the Dinophyceae class including Karenia mikimotoi, which toi blooms can reach high densities of >103 cells mL 1 (>10 mg m 3 Chl a) with dramatic effects for the marine ecosystem (Gentien, 1998). ⇑ Corresponding author. At local to regional scales, reports of coincident finfish, shellfish E-mail address: [email protected] (G.H. Tilstone). and other invertebrate mortalities have been attributed to Karenia 1 Present address: CNRS, Laboratoire d’Oceanographie de Villefranche, 06238 spp. although the extent to which biota and habitats are affected Villefranche-sur-Mer, France. http://dx.doi.org/10.1016/j.pocean.2015.04.018 0079-6611/Crown Copyright Ó 2015 Published by Elsevier Ltd. All rights reserved. M.K. Barnes et al. / Progress in Oceanography 137 (2015) 456–469 457 by the toxicity associated with large blooms is still unclear (Silke effects of K. mikimotoi blooms on a range of zooplankton species et al., 2005). Both ichthyotoxic compounds (Satake et al., 2005) are also analysed. and deoxygenation (Tangen, 1977) have been suggested to cause the observed mortalities although which of these is the main 2. Methods harmful agent remains uncertain. It is no surprise that extensive research is directed toward the detection (Shutler et al., 2012; 2.1. Study site and sampling Yuan et al., 2012) and, to a lesser extent, prediction of Karenia spp. blooms. Importantly, such blooms carry significant effects Station L4 (50°150 N, 4°130 W) is situated in the western English over larger scales, most notably their (temporal/spatial) contribu- Channel, 10 km south of Plymouth within a depth of ca. 50 m tion to ecosystem productivity. While blooms may occur during a (Fig. 1) and is one of Europe’s principal coastal time series stations. short period of a few weeks, the substantial increase in biomass Sampling at this site was established in the early 1900s; the zoo- and primary productivity can heavily dominate the overall season, plankton time-series began in 1988, and phytoplankton and as has been observed for Karenia brevis in West Florida waters chlorophyll a (Chl a) sampling were added in 1992. These initial (Bendis et al., 2004; Hitchcock et al., 2010). measurements have since been supplemented with other hydro- Blooms of K. mikimotoi have been seemingly unpredictable logical and biological measurements (Harris, 2010). To date, sam- events, occurring intermittently in UK waters. The species is ples are collected, when possible, on a weekly basis using a thought to over-winter in low numbers as motile cells awaiting Lagrangian sampling mode whereby the sampling vessel is allowed favourable bloom conditions (Gentien, 1998). Blooms are highly to drift with the body of water once the sampling location has been variable in timing, duration and magnitude and do not occur every reached. year (García-Soto and Pingree, 2009); thus the precursor and opti- Vertical profiles of temperature, salinity, density and fluores- mum blooming conditions of Karenia spp. are poorly understood. cence from a SeaBird SBE19+ CTD have been measured since K. mikimotoi is a slow-growing, shade-adapted species that is occa- 2002. During 2009 water samples were also collected from depths sionally able to outcompete much faster growing diatoms of 0, 10, 25 and 50 m for the measurement of all phytoplankton (Gentien, 1998). While prevailing hydrography (e.g. temperature pigments, absorption and primary production. Under conditions or salinity) may regulate the regional distribution of a particular of vertical heterogeneity in the fluorescence data, additional sam- species and contribute to the timing of the annual/seasonal max- ples were taken at depths delineating strong changes in the verti- ima, it is generally thought that light or nutrient availability deter- cal profile. Water was returned to the laboratory, within 2 h of mines the growth, biomass and duration of local scale blooms. sampling, in 10 L carboys stored within a dark cool-box. Mixed Precursor causes of large K. mikimotoi blooms are suggested to layer depth (MLD) was calculated as the depth at which the differ- include enhanced growth by sunlight-driven phototaxis, rainfall ence with the surface density is greater than 0.125 kg m 3 (Levitus, or benthic-mediated nutrient availability, and concentration pro- 1982). Meteorological measurements including wind speed, wind cesses such as wind-driven advection and frontal systems direction and rainfall have been taken at hourly intervals from (Gentien, 1998). However, these remain to be substantiated or the roof of Plymouth Marine Laboratory (PML) since 2003 (Smyth proven. et al., 2010). L4 is also monitored with autonomous buoys measur- Unravelling the factors that initiate, develop and sustain K. miki- ing temperature, salinity, fluorescence, wind speed and direction motoi blooms in highly dynamic coastal waters is critical to since 2009. Wind data from the L4 buoy show a good correlation improving our capacity to predict (and hence mitigate against) with those taken from the PML roof 13.8 km further north future blooms, but fundamentally requires comprehensive data- (r = 0.74, p < 0.05). sets spanning several years. Offshore time series of hydrological and environmental datasets in the North Atlantic are rare; how- ever, long term sampling for over 19 years has been conducted at 2.2. Nutrients, microscopy and phytoplankton pigments a station in the western English Channel (Southward et al., 2005) where K. mikimotoi blooms are reported to commonly occur. Surface-water phosphate, silicate, nitrate and nitrite concentra- Observations throughout this period have yielded evidence of tions were determined using the methods described by Woodward warming and periods of reduced wind stress (Smyth et al., 2010) and Rees (2001). Samples for phytoplankton enumeration were and changes to the phytoplankton community structure, with collected from 10 m depth as 200 mL subsamples which were notable recent decreases in diatom abundance and increases in drawn directly from the CTD Niskin bottle and fixed immediately dinoflagellates and coccolithophores (Widdicombe et al., 2010). with 2% (final concentration) of Lugol’s iodine solution However, as yet no single study has evaluated the impact of envi- (Throndsen, 1978) and then stored in cool, dark conditions until ronmental variability on K. mikimotoi abundance and therefore analysis by inverted settlement microscopy following established the proximal driver(s) inducing bloom formation. Widdicombe et al. (2010). Samples were gently homogenised and Similarly, the impact of K. mikimotoi on seasonal biomass and pro- a settling volume of 50 mL was then used to enumerate phyto- ductivity, i.e. the relative importance of this key species, is plankton to the nearest species. Cell volumes were calculated using unknown. Both goals are vital in attempting to understand the role approximate geometric shapes and converted to biomass using the that K. mikimotoi may play in coastal ecosystem productivity, par- equations of Menden-Deuer and Lessard (2000). Zooplankton ticularly within the context of a changing climate, whereby future abundance was determined weekly at L4 from vertical tows long-term variations to temperature, wind and rainfall could have (WP2 net with 200 lm mesh) from 50 m depth to the surface, profound effects on ocean productivity. stored in formalin and enumerated following Bonnet et al. (2010) We used a 19-year time series (1992–2010) to determine the and Harmer et al. (2010). frequency and magnitude of K. mikimotoi blooms, and to examine One-litre aliquots were filtered onto 0.47 lm glass-fibre filters the relationships between environmental variability and bloom for pigment analysis. The filters were flash-frozen and stored in liq- formation of K. mikimotoi in the western English Channel. Two very uid nitrogen until analysis in the laboratory. Lipophilic pigments distinct years, including a particularly intense bloom in 2009 and a were extracted into a solution of methanol and apo-carotenate smaller bloom in 2010, were used as case studies to investigate the using an ultrasonic probe following methods outlined by consequences of such K. mikimotoi blooms on photosynthetic activ- Llewellyn et al. (2005), centrifuged to remove filter and cell debris ity and on oxygen saturation in the water column. The potential and analysed using reversed-phase high-performance liquid 458 M.K. Barnes et al. / Progress in Oceanography 137 (2015) 456–469
Fig. 1. Station L4 situated in the western English Channel off the coast of Plymouth and the Tamar estuary. chromatography (HPLC) with gradient elution using techniques baseline flatness of no more than ±0.004 Å units. Detrital absorp- described in Barlow et al. (1997). tion was determined by degrading phytopigments with several drops of 1% sodium hypochlorite directly on the GF/F filters; each filter was maintained in solution for ca. 30–90 min and subse- 2.3. Absorption coefficient of phytoplankton quently rinsed with 50 mL of filtered sea water. Correction for pathlength amplification on the filters and conversion of measured The light absorption coefficient for phytoplankton a (m 1) ph absorbance to the equivalent suspension absorption was per- was determined from 2003 using the methods from Tassan and formed following Tassan and Ferrari (1998). Ferrari (1995) and data from 2009–2010 are used to examine the absorption characteristics during a K. mikimotoi bloom. One-litre samples were concentrated by filtration onto 25 mm GF/F filters. 2.4. Phytoplankton photosynthesis and primary production Absorbance was measured between 350 and 850 nm on a Perkin Elmer k-900 spectrophotometer fitted with a 60 mm spectralon Primary production (at 4–5 depths) was measured during integrating sphere. Zeroing of the instrument was performed with 2009–2010 via photosynthesis–irradiance (P–I) curves using a lin- high-grade spectralon plates at the exit and entrance ports, and a ear photosynthetron with 50 W tungsten halogen lamps, following M.K. Barnes et al. / Progress in Oceanography 137 (2015) 456–469 459
Tilstone et al. (2003), and is used here to understand the potential pooled observations based on environmental variables identified contribution of K. mikimotoi to carbon fixation in the WEC. For each from multiple regression. depth, 16 aliquots of 70 mL were inoculated with 5–10 lCi of 14C-labelled bicarbonate. Samples were maintained at in situ tem- 3. Results perature during the 1.5 h incubations. Samples were then filtered onto a glass-fibre filter (0.47 lm pore size; 25 mm diameter) at a 3.1. Frequency & abundance of Karenia mikimotoi vacuum of not more than 300 mbar below ambient pressure to reduce mechanical stress on cells. Filters were exposed to From 1992–2010, K. mikimotoi was present in samples collected 0.37 g/g fuming hydrochloric acid for 12 h and the beta-activity at 10 m depth throughout the year at concentrations varying from counted using a Wallac 4040 scintillation counter following addi- 0 to >1000 cells mL 1 (Fig. 2A). Peak cell abundance (and hence tion of 4 mL scintillation cocktail. Correction for quenching was bloom conditions) varied greatly both in terms of timing and mag- performed using the external-standard and the channel-ratio nitude of the bloom. Taking all years into consideration, K. mikimo- methods. Natural 12C carbon fixation within each sample was cal- toi was recorded in over half of all observations between June and culated following Tilstone et al. (2003). The equation by Platt et al. September. Peak abundance was usually attained between (1980) describing the light response of photosynthesis was fitted early-July and mid-August during which time K. mikimotoi was to the carbon fixation data using least-squares non-linear regres- present in ca. 90% of all observations. The start of the seasonal sion to determine the photosynthetic parameters PB (the m bloom was taken as an increase in abundance over 5 cells mL 1, light-saturated rate of photosynthesis), aB (the light-limited slope) on the basis that for all years, all increases above 5 cells mL 1 were and b (the rate of photoinhibition). Only data for which the Platt significantly greater than the concentrations of the preceding et al. model could be fitted to 90% (r2 P 0.9) were included in 3 months. K. mikimotoi was recorded during early June for 2003– the subsequent analyses. 2005 but as late as early September for 2001. From 2000–2008, An estimate of the daily-integrated production (PP;mgCm 2 d 1) greatest peak abundances of 458 and 568 cells mL 1 were was subsequently calculated from the photosynthetically-active observed during 2002 and 2005 respectively, yet peak values as radiation (E ), Chl a and the photosynthetic parameters using PAR low as 28 and 0.08 cells mL 1 were found during 2006 and 2008, the spectral model from Tilstone et al. (2003). Integration was car- ried out at hourly steps and 1-m depth intervals from the sea sur- face to the depth experiencing 0.1% of surface irradiance. EPAR was modelled using the approach of Gregg and Carder (1990) modified to include the effects of clouds (Reed, 1977) and using wind speed and percentage cloud cover from the European Centre for Medium Range Weather Forecasting (ECMWF) ERA-40 dataset for the grid point closest to the location of L4, as in Smyth et al. (2010). Chl a was linearly interpolated between depths from the discrete HPLC measurements.
2.5. Oxygen concentrations
For dissolved-oxygen measurements water was carefully siphoned into 70 mL borosilicate bottles and allowed to overflow twice. Winkler reagents (0.5 mL MnSO4 and 0.5 mL NaI-NaOH) were added and the bottle was closed without introducing atmo- spheric air. Samples were stored underwater and were analysed with an automated Winkler titration system to a photometric end- point (Williams and Jenkinson, 1982) within 24 h. Duplicates were taken from October 2009 onward and are presented as the average of both bottles with a mean standard deviation of 0.18 lmol L 1. Oxygen saturation was calculated using the equation of Garcia and Gordon (1992) and the equilibrium constants of Benson and Krause (1984).
2.6. Statistical analysis
The seasonal variability of Chl a, K. mikimotoi abundance and temperature was tested using a one-way ANOVA. Stepwise multi- ple linear regression was used to identify predictors of summer Chl a and K. mikimotoi abundance (restricted to >5 cells mL 1 to only account for blooming periods) from a database of environmental data including temperature, salinity, daily photosynthetically active radiation, wind speed, wind direction (categorised as a per- Fig. 2. Seasonal profiles of Karenia mikimotoi density (cells mL 1; A), total phyto- centage of observations in the predominant southwesterly direc- plankton carbon concentrations (ng C mL 1; B) and the surface Chl a (mg m 3;C)at tion i.e. 180–270 degrees), rainfall, mixed-layer depth and L4 from 1992–2010. Data are shown as crosses (B and C) or by year (A) while phosphate, silicate, nitrate and nitrite concentrations. All data were samples where K. mikimotoi cell densities are greater than 250 cells mL 1 are shown checked for normality using Kolmogorov–Smirnov and either log- as circles (B and C). The 10-day mean is indicated as the continuous line with the standard deviation shown as the light grey area. Bars at the base of the graph or square-root transformed to reduce dominance when necessary. indicate for each ten-day period the percentage of samples where K. mikimotoi was The Mann–Whitney test for differences in medians was used to present (A). The 10-day means of both Chl a (C) and phytoplankton carbon (B) left determine significant differences in K. mikimotoi densities between after subtracting K. mikimotoi specific carbon are shown as the dashed lines. 460 M.K. Barnes et al. / Progress in Oceanography 137 (2015) 456–469 respectively. In the late summer of 2009 cell densities of chlorophyll, while noticeable during July–August, is less than that 1104 cells mL 1 were recorded, almost double the maximum mea- for phytoplankton carbon. sured during the previous 10 years and significantly higher than MODIS Aqua (OC3M) Chl a images (weekly composites) demon- for other years (F = 9.21, p < 0.05). Only in 1997 were comparable strated the geographic extent of the 2009 K. mikimotoi bloom abundances recorded (1094 cells mL 1) though these were (Fig. 3A–D). Prior to the bloom (12–18 August), Chl a concentra- observed a month earlier. The 2009 bloom also occurred much tions up to 30 miles offshore were <1 mg m 3 (Fig. 3A). During later than usual and the high cell densities were maintained for the following week, near-shore Chl a increased along the southern several weeks. Bloom development effectively occurred in just coasts of eastern Cornwall and western Devon reaching concentra- one week from 0.3 cells mL 1 on the 17th August 2009 to the max- tions of up to 5 mg m 3 (Fig. 3B). Between the 26th August and the imum recorded value on the 24th August (1104 cells mL 1) and 1st September the bloom increased in both concentration, reaching subsequently declined to 521, 492 and 20 cells mL 1 in the follow- above 30 mg m 3 in several locations, and in geographical extent, ing three weeks. The interannual variability of K. mikimotoi at L4 is with high Chl a observed as far west as the western tip of highlighted by the stark contrast with 2010, with a maximum of Cornwall and up to 20 miles from the coast (Fig. 3C). Chl a concen- just 158 cells mL 1 occurring on 26th July. No long-term trends trations increased throughout the western English Channel but the in the timing or magnitude of K. mikimotoi abundance were evident bloom was at its peak along the coast. From the 2nd to the 8th of from this dataset. September chlorophyll concentrations were greatly reduced, During bloom periods, K. mikimotoi represented a substantial though some small patches of high-Chl a remained (Fig. 3D). component of the total phytoplankton carbon content of the L4 Thus, during 2009, K. mikimotoi accounted for the highest Chl a phytoplankton community (Fig. 2B). Total phytoplankton carbon concentrations and the highest phytoplankton carbon in the west- across the time series was low during winter months (November ern English Channel. to March; <25 ng C mL 1) and averaged between 50 and 60 ng C mL 1 during spring (mid-April to June), but the highest 3.3. Hydrography phytoplankton carbon concentrations were observed during the summer bloom. From early July to early September phytoplankton In order to understand the causes of variability in Chl a and K. carbon averaged >70 ng C mL 1 with the 10-day mean reaching mikimotoi we examined the hydrography in the western English 118 ng C mL 1 at the end of July. Total-phytoplankton- community Channel. The seasonality of thermal stratification in the study area carbon was highest when K. mikimotoi reached high densities was evident in the vertical temperature profiles and the mixed (>250 cells mL 1); disregarding the contribution from K. mikimotoi layer depth (Fig. 4). As a result of increasing solar irradiance, win- yields a value for the total community of just 48 ng C mL 1 during ter temperatures of ca. 8–10 °C increased during mid-to late spring the summer peak – less than that of the spring bloom period. to temperatures of 12 °C at the surface. During this time, the winter Maximum carbon concentrations of 622 ng C mL 1 and mixing maintained by strong winter winds and cooler air temper- 612 ng C mL 1 were recorded during the peak of the K. mikimotoi ature gave way to an increasingly stratified water column. blooms for 2009 and 1997, respectively. This represents ca. 6 times Mixed-layer depth thus declined to ca. 10 m depth. For a period the mean phytoplankton carbon for those periods. of 50–60 days after initial stratification, a surface to 50 m temper- ature gradient of over 3 °C was observed. Thermal stratification weakened from early August and by September the water column 3.2. Surface chlorophyll-a was completely mixed. High variability in salinity also influenced water-column stratification and the depth of the mixed layer, par- Surface Chl a concentrations in the western English Channel ticularly during the winter months from November to April. From from 1992–2010 showed clear seasonal patterns (Fig. 2C). A clear 2002–2010, surface salinity varied between 33.9 and 35.5. On and prominent annual spring bloom typically peaked during late occasion, e.g. September 2005 and late August 2009, changes in April. Maximum surface Chl a values during the spring bloom aver- salinity of as little as 0.4 resulted in changes in the stratification aged 4.3 (±1.3) mg m 3 (mean ± standard deviation) but ranged during the summer bloom period. between 1.8 and 7.3 mg m 3 throughout the time series. Following low Chl a during late May and June, a succession of sum- 3.4. Drivers of the summer Karenia mikimotoi blooms mer blooms occurred. These summer blooms peaked between late June and late August but varied substantially in timing and magni- Environmental parameters (daily downwelling irradiance, tude between years. Maximum summer Chl a concentration from 3-day mean wind velocity, 3-day mean percentage of south west- 1992–2010 averaged 5.2 (±2.6) mg m 3, and ranged from 2.4 to erly winds, 3-day mean rainfall, nutrient concentrations, 11.7 mg m 3. There was a significant difference between the sea-surface temperature, salinity and mixed-layer depth) that 2009 summer surface Chl a and that of the previous years co-varied with the western English Channel K. mikimotoi blooms (F = 2.56, p < 0.05) with mean summer Chl a of 3.3 mg m 3 for were identified using stepwise multiple regressions performed 2009 while mean values for previous years were 1.6 mg m 3. on both summer surface Chl a and cell densities from 2002–2010 As an indication of the relative contribution of K. mikimotoi to (Table 1). A 3-day mean was used for meteorological variables as total chlorophyll, for periods when K. mikimotoi densities were it sufficiently reduced the variance while not masking the mini- >250 cells mL 1, the mean Chl a concentration was 5.3 mum and maximum range in daily means. Significant regressions (±2.7) mg m 3. Furthermore, from the beginning of June to the were observed between Chl a and both salinity (T = 5.48, end of September ca. 67% of samples with Chl a concentrations p < 0.05) and mixed-layer depth (T = 3.33, p < 0.05), illustrating >4 mg m 3 had associated K. mikimotoi densities exceeding that increases in Chl a corresponded with decreases in salinity 250 cells mL 1. Staehr and Cullen (2003) estimated the mean cellu- and an increase in the mixed layer depth. Salinity explained lar chlorophyll concentrations of K. mikimotoi under high light con- 26.3% of the variance of summer Chl a, while the addition of ditions to be around 4 pg Chl a cell 1. By using this number to MLD explained a further16.7% (total = 43.0%). Wind speed was conservatively estimate the total K. mikimotoi Chl a and subtracting not a significant predictor of Chl a at the 95% level. The same anal- this from the measured chlorophyll we calculated the seasonal ysis was performed on K. mikimotoi using densities over running mean of chlorophyll with the contribution of K. mikimotoi 5 cells mL 1. Significant regressions were observed between cell disregarded (Fig. 2C). The effect of subtracting K. mikimotoi density and 3-day average rainfall (T = 3.26, p < 0.05) with greater M.K. Barnes et al. / Progress in Oceanography 137 (2015) 456–469 461
Fig. 3. MODIS weekly composite Chl a (mg m 3) images of the western English Channel for (A) 12–18 August 2009, (B) 19–25 August 2009, (C) 26 August to 1 September 2009, (D) 2–8 September 2009. The white cross indicates sampling station L4. rainfall corresponding to higher densities. Rainfall alone could depleted during the months of June and July 2009 (Fig. 6A). During explain 25% of the variation in cell densities during K. mikimotoi mid-August silicate increased to ca. 3 lmol L 1, and remained at a blooms. Wind speed was not a significant predictor of K. mikimotoi similar concentration for the next six weeks. The K. mikimotoi at the 95% level. bloom began 7 days after the initial increase in silicate. During that Analyses of salinity, silicate, rainfall and wind speed levels that period, nitrate concentrations remained low (<0.5 lmol L 1) and contributed to K. mikimotoi bloom formation are presented in only increased after the K. mikimotoi bloom had subsided. Fig. 5A–D. K. mikimotoi abundances were significantly higher Rainfall for the three weeks prior to the onset of the bloom ca. (W = 1083, p < 0.05) for the highest pooled-rainfall data 24th August was low with daily totals between 0 and 3 mm (90–100th percentile; mean 3-day rainfall >3 mm) than for lower (Fig. 6B). During the 23rd and 24th of August rainfall totalled rainfall (Fig. 5A). Median and mean abundances were 4.6-fold 13.6 mm. Thus the silicate increase likely reflected an increase in and 1.8-fold higher, respectively, when rainfall exceeded 3 mm. other nutrients through rainfall and riverine input that are then K. mikimotoi abundances were also higher for the lowest 10% of taken up by K. mikimotoi as a bloom forms (and therefore not salinities (<34.82; Fig. 5B) although this was not statistically signif- observable using weekly measurements). Overall wind speed also icant at the 95% level (W = 648, p > 0.05). Increases in the median increased slightly prior to the observed K. mikimotoi increase with and mean abundances under conditions of low salinity were com- mean and maximum wind speeds on the 19th August of 4.2 and parable to those of rainfall at 4.9 and 1.9-fold increases respec- 13.4 m s 1, respectively, while wind speeds were of a similar tively. Average K. mikimotoi abundances were highest for silicate strength on the 24th August and during the following week when concentrations within the 75–90th percentile range corresponding K. mikimotoi was highest (Fig. 6C). to 2.60–3.90 lmol L 1 silicate (Fig. 5C). Abundances were signifi- cantly higher when silicate exceeded 2.60 lmol L 1 (75–100th per- 3.5. Photosynthetic parameters & productivity centile) than when silicate was lower (W = 2024, p < 0.05). K. mikimotoi were consistently recorded at over 300 cells mL 1, when Depth- and time-dependence of the photosynthetic parameters associated silicate was greater than 2.6 lmol L 1. Average 3-day PB (the light-saturated rate of production), and aB (the wind speeds during summer varied between 0.23 and 3.62 m s 1. m light-limited slope) and the chlorophyll-specific light absorption No significant difference (W = 1431, p > 0.05) in average K. mikimo- by phytoplankton at 676 nm wavelength a⁄ during 2009 toi densities was observed for different pooled wind speeds ph and 2010 are presented (Fig. 7A–C). Maximum values were (Fig. 5D). recorded between the end of July and beginning of September Further analysis of the conditions leading to the exceptional 2009 (14.7 mg C [mg chl a] 1 h 1, 0.035 mg C [mg chl a] 1 h 1 2009 bloom is shown (Fig. 6). Silicate and nitrate were almost fully [lmol photons m 2 s 1] 1 and 0.043 m2 mg Chl a 1 respectively). 462 M.K. Barnes et al. / Progress in Oceanography 137 (2015) 456–469
Fig. 4. Annual L4 temperature depth contours (°C) for 2002–2010. Circles represent the mixed layer depth with dark and light circles representing a dominant bearing of salinity and temperature respectively on defining the mixed layer depth.
Table 1 2 1 Significant multiple stepwise regressions of (A) Chl a and (B) Karenia mikimotoi 0.004 and 0.04 m mg chl a but 77% of the observations were 2 1 abundance against daily irradiance, average 3-day wind speed, percentage of south- between 0.01 and 0.03 m mg chl a . During 2009, the maximal aph- westerlies, average 3-day rainfall, sea surface temperature, salinity, mixed layer depth ⁄ values were recorded during the K. mikimotoi bloom and particu- and nutrient concentrations. p: level of significance of the slopes; n: number of larly at 25 m and 50 m depth during the decline of the bloom. samples; df: degrees of freedom. During the 2010 K. mikimotoi bloom, values were not particularly R2 = 0.43 df = 35 Coeff. Tpelevated and the annual maximum occurred during the spring (A) Chl a (summer; n = 46) Phaeocystis bloom. Intercept 16.250 During 2009, Chl a values showed marked differences from the Salinity 0.459 5.48 p < 0.001 average seasonal cycle for the previous years (Fig. 2C). Winter sur- Mixed layer depth 0.013 3.33 p = 0.003 face Chl a values for 2009 were below 1 mg m 3 and values only 3-day wind speed 0.220 p = 0.078 exceeded 1 mg m 3 by late April, considerably later than for the R2 = 0.31 df = 29 Coeff. Tp previous years. There was also a substantial increase in total water 1 (B) Karenia (>5 cells mL ;n= 40) column Chl a during the K. mikimotoi bloom from 24th August to Intercept 1.285 7th September (Fig. 7E). Surface Chl a concentrations peaked at 3-day rainfall 0.135 3.26 p = 0.001 3 3-day wind speed 0.240 1.83 p = 0.075 6.7 mg m on the 24th August. However, although total water col- umn Chl a on the 24th August was 126 mg m 2, it was consider- ably higher on the 1st and 7th of September reaching 239 and B 1 1 202 mg m 2 respectively. During this period, Chl a was highest at For 82% of the time Pm was lower than 4 mg C [mg Chl a] h , but 3 increased for brief periods particularly in surface waters. Highest 10 and 25 m reaching 6.9 and 7.6 mg m respectively. Total water values were recorded at the peak of the 2009 K. mikimotoi bloom column primary production varied by almost two orders of magni- 2 1 at a depth of 10 m, while the water column mean on 24th tude from 24 mg C m d during the early winter to 2 1 August was 7.3 mg C [mg Chl a] 1 h 1. Values for aB varied compa- 1856 mg C m d during summer (Fig. 7D). Primary production B 1 1 was relatively low during spring and highest during the summer rably to Pm with values lower than 0.02 mg C [mg Chl a] h [lmol photons m 2 s 1] 1 for most of the time series and a similar period from late July to late August, reaching a maximum when proportional increase in aB during July and August 2009. An addi- the surface Chl a concentrations reached their peak on the 24th tional peak of 0.055 mg C [mg Chl a] 1 h 1 [lmol photons m 2 August. The annual carbon fixation at L4 was estimated at 2 s 1] 1 occurred at 25 m during the brief 2010 K. mikimotoi bloom. 142 g C m . Therefore, of the total annual production, 41% was The 2009 peak in aB however occurred in late July, a month earlier contributed from the 6-week period between 26th July and 7th B ⁄ September with 13% from between 20th August and 7th than for Pm. Values of aph showed ten-fold variations between M.K. Barnes et al. / Progress in Oceanography 137 (2015) 456–469 463
Fig. 5. Box and whisker plots showing K. mikimotoi abundance (cells mL 1) under different pooled environmental conditions of 3-day mean rainfall (mm; A), salinity (B), silicate (lmol L 1; C) and 3-day mean wind speed (m s 1; D). For each plot the abundance data are grouped according to the environmental variable. The boxes, from left to right, encompass the pooled environmental data for the 0–50, 50–75, 75–90, 90–100 percentile ranges with the highest percentile representing the highest rainfall, silicate and wind speed but the lowest salinity. The upper and lower limits to each box represent the first and third quartile respectively, while also shown are the median (bisecting line), mean (circles) and minimum and maximum values (vertical bars). The results of the corresponding Mann–Whitney test for differences between medians are shown for each graph. For A and B the test is between the 0–90 and 90–100 percentile grouped data while for C and D the groups tested were 0–75 and 75–100% (as indicated by the vertical dashed line).
September during the bloom of K. mikimotoi. By contrast, only 16% oversaturation of 7%. By the following week on the 14th of the annual carbon fixation occurred during April and May. September dissolved oxygen concentrations throughout the water No large bloom in K. mikimotoi was observed during 2010 and column returned to 240–253 lmol L 1 (94–98% saturation) and maximum concentrations of 158 cells mL 1 were recorded. steadily increased over the next 3 months in accordance with Accordingly, very little photosynthetic biomass was observed dur- decreasing temperature. During the bloom, the water- column ing summer 2010 with mean and peak chlorophyll of 44.4 and inventory of oxygen decreased from 12.5 mol m 2 on 24th 65.8 mg m 2 respectively. Less than 24% of the total annual pro- August to 11.7 and 11.9 mol m 2 on 1st and 7th of September, duction occurred between 26th July and 9th September 2010, yet respectively. Although 11.7 mol m 2 is the minimum recorded peak production of 1279 mg C m 2 d 1 occurred on 26th July dur- during 2009, similar values (11.9 mol m 2) were observed in July ing the peak in K. mikimotoi abundance, despite far greater prior to the bloom, suggesting surface production during the bloom water-column chlorophyll during April–May when large numbers helps to offset deeper oxygen depletion. The effect of K. mikimotoi of Phaeocystis sp. were recorded. on oxygen concentrations was much less marked in 2010, with a slight increase in surface concentrations on 26th July reaching an 3.6. Effects of Karenia bloom on oxygen saturation & zooplankton oversaturation of 16%, equalling the annual maximum. Unlike the abundance more extensive bloom of 2009, there was no immediate decrease in oxygen concentration following the 2010 peak in K. mikimotoi Both the 2009 and 2010 K. mikimotoi blooms had noticeable abundance, though by 31st August oxygen concentrations at effects on the oxygen concentrations of the water column. Prior 50 m depth had decreased to 219 lmol L 1 from the April maxi- to the 2009 K. mikimotoi bloom, dissolved oxygen concentrations mum of 332 lmol L 1. were relatively low in deeper waters where concentrations were The effect of K. mikimotoi on zooplankton abundance was also ca. 232 lmol L 1 while surface concentrations were examined over the 19-year time series (Fig. 8). Zooplankton abun- 259 lmol L 1. During the bloom, oxygen concentrations increased dance at L4 exhibited characteristic seasonal variability with low in the upper 10 metres, reaching 268 lmol L 1 on the 1st abundance during January–February, followed by an increase in September. However, concentrations deeper in the water column March (to peak during early April) and a subsequent decrease until were reduced to minima of 196 and 192 lmol L 1 on the 1st and July. From mid-July to September, mean zooplankton abundance 7th of September, respectively. This represents a minimum satura- was 22% higher than during the preceding two months suggesting tion of ca. 74% at 50 m depth while the surface waters showed an increase following the late-summer phytoplankton blooms. 464 M.K. Barnes et al. / Progress in Oceanography 137 (2015) 456–469
parvus, Acartia clausi and Temora longicornis exhibited higher aver- age abundances following a K. mikimotoi bloom, whilst Calanus hel- golandicus and Pseudocalanus elongatus showed lower average abundances (Table 2). For each taxa however, T-Tests showed that zooplankton abundances in the two weeks following a K. mikimotoi bloom were not significantly different to those during the rest of the summer months.
4. Discussion
4.1. Frequency & magnitude of K. mikimotoi blooms in the western English Channel
From 1992–2009 there has been a decrease in diatom abun- dance and an increase in certain dinoflagellates in the western English Channel (Widdicombe et al., 2010). Decadal-scale changes in phytoplankton abundance and community structure have also been recorded in the North Atlantic (Reid et al., 1998; Richardson and Schoeman, 2004; Hinder et al., 2012) and in the North Sea (McQuatters-Gollop et al., 2007). HABs in particular are thought to be increasing in occurrence worldwide (Anderson et al., 2002) and recent evidence has revealed a long-term increase in Karenia brevis in Florida (USA) associated with increased anthropogenic nutrient availability (Brand and Compton, 2007). Relatively little is known about the temporal variability of Karenia mikimotoi despite exhibiting a widespread distribution. Analysis of the western English Channel time-series (1992– 2010) demonstrated high variability in the timing and magnitude of K. mikimotoi blooms. Peak abundance typically occurs between mid-June to late-August and contributes a substantial proportion of the total Chl a and carbon concentrations. Subtracting the esti- mated contribution of K. mikimotoi from total phytoplankton car- bon results in as much as a 50% reduction in the 10-day mean phytoplankton carbon concentrations. No other single species has been observed to have such an influence on coastal phytoplankton carbon or Chl a at L4 for such a portion of the year. We also found no significant relationships between average annual K. mikimotoi and other species, suggesting that K. mikimotoi neither co-occurs with (positive relationship) nor inhibits (negative relationship) other species. Our observations suggest that K. mikimotoi may have an important ecological function in the western English Channel acting as an important intermediary in the carbon cycle. No clear long-term trend in K. mikimotoi abundance has been observed at station L4, possibly due to the inherent interannual variability and short dataset (see also Widdicombe et al., 2010). Such high variability in abundance has only previously been identified using Fig. 6. Time series of silicate and nitrate (lmol L 1; A), rainfall (mm, B) and wind non-specific satellite imagery (García-Soto and Pingree, 2009)or speed (m s 1; C) during 2009. Weekly silicate (crosses; left axis) and nitrate during a much shorter time-series (Kelly-Gerreyn et al., 2004). (squares; right axis) measurements are shown for the entire year. Hourly rainfall The late summer K. mikimotoi bloom in 2009 was the largest (crosses; left axis) and daily totals (squares; right axis) are shown from 5th August to 9th September. Hourly wind speed (crosses) and daily averages (squares) are recorded since 1992 and had Chl a, abundance and shown for the same period. Shaded grey areas represent the period of the bloom (A) carbon-biomass anomalies. This bloom was not constrained to sta- and the timing of the first observed K. mikimotoi high density on 24th August (B and tion L4 and the Tamar estuary but occurred along the English coast C). as far west as the Helford estuary and as far east as the Avon estu- ary. Maximum cell abundances of 200–700 cells mL 1 were recorded in the Helford, Fal & Yealm estuaries between 11th and Zooplankton abundance at station L4 actually decreased in the 25th of August (Coates et al., 2009; Fig. 1). The densities recorded month following the start of the 2009 K. mikimotoi bloom. at L4 were close to the maximum recorded in the western English Zooplankton abundance was <2000 m 3 on the 7th and 14th of Channel in recent years, when a K. mikimotoi bloom reached September (44–50% less than seasonal means), whilst the mean 1371 cells mL 1 in 2003 (Vanhoutte-Brunier et al., 2008) and den- abundance for May–July was 4700 m 3. However, the longer sities above 1500 cells mL 1 were observed in the western English time-series reveals no statistical difference in total zooplankton Channel in 1981 (Jordan and Joint, 1984) and in 1987 (Garcia and abundance between samples taken during or after a K. mikimotoi Purdie, 1994). The rapid increase of the bloom over a one-week bloom or at any other time during the months of July– period and the relatively short duration of one to two weeks at September. The relationships between individual zooplankton spe- L4 are consistent with other observations (Davidson et al., 2009). cies was also analysed in a range of other species: Paracalanus It must be noted that the cell counts were from 10 m only, and M.K. Barnes et al. / Progress in Oceanography 137 (2015) 456–469 465
B 1 1 B 1 1 2 1 1 ⁄ Fig. 7. Depth contour plots (0–50 m) of the photo-physiological parameters Pm (A; mg C [mg Chl a] h ), a (B; mg C [mg Chl a] h [lmol photons m s ] ), aph(676) (C; m2 mg chl a 1), daily primary production PP (D; mg C m 3 d 1), Chl a (E; mg m 3) and dissolved oxygen (F; lmol L 1) during 2009 and 2010. Depth-integrated (0–50 m) production (mg C m 2 d 1), Chl a (mg m 2) and oxygen (mol m 2) are indicated on sections D–F as the thick line.
near and at the thermocline (Holligan et al., 1984) in the latter stages of the 2009 bloom (Fig. 7E) and can also migrate through the water column.
4.2. Causes of bloom development
Understanding the factors influencing the development of K. mikimotoi blooms is an important step towards predicting high-magnitude HABs. Mixed-layer depth was identified as a dri- ver of Chl a biomass during the summer months at station L4, but the largest proportion of the variability of summer Chl a was explained by salinity (Table 1), and a substantial proportion Fig. 8. Zooplankton abundance (cells m 3) at L4 from 1988–2010. Running 10-day (25%) of variability of K. mikimotoi abundance could be explained mean (thick black line), standard deviation (grey area) and data from 2009 (dashed by variance of rainfall. Only the highest levels of rainfall (>3 mm) line). Insert shows box plots (see Fig. 5) showing zooplankton abundance during a K. mikimotoi bloom (>250 cells mL 1; ‘‘Bloom’’), in the three weeks after (‘‘After’’), and lowest salinities (<34.82) were associated with and at any other time (‘‘Other’’). significantly-higher densities of K. mikimotoi. In contrast to general phytoplankton bloom formation, K. mikimotoi abundance showed no relationship with changing mixed-layer depth. Further analysis of parameter levels that triggered K. mikimotoi blooms suggested Table 2 1 Zooplankton abundance as average cells m 3 ca. 50 m from vertical hauls before and that silicate concentrations over 2.6 lmol L were associated with during blooms of Karenia mikimotoi and outside of bloom periods (other). ‘Bloom’ is significantly-higher cell densities. K. mikimotoi has been shown to defined as the period when Karenia mikimotoi abundance was >250 cells mL 1; ‘after’ be ichthyotoxic, detrimental to the growth of other algae, and is the three weeks following the last ‘bloom’ observation. Individual zooplankton limiting the growth of diatoms at K. mikimotoi concentrations over species are given in italics. 1 cell mL 1 (Arzul et al., 1993). Thus, the combined facts that Taxa After Bloom Other K. mikimotoi does not readily take up silicate and limits the Total Zooplankton 3911 3449 3082 concentrations of diatoms that do, render silicate a potential tracer Calanus helgolandicus 128 125 146 for nutrient input. Pseudocalanus elongates 151 248 259 Station L4 is characterised by summer nutrient depletion Paracalanus parvus 278 131 224 Oithona spp. 344 320 317 (Smyth et al., 2010). All variables correlating with increased K. Temora longicornis 839 414 385 mikimotoi abundance can be linked to nutrient-supply, i.e. Acartia clausi 316 253 206 increased nutrient concentrations via increased rainfall (leading to low-salinity high-nutrient riverine outflow). Despite its distance from the coast, previous studies have demonstrated the effects of we may have therefore under-sampled phytoplankton populations riverine discharge on the hydrography at station L4 and surround- within the 50-m water column. This is particularly likely for spe- ing waters (Siddorn et al., 2003). Estimates based on salinity data cies such as K. mikimotoi which can exhibit sub-surface blooms (using a conservative threshold of 34.9) indicate that during the 466 M.K. Barnes et al. / Progress in Oceanography 137 (2015) 456–469 historical K. mikimotoi 3-month blooming period, Tamar River Fig. 7E, a large portion of the biomass and abundance could have water reaches L4 for 12 days on average each year (Siddorn et al., been missed. Therefore it is possible that the rapid increase in cell 2003). Our observations suggest that increases in rainfall and the densities was due to vertical advection or migration of the popula- associated decreases in salinity coupled with increased nutrient tion. To verify this, future studies should collect phytoplankton concentrations (as traced by silicate) may have provided the pre- counts at a higher resolution, both vertically and temporally, which cursor conditions for K. mikimotoi bloom formation. However, would enable analysis of the effects of fronts, thin layers and tidal riverine outflow could provide sufficient nutrients in the surface cycles on K. mikimotoi blooms. Even so, the time-series data sug- layer for K. mikimotoi growth through two mechanisms (i) directly gest that the K. mikimotoi bloom was initiated in coastal waters through nutrient-rich river water and (ii) indirectly through by a rapid increase in nutrient-rich riverine outflow. changes in the buoyancy structure leading to increased nutrient Understanding the causes of such blooms is important, particu- diffusion across the nutricline. As K. mikimotoi is a motile species, larly in the context of current climate change predictions whereby increasing the nutrient diffusion may give it an advantage, long-term changes in environmental conditions could lead to an although our data (surface nutrients only) cannot distinguish increase in certain HAB species (Smayda, 1997). Relating harmful between these two processes. Nutrient-rich freshwater pulses algal blooms to a more-easily-detectable environmental variable from the Tamar River outflow, as a result of intense precipitation, could provide an early-warning system indicating not only bloom have been shown to induce increased nitrate (Rees et al., 2009). appearance but also the likelihood of harmful cell densities. The K. mikimotoi is thought to have a nitrogen content ranging between observed link between K. mikimotoi cell density and rainfall 40 to 160 pg N cell 1 (Dahl et al., 1987). With a cell density of >3 mm and salinity <34.82 would suggest that these levels could 1104 cells mL 1, and using a mean of the published cellular nitro- be used to predict the occurrence of K. mikimotoi. Studies off the gen range, the maximum nitrogen requirement of the 2009 L4 western and southern coasts of Ireland have suggested a link bloom at its peak was calculated as 8 lmol L 1 nitrogen. This is between low salinity or heavy rain and increased Karenia out- in the mid-range of winter-nutrient-maximum levels of total nitro- breaks (Raine and McMahon, 1998; O’Boyle, 2002). The onset of gen compounds (nitrate, nitrite and ammonia) at L4 Karenia blooms in Omura Bay in Japan were also linked to (7–12 lmol L 1; Rees et al., 2009). Our data thus suggest that these rain-runoff events (Smayda, 2004). In comparing two consecutive short-duration freshwater pulses were able to alleviate nutrient years, Kelly-Gerreyn et al. (2006) observed that the year (2003) limitation and sustain large blooms that may become the domi- of a K. mikimotoi bloom event at the southern entrance to the west- nant feature of the annual phytoplankton cycle. There was a partic- ern English Channel coincided with fresher, warmer surface ularly large bloom in 2012 associated with high spring rainfall (Tait waters, lower wind stress and a shallower mixed-layer depth. et al., 2015), though summer biomass of K. mikimotoi was low. We found a strong positive relationship between rainfall and There may be other factors influencing the magnitude of the K. mikimotoi abundance. In contrast, Davidson et al. (2009) found K. mikimotoi that were not significant from our analyses such as a negative association between rainfall and abundance but this the phytoplankton community and species succession prior to may be explained by a diluting effect exceeding any additional blooms of Karenia spp. It would be interesting to test the stimulated growth. Climatic variations leading to increased relationships given in Table 1 to assess their capacity at predicting episodic rainfall in the summer may lead to greater occurrence of K. mikimotoi blooms at L4 and other coastal sites. K. mikimotoi in the future in temperate coastal seas. Another mechanism that may have contributed to the unusu- ally large-scale bloom in 2009 is wind-driven advection from 4.3. Effects and significance of K. mikimotoi offshore waters. Most of the previously reported blooms of K. mikimotoi have been observed further offshore in the southern The causes for such major phytoplankton blooms are of partic- or central regions of the western English Channel (e.g. ular concern when considering the environmental impact of HABs Vanhoutte-Brunier et al., 2008). The increase in abundance of on coastal ecosystems, particularly in terms of pelagic and benthic K. mikimotoi cells, from 0.3 to 1104 cells mL 1 in one week, would communities and water-column biogeochemistry. Primary produc- indicate a minimum growth rate (assuming exponential growth tion during 2009 at L4 was observed to be highest during the sum- and no losses) of 2.93 d 1. This is far greater than the 0.3–1.0 d 1 mer months (July to August, Fig. 7D) and during late August 2009 it range of growth rates published by Gentien (1998) for K. mikimotoi. was higher than previously observed at L4. The light-saturated rate B Such growth rates have never been conclusively demonstrated for of photosynthesis Pm was highest during the K. mikimotoi bloom any dinoflagellate, however and such rates could be a physiological while the light-limited slope aB was relatively low. Holligan et al. impossibility. The increase in cell number from 0.3 to (1984) measured primary production at a frontal station in the 1104 cells mL 1 could suggest that populations have been missed western English Channel from late July 1981, during a K. mikimotoi due to the single depth sampling. bloom. Although the density of that bloom is not known, Chl a Strong southwesterly winds were observed prior to and during concentrations of 54.8 mg m 3 indicate high cell numbers. the bloom, but this was the prevalent wind direction for this Maximum surface-water carbon-assimilation rates were 1.7– region, and indeed no relationship between K. mikimotoi and wind 2.8 mg C [mg Chl a] 1 h 1 with total carbon fixation of direction was observed. It was clear from satellite imagery that the 152 mg C m 2 h 1, less than half of the maximum annual carbon bloom originated in nearshore waters. It was therefore considered fixation recorded in spring (Jordan and Joint, 1984). A study of unlikely that the observed relationship between wind speed and the central western English Channel during a K. mikimotoi bloom B K. mikimotoi abundance was only due to onshore advection. The in July 1987 found Pm to vary between 0.6 and 2.3 mg C [mg Chl 1 1 B increase in K. mikimotoi abundance could indicate that the growth a] h (Garcia and Purdie, 1994) while the Pm of cultured popu- rate was in fact higher than previously recorded by Gentien (1998). lations has been observed at 1.22 (±0.27) mg C [mg chl a] 1 h 1 However, previous observations have suggested that K. mikimotoi (Garcia and Purdie, 1992). These values are considerably lower B develops at or directly below the thermocline (Holligan et al., than the maximum Pm measured during the 2009 L4 bloom 1984) particularly at frontal regions between well-mixed and (0.8–14.7 mg C [mg Chl a] 1 h 1). However, studies on Karenia brevis B stratified waters (Pingree et al., 1977). Furthermore, under condi- have found large variations in Pm from 0.29 to 20 mg C [mg Chl tions of reduced stratification, K. mikimotoi may migrate vertically a] 1 h 1 (Bendis et al., 2004), and the values observed during with a daily range of up to 15 m (Koizumi et al., 1996). Only phy- this study for K. mikimotoi are within this range. The toplankton counts from 10 m were available here, but based on chlorophyll-specific light absorption efficiency of phytoplankton M.K. Barnes et al. / Progress in Oceanography 137 (2015) 456–469 467 also showed a peak during the K. mikimotoi bloom albeit during the life including microalgae, marine fauna, fish and seaweeds both in second week of the bloom, which would suggest that K. mikimotoi the Irish Sea (Silke et al., 2005) and off the coast of Scotland cells displayed a higher ability to absorb light. The observed associ- (Davidson et al., 2009). Monitoring of Karenia spp. is necessary ation between a particular species and changing photosynthetic for precautionary, management and predictive purposes, including properties suggests that community structure caused greater vari- the reduction of bloom associated economic losses (Heil and ability in photosynthetic parameters compared to environmental Steidinger, 2009). constraints (as observed in several studies on oceanic phytoplankton The high levels of oxygen depletion toward the end of the communities e.g. Bouman et al., 2005). bloom raise the question of whether the high productivity associ- Productivity of K. mikimotoi blooms is poorly understood. ated with K. mikimotoi is not being grazed by zooplankton. While a However, early non-specific satellite analyses have suggested a large phytoplankton bloom tends to induce a subsequent rapid potential contribution to the annual productivity of between increase in zooplankton at L4 (Widdicombe et al., 2010), zooplank- 28% and 47% (Holligan et al., 1983). Productivity during the ton abundance at station L4 actually decreased in the month fol- 2009 K. mikimotoi bloom was initially high, which might be lowing the start of the K. mikimotoi bloom. Palatability of Karenia expected due to high photosynthetic biomass, but was much brevis has previously been questioned due to detrimental effects lower as the bloom progressed despite persistently high Chl a to copepod survival, growth and behaviour (Turner and Tester, and K. mikimotoi concentrations. It is possible that phytoplankton 1997). However, high grazing rates of two copepod species during the bloom were light-limited, which can be explained by (Calanus helgolandicus and Acartia clausi) during a 2002 K. mikimo- the high photosynthetic biomass recorded during the bloom. A toi bloom has also been observed (Fileman et al., 2010). Our data high phytoplankton biomass concentrated in the upper water col- indicates that K. mikimotoi blooms did not significantly affect range umn would lead to shading of the populations beneath and sub- of zooplankton species at L4 over the 19 year time series. Large stantially reduce light levels until they become limiting. However, Karenia spp. blooms, such as in 2009, could nonetheless have a K. mikimotoi biomass was relatively low during 2010 and, despite considerable impact on coastal fisheries (Silke et al., 2005; Coates the bloom contributing a far lower percentage of the total annual et al., 2009; Davidson et al., 2009). Economic losses from a moder- carbon fixation than for 2009, the bloom coincided with the max- ate bloom in China in 1998 were estimated at US$ 40 million (Lu imum observed daily water column production for 2010. By util- and Hodgkiss, 2004), such that remediation may outweigh the ising the absorption-based production model of Barnes et al. impact cost as was recently observed for Phaeocystis pouchetii (2014, 2015) produced a longer time-series of production at L4 (Lancelot et al., 2011). Although the total variance explained by from 2003 to 2010. In half of those years (2003, 2004, 2005 environmental variables in this study remains relatively low, by and 2009), a peak in surface production over 100 mg C m 3 d 1 expanding existing monitoring databases and combining phyto- was associated with a dominant bloom of K. mikimotoi, and plankton and meteorological datasets we can hope to improve K. mikimotoi was a significant predictor of surface production the predictive power of such empirical relationships between during the 8 year time series. These results suggest K. mikimotoi K. mikimotoi and rainfall. Further studies on the palatability of blooms significantly contribute to carbon fixation at the L4 K. mikimotoi to zooplankton are required, so that the fate of carbon station. transfer from large blooms through the coastal food web is fully The productivity of the 2009 K. mikimotoi bloom could be understood. Dahl and Tangen (1993) showed that only by regular observed in the oxygen over-saturation in the surface layer during monitoring and analyses such as those presented here, can we the first two weeks of September, but it is the substantial hope to manage and mitigate the occurrence and effects of harmful under-saturation in the deeper waters which highlights a more algal blooms such as K. mikimotoi. This study has identified a novel immediate cause for concern. The observed 26% under-saturation relationship between K. mikimotoi and environmental variables in the deepest waters suggests that as the bloom developed and and identified key periods where significant bloom initiation is decayed, oxygen was being depleted at depths below the seasonal likely that may serve towards the goal of improved monitoring; thermocline. The observed deoxygenation was due to hetero- in particular as the Western Channel Observatory continues to trophic bacterial and zooplankton respiration. Silke et al. (2005) operate and collect data. recorded supersaturation during daylight hours and slight deple- tion during darkness suggesting diurnal variations, however, in Acknowledgements this study, depletion was recorded during daylight. Observations by Garcia and Purdie (1994) during a K. mikimotoi bloom in 1987 We would like to thank all who contribute to the Western indicated a significant (19%) depletion in oxygen saturation. Our Channel Observatory, in particular to D. Cummings and the crews results provide an estimate of total oxygen depletion in the water of Plymouth Marine Laboratory’s RV Quest and the Marine column. At L4, the largest measured biological oxygen depletion Biological Association’s RV Sepia who collect the weekly 2 equates to a reduction of 1.0 mol m relative to 100% saturation, time-series samples. We would also like to thank Ruth Airs for phy- though this could be much higher in hours of darkness due to toplankton pigment data quality control, E. Malcolm Woodward for reduced production. Although an under-saturation of this level is nutrient data, Rachel Hammer for zooplankton data and the Natural not thought to be harmful for the benthic communities at L4, in Environment Research Council (NERC) Earth Observation Data slightly shallower waters the same K. mikimotoi biomass would Acquisition and Analysis Service (NEODAAS) for their role in pro- lead to much more concentrated oxygen depletion. During cessing satellite imagery. We would like to thank the European August/September 2009 mass fish kills and macrobenthic animal Centre for Medium Range Weather Forecasts (ECMWF) who sup- mortalities recorded in several Cornish estuaries (e.g. Fal estuary) plied the initial atmospheric data. This work was supported by the were attributed to the oxygen depletion thought to be caused by Western Channel Observatory (WCO) as funded under the NERC K. mikimotoi blooms, and several commercial fisheries had to be National Capability. M.B. acknowledges financial support from a shut down for several weeks (Coates et al., 2009). Karenia spp. NERC studentship (PhD/0710/NERC). J.G. thanks NERC for support has long been known to display slow-acting toxicity (Chang, through SOFI studentship (NE/F012608/1). GHT was supported by 2011) and to have either detrimental effects on growth (Arzul the European Union funded contract Information System on the et al., 1993) or to cause direct mortalities of a wide range of marine Eutrophication of our Coastal Seas (ISECA) (Contract no. 468 M.K. Barnes et al. / Progress in Oceanography 137 (2015) 456–469
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