Journal of Marine Systems 78 (2009) 1827

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Journal of Marine Systems

j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / j m a r s y s

Estimation of global zooplankton biomass from satellite ocean colour

K.H. Patrik Strmberg a,, Timothy J. Smyth a, J. Icarus Allen a, Sophie Pitois b, Todd D. O'Brien c
a b c

Plymouth Marine Laboratory, Prospect Place, PL1 3DH, Plymouth, UK The Centre for Environment, Fisheries and Aquaculture Science, Pakeeld Road, Lowestoft, NR33 OHT, Suffolk, UK National Marine Fisheries Service-NOAA, Silver Spring, Maryland, USA

a r t i c l e

i n f o

a b s t r a c t
A changing Earth System requires knowledge on a global scale. The only way of obtaining detailed information at these scales is by using satellite remote sensing and/or modeling. In the marine environment, information on primary production (PP) is derivable from satellite data, whereas datasets of higher trophic levels are sparse. The challenge is to combine these two sources. A model relating the ow of energy from PP to zooplankton biomass, was used to address this problem. The model was parameterised with PP from the SeaWiFS satellite ocean colour record and a subset of a global dataset of zooplankton biomass. The model was then validated with the remaining zooplankton data. The model was used to: produce a map of annual global, zooplankton biomass, quantify the ow of carbon from PP to zooplankton and investigate the spatial variability of this ow. One of the more notable ndings is that more energy is transferred to zooplankton when PP is low. 2009 Elsevier B.V. All rights reserved.

Article history: Received 31 July 2008 Received in revised form 24 January 2009 Accepted 3 February 2009 Available online 15 February 2009 Keywords: Zooplankton biomass Primary production Global model Trophic efciency Satellite data

1. Introduction A fundamental challenge in Earth System science is the response of the marine ecosystem to changes in climatic forcing. In particular how will it affect ecosystem functioning and the sustainability of bio-resources. Datasets which allow us to map the distribution of marine biota are sparse. Satellite remote sensing can provide detailed information on a global scale for several bio-physical parameters, such as temperature and chlorophyll (Robinson, 2004). The challenge is to combine satellite data with the sparse in-situ datasets to generate global distributions of higher trophic levels. Models relating ocean colour to primary production are well documented (Eppley et al., 1985; Behrenfeld and Falkowski, 1997; O'Reilly et al., 1998; Joint et al., 2002; Smyth et al., 2005; Carr et al., 2006). However, the ow of energy from lower to higher trophic levels is less understood. The macroecological theory developed by Jennings and Blanchard (2004) provides a way of addressing this problem. The algorithm relates the ow of energy from one trophic level, TL, to another using allometric scaling laws (Brown et al., 2004). Allometric scaling in biology (a variable raised to the power 1, autonym: isometric), was rst documented by Kleiber (1932), in this case it refers to the scaling of metabolic rate, with body mass, M, usually as M 0.75 (Brown et al., 2004). In a size structured foodweb where organisms share a common energy source the higher levels will be constrained by inefcient transfer of energy, generally thought to be 10% between each level (Lindeman, 1942; Brown and Gillooly, 2003). This loss of energy is referred to as the trophic efciency, TE (predator production/prey production). To estimate the
Corresponding author. Tel.: +44 1752 633466; fax: +44 1752 633101. E-mail address: psto@pml.ac.uk (K.H.P. Strmberg). 0924-7963/$ see front matter 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.jmarsys.2009.02.004

energy, E, of a chosen TL the decrease of E from TL0 to TLn, scales as En = E0 TETLn 1 (Jennings and Blanchard, 2004). The attraction of this theory is that it provides a simple set of relationships which relates ow of energy through the marine foodweb. In order to demonstrate the applicability of this methodology the focus in this study is on generating a global climatology of zooplankton biomass. We combine the primary production information from the SeaWiFS record (1998 20051) with a subset of the NMFS Coastal and Oceanic Plankton Ecology, Production and Observation Database, COPEPOD (O'Brien, 2005), in order to parameterise the model. We then ran the model over the global datasets and validated it with the remaining COPEPOD data not used for the parametrisation. It has been debated, in the literature, whether or not TE should vary with the availability of nutrients or PP, e.g. TE is higher in regions with high PP and lower in regions with low PP (Sprules and Munawar, 1986; Ahrens and Peters, 1991). This can be compared with an alternative nding of higher grazing pressure in oligotrophic regions (Calbet, 2001). A study in the Atlantic ocean shows that high TE is not coupled with high PP (San Martin et al., 2006). TE was therefore investigated separately: I. on each grid point; and II. on regions subdivided based on levels of primary productivity. The overall aims of this study are: I. to provide a way of using satellite data to supplement otherwise sparse in situ data types (i.e. produce a global map of zooplankton biomass) II. to quantify the ow of energy to zooplankton biomass from primary production

1 (SeaWiFS data are currently available up to 2007, but COPEPOD data were up to and including 2005 and the aim here is annual biomass, hence the selection of SeaWiFS data).

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(i.e. determine TE); and III. to investigate the spatial variability of the transfer efciency of this ow (i.e. determine how TE varies). 2. Methods 2.1. Model theory The production, P, at a trophic level, TL, can be expressed as: PTL = PP TE
TL 1

PBR ensures that all possible values are tested and is narrowed down in the tuning process. The combination of TE and PBR that gave the best goodness of t (minimised RMSE) between modelled and observed biomass was then saved for further analysis. 2.2. Satellite data Satellite derived maps of ocean colour (O'Reilly et al., 1998) were used to produce monthly averaged values of PP using the methodology of Smyth et al. (2005); these were then composited into a mean annual eld, at a nominal resolution of 18 km, for the period between 1998 and 2005. The units for satellite derived PP are in mg C m 2 d 1. To make a direct comparison with the in-situ biomass, the units need to be converted to mg C m 3 d 1. This is achieved by dividing by the euphotic depth, Ze: (mg C m 2 d 1 m 1 = mg C m 3 d 1). To do this maps of Ze were produced using a similar technique as for PP (i.e. composited into annual mean). Ze, (m) was estimated from chlorophyll-a, as (Morel and Berthon, 1989): Ze = 200:0Ctot
0:293

where TE = trophic transfer efciency (TE = predator production/ prey production), PP = primary production and TL = trophic level (Jennings and Blanchard, 2004). In this study the trophic level of zooplankton is set to 2 (i.e. not 15N based (Owens, 1987) because: I. choosing a different TL(s) will not affect the outcome (model is tuned to a ratio TE/PBR, as explained below, TL falls out of the caluclation); II. data was not available on the species level; III. it keeps the model simple; IV. it is standard practice (Lindeman, 1942; Jennings and Blanchard, 2004; Gascuel, 2005). TL = 2 reduces Eq. (1) to: SP = PP TE 2

; if Ze b 102 Z Ze568:2Ctot

0:746

where SP is secondary production. TE can be set to a xed number because even if secondary production is higher in areas of high primary production, (for example upwelling areas compared with oligotrophic areas) the higher SP is not the result of higher TE per se (San Martin et al., 2006) but most likely the higher PP. To support this statement TE was investigated separately. In order to make the comparison of model and data from the database it was necessary to convert SP to biomass, B. An empirically derived P:B ratio (PBRe) was originally (i.e. Jennings and Blanchard (2004) used for this purpose: PBRe = 10
TL 3:471 0:386

where the total pigment content, Ctot, (mg m 2) from the sea surface down to D is expressed as a function of pigment concentration in the surface layer, Cs, (mg m 3); Ctot = 40:2Cs
0:507

; if Cs b 1 Z Ctot = 38Cs

0:425

2.3. COPEPOD database The COPEPOD database (O'Brien, 2005, http://www.st.nmfs.noaa. gov/plankton), is comprised of zooplankton biomass and abundance data from four general sources: I. National Marine Fisheries Services Ecosystem surveys; II. historical plankton data; III. data centres, institutions, and project data; and IV. direct investigator submissions. While the abundance data are sparse for many regions of the globe, COPEPOD does achieve near global coverage of zooplankton biomass data. Most of these data are located in the northern Hemisphere and around North America, with lesser amounts available for the southern Pacic and the south Atlantic. COPEPOD offers standardised mean zooplankton biomass values on a global one degree longitudelatitude spatial grid. Per O'Brien (2005), this compilation consists of total sampled biomass data (e.g., wet mass, dry mass) and/or biovolume data (e.g., displacement volume, settled volume), standardised to a common depth interval (0200 m) and a common mesh size (i.e. samples with mesh size 150200 m where converted to 330 m). These biomass and biovolume values are available as carbon mass, converted to carbon (mg C m 3) using the published conversions of Wiebe (1988) and others (O'Brien, 2005). The COPEPOD carbon mass elds are available by seasons and as a single annual eld. The seasons are dened as the meteorological seasons of the northern hemisphere: winter (Dec.Feb.); 3650 values, spring (Mar.May); 3792 values, summer (Jun.Aug.); 4484 values, autumn (Sep.Nov.); 3501 values (total of 15427 data values). The annual eld is created from the average of the four seasonal elds (O'Brien, 2005). This study used the annual zooplankton carbon mass eld, which was comprised of 9687 zooplankton carbon mass (mg C m 3) values. 2.4. CPR data set In addition to COPEPOD we also used the Continuous Plankton Recorder (CPR) data set as an independent validation and parametrisation source. The CPR survey has now been running for more than 70 years, and provides one of the longest and most extensive marine

Eq. (3) was specically determined for higher trophic levels (e.g. sh) (Simon Jennings, pers. comm.) and is not applicable for this study. Therefore we have a parametrisation problem of one equation and two unknowns; TE and PBR. A Monte Carlo randomisation approach with PBR and TE as variables was used to solve this problem. The PBR is added to the model resulting in: B= PP TE PBR 4

The model (Eq. (4)) was tuned and validated with observational data. Half the data was randomly selected for the parametrisation of the model (i.e. the data were indexed using random numbers drawn from a uniform distribution to ensure that all values were equally likely to be selected). The remaining half was retained for model validation purposes. This division of the data set enables a more independent way of tuning and then assessing the model. Satellite derived PP (details in next section) was extracted from the same geographical position as the COPEPOD data (n = 4843). TE for zooplankton can vary between 1020% (Lindeman, 1942; Kiorboe and Nielsen, 1994; Jennings and Blanchard, 2004; Gascuel, 2005). Hence, random values (20000) of TE were drawn from a uniform distribution (all values are equally likely to occur) between 0.10.2 and secondary production was calculated using Eq. (2). Simultaneously, random values (20000) of PBR from a uniform distribution between 0.05 to 1, were used to scale secondary production to biomass. This PBR range was selected based on observations: copepodites, 0.14 d 1 (McClatchie et al., 2004); generic zooplankton (excluding Larvaceans and Thaliaceans), 0.061.6 d 1 (Hirst et al., 2003). The broad range of

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Fig. 1. Regions used. A. As dened by the Rutgers basin mask; 1. Atlantic, 2. Pacic, 3. Indian ocean, 4. Arctic, 5. Antarctic, and 6. Mediterranean. B. Location of the regions of the COPEPOD database (approximate boundaries).

ecological time-series in the world (Beare et al., 2003; Reid et al., 2003). Information on the abundance of copepods and cladocerans (a total of 60 taxa) was extracted from the CPR database for the period 19982005 and covering the area delimited by latitudes 45N to 63N and longitude 15W to 10E. Copepods and cladocerans were selected because identication in CPR samples is generally carried out to species or genus level for these groups (in some other taxonomic groups, identication is limited to family or higher categories). Out of the original 60 species, only those contributing at least 0.1% of total biomass in at least one of the ve sub areas were kept, resulting in data on 29 key species being retained, accounting for N 99% of total biomass. The CPR survey collects samples at different times of day and at locations that do not follow a regular grid. The data therefore need to be spatially interpolated and regularised in time and space before being subjected to numerical analyses (Beare et al., 2003). This was undertaken on a 50 50 nautical mile (92.6 92.6 km) grid using Inverse Distance Interpolation (Lam, 1983; Legendre and Legendre, 1998). A search radius of 150 miles (i.e. 277.8 km), and a minimum of ve miles, and maximum of 100 neighbours were used, respectively. These values were chosen as a compromise between numerical efciency and the need to keep the number of missing values in the interpolated grid to a minimum. Average monthly abundances for individual species were calculated taking diel variability of the CPR data into account (Beaugrand et al., 2003). Unfortunately the CPR is known to under-estimate zooplankton abundance when compared with other datasets (John et al., 2001). To compensate for this, and to convert abundance values to biomass as mg dry mass m 3, the data was corrected for under-sampling by using WP-2 (200 m)/CPR (270 m) ratios as described in Pitois and Fox (2006). The biomass values were converted from mg dry weight, (DW) m 3 to mg C m 3 using the method of O'Brien (2005) for conversion of the COPEPOD zooplankton biomass data: log10(C)=(log10(DW) 0.499)/ 0.991 (Wiebe, 1988). This method of conversion was selected to enable a better comparison of CPR data and COPEPOD data. The resulting data set, comprising matrices of CPR biomass, was processed to condense the values for each year, 1998 to 2005, into a single value at each grid point (by combining all the matrices). This created a total of 328 annual mean biomass values. Half of these values were randomly selected to tune the model, and the remaining half was used to assess the skill (to decrease the dependence on data).

2.5. Denition of regions In the different analysis carried out different regions are analysed. These regions are: A. dened by the Rutger's basin mask2 and B. regions of the COPEPOD database. These regions are shown in Fig. 1. 2.6. Statistical methods The following criteria were used to evaluate model skill. The percentage model bias is dened as:

P
k bias =

M D

100

where D represents the observations and M the model predicted values. Values were categorised as b 10% excellent; 10 to 20% very good; 20 to 40% good; N 40% poor (Marechal and Holman, 2005). A negative value indicates a tendency to underestimate. The Root Mean Square Error (RMSE) was used for the model parametrisation: sP D M2 RMSE = n

RMSE can be used as a basic cost function (measure of goodness of t); the closer to zero, the better the t. Formal signicance tests for differences between regions were conducted using Analysis of Similarities, ANOSIM. The ANOSIM statistic, R, contrasts the ranks of resemblances within groups and those between groups, and is scaled to vary between 1 and + 1 (although values less than 0.1 are rarely achieved in practice). If groups are perfectly separated then all ranks within groups will be less than all ranks between groups, and R = 1. The null hypothesis of no differences between groups is addressed by randomisation. Multiple random rearrangements of the labels in the resemblance matrix are used to build up the distribution of R under the null hypothesis,

2 Provided by David Antoine at the Observatoire Oceanologique Laboratoire de Physique et Chimie Marines, France. WWW Page, http://marine.rutgers.edu/opp/ Mask/MASK1.html.

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Fig. 2. Annual (19982005) zooplankton biomass [mg C m 3] from the model (TE 0.16, PBR 0.3). The biomass spatial distribution is the same as the underlying PP as mapped from space. The quantities are similar to the COPEPOD (% bias ~1%, Fig. 3). Most values are below 10 mg C m 3, hence the plot is in log space. Values over 100 are removed (set to 100, i.e. appears in black).

Fig. 3. Histograms showing the model tuned to a randomly selected 50% of the COPEPOD. The remaining half is plotted as data and used for model data comparisons (location of the regions shown in Fig. 1B). For statistics see Table 1. The data have been binned with bin size 4 (e.g. 0 on x-axis is the range 04, etc). Values over 100 are set to 100 (max of data).

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Fig. 4. Mean zooplankton biomass [mg C m 3], when the model is tuned to regions (Fig. 1a), compared with the model tuned on global scale. Error bars are the standard deviation of the mean [mg C m 3].

against which the observed value is compared (P. Somereld, personal communication). Tests were conducted in Primer v6 (Clarke and Gorley, 2006). 2.7. The variability of trophic transfer efciency 2.7.1. Trophic transfer efciency on each grid point TE was estimated at each grid point (i.e. lat/lon position), where data were available (e.g. COPEPOD annual zooplankton biomass). A map of TE was then plotted to visualise any patterns (e.g. higher in upwelling regions and lower in oligotrophic regions). PBR was again allowed to vary 0.051. TE was allowed to vary between 0.1 to 0.2 and 20000 TE values were randomised (using uniform distribution) at each grid point, a total of 9686000 (4843 20000) randomisations. The resulting matrix of TE values was globally mapped. Additionally, the resulting TE versus PP relationship was tested for any correlation. This experiment was repeated with a xed PBR. 2.7.2. Trophic transfer efciency in regions dened by levels of PP The global ocean was divided into six basins (Fig. 1A); (1) Atlantic; (2) Pacic; (3) Indian Ocean; (4) Antarctic; (5) Arctic; and (6) Mediterranean. These regions were then subdivided based on levels of

PP, which where low (PP b 100.5 (~ 3.2) mg C m 3 d 1), medium (PP N 100.5 b 101.5 (~32) mg C m 3 d 1 and high (PP N 101.5 mg C m 3 d 1. The model was then tuned to the data in the regions to elucidate any patters related to levels of PP.

3. Results 3.1. Global map of zooplankton Fig. 2, shows the global map of annual zooplankton biomass, with clear featues such as higher biomass in uppwelling regions and on the continental shelves, compared to e.g. the oligotrophic gyres. Another feature is the stable patchiness of the Antarctic waters (annual scale). Fig. 3 illustrates one of the more important ndings; that the distributions of biomass are consistently lognormal (i.e. normal in logspace). The randomisation of TE and PBR, that gave the best goodness of t (minimises RMSE), are: TE 0.16, with a PBR 0.30, at RMSE b 0.01. (TEmodel/PBRmodel 0.53). The skill (assessed with data not used for tuning) of this t is RMSE 4.24, % bias 0.89. Mean global zooplankton biomass is 5.52 mg C m 3 (SD = 8.94, n = 4843). These statistics indicate that the map of zooplankton biomass (Fig. 2) is accurate on the global scale, but less accurate on the regional scale (Figs. 3, 4, Table 1 and Table A.1). Fig. 3 is showing the distributions of biomass, with most of the values in the lower bins. The distributions of data are similar for all regions except for one that will be addressed separately in the discussion. The results agree broadly with literature (Fig. 4, Table A.1).

Table 1 Statistics for histogram in Fig. 3. Region Global North Atlantic South Atlantic North Pacic South Pacic Indian ocean Arctic Antarctic BeringChukchi GulfCaribbean Mediterranean Indonesia CPR n 4533 456 371 1526 1263 743 163 83 391 206 33 304 164 % bias 0.89 4.55 31.91 28.1 40.29 53.01 36.81 44.92 68.49 28.33 193.2 8.18 2.68 RMSE 4.24 10.84 7.71 15.58 10.5 11.04 15.77 13.5 21.49 11.42 27.98 15.18 1.37 r2 0.33

The RMSE and % bias is the goodness of t between the model and the remaining data not used for tuning. r 2 from data used for tuning (because there is no correlation between data for tuning and data for assessing skill) is shown for regions which the model is tuned to. The regions are from the COPEPOD database denitions (Fig. 1B).

Fig. 5. Model tuned to a randomly selected 50% of the CPR data set. The data plotted are the remaining half of the CPR data set.

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Fig. 6. Annual (19982005) zooplankton biomass [mg C m 3] from the model tuned to the regions: 1. Atlantic 2. Pacic 3. Indian Ocean 4. Arctic 5. Antarctic 6. Mediterranean (Fig. 1a). (Values over 100 set to 100, i.e. black in the plot).

3.2. Comparison with CPR data When the model is tuned to and compared with CPR data the result is similar, but the average biomass is lower (Fig. 5). TE was 0.16 when PBR 0.25, (i.e. TEmodel/PBRmodel 0.63). The goodness of t was RMSE b 0.01. This TE and PBR results in a mean biomass of 4.1 mg C m 3 (SD = 1.34, n = 164). When the model is assessed, with the remaining data, the goodness of t was; RMSE 1.37 % bias 2.7% (indicating a total overestimation by ~2.7%, Table 1). 3.3. Tuning to regions Model performance is excellent when assessed globally (% bias ~ 1), but the model underestimates the lowest values (Fig. 3). When the model is compared to data on a regional basis (still tuned to the global) the trend is similar, with underestimation of the lower values (Fig. 3), but a poorer overall t with is indicated by the % bias (Table 1). To investigate if a better t could be obtained, for data in the basins, the model was also tuned to regions dened by Rutger's basin mask (Fig. 1a).

The basins contain enough data to make such a tuning and to assess it. The outcome of this exercise was that model performance was still good in terms of goodness of t, but the r2 was very poor (~ 0.09). This supports the feasibility of the original approach of using one value of TE and PBR globaly. It also means that the model is still able to extrapolate the zooplankton biomass from using the PP (e.g. reproduce the mean and standard deviation), but the trends (peaks) in the data are lost. The reason for the low r 2 could be that there are outliers, so the model becomes skewed to higher values and hence the mismatch (Table 1). Some effects on the plot of global zooplankton biomass (e.g. differences in Figs. 2 and 6) are: 1. lower values for Mediterranean; 2. the gyres are more clearly visible; 3. the low biomass region in the Indian Ocean is expanded; and 4. the biomass of the Arctic is higher. 3.4. The variability of trophic transfer efciency 3.4.1. Trophic transfer efciency on each grid point No spatial patterns were evident (hence plot not included) and there was no relationship between PP and TE (2 b 0.003, Spearman's rank correlation). This supports the nding of Gaudy et al. (2003) that high PP does not lead to higher ecological efciency. It also supports San Martin et al. (2006) who showed that TE is not related to trophic

Fig. 7. The total proportion (TE/PBR) of primary production required to reproduce the zooplankton biomass of the COPEPOD database for three different levels of primary production.

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conditions. This assumes that nutrients are coupled with PP (e.g. high nutrients leads to high sea surface chlorophyll). 3.4.2. Trophic transfer efciency in regions dened by the basin mask and levels of production Patterns become clearer when TE and PBR are examined in regions subdivided on levels of primary production, e.g. a higher TE/PBR ratio when PP is low, indicating that more carbon needs to be transferred from PP to reproduce the zooplankton biomass reported in COPEPOD (Fig. 7, Table A.3). The PP levels in Fig. 7 are: high; N 101.5 (~32), medium; N 100.5 b 101.5, and low; b 100.5 (~3.2) [mg C m 3 d 1]. Except: Mediterranean high; N 101 (10), medium; N 101 b100.8, and low; b 100.8 (~6.3). North Indian medium; N 100.8 b 101.5, low; b 100.8. South Indian high; N 101.2 (~ 16) medium; N 100.5 b 101.2. Arctic medium; N 100.9 (~ 8) b 101.5, low; b 100.9 (these exceptions are indicated by in Table A.3). The differences between the regions are statistically signicant when tested with ANOSIM (described in the method section). (Global R 0.35, p 0.001. High vs medium; R 0.45, p 0.001. High vs low; R 0.50, p 0.001. Medium vs low; R 0.18, p 0.017.) 4. Discussion An implication of simultaneously varying TE and PBR is tuning to the ratio TE/PBR (the fraction of PP transferred to zooplankton biomass). This means that TE and PBR are not independent. Any TE and PBR, within the given limits, results in the ratio that maximises the RMSE goodness of t, hence the TE/PBR ratio is given in Fig. 7, Tables A.2 and A.3. However it is clear that TE is often higher then the commonly used value of 10% but falls well within the range reported in the literature (Lindeman, 1942; Ikeda and Motoda, 1977; Kiorboe and Nielsen, 1994; Jennings and Blanchard, 2004; Gascuel, 2005). Furthermore this means that choosing a different TL in the model will only change PBR while the resulting TE/PBR ratio (amount of carbon required from PP to reproduce the biomass of COPEPOD) will remain the same (Table 2). The randomisation method for conversion of production to biomass (using the PBR variable) was selected over alternative methods because the COPEPOD data used are not at a species- or individual level but only bulk biomass. Alternative methods to convert production into biomass could involve individual growth rates (e.g. Huntley and Lopez, 1992; Hirst et al., 2003). These methods, especially those of Hirst et al. (2003), are excellent for use in a ner scale model (i.e. not bulk biomass but species or individual level). The main reason for choosing the simple model is that it suits the purpose of producing the global map of annual biomass. We are not neglecting the fact that the pelagic foodweb is highly complex with many factors at play. Some factors which potentially affect the production of zooplankton (and hence biomass), are; ontogenetic diet shifts (e.g. the juveniles are herbivorous and the adults are carnivorous and therefore at different TL); community structure and physics (e.g. turbulence, turbidity, temperature, density, and entrainment). On the smaller scale most of these factors are feasible to be included in a model (subject to computational power). This is probably also possible on the global scale, however there are no data available to thoroughly assess such a model. The fact that the model performs less well on the regional scale (Fig. 3, Table 1) is not surprising since it is tuned to the global scale.
Table 2 The effect of different TLs on the model parameters is that PBR will be lower as TL is higher, while the TETL 1/PBR ratio remains the same. TL 2 2.5 3 3.5 4 TETL 1 0.108 0.054 0.018 0.003 0.002 PBR 0.196 0.098 0.032 0.006 0.003 TETL 1/PBR 0.549 0.549 0.549 0.549 0.549 Fig. 8. The tted linear model for COPEPOD biomass vs PP was: log10 (biomass) 0.98log10 (PP) 0.37, r 2 0.36, p b 0.001). CPR biomass is marked as red squares in the plot. The regression for CPR biomass vs PP: log10 (CPR biomass) 0.20log10 (PP) 0.39, r 2 0.01, p 0.027 (no line was plotted). The PP data are from the same geographical coordinates as the biomass data.

One aim of this study was to produce a map of zooplankton biomass, given the data available. The RMSE used (as a cost function) to tune the model is optimal to obtain a good t. Furthermore, because the number of tunable parameters in this model are only two (TE and PBR) the model ability to generalise is not affected as much as if a lot of parameters would have been used (i.e. less dependant on data). To further examine the relation between PP and the zooplankton biomass data from COPEPOD, the data were tted to a linear model. A log transformation of the data was applied to make the data closer to normal distribution (improve homogeneity of variances), reduce inuence of outliers and improve linearity. The relation between log10 biomass and log10 primary production (PP) was investigated in a regression: log10(biomass) = k log10 (PP) + m, for both data sets (Fig. 8). This makes evident that the amount of variance that can be explained by regressing these two variables is r 2 ~ 0.36. The low correlation between model and data, r ~ 0.33 (Table A.1), is not surprising considering that the correlation between PP and data (COPEPOD) is also low; r ~ 0.36 (Fig. 8). The histogram plots of the different regions (Fig. 3) show generally similar distributions of the data, with the exception of BeringChuckhi. The BeringChukchi region has almost no biomass data for winter and autumn seasons (due to ice) and it is dominated by data from a regular survey that only samples in the summer. Hence the lower values from other seasons are less dominant compared with the other regions. The ecological explanation for the varying TE and PBR for the different regions is uncertain. But interestingly the TE/PBR ratio (i.e. amount of carbon transferred from PP to zooplankton biomass) is more or less the same for the Indian Ocean, Mediterranean and the Atlantic (Table A.2). This supports the initially proposed theory that xing TE and PBR to produce a global map gives a good estimate of the biomass in those regions. The high TE/PBR in the Arctic could be a result of underestimated primary production. For example if most of the zooplankton were sampled in the summer, then the proportion of annual PP (which is lower than during summer, dened as the meteorological season of the northern hemisphere (O'Brien, 2005)) that needs to be utilized to result in the SP biomass of COPEPOD will be high. The same could be true for the Pacic and Antarctic region, but with a less dramatic effect (Table A.2). However it could also be some other factor such as low chlorophyll maxima (production not seen by satellite) or importance of the microbial loop. In the case of the microbial loop it again means that the assumed direct grazing on

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the PP is not applicable or less dominant. The reason is that a large portion of carbon could originate from DOM (dissolved organic matter) via bacteria and not directly from PP. 4.1. Some possible sources of uncertainty 4.1.1. Tuning method The method of tuning the model using RMSE goodness of t clearly produce a model that reproduces the mean and standard deviation (low % bias and RMSE) correctly but fails to reproduce the trends (low r) of the data (Fig. 3, Table 1). 4.1.2. Zooplankton biomass data This could be a potential bias because the chosen TL = 2 should ideally only include organisms that feed directly on PP (TL = 1). The fact is that what is referred to here as TL = 2 is really TL = 2 to ~3.5. The COPEPOD annual carbon mass elds, however, cannot be converted back to individual zooplankton groups. This makes it impossible to assess and tune the model at each (TL) step. There are also areas (datasets) in the COPEPOD where data are perhaps not as reliable as in others, for example some data in the North Pacic. The choice of temporal resolution (annual) could possibly contribute to this bias. For example there was little sampling in the northern Pacic during the winter. However this should probably be of little concern because PP data were also calculated as annual (eight years 1998 to 2005) mean biomass. Both the COPEPOD and the CPR data have been processed in various different ways (explained in the method section). The COPEPOD data has many different origins. The zooplankton from COPEPOD have been sampled using changing techniques by different investigators and was then processed as described by O'Brien (2005) to produce the annual mean biomass elds. The CPR data have then been corrected for undersampling, interpolated to a regular grid (to enable comparisons from year to year) and converted from abundance to dry weight and nally to biomass. Both these data sources still give a good qualitative indication to of the steady state annual standing stock zooplankton biomass. 4.1.3. PP estimates PP may be underestimated as the Smyth et al. (2005) model only uses surface values of chlorophyll. For example the deep chlorophyll maxima could be higher (more important) than estimated in the PP model in some regions. The PP estimates are accurate on the global scale (Smyth et al., 2005). Also some regions where the PP algorithms are known to perform less well, for example the polar regions, the equatorial, northern Indian Ocean and in case II waters (affected by riverine output) (e.g. Carr et al., 2006). All of these issues affect the accuracy of the main result in this study; the map of zooplankton biomass. 4.1.4. A large proportion of the energy is re-circulated The importance of energy from the microbial loop and protozoa could be underestimated. The approach of setting the trophic level, TL=2 means that it is assumed that all energy (carbon) comes directly from PP. There is also the issue of ontogenetic diet shifts. In other words; all zooplankton are present in the carbon mass data elds, but only a small proportion feeds directly on PP. This could explain the fact that low primary production yields a high proportion of energy transferred to zooplankton biomass (Fig. 7, Table A.3). However, if the model was modied, using a different TL (or TL's), the proportion TE/PBR which gives the nal result of zooplankton biomass, would remain the same (Table 2). 5. Conclusions The map of annual zooplankton biomass is accurate (low RMSE and % bias) when assessed with the data available. It provides

information that is useful for comparisons with any future or past change in biomass. Furthermore, it demonstrates the feasibility of combining sparse in situ data with the data rich satellite remote sensing products. This study also has shown that proportionally less energy (carbon) is transferred from PP when PP is high then when PP is low. The spatial variability of transfer efciency is important and cannot be ignored if accurate zooplankton biomass is to be extrapolated on the globe. Acknowledgements

This research was funded by the EU Marie Curie EST project METAOCEANS (MEST-CT-2005-019678). Roger Harrisfor constructive comments on the manuscript. SAHFOS for consistently maintaining one of the longest plankton time series database in the world. All individual investigators and institutions who have contributed to COPEPOD. Simon Jennings for suggesting a different P:B-ratio approach. All statistical testing was performed using the R language and environment for statistical computing (http://CRAN.R-project.org). Satellite data was prepared in IDL. Ocean color data used in this study were produced by the SeaWiFS Project at Goddard Space Flight Center. The data were obtained from the Goddard Earth Sciences Distributed Active Archive Center under the auspices of the National Aeronautics and Space Administration. Use of this data is in accord with the SeaWiFS Research Data Use Terms and Conditions Agreement. Appendix A

Table A.1 Model (M) tuned to global, data (D) and literature (L) on zooplankton biomass [mg C m 3] from different regions as dened by the Rutgers basin mask (Fig. 1A). Ref. 1. Piontkovski et al. (2003), 2. Pitois and Fox (2006), 3. Olli et al. (2007) ([g DW m 2] converted by using sample depth (0200 m) and the method of O'Brien (2005), 4. Pakhomov and Froneman (2004) (2.69 mg C m 3 is at spring ice edge ~ 60S 6E and 12.32 mg C m 3 is at Antarctic polar front ~ 50S 6E during Austral summer), 5. Rakhesh et al. (2006) (shelf, bay of Bengal), 6. Batten and Welch (2004) (estimated from diagram. The data were from a cruise track ~ 35 N 120 W to 60 N 145 W. Annual estimates from three years; 1997, 2000 and 2001), and 7. Gaudy et al. (2003) (NW Mediterranean, mean of two investigations). Region Global Atlantic Source Min M D M D L M D M D L M D L M D L M D L 0.53 0.02 0.96 0.02 Median Mean 3.32 4.18 4.71 5.03 5.52 7.35 7.98 6.94 4.10 4.00 17.24 6.45 ~ 3.20 3.87 8.41 2.69 12.32 5.4 4.81 5.02 4.53 8.61 2.83 6.77 2.53 2.28 SD 8.94 8.62 13.12 6.67 1.34 2.41 17.45 8.78 Max 271.5 99.00 271.5 67.68 + 40 9.78 13.6 158.19 55.53 1 2 Ref. Comment

CPR Arctic

0.7 1.91 4.13 0.78 3.37 0.89 11.34 0.02 2.91 0.72 2.79 0.2 6.71 0.44 1.03 3.45 0.02 2.44 0.53 0.04 1.55 1.22 0.67 3.09 5.03 2.57 3.66 1.46

See also CPR S.Atlantic N.Atlantic

Converted DW

Antarctic

3.97 108.06 8.02 59.73 20.88 4 8.48 269.86 6.82 59.07 4.69 5 6.78 191.33 9.74 99.00 1.06 4.6 10.72 156.07 2.72 13.51 1.15

Converted DW

Indian Ocean

Converted DW

Pacic

Converted DW

Mediterranean M D L

Converted DW

26

K.H.P. Strmberg et al. / Journal of Marine Systems 78 (2009) 1827 Behrenfeld, M., Falkowski, P., 1997. Photosynthetic rates derived from satellite-based chlorophyll concentration. Limnology and Oceanography 42 (1), 120. Brown, J., Gillooly, J., 2003. Ecological food webs: high-quality data facilitate theoretical unication. PNAS 100, 14671468. doi:10.1073/pnas.0630310100. Brown, J., Gillooly, J., Allen, A., Savage, V., West, G., 2004. Toward a metabolic theory of ecology. Ecology 85, 17711789. Calbet, A., 2001. Mesozooplankton grazing effect on primary production: a global comparative analysis in marine ecosystems. Limnology and Oceanography 46 (7), 18241830. Carr, M., Friedrichs, M., Schmeltz, M., Aita Noguchi, M., Antoine, D., Arrigo, K., Asanuma, I., Aumont, O., Barber, R., Behrenfeld, M., Bidigare, R., Buitenhuis, E., Campbell, J., Ciotti, A., Dierssen, H., Dowell, M., Dunne, J., Esaias, W., Gentili, B., Gregg, W., Groom, S., Hoepffner, N., Ishizaka, J., Kameda, T., Le Quere, C., Lohrenz, S., Marra, J., Melin, F., Moore, K., Morel, A., Reddy, T., Ryan, J., Scardi, M., Smyth, T., Turpie, K., Tilstone, G., Waters, K., Yamanaka, Y., 2006. A comparison of global estimates of marine primary production from ocean color. Deep Sea Research Part II: Topical Studies in Oceanography 53 (57), 741770. Clarke, K., Gorley, 2006. PRIMER v6: User manual/tutorial. PRIMER-E, Plymouth. Eppley, R., Stewart, E., Abbott, M., Heyman, U., 1985. Estimating ocean primary production from satellite chlorophyll. Introduction to regional differences and statistics for the Southern California Bight. Journal of Plankton Research 7 (1), 5770. Gascuel, D., 2005. The trophic-level based model: a theoretical approach of shing effects on marine ecosystems. Ecological Modelling 189 (34), 315332. Gaudy, R., Youssara, F., Diaz, F., Raimbault, 2003. Biomass, metabolism and nutrition of zooplankton in the Gulf of Lions (NW Mediterranean). Oceanologica Acta 26, 357372. Hirst, A., Rolf, J., Lampitt, R., 2003. A synthesis of growth rates in marine epipelagic invertebrate zooplankton. Advances in Marine Biology 44. Huntley, M., Lopez, M., 1992. Temperature-dependent production of marine copepods: a global synthesis. The American Naturalist 140 (2), 201242. Ikeda, T., Motoda, S., 1977. Estimated zooplankton production and their ammonia excretion in the Kuroshio and adjacent seas. Fish Bulletin 76 (2), 357367. Jennings, S., Blanchard, J., 2004. Fish abundance with no shing: predictions based on macroecological theory. Journal of Animal Ecology 73 (4), 632642. John, E., Batten, S., Harris, R., Hays, G., 2001. Comparison between zoo-plankton data collected by the continuous plankton recorder survey in the English Channel and by WP-2 nets at station L4. Journal of Sea Research 46 (34), 223232. Joint, I., Groom, B., Wollast, R., Chou, L., Tilstone, G., Figueiras, L., Smyth, T., 2002. The response of phytoplankton production to periodic upwelling and relaxation events at the Iberian shelf break: estimates by the 14c method and by satellite remote sensing. Journal of Marine Systems 32, 219238. Kiorboe, T., Nielsen, T., 1994. Regulation of zooplankton biomass and production in a temperate, coastal ecosystem. 1. copepods. Limnology and Oceanography 39 (3), 493507. Kleiber, M., 1932. Body size and metabolism. Hilgardia 6, 315332. Lam, N.-N., 1983. Spatial interpolation methods: a review. The American Cartographer 10, 129149. Legendre, P., Legendre, L., 1998. Numerical Ecology: Developments in Enviromental Modelling. Elsevier, Amsterdam. Lindeman, R., 1942. The trophic-dynamic aspect of ecology. Ecology 4, 399417. Marechal, D., Holman, I., 2005. Development and application of a soil classicationbased conceptual catchment-scale hydrological model. Journal of Hydrology 312 (14), 277293. McClatchie, S., Macaulay, G., Coombs, R., 2004. Acoustic backscatter and copepod secondary production across the subtropical front to the east of New Zealand. Journal of Geophysical Research 109. Morel, A., Berthon, J., 1989. Surface pigments, algal biomass proles, and potential production of the euphotic layer: relationships reinvestigated in view of remotesensing applications. Limnology and Oceanography 34 (8), 15451562. O'Brien, T., 2005. Copepod: a global plankton database. U.S. Dep. Commerce, NOAA Tech. Memo. NMFS-F/SPO-73, 136. O'Reilly, J., Maritorena, S., Mitchell, B., Seigel, D., Carder, K., S.A., G., Kahru, M., McClain, C., 1998. Ocean color chlorophyll algorithms for SeaWiFS. Journal of Geophysical Research, [Oceans] 2493724953. Olli, K., Wassmann, P., Reigstad, M., Ratkova, T., Arashkevich, E., Pasternak, A., Matrai, P., Knulst, J., Tranvik, L., Klais, R., Jacobsen, A., 2007. The fate of production in the central Arctic Ocean top-down regulation by zooplankton expatriates? Progress In Oceanography 72, 84113. Owens, N.J.P., 1987. Natural variations in 15N in the marine environment. Advances in Marine Biology 24, 389451. Pakhomov, E., Froneman, P., 2004. Zooplankton dynamics in the eastern Atlantic sector of the Southern Ocean during the austral summer 1997/1998part 1: Community structure. Deep Sea Research Part II: Topical Studies in Oceanography 51 (Issues 2224), 25992616. Piontkovski, S., Landry, M., Finenko, Z., Kovalev, A., Williams, R., Gallienne, C., Mishonov, A., Skryabin, V., Tokarev, Y., Nikolsky, V., 2003. Plankton communities of the South Atlantic anticyclonic gyre. Oceanologica Acta 26, 255268. Pitois, S., Fox, C., 2006. Long-term changes in zooplankton biomass concentration and mean size over the northwest European shelf inferred from continuous plankton recorder data. ICES Journal of Marine Science 63, 785798. Rakhesh, M., Raman, A., Sudarsan, D., 2006. Discriminating zooplankton assemblages in neritic and oceanic waters: a case for the northeast coast of India, bay of Bengal. Marine Environmental Research 61, 93109. Reid, P., Colebrook, J., Matthews, J., Aiken, J., 2003. The Continuous Plankton Recorder: concepts and history, from plankton indicator to undulating recorders. Progress In Oceanography 58 (24), 117173.

Table A.2 Model (Mg) tuned to global, Model (Mr) tuned to region (Fig. 1A) and data (D). Zooplankton biomass [mg C m 3]. TE and PBR tuned to region. The over all (global) model performance after this tuning is % bias 0.81, RMSE 5.84, r2 0.09. The TE and PBR vary on regions and Global Mr is the summary of all regions (). Region Global Source Min Median Mean SD 5.52 7.29 7.35 4.53 6.09 8.61 7.98 6.68 6.94 5.4 4.03 4.81 17.24 6.46 6.45 3.87 8.41 8.41 6.77 4.97 2.53 Max TE PBR TE/PBR 0.53

Mg Mr D Pacic Mg Mr D Atlantic Mg Mr D Indian Ocean Mg Mr D Arctic Mg Mr D Antarctic Mg Mr D Mediterranean Mg Mr D

0.53 3.32 0 4.97 0.02 4.18 0.53 3.09 0.71 4.16 0.04 5.03 0.96 4.71 0.81 3.94 0.02 5.03 1.03 3.45 0.77 2.58 0.02 2.44 0.89 11.34 1.2 4.66 0.02 2.91 0.72 2.79 0.0 9.41 0.2 6.71 1.22 3.66 0.9 2.69 0.67 1.46

8.94 271.5 9.90 155.4 8.62 99.00 6.78 191.33 9.12 257.3 9.74 99.00 13.12 271.5 10.99 227.34 6.67 67.68 8.48 269.86 6.33 201.38 6.82 59.07 17.45 158.19 6.61 180.14 8.78 55.53 3.97 108.06 8.35 47.91 8.02 59.73 10.72 156.07 7.88 114.68 2.72 13.51

0.16 0.30

0.10 0.14

0.71

0.16 0.35

0.46

0.16 0.40

0.40

0.16 0.17

0.94

0.16 0.25

0.64

0.18 0.44 0.41

Table A.3 Model tuned to basin (Fig. 1A. North and South are separated at the equator) and level of primary production. indicates different bin sizes. Region Global PP level High Medium Low High Medium Low High Medium Low High Medium Low High Medium Low High Medium Low High Medium Low High Medium Low High Medium Low High Medium Low Mean PP 59 10 2.7 51.73 10.21 1.75 66.45 9.79 1.57 78.83 13.43 2.83 91.4 10.14 2.48 52.8 13.77 5.91 42.33 6.72 2.51 55.92 6.53 2.91 36.38 19.34 7.28 11.64 7.72 5.57 SD PP 43 6.3 0.36 29.1 6.35 1.34 37.65 5.02 1.26 71.94 6.62 0.23 56.6 5.89 0.37 34.98 6.21 0.71 2.01 2.67 0.33 23.87 4.11 0.17 8.18 5.25 0.82 1.93 0.89 0.44 n 549 7880 637 225 2948 534 53 678 108 92 1426 26 20 354 89 84 569 14 2 683 44 26 986 68 25 126 2 13 27 12 TE 0.16 0.16 0.19 0.14 0.18 0.17 0.13 0.19 0.2 0.12 0.1 0.19 0.16 0.2 0.16 0.17 0.16 0.15 0.14 0.18 0.14 0.18 0.11 0.16 0.13 0.16 0.12 0.14 0.12 0.11 PBR 0.63 0.24 0.34 0.38 0.21 0.05 0.9 0.28 0.07 0.75 0.2 0.08 0.96 0.49 0.15 0.56 0.34 0.07 0.82 0.72 0.33 0.7 0.13 0.04 0.76 0.28 0.13 0.48 0.54 0.19 TE/PBR 0.25 0.67 0.56 0.36 0.88 3.2 0.14 0.68 2.81 0.16 0.52 2.31 0.16 0.41 1.07 0.3 0.47 2.15 0.17 0.26 0.42 0.25 0.88 4.25 0.17 0.56 0.92 0.28 0.23 0.59

North Pacic

South Pacic

North Atlantic

South Atlantic

North Indian Ocean

South Indian Ocean

Antarctic

Arctic

Mediterranean

References
Ahrens, M., Peters, R., 1991. Patterns and limitations in limnoplankton size spectra. Canadian Journal of Fisheries and Aquatic Sciences 48 (10), 19671978. Batten, S., Welch, D., 2004. Changes in oceanic zooplankton populations in the northeast Pacic associated with the possible climatic regime shift of 1998/1999. Deep Sea Research Part II 51, 863873. Beare, D., Batten, S., Edwards, M., McKenzie, E., Reid, P., Reid, D., 2003. Summarising spatial and temporal information in CPR data. Progress In Oceanography 58 (24), 217233. Beaugrand, G., Ibanez, F., Lindley, J., 2003. An overview of statistical methods applied to CPR data. Progress In Oceanography 58 (24), 235262.

K.H.P. Strmberg et al. / Journal of Marine Systems 78 (2009) 1827 Robinson, I., 2004. Measuring the Oceans From Space the Principles and Methods of Satellite Oceanography. Springer-Praxis Publishing Ltd, Chichester, UK. San Martin, E., Irigoien, X., Harris, R., Lopez-Urrutia, A., Zubkov, M., Heywood, J., 2006. Variation in the transfer of energy in marine plankton along a productivity gradient in the Atlantic ocean. Limnology and Oceanography 51 (5), 20842091. Smyth, T., Tilstone, G., Groom, S., 2005. Integration of radiative transfer into satellite models of ocean primary production. Journal of Geophysical Research-Oceans 110, C10014. doi:10.1029/2004JC002784.

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Sprules, W., Munawar, M., 1986. Plankton size spectra in relation to ecosystem productivity, size, and perturbation. Canadian Journal of Fisheries and Aquatic Sciences 43 (9), 17891794. Wiebe, P., 1988. Functional regression equations from zooplankton displacement volume, wet weight, dry weight and carbon. A correction. Fishery Bulletin 86 (4).