Variations in the Distributions of Centropages Chierchiae and Temora Stylifera (Copepoda: Calanoida) in the North-Eastern Atlant

ICES Journal of Marine Science, 62: 869e877 (2005) doi:10.1016/j.icesjms.2005.02.009

Variations in the distributions of Centropages chierchiae and Temora stylifera (Copepoda: Calanoida) in the north-eastern Atlantic Ocean and western European shelf waters

J. A. Lindley and S. Daykin

Lindley, J. A., and Daykin, S. 2005. Variations in the distributions of Centropages chierchiae and Temora stylifera (Copepoda: Calanoida) in the north-eastern Atlantic Ocean and western European shelf waters. e ICES Journal of Marine Science, 62: 869e877.

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. Ó 2005 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved. Keywords: Bay of Biscay, Celtic Sea, climate change, copepods, distributions, English Channel, seasonal cycles, zooplankton. Received 3 September 2004; accepted 23 February 2005. J. A. Lindley: Sir Alister Hardy Foundation for Ocean Science, The Laboratory, Citadel Hill, Plymouth PL1 2PB, England, UK. S. Daykin: Institute of Marine Studies, University of Plymouth, Drake Circus, Plymouth PL4 8AA, England, UK. Present address: 11 Rother Close, Storrington, Pulborough, West Sussex RH20 3NX, England, UK. Correspondence to J. A. Lindley: tel: C44 1752 633133; fax: C44 1752 600015; e-mail: [email protected].

Introduction Centropages chierchiae Giesbrecht, 1889 and Temora stylifera Dana, 1849 are found in the tropical and sub- In the period 1988e2000 the warm-water copepods tropical waters, the former restricted to the eastern Atlantic, associated with the shelf edge current to the west of the Mediterranean, and western Indian Ocean while the latter is British Isles have occurred much further north than in known from all the oceans as well as the Mediterranean Sea earlier years (1948e1987) of the Continuous Plankton and Red Sea (Razouls, 1996). The most northerly record of Recorder (CPR) survey (Beaugrand et al., 2002). Distribu- C. chierchiae in the references summarized by Razouls was tions have shifted by approximately 10( northward. There that of Lysholm et al. (1945) who recorded the species off has been a great deal of attention paid to the increased southwest Ireland at 50(13#N, 11(23#W in July 1910. The warm-water component of zooplankton flowing into the distribution of C. chierchiae in the CPR survey up to 1968 North Sea (Lindley et al., 1990; Edwards et al., 1999; was limited to the southern Bay of Biscay and one record Holliday and Reid, 2001; Reid et al., 2001; Lindley and off the shelf edge southwest of Britain while T. stylifera Batten, 2002). Beaugrand et al. (2000) analysed the occurred in the western English Channel and in the Gulf patterns of change in common taxa in the plankton in Stream to the south of the Grand Banks (Edinburgh waters to the southwest and south of the British Isles and Oceanographic Laboratory, 1973). In more recent years north of the Iberian Peninsula, but otherwise variations in the two species have been more widespread in the the plankton in this area have been less thoroughly Northeast Atlantic and the western European continental described and analysed. shelf (CPR Survey Team, 2004) and the species have been

1054-3139/$30.00 Ó 2005 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved. 870 J. A. Lindley and S. Daykin noted in the samples taken at Station L4 off Plymouth Stream North Wall Index (GSNWI), transport through the (http://www.pml.ac.uk/L4/). The results of monitoring of Rockall Trough, and Lamb weather types for the British Iberian waters (Villate et al., 2004, http://www.seriestem- Isles. SST analyses were carried out using monthly mean porales-ieo.net/BDZoo/Santander/index.html) show that, data on a 1(!1( grid for the period 1959e2000 obtained in the southern Bay of Biscay, T. stylifera was present from the Hadley Centre, http://www.met-office.gov.uk/ from the late 1980s and both species have occurred research/hadleycentre/obsdata/GISST.html. This data set throughout the period from 1991 to 2000. Villate et al. combines in situ sea surface observations and satellite (1997) suggested that T. stylifera can be a key species in derived estimates (Rayner et al., 2003). For each of the monitoring climate changes in the Bay of Biscay. The three regions, SST values were averaged per year and the objective of this study was to provide detailed information maximum and minimum monthly temperatures for each on the occurrence of these species in the CPR survey and to year were extracted to provide unbroken 42-year time- analyse the changes in relation to some environmental series. The NAO values, based on the difference in variables. atmospheric pressure between Reykjavik and Lisbon (Hurrell, 1995), were from http://www.cgd.ucar.edu/~jhurrell/ Methods nao.stat.winter.html#winter. The values for the Gulf Stream North Wall Index, a measure of the latitude at which the Plankton sampling Gulf Stream diverges from the North American coast from The CPR survey has been described by Warner and Hays 1966 onwards (Planque and Taylor, 1998), were from http:// (1994). Ships-of-opportunity tow the recorders on regular www.pml.ac.uk/gulfstream/. The modelled flow through the routes at monthly intervals. The samples, each representing Rockall Trough, described further in Holliday and Reid the plankton retained from approximately 3 m3 of seawater (2001) and Reid et al. (2001), is a measure of the strength by a 280 mm mesh during 10 nautical miles (18 km) of tow, of the shelf edge current (SEC) from 1977 onwards. The are analysed for phytoplankton and zooplankton. Sampling Lamb weather types and northern hemisphere temperatures has been regular in the Celtic Sea since 1952 and in the were from the Climate Research Centre, University of East English Channel and Bay of Biscay since 1957 (Warner and Anglia (http://www.cru.uea.ac.uk/cru/data/). Lamb weather Hays, 1994). The Iberian coastal waters south of 42(N types are a classification of daily atmospheric pressure were only sampled from 1978 to 1986 and from 1997 patterns over the British Isles and the values used are onwards. Sampling in the Bay of Biscay east of the line numbers of days per year of a weather type. Northern between Ushant and Cape Finisterre was limited to a few hemisphere temperatures are variance adjusted combined tows in 1958 and 1959 and regular sampling from mid- land and SST anomalies on a 5( ! 5( grid. 1997 onwards. Centropages chierchiae and T. stylifera are counted in a 1/50 subsample and their presence is noted in counts of Statistical analyses total numbers of larger zooplankton. The variations in For each region, relationships between frequency of abundance were analysed using percentage of samples in occurrence of C. chierchiae or T. stylifera and temperature which the species occurred because there was a significant (SST or NHT) were identified using Pearson’s correlation. proportion of records of presence in the total sample rather To adjust for temporal autocorrelation in the abundance and than counts in the subsamples. Records of C. chierchiae temperature time-series, the correlation procedure was and T. stylifera in the CPR survey east of 20(W were adapted according to the modified Chelton method (Pyper extracted from the CPR database. Centropages chierchiae and Peterman, 1998). This procedure reduces the degrees of was first recorded in the samples in 1959 and the data freedom and thus the significance level of the test analysed comprised the results from that year to 2000. The procedure, but does not alter the correlation coefficients. distributions of records of these species were plotted. The To identify general patterns among the three regions, the percentages of samples in which each species occurred in meta-analytical method of Worm et al. (2003) was used to each calendar month over the years from 1959 to 2000 and combine individual correlation coefficients across the study in each year were calculated for each of the four areas; domain. Fixed-effects meta-analytic models, which assume Iberian coastal waters (40e43(N, 9e11(W), Bay of effect sizes are the same for all correlation coefficients, Biscay (43e48(N, 1e11(W), Celtic Sea (48e53(N, were found to be appropriate (Q non-significant). 5e11(W), and English Channel (48e51(N, 0e5(W). When a large number of hypothesis tests such as The annual values for the last three areas were used in correlations are conducted, the experiment-wise a-level a correlation analysis with environmental variables. can be inflated (Peres-Neto, 1999). This was minimized by using a 1% significance level throughout and using the Environmental data meta-analytic approach. The environmental variables used for analysis were sea These species are at the northern limits of their surface temperature (SST), northern hemisphere tempera- distributions in the Bay of Biscay, Celtic Sea, and English ture (NHT), the North Atlantic Oscillation (NAO), the Gulf Channel, so their occurrence in the area has almost Variations in the distributions of C. chierchiae and T. stylifera 871

Figure 1. The geographical distribution of occurrences of C. chierchiae and T. stylifera in CPR samples east of 20(W in the years 1959e1977, 1978e1987, and 1988e2000. Note that the Iberian coastal waters south of 42(N were only sampled from 1978 to 1986 and from 1997 onwards and the Bay of Biscay east of the line between Ushant and Cape Finisterre was sampled only on a few occasions in 1958 and 1959 and regularly from mid-1997 onwards. certainly been limited by temperature. As a result there are values of the correlation coeﬃcients listed in Tables 2 and 3 many zero value variables in the data set, so the analyses of later cannot be compared directly as levels required to the other variables for each area were carried out using the reach signiﬁcant probabilities vary according to the number data from years with non-zero values only. Therefore, the of years of data included in each case. 872 J. A. Lindley and S. Daykin

Results English Channel 50 Distributions C. chierchiae 40 T. stylifera In the period 1978e1987 T. stylifera did not occur north of 30 42(N, so charts are presented showing the distributions of the two species in the period before 1978, from 1978 to 1987, 20 and from 1988 to 2000 inclusive are shown in Figure 1. The 10 records before 1978 add little to the distributions up to 1968 0 shown in Edinburgh Oceanographic Laboratory (1973). JFMAMJJASOND There was a contrast between the records of C. chierchiae, Celtic Sea which showed some continuity with adjacent warmer water 50 areas, and the more isolated occurrences of T. stylifera in the 40 shelf areas around Brittany. From 1978 to 1987 the 30 distribution of C. chierchiae was more widespread in % contrast with the limited occurrence of T. stylifera. After 20 1988 both species have occurred much more frequently and 10 over a wider area. 0 JFMAMJJASOND Seasonal cycles Bay of Biscay The monthly percentage of the total number of occurrences 40 of each of the two species in each area of the three areas 30 described above and the Iberian coastal area, 40e43(N east of 11(W are illustrated in Figure 2. Again there is an 20 evident contrast between the species, C. chierchiae 10 occurring most frequently in summer, while most records of T. stylifera were late autumn or winter. 0 JFMAMJJASOND

Year-to-year changes Iberian coastal waters There is a clear difference between C. chierchiae, which 35 30 occurred regularly in the Bay of Biscay in earlier decades 25 but increased to unprecedented values in 1997 and 20 T. stylifera, which occurred more sporadically prior to 15 1988 and then increased steadily to reach record frequen- 10 cies of occurrence (Figure 3). 5 0 The results for the Bay of Biscay may have been JFMAMJJASOND influenced by the increase in numbers of samples and Months geographical change in sampling from 1997 onwards due to Figure 2. Seasonal cycles of occurrence of C. chierchiae and ( regular sampling east of 6 W between Ushant and Bilbao. T. stylifera in CPR samples in the English Channel, Celtic Sea, Bay However, the changes in the Bay of Biscay are consistent of Biscay, and Iberian coastal waters. Values on the y-axes are the with those in the other two regions. monthly percentage of the total number of records of each species The local sea surface temperatures differ in detail but in that area. show a common pattern of temperatures declining from high values in 1959 to values generally below or near to the mean until 1989 (Figure 4aec) after which higher values SEC series is the shortest, but this shows a peak in 1989 with predominate. The NHT values contrast with the local SSTs more or less steady rise from the start of the series and in that after a slight fall to lower values in the mid-1960s a decline to 2000, with exceptionally high values in 1978, and the 1970s there has been a more or less steady rise 1980, 1998, and 1999.The number of days of northwesterly since 1977 with five of the six highest values since 1995 weather over Britain is very variable but shows a slight (Figure 4d). The higher local SST values in the period after overall decline, but within that the highest value was in 1979 1989 match high NAO values over much of this period but and the values in 1998 and 1999, when C. chierchiae was there is a weaker relationship between the SST parameters abundant, were higher than most of the values for the 1990s. and NAO in the early part of the time-series (Figure 4d). The analyses using the annual mean, maximum monthly The shorter time-series for the GSI shows a period of low mean, and minimum monthly mean SST and NHT up to values in the 1970s and an increase comparable with that of 2000 are summarized in Table 1. The only correlations with NHT until 1995 and then low values in the late 1990s.The p ! 0.001 are those with NHT; the only coefficient not Variations in the distributions of C. chierchiae and T. stylifera 873

Centropages chierchiae 20 Bay of Biscay

Celtic Sea 15 English Channel

10 %

0 1950 1960 1970 1980 1990 2000

Temora stylifera 14

8 % 6

0 1950 1960 1970 1980 1990 2000 Figure 3. Interannual variations in the percentage of CPR samples in which C. chierchiae and T. stylifera were recorded in the English Channel, Celtic Sea, and Bay of Biscay. significant at that level was that with T. stylifera in the significance were lower than for the analyses of effects of Celtic Sea. Similarly, the only correlations with annual temperature (Tables 2 and 3). The most consistent pattern mean SST for which p O 0.05 was for the same species and was that the SEC was positively correlated with the area. Centropages chierchiae was significantly correlated frequency of occurrence of C. chierchiae and negatively with the maximum monthly SST in the English Channel but with that of T. stylifera. The reverse was true for the NAO with the minimum value in the other two areas. Temora but only one correlation was significant. The number of stylifera was significantly correlated with maximum value days of northwesterly weather over the British Isles was in the Bay of Biscay and the English Channel and also with positively correlated with C. chierchiae in the Celtic Sea the minimum value in the former area. but negatively with T. stylifera in the same area. Using the meta-analytic approach, the abundance of C. chierchiae throughout the study region was significantly related to mean SST (r Z 0.37, Z Z 3.24, p ! 0.01) and Discussion NHT (r Z 0.55, Z Z 4.56, p ! 0.0001). The abundance of T. stylifera was also significantly related to mean SST Beaugrand et al. (2002) found that the changes in (r Z 0.30, Z Z 2.97, p ! 0.01) and NHT (r Z 0.39, distribution of planktonic copepods in the CPR survey Z Z 2.81, p ! 0.01). were highly correlated with NHT with the NAO acting Probability values in Table 1 were not adjusted for synergistically, indicating that the large-scale changes in multiple correlations, but the number of very significant the plankton were reflecting climatic influences on an ocean values and the results of the meta-analysis indicate the basin scale. The analyses here, showing stronger correlation importance of temperature in influencing the abundance of with NHT than with parameters of local temperature, are these species in the studied areas. consistent with their conclusions. In the case of the species The correlation analysis with climatic indices (GSI, studied here, which are on the northern fringe of their NAO, SEC) using the only years in which each species was distributions in our sampling area, the frequencies of their present provides possible indications of differing responses. occurrence in this area may have resulted from environ- The smaller number of years and hence the number of mental variations closer to their long-term population degrees of freedom in some cases means that levels of centres. 874 J. A. Lindley and S. Daykin

English Channel a Mean

3 Max 2 Min 1 0 -1 -2 -3 -4 1950 1960 1970 1980 1990 2000

Celtic Sea b 3

-1

-2 Standard Deviations -3 1950 1960 1970 1980 1990 2000

Bay of Biscay c 3

-1

-2

-3 1950 1960 1970 1980 1990 2000

NHT d 3 NAO

2 GSI

1 SEC NW 0

-1

-2

-3 1950 1960 1970 1980 1990 2000 Year Figure 4. Standardized plots of mean SST, minimum monthly SST, and maximum monthly SST in (a) the Bay of Biscay, (b) the Celtic Sea, and (c) the English Channel. (d) Northern hemisphere temperature (deviation from 1961 to 1990 mean) (NHT), North Atlantic Anomaly (NAO), Gulf Stream North wall Index (GSI), shelf edge current (ﬂow through Rockall Trough) (SEC), and number of days of northwesterly weather over the British Isles (NW). Variations in the distributions of C. chierchiae and T. stylifera 875

Table 1. Correlations between the relative frequency of occurrence of C. chierchiae and T. stylifera in three areas and annual mean, maximum, and minimum monthly mean sea surface temperatures within those areas and northern hemisphere temperature. Signiﬁcance indicated by *(0.05 ! p ! 0.01), **(0.01 O p O 0.001), ***(0.001 O p). The modiﬁed Chelton method was used to adjust for autocorrelation. In all cases 42 years of data (1959e2000) were used.

Mean SST Max SST Min SST NHT

Bay of Biscay C. chierchiae 0.446** 0.293 0.428** 0.514*** T. stylifera 0.438** 0.464** 0.442** 0.525*** Celtic Sea C. chierchiae 0.307* 0.213 0.413** 0.566*** T. stylifera 0.139 0.149 0.276 0.221 English Channel C. chierchiae 0.368* 0.318* 0.222 0.602*** T. stylifera 0.389* 0.445** 0.114 0.538***

Table 2. Correlations between the relative frequency of occurrence (years with zero values excluded) of C. chierchiae and T. stylifera in three areas and the Gulf Stream Index (GSI), the North Atlantic Anomaly (NAO), and modelled ﬂow through the Rockall Trough (shelf edge current, SEC). The number of years of data (n) used in each case determines the number of degrees of freedom. Signiﬁcance indicated as in Table 1.

n GSI NAO SEC

Bay of Biscay C. chierchiae 30 0.16 ÿ0.03 0.45* T. stylifera 13 0.02 0.31 ÿ0.45* Celtic Sea C. chierchiae 7 ÿ0.37 ÿ0.61 0.59 T. stylifera 11 0.33 0.33 ÿ0.76** English Channel C. chierchiae 5 ÿ0.20 ÿ0.80 0.80 T. stylifera 13 ÿ0.07 0.57* ÿ0.27

Table 3. Correlations between the frequency of occurrence of C. chierchiae and T. stylifera in three areas and Lamb’s weather types. A Z anticyclonic, NW Z northwesterly, N Z northerly, S Z southerly, E Z easterly, W Z westerly, C Z cyclonic. The number of years of data used (hence the number of degrees of freedom) is the same as for the corresponding row in Table 2. Signiﬁcance indicated as in Table 1.

ANWN S E W C

Bay of Biscay C. chierchiae 0.16 ÿ0.20 ÿ0.26 ÿ0.14 ÿ0.00 ÿ0.16 ÿ0.24 T. stylifera ÿ0.14 ÿ0.44 0.00 0.11 0.03 ÿ0.44 0.22 Celtic Sea C. chierchiae ÿ0.34 0.90** 0.70 ÿ0.65 0.00 ÿ0.21 0.16 T. stylifera 0.47 ÿ0.76** ÿ0.21 0.35 0.13 ÿ0.38 0.11 English Channel C. chierchiae ÿ0.40 1.00 1.00 ÿ0.95 0.2 0.4 0.4 T. stylifera ÿ0.46 0.2 ÿ0.01 0.23 0.15 0.25 0.09 876 J. A. Lindley and S. Daykin

The influence of temperature on species that are at the by Hernańdez-Leon (1998) using data from Corral (1970). limits of their geographical ranges is unsurprising, but the The late seasonal maxima in more northern areas may, higher correlations with NHT rather than parameters of therefore, be due either to advection of populations from local temperature may be considered interesting. Temora warmer waters or to temperature limitation to hatching or stylifera occurred regularly in the samples in 1988 in which post-embryonic development. However, the higher corre- year the NHT was at its highest value (0.271) since the start lations with maximum monthly mean temperatures than of the CRU time-series in 1856. This value was exceeded in with minimum values suggest that the population is either 1990 (0.421), when T. stylifera started appearing regularly absent or dependent on dormant eggs during the coldest in the Celtic Sea and every year thereafter except for 1992, months (FebruaryeMarch) at the northern limits of its 1993, and 1996. The 1990 value was exceeded by 1995 range. Temora longicornis produces diapause eggs (Cas- (0.491), when T. stylifera was first recorded in the samples tellani and Lucas, 2003) but so far there is no evidence that at Station L4 off Plymouth, and that was surpassed by 1998 T. stylifera does so, although Halsband-Lenk et al. (2001) (0.662) when C. chierchiae was at its most abundant in all reported two size groups of eggs; the larger eggs were three areas. Temora stylifera occurred less frequently in produced in January and February. 1998 than in 1997 and 1999, when the local annual mean The results of the analyses of differences between the and maximum monthly mean temperatures were higher. species in the correlations with the SEC and the NAO, The time-series indicates that the arrival of a population indicate that ecological differences between species will of each of these two species in the Celtic Sea and English result in different responses to climate change. Lindley and Channel in the 1990s is consistent with a spread of the Reid (2002) showed that although the abundances of both population from more southern waters through the Bay of Calanus helgolandicus and C. typicus in the North Sea are Biscay. However, while C. chierchiae occurred frequently highly positively correlated with temperature, deviations in the Bay of Biscay in earlier years, the occurrences of from the relationship have occurred in response to other T. stylifera appear more isolated. It is at least possible that environmental variables. Our results, therefore, support the transport in ballast water may account for these Villate et al. (1997) in suggesting that Temora stylifera can occurrences, especially as the temperatures in the years of be a key species in monitoring climate changes in the Bay these earlier records were not exceptional. of Biscay (and now more northerly areas) but adding The seasonal cycles of C. chierchiae are very similar to Centropages chierchiae would help to avoid dependence on those of C. typicus in the English Channel and Celtic Sea the ecological characteristics of a single species. (Lindley and Reid, 2002). Centropages typicus is a perma- nent inhabitant of these areas but unlike C. hamatus does not appear to produce diapause eggs. However, nauplii of Acknowledgements this species have been hatched from sediments incubated in the laboratory (Lindley, 1990; Lindley and Reid, 2002) We acknowledge the work of the whole CPR survey team indicating that some subitaneous eggs are rendered dormant who have maintained the survey and produced the data by burial in sediment. It would seem that by the late 1990s presented and analysed in this paper. Anthony Richardson C. chierchiae had developed a resident population in the provided advice on statistics and carried out the meta- Celtic Sea and English Channel and the significant analysis. The survey would not be possible without the co- correlations with minimum temperature suggest that it operation of the owners, masters, and crews of the many persists mainly in the plankton rather than over-wintering ships that tow the CPRs. The CPR survey is supported by as eggs. The seasonal cycles described here from the Bay of public agencies in the UK, Canada, Denmark, France, Biscay and Iberian coastal waters are similar to the frequent Ireland, The Netherlands, Portugal, and the USA as well as occurrence through late spring and summer in data from the Commission of the European Communities, the monitoring samples off Santander although lacking the International Oceanographic Commission, the Atlantic clear June peak in those samples (http://www.seriestempor- Salmon trust, Pacific EVOS trust, and the World Wildlife ales-ieo.net/BDZoo/Santander/index.html). Fund. Part of this work was a thesis in partial fulfilment for The seasonal cycle of T. stylifera with its seasonal peak a BSc degree. We thank R. C. Thompson, University of late in the year is consistent with the results from Plymouth, Sean Daykin’s supervisor for his project. The the southern coastal area of the Bay of Biscay in Hadley Centre, UK Meteorological Office is thanked for 1988e1990 (Villate et al., 1997) although the August peak providing the SST data (HadISST Version 1.1) at no cost. off Santander (http://www.seriestemporales-ieo.net/BDZoo/ We are grateful for editorial comments and reviewers’ Santander/index.html) is earlier than the maximum values recommendations. in the CPR samples. Similar seasonal cycles have been reported from the northern Mediterranean (Gaudy, 1972; Razouls, 1973; Halsband-Lenk et al., 2001). However, References summer maxima were found in Saronikos Gulf (Aegean Beaugrand, G., Ibanez, F., and Reid, P. C. 2000. Spatial, seasonal and Sea) by Siokou-Frangou (1996) and in Canary Island waters long-term fluctuations of plankton in relation to hydroclimatic Variations in the distributions of C. chierchiae and T. stylifera 877

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