OCEANOLOGICA ACTA 1984- VOL. 7- W 2 ~ -----~1-

Macroplankton Climate Fluctuations in the "indicator" Competition Sagitta chaetognaths Sagitta elegans Fluctuations , Macroplancton Oimat and Sagitta setosa Compétition Sagitta in the Western Channel Fluctuations

A. J. Southward Marine Biological Association of the United Kingdom, The Laboratory, Citadel Hill, Plymouth, South Devon, PLl 2PB, UK.

Received 22/10/82, in revised form 18/11/83, accepted 24/11/83.

ABSTRACT Between 1930 and 1938 the arctic-boreal species Sagitta elegans was replaced as the dominant chaetognath off Plymouth by the temperate neritic species Sagitta setosa. The latter was dominant from 1939 to 1968. From 1969 S. elegans became abundant again and was dominant in 1979. There were corresponding changes in other zooplank­ ton organisms and among pelagie fish, the whole forming a cycle of events, the "Russell cycle". The fluctuation of the Sagitta species is a good example of changes in abundance of a pair of species as a result of environmental change, and provides a useful "indicator" of the general change in the ecosystem. The changes in Sagitta dominance occupied from 9 to 11 years, and the complete changes in the ecosystem took 10 to 15 years. Sorne aspects of the changes were comparatively abrupt, but the whole was quite graduai. The cycle can be correlated with a fluctuation in climate, the recent warming of the Northern hemisphere up to 1950, followed by cooling. The climatic effect may have operated through alterations in residual currents and through changes in sea temperature, but the influence on the organisms was indirect, mediated through interspecific competition and biological interactions in the whole ecosystem. Oceanol. Acta, 1984, 7, 2, 229-239 ..

RÉSUMÉ Fluctuations des chaétognathes « indicateurs » Sagitta elegans et Sagitta setosa en Manche occidentale Près de Plymouth, entre 1930 et 1939, Sagitta .elegans (boréo-arctique) a été remplacée en tant qu'espèce dominante par S. setosa (néritique-tempérée). Cette dernière a dominé de 1939 à 1968. A partir de 1969, S. elegans a vu à nouveau ses effectifs augmenter, pour redevenir dominante en 1979. D'autres organismes planctoniques, ainsi que des poissons pélagiques, ont présenté des fluctuations analogues, et l'ensemble de ces changements constitue le« cycle de Russell ». Les fluctuations de Sagitta offrent un bon exemple de variations d'abondance, sous l'influence des facteurs du milieu, chez deux espèces en compétition, et fournissent un moyen commode d'appréhender les changements généraux dans un écosystème. L'inversion de dominance chez les Sagitta s'est étendue sur 9 à 11 ans et l'ensemble des changements dans l'écosystème sur 10 à 15 ans. Certains aspects de ces changements ont été relativement brusques, l'ensemble étant cependant progressif. Le cycle peut être mis en relation avec des fluctuations climatiques récentes, telles que le réchauffement de l'hémisphère Nord jusque vers 1950, et le refroidissement qui a suivi. De tels changements climatiques peuvent agir par des modifications des courants résiduels et par le biais de la tempéra­ ture de la mer, mais l'effet sur les organismes est probablement indirect, à travers la compétition interspécifique et les interactions biologiques dans l'écosystème entier. Oceanol. Acta, 1984, 7, 2, 229-239.

0399-1784/84/02 229 11/$ 3.1 0/© Gauthier-Villars 229 A. J. SOUTHWARD

INTRODUCTION GEOGRAPHICAL AND VERTICAL DISTRIBU­ TION OF S. ELEGANS AND S. SETOSA Many changes have occurred in the species and ahun­ As Russell (1935; 1939 b) showed, following the earlier dance of zooplankton, fish and benthos in the Western work of Meek (1928), around the British Isles Sagitta Channel off Plymouth during the past 60 years (review setosa is usually restricted to coastal water, whereas by Southward, 1980; Ford, 1982). These changes forma S. elegans is more common in mixed coastaljoceanic cycle of events, the "Russell cycle" (Cushing, Dickson, water. This separation has puzzled sorne investigators 1976) which appears to be broadly linked with recent since both species are classed as neritic, in contrast to climatic fluctuations in the Northern hemisphere. Sorne the truly oceanic species of Chaetognatha (Tokioka, aspects of the changes, the apparent suddenness of 1979). Closer examination of the geographical distribu­ certain of them, are difficult to correlate with an envi­ tion shows that S. Elegans is a widespread Arctic­ ronmental factor such as sea-temperature which Boreal species which is neritic, and sometimes euryha­ changes gradually (Southward et al., 1975; Maddock, line, in the Arctic and northern Boreal parts of its Swann, 1977 and references therein). In discussing biolo­ range, but stenohaline and stenothermal in the North gical changes in the sea Cushing and Dickson (1976) Sea, Celtic Sea, Channel, and Northern Bay of Biscay refer to the alteration of the ecosystem in the Western (Southward, 1962; Alvarino, 1965; 1969); there is a Channel as a process of "rectification", and point out suggestion that at its southern limits it is restricted to that it occurred in stages over a decade. They appear a narrow band of salinities, around 34.0 to 35.0 in to be suggesting that a series of small changes may %, which case the variety living at lower salinities in the build up tension in the ecosystem to a level where Baltic Sea (cf. (j)resland, 1983) ought to be genetically change of state is necessary, followed by re-stabilization distinct. In contrast S. setosa is a less widely distributed at a different balancing point (Holling, 1973; May, temperate or transitional species, tolerant of changing 1977). salinity and mostly restricted to coastal waters. It has a discontinuous distribution, for in addition to the Part of the "Russell cycle" that bas attracted much main region of ~ccurrence, from the southern fjords of interest is the alternation in dominance of two common Norway and the Kattegat to Brittany, S. setosa is also species of Chaetognatha, Sagitta elegans Verrill and found along the northern side of the Eastern Mediterra­ Sagitta setosa J. Müller. In many previous studies these nean, in the Northern Adiatic, and in the Black Sea species have been considered from the point of view of and occurs locally in the Gulf of Naples and the Gulf their value as indicators of change in hydrographie of Gabes; this distribution suggests S. setosa may be a conditions, as originally suggested by Russell (1935). 1t relie form of previously wider range, now separating is proposed here to give details of the progress of the into local races or species, and indeed the Black Sea changes in dominance during two periods, from 1930 form is regarded as distinct by sorne authorities (Rus­ to 1938 when S. elegans was replaced by S. setosa, and sell, 1935; Hansen, 1951; Alvarino, 1965; 1969; Vucetié, from 1968 to 1979 when S. elegans returned again, 1961; 1970; 1973; Kahn, Williamson, 1970; GraU et al., and to include serious consideration of the effects of 1971; Jakobsen, 1971; Le Fèvre, 1971; Mironov, 1976; interspecific competition. As Darwin ( 1859) noted, com­ O'Brien, 1976; Furnestin, 1979; Sands, 1980; Le Fèvre petition between species is of profound importance to et al., 1981; Ibanez, 1982; (j)resland, 1983). To the geographical and vertical distribution of organisms. north of Bergen, S. setosa is replaced inshore by "Almost ali organisms can withstand more heat, cold ... S. elegans, and to the south of Brittany, as for example than they are exposed to within their natural range; in the southern Bay of Biscay and the Mediterranean, it the definitive limit to the range ~f most species, under is replaced by S agitta friderici. S. elegans and S. setosa gradually increasing unfavourable conditions being the overlap in distribution along a comparatively narrow presence of other competing forms better adapted to strip of sea extending from Southern Norway, down such conditions" ... "As species disappear other closely­ both sides of the British Isles, to Southern Brittany. allied or representative species, apparently filling nearly the same place in the economy of nature, take their Much of the available data on this distribution is place" (Darwin, in Stauffer, 1975, p. 264 and 267). obtained from vertical tows or oblique hauls with large These statements are particularly applicable to the pre­ nets. However, Russell ( 1939 b) noted that sorne exam­ sent problem of explaining why comparatively small ples of overlap were due to vertical differences, and changes in environmental factors appear to be asso­ when samples are taken at different depths in fully­ ciated with large biological changes. Darwin's view of stratified water, as for example in Oslo Fjord, Korsf­ what constituted competition was wider than that of jord, the northern North Sea and the western Channel, present-day ecologists, and today we have to take note the two species are seen to be vertically separated, with of competition for space, competition for food and also S. setosa dominant in the layer above the thermocline. the effects of direct predation of one species on another. In such circumstances the adults of S. elegans remain However, before describing the fluctuations in the two in the deeper water below the thermocline, although species and discussing the possible influence of their younger stages may mix with S. setosa in the hydrographie factors and competition it is necessary to surface layer (Furnestin, 1938; Hansen, 1951; Jakobsen, review the geographical and vertical distribution of the 1971; Southward, 1983). Data on food taken by the two species, and assess the validity of the sampling two species (Rakusa-Suszczewski, 1969) also suggest method that has provided the 55-year data series now S. setosa is more of a surface-living form than available. S. elegans (p. 16). Even in well-mixed inshore waters

230 FLUCTUATIONS IN CHAETOGNATHS there can be a separation in time, one species or the Calibrations are checked from time to time with a other appearing as a seasonal influx that can be linked benthos bathykimograph attached to the frame, and with hydrographie conditions (Kahn, Williamson, 1970; an Oceanics Instruments flow-meter placed in the O'Brien, 1976; see also Ibanez, 1982). Nevertheless, mouth of the net. Catches are preserved immediately although the two species may thus be separated for with borax-buffered 4% formaldehyde. Bef ore 1958 the part of the year in space or time, they do occur toge­ whole catch was searched for large individuals, and ther, especially as juveniles, and must therefore be then counts of the rest made on 1/10 subsamples. Plank­ considered in competition, as will be discussed later. ton organisms are usually distributed in a non-random pattern showing both small-scale and large-scale patchi­ ness (Steele, 1978), hence there is a practical limit to SAMPLING METHODS the precision of the methods (cf Frontier, 1969; Le Fèvre, 1971; Le Fèvre et al., 1981). Since 1958 the The station selected by Russel (1933) for weekly conti­ tedium of searching the large samples from L5 has nuation of the macroplankton sampling, station A, lies been reduced by systematic subsampling. Successively 2 n. miles east of the Eddystone Reef (Fig. 1), and its larger aliquots ranging from 1/500 to 1/2, taken with use followed earlier investigations (Russell, 1926) at Stempel pipettes and dipping beakers, are examined this position and at L4, L6 and El. After 1958 sampling until from 10 to 100 of the common species have been was moved to L5, 2 n. miles west of the Eddystone, a counted; the whole sample is searched only for the position used for sorne hydrographie work. Both rou­ rarer and larger forms. At the minimum leve! of tine stations are close enough to Plymouth for day 10 Sagitta elegans per aliquot the coefficient of varia­ trips ( 11 n. miles south of the Breakwater), and provide tion (SD as percent of mean) is 15%, which is less than depths of over 55 m. The proximity to the Eddystone the coefficient of variation in total biomass from a Lighthouse helped position finding in the days before rapid succession of vertical hauts on the same place electronic aids to navigation. Until 1980 most samples (25 %), and much less than the usual 95% confidence were taken with 1 or 2 rn diameter ring trawls with an limits for species in oblique samples, placed from x 2, average mesh size of 700 ~M (details in Southward, + 2 to x 4, + 4 by different authors (see, however, Van 1970), but recently the same netting has been used on Guelph et al., 1983). In summer, when large numbers a square frame of 0.9 x 0.9 m. The new frame provides of Calanus are present, and sorting is difficult, abon­ the same sample as the 1 rn ring trawl, since the dances of Sagitta below 10 per haut are classed as zero. improved mouth areajfiltration area ratio increases the Ali counts are converted to numbers per standard haut 3 efficiency. The nets are operated on oblique or double of the 2 rn net, approxima tel y 5 000 m of water oblique paths in the water, from 0 to 50 rn, to occupy filtered, the calibration basis for the pre-1958 samples 20 or 30 mins at a speed of either 2 knots or 4 knots. (Southward, 1970). The results are presented as total number of S. elegans per standard haut and as percen­ tage composition of the two species. It should be noted that two other species of Sagitta may occur occasio­ nally off Plymouth, S. tasmanica Thomson (=S. serratodentata of earlier publications) and S. friderici Ritter-Zahony, but not in sufficient number ----____ ... - -lsnt __ ...... - ..... , ',, to alter the ratios of the two dominant species. The ...... __ .. _,, ..... ___ , ...... __ -~--.. method of presentation follows previous publications

, ------id"'"'----- (Russell, 1935; 1937; 1938; 1939 a) and permits direct ..... ---.. comparison of the new data with the old. There are /,-- oi'4 ------.1_ 15' more sophisticated methods for analysis of zooplank­ ton temporo-spatial data to permit correlation with

•\,:· Eddystone ·-- abiotic factors (e.g. Ibanez, 1976; 1982; Frontier, 1969; n 1973; LeFèvre et al., 1981; Colebrook, 1982a, b). The Q (.) 0 simple graphs used here (Fig. 6 and 7) allow direct LS'' A 1o' inspection of seasonal and annual trends which is usually sufficient; however, a logarithmic transforma­ tion is used for Figure 5.

s'

OE1 CHARACTERIZA TION OF THE SAMPLING ST A­ TION s

231 A. J. SOUTHWARD

Table 1 Numbers of Sagitta per standard haul, and percentage S. elegans, in the daytime around stations L5, 15-7-83, when S. setosa was abundant at L4. See Figure 2 for positions and surface temperature.

L5 A 8 c D E Sagitta setosa . 1650 860 2630 1270 810 770 Sagitta elegans 950 1610 340 1530 3140 3100 %S. elegans 36.5 65.2 11.4 54.6 79.5 80.1

oE

L-.....___. _ _.___.__~__._--,;l•.., .,,-_._-...___.___.._ so• os' 4 2 0 Figure 2 Bathymetry around L5, and surface temperatures on 15-7-83. The number of dots on the contours gives the depth in tens of metres. The position of the front is shawn by hatching. Net stations shawn at L5 and positions A to E are those listed in Table 1. Figure 4 Vertical distribution ofSagitta elegans, as percentage on 17 July 1979, ing to weather. The inshore water, as was shown by 14.00-16.00 h BST. The total numbers per 250m3 were: L4, 4300; Harvey (1923; 1925; 1930), is partly stratified in çalm L5, 11,570; El, 4010. Samples taken a< 5 depths with a multiple weather, but is nevertheless always more mixed verti­ opening/closing net, mesh 330 J!M. · cally than the offshore water at El (Fig. 3). The advan­ tage of L5 and A lies in this vertical mixing, since it can often provide better samples of those species which tend to remain very low in the water column in strati­ RESULTS fied water. This effect is clearly shown in the results presented by Southward (1983), and by the new data The results of the weekly sampling at L5 and A are given here (Fig. 3 and 4). It has been found that during presented in three sections: first a detailed analysis of periods when S. elegans is abundant in the Western seasonal changes in 1979 to provide a standard of Channel, it can be more numerous in the samples at comparison, then summaries of the major trends L5 than in those from El, and also common inshore observable in the periods 1930-1939 and 1969-1979. at L4 (sorne hydrographie data for the L4 station is given by Wickstead, 1968). Conversely, when S. setosa is dominant inshore, the proportion of S. elegans in Seasonal changes in 1979 the samples increases to the south-west (Tab. 1). Howe­ ver, in the latter circumstances S. setosa dominates the Changes in abundance of S. elegans and S. setosa upper layer and S. elegans tends to be restricted to the during 1979 are shown in Figure 5, together with colder water below the thermocline (Southward, 1983). appropria te data on temperature and salinity. The great changes between successive samples, especially in spring and autumn are typical of the whole series. No correla­ tion can be found with the tidaf cycle or neapfspring differences, and only a small part of the variation is attributable to sampling and subsampling techniques (see Methods); confidence limits ( x 2, -:- 2) are shown on Figure 5 for the summer period, to illustrate the expected range of variation from these sources. Sorne of the remaining variation could be dueto changes in brood strength, as successive batches of the young are retained by the meshes (Russell, 1932; 1933; but cf Jakobsen, 1971; Q)resland, 1983), but rouch of it must be attributable to large scale patchiness, including advection, particularly the massive changes in spring and autumn. Fortunately the sampling frequency provided by weekly hauls is enough to allow seasonal Figure 3 trends to be discerned through the variation, and help Vertical distribution of temperature at the Plymouth stations (Fig. 1) is given by the smoothing effect of percentage composi­ on 11-7-79. The vertical difference in salinity was only 0.02°/00• tion (Fig. 6 and 7). The most notable feature of 1979

232 FLUCTUATIONS IN CHAETOGNATHS

(1975) attribute the lower salinity in summer to lesser advection of high salinity water into the Western Chan­ nel compared with the winter months, and suggest that the difference in salinity between the surface and the bottom could be explained solely by graduai transfer of low salinity through the thermocline by vertical turbulence. Taylor and Stephens (1983) have also illus­ trated the lesser advection in summer. If these models apply to individual years then the seasonal periods of abundance of S. setosa off Plymouth in 1979 would correspond to periods when advection of high salinity water was occurring, whereas the summer dominance of S. elegans would correspond to a period of stagna­ tion. This inference does not accord with sorne prëvious interpretations of changes in the local hydrographie ·c and plankton regime, and will be discussed more com­ 17 pletely below after the changes in 1930-1939 and 1969- 1979 have been summarized. T'

·························•···· M A M A S 0 N D

Figure 5 Fluctuations in abundance (log scale) ofSagitta elegans (black squares) and S. setosa (black circles) at station LS during 1979; the thick li ne shows the period of thermal stratification. Below: salinity at 10 m at station El (white circles) and at 50 m (white squares); sea temperatures in Plymouth Sound (dotted line) at El surface (solid line) and El broken line are shown as smoothed curves through the observations (monthly at El, twice weekly in Plymouth Sound. Confidence limits ( x 2, -+- 2) are shown for Sagitta elegans during its period ofdominance, but are omitted otherwise to reduce confusion between the points for each species.

was the almost complete dominance of S. elegans from April to September, coinciding with the period when the offshore water was stratified and when salinities were low. There was rouch greater fluctuation of both species before and after this period. The breakdown of 2 the thermocline in September coincided with a sudden decrease in S. elegans, and increase in S. setosa. An accompanying increase in south-western plankton indi­ cators (Southward, 1962) such as Muggiaea atlantica, Liriope tetraphylla and Euchaeta hebes leaves no doubt that this was an advective change, a view borne out by the 60 yr analysis of the average change in the beat content of the water column at El (Pingree, Penny­ cuick, 1975), where there is a positive anomaly for most of September and October. The south-western influence persisted to November, and there ..was a brief period of dominance of S. setosa, but S. elegans increased once more in December, and continued through into 1980. 1938 It is perhaps surprising to find a species of predomin­ antly cold-water distribution reaching its maximum 50 abundance in summer, and for a species regarded as characteristic of mixed oceanicfcoastal water to be associated with a period of lowered salinity. The salin­ Figure 6 ity trends shown in Figure 5 are quite typical of the Weekly fluctuations of Sagitta at A from 1930 to 1938, after Russell (1935; 1937; 1938; 1940}. For each year the upper graph shows 60 year averages for El, though of greater amplitude. total S. elegans in each standard haul; the lower histogram gives the From the 60 yr averages, Pingree and Pennycuick percentages of S. elegans (black) and S. setosa (white).

233 A. J. SOUTHWARD

Trends in 1930-1938 The compléte sequence of events during the changeover from S. elegans to S. setosa is shown in Figure 6, compiled from a series of publications by Russell (1935; 1937; 1938; 1939 a), and brought together here for the first time. The end of the dominance of S. elegans in 1930 began as a seasonal switch to S. setosa in the autumn, comparable to that already described for 1979. The change involved an influx of south-western indica­ tors, and was most probably the result of strong advec­ tion that included plankton from a south-western direc­ tion. S. elegans returned in sorne number the following winter, but was less dominant in the summer of 1931, and decreased markedly in 1932 and 1933. By 1935 S. elegans was a very minor element of the chaetognath population, and the apparent revival in 1936 was illu­ sory, so that by 1938 S. setosa was fully dominant ail year round. The samples for 1939 and 1940 are incomplete, but the dominance of S. setosa continued. When the investigations were resumed in 1946, S. ete­ gans was scare or absent (Russell, 1947; Corbin, 1948; 1949), and continued so up to 1968, the start of the ext sequence described fully below. A verage summer abundances of S. elegans for this period from 1939 to 1967 are shown by Southward (1980) as part of the whole sequence for 1924-1979; the occasional occur­ rence of S. elegans farther offshore to the south and west during the period of dominance of S. setosa off Plymouth is discussed by Southward (1961; 1962). Although the 1930-1938 sequence is most noticeable for the long term decline in S. elegans, we cao stiii extract sorne general seasonal trends. In particular there were two periods of abundance of S. elegans each year, one briefly in the late winter or carly spring, the other, of longer duration, corresponding to the summer period of stratification of the offshore water. In 1930, 1931, 1932, 1936 and 1937, and to a lesser extent in 1933 and 1934, there was an abrupt transition in the autumn, when S. elegans was replaced by S. setosa, and an influx of south-western indicators occurred. These gen­ eral trends are quite comparable with the events shown in more detail in 1979, and their continuity over the period of time suggests sorne relation to elima tic and/or hydrographie factors that undergo the same seasonal alternation every year.

Trends in 1968-1979

The evidence presented for the more recent period begins in 1968, wh en S. elegans was of rare occurrence at L5. The return may be said to have commenced in 1969, and in each year after that up to 1972 there was a graduai increase in summer abundance of S. elegans but little change in the winter. In 1973 and subsequent years S. elegans was also present in late winter or early spring, though in lesser number than in the summer. From 1977 to 1979·s. elegans was the dominant species Figure 7 at L5 for most of the year, and samples taken doser Weekly fluctuations of Sagitta at L5 from 1968 to !919. For each inshore at L4 and elsewhere confirm that it was gen­ year the upper graph shows total S. elegans as number per standard erally abundant in the shallow water off Plymouth. haul; the lower graph gives the percentages of S. elegans (black) and S. setosa (white). During the whole period of return of S. elegans,

234 FLUCTUATIONS IN CHAETOGNATHS

whether in summer or winter, it was usually accom­ species or population is of most interest to the investiga­ panied by north-western plankton indicators, most tor at the time. notably Aglantha digitale (Southward, 1980). Further­ more, the sudden decreases each autumn, as for exam­ ple from 1972 to 1979 were always marked by propor­ tional increases in S. setosa and by influxes of south Hydrographie factors western indicators, as noted for 1930-1938. Although there was an overall increase in abundance of S. elegans It might be objected that the changes observed at L5 from 1969 to 1979 the change was not a smooth progres­ and A could be due to minor displacements of the sion, and in 1971 and 1976 for example, there were hydrological front off the Eddystone, not to major periods of setback for the species. biological or environmental events. There are two main arguments against this interpretation: one is that the front is related to physical factors, topography and tides, which can be considered to be unchanging over the time scale being discussed; the other is deduced from the biological observations, which show that when SIGNIFICANCE OF THE CHANGES there is a substantial change in the dominance of the species at L5 and A this change is reflected at the The long-term trends inshore stations and over a much wider area than the immediate vicinity of the front. This is not to deny that Both periods of change in the chaetognath population hydrographie forcing is absent. Sorne of the variation occupied severa) years until one or the other species observed at L5 during periods of strong advection must predominated for most of the year. In the first phase be due to alterations in the strength and direction of the in the 1930s the complete change from S. elegans to water movement (Southward, 1961; 1962; Southward, S. setosa took 9 years; the reverse phase in 1968-1979 Demir, 1972). In fact there can be no doubt that from took 11 years. In both phases there were periods of September to March the plankton off Plymouth is varying dominance of the two species rather than a considerably influenced by advective changes. This ded­ sudden or progressive switch. A similar sort of varia­ uction from the biological data for L5 and from large­ tion occurred in associated species including medusae, scale surveys is confirmed by small scale plankton surv­ siphonophores, copepods, echinoderm larvae, tunicates eys over a grid of stations around L5 (Southward, and also in abundance of post-larval young fish (South­ Demir, 1972; unpublished surveys). There can be posi­ ward, 1980). The change in the community occupied tive correlations at certain stations between incursions many years, and the process can only be regarded as of higher salinity in winter and influxes of macroplank­ sudden relative to the 30 year period of comparative ton indicator species. However, it is not possible to stability from 1939 to 1968. Other biological changes show significant correlation of the seasonal biological in the W. Channel were also graduai. Data on the changes with seasonal change of salinities measured at herring fishery, which was supposed to have failed a single station. This is because the annual range is suddenly (Kemp, 1938), show a period of declining very small, of the same magnitude as the standard recruitment extending nack 5 years (Cushing, 1961). It deviation for the series (Pingree, Pennycuick, 1975). is likely that the herring failed in competition with Indeed, Cooper (1952) was quite justified in saying "in another clupeid fish, Sardina pilchardus (Cushing, 1961; our area it bas never been possible to correlate salinity Cushing, Dickson, 1976). The region being studied is with much else". This inability to detect possible advec­ close to the northern and ·southern limits of severa) tive changes from physical and chemical measurements species of plankton organisms and fish (Southward, was one of the major reasons for establishing the 1963), and there have been sorne well-marked short routine macroplankton sampling program, in the hope and long term changes in temperature (Southward et that the sensitivity provided by use of biological indica­ al., 1975; Southward, 1980). The ecosystem might thus tors would be more informative about changes in be expected to be Hable to periods of instability, caused water-masses and current strength (Russell, 1935; 1936; by changes in temperature and other abiotic factors 1939 b), as bas proved true both for the W. Channel which would alter the balance between competing spec­ and elsewhere (e.g. Russell, 1952; Fraser, 1952; 1969; ies of different geographical distribution (p. 3). Alvarino, 1965; 1969). Random fluctuations by chance occurring in synchrony might also produce what is called stochastic forcing (Saltzman, 1982) and initiate other biological fluctua­ Seasonal patterns tion. Many of the potential causes of disturbance can be absorbed by the resilience of an ecosystem (Holling, It was noted earlier that there are sorne regular seasonal 1973; Peterman et al., 1979). This resilience should patterns in the abundance of the Sagitta species, more mean that changes, when they do happen, will tend to obvious in sorne years, perhaps indicating the existence be abrupt, as an ecosystem switches from one stable of a regular cycle of hydrographie events. The most state to another (cf Jones, 1977), the process of rectific­ strikingly regular change is the autumn switch from ation referred toby Cushing and Dickson (1976). How­ S. elegans to S. setosa, apparently associated with ever, the changes observed off Plymouth were more advection of south-western plankton which approaches graduai than this: the abruptness of sorne aspects is the Plymouth stations as a cyclonic swirl (Southward, more in the eye of the beholder, and depends on which 1962; Southward, Demir, 1972). We can link this

235 A J. SOUTHWARD change with the simultaneous spread of Biscay species also suggested size frequency distribution patterns across the mouth of the Channel into the Bristol Chan­ might indicate different water masses (Rakusa­ nel, an intrusion that can in sorne years be detected as Suszczewski, 1967). Copepods appeared to be the com­ far north as the Irish Channel (Southward, 1962). The monest food taken by S. elegans, though few of the · Jess marked increases in S. elegans during the late win­ Western Channel population were feeding on Calanus ter and spring, often associated with northwestern indi­ (Rakusa-Suszczewski, 1969); at that time this species cators, are more variable in timing, but seem to be had not yet increased in abundance (Russell et al., associated with advection from a westerly or north­ 1971). Rakusa-Suszczewski (1969) also found that westerly direction. We may perhaps link this trend with S. setosa preyed chiefly on copepods, but in addition observations of a south-east going residual current off the Western Channel population fed intensively on the Isles of Scilly (Carruthers et al., 1951; Cooper et al., the cladoceran, Podon intermedius, which is usually 1960) and corresponding distributions of north-western restricted to surface water and always occurs above the indicators (Russel, 1936; Southward, 1961; 1962). A thermocline. This suggests these particular S. setosa period of summer abundance of S. elegans is also a were feeding at lesser depths than the S. elegans, and fairly regular seasonal occurrence, at least in those that the two species were vertically separated at the years when the species is a significant element of the time of sampling. A further analysis of the same data chaetognath population, and there is usually an accom­ and other information (Pearre, 1980) shows that the panying increase of north-western indicators. Of these two species differ in the relationship between size of regular or even cyclic events, those occurring from chaetognath and size of prey, bence, since S. elegans September to March are the easier to interpret, since grows larger than S. setosa, effective competition for advective effects are involved, but the summer period food will occur mostly at the smaller sizes. Less informa­ of S. elegans abundance is more puzzling. If, as Pingree tion is available on whether the two species prey on one and Pennycuick (1975) propose, this is a period when another. Chaetognaths are well-known to be capable of advection is less, and in which the major hydrographie cannibalism, which may have an adaptive value in factors are local surface heating, the development of ensuring population survival at difficult times (Pearre, the thermal discontinuity and transfer through it by 1981; 1982). The Sagitta in the Western Channel do vertical turbulence (see also Taylor, Stephens, 1983), eat other Sagitta (Rakusa-Susczczewski, 1969), whether then the presence of an elegans community is difficult their own or the other species is not known, but at to explain. In the absence of appreciable advection we a frequency lower by an order of magnitude than have to assume that S. elegans, during this period of consumption of copepods. Therefore, under summer abundance off Plymouth, is in sorne way better fitted conditions of relatively abundant small copepods, it than the more neritic species S. setosa to survive in the seems that competition for food in general will be more summer conditions of thermal stratification, lowered important than interspecific predation. salinity and partial stagnation. We need to consider From the data on feeding of Sagitta we could suggest how this apparent competitive advan tage could be medi­ that the presence of a larger number of Calanus, as for ated, or search for alternative explanations for the example after 1968 and before 1932 (Russell et al., presence of S. elegans in summer. 1971) provided better growth and survival of large S. elegans, thereby increasing the fecundity of the popu­ lation and allowing the young stages to outcompete Competition the young of S. setosa. Unfortunately this attractive hypothesis is not proved by comparing the mean sum­ As already noted, the two species of Sagitta do coexist, mer abundances for May to August inclusive (Tab. 2). though the area of overlap is small, and probably only It is true that the first notable abundance of S. elegans the smaller stages consistently occur together. In these occurred only 1 year after a major increase in Calanus circumstances is there competition for food or preda­ but regression of S. elegans on Calanus gives a low tion by one species upon the other? Chaetognaths have correlation (r = .22), bence most of the increase in been shown to eat a wide variety of plankton organisms S. elegans must be accounted for in other ways. (review by Alvarino, 1965), but copepods are the chief food. The data of Rakusa-Suszczewski (1969) are most relevant to the present problem, but it should be noted Stratification and competition that S. elegans was studied only from one station in the Western Channel, at a period (1965) when S. setosa Although we cannot demonstrate a direct correlation was dominant, most of the information, especially for between S. elegans abundance and the abundance of a the larger sizes, coming from stations farther north. suitable prey species, there is still a general association This author believed that the distribution of the two between S. elegans, north-western plankton indicators, species might be controlled by food availability, and and a high standing crop of macroplankton. The alter-

Table 2 Summer abundances of Calan us helgolandicus and Sagitta elegans at station L5; mean numbers per standard haul for May-August inclusive.

1966 1967 1968 1969 1970 197t 1972 1973 1974 1975 1976 1977 1978 1979

Cal anus 9170 3240 4610 21655 76690 32930 16900 35790 17420 40920 25350 31580 26230 15550 S. elegans 26 0 350 106 1070 169 1460 3130 980 1090 1460 2110 1310 3190

236 FLUCTUATIONS IN CHAETOGNATHS native association of S. setosa, south-western indica­ whether the hydrographie data from El could be fitted tors, and S ar dina pilchardus, is linked to lower standing by a model involving a local cyclonic swirl, with shear crops of macroplankton. The change from one plank­ at the thermocline and sorne advection of deep water ton regime to the other has been attributed to abiotic from the west or north-west, independent of surface factors, particularly the changes in sea temperature changés. If such water was of similar salinity but colder observed during the recent climatic fluctuation (South­ than the local bottom water (e.g. of Celtic Sea origin) ward, 1963; 1980). One of the characteristics of the its slow passage and heating up as it crossed the Ply­ northern side of the Western Channel off Plymouth, mouth region might give the same beat budget as a which it shares with sorne other sea areas where static model. Advection of this nature might also pro­ S. elegans can be abundant (e.g. Celtic Sea, Western vide one possible explanation of the large numbers of Irish Sea, Northern North Sea) is the presence of sum­ juvenile S. elegans found along the northern side of mer stratification. In contrast, regions where S. setosa the W. Channel in July 1935 (Russel, 1936), and the is frequently dominant in summer (Western Channel corresponding extent of juvenile Aglantha in July 1979 to the east and south of Plymouth, Eastern Channel, (Southward, 1980 and unpublished data). parts of the Bristol Channel, parts of the Southern and Eastern North Sea, Eastern Irish Sea) are less stratified CONCLUSION or vertically mixed (cf. Pingree, Griffiths, 1978), although there are exceptions to this generalization. It The evidence reviewed here suggests that advection is may be that it is the presence of cool bottom water a major factor controlling the chaetognath population in summer that gives S. elegans the advantage over off Plymouth from September to April, and the long S. setosa, by provision of a reserve for breeding stock. term changes in species dominance in that part of the year could be attributed to minor modifications of the Harvey (1925), following Orton (1920), pointed out the direction and strength of the advective forces (e.g. relatively large biological effects that might ensue from wind) under the control of climate. However, on pre­ comparatively small changes in sea temperature, by sent evidence we cannot separate such effects from alteration in the rate of metabolic processes and repro­ more general changes in the north-south distribution ductive capacity. Quick stratification helps to preserve of the communities farther to the west, which act as a cold bottom water, and the rate of downward transfer centre of abundance for S. elegans (see Southward, of beat is slow enough to ensure severa! months of low 1961; 1962). The situation in summer, May to August temperature on the bottom. Both S. elegans and the inclusive, is more complex than suggested earlier: the north-western medusa Aglantha digitale when they existing information may be inadequate to allow us to occur above the thermocline and in the mixed inshore determine the exact mechanisms responsible for the waters are often represented by juvenile stages, which summer changes in the chaetognath population off can apparently benefit from the higher temperatures Plymouth. In future it is evident that more attention and greater rate of growth possible there, but the adult must be given to differences in the vertical distribution stages are usually restricted to the deeper cold water, of plankton and of environmental factors. Nevertheless, which may be essential to gonad maturation of these the linking factor between ali the changes appears to arctic-boreal species. Thus it could be proximity of a have been the warming and then the cooling of the deep water breeding population, allied to minor chan­ Northern Hemisphere. If change in climate is partly ges in the bottom temperature and the rate at which it mediated through competition between species; if bio­ warms up, that controls the success or otherwise of logical changes lag behind environmental changes by an inshore population of S. elegans off Plymouth in varying intervals (Southward et al., 1975); if the process summer. The long term records for bottom temperature takes several years for each pair of species (as with at El are less complete than the surface data. However, Sagitta); and if each competing pair has differing sensiti­ Maddock and Swann (1977) suggest that during the vity to environmental change: then we would expect warm period from 1930 to the 1960s, when S. setosa the period of change for the whole community to be was dominant, the thermocline may have been extended, as it has proved to be in the Channel off established earlier and broken down earlier in the Plymouth. Criticism has been levelled at the concept autumn. that large biological changes can result from small Their analysis shows that bottom temperatures were changes in temperature, especially when there are generally higher in July and August during the warm seasonal ranges of go and vertical differences of 5°. period from 1930 to 1960 than before or after, but the This argument forgets that biological processes have differences are small and partly obscured by random rouch higher temperature exponents than physical pro­ variation. It may be significant in this connection that cesses (p. 18) and overlooks the possibility that even a in 1979, the year of maximum S. elegans, the bottom very small change in environmental factors, if persist­ water in July was much colder than the average. Per­ ent, may alter the competitive advantage of one species haps future analysis of a longer term series will be able over another, irrespective of the annual and vertical to demonstrate a better correlation between sub­ range normally experienced, since the effect will be thermocline conditions and local plankton. An addit­ cumulative or additive. The idea presented here that ional point to investigate would be the timing of the environmentally-linked changes of species or ahun­ onset of stratification in relation to advection from the dance can be graduai, even when the effects are west and north-west in the spring, a process that might sharpened by competition, is relevant whatever the be necessary to provide a nucleus for subsequent sum­ exact mechanism, temperature or advection or both, mer breeding. It would also be worthwhile investigating that provides the forcing factor.

237 A. J. SOUTHWARD

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