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The effects of tropical storm Dennis on coastal phytoplankton
Estuarine,
Coastal
and Shelf
Science
(1985) 20,403-418
The Effects of Tropical Coastal Phytoplankton
Stephan
Storm
Dennis
I. Zeemad
Marine Science Program and Baruch Institute for Marine Research, University of South Carolina, Columbia, South U.S.A. Received
on
19 December
Keywords: tropical waters; estuaries
I983
and in revised
storms;
form
phytoplankton;
24 May
Biology Carolina
and Coastal 29208,
1984
primary
production;
coastal
The effects of tropical storm Dennis were documented in the coastal waters of South Carolina during August 1981. Phytoplankton photosynthesis vs. irradiance curves showed initial depression of the parameter a followed by three- to five-fold increase of both a and the asymptotic maximum rate of photosynthesis c. Productivity rates were depressed in most samples immediately after the storm. Surface samples at the inshore stations were around 50 mg C me3 h-’ at saturating light intensities, while the offshore station rates were around 10 mg C m - 3 h - r . After a 1O-day lag these rates had increased to about 200 mg C m-3 h-’ inshore and 75 mg C mm3 h-’ offshore. These changes are thought to be primarily caused by changes in species composition. Some of the dominant diatom species changed and dinoflagellate species were introduced. No significant changes in nutrient concentrations were observed. Transient depressions of water temperature, salinity and light intensity may have contributed to the observed changes.
Introduction The southern and eastern coasts of the United States are often subjected to depredations by hurricanes or tropical storms. The onslaught of these weather systems can cause significant damage to natural and manmade features of the region. Although significant amounts of research effort have gone into prediction and damage assessment, very little is known about the effects of hurricanes on aquatic biota, especially phytoplankton. Previous biological studies on the effects of hurricanes have mostly been conducted in coral reef environments (e.g., Woodley, 1980; Porter et al., 1981; Woodley et al., 1981; Knowlton et al., 1981). These studies have mainly dealt with the storm effects on the corals themselves and have only briefly commented on plankton, fish, and algae. Yeo & Risk (1979) studied the effects of Hurricane Beulah on the benthos of the Bay of Fundy. Dobbs & Vozarik (1983) studied pre- and post-storm benthic and water column samples Contribution
574 of the Belle W. Baruch Institute
Research and contribution “Present address: Harbor 33450.
for Marine Biology and Coastal 442 from the Harbor Branch Foundation Inc. Branch Institution, Inc. RR 1, Box 196-A, Ft. Pierce, Florida
403 0272-7714/85/040403
+ 16 $02.00/00
0 1985 Academic
Press Inc. (London)
Limited
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for effects on coastal infauna. One of the most complete studies of tropical storm effects was done by the Chesapeake Research Consortium (1977). In this work, sections by Flemer et al. (1979) and Zubkoff & Warinner (1977) address chlorophyll concentrations in the estuary, while Loftus & Seliger (1977) present results from primary productivity measurements, chlorophyll and species composition. They found the amount of area1 productivity was not altered by the storm, but species composition changed dramatically, and long-term chlorophyll concentrations also changed. A multitude of effects might occur to either enhance or retard the growth of phytoplankton. The input of large amounts of freshwater may stress non-tolerant species or advect them to other regions. The physiological stress may hamper growth rates and eventually lead to local extinctions. Wholesale replacement by more tolerant forms is probably the usual consequence until salinities normalize. Rivers and runoff could enhance nutrient concentrations. In coastal waters nutrients could be upwelled from deeper waters through the action of bottom return-flow in response to seaward surface flows. In coastal waters turbulence might also reintroduce phytoplankton which had previously sunk below the photic depth, or, conversely, mix the phytoplankton downward. Similarly, turbidity might be increased due to resuspension of the bottom sediments. In addition, strong currents associated with storm passage can be a major advective force causing changes in the water masses found at a given location. Such advection could bring in new nutrients as well as new algal populations. In August 1981, I had the opportunity to study the effects of a tropical storm on nearshore environments. Ongoing studies were being conducted on light adaptation of phytoplankton populations in a pristine, high-salinity, saltmarsh estuary and the nearby coastal ocean (Zeeman, submitted). On 19 August, Tropical Storm Dennis passed within 30 miles of the field laboratory of the Belle W. Baruch Institute for Marine Biology and Coastal Research at Georgetown, South Carolina (Figure 1). Winds at the time were reported up to 96.5 km h- ’ (60 mph). This work documents the effects of the storm on the water masses and phytoplankton populations of the North Inlet estuary and the adjacent coastal waters. Photosynthesis-irradiance relationships were measured to assess physiological changes in the algae. In addition, several environmental parameters were also measured to determine which factors may have affected the phytoplankton populations. Experiments were performed along a transect from within the inlet to 8 km offshore. These experiments were conducted both before and after the passage of Tropical Storm Dennis to investigate possible short-term changes. Materials
and methods
The North Inlet estuary (33”20’N, 79”lO’W) is near Georgetown, South Carolina. Reported here are the results of two sampling dates prior to the storm (20 July and 11 August) and four datesafter passageof the storm (23 and 29 August, 27 September and 4 October). Samples were collected along a transect at four stations. Station 1 was located on a major creek about 2 km from the inlet proper. Station 2 was in the mouth of the inlet and station 3 just seaward of the ebb tidal delta. Station 4 was in 10m of water, 8 km offshore. Temperature and conductivity were measured at each station at one meter depth intervals from surface to bottom with a Beckman RS5-3 induction salinometer. Salinities were calculated from these data using the polynomial function of Cox et al. (1976).
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Effects of Tropical Storm Dennis
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30°
3o”
25’
25’
80’ 85O Figure 1. The path of Tropical Storm Dennis States. The track starts at the southern portion location at 0000 h GMT on 17 August. The GMT, open circles were positions at various
75O 7o” while near or over the continental United of the figure, and the first circle was the filled circles represent positions at 0000 h times.
Density was computed as sigma-t according to the method of Knudsen (1901) as outlined in Kjerfve (1979). Surface current was measured with a biplanar drogue at a depth of 1 m. The surface float of the drogue was attached by a 20-m line to the anchored boat and the drift time was measuredwith a stopwatch. Dye studies showed the drogue to accurately move with the surface waters. Water samplesat each station were collected with standard Niskin bottles and kept in plastic containers for transport to the field laboratory. Samplesfor chlorophyll measurements were collected from the surface, mid-depth, and bottom of the water column. Productivity and nutrient samples were collected at the surface from stations 1 and 2, and at the surface and bottom at stations 3 and 4. Samples for photosynthetic rate measurementswere maintained in darkness from the time of collection until preparation for the experiments, which was usually within 3 h. Upon return to the laboratory, duplicate chlorophyll sampleswere filtered through Whatman GF/F glass fibre filters with magnesium carbonate and frozen. These were later extracted in 900,, acetone with the aid of grinding and analyzed fluorometrically (Yentsch & Menzel, 1963; Holm-Hansen et al., 1965). Permanent mounts of phytoplankton sampleswere prepared using a membrane filter technique (Fournier, 1978). Volumes of 25 to 50 ml were passedthrough 0.45 pm HA Millipore filters. The wet filters were put on microscope slides and cleared with gluteraldehyde by heating to 60°C for 20min (Dozier & Richerson, 1975) then permanently mounted on the slides with a cover slip.
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Nutrient samples were filtered through Whatman GF/F filters and stored frozen in glass scintillation vials. Prior to freezing, the phosphate samples were poisoned with mercuric chloride, the nitrate-nitrite samples poisoned with phenol. These samples were later analyzed with a Technicon Autoanalyzer for nitrate plus nitrite and orthophosphate using standard Technicon methods (Technicon Industrial Systems, 1973, 1977). Photosynthesis versus irradiance (P-I) curves were obtained by using a constant temperature incubator at the field laboratory. Temperature was within 2 “C of the seasurface. Light intensity was provided by a bank of 10 tungsten outdoor spot lamps in the range of about 50 to 900 uEin m- ’ s- ‘. Neutral density plastic screening material provided intensity reduction in steps of about 500,. Excess heat from the lamps was removed by a water filter between the lamps and the incubator. All incubations were started around midday and lasted 4 h. This reduced the possible influence of diurnal rhythms in chlorophyll (Glooschenko et al., 1972) aswell asin the P versus I parameters (Harding et al., 1982; MacCaull & Platt, 1977). Duplicate bottles were incubated from all samplesat five light intensities and also in the dark. Each bottle was injected with 1 to 5 microcuries of 14C sodium carbonate. After incubation the bottles were vacuum filtered (< 180 mmHg) through Gelman GA-6 membrane filters (0.45 urn pore size) and rinsed with filtered seawater. The radioactivity on the filters was determined by liquid scintillation counting. The counting efficiency of each sample was determined by external standard channels ratios using a quench curve prepared from natural plankton populations and 14Ctoluene standard. The P-I relationship is in the shape of a rectangular hyperbola. The initial slope is described by the parameter a while P, is the asymptotic maximum rate of photosynthesis. All photosynthetic rate measurements were normalized to a mg Chlorophyll basis prior to P-I analysis. The P-I parameters, were estimated by a nonlinear least-squarescurve fitting procedure which utilized a derivative-free algorithm (Ralston & Jennrich, 1978). For most of the cases,the model applied to the data was the hyperbolic tangent function of Jassby & Platt (1976). For those casesinvolving photoinhibition, the model of Platt et al. (1980) was used. Lederman & Tett (198 1) have shown that a variety of models would work equally well, although they suggested using the older models. In both models, an additional parameter was specified so asnot to constrain the curves to intercept at zero on the Y axis. This additional parameter was not meant to serve as an estimate of any physiological rate, i.e. respiration, but only to allow better curve fitting. Results
P-I curves were determined for the six sampling dates. In the range of light intensities used, photoinhibition was only observed once. Figure 2 showsthe estimatesof a and the standard error associatedwith each estimate. Values of a were not much different among stations on a given date, but significant changes did occur between dates. Within 4 days after passageof the storm, there was a decrease in a at all stations and at all depths. A week later, on 29 August, the initial slope for all sampleshad increased by a factor of 3 to 5. After this time there was a decline once again to roughly pre-storm values. There was, however, an indication of another increasein October. Estimates of 2 are presented along with their standard errors in Figure 3. The pre-storm and immediate post-storm samplesdid not have different Pi values. However,
407
Effects of Tropical Storm Dennis
0~00
I
’ 20
Jul
I II Aug
I 23
I 29
Aug
Aug
I 27
Sep
4 act
Date
Figure 2. Plot of alpha values shown with + 1 standard error bars (k-station x-station 2; A-station 3s; V-station 3B; G-station 4s; e-station 4B).
1;
10 days after the passageof Tropical Storm Dennis, these values increased by factors of 4 to 5. After this time there was a gradual decline back to pre-storm values. The chlorophyll concentrations (Figure 4) declined in the surface samplesat the nearshore station (3) and in the bottom samplesof the offshore station (4) after the storm. At the sametime, the surface samplesat station 4 showed a slight increase. The other 3 sets of samplesremained constant. There was a decline after August in chlorophyll values at all stations. Productivity rates at saturating light intensities are shown in Figure 5. The mean rates ranged between 8 and 210 mg C mP3 h- ’ . At the three inshore stations maximal rates were cu. 200 mg C mm3h- ’ while the offshore station remained below 85 mg C m- 3h- ‘. A depression of the productivity rates took place in most of the sampleson 23 August, immediately after the storm passed. The most notable feature, however, is the occurrence of a peak on 29 August, which was seenin all samples.The observed changeswere more influenced by changesin the P-I parameters than by chlorophyll concentrations. The data for nitrate-nitrite concentrations are shown in Figure 6 and those for ortho-phosphate concentrations in Figure 7. The nutrient concentrations fluctuated and this was perhaps due to a tidal signature on the estuarine concentrations. High tides generally show low nutrient concentrations within the estuary and low tides have high nutrient concentrations (McKellar er al., 1982). The nutrient samples for 11 August were not taken, thus the second point on the graphs corresponds to immediate poststorm conditions. The nitrate-nitrite concentrations increased within the estuary (stations 1 and 2). A similar, but smaller, increase in the orthophosphate concentrations
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S. I. Zeeman
50
I
01 20
I
Jul
II Aug
I 23
Aug
I 29
Aug
I 27
Sep
4 act
Date
Figure 3. Plots of the e A-station 3s; V-station
values + 1 standard error bars (W-station 3B; @-station 4s; O-station 4B.
1; x -station
2;
12-
9-
6-
3-
-I
oJUI
Aug
Figure 4. P:ot of the chlorophyll concentrations at each location study period. Arrow indicates day of storm passage.
5ep
sampled
during
the
Effects of Tropical
Stotlon
I
StatIon
,
4
Stotlon
3
I JUI
2
A A 4
stot1on
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Storm Dennis
Pug
I
4
I Sw
Ott
JUI
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Sep
act
Figure 5. Primary productivity at saturating light intensities. The arrows indicate the day of storm passage. Circles are surface samples, squares are bottom samples. Bars represent k 1 standard deviation. Where no bars are apparent, symbols are larger than standard deviation.
was also evident at station 1. The second peaks for both nitrate-nitrite and phosphate occurred on 4 and 18 October. The highest concentrations of both nutrients were seen only at station 1, and at this time the orthophosphate peak was relatively greater than the 23 August peak, when compared with the nitrogen results. There was a general rise in the phosphate levels at station 4 after 23 August. Dissolved organic nutrients were not measured for this project. A concurrent study however, collected these data at three locations within the estuary (Long Term Ecological research program). Dr E. Blood has kindly allowed me accessto this information, which is presented in Figure 8. These data were collected daily at 1000 h (EDT) at two sites near stations 1 and 2 in this study, and also at a location on a creek closer to the landward edge of the marsh. Most of the temporal variability is due to sampling at different tidal stages(Kjerfve & McKellar, 1980). The DON and DOP data from the sitesnear stations 1 and 2 showed virtually no storm induced changes, but major fluctuations were evident at the upper marsh site. There were no discernible trends in the ammonium data causedby the storm. Concentrations of all 3 organic nutrients tended to be highest at the upper marsh site and lowest at the site near station 2. Heavy rainfall from the storm decreased the salinity within the estuary, but had little effect on the offshore waters (Figure 9). Salinities within the inlet were already lower prior to the storm event ason 11 August (31.4% vs. 34.3% offshore). Enough freshwater entered the system, due to the storm, to stratify this normally vertically homogenous estuary. On 23 August there was a 4 ppt salinity difference between surface and bottom
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S. I. Zeeman
Figure study.
JUI
Figure study.
-
6. Plot of the combined nitrate-nitrite Arrow indicates the day of storm passage.
concentrations
WI
7. Plot of the phosphate concentrations found Arrow indicates day of the storm passage.
measured
during
the
during
this
Sep
at locations
sampled
at the innermost station (1). Salinities returned to normal by 29 August, ten days after the storm. Sigma-t values follow the salinity data except that there was a steady rise at the offshore stations (Figure 9). The offshore waters more strongly reflect the intluence of temperature (Figure 9) on sigma-t, while the estuarine waters show the effect of salinity
Efiects of Tropical
Storm
411
Dennis
0
Figure 8. Organic nutrient concentrations (pg-at 1-l) at three estuarine locations (unpublished data, E. Blood). Day 0 is 1 July, storm passage occurred on day 50 (symbols: O-near station 1; O-near station 2; V-upper marsh area).
changes. The density structure of these waters immediately after the storm showed that estuarine (station 1) waters were stratified and distinct from coastal waters, but that mixing near the mouth (station 2) was rapid. Stratification was also evident at station 3 due to lower salinity water from the inlet overlaying higher salinity water from offshore. The plume of low salinity water was not evident at the offshore station (4).
17
:d:
25 -
26
JUI
I
Sep
I
Ott
Jul
%? I
I
Aug
I
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Station
Sep
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I
Ott
Jul
I Aug
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Stotion
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I Ott
t Jul
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Figure 9. Plots of salinity, temperature, and sigma-t at each location sampled during the study. of storm passage. Open symbols show bottom samples, closed symbols are surface samoles.
Aug
I
Station
Arrow
Aug
I
Station
I indicates
Sep
4
day
act
Effects of Tropical
Storm
413
Dennis
Figure IO. Plot of daily rainfall measured at a site near the field Inlet. Arrow indicates the day of storm passage.
laboratory
at North
Storm passagebrought on a rapid decline in water temperatures at all stations and causeda reversal of the relative temperature gradient from inshore to offshore (Figure 9). The temperature decline was greatest in the estuary. Ten days after the storm passed,the water column became well mixed from inshore to offshore, with a concomitant rise in temperature. The temperture never reached pre-storm levels, but from this point on continued to decline for the rest of the winter. A thermal gradient had been reestablished by the end of September, but with the coldest temperatures found in the estuary rather than offshore. Precipitation during this period was very heavy, not only in this general vicinity but along the entire coastline of both North and South Carolina (Wagner, 1981). Daily rainfall data for July through September at one site are shown in Figure 10. The highest daily precipitation recorded for any of the 7 rain gaugesin the vicinity of the laboratory was 18.59 cm (7.32 in) on 19 August. The total monthly rainfall for August was ca. 34.3 cm (13.5 in). Dominant phytoplankton species prior to the storm included Rhizosolenia alata, Skeletonema costatum, Thallasiothrix sp. and Ondontella aurita. After the storm the dominant speciesincluded R. alata, S. costatum, Pleurosigmasp., and Coscinodiscus sp. A number of dinoflagellates also appeared after the storm, including Ceratium trichoceros, Gymnodinium sp., and Dinophysis caudata.
Discussion The results of this study document several conditions which occur after the passage of a tropical storm. The major changes observed in this study were in the I? versus I parameters. The initial responsewas a decreasein a. After a lag of at least 4 to 5 days, an
414
S. I. Zeeman
DOY
Figure 11. Amount of sunshine relative to possible sunshine during the month of August. Taken from NOAA weather data at Charleston, South Carolina. Arrow indicates the day of storm passage.
increase in both a and e, after which there is a slow return of both parameters to pre-storm levels. Turner et al. (1979) showed a negative effect of storms on e and also state that flushing of the estuary by storms increasesproduction offshore. The latter may have occurred in this study. However, the productivity increaseat the end of August was observed at all stations and was the result of increasesin the P-I parameters. The usual interpretation of a is that it represents the photochemical processesof the light reactions of photosynthesis. As such, the parameter should be independent of temperature. It may be affected, however, by physiological status of the cells and Platt & Jassby (1976) found that a was also correlated to the light history of the cells. Correlations to salinity have been observed in other studies (Platt & Jassby, 1976), while one response to lowered light intensities is an increase in chlorophyll per cell, which could decreasea (Falkowski, 1980). The time scalesfor changes in the photosynthetic mechanism are on the order of minutes or hours to a few days (Platt & Gallegos, 1980; Prezelin & Matlick, 1980; Jones, 1978). Data on percent of possible sunshine were obtained from the NOAA Environmental Data and Information Service for Charleston, South Carolina. These data, presented in Figure 11, show that there was a period of about a week with heavy cloud cover around the time of the storm. The duration of the decreasedlight intensity wason the sameorder asphotosystem changes,and might thus have had an effect. The other parameter, e, is generally interpreted as representing the dark reactions of photosynthesis. This is an enzyme mediated process and Platt & Jassby (1976) found a positive correlation between temperature and p”,. In addition, Senft (1978) found Pi to be dependent on internal phosphorus concentrations. It is obvious, however, that the temperature during this study could not have been the causeof the rise in I’,,. Nutrient sequestering by the phytoplankton cannot be ruled out after the storm becauseit wasnot measured. However, asdiscussedlater, the external nutrient concentrations did not vary beyond normal levels.
Effects of Tropical
Storm Dennis
415
A more plausible explanation is that the speciescomposition changed in the aftermath of the storm. Examination of permanent mounts of phytoplankton collected at the time of sampling do indeed show population shifts. Phytoplankton populations prior to the storm were almost totally composed of diatoms. After storm passage,diatoms were still the most abundant taxa, but some of the dominant specieshad changed. In addition, there appeared several dinoflagellate species. Loftus & Seliger (1977) also report an abundance of dinoflagellates in ChesapeakeBay after passageof Tropical Storm Agnes. Dinoflagellates have been known to utilize organic substrates for nutrition, and the storm could have enriched the waters with organic compounds through runoff. There was a concentration gradient of DON, DOP and ammonium, which shows runoff to be a source of oganic nutrients. Furthermore, Rivkin et al. (1982) have shown that dinoflagellates may retain high division rates despite low light intensities, or to resume high division rates upon reexposure to higher light. From measurements of chlorophyll concentrations, apparently no drastic changes in the phytoplankton biomass occurred, although a slight decline, evident by the end of September, was possibly related to normal seasonaltrends. From other work, it was also confirmed that the values found during this study are within the normal range for this time of the year (Kjerfve & McKellar, 1980; Zingmark, unpublished data). The chlorophyll concentrations found at the estuarine stations (1 and 2) remained constant during this time and declined only slightly in September, probably asa result of normal seasonaldecline toward winter conditions. The decreaseof chlorophyll in the surface water at station 3 after the storm is the result of low density estuarine water, containing lower chlorophyll concentrations, overlaying offshore water. The higher chlorophyll levels in the bottom waters at station 3 were perhaps the result of turbulence. Bottom waters often have higher pigment concentrations due to resuspension by tidal currents (Roman 8zTenore, 1978), and also due to higher pigment content per cell in response to low light intensities (Falkowski, 1980). The offshore station (4) showed a decreasein chlorophyll levels in the bottom waters with a concomitant increase at the surface. This was due to the breakdown of stratification and turbulent mixing of phytoplankton throughout the water column. Nitrate-nitrite concentrations seemedelevated at stations 1 and 2 immediately after the storm while phosphate was higher only at station 1. The increases, however, were well within the normal ranges for the seasonand may only be a reflection of the tidal stage at which the samples were collected. Other concurrent studies, employing daily sampling, also showed that these nutrient levels are not unusual (Wolaver, unpublished data). The lack of any significant response to a storm by phosphate concentrations has also been documented for the Chesapeake (Flemer et al., 1979; Schubel et al., 1977; Smith et al., 1977). These authors did, however, report increasesof nitrate and nitrite concentrations by factors of 2 to 3 after Tropical Storm Agnes. Slight increasesin phosphate at the offshore station (4) were probably a reflection of the advection of water offshore. The consistent patterns of decreasing nutrient concentrations from station 1 to station 4 indicates that the source of the nutrients was in the estuary rather than the coastal waters (Turner et al., 1979; Yoder et al., 1981). Organic nutrient concentrations, although confined to estuarine samples,also confirm a terrestrial (or at least high marsh) source. The source of the nutrients could be from nutrient regeneration in the sediments, land runoff, precipitation, or exchangeswith the nearby Winyah Bay estuary. Correll (1981) has indicated that land runoff could be a major source of nutrients and
416
S. I. Zeeman
should not be ignored. Michner & Allen (1982), however, state that freshwater input is minimal in the study area, due to the small size of the drainage basin associated with North Inlet. Examination of the organic nutrient concentrations showed that there was some response to rainfall often after a short lag time (compare Figures 8 and 10). The volume input however seemedsmall since the elevated concentrations were restricted to the site closestto the landward edge of the marsh. The lower concentrations at the other two locations probably indicate the rapid dilution of the runoff. However, biological or chemical binding cannot be ruled out. Recycling of nutrients is probably important in both the estuarine and coastal waters, but the extent of this has not been evaluated for these waters. The nutrient input from precipitation directly was probably small aswas exchange with Winyah Bay. Schwing & Kjerfve (1980) studied a major creek between North Inlet and Winyah Bay. They report finding a nodal point in the creek which limits exchange between the two systems. Nothing definitive can be said of the current patterns during this time since I had no recording current meters. However, the surface currents which had been measured showed no unusual trends. Smith (1978) found that current speed was affected by Hurricane Anita in the Gulf of Mexico but direction remained shore parallel and constant. On the east coast of southern Florida, Smith (1982) found that current patterns inshore and offshore differed during the passageof Hurricane David. He concluded that the inshore site (in 10m of water) was more subject to wind stress while the offshore waters reacted to pressure gradients. This could also have been the casefor my study which was also conducted in waters up to 10 m deep. However, the study sites were not similar in terms of bathymetry. In Smith’s study, the shelf break was much closer to shore and upwelling was observed. In the present study, upwelling at the shelf break probably had no influence becauseof the wide continental shelf (130 km) off the South Carolina coast. In conclusion then, the effects of the storm were a transient depression of water temperature and salinity. No significant changes in nutrient concentrations were observed in the estuary or offshore, although there was an enrichment of DON and DOP at a high marsh site. Depression of the initial slope of the P-I curves were probably related to some form of stress such as low salinities or low light intensities due to prolonged cloud cover. Within ten days, both a and I$ were significantly greater than prior to the storm. The most likely causative factor was a change in speciescomposition. Acknowledgements I wish to thank Drs E. Blood, T. Wolaver and R. Zingmark for accessto unpublished data. D. L. Barker aided in sampling and W. Johnson and S. Hutchinson did the nutrient analyses. Comments on earlier drafts were made by R. A. Gibson, S. Blair and an anonymous reviewer. This research was supported by a pre-doctoral fellowship from the Belle W. Baruch Foundation, the Marine Science Program and U.S.C., NSF grant DEB8O-12165, F. J. Vernberg, project director, and the Harbor Branch Foundation, Inc. References Chesapeake Research Consortium, The. 1977 The effects of Tropical Storm escuarine system, CRC Publication no. 54. The Johns Hopkins University
Agnes on the Chesapeake Bay Press, Baltimore. 639 pp.
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Correll, D. L. 1981 Nutrient mass balance for the watershed, headwaters, intertidal zone and basin of the Rhode River estuary. Limnology and Oceanography 26,1142-l 149. Cox, R. A., Culkin, F. & Riley, J. P. 1967 The electrical conductivity/chlorinity relationship in natural sea water. Deep-Sea Research 14,203-220. Dobbs, F. C. & Vozarik, J. M. 1983 Immediate effects of a storm on coastal infauna. Marine Ecology Progress Series 11,273-279. Dozier, B. J. & Richerson, P. J. 1975 An improved membrane filter method for the enumeration of phytoplankton. Verhandlungen internationale Vereinigung fiir theoretische und angewandte Limnologie 19(2), 15241529. Falkowski, P. G. 1980 Light-shade adaptation in marine phytoplankton. In Primary Productivity in the Sea (P. G. Falkowski, ed.). Plenus Press, New York. pp. 99-l 19. Flemer, D. A., Ulanowicz, R. E. & Taylor, D. L. 1979 Some effects of Tropical Storm Agnes on water quality in the Patuxent River estuary. In The Effects of Tropical Storm Agnes on the Chesapeake Bay Estuarine System, CRC Publication no., 54. The Johns Hopkins University Press, Baltimore. pp. 251-287. Foumier, R. 0. 1978 Membrane filtering. In Phytoplankton Manual (Soumia, A., ed.). Monographs on oceanographic methodology 6. UNESCO, Paris. pp. 108-l 14. Glooschenko, W. A., Curl, R. Jr & Small, L. F. 1972 Die1 periodicity of chlorophyll a concentrations in Oregon coastal waters. Journal of the Fisheries Research Boardof Canada 29,1253-1259. Harding, L. W. Jr, Prezelin, B. B., Sweeney, B. M. & Cox, J. L. 1982 Die1 oscillations of the photosynthesis irradiance (P-I) relationship in natural assemblages of phytoplankton. Marine Biology 67, 167-178. Helm-Hansen, O., Lorenzen, C. J., Holmes, R. W. & Strickland, J. D. H. 1965 Fluorometric determination of chlorophyll. 3ournal du Comer’1 International pour 1’Exploration de la Mer 30,3-15. Jassby, A. D. & Platt, T. 1976 Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnology and Oceanography 21,54&547. Jones, R. I. 1978 Adaptation to fluctuating irradiance by natural phytoplankton communities. Limnology and Oceanography 23,920-926. Kjerfve, B. 1979 Measurement and analysis of water current, temperature, salinity, and density. In Estuarine Hydrography and Sedimentation (Dyer, K. R., ed.). Cambridge University Press, Cambridge. pp. 186-226. Kjerfve, B. & McKellar, H. N. 1980 Time series measurements of estuarine material fluxes. In Estuarine Perspectiwes (Kennedy, V. S., ed.). Academic Press, New York. pp. 341-357. Knowlton, N., Lang, J. C., Rooney, M. C. & Clifford, P. 1981 Evidence for delayed mortality in hurricane-damaged Jamaican staghom corals. Nature 294,251-252. Knudsen, M. H. C. 1901 Hydrographical Tables. G.E.C. Gad, Copenhagen. 63 pp. Lederman, T. C. & Tett, P. 1981 Problems in modelling the photosynthesis-light relationship for phytoplankton. Botanica Marina 24,125-134. Loftus, M. E. 81 Seliger, H. H. 1977 A comparative study of primary production and standing crop of phytoplankton in a portion of the upper Chesapeake Bay subsequent to Tropical Storm Agnes. In The Effects of Tropical Storm Agnes on the Chesapeake Bay Estuarine System. CRC Publication no. 54. The Johns Hopkins University Press, Baltimore. pp. 509-521. McCaull, W. A. & Platt, T. 1977 Die1 variations in the photosynthetic parameters of coastal marine phytoplankton. Limnology and Oceanography 22,723-731. McKellar, H. N., Jr, Whiting, G. & Kjerfve, B. 1982 Summer flux of inorganic nitrogen and phosphorus from a southeastern marsh-estuarine ecosystem. Abstract. 45th Annual Meeting of the American Society of Limnology and Oceanography, Raleigh, NC, June 1982. Michner, W. K. 81 Allen, D. M. 1982 Description of study area. In Ecology of Winyah Bay, SC and Potential Impacts of Energy Development (Allen, D. M., Stancyk, S. E. & Michner, W. K., eds). Special Publication no. 82-l. Belle W. Baruch Institute for Marine Biology and Coastal Research, Columbia, SC. pp. I-l-I-14. Platt, T. & Jassby, A. D. 1976 The relationship between photosynthesis and light for natural assemblages of coastal marine phytoplankton. Journal of Phycology 12,421430. Platt, T. & Gallegos, C. L. 1980 Modelling primary production. In Primary Productivity in the Sea (Falkowski, P. G., ed.). Plenum Press, New York. pp. 339-361. Platt, T., Gallegos, C. L. & Harrison, W. G. 1980 Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. Journal of Marine Research 38,687-701. Porter, J. W., Woodley, J. D., Smith, G. J., Neigel, J. E., Battey, J. F. & Dallmeyer, D. G. 1981 Population trends among Jamaican reef corals. Nature 294,24%250. Prezelin, B. B. & Matlick, H. A. 1980 Time course of photoadaptation in the photosynthesis-irradiance relationship of a dinoflagellate exhibiting photosynthetic periodicity. Marine Biology 58,85-96. Ralston, M. L. & Jemuich, R. I. 1978 Dud, a derivative-free algorithms for nonlinear least squares. Technometrics 20, 7-14. Rivkin, R. B., Voytek, M. A. & Seliger, H. H. 1982 Phytoplankton Division rates in light-limited environments: two adaptations. Science 215, 1123-l 125.
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Roman, M. R. & Tenore, K. R. 1978 Tidal resuspension in Buzzards Bay, Massachusetts. I. Seasonal changes in the resuspension of organic carbon and chlorophyll a. Estuarine and Coasral Marine Science 6,37-46. Schubel, J. R., Taylor, W. R., Grant, V. E., Cronin, W. B. & Glendenning, M. 1977 Effects of Agnes on the distribution of nutrients in upper Chesapeake Bay. In The Effects of Tropical Storm Agnes on the Chesapeake Bay Estuarine System. CRC Publication no. 54. The Johns Hopkins University Press, Baltimore. pp. 311-319. Schwing, F. B. & Kjerfve, B. 1980 Longitudinal characterization of a tidal marsh creek separating two hydrographically distinct estuaries. Estuaries 3,236-241. Senft, W. H. 1978 Dependence of light-saturated rates of algal photosynthesis on cellular concentrations of phosphorus. Limnology and Oceanography 23,709-718. Smith, N. P. 1978 Longshore currents on the fringe of Hurricane Anita. Journal of Geophysical Research 83, 6047-605 1. Smith, N. P. 1982 Response of Florida Atlantic shelf waters to Hurricane David. Journal of Geophysical Research 81,2007-2016. Smith, C. L., MacIntyre, W. G., Lake, C. A. &Windsor, J. G., Jr 1977 Effects of Tropical Storm Agnes on nutrient flux and distribution in lower Chesapeake Bay. In The Effects of Tropical Storm Agnes on the Chesapeake Bay Estuarine System. CRC Publication no. 54. The Johns Hopkins University Press, Baltimore. pp. 299-310. Technicon Industrial Systems. 1973 Ortho-phosphate in water and sea water. Industrial Method 155-71W. Technicon, Tarrytown, New York. 2 pp. Technicon Industrial Systems 1977 Nitrate and nitrite in water and sea water. Industrial Method 15&71W/A, revised 1977. Technicon, Tarrytown, New York. 2 pp. Turner, R. E., Woo, S. W. & Jitts, H. R. 1979 Phytoplankton production in a turbid, temperate salt marsh estuary. Estuarine and Coastal Marine Science 9,603-613. Wagner, A. J. 1981 Weather and circulation of August 1981. Monthly Weather Review 109,2405-2413. Woodley, J. D. 1980 Hurricane Allen Destroys Jamaican coral reefs. Nature 287,387. Woodley, J. D. et al. 1981 Hurricane Allen’s impact on Jamaican coral reefs. Science 214,749-755. Yentsch, C. M. & Menzel, D. W. 1963 A method for determination of phytoplankton chlorophyll and phaeophytin by fluorescence. Deep-Sea Research 10,221-231. Yeo, R. K. & Risk, M. J. 1979 Intertidal catastrophes: Effect of storms and hurricanes on intertidal benthos of the Minas Basin, Bay of Fundy. Journal of the Fisheries Research Board of Canada 36,667-669. Yoder, J. A., Atkinson, L. I’., Blanton, J. O., Deibel, D. R., Menzel, D. W. & Paffenhofer, G.-A. 1981 Plankton productivity and the distribution of fishes on the southeastern U.S. continental shelf. Science 214,352-353. Zeeman, S. I. Phytoplankton light adaptation in coastal waters. Estuarine, Coastal and SheIf Science (submitted for publication). Zubkoff, P. L. & Warinner, J. E. III. 1977 The effect of Tropical Storm Agnes as reflected in chlorophyll a and heterotrophic potential of the lower Chesapeake Bay. In The Effects of Tropical Storm Agnes on the Chesapeake Bay Estuarine System. CRC Publication no. 54. The Johns Hopkins University Press, Baltimore. pp. 368-388.
Coastal
and Shelf
Science
(1985) 20,403-418
The Effects of Tropical Coastal Phytoplankton
Stephan
Storm
Dennis
I. Zeemad
Marine Science Program and Baruch Institute for Marine Research, University of South Carolina, Columbia, South U.S.A. Received
on
19 December
Keywords: tropical waters; estuaries
I983
and in revised
storms;
form
phytoplankton;
24 May
Biology Carolina
and Coastal 29208,
1984
primary
production;
coastal
The effects of tropical storm Dennis were documented in the coastal waters of South Carolina during August 1981. Phytoplankton photosynthesis vs. irradiance curves showed initial depression of the parameter a followed by three- to five-fold increase of both a and the asymptotic maximum rate of photosynthesis c. Productivity rates were depressed in most samples immediately after the storm. Surface samples at the inshore stations were around 50 mg C me3 h-’ at saturating light intensities, while the offshore station rates were around 10 mg C m - 3 h - r . After a 1O-day lag these rates had increased to about 200 mg C m-3 h-’ inshore and 75 mg C mm3 h-’ offshore. These changes are thought to be primarily caused by changes in species composition. Some of the dominant diatom species changed and dinoflagellate species were introduced. No significant changes in nutrient concentrations were observed. Transient depressions of water temperature, salinity and light intensity may have contributed to the observed changes.
Introduction The southern and eastern coasts of the United States are often subjected to depredations by hurricanes or tropical storms. The onslaught of these weather systems can cause significant damage to natural and manmade features of the region. Although significant amounts of research effort have gone into prediction and damage assessment, very little is known about the effects of hurricanes on aquatic biota, especially phytoplankton. Previous biological studies on the effects of hurricanes have mostly been conducted in coral reef environments (e.g., Woodley, 1980; Porter et al., 1981; Woodley et al., 1981; Knowlton et al., 1981). These studies have mainly dealt with the storm effects on the corals themselves and have only briefly commented on plankton, fish, and algae. Yeo & Risk (1979) studied the effects of Hurricane Beulah on the benthos of the Bay of Fundy. Dobbs & Vozarik (1983) studied pre- and post-storm benthic and water column samples Contribution
574 of the Belle W. Baruch Institute
Research and contribution “Present address: Harbor 33450.
for Marine Biology and Coastal 442 from the Harbor Branch Foundation Inc. Branch Institution, Inc. RR 1, Box 196-A, Ft. Pierce, Florida
403 0272-7714/85/040403
+ 16 $02.00/00
0 1985 Academic
Press Inc. (London)
Limited
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for effects on coastal infauna. One of the most complete studies of tropical storm effects was done by the Chesapeake Research Consortium (1977). In this work, sections by Flemer et al. (1979) and Zubkoff & Warinner (1977) address chlorophyll concentrations in the estuary, while Loftus & Seliger (1977) present results from primary productivity measurements, chlorophyll and species composition. They found the amount of area1 productivity was not altered by the storm, but species composition changed dramatically, and long-term chlorophyll concentrations also changed. A multitude of effects might occur to either enhance or retard the growth of phytoplankton. The input of large amounts of freshwater may stress non-tolerant species or advect them to other regions. The physiological stress may hamper growth rates and eventually lead to local extinctions. Wholesale replacement by more tolerant forms is probably the usual consequence until salinities normalize. Rivers and runoff could enhance nutrient concentrations. In coastal waters nutrients could be upwelled from deeper waters through the action of bottom return-flow in response to seaward surface flows. In coastal waters turbulence might also reintroduce phytoplankton which had previously sunk below the photic depth, or, conversely, mix the phytoplankton downward. Similarly, turbidity might be increased due to resuspension of the bottom sediments. In addition, strong currents associated with storm passage can be a major advective force causing changes in the water masses found at a given location. Such advection could bring in new nutrients as well as new algal populations. In August 1981, I had the opportunity to study the effects of a tropical storm on nearshore environments. Ongoing studies were being conducted on light adaptation of phytoplankton populations in a pristine, high-salinity, saltmarsh estuary and the nearby coastal ocean (Zeeman, submitted). On 19 August, Tropical Storm Dennis passed within 30 miles of the field laboratory of the Belle W. Baruch Institute for Marine Biology and Coastal Research at Georgetown, South Carolina (Figure 1). Winds at the time were reported up to 96.5 km h- ’ (60 mph). This work documents the effects of the storm on the water masses and phytoplankton populations of the North Inlet estuary and the adjacent coastal waters. Photosynthesis-irradiance relationships were measured to assess physiological changes in the algae. In addition, several environmental parameters were also measured to determine which factors may have affected the phytoplankton populations. Experiments were performed along a transect from within the inlet to 8 km offshore. These experiments were conducted both before and after the passage of Tropical Storm Dennis to investigate possible short-term changes. Materials
and methods
The North Inlet estuary (33”20’N, 79”lO’W) is near Georgetown, South Carolina. Reported here are the results of two sampling dates prior to the storm (20 July and 11 August) and four datesafter passageof the storm (23 and 29 August, 27 September and 4 October). Samples were collected along a transect at four stations. Station 1 was located on a major creek about 2 km from the inlet proper. Station 2 was in the mouth of the inlet and station 3 just seaward of the ebb tidal delta. Station 4 was in 10m of water, 8 km offshore. Temperature and conductivity were measured at each station at one meter depth intervals from surface to bottom with a Beckman RS5-3 induction salinometer. Salinities were calculated from these data using the polynomial function of Cox et al. (1976).
-._-
Effects of Tropical Storm Dennis
405
30°
3o”
25’
25’
80’ 85O Figure 1. The path of Tropical Storm Dennis States. The track starts at the southern portion location at 0000 h GMT on 17 August. The GMT, open circles were positions at various
75O 7o” while near or over the continental United of the figure, and the first circle was the filled circles represent positions at 0000 h times.
Density was computed as sigma-t according to the method of Knudsen (1901) as outlined in Kjerfve (1979). Surface current was measured with a biplanar drogue at a depth of 1 m. The surface float of the drogue was attached by a 20-m line to the anchored boat and the drift time was measuredwith a stopwatch. Dye studies showed the drogue to accurately move with the surface waters. Water samplesat each station were collected with standard Niskin bottles and kept in plastic containers for transport to the field laboratory. Samplesfor chlorophyll measurements were collected from the surface, mid-depth, and bottom of the water column. Productivity and nutrient samples were collected at the surface from stations 1 and 2, and at the surface and bottom at stations 3 and 4. Samples for photosynthetic rate measurementswere maintained in darkness from the time of collection until preparation for the experiments, which was usually within 3 h. Upon return to the laboratory, duplicate chlorophyll sampleswere filtered through Whatman GF/F glass fibre filters with magnesium carbonate and frozen. These were later extracted in 900,, acetone with the aid of grinding and analyzed fluorometrically (Yentsch & Menzel, 1963; Holm-Hansen et al., 1965). Permanent mounts of phytoplankton sampleswere prepared using a membrane filter technique (Fournier, 1978). Volumes of 25 to 50 ml were passedthrough 0.45 pm HA Millipore filters. The wet filters were put on microscope slides and cleared with gluteraldehyde by heating to 60°C for 20min (Dozier & Richerson, 1975) then permanently mounted on the slides with a cover slip.
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Nutrient samples were filtered through Whatman GF/F filters and stored frozen in glass scintillation vials. Prior to freezing, the phosphate samples were poisoned with mercuric chloride, the nitrate-nitrite samples poisoned with phenol. These samples were later analyzed with a Technicon Autoanalyzer for nitrate plus nitrite and orthophosphate using standard Technicon methods (Technicon Industrial Systems, 1973, 1977). Photosynthesis versus irradiance (P-I) curves were obtained by using a constant temperature incubator at the field laboratory. Temperature was within 2 “C of the seasurface. Light intensity was provided by a bank of 10 tungsten outdoor spot lamps in the range of about 50 to 900 uEin m- ’ s- ‘. Neutral density plastic screening material provided intensity reduction in steps of about 500,. Excess heat from the lamps was removed by a water filter between the lamps and the incubator. All incubations were started around midday and lasted 4 h. This reduced the possible influence of diurnal rhythms in chlorophyll (Glooschenko et al., 1972) aswell asin the P versus I parameters (Harding et al., 1982; MacCaull & Platt, 1977). Duplicate bottles were incubated from all samplesat five light intensities and also in the dark. Each bottle was injected with 1 to 5 microcuries of 14C sodium carbonate. After incubation the bottles were vacuum filtered (< 180 mmHg) through Gelman GA-6 membrane filters (0.45 urn pore size) and rinsed with filtered seawater. The radioactivity on the filters was determined by liquid scintillation counting. The counting efficiency of each sample was determined by external standard channels ratios using a quench curve prepared from natural plankton populations and 14Ctoluene standard. The P-I relationship is in the shape of a rectangular hyperbola. The initial slope is described by the parameter a while P, is the asymptotic maximum rate of photosynthesis. All photosynthetic rate measurements were normalized to a mg Chlorophyll basis prior to P-I analysis. The P-I parameters, were estimated by a nonlinear least-squarescurve fitting procedure which utilized a derivative-free algorithm (Ralston & Jennrich, 1978). For most of the cases,the model applied to the data was the hyperbolic tangent function of Jassby & Platt (1976). For those casesinvolving photoinhibition, the model of Platt et al. (1980) was used. Lederman & Tett (198 1) have shown that a variety of models would work equally well, although they suggested using the older models. In both models, an additional parameter was specified so asnot to constrain the curves to intercept at zero on the Y axis. This additional parameter was not meant to serve as an estimate of any physiological rate, i.e. respiration, but only to allow better curve fitting. Results
P-I curves were determined for the six sampling dates. In the range of light intensities used, photoinhibition was only observed once. Figure 2 showsthe estimatesof a and the standard error associatedwith each estimate. Values of a were not much different among stations on a given date, but significant changes did occur between dates. Within 4 days after passageof the storm, there was a decrease in a at all stations and at all depths. A week later, on 29 August, the initial slope for all sampleshad increased by a factor of 3 to 5. After this time there was a decline once again to roughly pre-storm values. There was, however, an indication of another increasein October. Estimates of 2 are presented along with their standard errors in Figure 3. The pre-storm and immediate post-storm samplesdid not have different Pi values. However,
407
Effects of Tropical Storm Dennis
0~00
I
’ 20
Jul
I II Aug
I 23
I 29
Aug
Aug
I 27
Sep
4 act
Date
Figure 2. Plot of alpha values shown with + 1 standard error bars (k-station x-station 2; A-station 3s; V-station 3B; G-station 4s; e-station 4B).
1;
10 days after the passageof Tropical Storm Dennis, these values increased by factors of 4 to 5. After this time there was a gradual decline back to pre-storm values. The chlorophyll concentrations (Figure 4) declined in the surface samplesat the nearshore station (3) and in the bottom samplesof the offshore station (4) after the storm. At the sametime, the surface samplesat station 4 showed a slight increase. The other 3 sets of samplesremained constant. There was a decline after August in chlorophyll values at all stations. Productivity rates at saturating light intensities are shown in Figure 5. The mean rates ranged between 8 and 210 mg C mP3 h- ’ . At the three inshore stations maximal rates were cu. 200 mg C mm3h- ’ while the offshore station remained below 85 mg C m- 3h- ‘. A depression of the productivity rates took place in most of the sampleson 23 August, immediately after the storm passed. The most notable feature, however, is the occurrence of a peak on 29 August, which was seenin all samples.The observed changeswere more influenced by changesin the P-I parameters than by chlorophyll concentrations. The data for nitrate-nitrite concentrations are shown in Figure 6 and those for ortho-phosphate concentrations in Figure 7. The nutrient concentrations fluctuated and this was perhaps due to a tidal signature on the estuarine concentrations. High tides generally show low nutrient concentrations within the estuary and low tides have high nutrient concentrations (McKellar er al., 1982). The nutrient samples for 11 August were not taken, thus the second point on the graphs corresponds to immediate poststorm conditions. The nitrate-nitrite concentrations increased within the estuary (stations 1 and 2). A similar, but smaller, increase in the orthophosphate concentrations
408
S. I. Zeeman
50
I
01 20
I
Jul
II Aug
I 23
Aug
I 29
Aug
I 27
Sep
4 act
Date
Figure 3. Plots of the e A-station 3s; V-station
values + 1 standard error bars (W-station 3B; @-station 4s; O-station 4B.
1; x -station
2;
12-
9-
6-
3-
-I
oJUI
Aug
Figure 4. P:ot of the chlorophyll concentrations at each location study period. Arrow indicates day of storm passage.
5ep
sampled
during
the
Effects of Tropical
Stotlon
I
StatIon
,
4
Stotlon
3
I JUI
2
A A 4
stot1on
409
Storm Dennis
Pug
I
4
I Sw
Ott
JUI
4
Sep
act
Figure 5. Primary productivity at saturating light intensities. The arrows indicate the day of storm passage. Circles are surface samples, squares are bottom samples. Bars represent k 1 standard deviation. Where no bars are apparent, symbols are larger than standard deviation.
was also evident at station 1. The second peaks for both nitrate-nitrite and phosphate occurred on 4 and 18 October. The highest concentrations of both nutrients were seen only at station 1, and at this time the orthophosphate peak was relatively greater than the 23 August peak, when compared with the nitrogen results. There was a general rise in the phosphate levels at station 4 after 23 August. Dissolved organic nutrients were not measured for this project. A concurrent study however, collected these data at three locations within the estuary (Long Term Ecological research program). Dr E. Blood has kindly allowed me accessto this information, which is presented in Figure 8. These data were collected daily at 1000 h (EDT) at two sites near stations 1 and 2 in this study, and also at a location on a creek closer to the landward edge of the marsh. Most of the temporal variability is due to sampling at different tidal stages(Kjerfve & McKellar, 1980). The DON and DOP data from the sitesnear stations 1 and 2 showed virtually no storm induced changes, but major fluctuations were evident at the upper marsh site. There were no discernible trends in the ammonium data causedby the storm. Concentrations of all 3 organic nutrients tended to be highest at the upper marsh site and lowest at the site near station 2. Heavy rainfall from the storm decreased the salinity within the estuary, but had little effect on the offshore waters (Figure 9). Salinities within the inlet were already lower prior to the storm event ason 11 August (31.4% vs. 34.3% offshore). Enough freshwater entered the system, due to the storm, to stratify this normally vertically homogenous estuary. On 23 August there was a 4 ppt salinity difference between surface and bottom
410
S. I. Zeeman
Figure study.
JUI
Figure study.
-
6. Plot of the combined nitrate-nitrite Arrow indicates the day of storm passage.
concentrations
WI
7. Plot of the phosphate concentrations found Arrow indicates day of the storm passage.
measured
during
the
during
this
Sep
at locations
sampled
at the innermost station (1). Salinities returned to normal by 29 August, ten days after the storm. Sigma-t values follow the salinity data except that there was a steady rise at the offshore stations (Figure 9). The offshore waters more strongly reflect the intluence of temperature (Figure 9) on sigma-t, while the estuarine waters show the effect of salinity
Efiects of Tropical
Storm
411
Dennis
0
Figure 8. Organic nutrient concentrations (pg-at 1-l) at three estuarine locations (unpublished data, E. Blood). Day 0 is 1 July, storm passage occurred on day 50 (symbols: O-near station 1; O-near station 2; V-upper marsh area).
changes. The density structure of these waters immediately after the storm showed that estuarine (station 1) waters were stratified and distinct from coastal waters, but that mixing near the mouth (station 2) was rapid. Stratification was also evident at station 3 due to lower salinity water from the inlet overlaying higher salinity water from offshore. The plume of low salinity water was not evident at the offshore station (4).
17
:d:
25 -
26
JUI
I
Sep
I
Ott
Jul
%? I
I
Aug
I
I
Station
Sep
2
I
I
Ott
Jul
I Aug
I
Stotion
Sep
3
I Ott
t Jul
I
Figure 9. Plots of salinity, temperature, and sigma-t at each location sampled during the study. of storm passage. Open symbols show bottom samples, closed symbols are surface samoles.
Aug
I
Station
Arrow
Aug
I
Station
I indicates
Sep
4
day
act
Effects of Tropical
Storm
413
Dennis
Figure IO. Plot of daily rainfall measured at a site near the field Inlet. Arrow indicates the day of storm passage.
laboratory
at North
Storm passagebrought on a rapid decline in water temperatures at all stations and causeda reversal of the relative temperature gradient from inshore to offshore (Figure 9). The temperature decline was greatest in the estuary. Ten days after the storm passed,the water column became well mixed from inshore to offshore, with a concomitant rise in temperature. The temperture never reached pre-storm levels, but from this point on continued to decline for the rest of the winter. A thermal gradient had been reestablished by the end of September, but with the coldest temperatures found in the estuary rather than offshore. Precipitation during this period was very heavy, not only in this general vicinity but along the entire coastline of both North and South Carolina (Wagner, 1981). Daily rainfall data for July through September at one site are shown in Figure 10. The highest daily precipitation recorded for any of the 7 rain gaugesin the vicinity of the laboratory was 18.59 cm (7.32 in) on 19 August. The total monthly rainfall for August was ca. 34.3 cm (13.5 in). Dominant phytoplankton species prior to the storm included Rhizosolenia alata, Skeletonema costatum, Thallasiothrix sp. and Ondontella aurita. After the storm the dominant speciesincluded R. alata, S. costatum, Pleurosigmasp., and Coscinodiscus sp. A number of dinoflagellates also appeared after the storm, including Ceratium trichoceros, Gymnodinium sp., and Dinophysis caudata.
Discussion The results of this study document several conditions which occur after the passage of a tropical storm. The major changes observed in this study were in the I? versus I parameters. The initial responsewas a decreasein a. After a lag of at least 4 to 5 days, an
414
S. I. Zeeman
DOY
Figure 11. Amount of sunshine relative to possible sunshine during the month of August. Taken from NOAA weather data at Charleston, South Carolina. Arrow indicates the day of storm passage.
increase in both a and e, after which there is a slow return of both parameters to pre-storm levels. Turner et al. (1979) showed a negative effect of storms on e and also state that flushing of the estuary by storms increasesproduction offshore. The latter may have occurred in this study. However, the productivity increaseat the end of August was observed at all stations and was the result of increasesin the P-I parameters. The usual interpretation of a is that it represents the photochemical processesof the light reactions of photosynthesis. As such, the parameter should be independent of temperature. It may be affected, however, by physiological status of the cells and Platt & Jassby (1976) found that a was also correlated to the light history of the cells. Correlations to salinity have been observed in other studies (Platt & Jassby, 1976), while one response to lowered light intensities is an increase in chlorophyll per cell, which could decreasea (Falkowski, 1980). The time scalesfor changes in the photosynthetic mechanism are on the order of minutes or hours to a few days (Platt & Gallegos, 1980; Prezelin & Matlick, 1980; Jones, 1978). Data on percent of possible sunshine were obtained from the NOAA Environmental Data and Information Service for Charleston, South Carolina. These data, presented in Figure 11, show that there was a period of about a week with heavy cloud cover around the time of the storm. The duration of the decreasedlight intensity wason the sameorder asphotosystem changes,and might thus have had an effect. The other parameter, e, is generally interpreted as representing the dark reactions of photosynthesis. This is an enzyme mediated process and Platt & Jassby (1976) found a positive correlation between temperature and p”,. In addition, Senft (1978) found Pi to be dependent on internal phosphorus concentrations. It is obvious, however, that the temperature during this study could not have been the causeof the rise in I’,,. Nutrient sequestering by the phytoplankton cannot be ruled out after the storm becauseit wasnot measured. However, asdiscussedlater, the external nutrient concentrations did not vary beyond normal levels.
Effects of Tropical
Storm Dennis
415
A more plausible explanation is that the speciescomposition changed in the aftermath of the storm. Examination of permanent mounts of phytoplankton collected at the time of sampling do indeed show population shifts. Phytoplankton populations prior to the storm were almost totally composed of diatoms. After storm passage,diatoms were still the most abundant taxa, but some of the dominant specieshad changed. In addition, there appeared several dinoflagellate species. Loftus & Seliger (1977) also report an abundance of dinoflagellates in ChesapeakeBay after passageof Tropical Storm Agnes. Dinoflagellates have been known to utilize organic substrates for nutrition, and the storm could have enriched the waters with organic compounds through runoff. There was a concentration gradient of DON, DOP and ammonium, which shows runoff to be a source of oganic nutrients. Furthermore, Rivkin et al. (1982) have shown that dinoflagellates may retain high division rates despite low light intensities, or to resume high division rates upon reexposure to higher light. From measurements of chlorophyll concentrations, apparently no drastic changes in the phytoplankton biomass occurred, although a slight decline, evident by the end of September, was possibly related to normal seasonaltrends. From other work, it was also confirmed that the values found during this study are within the normal range for this time of the year (Kjerfve & McKellar, 1980; Zingmark, unpublished data). The chlorophyll concentrations found at the estuarine stations (1 and 2) remained constant during this time and declined only slightly in September, probably asa result of normal seasonaldecline toward winter conditions. The decreaseof chlorophyll in the surface water at station 3 after the storm is the result of low density estuarine water, containing lower chlorophyll concentrations, overlaying offshore water. The higher chlorophyll levels in the bottom waters at station 3 were perhaps the result of turbulence. Bottom waters often have higher pigment concentrations due to resuspension by tidal currents (Roman 8zTenore, 1978), and also due to higher pigment content per cell in response to low light intensities (Falkowski, 1980). The offshore station (4) showed a decreasein chlorophyll levels in the bottom waters with a concomitant increase at the surface. This was due to the breakdown of stratification and turbulent mixing of phytoplankton throughout the water column. Nitrate-nitrite concentrations seemedelevated at stations 1 and 2 immediately after the storm while phosphate was higher only at station 1. The increases, however, were well within the normal ranges for the seasonand may only be a reflection of the tidal stage at which the samples were collected. Other concurrent studies, employing daily sampling, also showed that these nutrient levels are not unusual (Wolaver, unpublished data). The lack of any significant response to a storm by phosphate concentrations has also been documented for the Chesapeake (Flemer et al., 1979; Schubel et al., 1977; Smith et al., 1977). These authors did, however, report increasesof nitrate and nitrite concentrations by factors of 2 to 3 after Tropical Storm Agnes. Slight increasesin phosphate at the offshore station (4) were probably a reflection of the advection of water offshore. The consistent patterns of decreasing nutrient concentrations from station 1 to station 4 indicates that the source of the nutrients was in the estuary rather than the coastal waters (Turner et al., 1979; Yoder et al., 1981). Organic nutrient concentrations, although confined to estuarine samples,also confirm a terrestrial (or at least high marsh) source. The source of the nutrients could be from nutrient regeneration in the sediments, land runoff, precipitation, or exchangeswith the nearby Winyah Bay estuary. Correll (1981) has indicated that land runoff could be a major source of nutrients and
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should not be ignored. Michner & Allen (1982), however, state that freshwater input is minimal in the study area, due to the small size of the drainage basin associated with North Inlet. Examination of the organic nutrient concentrations showed that there was some response to rainfall often after a short lag time (compare Figures 8 and 10). The volume input however seemedsmall since the elevated concentrations were restricted to the site closestto the landward edge of the marsh. The lower concentrations at the other two locations probably indicate the rapid dilution of the runoff. However, biological or chemical binding cannot be ruled out. Recycling of nutrients is probably important in both the estuarine and coastal waters, but the extent of this has not been evaluated for these waters. The nutrient input from precipitation directly was probably small aswas exchange with Winyah Bay. Schwing & Kjerfve (1980) studied a major creek between North Inlet and Winyah Bay. They report finding a nodal point in the creek which limits exchange between the two systems. Nothing definitive can be said of the current patterns during this time since I had no recording current meters. However, the surface currents which had been measured showed no unusual trends. Smith (1978) found that current speed was affected by Hurricane Anita in the Gulf of Mexico but direction remained shore parallel and constant. On the east coast of southern Florida, Smith (1982) found that current patterns inshore and offshore differed during the passageof Hurricane David. He concluded that the inshore site (in 10m of water) was more subject to wind stress while the offshore waters reacted to pressure gradients. This could also have been the casefor my study which was also conducted in waters up to 10 m deep. However, the study sites were not similar in terms of bathymetry. In Smith’s study, the shelf break was much closer to shore and upwelling was observed. In the present study, upwelling at the shelf break probably had no influence becauseof the wide continental shelf (130 km) off the South Carolina coast. In conclusion then, the effects of the storm were a transient depression of water temperature and salinity. No significant changes in nutrient concentrations were observed in the estuary or offshore, although there was an enrichment of DON and DOP at a high marsh site. Depression of the initial slope of the P-I curves were probably related to some form of stress such as low salinities or low light intensities due to prolonged cloud cover. Within ten days, both a and I$ were significantly greater than prior to the storm. The most likely causative factor was a change in speciescomposition. Acknowledgements I wish to thank Drs E. Blood, T. Wolaver and R. Zingmark for accessto unpublished data. D. L. Barker aided in sampling and W. Johnson and S. Hutchinson did the nutrient analyses. Comments on earlier drafts were made by R. A. Gibson, S. Blair and an anonymous reviewer. This research was supported by a pre-doctoral fellowship from the Belle W. Baruch Foundation, the Marine Science Program and U.S.C., NSF grant DEB8O-12165, F. J. Vernberg, project director, and the Harbor Branch Foundation, Inc. References Chesapeake Research Consortium, The. 1977 The effects of Tropical Storm escuarine system, CRC Publication no. 54. The Johns Hopkins University
Agnes on the Chesapeake Bay Press, Baltimore. 639 pp.
Effects
of Tropical
Storm
Dennis
417
Correll, D. L. 1981 Nutrient mass balance for the watershed, headwaters, intertidal zone and basin of the Rhode River estuary. Limnology and Oceanography 26,1142-l 149. Cox, R. A., Culkin, F. & Riley, J. P. 1967 The electrical conductivity/chlorinity relationship in natural sea water. Deep-Sea Research 14,203-220. Dobbs, F. C. & Vozarik, J. M. 1983 Immediate effects of a storm on coastal infauna. Marine Ecology Progress Series 11,273-279. Dozier, B. J. & Richerson, P. J. 1975 An improved membrane filter method for the enumeration of phytoplankton. Verhandlungen internationale Vereinigung fiir theoretische und angewandte Limnologie 19(2), 15241529. Falkowski, P. G. 1980 Light-shade adaptation in marine phytoplankton. In Primary Productivity in the Sea (P. G. Falkowski, ed.). Plenus Press, New York. pp. 99-l 19. Flemer, D. A., Ulanowicz, R. E. & Taylor, D. L. 1979 Some effects of Tropical Storm Agnes on water quality in the Patuxent River estuary. In The Effects of Tropical Storm Agnes on the Chesapeake Bay Estuarine System, CRC Publication no., 54. The Johns Hopkins University Press, Baltimore. pp. 251-287. Foumier, R. 0. 1978 Membrane filtering. In Phytoplankton Manual (Soumia, A., ed.). Monographs on oceanographic methodology 6. UNESCO, Paris. pp. 108-l 14. Glooschenko, W. A., Curl, R. Jr & Small, L. F. 1972 Die1 periodicity of chlorophyll a concentrations in Oregon coastal waters. Journal of the Fisheries Research Boardof Canada 29,1253-1259. Harding, L. W. Jr, Prezelin, B. B., Sweeney, B. M. & Cox, J. L. 1982 Die1 oscillations of the photosynthesis irradiance (P-I) relationship in natural assemblages of phytoplankton. Marine Biology 67, 167-178. Helm-Hansen, O., Lorenzen, C. J., Holmes, R. W. & Strickland, J. D. H. 1965 Fluorometric determination of chlorophyll. 3ournal du Comer’1 International pour 1’Exploration de la Mer 30,3-15. Jassby, A. D. & Platt, T. 1976 Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnology and Oceanography 21,54&547. Jones, R. I. 1978 Adaptation to fluctuating irradiance by natural phytoplankton communities. Limnology and Oceanography 23,920-926. Kjerfve, B. 1979 Measurement and analysis of water current, temperature, salinity, and density. In Estuarine Hydrography and Sedimentation (Dyer, K. R., ed.). Cambridge University Press, Cambridge. pp. 186-226. Kjerfve, B. & McKellar, H. N. 1980 Time series measurements of estuarine material fluxes. In Estuarine Perspectiwes (Kennedy, V. S., ed.). Academic Press, New York. pp. 341-357. Knowlton, N., Lang, J. C., Rooney, M. C. & Clifford, P. 1981 Evidence for delayed mortality in hurricane-damaged Jamaican staghom corals. Nature 294,251-252. Knudsen, M. H. C. 1901 Hydrographical Tables. G.E.C. Gad, Copenhagen. 63 pp. Lederman, T. C. & Tett, P. 1981 Problems in modelling the photosynthesis-light relationship for phytoplankton. Botanica Marina 24,125-134. Loftus, M. E. 81 Seliger, H. H. 1977 A comparative study of primary production and standing crop of phytoplankton in a portion of the upper Chesapeake Bay subsequent to Tropical Storm Agnes. In The Effects of Tropical Storm Agnes on the Chesapeake Bay Estuarine System. CRC Publication no. 54. The Johns Hopkins University Press, Baltimore. pp. 509-521. McCaull, W. A. & Platt, T. 1977 Die1 variations in the photosynthetic parameters of coastal marine phytoplankton. Limnology and Oceanography 22,723-731. McKellar, H. N., Jr, Whiting, G. & Kjerfve, B. 1982 Summer flux of inorganic nitrogen and phosphorus from a southeastern marsh-estuarine ecosystem. Abstract. 45th Annual Meeting of the American Society of Limnology and Oceanography, Raleigh, NC, June 1982. Michner, W. K. 81 Allen, D. M. 1982 Description of study area. In Ecology of Winyah Bay, SC and Potential Impacts of Energy Development (Allen, D. M., Stancyk, S. E. & Michner, W. K., eds). Special Publication no. 82-l. Belle W. Baruch Institute for Marine Biology and Coastal Research, Columbia, SC. pp. I-l-I-14. Platt, T. & Jassby, A. D. 1976 The relationship between photosynthesis and light for natural assemblages of coastal marine phytoplankton. Journal of Phycology 12,421430. Platt, T. & Gallegos, C. L. 1980 Modelling primary production. In Primary Productivity in the Sea (Falkowski, P. G., ed.). Plenum Press, New York. pp. 339-361. Platt, T., Gallegos, C. L. & Harrison, W. G. 1980 Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. Journal of Marine Research 38,687-701. Porter, J. W., Woodley, J. D., Smith, G. J., Neigel, J. E., Battey, J. F. & Dallmeyer, D. G. 1981 Population trends among Jamaican reef corals. Nature 294,24%250. Prezelin, B. B. & Matlick, H. A. 1980 Time course of photoadaptation in the photosynthesis-irradiance relationship of a dinoflagellate exhibiting photosynthetic periodicity. Marine Biology 58,85-96. Ralston, M. L. & Jemuich, R. I. 1978 Dud, a derivative-free algorithms for nonlinear least squares. Technometrics 20, 7-14. Rivkin, R. B., Voytek, M. A. & Seliger, H. H. 1982 Phytoplankton Division rates in light-limited environments: two adaptations. Science 215, 1123-l 125.
418
S. I. Zeeman
Roman, M. R. & Tenore, K. R. 1978 Tidal resuspension in Buzzards Bay, Massachusetts. I. Seasonal changes in the resuspension of organic carbon and chlorophyll a. Estuarine and Coasral Marine Science 6,37-46. Schubel, J. R., Taylor, W. R., Grant, V. E., Cronin, W. B. & Glendenning, M. 1977 Effects of Agnes on the distribution of nutrients in upper Chesapeake Bay. In The Effects of Tropical Storm Agnes on the Chesapeake Bay Estuarine System. CRC Publication no. 54. The Johns Hopkins University Press, Baltimore. pp. 311-319. Schwing, F. B. & Kjerfve, B. 1980 Longitudinal characterization of a tidal marsh creek separating two hydrographically distinct estuaries. Estuaries 3,236-241. Senft, W. H. 1978 Dependence of light-saturated rates of algal photosynthesis on cellular concentrations of phosphorus. Limnology and Oceanography 23,709-718. Smith, N. P. 1978 Longshore currents on the fringe of Hurricane Anita. Journal of Geophysical Research 83, 6047-605 1. Smith, N. P. 1982 Response of Florida Atlantic shelf waters to Hurricane David. Journal of Geophysical Research 81,2007-2016. Smith, C. L., MacIntyre, W. G., Lake, C. A. &Windsor, J. G., Jr 1977 Effects of Tropical Storm Agnes on nutrient flux and distribution in lower Chesapeake Bay. In The Effects of Tropical Storm Agnes on the Chesapeake Bay Estuarine System. CRC Publication no. 54. The Johns Hopkins University Press, Baltimore. pp. 299-310. Technicon Industrial Systems. 1973 Ortho-phosphate in water and sea water. Industrial Method 155-71W. Technicon, Tarrytown, New York. 2 pp. Technicon Industrial Systems 1977 Nitrate and nitrite in water and sea water. Industrial Method 15&71W/A, revised 1977. Technicon, Tarrytown, New York. 2 pp. Turner, R. E., Woo, S. W. & Jitts, H. R. 1979 Phytoplankton production in a turbid, temperate salt marsh estuary. Estuarine and Coastal Marine Science 9,603-613. Wagner, A. J. 1981 Weather and circulation of August 1981. Monthly Weather Review 109,2405-2413. Woodley, J. D. 1980 Hurricane Allen Destroys Jamaican coral reefs. Nature 287,387. Woodley, J. D. et al. 1981 Hurricane Allen’s impact on Jamaican coral reefs. Science 214,749-755. Yentsch, C. M. & Menzel, D. W. 1963 A method for determination of phytoplankton chlorophyll and phaeophytin by fluorescence. Deep-Sea Research 10,221-231. Yeo, R. K. & Risk, M. J. 1979 Intertidal catastrophes: Effect of storms and hurricanes on intertidal benthos of the Minas Basin, Bay of Fundy. Journal of the Fisheries Research Board of Canada 36,667-669. Yoder, J. A., Atkinson, L. I’., Blanton, J. O., Deibel, D. R., Menzel, D. W. & Paffenhofer, G.-A. 1981 Plankton productivity and the distribution of fishes on the southeastern U.S. continental shelf. Science 214,352-353. Zeeman, S. I. Phytoplankton light adaptation in coastal waters. Estuarine, Coastal and SheIf Science (submitted for publication). Zubkoff, P. L. & Warinner, J. E. III. 1977 The effect of Tropical Storm Agnes as reflected in chlorophyll a and heterotrophic potential of the lower Chesapeake Bay. In The Effects of Tropical Storm Agnes on the Chesapeake Bay Estuarine System. CRC Publication no. 54. The Johns Hopkins University Press, Baltimore. pp. 368-388.