© 2003 by ICES/CIEM International Council for the Exploration of the Sea/Conseil International pour l'Exploration de la Mer
Long-term, predation-based control of a central-west North Sea zooplankton community
a Centre for Environment, Fisheries and Aquaculture Science (CEFAS) Pakefield Road, Lowestoft NR33 0HT, UK
b Dove Marine Laboratory, University of Newcastle-upon-Tyne Cullercoats, North Shields NE30 4PZ, UK
*Correspondence to C. L. J. Frid; tel: +44 191 2524850. e-mail: c.l.j.frid{at}ncl.ac.uk.
Long-term monitoring of the zooplankton community at a station 5.5 miles from the English coast in the central-west North Sea has been performed since 1968. Analyses of these data have revealed an inverse relationship between annual total zooplankton abundance and the position of the Gulf Stream North Wall (GSNW). This long-term relationship is opposite to the long-term positive association observed between the GSNW and total zooplankton abundances throughout most of the oceanic NE Atlantic region and the northern and central North Sea using Continuous Plankton Recorder data.
This study investigates the mechanism behind the inverse relationship with the GSNW, focussing on the importance of zooplankton predators in influencing long-term changes in the zooplankton community of the central-west North Sea. The results suggest that the dominant zooplankton predator Sagitta elegans plays a key role in mediating spring copepod population growth rates and thus their maximum and overall productivity during any one particular year. In turn, the abundance of Sagitta during the spring appears to be related to climatic factors. The implications of this on the zooplankton community are discussed.
Keywords: zooplankton community, North Sea, long-term trends, top-down control, climatic forcing
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Introduction |
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 Top Introduction MethodsResultsDiscussionReferences |
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The importance of zooplankton as secondary producers in the marine ecosystem, and thus their potential influence on fish stocks, has been the primary reason why researchers have attempted to determine how their long-term dynamics are influenced by climatic (e.g. Taylor, 1995; Fromentin and Planque, 1996), and/or anthropogenic factors (Greve et al., 1996).
Previous evidence has suggested that zooplankton dynamics across the NE Atlantic and North Sea region are principally controlled by processes occurring during the spring (e.g. Dickson et al., 1988), which set in train the dynamics of the rest of the seasonal cycle. In the North Sea, long-term trends in zooplankton are influenced by the (weather-driven) timing of the stratification of the water column and the resulting spring bloom (e.g. Dickson et al., 1988). Further research found that long-term zooplankton trends throughout most of the North Sea and NE Atlantic regions were related to long-term changes in the Gulf Stream North Wall (GSNW) (Taylor and Stephens, 1980; Taylor et al., 1992; Taylor, 1995, 1996). In NW Europe, northerly positions of the GSNW are related to warmer/wetter weather (Topliss, 1997), and to increased zooplankton productivity across the NE Atlantic and in the northern and central-eastern North Sea (Figure 1). However, such relationships were absent from those areas of the North Sea and Irish Sea, which lack a coupling between productivity and wind-induced mixing of the water column. This suggested that changes in the GSNW were associated with changes in the timing and intensity of the spring bloom (in a development of the model of Dickson et al., 1988). These associations were considered to be further evidence of a climatic connection spanning the North Atlantic, and suggested that the long-term trends in plankton (or at least those recorded by the Continuous Plankton Recorder (CPR) device) were predominantly externally driven rather than controlled through trophic interactions (Taylor et al., 1992).
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- -) and total copepods in CPR area B2 (northwest North Sea) over the 1966 to 1993 period (– • –). Adapted from In the central-west North Sea, monthly zooplankton sampling by the Dove Marine Laboratory at a single station has been performed since 1968 (Roff et al., 1988). Long-term zooplankton trends observed in this series have been found to be dissimilar to those observed from the CPR data in other North Sea regions (Huliselan, 1995; Clark and Frid, 2001). Furthermore, Frid and Huliselan (1996) observed that total zooplankton abundances in the Dove series over the 1969 to 1992 period were negatively related to the GSNW, contrary to those observed in the northern and central-eastern North Sea regions (Figure 1) by Taylor (1995). Such disparate observations are not due to differences in sampling methods, as the relative interannual fluctuations in zooplankton abundance and community structure observed in the Dove series are comparable to those in the CPR series for an area centred on the Dove zooplankton station (Clark and Frid, 2001). Previous studies (e.g. Austen et al., 1991; Evans and Edwards, 1993), on the Dove series have suggested that long-term plankton trends in the central-west North Sea were predominantly influenced by environmental factors, yet more recent investigations have proposed that biotic factors are more important in affecting long-term zooplankton dynamics in this region (Roff et al., 1988; Frid et al., 1994; Huliselan, 1995; Frid and Huliselan, 1996). A number of processes influence the growth rate and development of zooplankton populations. While many studies have focussed on the processes, which influence zooplankton "birth" rates, fewer studies have addressed the importance of zooplankton "death" on zooplankton dynamics (Ohman and Wood, 1995), and this is especially true for examinations of the long-term dynamics of zooplankton populations. This is based on the incorrect assumption that marine plankton communities are purely bottom-up rather than top-down controlled systems (Ohman and Wood, 1995). Yet studies of some zooplankton communities suggest that even at conservative levels of predation, predators are able to control the dynamics (Steele and Henderson, 1992) and the population growth rates of some zooplankton populations (Davis, 1984b; Ohman, 1986; Frid et al., 1994; Ohman and Wood, 1995; Sullivan and Meise, 1996). This study presents analyses of the Dove zooplankton series (1969–1996), focussing on the month to month and interannual relationships of the predators and omnivores within the zooplankton community. A mechanism is proposed as to how long-term interannual fluctuations in zooplankton abundance might be influenced by predation, and why changes in the latitude of the GSNW might be related to long-term zooplankton trends.
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Methods |
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TopIntroductionMethodsResultsDiscussionReferences |
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Dove Marine Laboratory time series
Zooplankton sampling by the Dove Marine Laboratory was initiated at a station approx. 5.5 n miles east of Blyth on the Northumberland coast at 55°07'N 01°20'W in August 1968. Sampling has taken place on a monthly basis except in 1989 when no samples were taken. Sampling consisted of four vertical hauls from 50 m to the surface (water depth approximately 54 m), which were pooled, using a 200 µm meshed WP2 net (UNESCO, 1968) with a mouth diameter of 0.56 m.
In addition, to enable a more accurate quantification of larger, but rarer zooplankton taxa, a 10 min horizontal trawl at approximately 30 m depth was taken using a 1 mm meshed WP3 net with a 1 m mouth diameter (UNESCO, 1968). On return to the laboratory, zooplanktons were identified to species level where possible, and abundances were determined. The abundance of each taxon was derived, according to its size, from either the WP2 or the WP3 net (see Evans and Edwards, 1993 for rationale). Certain taxa were further subdivided into sexes, or were categorized as juveniles and adults.
Initial data manipulations
Monthly data from the Dove zooplankton data covered the period 1969–1996 (excepting 1989). Due to the large number of taxonomic entities recorded in the Dove series (89 entities), only those predator and omnivore taxa, which represented at least 2% of the total zooplankton community in any one monthly sample, were used in the following analyses [a total of 46 taxa (see Table 1 for taxa list)]. Predators were considered to be those zooplankton species which were known to be carnivorous, whereas omnivores were those taxa, which were predominantly herbivorous zooplankton, but could include those taxa, which were opportunistic feeders, consuming both plant and animal materials.
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=0.05 are included, significant correlations after correction are in bold. Global p = 0.026.Relationships between zooplankton and the GSNW
Correlation analysis was employed to examine long-term relationships between taxa and the position of the GSNW. For all taxa, abundances were log10 + 1-transformed. Due to the problem of autocorrelation inherent in time series data (Jassby and Powell, 1990), additional post correlational corrections were employed to compensate for this. Thus, the number of degrees of freedom used for testing the significance of correlations between taxa and potential forcing factors was reduced according to the method of Quenouille (1952), which calculates the effective number of independent observations (E) as follows:
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Predator–prey relationships over the seasonal cycle
The seasonal cycle of omnivores and predators were compared between low zooplankton years [defined as years where the mean annual total zooplankton abundance was more than 0.5 standard deviation below the long-term mean (Table 2)], and high zooplankton years [defined as years where the mean annual total zooplankton abundance was more than 0.5 standard deviation above the long-term mean (Table 2)]. From these plots, differences in the seasonal cycle between low and high abundance years, and possible relationships between the predators and omnivores were investigated.
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Long-term predator–prey relationships
The dominant zooplankton predator in the central-west North Sea zooplankton system (as observed in the Dove zooplankton series) is the chaetognath Sagitta elegans Verrill (Table 1). As such, the investigations of predator–prey relationships within the zooplankton community dealt primarily with this predatory species. Those factors, which influence spring omnivore population growth rates, such as predation are likely to moderate the overall annual productivity during that year. Thus, the examination of predator–prey relationships concentrated on the ability of Sagitta to moderate the annual maximum omnivore productivity through regulation of their population growth rate during the spring. Thus, the presence of long-term relationships between mean spring (February to April) Sagitta abundances and the maximum abundance of each omnivorous taxa over the 27-year time series were explored using correlation analysis. All significance tests were corrected for autocorrelation using the formula of Quenouille (1952), and a global significance level was calculated based on the number of significant correlations present.
Relationships between spring Sagitta and environmental factors
The main periods of Sagitta recruitment are said by Feigenbaum and Maris (1984) to coincide with sharp increases in the abundance of Pseudocalanus nauplii (the main prey item of young chaetognaths), which would be expected to be greater with increased spring phytoplankton productivity (Feigenbaum and Maris, 1984). Thus, in order to establish whether spring Sagitta abundances were related to spring phytoplankton or weather, standardized time series of log10 February–April Sagitta abundances were plotted alongside standardized February–April values of air temperatures and daily sun duration taken at nearby Tynemouth (obtained from the British Atmospheric Data Centre), the annual mean position of the GSNW, and mean February–April phytoplankton index data from the CPR survey for the central-west North Sea.
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Results |
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TopIntroductionMethodsResultsDiscussionReferences |
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Over the 1969 to 1996 period, long-term trends in total zooplankton abundance were negatively correlated with the GSNW (r=–0.4, p=0.046; Figure 2a), confirming the analyses of Frid and Huliselan (1996). Of the 46 taxa examined, long-term trends in four taxa were negatively related to the GSNW, and one taxon was positively related (Table 1). The strongest relationship observed with the GSNW was with the most dominant taxonomic group, the Pseudocalanus/Paracalanus/Microcalanus group (r=–0.61, p=0.006; Figure 2b). The second most abundance taxa, Oithona similis, was also significantly negatively associated with the GSNW (r=–0.41, p=0.03; Figure 2c). Together, these two taxa make up 40% of the total zooplankton abundance observed in the Dove series (Table 1).
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On average, the spring omnivore increase began in March and continued until June, followed by a steady decline in abundance until the winter nadir from December to February (Figure 3). Omnivore abundances during the winter and early spring showed no relationship to maximum omnivore abundances during that year (Figure 4). Only by May did omnivore abundances bear any significant relationship to the maximum annual abundance attained. There was also a significant correlation between the difference in the abundance of the total omnivores from February to April (i.e. their increase in abundance over this period), and their maximum annual abundance (r=–0.45, p=0.02). Thus, smaller differences in abundance (indicating higher rates of omnivore population growth from February to April), were related to a higher maximum abundance attained during that particular year, suggesting that the rate of increase during these months was critical in determining the maximum annual abundance reached.
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From February to April, predator abundances were relatively low, and only started to increase after the increase in omnivore abundance (Figure 5). Except during May, when gelatinous zooplankton dominated (Figure 5), S. elegans Verrill (Chaetognatha) was the dominant predator in the zooplankton community, and from February to April this taxa made up 73% of total predator abundances (Table 3).
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Month to month and long-term predator–prey relationships
During high zooplankton abundance years, the rate of omnivore increase from February to the end of April was greater than that during low abundance years (Figure 6a), leading to an overall higher peak of abundance in the summer. During these high abundance years, predator abundances during the spring omnivore increase from February to April were relatively low (Figure 6a). Conversely, during years with higher spring predator abundance, the rate of omnivore increase from February to April was lower, leading to an overall reduced abundance. Based on the observations in Feigenbaum and Maris (1984) that North Sea Sagitta are able to consume 2.04 prey items per day, and on the abundance of Sagitta observed in March during low and high zooplankton abundance years, this equates to 5.93% of the omnivore community consumed in March during low abundance years against 1.34% of the omnivore community consumed during March in high abundance years. As omnivore abundances from November to February in both low and high abundance years were similar, the differences later on in the seasonal cycle do not arise from differences during the early part of the year, supporting the conclusion that abundances during the winter are unrelated to those during the summer.
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Similar patterns were observed in the relationship between the dominant two taxa (the Pseudocalanus/Paracalanus/Microcalanus group and O. similis) with the main predator Sagitta. For Pseudocalanus/Paracalanus/Microcalanus, the spring increase occurs during March and April (Figure 6b), whilst for O. similis, the increase occurs during February to April (Figure 6c). In both of these taxa, when the rate of population growth during the spring was low, Sagitta abundances were higher during winter, and vice versa (Figure 6b, c).
Over the 27-year series, there was a significant inverse relationship between the mean spring total predator (February–April) abundance and mean summer omnivore (June–August) abundance (r=–0.40, p=0.046; Figure 7a). This relationship was especially strong during the 1974–1990 period, although 1980 had a lower omnivore abundance than would be expected given the numbers of predators present. Significant negative correlations (Table 4) were also observed between the spring (February–April) abundance of Sagitta and the maximum annual abundance of the Pseudocalanus/Paracalanus/Microcalanus juveniles (r=–0.45, p=0.018; Figure 7b), Calanus spp. juveniles (r=0.55, p=0.006), gastropod larvae (r=–0.44, p=0.023), euphausiid nauplii (r=–0.42, p=0.03) and Oithona spp. (r=–0.41, p=0.041; Figure 7c). Calanus finmarchicus was the only taxon to show a positive relationship between spring Sagitta abundances and its maximum abundance during the year (Table 4).
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Environmental control during the spring
Spring Sagitta abundances (February–April) were low from the start of the Dove series until 1980 (excepting a peak in 1977), as was noted by Evans and Edwards (1993). Following this, there was a gradual increase in Sagitta abundances until 1983 (Figure 8a–d). These spring Sagitta abundances were found to be significantly related to a number of environmental variables over the entire 27-year time series. Positive associations were present between Sagitta and mean spring Tynemouth air temperature (Figure 8a), mean spring Tynemouth sunshine (Figure 8b), the GSNW (Figure 8c) and mean spring C2 phytoplankton index (Figure 8d). However, before 1977, due to the low spring Sagitta abundances, there was no response to fluctuations in these environmental variables, although the peak in Sagitta during 1977 did coincide with peaks in sunshine and temperature.
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—) and Tynemouth air temperatures (- - |
Discussion |
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TopIntroductionMethodsResultsDiscussionReferences |
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Previous studies by Roff et al. (1988) in the central-west North Sea suggested that the standing stock of zooplankton over the winter governed their maximum abundance the following year. However, this study has shown that over the whole series, there was no relationship between the standing stock of omnivores during the winter months, and peak omnivore abundances the following summer. In addition, omnivore abundances observed in January and February during low zooplankton years were similar to those observed during high zooplankton years. Thus, it appears that those processes occurring during the spring are crucial in determining the annual abundance and productivity of zooplankton in the central-west North Sea.
Sagitta has often been cited as a predator of copepod populations (Oresland, 1985; Conway and Williams, 1986; Alvarez-Cadena, 1993; Sullivan and Meise, 1996) and limitation of Pseudocalanus population growth and the interannual variability in the abundance of predators such as Sagitta was related to the annual mortality of Pseudocalanus in Dabob Bay, Washington (Ohman, 1986). Certainly we have shown that there are large differences in the percentage of the standing stock that are removed during low and high abundance years. This study has also shown that the peak annual abundances of four omnivorous taxa, of which two, Pseudocalanus/Paracalanus/Microcalanus and O. similis, are the most numerically dominant taxa recorded in the Dove series, were inversely related to spring Sagitta abundances. This suggests that predation upon these taxa by Sagitta was limiting their spring population growth and hence their annual maximum abundances and productivity. These four omnivorous taxa could all be classified as small or medium sized (<2 mm length) copepods (Nicholas and Frid, 1999). Larger taxa (e.g. Centropages spp.) were found to show no such relationship to spring Sagitta abundances (Nicholas and Frid, 1999). Chaetognaths are ambush predators, sensing prey through vibrations (Feigenbaum and Maris, 1984). As such, they will prey upon whatever they encounter in the water column and emit the signals to trigger an attack response. However, there is a relationship between the size of a Sagitta individual and the size of prey taken (Figure 9; Feigenbaum and Maris, 1984).
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It would be expected that only juvenile Sagitta (stages I and II) individuals below approximately 15 mm length (Huliselan, 1995) would prey upon those omnivorous taxa identified in Table 4 (Feigenbaum and Maris, 1984). Larger omnivores, such as adult Calanus would not be expected to be consumed by juvenile Sagitta, although they could be consumed by those individuals greater than 15 mm length (Figure 9).
Given that small copepods are the principle target of predation by Sagitta, it might be expected that other small sized copepod taxa would be influenced by such predation. Yet at the population level, each taxon is likely to have a different susceptibility to control by predation, based on its life-history characteristics. For example, the Pseudocalanus/Paracalanus/Microcalanus group shows the strongest evidence of control by Sagitta (Table 4). It is known that Pseudocalanus at least does have a relatively low rate of population growth due to its low fecundity (Corkett and McLaren, 1978), which is limited by water temperatures rather than food supply (McLaren, 1965; Davis, 1984a). Therefore, it would be expected that this taxa would be relatively more sensitive to predation. The copepod Acartia clausi, on the other hand, might also be expected to be vulnerable to predation given its similar size to Pseudocalanus. Yet, due to its high reproductive rate (Colebrook, 1982) A. clausi will be relatively unaffected by predation, and thus it displays no relationship to the abundance of Sagitta.
Therefore, it is suggested that predation by Sagitta on the omnivores plays an important role in controlling the long-term dynamics of the coastal central-west North Sea zooplankton community, and as a result, this inverts the relationship which is observed between copepod abundances and the GSNW. The suggestion that predation reverses the sign of the relationship with the climatic variable (the GSNW) is also supported by the fact that the Pseudocalanus/Paracalanus/Microcalanus group were the taxa most strongly limited by Sagitta, and which also presented the strongest inverse relationship to the GSNW (Table 4). Conversely, those taxa, which were not related to Sagitta abundances, either due to their size, or due to high reproductive rates, were less influenced by predation and do not exhibit such a negative relationship with the GSNW.
Increased Sagitta abundances during the spring were related to higher spring temperatures and more northerly positions of the GSNW (Figure 8). Why Sagitta should show any relationship to climate is unclear. Although temperature is known to be linked to the growth rate and generation time of Sagitta (Oresland, 1985, 1986), food is more important to its fecundity and therefore its overall abundance (Feigenbaum and Maris, 1984). However, Feigenbaum and Maris (1984) did note that the periods of recruitment of a new Sagitta cohort coincided with sharp increases in the abundances of Pseudocalanus nauplii (which are the main food source of young Sagitta; Baier and Purcell, 1997). Yet, as mature chaetognaths do not feed on small prey, and thus cannot detect their presence (Feigenbaum and Maris, 1984), it is more likely that the reproductive timing of Sagitta was related to the abundance of adult and larger prey items (which are consumed by mature chaetognaths; Feigenbaum and Maris, 1984).
It is proposed that the mechanism influencing the long-term control of the zooplankton system in the central-west North Sea ultimately functions through the presence of particular weather conditions during the spring. Northerly GSNW years produced suitable weather conditions to induce a spring bloom and increase the abundance of suitable prey for Sagitta (Figure 10a). This resulted in a new cohort of Sagitta, which was then able to reduce the growth rate of the small spring copepod population in proportion to their abundance, effectively inverting the signal of climate observed in the Dove zooplankton time series. Conversely, those weather patterns associated with southerly GSNW years resulted in a delayed spring bloom and a reduced fecundity of Sagitta. This smaller Sagitta population was then less able to restrict the population growth of the small copepods, resulting in a relatively higher rate of population growth (Figure 10b).
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Although not considered in detail here, as high abundance years show an increased predator abundance during the summer months (Figure 6a), it appears, as originally suggested by Roff et al. (1988), that there are two main groups of predators present. There are those that regulate omnivore abundance through limiting the rate of population growth in the spring (i.e. Sagitta), and there are those other predators which follow omnivore abundances (e.g. fish larvae and Pleurobrachia pileus (Frid et al., 1994; Nicholas and Frid, 1999)). The abundance of this latter group responds to the abundance of the omnivores (i.e. their food source), and these summer predators do not tend to have such a strong effect on omnivore abundance, as the established summer omnivore population and summer water temperatures allow a high omnivore reproductive rate (food availability permitting). In contrast, during the increase in copepod abundance during the spring, lower water temperatures and lower standing stocks mean that populations are more vulnerable to predation. Baier and Purcell (1997) and Kehayias et al. (1996) have shown that chaetognath predation has the greatest effect during periods of low copepod reproduction.
In previous analysis of the Dove zooplankton series, Evans and Edwards (1993) observed a marked change in zooplankton species composition between 1979 and 1980, and suggested that the species most responsible for the observed change was Sagitta. Spring Sagitta abundances around 1980 did increase markedly at this time (Figure 8). Other work has put forward chaetognaths as being sensitive to climatic shifts, and as indicators of changes in water temperature (Southward, 1980), and the timing of the increase in spring Sagitta abundances does coincide with the nadir in zooplankton abundances. As remarked by Roff et al. (1988), the interannual dynamics of zooplankton are highly complex, and during years when spring Sagitta abundances are low, other factors such as water temperature, food, or the standing stock of omnivores surviving the winter may be more important in influencing the seasonal zooplankton dynamics during that year. In addition, it is also likely that for those taxa with a relatively slow growth rate, reduction of the winter standing stock due to predation (as suggested by Roff et al., 1988; Frid et al., 1994; Nicholas and Frid, 1999), may also influence the productivity of these taxa the following year. However, previous studies have suggested that despite Sagitta being the dominant predator observed during the winter and spring period, other predators (e.g. Themisto spp.; fish larvae) are more voracious and may have a higher impact on copepod stocks (Frid et al., 1994; Nicholas and Frid, 1999).
Sullivan and Meise (1996) noted that, on Georges Bank, Sagitta preferred the shallower well-mixed areas of the Bank, and as such, predation by Sagitta may be confined to shallower, well-mixed or coastal areas of the North Sea. Although the results presented in this study have focussed on the data collected from a single sampling station (i.e. the Dove series), as the relative interannual fluctuations in CPR data over the central-west North Sea region show similar long-term trends to the Dove series (Clark and Frid, 2001), the mechanism proposed here could operate over a wide area of the central North Sea. However, further analysis of CPR data is required to determine in which areas of the North Sea, chaetognaths might have the potential to influence copepod populations.
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References |
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TopIntroductionMethodsResultsDiscussionReferences |
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