# Geographical distribution and seasonal and diel changes in the diversity of calanoid copepods in the North Atlantic and North Sea

G Beaugrand, F Ibanez, Ja Lindley

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G Beaugrand, F Ibanez, Ja Lindley. Geographical distribution and seasonal and diel changes in the diversity of calanoid copepods in the North Atlantic and North Sea. Marine Ecology Progress Series, 2001, 219, pp.189-203. 10.3354/meps219189. hal-03483070

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# Geographical distribution and seasonal and diel changes in the diversity of calanoid copepods in the North Atlantic and North Sea

Grégory Beaugrand<fnref n="1" />,<fnref n="2" />*, Frédéric Ibañez<fnref n="2" />, J. Alistair Lindley<fnref n="1" />

**ABSTRACT:** This paper examines spatial distribution in the pelagic diversity of calanoid copepods in the North Atlantic and the North Sea, taking into account changes at seasonal and diel scales. Based on 40 yr of sampling by the Continuous Plankton Recorder (CPR) survey, the diversity (as number of taxa) was estimated on a regular grid for each month and time of day. Principal components analysis (PCA) allowed spatial decomposition of diversity, detection of major seasonal and diel patterns, the location of regions where these occur, and finally the modelling of temporal changes at seasonal and diel scales. The results underline the importance of hydrography and topography in the regulation of pelagic diversity. By considering these abiotic factors and the characteristics of seasonal and diel changes in diversity, a partition of the North Atlantic and the North Sea is proposed. This demonstrates the importance of the warm North Atlantic Current and the continental slope currents and undercurrents along the European Continental Shelf. It is suggested that modification in the path or intensity of these currents could imply marked changes in the structure and functioning of ecosystems west and north of the British Isles.

**KEY WORDS:** Pelagic diversity · Calanoid copepods · Spatial distribution · Seasonal variations · Diel changes · Continuous Plankton Recorder (CPR) survey

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## INTRODUCTION

Knowledge about geographical distribution of plankton in the northern North Atlantic has been intensively documented from the Continuous Plankton Recorder (CPR) survey (Edinburgh Oceanographic Laboratory 1973). Seasonal and year-to-year fluctuations of plankton have also largely been investigated (e.g. Colebrook 1984, Lindley 1987, Reid et al. 1998, Beaugrand et al. 2000a). On the other hand, little attention has been devoted to the analysis of spatial changes in pelagic diversity at various temporal scales, and the literature on this remains scarce (Lindley 1998, Beau-

grand et al. 2000b). Nevertheless, this diversity is a key biological property of the structure and function of ecosystems.

Examination of biodiversity at the scale of the North Atlantic should take into consideration that present-day geographic distribution patterns have been established at many scales (Angel 1997). At the geological scale, events such as continental drift have led to the opening or closure of sea ways and modification of oceanic circulation. Insolation variations at the Earth's surface resulting from orbital forcing (e.g. Milankovitch cycles) have a large influence on the climate and may have played an important role in the origin of large-scale patterns in biodiversity (Crame 1993, Molfino 1994). These large-scale factors are probably responsible for the polar-tropical difference in the num-

<footnote n="1">¹Sir Alister Hardy Foundation for Ocean Science, The Laboratory, Citadel Hill, Plymouth PL1 2PB, United Kingdom</footnote>

<footnote n="2">²Observatoire Océanologique, Laboratoire d'Océanologie Biologique et Écologie du Plancton Marin, BP 28, 06230 Villefranche sur mer, France</footnote>

<footnote>*E-mail: gbea@wpo.nerc.ac.uk</footnote>
ber of species reported in the literature (e.g. Ruddiman
1969, Rex et al. 1993, Rosenzweig 1995, Rohde 1997,
Rutherford et al. 1999). However, smaller-scale pro-
cesses may also contribute, through biogeographic or
ecological factors, to the regulation of diversity (Beau-
grand et al. 2000b).

A comprehensive map of the mean spatial distribu-
tion of biodiversity of calanoid copepods has been
recently proposed for the North Atlantic and the North
Sea (Beaugrand et al. 2000b). Based on 168 162 CPR
samples, it was possible to detect mesoscale (ca 200 km)
spatial features in pelagic biodiversity at an oceanic
basin level for the first time. In addition, each month
and time of day were considered, with the same
weight, to eliminate spatial difference due to the
temporal heterogeneity of sampling. Results have de-
monstrated a pronounced local variability and an east-
west asymmetry in the spatial patterns of diversity of
calanoid copepods. In the present study, we examine
spatial changes in the diversity of this taxonomic group
more finely by combining a diversity index and mul-
tivariate techniques. Principal components analysis
(PCA) was used: (1) to detect the average locations of
ecological regions and boundaries over the North
Atlantic, (2) to identify regions with a distinct seasonal
and day-night pattern, and (3) to statistically model
seasonal and diel changes in diversity in this region.
On the basis of these results, we outline a partition
scheme for the North Atlantic. Finally, the results are
discussed in a global context demonstrating the im-
portance of the North Atlantic Current and the Euro-
pean Continental Shelf Current in the maintenance
and regulation of diversity in the North Atlantic Drift
Province.

MATERIALS AND METHODS

The Continuous Plankton Recorder (CPR) survey is
an upper-layer plankton monitoring programme in the
North Atlantic and North Sea based on consistent
methods of sampling and analysis of plankton since
1948 (Warner & Hays 1994). Sampling is carried out by
a high-speed plankton recorder (ca 20 km h⁻¹) that is
towed behind voluntary merchant ships at a standard
depth of ca 6.5 m (Hays & Warner 1993). Plankton is
filtered by a slowly moving band of silk with an aver-
age mesh size of 270 µm taking samples corresponding
to approximately 3 m³ of seawater filtered per sample
(Hays 1994). Methods of counting and data-processing
have been described by Colebrook (1960, 1975) and
Warner & Hays (1994).

Calanoid copepods (108 taxa) were selected because
of their key position in the food web (e.g. Williams et al.
1994) and because CPR sampling and identification are

optimal with these taxa. Indeed, in most cases (92.5 %)
the organisms can be identified to species level, except
for small calanoids for which identification is limited to
genus level, and *Para-Pseudocalanus* which are not dis-
tinguished in routine analysis. Even though this group
combines species (mainly *Pseudocalanus elongatus* and
*Paracalanus parvus*) which may display different be-
haviour at diel and seasonal scales, we chose to keep
this group because it represents a major component
of the plankton diversity in the survey area. Data
(168 162 samples) from January 1958 to December 1997
have been used, as the taxonomic resolution of analysis
remained unchanged over this period.

Data in the CPR database are coded in such a way
that local time is known for each sample. In this pre-
sent work, we have directly used this information. For
each of the 168 162 samples, diversity as the average
number of taxa per CPR sample (i.e. taxonomic rich-
ness for each CPR sample) was first calculated. We
used this qualitative index as some rare taxa (e.g. *Can-
dacia varicans*, *Heterostylites longicornis*) are re-
corded as presence/absence in the CPR database. Data
was then clustered by 2 h periods from 0:00 to 24:00 h
for each month, integrating 40 yr sampling. Thus, 144
subgroups of data were constituted (12 mo × 12 two h
periods). For example, Subgroup 5 contained all CPR
data for 10:00 to 12:00 h in January.

Another problem arose from the spatial heterogene-
ity of the CPR sampling. The number of samples and
their locations vary between regions. Spatial regulari-
sation for each subgroup of samples was thus needed.
This was achieved by an inverse square-distance inter-
polation method (Lam 1983). Latitude and longitude
were transformed to conical Lambert coordinates
(Planque et al. 1997), an equal-area polar projection
that allowed surfaces on the map to be proportional to
actual surfaces over the survey area and thus avoided
a strong alteration of distances on the map (Richardus
& Adler 1972). A grid of 50 × 50 n. mile was selected,
and interpolation of diversity value was made by using
a search radius of 250 n. mile. As the diversity index
we used is very sensitive to sample size, the number of
neighbours selected is constant throughout each map
and equal to 10. If <10 neighbours were found inside
the search area, no estimation of diversity was per-
formed; if >10 neighbours were detected, the 10 near-
est were used to estimate the number of taxa (Beau-
grand et al. 2000b). The resulting 144 matrices were
combined to construct a general data table within
which each row denotes a geographical location and
each column a 2 h period for a specific month.

This general data table was analysed using PCA.
Firstly, from each diversity value of the general data
table we subtracted the mean diversity value of its
column. As the general data table was homogeneous,
it was not divided by the standard deviation. Thus, this analysis was computed on a variance-covariance matrix of 1046 × 1046 pixels. Secondly, the most important eigenvectors and principal components were examined with the aim of detecting major different regions over the North Atlantic and the North Sea and monthly and diel patterns of diversity. Finally, values of diel and seasonal variations were re-estimated from the first 4 eigenvectors and principal components. This step allowed elimination of the non-explicative variability, which may have been related to the characteristics of the CPR sampling, the well-known patchy distribution of calanoid copepods, or to some year-to-year differences in the boundaries between different regions.

Seasonal changes were examined by considering day (light) and night (dark) periods separately. As these vary seasonally and with latitude (Fig. 1), only 2 h periods of the dark or the light periods for the whole area were selected to characterise the seasonal cycle of calanoid diversity (Fig. 1). A slight overlapping of both the sunrise and sunset times and the selected 2 h periods occurred in June at about 64°N. However, cluster analyses (not shown) for each month demonstrated that this feature had no significant influence on spatial changes in diversity at a diel or monthly scale.

## RESULTS

Fig. 2 maps the first 4 eigenvectors (EV 1 to 4) and shows monthly and diel changes from January to December of the corresponding principal components (PC 1 to 4), based on the integration of 40 yr CPR sam-

<figure><img src="image_2.png" /><figcaption>Fig. 1. Seasonal changes in daylight and dark periods. Hours (Greenwich Mean Time) of sunset and sunrise are indicated for latitudes 45°N (continuous black lines) and 64°N (continuous grey lines). Shading denotes latitudinal variations in sunset and sunrise times; black dashed lines indicate 2 h periods selected for examination of seasonal variations in diversity at night, grey dashed lines denote 2 h periods selected for examination of seasonal variations in diversity during day</figcaption></figure>

pling and representing a total explained variance of 62.95%. The monthly and diel plots of the first principal component (Fig. 2A, 47.83%) shows strong diel variations throughout the year. These diel changes were more pronounced from April to October. Seasonal variations were also detected, but were weaker than diel changes. Minimum values and intensity of the diel variations were recorded during winter. As the first eigenvector (EV1) is only composed of positive values, high values (in red on EV1 in Fig. 2A) indicate regions where monthly and diel changes were followed. This pattern was mainly present in the southwestern part of the North Atlantic Drift Province, as defined by Longhurst (1998).

PC2 (Fig. 2B, 8.36%) highlights seasonal changes in diversity, although diel variations are still clearly detectable for almost all months. Diel changes appeared to be stronger in spring, autumn and winter and weaker in summer. The corresponding eigenvector (EV2, Fig. 2B) displays both negative and positive values. High negative values should be negatively related to the PC2 signal and high positive values should be positively related to the eigenvector elements. Thus, the northern part of the North Atlantic Drift Province, the southern part of the Atlantic Subarctic Province and the North Sea displayed large seasonal changes in diversity (with high values mainly in summer) and weaker diel changes. In contrast, regions south of 50°N displayed high diversity mainly in spring, with higher diel variations.

PC3 (Fig. 2C, 4.59%) shows the seasonal contrast between spring and autumn months. The high negative values of EV3 (Fig. 2C) in the Bay of Biscay region were related to high negative PC3 values (and also high diversity) during spring, and the high positive values in the Gulf Stream extension reflected high PC3 values (and also high diversity) mainly during autumn. Diel changes were detectable for these periods and regions.

PC4 (Fig. 2D, 2.17%) reveals 2 seasonal strongly positive periods in March and April and in July to October. May, June and the winter months were characterised by high negative values. Examination of EV4 shows this pattern to be positively related to the Iberian coast region. Examination of the original matrix showed that PC4 corresponds to seasonal variations in diversity in this region.

The original matrix was re-estimated using the first 4 eigenvectors and principal components that accounted for 62.95% of the total variance. Examination of residual variation (37.05%, not shown) revealed no clear spatial pattern, indicating that the first 4 principal components provide a relatively accurate model of diel and seasonal variations in diversity. The recalculated matrix was of great advantage for showing diel and
<figure><img src="image_3.png" /><figcaption>Fig. 2. First 4 eigenvectors (EV 1 to 4) and monthly and diel changes in corresponding principal components (PC 1 to 4). When an eigenvector is composed only of positive values, high values indicate regions where monthly and diel changes in the corresponding principal components occur (EV1 and PC1). When an eigenvector is composed of both negative and positive values, high positive values denote regions that contribute to positive part of the principal component and high negative values indicate regions contributing to negative part of the principal component (remaining eigenvectors and corresponding principal components). Arrows above each graph indicate midnight, and dashed vertical lines between these midday</figcaption></figure>
seasonal variations. The unexplained variance (37.05%) may mainly have been due to the well-known patchy distribution of calanoids, the CPR sampling method or the integration of 40 yr CPR sampling; some anomalous years may have contributed to an increase of variance. Thus, elimination of this unexplained variance allowed seasonal and diel patterns in diversity to be clarified.

Fig. 3 shows diel patterns in taxonomic diversity for calanoids in the North Atlantic and North Sea. From 0:00 to 4:00 h and from 20:00 to 24:00 h (periods 0:00–2:00, 2:00–4:00, 20:00–22:00, 22:00–24:00 h), a south-north difference occurred with higher diversity in south. An east-west difference was also apparent between 50 and 60°N as high diversity spread further north in the east. Diversity was especially high over the Gulf Stream extension and the Bay of Biscay. Southeast North Sea diversity is less elevated than for these 2 areas. The periods 4:00–6:00 and 18:00–20:00 h were

still characterised by high diversity in the Bay of Biscay and the Gulf Stream extension, although this decreased elsewhere. From 6:00 to 18:00 h (periods 6:00–8:00, 8:00–10:00, 10:00–12:00, 12:00–14:00, 14:00–16:00, 16:00–18:00 h), the southeast North Sea was characterised by a higher taxonomic diversity. Diversity was also higher over the European shelf break, although this phenomenon was not evident on the American side. The difference between diurnal and nocturnal taxonomic richness increased with decreasing latitude in the survey area: Fig. 4 shows the degree of diel variation in taxonomic diversity, corroborating the difference and highlighting the contrast between continental shelves and the open ocean. Diel variation was particularly weak in the southeast North Sea, the American continental shelf, the European shelf break and off northwest Portugal, and was highest in the Gulf Stream extension to 20°W in the southern part of the study area.

<figure><img src="image_4.png" /><figcaption>Fig. 3. Re-estimated diel changes in diversity of calanoids from first 5 principal components, which allowed unexplained variance to be removed and better detection of the diel signal. Average values, based on integration of all months. Units are mean number of taxa per CPR sample</figcaption></figure>
<figure><img src="image_5.png" /><figcaption>Fig. 4. Coefficient of variation (%) of diversity of calanoids within each pixel (calculated from matrix used to represent diel changes in Fig. 3), indicating regions where diel variation was highest</figcaption></figure>

The strong contrast between day and night indicated a need to interpret diurnal and nocturnal seasonal changes in diversity separately. Fig. 5 shows seasonal patterns in diversity using only nocturnal data from the reestimated matrix (see Fig. 1). In January, diversity was higher in the Bay of Biscay and over the Gulf Stream extension. This pattern was strengthened in February and March. In April, all the southern parts of the studied area had a high diversity. This pattern was similar in May and June, although slightly decreasing in intensity for all regions and especially over the North American continental shelf. East of the Mid-Atlantic Ridge, high diversity started to spread northwards. From July to September, diversity clearly increased northwards between 20°W and the European continental shelf. During this

<figure><img src="image_6.png" /><figcaption>Fig. 5. Seasonal variations in diversity of calanoid copepods in night samples re-estimated from first 5 principal components. Average values, based on night samples (20:00 to 4:00 h) only. Units are mean number of taxa per CPR sample</figcaption></figure>
period, diversity was still low over the Newfoundland
shelf. From October to December, diversity declined in
northern areas, although it slightly increased south of
Newfoundland. In December, it was still high over the
Gulf Stream extension current. Fig. 6 indicates that
seasonal variation was much greater north of 55°N in
the northern part of the North Atlantic Drift Province
and the Atlantic Subarctic province (as defined by
Longhurst 1998). It remained especially low over the
American continental shelf and to the southwest of
Greenland. Low seasonal variations occurred over the
Celtic Shelf break and to the southeast of the North
Sea.

DISCUSSION

For pelagic taxa, global-scale patterns such as latitu-
dinal gradients have been documented using taxa
such as Foraminifera, Ostracoda, Euphausiacea, Deca-
poda and Pisces (Stehli et al. 1969, Reid et al. 1976,
Angel 1993, Pierrot-Bults 1997). However, these pat-
terns are far from constituting a cline of continual
decrease in the number of species from the equator to
the pole. Numerous tropical-polar gradients show a
maximum not at the equator but to either side of it
(Angel 1993, Rosenzweig & Abramsky 1993). Ruddi-
man (1969), investigating foraminiferan biodiversity in
the North Atlantic, stressed that the diversity gradient

was virtually erased by the strength of the diverse Sub-
tropical North Atlantic Gyre. On a global scale, Ruther-
ford et al. (1999) recently demonstrated that the diver-
sity of Foraminifera is maximum in middle latitudes,
minimum in high latitudes, and intermediate at the
equator.

Our study covered an area ranging from 40 to 67°N. Thus, our perception of this cline is limited to the extreme northward extension of the Subtropical North Atlantic Gyre, the Atlantic Polar and Subpolar Province and the transitional region between them. Nevertheless, the effects of the polar-tropical difference in diversity was clearly evidenced by this study (see for example Fig. 3). The results, however, also revealed a pronounced local spatial variability and a clear east to west asymmetry in the spatial distribution of taxonomic richness. The use of multivariate analysis in conjunction with a diversity index (here, the number of taxa per CPR sample) allowed separation of the spatial distribution of the diversity at diel and seasonal scales as well as partitioning of the North Atlantic and the North Sea. This partition will be discussed in relation to the hydrography, topography, seasonal and diel changes and the biogeochemical provinces recently proposed by Longhurst (1998). Table 1 summarises the main characteristics of the regions described in the following discussion.

The Gulf Stream extension region

The Gulf Stream extension is the
region with the highest diversity in the
study area (Figs 3 & 5, and Beaugrand
et al. 2000b). The centre of this region
is relatively small, ranging from 43 to
50°N and from 40 to 48°W (Fig. 2C). The
northern boundary of this tongue of
high diversity lies between 47 and 52°N
when seasonal fluctuations are consid-
ered (Fig. 5). High diversity originates
from the hydrographical processes asso-
ciated with the northern branching of
the Gulf Stream. Fig. 7 shows the major
surface currents over the North Atlantic
from a compilation of recent works. The
North Atlantic Current (NAC) flows
from 42°N, 48°W along the Canadian
Continental shelf going along the
4000 m isobath as far as Flemish Cap
(47°N, 45°W; Käse & Krauss 1996). It
then leaves the continental shelf, reach-
ing its northernmost extremity in an area
called ‘the Northwest Corner’ (51°N,
44°W; Worthington 1976). Subsequently,

<figure><img src="image_7.png" /><figcaption>Fig. 6. Coefficient of variation (%) of diversity of calanoids within each pixel (calculated from matrix used to represent seasonal changes [night samples] in Fig. 5), indicating regions where daily variation was highest</figcaption></figure>
<figure><img src="image_8.png" /></figure>

Fig. 7. Schematic representation of main surface and intermediate currents over North Atlantic based on compilation of findings or reviews from Krauss (1986), Sy (1988), Sy et al. (1992), Schmitz & McCartney (1993), Käse & Krauss (1996): Gulf Stream and the North Atlantic Current; van Aken & Becker (1996), Hansen & Osterhus (2000): northeastern currents; Madelain & Kerut (1978), John et al. (1998), Pingree & Le Cann (1990), Pingree (1993), Richardson et al. (2000): Bay of Biscay region; Ikeda et al. (1996), Petrie & Buckley (1996), Han & Tang (1999): Canadian region; Pingree et al. (1978), de Wilde et al. (1992): North Sea region. Currents = AC: Azores Current; CSC: Continental Shelf Current; CSIC: Continental Shelf Intermediate Current; EGC: East Greenland Current; FC: Faroe Current; IC: Irminger Current; LC: Labrador Current; MIC: Mediterranean Intermediate Current; NAC: North Atlantic Current; NWAC: Norwegian Atlantic Current; WGC: Western Greenland Current. Frontal structures = FF: Flamborough Front; IFF: Iceland-Faroe Front; OPF: Oceanic Polar Front. Other abbreviations = CGFZ: Charlie Gibbs Fracture Zone; FC: Flemish Cape; FF: Flamborough Front; GB: Grand Banks; HPC: High Pressure Cells; IMW: northern boundary of the influence of Mediterranean Water (1100 m of depth); NC: Northwest Corner; PB: Porcupine Bank; SWEB: South-West European Basin

it flows towards the Mid-Atlantic Ridge. Between the beginnings of the NAC and Flemish Cap, anticyclonic eddies occur, associated with high pressure cells (Käse & Zenk 1996). This pattern occurs when there is only 1 pressure cell along the Newfoundland ridge from 40 to 50°N, but the pressure cell can subdivide and open other water gateways eastwards (Fig. 7). Thus, the North Atlantic Current can diverge from the Canadian Continental shelf at Flemish Cap or even further southwards (Fig. 7), with a significant flow on the eastern flank of the cell turning southwards again and joining the Azores Current. This process could explain why the high diversity in this region is so restricted south of the Oceanic Polar Front (Figs 2C & 5). Considering only the EV3 and PC3 results (Fig. 2C), the northern limit of this high diversity with its associated temporal pattern seems to be localised more at Flemish Cap than at the Northwest Corner. This is consistent with high diversity in this latter region being connected only

with sporadic occurrences of the NAC (Käse & Zenk 1996). Our results, reinforced by results of hydrographic studies, clearly indicate that this small area differs significantly from the North Atlantic Drift Province (NADR). Käse & Krauss (1996) suggested that this area may be a direct continuation of the Atlantic Subtropical Gyre, and we propose that it be separated from the NADR to the west. The area probably corresponds to the northeastern part of the Gulf Stream extension province proposed by Longhurst (1998). However, examination of seasonal charts (Fig. 5) shows that the Northwest Corner clearly represents the northwest boundary for the seasonal spatial extension of high diversity. There is great similarity between these results and the recent map of eddy kinetic energy presented by Ducet et al. (2000).

Other processes may also contribute to enhanced diversity in this region. The path of the NAC along the Newfoundland ridge marks the separation between
<table><caption>Table 1. Diel and seasonal changes and abiotic factors characteristic of regions discussed in text. Boundaries are arbitrary and regions often overlap (see Figs. 2 to 7). Some regions are clearly definable only at specific periods of time (e.g. West European Basin) while others are more constant on both seasonal and diel scales (e.g. Atlantic Arctic Province). The general term 'regions' is used to avoid the word 'ecosystem', the usefulness and relevance of which for the pelagic are debatable (e.g. van der Spoel 1994). Effects of large-scale factors responsible for tropical–polar difference in diversity (e.g. latitudinal variation in energy, and historical factors) are not shown</caption><thead><tr><th>Provinces<br>(as defined by<br>Longhurst 1998)</th><th>Regions identified<br>in present study</th><th>Changes in diversity:<br>Seasonal</th><th>Diel</th><th>Main abiotic characteristics</th><th>Figs</th></tr></thead><tbody><tr><td>Gulf Stream;<br>North Atlantic<br>Drift</td><td>Gulf Stream<br>extension<br>(43–52° N, 40–48° W)</td><td>Slight, maximum in autumn.<br>Diversity still high in winter<br>compared to other regions</td><td>Strong</td><td>High subtropical influence and<br>strong hydrodynamic processes</td><td>2C, 3, 3,<br>4, 5, 6, 7</td></tr><tr><td>North Atlantic<br>Drift</td><td>Southwest North<br>Atlantic Drift<br>(south of 53°N,<br>west to 20° W)</td><td>Medium,<br>maximum in autumn</td><td>Strong</td><td>High hydrodynamic processes</td><td>2A, 3, 4,<br>5, 6, 7</td></tr><tr><td>North Atlantic<br>Drift</td><td>Southeast North<br>Atlantic Drift (south<br>of 53°N, east to the<br>Mid-Atlantic Ridge)</td><td>Medium,<br>maximum in spring</td><td>Medium</td><td>Low hydrodynamic processes,<br>spread of Intermediate<br>Mediterranean Water</td><td>2C, 3, 4,<br>5, 6, 7</td></tr><tr><td>North Atlantic<br>Drift</td><td>Northern North<br>Atlantic Drift (north<br>of 53°N, east of the<br>Mid-Atlantic Ridge</td><td>Strong,<br>maximum in summer</td><td>Weaker</td><td>High seasonal variability in<br>sea-surface temperature</td><td>2B, 3, 4,<br>5, 6, 7</td></tr><tr><td>Northeast<br>Atlantic Shelves;<br>North<br>Atlantic Drift</td><td>European<br>Continental<br>Shelf Break and<br>Bay of Biscay</td><td>Weak (stronger to north),<br>maximum from March<br>(south) to September (north)</td><td>Weak<br>(slightly<br>stronger<br>to south)</td><td>Topography (shelf edge)<br>Shelf-edge current<br>Intermediate Mediterranean<br>Water (south of about 50°N)</td><td>2B, 3, 4,<br>5, 6, 7</td></tr><tr><td>North Atlantic<br>Subtropical<br>Gyral</td><td>Portuguese and<br>Spanish west<br>coasts</td><td>Strong,<br>maximum in spring<br>and autumn</td><td>None<br>detected</td><td>Upwelling</td><td>2B, 3, 4,<br>5, 6, 7</td></tr><tr><td>Northeast<br>Atlantic Shelves</td><td>North Sea</td><td>Strong in northwest,<br>Weaker towards south<br>maximum in summer</td><td>Stronger towards<br>north and very<br>weak in<br>southeast</td><td>Boreal water influence to<br>northeast, coastal, warm-water<br>influence to southeast; north-<br>west influenced by advection<br>of warm North Atlantic Water</td><td>2B, 3, 4,<br>5, 6, 7</td></tr><tr><td>Atlantic Arctic</td><td>Atlantic Subarctic</td><td>Medium (stronger to east),<br>maximum in late summer</td><td>Medium</td><td>Subarctic water,<br>low hydrodynamic processes</td><td>3, 4, 5,<br>6, 7</td></tr><tr><td>Northwest<br>Atlantic Shelves</td><td>Canadian Continental<br>Shelf and Slope</td><td>Weak (stronger to east),<br>maximum in early spring<br>and late summer</td><td>Weak</td><td>Subarctic and arctic water,<br>Labrador current,<br>eddies in south</td><td>3, 4, 5,<br>6, 7</td></tr></tbody></table>

the Labrador Current to the west and subtropical water to the east. A contrast between these water masses is particularly seen from April to December with a maximum from May to August (Fig. 5). Mixing of these water masses occurs in the Newfoundland Basin through hydrographic processes such as stirring and extrusion of cold water related to the presence of anticyclonic eddies (Käse & Krauss 1996, Ducet et al. 2000). Subpolar species are probably imported increasing the number of taxa in this region. However, this process probably plays a minor role in comparison with the transport of subtropical species by the Gulf Stream extension.

## Southwest North Atlantic Drift Province

South of 53°N, the NADR can be subdivided into 2 by the Mid-Atlantic Ridge. In the western part (red region in Fig. 2A), the NAC spreads from the western margin of the Newfoundland basin to the Charlie Gibbs Fracture Zone (35 to 24°W, 52 to 53°N; Käse & Krauss 1996). The northmost flow of the NAC is located at about 52 to 53°N, and is closely related to the location of the Oceanic Polar Front (Sy 1988, Käse & Krauss 1996). From EV1 (Fig. 2A) and seasonal charts (Fig. 5), it is clear that the Oceanic Polar Front acts as a barrier to the spread of calanoid diversity
northwards. This front also corresponds to the north-
ern boundary of the region characterised by notable
diel changes and weak seasonal fluctuations in diver-
sity (Fig. 3). Fig. 5 shows the position of this front to be
seasonally stable, with its northernmost extension gen-
erally being reached from September to October.

Southeast North Atlantic Drift Province
(southwest European Basin)

In the southeastern part of the NADR (blue region in Fig. 2C), a seasonal maximum in number of taxa occurs during spring, with a decrease in summer (Fig. 5). A slight increase is observed in autumn; the seasonal minimum occurs in winter. Diel changes in diversity occur from January to July, with their highest amplitude in spring. This strong contrast to the seasonal and diel variations in the area to the west of the Mid-Atlantic Ridge may indicate a difference in plankton composition. The southwestern part of the NADR is distinguished by strong hydrodynamic processes (Ducet et al. 2000). Conversely, the southeastern part of the NADR between the North Atlantic Current and the Subtropical Gyre tends comprise relatively slack waters (Pingree 1993). Thus, many more subtropical species must be present in the western part. This area has also been identified by Strass (1990; his Fig. 4), Weeks et al. (1993; their Fig. 14), and Campbell & Aarup (1992; their Figs 1 & 7). This feature was also detected by Ottens (1991), who found a different planktonic foraminiferal assemblage above and below 50°N; he also detected another boundary at 44°N, which is south of the area covered by the present study.

Another explanation might account for the observed
differences. The area corresponds closely to the north-
ward spreading of Intermediate Mediterranean Water
(present Fig. 7, and Sy 1988, Käse & Zenk 1996, Richard-
son et al. 2000). This water mass has maximum influ-
ence at 1000 m depth, but its range extends from 600 to
2500 m (Käse & Zenk 1996). This could contribute to
different patterns of diel changes. It is still questionable
if such changes in the intermediate circulation would
influence the biological composition of subsurface
samples; however, it has been recently stressed that
Calanoides carinatus may use the Mediterranean
Outflow Water along the European Continental Slope
(John et al. 1998, see following subsection).

Northern part of North Atlantic Drift Province
(above 53°N)

The meridional distribution of diversity is much more
variable at a seasonal scale east of the Mid-Atlantic

Ridge above 53°N (Figs 5 & 6). This is closely linked to
spatial changes in the Oceanic Polar Front associated
with a modification of the path of the NAC northwards
(Fig. 7, Krauss 1986, Sy 1988). The western limit is
stable at diel and seasonal scales (Figs 3 & 5). The mean
northern boundary closely corresponds with the posi-
tion of the branching of the NAC west of Iceland
around the Reykjanes Ridge between 60 and 62°N
(Krauss 1995). One branch flows mainly across the
Iceland-Faroe Ridge toward the Norwegian Sea (van
Aken & Becker 1996), and seems to set the northern
average limit of the NADR between Iceland and Faroe
Islands. The other branch is the flow of the Irminger
Current towards the northwest. However, no link be-
tween this current and calanoid diversity was detected.
Other processes, such as forcing by temperature, might
control diversity, which has a high seasonal amplitude
in this area. This feature is clearly evident from Fig. 6.
Examination of seasonal charts indicated that the
northeastern boundary seasonally fluctuates and over-
flows into the Norwegian Sea in September (Fig. 5).

European continental shelf break and Bay of Biscay

That part of the European continental shelf extending
from 40 to 56°N also has high diversity, which spreads
westwards far beyond the Bay of Biscay (Beaugrand
et al. 2000b). Some species display clear subtropical
affinities (Poulet et al. 1996). The association of hydro-
dynamic processes with topography is complex in this
region (Koutsikopoulos & Le Cann 1996) and observed
patterns in diversity may result from the concurrence
of a large number of hydrographic processes such as
wind-driven or geostrophic currents, near-surface
tidal currents, undercurrents, and upwelling near the
Spanish and Portuguese coasts.

Surface circulation is sluggish, and varies seasonally
in the Bay of Biscay, being anticyclonic in summer and
cyclonic in winter (Pingree 1993). From October to
April, due to the dominance of southerly wind, a warm
and saline surface current flows polewards along the
Iberian coast (Pingree & Le Cann 1990, Drago et al.
1998, Castro et al. 2000). At Cape Finisterre, this
current penetrates eastwards into the southern part of
the Bay of Biscay. Fernandez & Bode (1994) reported
the presence of subtropical diatoms and dinoflagellates
between Cape Peñas and Cape Vidio, near the north-
ern Spanish coast, in December 1987. They attributed
this feature to an intensification of this surface current.

In contrast to surface currents, northward undercurrents are a permanent feature (Daniault et al. 1994). Between approximately 200 and 600 m, the Intermediate Slope undercurrent flows from the equator towards the north, transporting an admixture of South Atlantic Cen-
tral Water (John et al. 1998). This might also be a pos-
sible vector for the transport of subtropical or tropical
species. At greater depth, between 600 and 1400 m,
Intermediate Mediterranean Water also flows to the
north (Diaz del Rio et al. 1998). Based on multidiscipli-
nary evidence, John et al. (1998) showed that this
undercurrent could spread to the north beyond Cape
Finisterre and directly join the Celtic Slope at about 47
to 48° N, although another branch is still guided by the
continental slope and enters to the south of the Bay of
Biscay (Fig. 7). John et al. (1998) suggested that the
spatial distribution of species able to migrate at depth
(such as *Calanoides carinatus* in winter) is influenced
by Intermediate Mediterranean Water. Species inside
the 500 m depth water-column (such as *Calanus helgo-
landicus*) could be more influenced by the Continental
Slope Current. According to John et al. (1998), this
explains why the spatial distribution of *Calanus helgo-
landicus* is more restricted to the continental slope than
that of *Calanoides carinatus*, which can cross the
oceanic part from Cape Finisterre to the Celtic slope.
Factors linked to life history and behaviour of organ-
isms seem therefore to be also important in controlling
of diversity in this region. Slow surface currents may
also play a role in the subsequent spatial redistribution
of such species in the Bay of Biscay. As observed by
Hopkins et al. (1981) in the Gulf of Mexico, oceanic
species may penetrate into waters over the European
Continental Shelf Break and mix with neritic species.
Pseudo-oceanic species recorded in this region (e.g.
*Calanoides carinatus*, John et al. 1998, Beaugrand et
al. 2000b) also increase the number of taxa.

Portuguese and Spanish west coastal regions

At latitudes off Lisbon (38°N), seasonal intermittent
upwelling occurs from July to September (Wooster et
al. 1976). According to Colebrook (1979), they are
delayed by about 1 mo northward in the region
defined by EV4 and PC4 (Fig. 2D). In this region,
seasonal patterns in diversity are characterised by 2
seasonal maxima, 1 in spring and the other from
August to October. The second period corresponds to
the timing of the intensification of the Iberian up-
welling. To the north, off Cape Finisterre, the seasonal
pattern in diversity has 1 maximum in spring, indicat-
ing that local upwelling has no influence on diversity
at this scale.

North Sea

Examination of seasonal and diel changes (Figs 2, 3
& 5) revealed 2 main areas in the North Sea and 2

areas representing more transitional regions between
the major pelagic systems. South of the Flamborough
Frontal structure, which separates seasonally ther-
mally stratified water to the north and tidally mixed
water to the south (Fig. 7, and Pingree et al. 1978),
high diversity was detected (Figs 3 & 5). This area
is probably more influenced by warm Atlantic waters
than boreal Atlantic water. Local conditions such as
freshwater input from rivers such as the Rhine may
also exert an influence (Simpson et al. 1993). This
region is also distinguished by its own copepod com-
position. Species such as *Isias clavipes* are largely dis-
tributed throughout this area, although to the north
their occurrence is more restricted to the coast. No
clear seasonal and diel patterns were detected in the
south (Figs 2 & 3). The northeast North Sea has lower
diversity (Figs 3 & 5, and Beaugrand et al. 2000b).
There is a high abundance of *Calanus finmarchicus* in
this region (Planque & Fromentin 1996), indicating the
influence of boreal water.

Between these 2 major regions, a transitional zone
was detected in the Mixed Central North Sea Water
(Otto et al. 1990). These 3 regions roughly correspond
to the 3 major ecological subdivisions suggested by
some studies based on phytoplankton (Reid et al.
1990), zooplankton (Fransz et al. 1991) and fishes
(Daan et al. 1990). Examination of seasonal variability
revealed a fourth region in the northwest North Sea
that seems to have characteristics in common with the
northern part of the North Atlantic Drift Province
(Fig. 6). To the north of the Flamborough Front, the
number of taxa increases from March, reaching a
maximum in June to September, and then decreasing.
Seasonal changes in diel variations appear to be
localised after the appearance of stratification at the
end of spring (de Wilde et al. 1992).

Atlantic subarctic region

Atlantic subpolar and polar regions (Longhurst 1998)
have the lowest calanoid diversity in the study area
(Fig. 5, and Beaugrand et al. 2000b). This characteris-
tic is well-documented for these high-latitude areas
(Richter 1994, Angel 1997, Rutherford et al. 1999),
although the number of samples considered in the
present analysis allowed the average boundary to be
better defined. A large maximum in diversity occurs
from March to December, with a peak between July
and September (Fig. 5). Diel changes are detectable
throughout the year, except in winter when most spe-
cies such as *Calanus finmarchicus* overwinter at great
depth (Planque & Fromentin 1996). These seasonal
and diel variations are shared with the North Atlantic
Drift Province and the north and central part of the
North Sea, indicating that diversity differences be-
tween all these regions are directly due to differences
in the number of taxa. Many hypotheses have been
proposed to explain the low diversity in polar regions,
which comprises part of the large-scale tropical–polar
difference in diversity (e.g. Rohde 1992, Crame 1993,
Huston 1994, Rosenzweig 1995). It is not the purpose
of this publication to review all of these. However, it
appears that more than one hypothesis may explain
the low diversity of this region. Historical factors such
as the effects of the last glaciation, available energy
(temperature), area and environmental stress could all
possibly prevent or reduce diversity in this region.

Canadian continental shelf and slope

The Canadian continental shelf and slope display
low calanoid diversity (Figs 3 & 5, Beaugrand et al.
2000b). The Nova Scotian shelf has permanently
higher diversity in comparison to the eastern and
northern parts of the Canadian shelf. Diversity on the
Grand Banks is maximal from November to April and
minimal in summer. To the north, diversity declines,
reaching levels similar to the Atlantic Subarctic pro-
vince. This region is largely influenced by the southerly
Labrador Current which flows southwards along the
shelf break (Han & Tang 1999). There is a strong con-
trast between this region and the Gulf Stream exten-
sion to the east (Fig. 3), particularly from May to
December (Fig. 5). This last feature strongly differs
from that along the European continental shelf, where
high diversity is localised above the slope.

Seasonal and diel changes

Four major different patterns in seasonal and diel
fluctuations in the number of taxa were detected.
Some similarities exist with regions detected by Camp-
bell & Aarup (1992) based on seasonal patterns of sur-
face chlorophyll (Coastal Zone Color Scanner data).
North of ~50°N, the seasonal pattern of diversity
seems to conform to the pattern of the third region
described by Campbell & Aarup (1992) (Fig. 5). To the
south of 52°N, the seasonal pattern in diversity also
matches that of chlorophyll (the second zone described
by Campbell & Aarup). However, there is a clear dif-
ference between the southeast and southwest part of
the survey area, where diversity is still high in autumn
and even into the winter in the Gulf Stream extension
area. This latter area represents an intermediate pat-
tern between the first and second chlorophyll pattern
detected by Campbell & Aarup (1992). Diel changes
reinforce the difference between the 2 oceanic regions,

and indicate the presence of distinct pelagic assem-
blages (Fig. 3). The fourth region corresponds to the
upwelling region of the Iberian coast.

The spring bloom in the North Atlantic Drift Province
was intensively studied during the North Atlantic
Bloom Experiment (NABE) as part of the Join Global
Ocean Flux Study (JGOFS) in 1989. Sampling was
mainly along the 20°W meridian at approximately 47,
52, 56° and 60°N (Ducklow & Harris 1993, Lochte et al.
1993). At these latitudes, the spring bloom occurred
in mid-April, early May, mid-May and early June,
respectively (Joint et al. 1993); it was associated with
increasing water stability and coincided well with
modelling studies (Yentsch 1990). Reconstruction of
the seasonal signal from the first 4 principal compo-
nents clearly showed a large meridional variation in
diversity at a seasonal scale in the North Atlantic Drift
Province. Fig. 5 shows that the meridional variation
below 52°N, to the east of the Mid-Atlantic Ridge, cor-
responds with the onset of the spring bloom, which is
linked with the start of seasonal stratification (Weeks
et al. 1993). However, at 56 and 60°N, the bloom and
the increase in calanoid diversity appear to be unre-
lated, and there seems to be a delay of about 2 mo
between bloom and the increase in diversity. This
underlines the singularity of the region south of 52°N
and east of the Mid-Atlantic Ridge.

Many factors, such as northward advection, progres-
sion of summer stratification, sea temperature or food
availability may contribute to the delay between the
timing of the spring bloom and the diversity maximum
above 52°N (Carlotti et al. 1993, Planque et al. 1997,
Richardson & Verheye 1999). It is difficult to propose a
reasonable explanation from the results of the present
study. However, a bottom-up control of copepod diver-
sity within the limits imposed by the thermal environ-
ment can be envisaged. The results of the NABE
showed a clear change in the species contributing to
primary productivity (associated with a decrease in
diatoms) after the bloom (Joint et al. 1993, Weeks et al.
1993) as well as in the abundance of microzooplank-
ton, which was found to be correlated with phyto-
plankton standing crop (Burkill et al. 1993). Diversity
in the size fractions of the phytoplankton and micro-
zooplankton could have increased after the bloom,
and might explain why copepod diversity increased
2 mo later. Furthermore, Kleppel (1993) showed
that copepods have a high dietary diversity. Kleppel
& Burkart (1995) demonstrated that dietary diversity
enhanced egg production. The delay of 2 mo between
the bloom and increased copepod diversity would
arise from changes in community structure following
diatom dominance in the first part of the spring bloom
and the response to these changes by the mesozoo-
plankton.
Consideration of diel changes allowed discrimination between regions to be improved. Neither seasonal nor diel changes in diversity have ever been used with CPR data with the goal of identifying regions, although they comprise an important biological characteristic of pelagic ecosystems. Diel changes in diversity were more significant in the south than in the north (Figs 3 & 4), in direct contrast to seasonal variation (Fig. 6). Throughout the southwest European basin, diel changes are clearly important in spring. In the southwest, diel changes were clearly evident throughout the year, being weaker in winter. The persistence of diel changes in winter in the south indicates overwintering of some species in the epipelagic zone in this region. In contrast, in the north there are no diel changes in winter. This difference has a strong implication for the spring bloom. Colebrook (1979, 1982) first suggested that the spring bloom in the North Atlantic is underexploited by grazing, a result that also emerged from the NABE (Burkill et al. 1993, Dam et al. 1993, Joint et al. 1993). Colebrook (1984) showed that south of 44°N grazing had a significant impact on the termination of the spring bloom in contrast to more northern areas. Our results clearly show the presence of a copepod assemblage in the epipelagic stage during winter, and thus are in agreement with Colebrook's findings. However, 50°N seems to be a more appropriate boundary between the 2 regions.

## CONCLUSION

The combination of an index of diversity (here number of taxa per CPR sample) calculated at seasonal and diel scales and multivariate analysis (PCA) has allowed spatial decomposition of calanoid diversity, and partitioning of the North Atlantic and the North Sea has been proposed. In this region and at this scale, hydrography and topography play a major role in the regulation of diversity. Although these factors probably do not explain a large part of the tropical–polar difference in the diversity (for which energetic, geographic, historic, and environmental stress hypotheses have been proposed), they are of great importance in the spatial redistribution of diversity, which, considering the size of the spatial structures involved, probably occurs on year-to-year to multidecadal scales. Thus, detectable year-to-year or decadal changes in pelagic diversity in this region have probably already occurred, and are foreseeable in the future in response to climate changes. Considering a possible relationship between diversity and ecosystem function, which has yet to be demonstrated for the marine pelagic, although reported for other systems (e.g. Stachowicz et al. 1999, Tilman 1999), fluctuation in the diversity of calanoid

copepods key group could be accompanied by major changes in the structure and functioning of ecosystems. It is expected that the flow of the North Atlantic Current and the Continental Slope Current along the European Shelf Break, which determine the transportation rate of warm water to Europe (e.g. Bigg 2000, Hansen & Osterhus 2000) may greatly influence pelagic diversity. Thus, a modification in the path of these currents (e.g. Lehman & Keigwin 1992) could imply marked changes in the northeastern path of the North Atlantic Drift Province, the European Shelf Break and the North Sea.

*Acknowledgements.* The authors are grateful to all former and present members and supporters of the Sir Alister Hardy Foundation for Ocean Science, whose continuous efforts have allowed the long-term establishment and maintenance of the CPR data-set. We are particularly grateful to P. Christopher Reid, Arnold H. Taylor, Jean-Pierre Durbec, Martin Edwards and the 3 anonymous referees for advice and comments on the manuscript. The survey depends on the owners, masters and crews of the ships that tow the CPRs. This research was supported by the European Community Research Project No. MAS3-CT98-5058, the Netherlands (SAHFOS contract RKZ595), and the French programme 'Programme National en environnement côtier, thème: influence des facteurs hydroclimatiques ou anthropiques sur la variabilité spatio-temporelle des populations et écosystèmes marins' (PNEC art 4).

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