Estuary of Mundaka, Bay of Biscay)

SCI. MAR., 61 (2): 173-188 SCIENTIA MARINA 1997

Tidal influence on zonation and occurrence of resident and temporary zooplankton in a shallow system (Estuary of Mundaka, Bay of Biscay)

F. VILLATE Landare-Biologia eta Ekologia Saila, Ekologi Laborategia, Zientzi Fakultatea, Euskal Herriko Unibertsitatea, 644 P.K. E-48080 Bilbao, Spain.

SUMMARY: Tide-induced variability in the zooplankton community was analysed during 2 tidal series of 14 h during spring tides and neap tides in the shallow estuary of Mundaka by relating short-term changes in composition and spatial distribution of populations to tide-associated parameters (water level, current velocity and direction, mixing and stratification, and salinity). A strong tidal influence was found in the zooplankton composition and distribution on a day-week time scale (spring-neap tidal cycles) and at hour time scale (high-low tidal cycle). During spring tides, suspended meiofauna shows high densities at flood and ebb tides; the neritic zooplankton can reach the inner estuary at high water, and the autochthonous zooplankton move from the inner zone, at high water, to the outer zone, at low water, over distances of more than one third of the estuary length. During neap tides, autochthonous populations remain around the low middle estuary, the penetration of neritic zooplankton is feeble, and the occurrence of benthic forms in the water column is negligible. The observed effects on the abundance and zonation of resident and temporary zooplankton indicate that tides are a key factor in the estuary of Mundaka by regulating the stock of neritic and autochthonous zooplankton within the estuary, the reproductive success of benthic populations which have planktonic larval development, and meiofauna dispersion and availability as food in the water column.

Key words: Zooplankton, tychoplankton, tidal cycle, transport, estuaries.

RESUMEN: INFLUENCIA DE LAS MAREAS EN LA ZONACIÓN Y PRESENCIA DEL ZOOPLANCTON EN UN SISTEMA COSTERO (ESTUARIO DE MUNDAKA, BAHIA DE VIZCAYA). – Los cambios en la comunidad zooplanctónica por efecto de las mareas fueron analiza- dos durante 2 series mareales de 14 h en mareas vivas y muertas en el estuario somero de Mundaka, relacionando los cambios a pequeña escala temporal de la composición y distribución espacial de las poblaciones con parámetros ligados a las mareas (nivel del agua, velocidad y dirección de corriente, mezcla y estratificación y salinidad). El efecto de la marea sobre la composición y la distribución del zooplancton fue muy notorio tanto a una escala temporal de dias-semanas (ciclos de marea vivas-muertas) como a una escala de tiempo horaria (ciclos pleamar-bajamar). En mareas vivas, la densidad de meiofauna resuspendida es elevada durante el ascenso y el descenso de la marea, el zooplancton nerítico alcanza el tramo interi- or del estuario en pleamar y el zooplancton autóctono es transportado desde el tramo alto del estuario, en pleamar, hasta el tramo exterior, en bajamar, sobre distancias superiores a un tercio de la longitud total del estuario. En mareas muertas, las poblaciones autóctonas permanecen alrededor del tramo medio bajo del estuario, la penetración del zooplancton nerítico es escasa y la aparición de formas bentónicas en la columna de agua es irrelevante. El efecto observado sobre la abundancia y distribución del zooplancton residente y temporal indica que en el estuario de Mundaka las mareas son un factor determi- nante en la regulación de los efectivos de zooplancton nerítico y autóctono en el estuario, los sucesos reproductivos de las poblaciones bentónicas con desarrollo larvario planctónico, y la dispersión y disponibilidad como alimento de la meiofauna en la columna de agua.

Palabras clave: Zooplancton, ticoplancton, ciclos de marea, transporte, estuarios.

*Received August 23, 1996. Accepted February 10, 1997.

TIDAL EFFECTS ON ESTUARINE ZOOPLANKTON 173 INTRODUCTION (Whitfield, 1988); and tidal influence on sediment transport and settling (Uncles et al., 1992; Ten Tides play a major role in the functioning of Brinke & Dronkers, 1993; Ten Brinke, 1994; Smith many coastal systems, being responsible for notice- and FitzGerald, 1994). able mid-term (spring-neap cycles) and short-term Regarding zooplankton, several papers have (low-high water cycles) variations in the abiotic and pointed to the importance of tidal dynamics induc- biotic characteristics of these systems. This role has ing spatial variability in zooplankton distribution inspired several authors to analyse tidal control of within estuaries (e.g. Lee and McAlice, 1979; All- communities and processes in different systems. dredge and Hammer, 1980; Gagnon and Lacroix, Examples include: tide-induced phytoplankton and 1981, 1982). However, tides are not only responsi- microphytobenthos exchanges (Riaux-Gobin, ble for distributional patterns, but also for dynamic 1987); tidal influence on bacteria, microphytoplank- events and survival of endemic populations by ton and microzooplankton abundance (Morales- exporting and reducing their standing stocks. This Zamorano et al., 1991); tidal control of seston quan- effect of tidal exchange in regulating estuarine zoo- tity and quality (Flegey et al., 1992); tidal export of plankton may be especially relevant in small sys- particulate organic matter (Boto and Bunt, 1981); tems where strong river discharges can occur (Ken- tidal redistribution of macrodetrital aggregates nish, 1990).

FIG. 1. – Map of the estuary of Mundaka showing the sampling sites, and the boundaries of the three parts mentioned in the text.

174 F. VILLATE This report examines the effects of tides on mid- around 13 km long, and is characterized by three term and short-term variability of suspended living clearly distinguishable physiographic parts. The organisms larger than 200 µm in a shallow tidal sys- outer part is a broad area open to the sea and filled tem (the estuary of Mundaka). The aim of the study by large intertidal flats, the middle part is occupied was to evaluate the importance of changes in zoo- mainly by emerging salt-marshes, and the inner part plankton composition, abundance and zonation comprises a narrow man-made channel that meets induced by tides in this type of estuary. the meandering channel of the river in the upper estuary and its surrounding wetlands. The river inflow is normally low (monthly mean MATERIAL AND METHODS about 1 m3 s-1 from the main tributary) in relation to the volume of the estuarine basin (mean volume of Study area 32.9 105 m3), such that the estuary is mainly polyha- line and euhaline. However, strong increases in The estuary of Mundaka is a shallow meso-tidal freshwater inputs are frequent due to the torrential system located in the south-east of the Bay of Bis- regime of tributary streams. As a result, the resi- cay, on the Basque Coast (Fig. 1). It forms the cen- dence time is highly variable, and calculated flush- tral axis of the Urdaibai Biosphere Reserve, is ing times (21 to 581 days) at moderate and low river

FIG. 2. – Time series of water height, salinity and current velocity during spring tides atB and G sites of the estuary of Mundaka. Circles: time series on 12 August 1991. Squares: time series on 13 August 1991. For salinity and current velocity plots, open symbols: surface data, filled symbols: bottom data, semi-filled symbols: mid-depth data.

TIDAL EFFECTS ON ESTUARINE ZOOPLANKTON 175 discharges differ largely (Villate et al., 1989). Tides Sampling and data are semidiurnal, and at spring tide the high water is not significantly delayed between the outer estuary Data presented here were obtained from analy- and the upper reaches. The tidal exchange is high, ses of samples collected during a study on the tidal with the mean tidal prism-mean basin volume ratio effects on seston quantity and quality in the estuary greater than 1 (Villate et al., 1989). of Mundaka. The study was carried out in summer Previous research on mesozooplankton (Vil- (August 1991) when disturbances induced by river- late, 1989-90; 1991; Villate et al., 1993) showed runoff fluctuations are smaller and the develop- that true estuarine holoplankters such as Eury- ment of endemic zooplankton reaches the annual temora species cannot develop in the estuary of maximum. Mundaka. The endemic mesozooplankton is dom- Sampling was performed at two sites in the inated by the estuarine-marine species Acartia main channel during two spring tidal cycles on 12- bifilosa, which reach the highest density in sum- 13 August and two neap tidal cycles on 18-19 mer. The meroplankton contributes largely to the August. Sampling sites were located at the lower total zooplankton, and is dominated by barnacle part (station B) and at the upper part (station G) of and polychaete spionid larvae in spring and by the middle estuary (Fig. 1). These sites were gastropod larvae in summer. selected to obtain the most accurate estimation of

FIG. 3. – Time series of water height, salinity and current velocity during neap tides at B and G sites of the estuary of Mundaka. Circles: time series on 18 August 1991. Squares: time series on 19 August 1991. For salinity and current velocity plots, open symbols: surface data, filled symbols: bottom data, semi-filled symbols: mid-depth data.

176 F. VILLATE populations moving throughout the estuary during using a hydraulic flow meter General Oceanics. the tidal cycle. Seaward to the B site, data record- The tidal height was determined by recording the ed at a single point may be less suitable because water level on graduated stakes located at each the basin is wider and the water circulation sampling site. Measurements were made just becomes more complex. Upward to the G site, before and after sampling. although most the water volume moves into the For zooplankton analysis, the entire sample was artificial channel, estuarine waters and popula- examined under a stereoscopic microscope. All indi- tions are also derived from the original channel. viduals were counted, and keyed to different taxo- When tides fall, waters coming from both chan- nomic categories. Most of the holoplanktonic forms nels meet just up from the G site. were identified to species level, while meroplank- Samples were taken from a central point at each tonic larvae and benthic or littoral forms were usu- site over a 14-hour period, beginning at high tide in ally keyed to family, order or class categories. After spring tide series and at low tide in neap tide series. identification, and for this study, all taxa were Zooplankton samples were taken by pump at 2- grouped into wider categories with ecological mean hour intervals from surface water (within the in the estuarine ecosystem. upper 0.5 m layer), 0.5 m above the bottom, and at Abundance of zooplankton taxa is expressed as mid depth (equi-distance from the surface and bot- number of individuals per litre of water, and as a tom samples). Mid-depth samples were not taken percentage of the total zooplankton in each sampling when the water column was less than 2 m deep. series. Short-term changes in zooplankton are Zooplankton samples were obtained by filtering expressed in relative abundance, and data from con- 30 l of the pumped water through a 200 µm sieve, secutive days are plotted together in figures, after preserved in 5% formalin and stained with Rose settling high-tide times, in an attempt to obtain a Bengal. more accurate estimate and to show the general Hourly profiles of salinity were recorded with a trends of zooplankton populations at both spring and field salinometer WTW 196, and discrete mea- neap tides. Organism abundance in relation to tidal surements of the current velocity (at the same phases is expressed as a percentage of the total for depth as zooplankton samples), were also made by each taxon and sampling series.

TABLE I. – Abundance of reported taxa in each sample series expressed in absolute units (mean and maximal values) and relative units (mean values).

SPRING TIDES NEAP TIDES

August 12 August 13 August 18 August 19

Density (ind/l) Percent. Density (ind/l) Percent. Density (ind/l) Percent. Density (ind/l) Percent. TAXA Mean Max. (%) Mean Max. (%) Mean Max. (%) Mean Max. (%)

Estuarine copepods .07 1.1 7.43 .61 9.5 31.68 .03 .2 .21 .02 .2 .35 Neritic copepods .13 .8 11.35 .25 1.3 13.71 .02 .1 .11 .01 .2 .22 Estuarine isopods .11 .6 10.37 .07 .2 2.92 .01 <.1 .04 .01 .1 .12 Gastropod larvae (estuarine sp.) .27 1.3 25.88 .17 1.1 9.09 16.86 190.3 99.06 7.46 75.7 96.82 Gastropod larvae (others) .14 1.0 12.49 .38 3.4 19.86 .00 .0 .00 <.01 <.1 <.01 Bivalve larvae .08 .5 6.86 .27 2.0 14.23 <.01 <.1 .02 <.01 <.1 .04 Polychaete larvae .00 .0 .00 .00 .0 0.00 .04 .3 .25 .09 1.9 1.15 Barnacle larvae .02 .1 2.45 .02 .1 1.00 .01 .1 .06 .06 0.4 .79 Brachyurian larvae (zoea) .01 <.1 1.47 <.01 .1 .30 .02 .4 .15 .02 0.2 .24 Benthic foraminiferans .07 1.3 6.61 .04 .6 2.05 .00 .0 .00 .01 <.1 .01 Benthic ostracods .03 .1 2.69 .02 .1 1.00 .01 .1 .04 <.01 .1 .08 Benthic harpacticoids .08 .6 6.20 .05 .5 2.61 <.01 <.1 .01 <.01 <.1 .02 Mites .03 .2 2.61 .01 .1 .70 <.01 <.1 .01 .00 .0 .00 Others .03 .2 3.59 .01 .1 .83 .01 .1 .04 .01 .1 .16

TIDAL EFFECTS ON ESTUARINE ZOOPLANKTON 177 RESULTS which occurred around seven and a half hours after high water. The flooding period was shorter than the Hydrodynamic features ebb, and the step from maximum flood to maximum ebb occurred in less than three hours, with only a At spring tides (Fig. 2), tidal amplitude ranged brief period of slack currents around high water. The from 3.13 m (12 August) to 2.94 m (13 August), and main differences between surface and bottom cur- the deep-channel water depth at low tide was rent velocities occurred during ebb at the inner sta- approximately 3.25 m at station B and 1.25 m at station (G), and was lower at near-bed velocity. tion G. The water column appeared homogenous During neap tides (Fig. 3), tidal amplitude was most of the time, although a weak stratification between 1.48 m (18 August) and 1.39 m (19 developed in both stations at low water. Salinity August), but depths at low water were similar to above 35‰ was found in both stations at high water, those measured during spring tides (3.5 m at station while values fell to 29-25‰ at station B and to 25- B and 1.5 at station G). Salinity stratification was 22‰ at station G at low water. Current-speed mea- notable at both stations, being maximal around the surements showed that a sudden rise followed by a low tide slack. Surface salinity ranged between more gradual decrease of the ebb-tide velocity 24‰ and 33‰ at the outer station, and between occurred after the high tide slack, and an extended 18‰ and 30‰ at the inner station. Bottom salinity period of slow currents began before low water, was of 30-34‰ and 24-32‰ at the outer and inner

FIG. 4. – Time series of neritic copepods, gastropod larvae (excluded a estuarine species) and bivalve larvae occurrence during spring tides at B and G sites of the estuary of Mundaka. Circles: time series on 12 August 1991. Squares: time series on 13 August 1991. Open symbols: surface data, filled symbols: bottom data, semi-filled symbols: mid-depth data.

178 F. VILLATE stations respectively. Flood and ebb times were Both flood and ebb currents were always similar, but the velocity structure in the water col- stronger at the outer station. During the neap tide, umn, and the salinity vertical pattern differed maximal current velocities were around three times between flood and ebb tides. Higher flood currents smaller than those of spring tides at the surface, and in surface and near-bed occurred in a short period at four to five times smaller near the bottom. the middle flood, when the water column showed a greater saline homogeneity at the same time. As the Zooplankton composition and abundance tide fell, downstream currents were only evident at the surface, where salinity decreased more drasti- As shown in Table I, gastropod larvae, holoplank- cally. Near-bed salinity also decreased at the inner tonic estuarine and neritic copepods, bivalve larvae and station, but the highest saline waters (33-34‰) estuarine isopods were the most abundant taxa in sam- remained in depth at the outer station until low ples taken at the spring tide series. Among gastropod water. Salinity also differed in sampled sites from larvae one species inhabiting brackish waters (estuar- the first day to the next. Waters of 34‰ and 31‰ ine species) was distinguished from species with high reached in depth the outer and the inner stations salinity preferences. These estuarine larvae probably respectively the first day, but the next day the high- belong to the mud snail Hydrobia ulvae, which is very er salinities recorded were around 33‰ and 30‰ abundant in the intertidal sediments of the estuary of respectively. Mundaka, although we found that the planktonic phase

FIG. 5. – Time series of estuarine isopods, estuarine copepods and estuarine gastropod larvae occurrence during spring tides at B and G sites of the estuary of Mundaka. Circles: time series on 12 August 1991. Squares: time series on 13 August 1991. Open symbols: surface data, filled symbols: bottom data, semi-filled symbols: mid-depth data.

TIDAL EFFECTS ON ESTUARINE ZOOPLANKTON 179 time of these larvae was at least two weeks (Villate et representative species. Isopods were mainly of the al., 1993) while the planktonic larval phase reported estuarine species Paragnathia formica. Benthic cope- from other locations is very short (e.g., Armonies and pods (mainly harpacticoids), foraminiferans and ostra- Hartke, 1995). Endemic copepods (grouped in the cods, and mites were also found in zooplankton sam- estuarine copepod category) were dominated by Acar- ples taken during spring tides. tia bifilosa. Low densities of Acartia grani, and some Gastropod larvae of the estuarine species domi- individuals of Calanipeda aquae-dulcis were also nated zooplankton largely in the middle estuary at found. Among neritic copepods, Paracalanus parvus, neap tides. A maximal density of 190 ind l-1 was Oncaea media and Euterpina acutifrons were the more recorded from a sample taken on August 18. These

FIG. 6. – Time series of benthic foraminiferans, benthic copepods, benthic ostracods and mites occurrence during spring tides at B and G sites of the estuary of Mundaka. Circles: time series on 12 August 1991. Squares: time series on 13 August 1991. Open symbols: surface data, filled symbols: bottom data, semi-filled symbols: mid-depth data.

180 F. VILLATE high densities of gastropod larvae constituted more Zooplankton dynamics throughout the high-low than 95% of the total zooplankton sampled in both water cycles neap-tide series. Polychaete, barnacle and brachyuran larvae, and holoplanktonic estuarine and neritic Spring tides copepods were abundant in some samples, but their contribution to the total zooplankton was very small. Taxa of neritic origin showed higher densities The occurrence and contribution of benthic forms, around high water, and were almost absent at low however, was negligible. Copepod species composi- water at both stations (Fig. 4). Their maximal tion did not differ from that observed at spring tides: densities, however, were found moving upstream A. bifilosa dominated in the autochthonous assem- across the outer station at flood-tide, just after blage and P. parvus, O. media and E. acutifrons in the sudden flood rise occurred and waters above the neritic assemblage. 35‰ reached the middle estuary. They moved The densities of estuarine larvae of gastropods upstream across the outer station mainly in the polychaetes barnacles and brachyurans increased surface on August 12, but mainly at depth on from the spring to the neap tide period, while the August 13. densities of estuarine copepods and isopods, and Among autochthonous taxa (Fig. 5), the highest neritic populations decreased. abundance of estuarine isopods (P. formica)

FIG. 7. – Time series of neritic copepods, barnacle larvae and brachyuran larvae occurrence during neap tides at B and G sites of the estuary of Mundaka. Circles: time series on 18 August 1991. Squares: time series on 19 August 1991. Open symbols: surface data, filled symbols: bottom data, semi-filled symbols: mid-depth data.

TIDAL EFFECTS ON ESTUARINE ZOOPLANKTON 181 appeared around low water at the outer station, but cycle. They moved downstream and upstream at only occurred occasionally at this station around the middle ebb and flood respectively, but their high water. At the inner station they were found higher densities skewed towards higher salinity over all tidal phases, although the highest densities waters. in the water column were observed around low Among the tychoplankton (Fig. 6), organisms water. On August 12, the highest densities of A. inoculated periodically into the plankton by bot- bifilosa were recorded at the outer station moving tom currents (Kennish, 1990), the density of ben- downstream at the middle ebb, in waters of 31- thic foraminiferans in the water column differed 32‰, but this peak was not found moving greathy between the outflow and the inflow peri- upstream at flood. The next day, however, the ods. They peaked mainly in the water column highest densities were only recorded moving coinciding with the stronger flood currents, and upstream at the first flooding period, in waters of moved upstream in waters above 35‰. In con- 29-30‰. Although maximal abundance observed trast, benthic harpacticoids appeared in similar at the inner station was always lower, we can sup- numbers at ebb and flood phases, but ebb and pose that the population patch moved across this flood peaks occurred at different current veloci- station during unsampled flood and ebb times. The ties, and in waters of different salinity. At ebb, gastropod larvae of the estuarine species showed a harpacticoids peaked in waters of 31-32‰, and similar variation pattern in relation to the tidal after maximal currents occurred. At flood, how-

FIG. 8. – Time series of polychaete larvae, estuarine gastropod larvae and estuarine copepods occurrence during neap tides at B and G sites of the estuary of Mundaka. Circles: time series on 18 August 1991. Squares: time series on 19 August 1991. Open symbols: surface data, filled symbols: bottom data, semi-filled symbols: mid-depth data.

182 F. VILLATE ever, they peaked in waters around 35‰ during peaked during high water at the outer station, but the maximum flooding current. Benthic ostracods on August 18 their abundance also increased dur- showed an occurrence pattern similar to that of ing low water at this site. The brachyuran larvae harpacticoids. However, the higher densities of were mainly found at high water and the first half ostracods were recorded at mid depth while the of the ebb. All these groups only appeared spo- higher densities of foraminiferans and harpacti- radically at the inner station. coids appeared at the bottom. Mites were more The higher densities of polychaete larvae, gas- abundant in surface and mid depth around high tropod larvae and autochthonous copepods (Fig. 8) water at the inner station, and just after the high occurred at the outer site around high tide or in the water slack at the outer station. late flood period, just following a sudden rise of the flood-tide velocity and a decrease of the saline Neap tides heterogeneity in the water column. Over the ebb tide they remained at this site in greater abundance As shown in Fig. 7, neritic copepods only than that found in the early flood. Polychaete and occurred in noticeable numbers at high water in gastropod larvae decreased more drastically than the outer station. At this site they were present estuarine copepods toward the inner station, where longer during ebb, and in waters of higher salini- their temporal trends in relation to the tidal cycle ty remained near the bottom. Barnacle larvae also were not so clear.

FIG. 9. – Abundance of neritic copepods, gastropod larvae (excluded a estuarine species) and bivalve larvae vs. salinity during spring FIG. 10. – Abundance of estuarine isopods, estuarine copepods and tides in the estuary of Mundaka, showing the calculated salinity for estuarine gastropod larvae vs. salinity during spring tides in the the mean value of abundance distributions in days 12 (open sym- estuary of Mundaka, showing the calculated salinity for the mean bols) and 13 (filled symbols), and at flood (circles) and ebb value of abundance distributions in days 12 (open symbols) and 13 (squares) phases. (filled symbols), and at flood (circles) and ebb (squares) phases.

TIDAL EFFECTS ON ESTUARINE ZOOPLANKTON 183 Variations in relation to water masses towards higher salinity at the ebb phase, but did not show clear variations among tidal cycles. By Spring tides contrast, the population of estuarine gastropods skewed towards higher salinity from the first to The distribution of neritic populations in rela- the second tidal cycle, and from ebb to flood tion to salinity (Fig. 9) did not show clear varia- phases. Among tychoplanktonic groups (Fig. 11), tions among tidal cycles, or among tidal phases. foraminiferans, harpacticoids and mites distrib- As shown in Fig. 10, the distribution of estuarine uted in general towards higher salinity during the isopods and copepods appeared more skewed second tidal cycle, while ostracod distributions in relation to salinity remained similar among tidal cycles. On the other hand, harpacticoids and ostracods appeared clearly associated with higher salinity during the flood phase, while mites were found in higher salinity waters at ebb.

FIG. 11. – Abundance of benthic foraminiferans, benthic copepods, FIG. 12. – Abundance of barnacle larvae, estuarine copepods and benthic ostracods and mites vs. salinity during spring tides in the gastropod larvae vs. salinity during neap tides in the estuary of estuary of Mundaka, showing the calculated salinity for the mean Mundaka, showing the calculated salinity for the mean value of value of abundance distributions in days 12 (open symbols) and 13 abundance distributions in days 18 (open symbols) and 19 (filled (filled symbols), and at flood (circles) and ebb (squares) phases. symbols), and at flood (circles) and ebb (squares) phases.

184 F. VILLATE optimal salinity range (above 34‰ for neritic populations) during neap tides prevents suitable compar- isons.

DISCUSSION

According to data obtained here, hydrological and biotic pictures change drastically within the estuary of Mundaka on a weekly basis as a result of spring-neap cycles. The observed shift from a stratified state at neap tides to a mixed state at spring tides is a frequently reported feature of tidal estuaries (e.g. MacKay and Schuman, 1990; Vale and Sundby, 1987), and is accounted for by a rapid decrease of the vertical gravitational circulation towards spring tides (Dyer et al., 1992). Velocity structure appears influenced by tidal asymmetry at spring tides. Both flood and ebb currents reach maximum values in the entire water column shortly before and after high tide. Slow downstream velocities before low water are shortly followed by high upstream velocities just after low water. During neap tides, however, the main differences in the velocity structure between flood and ebb tides seems to be influenced by vertical density gradient effects caused by salinity. Dur- ing ebb, the evidence of noticeable downstream cur- FIG. 13. – Abundance of neritic copepods, polychaete larvae and rents only at the surface, and the maintenance (either brachyuran larvae vs. salinity during neap tides in the estuary of Mundaka, showing the calculated salinity for the mean value of increase during the early ebb) of salinity at the bot- abundance distributions in days 18 (open symbols) and 19 (filled tom, suggests the existence of upstream slow resid- symbols), and at flood (circles) and ebb (squares) phases. ual currents at depth, at least at the outer site. In fact, the stratification is an essential requirement for pro- ducing gravitational circulation and two-way circu- Neap tides lation (Uncles and Stephens, 1990). In contrast, rising tides produce a short acceleration both in surface The abundance distributions of barnacle larvae, and near-bed velocities at the mid flood, resulting in estuarine copepods and estuarine gastropod larvae a brief vertical mixing of the water column. skewed towards higher salinity at ebb, and from the Under the stationary conditions of low river dis- first to the second tidal cycle (Fig. 12). By contrast, charge analysed, at spring tides, offshore water neritic copepods, polychaete larvae and brachyuran (salinity > 35‰) fills the outer and middle regions, larvae did not show clear trends among tidal phases, reaching the inner estuary at high water. The fol- but their abundance distributions skewed towards lowing salinity fall (below 29‰) at low water in the lower salinity from the first to the second tidal cycle middle estuary suggests that seawater located in the (Fig. 13). estuary mouth moves along at least two thirds of the In comparison with spring tide distributions, estuary length during the spring tidal excursion. estuarine populations moved towards more saline Because of this, neritic zooplankton penetrate waters from spring to neap tides, especially in cope- beyond the middle estuary with flooding waters, pods. Although the calculated salinity for the mean while estuarine populations are confined to the value of abundance in neritic copepods was clearly upper reaches at high water and transported sea- lower at neap tides, this cannot be used to obtain wards by ebb tides to reach the outer estuary at low conclusions. The lack of data on copepods at their water. The vertical mixing and sequential displace-

TIDAL EFFECTS ON ESTUARINE ZOOPLANKTON 185 ment of mixohaline water bodies over the entire ing spring tides in the microzooplancton fraction water column prevent the success of a behavioural while larger individuals peak during neap tides in vertical migration to enable the estuarine popula- the mesozooplankton fraction (Villate et al. 1993). tions to maintain their location, as has been reported Settlement around neap tides agrees with models in larger estuaries with a two-way circulation pattern that predict that little settlement will occur during (e.g. Wooldridge and Erasmus, 1980). In spite of periods of stronger flow (Gross et al., 1992). Reten- this, results indicate that under low river discharge tion of these larvae prior to settlement could be conditions the net seaward transport of estuarine favored by vertical active migration in the highly populations during spring tides seems slow (estuar- stratified water column that develops at neap tides in ine gastropod larvae apparently moved toward high- the middle estuary. In this study, the highest densi- er salinity waters from one day to the next) or negli- ties of gastropod larvae entering the middle estuary gible (estuarine copepods did not show clear varia- with the rising tide appeared at middle depth, while tion in relation to salinity during consecutive days). the higher densities were found deeper as the tide However, taking into account that outgoing water fell. This suggests that larvae might concentrate at displaces estuarine populations to the outer estuary, the bottom to mitigate seaward transport because of their maintenance could become critical when river- the upward flow of water in deeper zones. Larval ine discharges increase. In deeper estuarine systems, retention due to the interaction between residual cur- population abundance can be unaffected by dis- rents and vertical distribution of larvae is one of the charges by migrating from the seaward surface cur- more frequently observed larval transport patterns in rent to the deep landward compensation current estuaries (Lagadeuc, 1992), where the interaction of (Kaartvedt and Nordby, 1992; Kaartvedt and Svend- larval transport processes with larval behavior is sen, 1995). In the shallow estuary of Mundaka the better understood in general terms (Le Fèvre and coupled effect of strong river inflows and spring Bourget, 1992). On the other hand, the clear avoid- tides could bring estuarine populations out of the ance of the surface layer by larval groups at neap estuary. tides and their more homogenous distribution in the At neap tides, waters above 35‰ do not reach water column at spring tides corroborate that the the middle estuary even at high tide. As a result, vertical distribution of larvae is a function of verti- estuarine populations remain around the low middle cal migration, which results in concentration of lar- part of the estuary, while the penetration of neritic vae at top or bottom layers, and turbulence, which forms is very poor. A previous recording (Villate, tends to produce vertically uniform concentrations 1991) on zooplankton in the outer and middle zones (Smith and Stoner, 1993). In this sense, the skewed of this estuary, conducted at high tides, showed that distribution of estuarine populations (both copepods seasonal changes in neritic populations within the and gastropod larvae) towards higher salinity at estuary did not agree at all with their seasonal neap tides, if compared with spring tides, is account- dynamics in neritic waters, but were related to vari- ed for by a stronger aggregation in depth within the ations in tidal amplitude. The differences in the highly stratified water column rather than for a net abundance of estuarine populations between spring seaward displacement along the estuary. and neap tides can be linked in part to behavioural Tychoplankton were only abundant during spring responses to spring-neap cycles. Although an tides. Although the behavioural responses of organ- enhancement of copepod populations under strati- isms are implied, the occurrence of benthic forms in fied conditions is suggested in coastal marine sys- the water column of the estuary of Mundaka appears tems (Sullivan, 1993), the tides regulated stratifica- modulated mainly by spring-neap variations and tion in estuarine systems should have different velocity asymmetries in the tidal currents, in the effects since autochthonous copepods (mainly A. same way that is described for total suspended solid bifilosa) clearly decreased from the well-mixed con- concentrations in other tidal systems (Leonard et al., ditions at spring tides to the highly stratified condi- 1995). If under natural conditions particle suspen- tions at neap tides. In the estuary of Mundaka, short sion starts at current velocities of about 10 cm s-1 term changes in the A. bifilosa population have not (Jonge and Bergs, 1987), this would account for the been related to tidal rhythms. Conversely the scarcity of benthic forms at neap tides. The quanti- release, development and settlement of gastropod tative importance of tychoplankton at spring tides is larvae seem to follow a semilunar rhythmicity: evidenced by the high density of benthic organisms smaller individuals are found in larger number dur- recorded at flood and ebb tide, which sometimes

186 F. VILLATE was similar to that of true planktonic forms. This required to evaluate the overall significance of the corroborates the finding observed in other shallow tidal suspension on meiofauna in our study area. systems where meiobenthos is found to contribute The higher abundance of mites around the high largely to the mesozooplankton biomass over the water slack permits us to suppose that these organ- entire tidal cycle (Armonies, 1989), and indicates isms are mainly flushed to the estuary channel when that the cyclic inputs of meiofauna into the water water overflows upper intertidal areas and salt- column might be relevant in the diet patterns of marshes of the estuary shores. Mites are mainly dis- pelagic planktophages and filter feeding benthic tributed in the littoral zone, where some supralit- populations. toral-terrestrial invader forms are found together The occurrence patterns of benthic forms in rela- with mites from the phytal meiofaunal communities tion to the tidal currents, however, differed among (Somerfiel and Jeal, 1995). taxa and denoted differences between passive and In conclusion, results show that tidal hydrody- actively swimming organisms. The significant high- namism has strong effects on the composition and er densities of benthic foraminiferans, which were zonation of permanently and temporarily resident accompanied by high amounts of sand, during the organisms in the pelagic habitat of the estuary of rising tide suggest a net upward transport of these Mundaka. That, in combination with river dis- biotic and abiotic materials within the estuary of charge, will have implications in the regulation of Mundaka. In fact, low river flow spring tide periods planktonic and benthic populations by translocation can lead to upstream storage of materials under tidal of individuals from one part to another within the asymmetric conditions (Burton et al., 1995), and estuary, or even outside the estuary. benthic foraminiferal tests are used to state the net transport of sands within tidal systems (Gao and Collins, 1995). ACKNOWLEDGEMENTS Moving forms such as benthic harpacticoids and ostracods not only peaked at maximal flood but also This study has been supported financially by the at the mid-ebb, after strongest downstream currents University of the Basque Country (UPV 118.310- occurred. In addition, these peaks were associated E054/90). Many thanks to Astilleros de Murueta with waters of different salinity at flood and ebb S.L. for providing a place for field work. periods, denoting behavioural responses associated with tides. 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188 F. VILLATE