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The variability in the zooplankton spatial pat- tern throughout the annual cycle ...... (e.g., Lee & McAlice,1979; Gagnon & Lacroix,. 1982, 1983; Costello & Stancyk ...
Hydrobiologia 288: 79-95, 1994. © 1994 Kluwer Academic Publishers. Printedin Belgium.

79

Temporal variability of the spatial distribution of the zooplankton community in a coastal embayment of the basque country in relation to physical phenomena Fernando Villate Laboratoriode Ecologia, Facultadde Ciencias, Universidaddel Pais, Vasco/Euskal Herriko Unibertsitatea, Bilbao, Spain Received 6 March 1993; in revised form 28 July 1993; accepted 10 November 1993

Key words: zooplankton, spatial patterns, physical phenomena, harbour system

Abstract The hydrographic structure of Abra Harbour, a tidal embayment located at the seaward end of the highly polluted estuary of Bilbao, is influenced by the inflow of a polluted estuarine plume, the asymmetry of the harbour basin, and the tidal circulation pattern. Multivariate analysis of the spatial variability of the zooplankton between May 1981 and May 1982 showed that significant differences in zooplankton abundance and species composition occurred from the inner-eastern to the outer-western side, related to the horizontal structure of the system. The annual temperature cycle, however, was the major source of temporal variability, and the seasonal stratification in the water column was responsible for the predominance of vertical differences in zooplankton composition during the spring-summer period. Wind-induced turbulence and tides were other sources of variation. With increasing turbulence (rough sea), the spatial gradients in zooplankton composition were not as clear, and with decreasing tidal height the compositional differences in the horizontal dimension tended to be more evident. Spionid larvae accounted for strong local differences within the Harbour. They were usually segregated from other taxa, and mainly associated to the deeper waters characterized by a greater hydrological instability.

Introduction The spatial organization of zooplankton community is governed by physical, chemical and biological properties of water masses. Physical phenomena are situated at the basis of the hierarchy of ecological processes in coastal systems (Amanieu et al., 1989), where riverine run-off, tides and wind stress may induce major environmental changes over different temporal and spatial scales (Cloern & Nichols, 1985). Human wastes, when present, may also induce drastic

changes in the environmental properties and population dynamics. Detailed investigations of the spatial distribution of zooplankton in relation to environmental variability are therefore necessary in order to understand the ecological processes in these systems, and the way in which they are affected by anthropogenic influences. The Abra Harbour is an appropriate system to observe the effect of several factors such as pollution, thermal stratification, wind-induced turbulence and tides on the spatial organization of the zooplankton community on a fine scale. Thus, the

80 present study describes the spatial heterogeneity of zooplankton in Abra Harbour throughout an annual cycle at approximately monthly intervals. The aim of this report is to define the hierarchical contribution of the above mentioned factors to the temporal variability of the zooplankton spatial distribution within this coastal system. This was carried out by using multivariate statistical treatment of the zooplankton data.

Study area Abra Harbour (Fig. 1) is a semienclosed embayment at the seaward end of the estuary of Bilbao (southeast coast of the Gulf of Biscay). The main hydrographic features of this estuary and Abra Harbour have been studied by Urrutia (1986). The estuary receives a moderate river run-off and waste from a wide urban and industrial area, resulting in a highly polluted system. However, the volume of the estuary is relatively small in relation to the volume of the harbour, and the estuarine plume which flows throughout Abra Harbour contains a high percentage of seawater (salinities of less than 30%0 are not frequent). The plume usually moves seaward along the eastern section (Coreolis forces), which is shallower than the western that has typically marine water masses. These hydrological and topographical peculiarities confer the Abra Harbour with a particular asymmetry, showing a longitudinal gradient in depth and hydrological properties from the inner eastern to the outer western part. Tidal amplitude ranges approximately between 0.8 m at neap tides and 4.3 m at spring tides. Phytoplankton dynamics within Abra Harbour have been studied by Urrutia & Casamitjana (1981) and Urrutia (1986), and the first observations on mesozooplankton abundance and composition were made by Casamitjana & Urrutia (1982). Compositional differences in phytoplankton and mesozooplankton between this system and the adjacent shelf waters were analysed in late spring-early summer by Orive (1989) and Velez et al. (1988) respectively.

Methods Abra Harbour surveys included a series of eight sampling sites (Fig. 1) where samples were taken at approximately monthly intervals from May 1981 to May 1982. On each occasion, two consecutive cruises were made during daylight hours, one on the ebb tide and the other on the flood tide. The sea state differed among surveys during the study period. Only on cruises in June, August and November 81, and May 82 was the sea calm. There were rough seas in October 81 and March 82, and moderately rough seas in July 81 and April 82. Choppy or slightly choppy conditions were usually found on the other cruises. Water samples for chlorophyll determination and zooplankton analysis were simultaneously collected using 7 1 single Van Dorn bottles and 30 1 double sets of Van Dorn translucent bottles respectively at each sampling site and depth. The depths sampled were 20, 15, 10, 5 and 0 m at the deep sampling sites (stations D, E, P and X); 15,10, 5, 2 and 0 m at station C and 10, 5, 2 and 0 m at the shallow sampling sites of the inner zone (stations A, B and T). Temperature profiles were obtained simultaneously to zooplankton samplings with a Ramptor bathythermograph at the selected depths. Chlorophyll 'a' was estimated spectrophotometrically in 90% acetone extracts after filtering 0.5-21 subsamples taken from the 71 water samples. Zooplankton were collected by filtering 30 1 water samples through a 45 m mesh net, and preserved in buffered 4% formalin until samples were analysed under a stereomicroscope. The zooplankton was counted and identified to species level in the majority of holoplankters, except for copepod nauplii, while meroplankters were differentiated into species, genus, order or class according to the difficulty of identification. Zooplankton samples of the flood tide cruises were only analysed in May, July and November 1981, which were surveys representative of the spring surface warming, the mid-summer stratification and the autumn mixing periods respectively. Samples taken at station X were only analysed in May, June, July and November

81

Fig. 1. Map showing sampling sites in the study area.

cruises. Samples obtained at 2 and 15 m depth were analysed for the ebb tide survey in May, and for both surveys in July and November. The variability in the zooplankton spatial pattern throughout the annual cycle, and between the

flow and ebb tides in May, July and November 1981, was examined by multivariate analysis. The technique selected to determine the spatial heterogeneity of zooplankton community was the correspondence analysis (CA), using the statisti-

82 adults and copepodites of the genus Paracalanus,

cal package programs of Lebart and Morineau (1982). The advantages of the CA in the treatment of zooplankton data are discussed by Ortner etal. (1989). Analyses were performed for each cruise with taxa present in more than

'/2

Clausocalanus, Pseudocalanus and Ctenocalanus were included, but Paracalanusparvus dominated

largely in all surveys. Oithona spp included 0. nana which dominated from June to November, and 0. helgolandica which dominated from December to May. Oncaea spp included O. subtills as the dominant species and 0. media. Among the pluteus larvae of Echinodermata, echinopluteus of Spatangoids dominated in May, ophiopluteus in June and July, and echinopluteus of Diadematoids in August and April. Fritillaria spp was

of

all samples. The taxa employed in each CA are listed in Table 1. Among Medusae, Sarsia sp and Lizzia blondina dominated in May and June, Obelia sp in July, and Liriope tetraphylla in August and October. Muggiaea atlantica was the dominant

siphonophore in all surveys. Evadne sp was E. nordmanni in March, May and June, and E. spinifera in August. In the P-calanus category the

mainly constituted by F. borealis, and Oikopleura spp by 0. dioica.

Table I. List of taxa used in correspondence analyses indicating the code of taxa and which taxa were included in each analysis. Taxa

Surveys Code

Noctiluca scintillans Stenosetmella ventricosa Proplectella sp Favella markuzouvski Acantharians Foraminiferes Medusae Siphonophora Ciphonauta larvae Gastropod veligers Bivalve veligers Spionid larvae Sabellarid larvae Podon intermedius Evadne spp Copepod nauplii Calanus sp P-calanus Cetropages tpicus

NOC STE PRO FAV ACN FOR MED SIF CIF GAV BIV SPL SAL POD EVA CNA CAL PCA CEN

M81

J81

J81

A81

081

.

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.

. .

.

. .

. .

. .

. .

.

.

.

.

.

.

.

.

.

.

.

.

.

.

.

. .

.

.

.

.

. .

.

.

.

Temnora longicornis

TEM

Acartia clausi

ACR

.

Oithona spp

OIT

.

Oncaea spp Euterpina acutiftons Barnacle nauplii Sagitta friderici Pluteus larvae Doliolumn nationalis Fritillariasp Oikopleura spp

ONC EUT BNA SAG PLU DOL FRI OIK

. .

D81

F82

M82

.

.

.

.

N81

.

.

..

.

A82

M82

83 Results Abundance distributions

Figure 2 shows the vertical variability in zooplankton abundance and profiles of temperature and chlorophyll for each cruise. In May 1981, temperature and chlorophyll values were relatively homogeneous in the water column, although temperatures were slightly higher in the surface layer, and zooplankton abundance was higher in the deeper water. In June and July, the water column was thermally stratified, and the chlorophyll content and the zooplankton abundance increased significantly in the surface waters. The phytoplankton maxima were in the uppermost layer and zooplankton maxima at 5 m depth. In August, a well-established thermocline was found between 10 and 20 m depth. The chlorophyll maximum remained at the surface but chlorophyll values increased below the thermocline, and zooplankton abundance was highest in the 5-10 m stratum. From October 1981 to March 1982, temperature and chlorophyll content were relatively homogeneous in the water column. Zooplankton showed the highest densities at 10 m depth (October, February and March) or was relatively constant below the surface layer where abundances were lower (November and December). In April and May 1982, slight gradients of temperature were found in the upper 10 m layer, chlorophyll content showed no remarkable differences in relation to depth, and highest abundances of zooplankton occurred at 10 and 5 m depth respectively. The horizontal distributions in zooplankton abundance and chlorophyll content within Abra Harbour (Fig. 3) show that both zooplankton and chlorophyll increased towards the outer part, and from the eastern section to the western section, in most cruises. This spatial pattern was more marked in zooplankton abundance for the cruises of May, June, July, November, February and March. By contrast, in October chlorophyll concentrations were higher in all the inner sites while no clear differences in zooplankton abundance were found between the inner and the outer part.

In December, chlorophyll values were low in general, and the highest chlorophyll content was found in the inner zone of the western section.

Spatial organization of zooplankton

The temporal changes in the spatial segregation patterns of zooplankton populations are well summarized by the ordinations of samples and zooplankton taxa in the space formed by axes 1 and 2 of correspondence analysis performed for each cruise (Fig. 4). Late spring cruises

In May 81, at flood tide, the analysis reveals that the main compositional differences in zooplankton occurred between surface and subsurface waters. The good correlation of axis 1 with temperature (r=0.690, p>0.001) suggests that these compositional differences were associated with thermal differences. Axis 2 accounted for horizontal differences in the zooplankton composition between the western and the eastern sections within the harbour. Favella was the most representative zooplankter in surface waters, Calanus and pluteus larvae of Echinodermata characterized the western area assemblage, and Spionid larvae were clearly restricted to the deepest zone of station D. At ebb tide, however, the main compositional differences in zooplankton distribution occurred horizontally between the inner-eastern and the outer-western regions. The differences between surface and subsurface waters were accounted for by axis 2, which was strongly correlated with depth (r= -0.723, p>0.001) and temperature (r=0.729, p>0.001). Surface assemblage was characterized by Acartia and Favella in the inner and outer regions respectively. Among taxa associated to subsurface waters, pluteus larvae of Echinodermata, Siphonophores, Medusae, Fritillaria, Bivalve veligers and Podon were the most representative taxa of the outer area while Oncaea, Oithona and P-calanus characterized the inner area. The Spionid larvae appeared mainly associated to the innermost zone of the eastern

84 TEMPERATURE ('C ) 14

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AUGUST Fig. 2. Vertical distribution of zooplankton abundance in relation to temperature and chlorophyll profiles from May 1981 to May 1982. Circles: mean values. Lines: range of values.

85 CHLOROPHYLL (mgChlm -3 )

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86 TEMPERATURE ('C )

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MAY 82 Fig. 3. Horizontal distribution of zooplankton abundance and chlorophyll content from May 1981 to May 1982. Circles: mean values. Lines: range of values.

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Fig. 4. (continued)

section and to the deepest layer of the outermost zone of the same section. In June (Ebb tide) the ordination of samples along axis 1 shows that the main compositional differences in zooplankton occurred between the surface and the deepest layers in the outer-western sites. This axis was correlated with depth (r = - 0.677, p> 0.001), temperature (r = - 0.501,

p>0.005) and chlorophyll (r = - 0.558, P> 0.001) while axis 2 accounted for horizontal differences in zooplankton composition between the outer-western and the inner-eastern sites. Temora, Oncaea and Fritillariawere the most representative zooplankters in the deepest waters of the outer-western area, and pluteus larvae of Echinodermata in the surface waters of the same

91 area. Acartia, Oikopleura and Copepod nauplii also showed a superficial trend. Spionid larvae appeared mainly associated to the deepest layers of the sites located in the inner-eastern zone.

dermata showed the most superficial trends in waters above the thermocline. Compositional differences between the inner and the outer parts were accounted for by axis 2, although it was also correlated with depth (r=0.489, p>0.01) and

Summer cruises In July, at ebb tide, clear vertical differences were found in relation with the profiles of temperature and chlorophyll, since the first axis was strongly correlated with depth (r = 0.828, p> 0.001), temperature (r = - 0.893, p> 0.001) and chlorophyll (r = - 0.621, p> 0.001). Noctiluca and pluteus larvae of Echinodermata were the most restricted taxa to surface waters, and Foraminiferans and Temora to the deeper waters. Acartia, Medusae and Oikopleura also distributed towards the upper layers, while Acantharians, Siphonophores, Gastropod and Bivalve veligers and Oncaea predominated in the deeper layers. Axis 2 accounted for differences between the outer-western and the inner-eastern sections, Temora, Sagitta, Siphonophores and pluteus larvae of Echinodermata being the most characteristic taxa of the outer-western area. Euterpina and Spionid larvae showed aggregation in depth at stations C and D. At flood tide, the vertical differences in relation to temperature and chlorophyll remained, since axis 1 was well correlated with depth (r = - 0.753, P> 0.001), temperature (r = 0.858, p> 0.001) and chlorophyll (r = 0.546, p > 0.001), but differences were not so clear as at ebb tide. Axis 2 accounted mainly for the segregation of the Spionid larvae which were associated to station C. Medusae and Noctiluca were the most representative taxa in the surface waters. Pluteus larvae of Echinodermata were mainly restricted to the upper layers of the outer area while Acantharians and Foraminiferans were the most characteristic zooplankters in the deeper layers. In August (Ebb tide) the main compositional differences occurred between waters bellow and above the thermocline in the outer area, as it was corroborated by significative correlations of axis 1 with depth (r = 0.682, p> 0.001) and temperature (r = - 0.570, p> 0.005). Oncaea dominated zooplankton bellow the thermocline while Centropages, Evadne and pluteus larvae of Echino-

temperature (r= - 0.529, p>0.005). Acanthar-

ians and Foraminiferans showed the outermost trends, and Medusae and Spionid larvae the innermost trends. Autumn cruises

In October (Ebb tide) no clear horizontal or vertical gradients in zooplankton composition can be inferred from the analysis. The main differences were accounted for by Spionid larvae which were associated to subsurface waters of the station located in the innermost zone of the eastern section, and Evadne, Medusae and Foraminiferans which characterized the upper layers of the outer-western area. Axis 2 was not easily interpretable. In November, at ebb tide, a clear compositional gradient from the inner-eastern area to the outer-western area was stated by axis 1 while no clear horizontal or vertical gradients could be inferred from axis 2. Oithona and Euterpinawere the most representative taxa in the inner-eastern area, and Oncaea in the outer-western area. Spionid larvae were found to be mainly restricted to the deepest waters in station B. At flood tide, the compositional differences between the inner-eastern and the outer-western sites of the harbour were more evident, the region of stations T and D appearing to be an intermediate area. Zooplankton taxa showed greatest segregation within the harbour than observed at ebb tide but the distribution pattern was similar. Oithona and Euterpina remained dominant in the zooplankton assemblage of the inner-eastern area, and Spionid larvae appeared in the deepest layers of stations B and C. Winter cruises

In December (Ebb tide), compositional differences from the inner part to the outer part were

92 inferred from the analysis, but much of the compositional contrast between the Abra sites was between the inner-western part (station T), where Acartia was the dominant zooplankter, and the outer area. In general, the inner assemblage was characterized by Acartia and the outer assemblage by Oncaea. Spionid larvae and Euterpina were found to be strongly associated to the deepest layers of the inner-eastern and outer-eastern zones respectively. In February (Ebb tide) the analysis illustrates differences in zooplankton composition between the outer-western and the inner-eastern sites. However, most of the taxa were plotted near the axis origin, denoting a feeble spatial segregation among them. Oikopleura and Sabellarid larvae showed the outermost and the innermost trends respectively, while Spionid larvae and Bivalve veligers characterized the deepest zooplankton assemblage in the inner area. The percentage of variance explained by axis 2 was not found to be significant. In March (Ebb tide) the interpretation of samples ordination in the space formed by axes 1 and 2 was difficult, and most of the taxa were grouped at the center of the axes. Proplectella, which was associated to the deep sites in the eastern section, and Spionid larvae, which were associated to the innermost site in the eastern section, showed more local distributions than the other taxa. Early spring cruises

In April (Ebb tide) compositional differences between the inner and the outer areas were evident. Feeble vertical differences in zooplankton composition were also inferred from axis 2, since it was correlated with depth (r = - 0.550, p> 0.005)

but only accounted for an 18% variance. Euterpina and Oncaea were the most representative zooplankters in the inner area while pluteus larvae of Echinodermatha characterized the outer assemblage. Spionid larvae showed aggregation at station C in depth. In May 1982 (Ebb tide) the main differences in zooplankton composition occurred vertically, since axis 1 was correlated with depth

(r= -0.506,

p>0.005). Evadne and Siphono-

phores were the most representative taxa in surface waters while Spionid larvae and Euterpina characterized the zooplankton assemblage in the deepest layers of the eastern section, and Bivalve and Gastropod veligers the deeper layers of the western section. Axis 2 was found to be of difficult interpretation.

Discussion The spatial pattern of zooplankton differed among surveys and was coherent with physical processes observed in the Abra harbour during the study period. In spring, the slight thermal gradient in the upper layers was already responsible for the differences in zooplankton composition between the surface and subsurface waters (e.g., in May 81), but these differences were less consistent than in late spring and summer. From June to August, seasonal stratification in the water column was the major physical factor regulating the spatial organization of the zooplankton. Chlorophyll profiles were closely related to the thermal structure of the water column, and the highest zooplankton variance was accounted for by compositional differences in the vertical. In June and July, when the thermocline was not yet defined, chlorophyll showed surface maxima and was positively correlated with temperature. In August, when the thermocline was well defined, the chlorophyll maximum remained in the surface layer, but a secondary peak was associated with the depth of the thermocline. Townsend et al. (1984) have described a similar evolution of the chlorophyll profiles in relation to the structure of the water column. They found chlorophyll maxima in the surface waters when the pycnocline was not well defined, and at or just above the pycnocline when a pronounced pycnocline occurred. Different patterns of zooplankton distribution in relation to profiles of chlorophyll and temperature have been reported in epiplanktonic communities. Southward & Barret (1983) observed that

93 only a small part of zooplankton showed signs of aggregation at the thermocline or the chlorophyll maximum, while Fragopoulu & Lykakis (1990) found that the majority of the zooplankton tend to aggregate at the thermocline layer. Pingree et al. (1982) found the highest densities of microzooplankton in the chlorophyll maximum, but no consistent associations between the abundance of the dominant species of metazoans and the chlorophyll concentration. Herman (1984) described a major aggregation of the dominant zooplankton species within the depression located between the surface and the subsurface chlorophyll peaks. Our results show that zooplankton maxima did not coincide with the chlorophyll maxima. The highest zooplankton densities were just below depths of the chlorophyll maxima in June and July, and in layers between the surface chlorophyll maximum and the thermocline in August. Noctiluca, which was the most representative protozooplankter in summer, was associated with the surface chlorophyll maximum in July, but not in August. Only pluteus larvae maintained a consistent association with the chlorophyll maximum from June to August. Pluteus larvae have little capability for movement (Chia et al., 1984), and seem to be mainly phytoplanktophagous, feeding on a wide range of particles including small diatoms and flagellates and relatively large dinoflagellates (Thorson, 1946; Strathmann, 1971; Fransz et al., 1984). The taxonomic segregation in relation to depth during this period shows that Medusae and Evadne were both associated with the uppermost layer, while Temora, Oncaea and Foraminiferans distributed towards the deepest waters. Acartia, Oikopleura and Copepod nauplii showed higher densities in the upper layers, Bivalve and Gastropod veligers in the deeper layers, and Oithona and P-calanus in the intermediate layers. In general, these patterns are in agreement with those of others. Fiedler (1983) found Paracalanusand Oithona maxima above the Oncaea maximum, and the highest abundance of Evadne in surface waters above the Acartia and Paracalanusmaximum.

Pugh & Boxshall (1984) observed the highest abundances of Appendicularians and Oithona in

the upper layers, and of Oncaea and Foraminiferans in the deepest layers, and Magnesen et al. (1989) found highest abundances of Acartia, Paracalanus, Copepod nauplii, Evadne and Appendicularians at the surface (0.5-5m), highest

abundances of Temora and Bivalvia larvae at 10 m, and the maximum of Oncaea at 20 m. A scarcity of Oncaea in surface waters was also pointed out by Skjoldal et al. (1983). The disappearance of thermal stratification was accompanied by a predominance of horizontal differences in zooplankton composition. These differences coincided mostly with the pattern of zooplankton abundance, and followed a similar gradient from inner-east to outer-west in relation to the horizontal structure of water masses and topography of the Harbour. The decrease in zooplankton abundance towards the area with most pollution is common in coastal systems that receive urban and industrial effluents (EPOPEM, 1979). The zooplankton assemblage of the innereastern area was characterized by different taxa throughout the autumn-winter period. Oithona nana and E. acutifrons, two neritic species able to colonize relatively desalted waters in coastal embayments (Castel & Courties, 1982), dominated the inner-eastern area in November. Acartia and meroplanktonic groups were the more representative taxa of the inner harbour assemblage in December and February respectively, while E. acutifrons and Oncaea characterized the inner harbour zooplankton in April. A notable aspect is the contribution of Spionid larvae to variability within Abra Harbour. In most analyses, Spionid larvae were responsible for a great percentage of the zooplankton spatial variance in abundance, and appeared strongly segregated from other taxa and associated with deeper waters from different sites in the eastern section (mainly the inner part). This pattern, which agrees with the distribution of benthic forms in the Abra sediments (Rallo et al., 1988), confirms that Spionid larvae occur at high numbers in hydrologically unstable areas (Cazaux, 1973), and include species resistant to pollution (Daro & Polk, 1973). The strong aggregation shown by Spionid larvae, which usually appear in

94 small patches near the bottom, seems a behavioural response to avoid outward transport. According to Levin (1983), the transport of Spionid larvae seawards seems low, although they inhabit coastal systems where net flow is outward going. Tidal circulation is a principal factor in zooplankton short-term spatial variability in tidal coastal systems, as reported by many authors (e.g., Lee & McAlice,1979; Gagnon & Lacroix, 1982, 1983; Costello & Stancyk, 1983; Gajbhiye et al., 1983; Lewis & Thomas, 1986). Our results suggest that compositional differences within the Abra are more evident in the horizontal dimension with decreasing tidal height. In May 1981, samples taken at flood, when the mean tidal height was 2.52 m, showed stronger compositional differences between surface and subsurface waters than between sites. However, at ebb, when mean tidal height was 1.40 m, horizontal differences in zooplankton composition predominated. In November, although horizontal differences in zooplankton composition predominated in both cruises, the magnitude in between sites-difference at flood (mean tidal height 3.44 m) was smaller than at ebb (mean tidal height 1.61). In July, at neap tide, there was no clear horizontal difference, probably due to stratification of the water column and to small differences in tidal height between cruises (2.37 m at ebb tide and 2.12 m at flood tide). Wind induced turbulence also seemed significant governing the spatial organization of zooplankton populations within Abra Harbour. In the October and March surveys, under rough sea conditions, vertical or horizontal segregation patterns were not as clear as in the other surveys. It is known that, in pelagic systems, the role of organisms controlling the system structure decreases when external energy increases (Margalef & Estrada, 1980), and weak swimmer zooplankton species that are vertically separated under low energetic conditions may become mixed by the effect of turbulent flows (Haury et al., 1990). In July and April, although turbulence was relatively high (moderate rough sea) a noticeable vertical and horizontal organization of populations was observed. The maintenance of vertical order in

the zooplankton in July indicates that a moderately rough sea was insufficient for a vertical mixing of water and of populations.

Acknowledgements I thank reviewers for many constructive criticisms on an earlier version of this manuscript. The present paper is part of a doctoral thesis supported by a grant from the Education Universities and Research Department of the Basque Government. I would also like to thank Iberduero for providing the ship. Special thanks go to the crew of the ship and survey colleagues for their help in field sampling.

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