Multiscale in Situ Measurements of Intertidal Benthic Production and Respiration
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1 6 Multiscale in Situ Measurements of Intertidal Benthic Production and Respiration Dominique Davoult, Aline Migné, and Nicolas Spilmont CONTENTS 6.1 Introduction Materials and Methods Results In Situ Measurements and Estimation of Daily Potential Primary Production Seasonal Variations of Primary Production and Respiration Temporal Resolution of Measurements and Microscale Adaptation of Microphytobenthos to Variations in Irradiance Mesoscale Variations within the Gradient of Exposure Microscale Variability Conclusion and Perspectives Aknowledgments References Introduction Although phytoplankton are considered to be responsible for the major part of marine primary production, both macrophytobenthos and microphytobenthos can play an important role in coastal ecosystems. 1,2 Microphytobenthos can provide as much as two thirds of total primary production in some estuaries 3 and macroalgae as much as three quarters of total primary production in some bays 4. Such estimations need direct (in situ monitoring of changes in CO 2 or O 2 ) or indirect (modelling or laboratory incubations under artificial irradiance conditions) measurements of gross primary production and the knowledge of both temporal and spatial variablity of the studied system. Temporal variations can act at mesoscale (interannual and seasonal variations), small scale (e.g., meteorological or spring tides/neap tides variations) and microscale (e.g., tidal cycle or irradiance variations) and so can spatial variations (salinity gradient, granulometric heterogeneity such as variations in silt content, water retention, duration of emersion, etc.). Our purpose was to use an in situ method for measuring net primary production and respiration, as opposed to experimental indirect methods 5-7 which are unable to estimate short time and space variations of these processes. The aim of this study was to accurately evaluate both trends and variability in primary production and respiration of sandy and muddy intertidal estuarine or marine flats in the eastern English Channel. Differences were expected along a gradient of exposure (characterized by the amount of mud within the sediment), particularly between exposed sandy beaches and sheltered estuarine mud flats. A closed-chamber method was used, based on CO 2 concentration measurements performed with an Infrared gas analyser /4/$.+$ by CRC Press LLC
2 98 Handbook of Scaling Methods in Aquatic Ecology: Measurements, Analysis, Simulation A B FIGURE 6.1 (A) The whole system during a light incubation in the Seine estuary. (B) Portable container with circuit of CO 2 analysis (a pump, a drying column, an infrared gas analyser) and data logger. In this study, spatial variability was considered from the elementary surface of measurement of the closed chamber (.126 m 2 ) to the comparison between several intertidal systems (an exposed sandy beach typical of the conditions in the eastern English Channel and two estuarine flats) and temporal variability was considered from the frequency of data logging (every 3 s for CO 2 concentration) to the annual scale for carbon budget estimation. All measurements were made under emersed conditions as it was assumed that no primary production occurred during immersion because of strong light limitation due to particulate suspended matter, particularly in estuaries 8,9 (up to 12 mg l -1 in the Somme estuary 1 ). 6.2 Materials and Methods The closed chamber used for CO 2 flux measurement at the air-sediment interface was constructed using a dome (16.75 l, 4 cm in diameter) of transparent (or opaque) Perspex fitted on a crown wheel of stainless steel, which is pushed into the substrate to a depth of 1 cm, enclosing a volume of l and a surface area of.126 m 2. A pump (Brailsford and Co., TD-2SA) maintained an air flow of about 2 l min -1 through the closed circuit. Variations of CO 2 concentration were measured with an infrared gas analyser (LiCor Li-6251) and PAR (Photosynthetically active radiations, 4 to 7 nm) inside the chamber was quantified with a quantum sensor (LiCor Li-192SA). Analyser data (internal temperature, CO 2 concentration) as well as environmental data (PAR, temperature in the enclosure) were stored on a data logger (LiCor Li-14). The logging frequency was 3 s for analyser data and 1 min for environmental data. The whole system of analysis was placed in a portable container (Figure 6.1). More details on calibration and conditions of measurements are given in Migné et al. 11. Experiments were carried out in ambient light and darkness to estimate community net primary production and respiration, respectively. Gross community production was calculated from net production corrected with respiration. One experiment consisted of a series of incubations under different conditions of irradiance during the day, from dawn to zenith or from zenith to twilight. One incubation occurred during 1 to 2 min according to the site and the season, depending on the rate of variation of CO 2 concentration within the chamber and on the duration of a stable (linear) signal to make consistent calculations of CO 2 fluxes. Respiration (dark incubation) was measured from 1 to 7 times per day to deal with variability of respiration during emersion. Measurements were performed during the year 2-21 on four stations located in three different sites along the french coast of the English Channel (Figure 6.2), chosen within a gradient from exposed to sheltered conditions: an exposed sandy beach at Wimereux ( 'N, 'E), a muddy-sand sediment (about 2 % mud in the sediment) at Le Crotoy (Somme estuary, 'N, 'E), a muddy-sand sediment (about 15 % mud in the sediment, 'N, 'E) and a sandy-mud sediment (about 5 % mud in the sediment, 'N, 'E) near Le Havre (Seine estuary).
3 Multiscale in Situ Measurements of Intertidal Benthic Production and Respiration 99 FIGURE 6.2 Location of the different sites of measurements. All sites were located in the zone of retention, between mean high water of neap tides and mean tide level and were then subject to flooding (3 hours per tidal cycle) twice a day. Measurements were made seasonally in the Seine estuary, monthly at Le Crotoy and Wimereux, with a higher frequency in this latter site during spring. Annual carbon production due to gross primary production was estimated at Le Crotoy, using four production-irradiance curves (February, April, July and October). An estimation was realized every day by taking into account a daily theoretical irradiance curve (see below in results), the combination of the times of sunrise, sunset and the duration of emersion, with a time step of 1 min. 6.3 Results In Situ Measurements and Estimation of Daily Potential Primary During each incubation, linear variations of CO 2 concentration (Figure 6.3) occurred after a period of stabilization (about 1 to 1 min) which was generally longer in dark incubations than in light ones. The slope of CO 2 concentration vs. time was calculated (least square regression) from the linear part of each recording: it changed as a function of irradiance and a series of incubations within one day allowed us to fit a production-irradiance (P-I) curve (Figure 6.4), according to the following equation: 12 P = P max [1 exp(-i/i k )] (6.1) where P = gross primary production (mgc m -2 h -1 ) ; P max = maximal gross primary production under saturating irradiance ; I = irradiance (µmol m -2 s -1 ) ; I k = onset of saturating irradiance (µmol m -2 s -1 ), determined as the point of inflection on the P-I curve CO 2 (ppm) :16 6:28 7:4 8:52 1:4 11:16 Universal Time FIGURE 6.3 Example of variations of CO2 concentration during successive light incubations under different irradiances from dawn to zenith; the last incubation is a dark one (Seine estuary, sandy mud, August 21).
4 1 Handbook of Scaling Methods in Aquatic Ecology: Measurements, Analysis, Simulation P (mgc m -2 h -1 ) I (µmol m -2 s -1 ) P=68.6 [1-exp(-I/199)] r 2 =.994 ; N=16 FIGURE 6.4 Example of gross production-irradiance curve fitted with results of field incubations presented in Figure 6.3. A daily potential gross primary production can then be estimated taking into account both the theoretical daily irradiance curve and the duration of emersion on the site. A theoretical daily irradiance curve can be calculated as a function of time: 13 I t = I max.sin(πt/dl) (6.2) where I t = irradiance at time t (µmol m -2 s -1 ); I max = maximal irradiance (µmol m -2 s -1 ) ; t = time (h) ; DL = day length (h). Two examples were given for February and July at Le Crotoy. In both cases, we chose two close dates with the highest difference in daily carbon production within the month. The P-I curve used in February was: P = 6.69[1 - exp(-i/12)] (r 2 =.959, n = 9). Calculations were made on February 6 and 16. The two daily irradiance curves were slightly different (from 7:16 to 16:55 U.T. on February 6, from 6:59 to 17:12 U.T. on February 16) but the period and the duration of emersion before the night were very different from one day to another (from 1:34 to 16:55 U.T. on February 6, from 6:59 to 15:56 U.T. on February 16), which led to a potential production 41.2% higher on February 16 (57.6 mgc m -2 ) than on February 6 (4.8 mgc m -2 ). This result indicated that not only the duration but also the timing of flooding (in the morning or at noon, for example) could be a major factor controlling daily gross primary production and so should be taken into account for budget estimation at longer timescales. The P-I curve used in July was: P = 97.71[1 - exp(-i/31)] (r 2 =.989, n = 12). Calculations were made on July 1 and 15. The two daily irradiance curves were very close (from 4: to 19:52 U.T. on July 1, from 4:5 to 19:48 U.T. on July 15) but the period and duration of emersion before the night were different from one day to another (from 4: to 12:23 U.T. and from 15:23 to 19:52 U.T. on July 1, from 6:47 to 16:19 U.T. and from 19:19 to 19:48 U.T. on July 15), which led to a potential production 18.5% higher on July 1 ( mgc m -2 ) than on July 15 th (938.1 mgc m -2 ). The lower relative difference observed in July is mainly due to the longer duration of the day but the absolute difference is higher in July (173.1 mgc m -2 ) than in February (16.8 mgc m -2 ) and so summer variations may play a significant role in the estimation of the annual carbon production. We also calculated gross primary production, on the one hand using a theoretical irradiance curve, on the other hand using the actual irradiance data (Figure 6.5) during 3 h on February 16 and during 5 h on July 1. On February 16, calculations led to 19.9 mgc m -2 with the theoretical curve and 16.4 mgc m -2 with the actual data, that is 17.6% lower. On July 1, calculations led to mgc m -2 with the theoretical curve and mgc m -2 with the actual data, that is, 28.8% lower. The absolute difference (per hour) is of course higher in summer when production is higher than in winter, but the relative difference is also higher in summer. That may be explained by the higher value of I k in July (31 µmol m -2 s -1 instead of 12 µmol m -2 s -1 in February): actual data of irradiance stayed above I k in February even under a cloudy sky whereas irradiance recorded on July 1 stayed a long time below I k and led to a low primary production under unsaturating irradiance Seasonal Variations of Primary Production and Respiration No seasonal response seemed to clearly occur for gross primary production in the exposed sandy beach at Wimereux, certainly because of short-term instability of sediment which did not allow microphytobenthic
5 Multiscale in Situ Measurements of Intertidal Benthic Production and Respiration 11 A 2 Irradiance (µmol m -2 s -1 ) : 6:24 8:48 11:12 13:36 16: 18:24 Universal Time B 2 Irradiance (µmol m -2 s -1 ) : 6:24 8:48 11:12 13:36 16: 18:24 Universal Time FIGURE 6.5 Theoretical irradiance curve and actual data recorded on (A) February 16th and (B) july 1th in Le Crotoy (Somme estuary) mgc m -2 h R GPP FIGURE 6.6 Seasonal variations of respiration and maximal gross primary production in Le Crotoy (Somme estuary) as a function of days. resilience (chlorophyll a, or Chla concentration was very variable and always less than 5 mgchla m -2 ) and so continuous production. Gross primary production remained low and highly variable all along the year, always less than 16 mgc m -2 h -1 (generally less than 5 mgc m -2 h -1 ) as did respiration (always less than 7 mgc m -2 h -1 ). In the sheltered conditions of estuaries, both gross primary production and respiration remained higher and a seasonal trend in production and respiration could be observed. In Le Crotoy, for example, the community respiration showed a strong seasonal trend, varying from.5 mgc m -2 h -1 in December to 61.5 mgc m -2 h -1 in June (Figure 6.6). Variability of respiration remained low during the emersion, except in August when it varied with temperature (see standard deviations in Figure 6.6). A seasonal response was also observed for maximal gross primary production (Figure 6.6), with a minimum value in winter (1.1 mgc m -2 h -1 in November), a maximum value in spring (13.5 mgc m -2 h -1 in March), a decrease in spring down to 27.2 mgc m -2 h -1 in May, and a relative maximum value at the beginning of summer (122.8 mgc m -2 h -1 in July). This seasonal pattern looks almost identical to that of respiration, with the
6 12 Handbook of Scaling Methods in Aquatic Ecology: Measurements, Analysis, Simulation A P (mgc m -2 h -1 ) P = 73,4 [1-exp(-I/ 218)] r 2 =,988 ; N = I (µmol m -2 s -1 ) B P (mgc m -2 h -1 ) P = 7,7 [1-exp(-I /26)] r 2 =,984 ; N = I (µmol m -2 s -1 ) FIGURE 6.7 Gross production-irradiance curves derivated from the curve of the Figure 6.4 and recalculated with periods of 5 min and 1 min of recordings, respectively. notable exception of the spring maximum value. This very high production was due to a very high productivity and not to a very high Chla concentration (36.2 ± 9.2 mgchla m -2 in March vs ± 61.4 mgchla m -2 in July), that could indicate small phytoplanktonic cell deposits on the sediment surface following a water column spring bloom: actually, small cells showed higher productivity 14 and large blooms due Phaeocystis sp. (Prymnesiophyceae) occurred in the eastern English Channel during spring every year 15. This strong seasonal response allowed us to estimate an annual potential gross primary production at Le Crotoy, using both seasonal P-I curves and day to day changes in irradiance and tidal variations, with the aim to take into account observed short time variability. This production was estimated to 14.3 gc m -2 y Temporal Resolution of Measurements and Microscale Adaptation of Microphytobenthos to Variations in Irradiance Previous calculations (P-I curves) have been made using trends (slopes of CO 2 concentration versus time) during recordings from 1 to 2 minutes. It could be assumed that response of microphytobenthos to steady variations of irradiance might be recorded with a high frequency as it has already been shown under subtidal conditions 16. Then, as logging frequency was 3 s for CO 2 concentration and 1 min for irradiance, CO 2 production was successively calculated during each period of 5 min of recordings, then during each period of 1 min, and new P-I curves were established according to Equation 6.1. Photosynthetic parameters of equations were very close as well as determination coefficients (e.g., in Figure 6.7). It clearly showed a progressive adaptation of microphytobenthos to continuous increasing or decreasing irradiance. On the contrary, when fast and irregular variations of irradiance occurred (cloudy conditions, for example), it was impossible to calculate a P-I curve in some of the experiments, whatever the timescale, because variations of CO 2 production did not always follow irradiance variations Mesoscale Variations Within the Gradient of Exposure Beyond seasonal variations which can be seen, particularly for respiration, a significant variability occurred within the gradient of exposure (Figure 6.8), both for respiration and primary production. In
7 Multiscale in Situ Measurements of Intertidal Benthic Production and Respiration 13 A Gross primary production mgc m -2 h March May August November Wimereux Le Crotoy Le Havre (muddy sand) Le Havre (sandy mud) mgc m -2 h -1 B Respiration Wimereux Le Crotoy Le Havre (muddy sand) Le Havre (sandy mud) March May August November FIGURE 6.8 Comparison of (A) maximal gross primary production and (B) respiration measured on the four sites in March, May, August and November. the exposed conditions of the sandy marine beach of Wimereux, respiration and gross primary production remained very much lower than those of other locations all along the year. Gross primary production (Figure 6.8A) showed a greater variability, the maximum value being in March in Le Crotoy, May in Wimereux and in the sandy-mud sediment in the Seine estuary and August in the muddy-sand sediment in the Seine estuary. It was higher in the sandy mud than in the muddy sand, except in winter conditions. Neither gross production nor respiration therefore seemed to follow evenly the gradient of exposure, but they clearly indicated a higher benthic metabolism, both autotrophic and heterotrophic, in more or less muddy estuarine sediments Microscale Variability A microscale variability experiment was carried out on three adjacent (a few centimeters from each other) areas (each.126 m 2 ) in Le Crotoy in October. Three series of incubations were conducted, each series consisting of successive 15-min measurements of net production, under saturating irradiance, from 2 h before zenith to 2 h after. Irradiance during this period was 795 (± 189) µmol m -2 s -1 (± standard deviation). A single dark incubation was then performed at each area with the aim of comparing respirations, and to estimate gross primary production. Results (Figure 6.9) did not show significant differences for gross primary production (p >.5, Kruskal-Wallis test) between areas, and variability within each area remained low (gross primary productions ± standard deviation: P 1 = 42.9 ± 2.9 mgc m -2 h -1, P 2 = 45.8 ±.4 mgc m -2 h -1, P 3 = 41.2 ±.8 mgc m -2 h -1, respectively). Respiration also varied little between locations (Figure 6.9). At this spatial scale, the intertidal system appeared relatively homogeneous. Surficial sediment seemed homogeneous and microscale patchiness of microphytobenthos, such as shown by Blanchard, 17 is integrated within the area of measurement: three measurements of Chla concentration (1.6 cm of diametre, 1 cm deep) were realised within each of the three experimental areas; values varied from 55.5 to
8 14 Handbook of Scaling Methods in Aquatic Ecology: Measurements, Analysis, Simulation 5 Location 1 Location 2 Location 3 4 mgc m -2 h GPP1 GPP2 GPP3 R -1 FIGURE 6.9 Comparison of respiration and gross primary production measured on three adjacent elementary areas in Le Crotoy (Somme estuary). GPP1: gross primary production during incubation 1, GPP2: gross primary production during incubation 2, GPP3: gross primary production during incubation 3, R: respiration mgchla m -2 but there was no significant difference between areas (p >.5, Kruskal-Wallis test), with variability within each area higher than variability between areas (Chla concentration ± standard deviation: C 1 = 79.9 ± 7.5 mg m -2, C 2 = 71.2 ± 14. mg m -2, C 3 = 63.6 ± 11.8 mg m -2, respectively) Conclusion and Perspectives Coastal ecosystems are well known for their high physical, chemical and biological variability, 18 mainly due to multiscale physical forcings (seasonal, tidal, mesoscale weather and currents) and to the closeness of interfaces with other systems (continent, atmosphere, offshore ocean). Intertidal areas are subject to all these forcings and particularly to specific variations due to the alternance of emersion and immersion, which induces drastic thermal and irradiance changes. Consequently, short-term variations of intertidal primary production and respiration during a tidal cycle could be almost as dramatic as long-term variability such as seasonal or interannual processes. In the present study, microalgal communities appear to be able to respond to gradual changes in light intensity over the course of a day following a relationship which can generally be described in a P-I curve. However, P-I curves cannot be easily constructed when unsteady changes in irradiance have occurred, under cloudy sky for example. It could be due to several reasons such as a measurement artifact if changes in irradiance occur faster than irradiance data were collected, but this may be because algal community cannot respond to a highly variable light environnement (fast and short successive increases and decreases in light intensity). The daily gross primary production within a given season, at least in winter, may vary more from one day to another due to the timing between the emersion and the sun course, rather than with the cloudiness of the sky. It might even vary as much from one day to another (in summer, for example) as between different seasons (between spring and autumn, for example), thus making the calculation of a monthly carbon budget difficult. Carbon budget calculations are also made more difficult by poor knowledge of the role of seasonal development of microphytobenthic assemblages in the productivity of intertidal sediments and, on the other hand, the potential ability for deposited phytoplankton (such as during spring blooms), to carry on photosynthesis on intertidal sediments during emersion. In the present study, our calculations took into account day-to-day changes in irradiance and tidal variations and allowed us to integrate a part of shorttime variability at Le Crotoy (Somme estuary). The estimation (14.3 gc m -2 y -1 ) is rather high, in the upper part of estimates of primary production in intertidal sand beaches and mudflats. 18 However, small spatial variability is not yet well understood and measured enough to estimate the annual production of the whole system (see below).
9 Multiscale in Situ Measurements of Intertidal Benthic Production and Respiration 15 Moreover, it appeared that the response of microphytobenthos to short-term variations in irradiance was not regular and depended on the variation patterns. Production regularly increased from dawn up to saturation or decreased toward twilight if irradiance increase or decrease was regular, but it did not seem to show fast adaptability when irradiance development was disturbed by cloudy periods before saturation. Seasonal variations of respiration clearly occurred in the four sites, depending both on the abundance of heterotrophs (microbiota are assumed to be the major group responsible of heterotrophic activity) and on the temperature. No seasonal patterns in gross primary production occurred in the exposed sandy beach at Wimereux, whereas seasonal effects were strong but unsteady from one site to another in estuaries (maxima in spring at Le Crotoy and in summer in the Seine estuary). Both marine sandy beaches and estuarine tidal flats showed a characteristic spatial distribution of zoobenthic communities at small scale, strongly correlated with geomorphological features, granulometric properties and water retention characteristics of the sediment. 2,21 As zoobenthic zonation resulted from these characteristics and general dynamics of the system, it can be assumed that it also influenced the general distribution of microphytobenthos and so its production. 18 However, Guarini et al. 22 reported large patches of microphytobenthos in Marennes-Oléron Bay (Atlantic coast, France) distributed independently from the geomorphological structure and dominant gradient (emersion) of the area. At a smaller scale of few tens of square meters, small variations in the level of sediment or of water content could act on production and respiration 23,24 and should be estimated. In the present study, although microscale variability occurred in Chla concentration, which indicated a typical patchiness of microalgal communities 25, gross photosynthesis and respiration were homogeneous on a larger scale of several square meters (Figure 6.9). At the mesoscale, spatial variations of primary production clearly followed general features of structure and dynamics between, on the one hand, exposed sandy beaches and, on the other hand, sheltered mudflats. However, variations in production and respiration could not be simply related to the gradient of exposure as expressed by the granulometric gradient (percent of mud in sediment). This may be true even for cases where the abundance of bacteria increased with smaller sediment particle size and higher carbon and nitrogen occurring in finer sediments 18 or with nutrients available in the sediment. 8 Decreasing exposure and increasing sediment stability favor biodiversity and production in sheltered shores, 18 as has been shown by composite measures of exposure, particle size, and slope of the beach (the beach stability index of McLachlan, 19 for example). However, diversity generally declines with salinity in sheltered bays or estuarine gradients. In the present study, it could be assumed that the greater production and respiration measured in muddy estuarine sediments than in the sandy exposed beach of Wimereux is due to the occurrence of a threshold energy level, mainly controlled by wave action, for microalgal colonization of sediment. As the exposed sandy beach at Wimereux is generally above that level, microphytobenthos cannot become well established so production and respiration rates remain low. On the contrary, the energy level could generally stay below a critical threshold in more sheltered estuarine areas so favor sediment colonization and stabilization by microphytobenthos, which could then be more abundant and productive. The next interesting step would be to test the effect of different patterns of irradiance variability by laboratory simulation to gain a better understanding of the adaptability of microphytobenthos. Environmental factors, such as temperature variations and meiobenthic/microbenthic biomass variations, acting on seasonal variations of primary production and respiration, also need to be precisely taken into account. Furthermore, it appears important to deal with spatial distribution and photosynthetic characteristics of microphytobenthos in relation to standard features of intertidal zonation and other small scale heterogeneity of sand and mudflats. Further experiments will be conducted using three similar systems simultaneously, with a view to dealing with microscale (several square meters) and small scale (from few tens of square meters within a facies to variability between facies) variations in the four studied sites. Acknowledgments This study has been supported by a grant (Action Thématique Innovante 99N5/345) from the Institut National des Sciences de l'univers (INSU) and by the scientific programmes Seine-Aval 2 and PNEC
10 16 Handbook of Scaling Methods in Aquatic Ecology: Measurements, Analysis, Simulation (Programme National Environnement Côtier). The authors thank the anonymous reviewers and Pete Strutton for their very helpful comments on the manuscript and Mr & Mrs Migné for providing croquet equipment. References 1. Charpy-Roubaud, C. and A. Sournia, The comparative estimation of phytoplanktonic, microphytobenthic and macrophytobenthic primary production in the oceans. Mar. Microbial Food Webs, 4, 31, Mann, K H., Seaweeds: their productivity and strategy for growth. The role of large marine algae in coastal productivity is far more important than has been suspected. Science, 182, 975, Asmus, R., Field measurements on seasonal variation of the activity of primary producers on a sandy tidal flat in the northern Wadden Sea. Neth. J. Sea Res., 16, 389, Mann, K. H., Ecological energetics of the seaweed zone in a marine bay on the Atlantic coast of Canada. II. Productivity of the seaweeds. Mar. Biol., 14, 199, Blanchard, G. and J.-M. Guarini, Studying the role of mud temperature on the hourly variation of the photosynthetic capacity of microphytobenthos in intertidal areas. C. R. Acad. Sci. Paris, 319, 1153, Mortimer, R. J. G., Krom, M. D., Watson, P. G., Frickers, P. E., Davey, J. T. and R. J. Clifton, Sediment-water exchange of nutrients in the intertidal zone of the Humber estuary, U.K. Mar. Poll. Bull., 37, 261, Hondeveld, B. J. M., Bak, R. P. M., Raaphorst, van W. And F. C. Van Duyl, Impact of grazing by benthic eucaryotic organisms on the nitrogen sediment-water exchange in the North Sea. J. Sea Res., 41, 255, Barranguet, C., Kronkamp, J. and J. Peene, Factors controlling primary production and photosynthetic characteristics of intertidal microphytobenthos. Mar. Ecol. Prog. Ser., 173, 117, Underwood, G. J. C. and J. Kronkamp, Primary production by phytoplancton and microphytobenthos in estuaries. Adv. Ecol. Res., 29, 92, Loquet, N., Rybarczyk, H. and B. Elkaïm, Echanges de sels nutritifs entre la zone côtière et un système estuarien intertidal: la Baie de Somme (Manche, France). Oceanol. Acta, 23, 47, Migné, A., Davoult, D., Spilmont, N., Menu, D., Boucher, G., Gattuso, J.-P. & H. Rybarczyk, A closedchamber CO 2 flux method for estimating intertidal primary production and respiration under emersed conditions. Mar. Biol., 14, 865, Webb, W.L., Newton, M. and D. Starr, Carbon dioxide exchange of Almus rubra: a mathematical method. Oecologia, 17, 281, Lizon, F., Seuront, L. and Y. Lagadeuc, Photoadaptation and primary production study in tidally mixed coastal waters using a Lagrangian model. Mar. Ecol. Prog. Ser., 169, 43, Kirk, J.T.O., Light and photosynthesis in aquatic ecosystems, 2 nd ed., Cambridge University Press, Cambridge, U.K., 1994, chap Gentilhomme, V. and F. Lizon, Seasonal cycle of nitrogen and phytoplankton biomass in a well-mixed coastal system (eastern English Channel). Hydrobiologia, 361, 191, Boucher, G., Clavier, J., Hily, C. and J.-P. Gattuso, Contribution of soft-bottoms to the community metabolism (primary production and calcification) of a barrier reef flat (Moorea, French Polynesia). J. Exp. Mar. Biol. Ecol., 225, 269, Blanchard, G., Overlapping microscale dispersion patterns of meiofauna and microphytobenthos, Mar. Ecol. Prog. Ser., 68, 11, Raffaelli, D. and S. Hawkins, Intertidal Ecology, 2nd ed., Kluwer Academic, Dordrecht, the Netherlands, 1999, chap McLachlan, A., Sand beach ecology, swash features relevant to the macrofauna, J. coast. Res., 8, 398, Salvat, B., Les conditions hydrodynamiques interstitielles des sédiments meubles intertidaux et la répartition verticale de la faune endogée, C. R. Acad. Sci. Paris, 259, 1576, McLachlan, A., Dissipative beaches and macrofauna communities on exposed intertidal sands, J. coast. Res., 6, 57, Guarini, J.-M., et al., Dynamics of spatial patterns of microphytobenthic biomass: inferences from a geostatistical analysis of two comprehensive surveys in Marennes-Oléron Bay (France), Mar. Ecol. Prog. Ser., 166, 131, 1998.
11 Multiscale in Situ Measurements of Intertidal Benthic Production and Respiration Toulmond, A., La respiration chez les Annélides. Oceanis, 3 (7), 38, Dye, A. H., Tidal fluctuations in biological oxygen demand in exposed sand beaches. Estuar. Coasal. Mar. Sci., 11, 1, Seuront, L. & N. Spilmont, Self-organized criticality in intertidal microphytobenthos patch patterns. Physica A, 313, 513, 22.
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