© 2005 International Council for the Exploration of the Sea
Variations in the distributions of Centropages chierchiae and Temora stylifera (Copepoda: Calanoida) in the north-eastern Atlantic Ocean and western European shelf waters
a Sir Alister Hardy Foundation for Ocean Science, The Laboratory Citadel Hill, Plymouth PL1 2PB, England, UK
b Institute of Marine Studies, University of Plymouth Drake Circus, Plymouth PL4 8AA, England, UK
*Correspondence to J. A. Lindley: tel: +44 1752 633133; fax: +44 1752 600015. e-mail: jal{at}sahfos.ac.uk.
Centropages chierchiae and Temora stylifera occurred rarely in the Continuous Plankton Recorder (CPR) survey in the Bay of Biscay, Celtic Sea, and English Channel before 1988. By 2000 they were found frequently and in abundance. The seasonal cycles of abundance of these species differ, C. chierchiae occurring mainly in the summer while T. stylifera was found most frequently in late autumn or winter towards the northern limits of its distribution. The increase in abundance of both species is related to temperature. However, in the years when it was found in the samples, the frequency of occurrence of C. chierchiae was correlated positively with the strength of the shelf edge current and negatively with the North Atlantic Oscillation (NAO) while the reverse was true for T. stylifera.
Keywords: Bay of Biscay, Celtic Sea, climate change, copepods, distributions, English Channel, seasonal cycles, zooplankton
Received 3 September 2004; accepted 23 February 2005.
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Introduction |
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In the period 1988–2000 the warm-water copepods associated with the shelf edge current to the west of the British Isles have occurred much further north than in earlier years (1948–1987) of the Continuous Plankton Recorder (CPR) survey (Beaugrand et al., 2002). Distributions have shifted by approximately 10° northward. There has been a great deal of attention paid to the increased warm-water component of zooplankton flowing into the North Sea (Lindley et al., 1990; Edwards et al., 1999; Holliday and Reid, 2001; Reid et al., 2001; Lindley and Batten, 2002). Beaugrand et al. (2000) analysed the patterns of change in common taxa in the plankton in waters to the southwest and south of the British Isles and north of the Iberian Peninsula, but otherwise variations in the plankton in this area have been less thoroughly described and analysed.
Centropages chierchiae Giesbrecht, 1889 and Temora stylifera Dana, 1849 are found in the tropical and sub-tropical waters, the former restricted to the eastern Atlantic, Mediterranean, and western Indian Ocean while the latter is known from all the oceans as well as the Mediterranean Sea and Red Sea (Razouls, 1996). The most northerly record of C. chierchiae in the references summarized by Razouls was that of Lysholm et al. (1945) who recorded the species off southwest Ireland at 50°13'N, 11°23'W in July 1910. The distribution of C. chierchiae in the CPR survey up to 1968 was limited to the southern Bay of Biscay and one record off the shelf edge southwest of Britain while T. stylifera occurred in the western English Channel and in the Gulf Stream to the south of the Grand Banks (Edinburgh Oceanographic Laboratory, 1973). In more recent years the two species have been more widespread in the Northeast Atlantic and the western European continental shelf (CPR Survey Team, 2004) and the species have been noted in the samples taken at Station L4 off Plymouth (http://www.pml.ac.uk/L4/). The results of monitoring of Iberian waters (Villate et al., 2004, http://www.seriestemporales-ieo.net/BDZoo/Santander/index.html) show that, in the southern Bay of Biscay, T. stylifera was present from the late 1980s and both species have occurred throughout the period from 1991 to 2000. Villate et al. (1997) suggested that T. stylifera can be a key species in monitoring climate changes in the Bay of Biscay. The objective of this study was to provide detailed information on the occurrence of these species in the CPR survey and to analyse the changes in relation to some environmental variables.
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Methods |
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Plankton sampling
The CPR survey has been described by Warner and Hays (1994). Ships-of-opportunity tow the recorders on regular routes at monthly intervals. The samples, each representing the plankton retained from approximately 3 m3 of seawater by a 280 µm mesh during 10 nautical miles (18 km) of tow, are analysed for phytoplankton and zooplankton. Sampling has been regular in the Celtic Sea since 1952 and in the English Channel and Bay of Biscay since 1957 (Warner and Hays, 1994). The Iberian coastal waters south of 42°N were only sampled from 1978 to 1986 and from 1997 onwards. Sampling in the Bay of Biscay east of the line between Ushant and Cape Finisterre was limited to a few tows in 1958 and 1959 and regular sampling from mid-1997 onwards.
Centropages chierchiae and T. stylifera are counted in a 1/50 subsample and their presence is noted in counts of total numbers of larger zooplankton. The variations in abundance were analysed using percentage of samples in which the species occurred because there was a significant proportion of records of presence in the total sample rather than counts in the subsamples. Records of C. chierchiae and T. stylifera in the CPR survey east of 20°W were extracted from the CPR database. Centropages chierchiae was first recorded in the samples in 1959 and the data analysed comprised the results from that year to 2000. The distributions of records of these species were plotted. The percentages of samples in which each species occurred in each calendar month over the years from 1959 to 2000 and in each year were calculated for each of the four areas; Iberian coastal waters (40–43°N, 9–11°W), Bay of Biscay (43–48°N, 1–11°W), Celtic Sea (48–53°N, 5–11°W), and English Channel (48–51°N, 0–5°W). The annual values for the last three areas were used in a correlation analysis with environmental variables.
Environmental data
The environmental variables used for analysis were sea surface temperature (SST), northern hemisphere temperature (NHT), the North Atlantic Oscillation (NAO), the Gulf Stream North Wall Index (GSNWI), transport through the Rockall Trough, and Lamb weather types for the British Isles. SST analyses were carried out using monthly mean data on a 1°x1° grid for the period 1959–2000 obtained from the Hadley Centre, http://www.met-office.gov.uk/research/hadleycentre/obsdata/GISST.html. This data set combines in situ sea surface observations and satellite derived estimates (Rayner et al., 2003). For each of the three regions, SST values were averaged per year and the maximum and minimum monthly temperatures for each year were extracted to provide unbroken 42-year time-series. The NAO values, based on the difference in atmospheric pressure between Reykjavik and Lisbon (Hurrell, 1995), were from http://www.cgd.ucar.edu/~jhurrell/nao.stat.winter.html#winter. The values for the Gulf Stream North Wall Index, a measure of the latitude at which the Gulf Stream diverges from the North American coast from 1966 onwards (Planque and Taylor, 1998), were from http://www.pml.ac.uk/gulfstream/. The modelled flow through the Rockall Trough, described further in Holliday and Reid (2001) and Reid et al. (2001), is a measure of the strength of the shelf edge current (SEC) from 1977 onwards. The Lamb weather types and northern hemisphere temperatures were from the Climate Research Centre, University of East Anglia (http://www.cru.uea.ac.uk/cru/data/). Lamb weather types are a classification of daily atmospheric pressure patterns over the British Isles and the values used are numbers of days per year of a weather type. Northern hemisphere temperatures are variance adjusted combined land and SST anomalies on a 5° x 5° grid.
Statistical analyses
For each region, relationships between frequency of occurrence of C. chierchiae or T. stylifera and temperature (SST or NHT) were identified using Pearson's correlation. To adjust for temporal autocorrelation in the abundance and temperature time-series, the correlation procedure was adapted according to the modified Chelton method (Pyper and Peterman, 1998). This procedure reduces the degrees of freedom and thus the significance level of the test procedure, but does not alter the correlation coefficients.
To identify general patterns among the three regions, the meta-analytical method of Worm et al. (2003) was used to combine individual correlation coefficients across the study domain. Fixed-effects meta-analytic models, which assume effect sizes are the same for all correlation coefficients, were found to be appropriate (Q non-significant).
When a large number of hypothesis tests such as correlations are conducted, the experiment-wise 
-level can be inflated (Peres-Neto, 1999). This was minimized by using a 1% significance level throughout and using the meta-analytic approach.
These species are at the northern limits of their distributions in the Bay of Biscay, Celtic Sea, and English Channel, so their occurrence in the area has almost certainly been limited by temperature. As a result there are many zero value variables in the data set, so the analyses of the other variables for each area were carried out using the data from years with non-zero values only. Therefore, the values of the correlation coefficients listed in Tables 2 and 3 later cannot be compared directly as levels required to reach significant probabilities vary according to the number of years of data included in each case.
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Results |
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Distributions
In the period 1978–1987 T. stylifera did not occur north of 42°N, so charts are presented showing the distributions of the two species in the period before 1978, from 1978 to 1987, and from 1988 to 2000 inclusive are shown in Figure 1. The records before 1978 add little to the distributions up to 1968 shown in Edinburgh Oceanographic Laboratory (1973). There was a contrast between the records of C. chierchiae, which showed some continuity with adjacent warmer water areas, and the more isolated occurrences of T. stylifera in the shelf areas around Brittany. From 1978 to 1987 the distribution of C. chierchiae was more widespread in contrast with the limited occurrence of T. stylifera. After 1988 both species have occurred much more frequently and over a wider area.
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Seasonal cycles
The monthly percentage of the total number of occurrences of each of the two species in each area of the three areas described above and the Iberian coastal area, 40–43°N east of 11°W are illustrated in Figure 2. Again there is an evident contrast between the species, C. chierchiae occurring most frequently in summer, while most records of T. stylifera were late autumn or winter.
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Year-to-year changes
There is a clear difference between C. chierchiae, which occurred regularly in the Bay of Biscay in earlier decades but increased to unprecedented values in 1997 and T. stylifera, which occurred more sporadically prior to 1988 and then increased steadily to reach record frequencies of occurrence (Figure 3).
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The results for the Bay of Biscay may have been influenced by the increase in numbers of samples and geographical change in sampling from 1997 onwards due to regular sampling east of 6°W between Ushant and Bilbao. However, the changes in the Bay of Biscay are consistent with those in the other two regions.
The local sea surface temperatures differ in detail but show a common pattern of temperatures declining from high values in 1959 to values generally below or near to the mean until 1989 (Figure 4a–c) after which higher values predominate. The NHT values contrast with the local SSTs in that after a slight fall to lower values in the mid-1960s and the 1970s there has been a more or less steady rise since 1977 with five of the six highest values since 1995 (Figure 4d). The higher local SST values in the period after 1989 match high NAO values over much of this period but there is a weaker relationship between the SST parameters and NAO in the early part of the time-series (Figure 4d). The shorter time-series for the GSI shows a period of low values in the 1970s and an increase comparable with that of NHT until 1995 and then low values in the late 1990s.The SEC series is the shortest, but this shows a peak in 1989 with more or less steady rise from the start of the series and a decline to 2000, with exceptionally high values in 1978, 1980, 1998, and 1999.The number of days of northwesterly weather over Britain is very variable but shows a slight overall decline, but within that the highest value was in 1979 and the values in 1998 and 1999, when C. chierchiae was abundant, were higher than most of the values for the 1990s.
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The analyses using the annual mean, maximum monthly mean, and minimum monthly mean SST and NHT up to 2000 are summarized in Table 1. The only correlations with p < 0.001 are those with NHT; the only coefficient not significant at that level was that with T. stylifera in the Celtic Sea. Similarly, the only correlations with annual mean SST for which p > 0.05 was for the same species and area. Centropages chierchiae was significantly correlated with the maximum monthly SST in the English Channel but with the minimum value in the other two areas. Temora stylifera was significantly correlated with maximum value in the Bay of Biscay and the English Channel and also with the minimum value in the former area.
Using the meta-analytic approach, the abundance of C. chierchiae throughout the study region was significantly related to mean SST (r = 0.37, Z = 3.24, p < 0.01) and NHT (r = 0.55, Z = 4.56, p < 0.0001). The abundance of T. stylifera was also significantly related to mean SST (r = 0.30, Z = 2.97, p < 0.01) and NHT (r = 0.39, Z = 2.81, p < 0.01).
Probability values in Table 1 were not adjusted for multiple correlations, but the number of very significant values and the results of the meta-analysis indicate the importance of temperature in influencing the abundance of these species in the studied areas.
The correlation analysis with climatic indices (GSI, NAO, SEC) using the only years in which each species was present provides possible indications of differing responses. The smaller number of years and hence the number of degrees of freedom in some cases means that levels of significance were lower than for the analyses of effects of temperature (Tables 2 and 3). The most consistent pattern was that the SEC was positively correlated with the frequency of occurrence of C. chierchiae and negatively with that of T. stylifera. The reverse was true for the NAO but only one correlation was significant. The number of days of northwesterly weather over the British Isles was positively correlated with C. chierchiae in the Celtic Sea but negatively with T. stylifera in the same area.
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Discussion |
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Beaugrand et al. (2002) found that the changes in distribution of planktonic copepods in the CPR survey were highly correlated with NHT with the NAO acting synergistically, indicating that the large-scale changes in the plankton were reflecting climatic influences on an ocean basin scale. The analyses here, showing stronger correlation with NHT than with parameters of local temperature, are consistent with their conclusions. In the case of the species studied here, which are on the northern fringe of their distributions in our sampling area, the frequencies of their occurrence in this area may have resulted from environmental variations closer to their long-term population centres.
The influence of temperature on species that are at the limits of their geographical ranges is unsurprising, but the higher correlations with NHT rather than parameters of local temperature may be considered interesting. Temora stylifera occurred regularly in the samples in 1988 in which year the NHT was at its highest value (0.271) since the start of the CRU time-series in 1856. This value was exceeded in 1990 (0.421), when T. stylifera started appearing regularly in the Celtic Sea and every year thereafter except for 1992, 1993, and 1996. The 1990 value was exceeded by 1995 (0.491), when T. stylifera was first recorded in the samples at Station L4 off Plymouth, and that was surpassed by 1998 (0.662) when C. chierchiae was at its most abundant in all three areas. Temora stylifera occurred less frequently in 1998 than in 1997 and 1999, when the local annual mean and maximum monthly mean temperatures were higher.
The time-series indicates that the arrival of a population of each of these two species in the Celtic Sea and English Channel in the 1990s is consistent with a spread of the population from more southern waters through the Bay of Biscay. However, while C. chierchiae occurred frequently in the Bay of Biscay in earlier years, the occurrences of T. stylifera appear more isolated. It is at least possible that the transport in ballast water may account for these occurrences, especially as the temperatures in the years of these earlier records were not exceptional.
The seasonal cycles of C. chierchiae are very similar to those of C. typicus in the English Channel and Celtic Sea (Lindley and Reid, 2002). Centropages typicus is a permanent inhabitant of these areas but unlike C. hamatus does not appear to produce diapause eggs. However, nauplii of this species have been hatched from sediments incubated in the laboratory (Lindley, 1990; Lindley and Reid, 2002) indicating that some subitaneous eggs are rendered dormant by burial in sediment. It would seem that by the late 1990s C. chierchiae had developed a resident population in the Celtic Sea and English Channel and the significant correlations with minimum temperature suggest that it persists mainly in the plankton rather than over-wintering as eggs. The seasonal cycles described here from the Bay of Biscay and Iberian coastal waters are similar to the frequent occurrence through late spring and summer in data from monitoring samples off Santander although lacking the clear June peak in those samples (http://www.seriestemporales-ieo.net/BDZoo/Santander/index.html).
The seasonal cycle of T. stylifera with its seasonal peak late in the year is consistent with the results from the southern coastal area of the Bay of Biscay in 1988–1990 (Villate et al., 1997) although the August peak off Santander (http://www.seriestemporales-ieo.net/BDZoo/Santander/index.html) is earlier than the maximum values in the CPR samples. Similar seasonal cycles have been reported from the northern Mediterranean (Gaudy, 1972; Razouls, 1973; Halsband-Lenk et al., 2001). However, summer maxima were found in Saronikos Gulf (Aegean Sea) by Siokou-Frangou (1996) and in Canary Island waters by Hernández-Leon (1998) using data from Corral (1970). The late seasonal maxima in more northern areas may, therefore, be due either to advection of populations from warmer waters or to temperature limitation to hatching or post-embryonic development. However, the higher correlations with maximum monthly mean temperatures than with minimum values suggest that the population is either absent or dependent on dormant eggs during the coldest months (February–March) at the northern limits of its range. Temora longicornis produces diapause eggs (Castellani and Lucas, 2003) but so far there is no evidence that T. stylifera does so, although Halsband-Lenk et al. (2001) reported two size groups of eggs; the larger eggs were produced in January and February.
The results of the analyses of differences between the species in the correlations with the SEC and the NAO, indicate that ecological differences between species will result in different responses to climate change. Lindley and Reid (2002) showed that although the abundances of both Calanus helgolandicus and C. typicus in the North Sea are highly positively correlated with temperature, deviations from the relationship have occurred in response to other environmental variables. Our results, therefore, support Villate et al. (1997) in suggesting that Temora stylifera can be a key species in monitoring climate changes in the Bay of Biscay (and now more northerly areas) but adding Centropages chierchiae would help to avoid dependence on the ecological characteristics of a single species.
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Acknowledgements |
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We acknowledge the work of the whole CPR survey team who have maintained the survey and produced the data presented and analysed in this paper. Anthony Richardson provided advice on statistics and carried out the meta-analysis. The survey would not be possible without the co-operation of the owners, masters, and crews of the many ships that tow the CPRs. The CPR survey is supported by public agencies in the UK, Canada, Denmark, France, Ireland, The Netherlands, Portugal, and the USA as well as the Commission of the European Communities, the International Oceanographic Commission, the Atlantic Salmon trust, Pacific EVOS trust, and the World Wildlife Fund. Part of this work was a thesis in partial fulfilment for a BSc degree. We thank R. C. Thompson, University of Plymouth, Sean Daykin's supervisor for his project. The Hadley Centre, UK Meteorological Office is thanked for providing the SST data (HadISST Version 1.1) at no cost. We are grateful for editorial comments and reviewers' recommendations.
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Footnotes |
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1 Present address: 11 Rother Close, Storrington, Pulborough, West Sussex RH20 3NX, England, UK.
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