Plankton responses to hydrological changes induced by Freshets in a shallow mesotidal estuary

Estuarine, Coastal and Shelf Science (1992) 35,425-434

Plankton Responses to Hydrological Changes Induced by Freshets in a Shallow Mesotidal Estuary

I. de M a d a r i a g a , L. G o n z ~ i l e z - A z p i r i , F. V i l l a t e a n d E. O r i v e Ekologi Laborategia, Landare-Biologia eta Ekologia Saila, Zientzi Fakultatea, Euskal Herriko Unibertsitatea, 644 P.K. E-48080 Bilbao, Spain Received 30 September 1991 and in revisedform 6 March 1992

Keywords: plankton dynamics; hydrography; freshets; natural perturbations; Gernika estuary Daily variations in the plankton community of the Gernika estuary (Bay of Biscay) were studied over three week-long periods in order to evaluate the effects of large increases in river runoff due to intense rain pulses. Both tidal and river inflow changes determined the hydrological zonation within the estuary during the study periods. Chlorophyll a appeared to be related to riverine inputs and resuspension processes rather than to phytoplankton growth dynamics. The spatio-temporal distributions of plankton assemblages were related to hydrological conditions. Thus, a successional progression involving short-term interactions among plankton populations was severely affected by increased river discharge. Freshets removed neritic populations and returned the plankton community to an initial state. As hydrological conditions became more marine, the progression towards a community with metazoan predominance was paralleled with a rise in neritic plankton abundance further up the estuary. The development of estuarine populations, which can reach high densities under stable conditions, seemed to be limited by frequent river runoff disturbances occurring in this estuarine system.

Introduction Plankton communities are exposed to a variety of scales of spatial and temporal variability in their natural habitats, but the role of short-term processes in plankton ecology has traditionally received little attention (Harris, 1980). Recent studies have pointed out that the understanding of the role of short-term changes in environmental conditions is essential to characterize planktonic processes in any coastal ecosystem (Sinclair et al., 1981; C6te & Platt, 1983; Cloern & Nichols, 1985; Sournia et al., 1987; Litaker et al., 1987; Lindahl & Perissinotto, 1987). In particular, shallow estuaries are subjected to a high variability on a time scale of days depending on freshwater inflow (freshets), tides (neap/ spring), wind (storms), and other episodic events (Cloern & Nichols, 1985). Many of these natural perturbations are unpredictable and lead to pronounced gradients in the environmental habitat properties of a given estuary, and therefore influence the composition and dynamics of estuarine plankton communities. 0272-7714/92/100425 + 10 $03.00/0

© 1992AcademicPress Limited

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T h e Basque Country is characterized by a large n u m b e r of small mesotidal estuaries along its coast. T h r o u g h o u t most of the year irregular atmospheric low-pressure systems move over this area. T h e y cause intense rain pulses that increase down-stream runoff and drastically alter estuarine conditions and biota. T h e aim of this study was to investigate the estuarine plankton responses to freshwater pulses in the Gernika estuary. T h e effects of these phenomena on phyto- and zooplankton population dynamics on a day-to-day temporal scale were determined. Material and methods T h i s research was carried out in the Gernika estuary (also called Mundaka estuary), a shallow mesotidal estuary located in Biscay (43°22'N 2°40'W), N o r t h Spain (Figure 1). It extends approximately 12.5 km from its entrance to an artificial channelreaching Gernika, normally the upper limit of tidal influence. T h e mean depth and m a x i m u m tidal range in the mouth are about 3-0 m and 3.2 m, respectively. It is bordered by relatively extensive tidal flats along its lower part and by salt-marshes in its middle part. D u e to its geomorphology, this estuarine system can vary considerably in its volume and flushing rates, which affects strongly its biological and chemical properties (Madariaga & Ruiz, 1988; Madariaga & Orive, 1989; Madariaga et al., 1989). Daily surveys were conducted from 29 October to 3 N o v e m b e r 1987 in autumn, from 25 to 30 January 1988 in winter, and from 22 to 28 April 1988 in spring. T h r e e permanent sampling sites were located in the central channel along a longitudinal transect from near the m o u t h of the estuary to its confluence with the artificial channel (Figure 1). Water samples were always collected at high tide in the morning with a 71 opaque Van D o r n bottle from 0.5 m below the surface and also 0-5 m above the bottom (only subsurface samples are considered in this study as bottom samples only reflected sediment resuspension processes). Vertical temperature profiles were determined using a thermistor. Salinity was measured with a Beckman induction salinometer and oxygen by the Winkler titration method. Samples for nutrient analyses and for total photosynthetic pigment determinations were subsequently filtered through glass-fibre filters (Whatman GF/C). Filters were homogenized and extracted for 24 h in 90% acetone and absorbances were measured with a Shidmazu UV-24 spectrophotometer. Chlorophyll a concentrations were calculated using the tri-chromatic equations of Strickland and Parsons (1972). Prefiltered samples for nutrient analyses were kept frozen and dark for a m a x i m u m period of 10 days. All analyses were made according to the methods described in Strickland and Parsons (1972) and Parsons et al. (1984). T h i r t y litre water volumes were taken at the surface and filtered through 45 g m nylon filters to retain zooplankton organisms. T h e s e samples were preserved in 5 % formalin and examined under a stereoscopic microscope. Phytoplankton samples were preserved in Lugol's iodine solution, and later identified and counted under an inverted microscope (Utermh61, 1958). A principal component analysis (PCA) was performed upon raw data using the hydrographical parameters in order to identify the main trends in sample variability. Results Environmental conditions during the study periods are shown in Figure 2. I n all cases, intense and irregular rain pulses immediately altered river inflow rates. Strong winds also

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[Figure 3(a)]. Strong salinity and nutrient gradients were observed when river discharge increased after rain pulses. Riverine waters were characterized by higher nutrient levels and lower temperature than in the neritic waters. Chlorophyll a patterns differed spatially between surveys [Figure 3(b)]. Different maxima were associated either with low salinities in the upper estuary after a rain pulse, or with increases in salinity in the lower reaches, coinciding with lower river runoffand a rise in tidal amplitude. In general, chlorophyll a concentrations were always higher at the upper site and ranged between 0.2-3.5 ~tg 1-1. Changes in plankton densities are shown in Figure 3(c-d), for total phytoplankton and total zooplankton respectively. Temporal rather than spatial variations appeared to be more important in all cases and are clearly dependent on riverine perturbations. T h e same

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TABLE 1. Correlation coefficients (loads) of the hydrographical parameters with the principal componentof the analysis Autumn Salinity Temperature pH Alkalinity Oxygen Phosphate Nitrite Silicate Ammonium Nitrate Variance

Winter -0.95 - 0-87 -0.75 -0.10 + 0'54 +0.88 +0-92 +0-93 +0.94 +0.97 56-06%

Oxygen -0.87 Salinity - 0.80 Temperature-0.78 pH - 0.76 Alkalinity - 0 - 2 9 Nitrate +0.24 Ammonium +0.27 Nitrite +0-67 Silicate +0-77 P h o s p h a t e +0-97 49-50%

Spring Salinity -0-99 pH - 0.92 Temperature--0.67 Oxygen - 0-53 Alkalinity -- 0.26 Nitrite +0.93 Ammonium +0-93 P h o s p h a t e +0.95 Silicate +0.97 Nitrate +0-98 65.07%

effect was observed for phytoplankton specific composition (Figure 4). In autumn, the phytoplankton community was dominated by neritic diatoms (mainly Leptocylindrus danicus Cleve), and, to a lesser extent, by large dinoflagellates of the genus Ceratium. In contrast, winter phytoplankton was almost exclusively represented by small flagellates (mainly crytophyceans) and benthic forms, whereas in spring a diverse contingent of neritic species (dominated by Nitzschia seriata Cleve) were the most abundant taxa in the lower reaches of the estuary. Unfortunately, both in winter and spring surveys, high proportions of detritus were found in some samples of the upper reach after high river discharges, thus preventing reliable identification and counting of phytoplankton. Zooplankton was grotlped in five different functional groups: protozoans, copepod nauplii, holoplankton (other than previous groups), meroplankton, and semiplankton (sensu Armonies, 1989) (Figure 5). Copepod nauplii generally showed the highest relative contribution to the total zooplankton density, but when salinities decreased due to increased river runoff, postnaupliar individuals of the meiobenthic harpacticoids (representing more than 90% of semiplankton) were more abundant in the upper reaches. Among them, Tachidius discipes Giesbrecht dominated in autumn and winter, and Paronychocamptus nanus Sars in spring. When freshets occurred, the protozoan component was also important; this group was dominated by tintinnids of the genus Stenosemella in winter and spring, and by Propectella sp in autumn. Postnaupliar copepods (mainly Oithona nana Giesbrecht in autumn, Oithona helgolandica Claus in winter, and Acartia clausi Giesbrecht in spring) accounted for more than 90% of total holoplankton abundance, and reached highest densities under marine conditions. Meroplankton, strongly dominated by gastropod and polychaete larvae, was more abundant in winter and spring than in autumn, but no clear spatial or temporal trends were observed for this group in any of the surveys.

Discussion T h e Gernika estuary is characterized by a high spatial and temporal variability under unstable atmospheric situations, mainly due to its exposure and geomorphology (Madariaga & Orive, 1989). Rain pulses immediately generate strong variations in river runoff, which determine the salinity structure. Changes in nutrient loading and temperature are also clearly dependent on river inflow. T h e conservative behaviour of all nutrients

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on this short time scale is a common feature in estuaries (Morris, 1981), especially when flushing rates are high relative to the slow uptake rates of phytoplankton. Chlorophyll a distribution patterns during the study periods were also related to this phenomenon. Chlorophyll a maxima in the upper estuary were associated with the riverine waters. Similar results were found by Litaker et al. (1987) for the N e w p o r t River estuary and S chuchardt and S chirmer (1991) for the Weser and Elbe estuaries. However, in the lower part, where tidal flats are extensive and the wind effect is higher, sediment resuspension could have been an important mechanism providing the water column with considerable amounts of chlorophyll (Lukatelich & M c C o m b , 1986; Jonge & Bergs, 1987; Riaux-Gobin, 1987). No apparent relationship was found between chlorophyll a distributions and phytoplankton growth dynamics during the study periods. Freshets not only control the circulation of water masses and their hydrographic properties, but also modify the structure and zonation of plankton populations. Increased river discharge removed neritic populations from the upper estuary and created clear gradients in plankton abundance. When freshwater inflow diminished, seawater intruded gradually further up the estuary, and marine plankton populations reached their maxim u m ; the occurrence of a subsequent freshwater pulse reverted the situation to the initial state. T h u s , the advective transport from adiacent coastal waters seems to be a primary

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mechanism by which plankton density increases in the estuary (Malone et al., 1980; Revelante & Gilrnartin, 1987). This result agrees with the hypothesis that the distribution of plankton in estuaries is strongly correlated with an hydrologically established scheme (Taw & Ritz, 1978), and it might be predictable knowing the dispersal patterns of the inflows and the inflow rates (Hayward & Avyle, 1986). During the study periods, the zooplankton community was almost entirely formed by neritic assemblages and a semiplanktonic component dominated by meiobenthic organisms. Riverine plankton, which is frequently flushed into mixing waters under conditions of high river flow (Roper et a l . , 1983), was not detected, and estuarine holoplankton was negligible. T h e negative influence of turbulent water movement, coupled with tidal exchange on the establishment and maintenance of estuarine populations (Bakker & De Pauw, 1975), could account for the scarcity of this assemblage in the Gernika estuary during periods of hydrological instability, since high densities of estuarine species have been found previously in this system (Villate, 1991). In contrast, semiplankton can reach high densities in the upper reach of the estuary, although they occur irregularly (Villate, 1984). T h e unpredictability of semiplankton occurrence is due to the complexity of the mechanisms governing the presence of meiobenthic organisms in the water column. Small benthic animals such as harpacticoid

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copepods, ostracods, and amphipods, commonly emerge to short distances above the bottom (Alldredge & King, 1985), but the occasional occupation of the entire water column by large numbers of a meiobenthic copepod involves specific behavioural responses related to population dynamics (Service & Bell, 1987). Although the spatio-temporal variations of different plankton assemblages generally reflected hydrological conditions, temporal variations in the community structure within assemblages cannot be directly related to these physico-chemical changes. Short-term variations in the plankton species composition were consistently observed throughout the surveys as a consequence of the rapid interaction and replacement of diverse taxa in the time. Thus, after a freshwater pulse occurred, phytoplankton was dominated by small flagellates and benthic forms, and tintinnid density increased. As discussed above, an important community of meiobenthic harpacticoids also emerged in the water column at the upper reaches. When conditions became more marine, diatom-dominated phytoplankton grew, tintinnids were replaced by metazoan holoplankters and meiobenthic harpacticoids gradually disappeared. Finally, as zooplankton metazoans reached their maximum, diatom number decreased but large phytoplankton, represented mainly by the dinoflagellate Ceratium sp., became more important. T h e recurrence of these results illustrates a successional pattern in the plankton community of the Gernika estuary, as it involves the progression from an initial community dominated by protozoans to a community dominated by crustaceans, coupled with an increase in the size-structure towards bigger organisms (Witek, 1986; Legendre et al., 1987). Similar successional stages in the development of plankton communities were defined by Vinogradov and Shushkina (1984). This pattern was affected by the river discharge and water residence time, the main factors that controlled the composition and growth dynamics of plankton communities in the Gernika estuary during the study periods.

Acknowledgements We would like to thank two anonymous referees for their helpful comments on earlier versions of this paper. This work was partially financed by a grant from the Department of Education, Universities and Investigation of the Basque Government.

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