Seasonal and interannual variation of the ...

Seasonal and interannual variation of the phytoplankton and copepod dynamics in Liverpool Bay Naomi Greenwood, Rodney M. Forster, Veronique Créach, Suzanne J. Painting, Anna Dennis, Stewart J. Cutchey, Tiago Silva, David B. Sivyer, et al. Ocean Dynamics Theoretical, Computational and Observational Oceanography ISSN 1616-7341 Ocean Dynamics DOI 10.1007/s10236-011-0500-x

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Author's personal copy Ocean Dynamics DOI 10.1007/s10236-011-0500-x

Seasonal and interannual variation of the phytoplankton and copepod dynamics in Liverpool Bay Naomi Greenwood & Rodney M. Forster & Veronique Créach & Suzanne J. Painting & Anna Dennis & Stewart J. Cutchey & Tiago Silva & David B. Sivyer & Tim Jickells

Received: 21 March 2011 / Accepted: 10 October 2011 # Her Majesty the Queen in Right of Britain 2011

Abstract The seasonal and interannual variability in the phytoplankton community in Liverpool Bay between 2003 and 2009 has been examined using results from high frequency, in situ measurements combined with discrete samples collected at one location in the bay. The spring phytoplankton bloom (up to 29.4 mg chlorophyll m−3) is an annual feature at the study site and its timing may vary by up to 50 days between years. The variability in the underwater light climate and turbulent mixing are identified Responsible Editor: Claire Mahaffey This article is part of the Topical Collection on the UK National Oceanography Centre’s Irish Sea Coastal Observatory Electronic supplementary material The online version of this article (doi:10.1007/s10236-011-0500-x) contains supplementary material, which is available to authorized users. N. Greenwood (*) : R. M. Forster : V. Créach : S. J. Painting : S. J. Cutchey : T. Silva : D. B. Sivyer Centre for Environment Fisheries and Aquaculture Science (Cefas), Pakefield Road, Lowestoft, Suffolk NR33 0HT, UK e-mail: [email protected] A. Dennis National Oceanography Centre, Southampton, European Way, Southampton SO14 3ZH, UK T. Jickells Laboratory of Global Marine and Atmospheric Chemistry, School of Environmental Sciences, University of East Anglia, Norwich NR4 7TJ, UK Present Address: S. J. Cutchey Gardline Geosurvey Limited, Endeavour House, Admiralty Road, Great Yarmouth, Norfolk NR30 3NG, UK

as key factors controlling the timing of phytoplankton blooms. Modelled average annual gross and net production are estimated to be 223 and 56 g C m−2 year−1, respectively. Light microscope counts showed that the phytoplankton community is dominated by diatoms, with dinoflagellates appearing annually for short periods of time between July and October. The zooplankton community at the study site is dominated by copepods and use of a fine mesh (80 μm) resulted in higher abundances of copepods determined (up to 2.5×106 ind. m−2) than has previously reported for this location. There is a strong seasonal cycle in copepod biomass and copepods greater than 270 μm contribute less than 10% of the total biomass. Seasonal trends in copepod biomass lag those in the phytoplankton community with a delay of 3 to 4 months between the maximum phytoplankton biomass and the maximum copepod biomass. Grazing by copepods exceeds net primary production at the site and indicates that an additional advective supply of carbon is required to support the copepod community. Keywords Primary production . Grazing . Phytoplankton . Zooplankton . Liverpool Bay . Coastal

1 Introduction Phytoplankton blooms in coastal environments typically occur due to changes in physical forcing factors which include weather, tides, nutrient inputs and anthropogenic disturbance (Cloern 1996). In coastal environments, complex interactions exist between the land, open ocean and climate and long-term datasets are required to begin to understand the dynamics and forcing factors at any given site (Cloern and Jassby 2010; Eloire et al. 2010; Gameiro and Brotas 2010; Widdicombe et al. 2010; Wiltshire et al.

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2008). Recent estimates of global marine primary production range between 40 and 60 Pg C year−1 (Carr et al. 2006; Westberry et al. 2008) with higher rates found in shallow seas and in the coastal zone than in the open ocean. However, high gross rates of production in coastal seas can be balanced by equally high loss rates due to respiration and grazing, leading to considerable uncertainty as to whether the overall carbon balance of coastal seas is autotrophic or heterotrophic (Gattuso et al. 2006; Gazeau et al. 2004). Coastal shelf seas are highly productive environments which are subject to many human pressures (Jickells 1998). Globally, the input of nutrients into the coastal environment has continued to increase over recent decades (Liu et al. 2010a) although management measures may now have reduced loads in some western European estuaries (Soetaert et al. 2006). Elevated nutrient inputs may cause excessive phytoplankton production which can lead to undesirable disturbance (Tett et al. 2007) such as low oxygen/hypoxia, changes in species composition and impacts on fisheries (de Jonge et al. 2002; Liu et al. 2010b; Middelburg and Levin 2009). Determination of the status of water bodies with respect to eutrophication such as carried out under Oslo and Paris Commission (OSPAR 2005) requires an assessment of change in ecosystem health induced by anthropogenic (i.e. nutrient) pressures. It is therefore necessary to establish the seasonal and interannual variability in relevant biological variables such as chlorophyll biomass and primary production in order to identify anthropogenic change against natural variability and determine appropriate management measures (Cloern and Jassby 2010; Widdicombe et al. 2010). Liverpool Bay has been identified as a region which receives elevated inputs of fluvial nutrients (approximately 29,000 t of inorganic nitrogen per year; Cefas 2008) and therefore has the potential for undesirable disturbance (Tett et al. 2007). A recent review of the Irish Sea including Liverpool Bay showed that despite nutrient-induced high chlorophyll concentrations, other signals of disturbance including oxygen depletion and changes in primary production (and hence eutrophication) could not be found (Gowen et al. 2008) and under the most recent OSPAR assessment of eutrophication, Liverpool Bay was designated as a non-problem area due to a lack of undesirable disturbance (Foden et al. 2010). Liverpool Bay is a region of freshwater influence (ROFI) with large freshwater inputs from several rivers (~200 m3 s−1) and a strong tidal regime. It has a complex circulation and a water column which may vary between well-mixed and vertically stratified conditions, dependent on the prevailing weather and the neap– spring cycle (Palmer 2010), which will have a profound effect on biogeochemical cycling in the bay (Howarth and Palmer 2011). Within the Liverpool Bay Coastal Observatory (Howarth and Palmer 2011), high frequency in situ measurements of

physical, chemical and biological parameters have been made since 2002 as part of the UK national monitoring programme for the assessment of eutrophication status under the OSPAR Comprehensive Procedure (OSPAR 2005). Measurements have included high-frequency inorganic nutrient concentrations, chlorophyll biomass and phytoplankton species composition and abundance. In addition, vertical haul samples for mesozooplankton composition and abundance have been taken at the SmartBuoy location up to nine times per year. Previous studies of phytoplankton and zooplankton dynamics in the area have been conducted over short timescales up to 1 year (Figueiredo et al. 2009; Foster et al. 1982; Gowen et al. 2000), with low-frequency (monthly) sampling of the site from research vessels. Analysis of the 7-year time series of high-frequency data collected in this monitoring programme will provide greater understanding of the seasonal and interannual variability in primary producers in this dynamic region in order to help improve confidence in assessing change in ecosystem function due to nutrient pressure. This paper addresses the following questions: 1. How do physical mixing processes influence the distribution of primary producers and the magnitude of primary production in Liverpool Bay? 2. Can copepod grazing requirements be met by net primary production at the study site? 3. What are the consequences for eutrophication monitoring in Liverpool Bay?

2 Methods 2.1 Discrete measurements Discrete samples were collected at the study site (53°32′ N, 3°21.8′ W) in Liverpool Bay (Fig. 1) where the mean depth was 23 m (minimum depth 18.7, maximum 30.0). The site was visited up to nine times per year according to Greenwood et al. (2011). Samples were analysed for salinity (Greenwood et al. 2011), chlorophyll and phaeopigments. The concentrations of chlorophyll and phaeopigments were determined according to Tett (1987). This method includes some chlorophyllides in the analysis; therefore, results are referred to as ‘chlorophyll’ rather than ‘chlorophyll a’ (Tett 1987). Discrete samples were collected and analysed for dissolved inorganic nutrients according to Kirkwood (1996) (for full details, see Greenwood et al. 2011). Water samples (150 ml) were collected at daily intervals using an Aquamonitor (Envirotech, USA) which were preserved with 2.5 ml acidified Lugol’s solution. Samples were analysed for phytoplankton species and abundance by

Author's personal copy Ocean Dynamics Fig. 1 The location of (a) Liverpool Bay in the UK showing the different salinity regimes in the bay (modified from Vincent et al. 2004) and b the study site highlighted in red with typical positions of the 31, 32 and 33 isohalines

a

b

inverted microscope after a 12-h sedimentation step in a 25ml glass chamber (Utermöhl 1931). A total of 91 samples collected between 2003 and 2009 were analysed at two different laboratories, one analysed for all species and one using a Reduced Taxon List (RTL), prepared by the Marine Plants Task Team for use under the Water Framework Directive. The data from the full species list were transformed to the RTL and the combined datasets were statistically tested for homogeneity (online resource 1). Similarities between samples were calculated using the Bray Curtis coefficient and the similarity profile routine (SIMPROF) was used to examine the significance of the groups in the dendrogram. Statistical analysis was carried

out using Primer (Clarke and Warwick 1994). Analysis of preserved phytoplankton samples by light microscopy provides information on the abundance of the larger algal cells in the phytoplankton community, typically diatoms and dinoflagellates greater than 5 μm in diameter. Zooplankton samples were collected at the study site using two ring nets hauled vertically through the water column from near bed to the surface; a 0.5 m diameter ring net with 80 μm mesh and a 1 m diameter ring net with a 270 μm mesh. The volume of water passing through the net (used to derive zooplankton abundance) was calculated from the readings of a mechanical flowmeter (GO, USA) mounted at the mouth of each net. Five repeat hauls were


completed with each net, combined and preserved with buffered formalin (4% final concentration). Samples were analysed by microscope to determine species diversity and abundances. For microscope analysis, each sample was washed into observation fluid (Steedman 1976), subsamples (0.5 to 10 ml) were taken using a Stempel pipette and individual animals were counted. Copepod biomass (milligrammes dry weight per cubic metre) per sample was estimated using dry weight values (milligrammes per individual) for species taken from Peterson et al. (1990) and Pitois et al. (2009) where available. Where no value was available for a particular species, an estimate was made using data for similar species. Biomass results were converted to give an estimate of carbon biomass (milligramme carbon per cubic metre) assuming a dry weight to carbon ratio of 0.4 (Andrews and Hutchings 1980; Parsons et al. 1984). Estimates of zooplankton abundance and biomass per square metre were calculated by multiplying over the depth of the water column at the time of each sampling event. The grazing rate of copepods was estimated assuming a daily consumption rate of 40% of copepod biomass (Fock et al. 2001).

In situ measurements of conductivity, temperature, chlorophyll and underwater irradiance were measured every half an hour using SmartBuoy (Mills et al. 2005). Measurements of conductivity, temperature and pressure were made every 10 min near the seabed at the same location (Howarth et al. 2008) using a SeaBird SBE 16plus (Seabird, USA) mounted on a lander. The attenuation coefficient for downward irradiance, Kd (per metre), was calculated as: Ed1 Kd ¼ ln ð1Þ Ed2 where Ed1 and Ed2 are the values of downwelling PAR irradiance at 1 and 2 m, respectively. The depth of the euphotic layer, Zeu (metre), was determined as the depth at which PAR was reduced to 1% of its subsurface value: lnð100Þ Kd

ð2Þ

The mean water column irradiance, Em (micromole photon per square metre per second), was calculated for each timestamp as: Em ¼ E0

1 eKd Z Kd Z

2.3 Estimation of primary production Two models were used to derive estimates of primary production:

2.2 In situ measurements

Zeu ¼

depth (ZML). A mean value of Em was calculated from all values for each day, referred to as daily mean Em (micromole photon per square metre per second). Data from the mooring was passed through a defined quality assurance protocol and only data which passed the protocol is presented here. Results of discrete chlorophyll analysis were used to calibrate the chlorophyll fluorometer to units of milligrammes per cubic metre. Effects of nonphotochemical quenching of in situ fluorescence were avoided by only using fluorescence values obtained at irradiance values 80 μm size fraction and exhibited strong seasonal cycles with lowest values of 7.8×102 ind. m−3 (3.4 mg C m−2) and 7.7×104 ind. m−2 (98 mg C m−2) in the >270 and >80 μm size classes, respectively, between December and March (Fig. 8). Copepod abundance in the >80 μm size class increased gradually from April and reached a maximum of 2.4×106 ind. m−2 in September (2,950 mg C m−2, Fig. 8). This size class included predominantly juvenile stages of neritic copepods such as Oithona, Harpacticoida, Centropages, Acartia, Temora and Paracalanus species. Total abundances were lower in the >270 μm size class, with abundances increasing sharply from April to a maximum of 2.8×104 ind. m−2 in June (144 mg C m−2, Fig. 8) with a smaller peak in September to October. The >270 μm size class was dominated by late stage juveniles and adults of Temora, Centropages, Acartia, Paracalanus and Pseudocalanus species. Copepod abundance and biomass values decreased during autumn to return to winter biomass levels by December (Fig. 8). Grazing followed the same trends as abundance with estimated grazing remaining below 100 mg C m−2 day−1 between December and April. Maximum estimated grazing rates of 58 mg C m−2 day−1 were observed in June for the >270 μm size class and up to 1,180 mg C m−2 day−1 in September for the >80 μm size class (Fig. 9). Seasonal trends in copepod biomass lagged those in the phytoplankton community with an offset of 4 months between the maximum net primary production in May and the maximum copepod grazing in September (Fig. 9). Average annual grazing was estimated to be 151 g C m−2 year−1

Fig. 9 Monthly mean carbon grazed at the SmartBuoy site plotted with monthly mean net primary production for years 2002 to 2009 combined

(Table 3) which was dominated by grazing in the size class 80–270 μm.

4 Discussion 4.1 Controls on phytoplankton bloom dynamics In order to make robust assessments of change in ecosystem health over time, such as required under the OSPAR Comprehensive Procedure, it is important to establish the magnitude and causes in natural variability for any given assessment area. Data collected over 7 years within the monitoring programme in Liverpool Bay show that there is a repeatable seasonal cycle in production although the magnitude of gross and net primary production varies greatly between years (e.g. annual GPP in 2006 was 56% of GPP in 2003). Positive rates of net primary production were restricted by the availability of light to a period of 4–6 months during spring and summer. In a phytoplankton community dominated by diatoms, it is the change in species composition with the appearance of dinoflagellates in the summer which differentiates the phytoplankton community structure between months, rather than changes in species diversity. It has been demonstrated that the spring–neap cycle is important in controlling bloom formation and dispersion in Liverpool Bay as has been reported for other coastal ecosystems (Holley and Hydes 2002; Ragueneau et al. 1996). Vertical stratification in coastal environments such as Liverpool Bay is controlled Table 3 Estimates of annual copepod grazing requirements Carbon biomass (g C m−2 year−1)

Fig. 8 Abundance of copepods in the size classes >80, 80–270 and >270 μm

Annual grazing (>80 m) Annual grazing (>270 m) Annual grazing (80–270 m)

151 8 143


on short timescales by tidal stirring (Cloern 1996; Palmer 2010) and increases the mean irradiance to which phytoplankton are exposed (Figs. 2b and 5a). The underwater light regime in this study was controlled by the depth of mixing due to vertical stratification and the light attenuation coefficient, itself controlled by resuspension of sediment (Devlin et al. 2008; van der Molen et al. 2009). High concentrations of suspended sediment caused rapid extinction of light so that, on average, less than one third of the water column was exposed to solar radiation. Nutrient inputs required to support continued production throughout the summer may be supplied from the rivers entering Liverpool Bay (Greenwood et al. 2011) and release from sediments during turbulent mixing. Values of production presented in this paper have been calculated using best available estimates available for a number of physiological and optical parameters which will vary over the season. The best-constrained variable was the surface irradiance for which complete, high-resolution measurements were available from a local metereological station supplemented with regional estimates of PAR from a geo-stationary satellite. The seasonal aspect of Kd variability was very well represented with valid data recovered for 82% of the measurement period, but the variability of Kd with depth is an unknown aspect of the study. The propagation of irradiance down through the water column was represented by a single attenuation coefficient derived from a pair of PAR sensors at 1 and 2 m. Further work is required to test if the assumption of a constant Kd with depth is valid. Reflective losses of irradiance at the air– water interface are another cause of potential uncertainty, particularly under windy conditions, although the loss of irradiance is usually less than 7%. Phytoplankton biomass was also very well represented, with valid measurements on 78% of all days within the 2003–2009 period. However, the conversion from a proxy parameter (chlorophyll fluorescence) to chlorophyll units increases uncertainty, as does the lack of information on chlorophyll distribution throughout the water column. Confidence in the chlorophyll values is gained from the good agreement between remotely sensed chlorophyll a and in situ chlorophyll. Thus, the main ‘biomass-light’ variables can be said to be well-constrained, and the high density of points in time represent a major increase in confidence over what can be achieved from infrequent ship sampling. The composite bio-optical model B.Zeu.E0 has been widely used in deep estuaries and coastal waters with a shallow euphotic depth (Brush et al. 2002; Brawley et al. 2003), where it explains >90% of the directly measured gross primary production. The Liverpool Bay observatory programme did not include direct measurements of phytoplankton physiology; therefore, the choice of values for photosynthesis-irradiance parameters (Pbm and α) was made by expert judgement.

Data from other sites and similar values for coastal embayments (Grangeré et al. 2009) were compared and led to the choice of a fixed value of 0.034 for α and a temperature-dependent Pbm. When these parameters were used in the time- and depth-resolved model the daily GPP values obtained showed a strong correlation with the product of the composite bio-optical model. The estimates of mean gross primary production of 167 to 296 g C m−2 year−1 from this study are similar to an earlier estimate of 182 g C m−2 year−1 by Gowen et al. (2000) for the same site in 1997. Improvements in the parameterisation of this model may be made in the future using results from 14C or variable fluorescence-based incubations conducted at this site over different seasons which have recently commenced and will provide further validation of results from this study. The measurements presented here were made at a fixed location, and it is valid to consider how results from this location may be applicable to a wider area. Surface chlorophyll climatological maps generated from satellite ocean colour show a strong gradient in algal concentration controlled by the spatial extent of the ROFI, with the highest values close to the southern coastline of the bay and lowest values offshore in the eastern Irish Sea. These gradients in chlorophyll and salinity are confirmed in a companion paper (Greenwood et al. 2011). The study site is located on the northern edge of the coastal high-chlorophyll zone, and appears to be intermediate in character between the coastal and offshore waters. It is highly likely that movement of water masses away from the coast will advect water which is high in algal biomass through the study site and that a combination of advective and in situ processes are responsible for the phenomena observed in the time series. Estimates of grazing rate in this study are dependent on the conversion factors used and intermediate values of those reported in the literature have been taken. There are a wide range of values for C/chlorophyll reported in the literature and an intermediate value of 40 has been used in this study. The dry weight/C conversion of 40% (Andrews and Hutchings 1980; Parsons et al. 1984) is slightly lower than the 45% given by Kiørboe et al. (1985). Copepod consumption rates of between 22% and 70% have been reported (Dam and Lopes 2003; Maar et al. 2004) with 40% used in this study. Grazing rates in this study were also calculated using the ingestion rates given by Gowen et al. (1998) of 2.7 μg C ind.−1 day−1 for small copepods species and 30 μg C ind.−1 day−1 for larger species which gave grazing rates between two and ten times higher than those reported here (data not shown). During the spring bloom, net primary production is sufficient to meet the grazing requirements of the copepod community with net production exceeding grazing require-


ments between April and June (Fig. 9) although average annual copepod grazing (151 g C m−2 year−1) at the mooring site is estimated to be 2.7 times greater than the average net primary production (56 g C m−2 year−1) which would indicate that the site is net heterotrophic. However, for 2009, net community production, (i.e. the amount of carbon available for export from the euphotic zone; NPP minus heterotrophic respiration) at the site was estimated to be between 30.8 and 50.4 g C m−2 year−1 (Panton et al. 2011) indicating that the site was net autotrophic. Additional supply of carbon to the site would therefore be required to support the copepod community, such as through advection offshore of the coastal waters which are high in algal biomass (Fig. 3) and dissolved organic matter from riverine input (Yamashita et al. 2010). Previous studies have found that copepods in the Irish Sea obtain 1–40% of their feeding requirements from the protozooplankton (Figueiredo et al. 2009) with similar values of 3– 52% in the Celtic Sea (Fileman et al. 2007) and that with low abundances of microprotozooplankton in the coastal areas of the Irish Sea, copepods must also feed on phytoplankton (Figueiredo et al. 2009). 4.2 Consequences for monitoring in Liverpool Bay Few studies of zooplankton communities in UK waters have included the use of sampling nets with small mesh sizes, with sampling traditionally conducted using 200 or 270 μm nets. Recent studies by Pitois et al. (2009) and Painting et al. (submitted) have indicated that zooplankton abundances and biomass may have been under-estimated in many of these studies, particularly in coastal waters or where the zooplankton community is dominated by small neritic copepod species, such as those found during this study. In this study, both 80 and 270 μm nets were used, and total abundances and biomass of copepods were much higher than previously reported (Gowen et al. 1998, 1999). Results from Figueiredo et al. (2009) also showed that the copepod community in the Irish Sea is dominated by small species and that a combination of fine and coarse mesh nets is required to accurately sample the copepod biomass. The importance of collecting data over multiple years in drawing robust conclusions regarding changes in phytoplankton and zooplankton community structure, in particular when relating to changes in environmental variables, has been previously highlighted (Widdicombe et al. 2010). Phytoplankton biomass and composition changed rapidly in Liverpool Bay, often within periods of less than 1 week, in response to changing nutrient and irradiance conditions as well as to advective processes. A typical ship-based monitoring programme with biweekly or monthly sampling intervals would not have sufficient resolution to identify the rapid responses to changing irradiance shown here, which

is typical of such a shelf sea. High-frequency measurements allow the different processes which impact on production including nutrient supply, light limitation and impact of grazing to be identified and quantified and provide data for the validation of physical and ecosystem models (e.g. van der Molen et al. 2009) and evaluation of assessment thresholds such as those used by OSPAR (Heffernan et al. 2010). Ongoing work to integrate measurements made over different time and space scales for robust assessment of ecosystem health in Liverpool Bay, such as required under the Marine Strategy Framework Directive (EU 2008) is key to the structure of the future marine monitoring programme. Acknowledgements Work was carried out by Cefas under Defra contracts A1228, SLA25, E2202 and E5302. We are grateful to Lars Edler, Katie Owen and Thomas McGowan for analysis of phytoplankton samples and Cheryl Crisp and Oliver Williams for analysis of zooplankton samples. The authors would like to acknowledge the NERC funding of the Coastal Observatory and to thank all the sea going staff at Cefas, NOCL, University of Bangor and University of Liverpool and the ship’s crew who assisted in the collection of samples. MODIS and MERIS ocean colour data were obtained under a service level agreement with the MarCoast I and II projects. Lander data were supplied by NOCL. We are grateful to two anonymous reviewers for their constructive comments.

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