Grantee Research Project Results
Final Report: Grazing and Windows of Opportunity for Dinoflagellate Blooms
EPA Grant Number: R829366Title: Grazing and Windows of Opportunity for Dinoflagellate Blooms
Investigators: Stoecker, Diane K. , Boicourt, William C. , Roman, Michael R.
Institution: University of Maryland Center for Environmental Science , Horn Point Laboratory
EPA Project Officer: Packard, Benjamin H
Project Period: January 1, 2002 through December 31, 2004
Project Amount: $428,184
RFA: Ecology and Oceanography of Harmful Algal Blooms (2001) RFA Text | Recipients Lists
Research Category: Water , Aquatic Ecosystems
Objective:
When conditions (light, temperature, nutrients) are suitable for dinoflagellate growth, grazing may prevent population increases and bloom formation. The objectives of this research project were to: (1) determine if “windows of opportunity” occur when and where grazing pressure is low on small (< 25 μm) dinoflagellates; (2) determine if these windows are a necessary condition for the initiation of blooms; and (3) define the physical and chemical conditions that can create these windows.
Our goal was to test the following hypotheses:
- Microzooplankton community grazing is greater than mesozooplankton community grazing on small (< 25 μm) dinoflagellates.
- Microzooplankton community grazing coefficients (g) are usually higher than growth rates (μ) of small dinoflagellates and prevent net population growth.
- Blooms occur when, in addition to environmental conditions being conducive to growth, there is a window of reduced grazing pressure in which μ is greater than g. There is no bloom if g is greater than μ.
- Windows occur following the spring diatom bloom because microzooplankton that consume dinoflagellates are low in abundance because of lack of appropriate sized food and top down control by copepods.
- Windows occur after influxes of freshwater that alter boundaries between oligohaline and mesohaline waters. Transition areas that have sufficient nutrients and light, but where densities of microzooplankton grazers are low, support blooms.
Summary/Accomplishments (Outputs/Outcomes):
Our investigation was based on a combination of in situ observations, sampling, and microzooplankton and copepod grazing experiments in two subestuaries of the Chesapeake Bay, the Choptank, and Patuxent Rivers. Blooms of potentially harmful small dinoflagellates, including Prorocentrum minimum (= P. cordatum) and Karlodinium veneficum (= K. micrum, Gyrodinium galatheanum) are common during mid to late spring in these rivers. We conducted conductivity, temperature, and depth (CTD) casts at all stations (Figure 1) to determine temperature, salinity and if a chlorophyll maximum layer was present. Data were used to describe water column structure and used in combination with other data to calculate residence times. At lower, middle, and upper stations in each river, samples were collected for inorganic nutrients, chlorophyll a, phytoplankton (including small dinoflagellates, which were identified to species), microzooplankton, and mesozooplankton. Microzooplankton and copepod grazing experiments were conducted with water samples and organisms from the lower, middle, and upper stations (Figure1).
Figure 1. Sampling Stations. Circles indicate biological sampling and CTD stations; triangles indicate CTD stations.
To determine if windows of low grazing pressure on small dinoflagellates occurred, microzooplankton potential grazing experiments were conducted with natural plankton assemblages from the “biological” stations. Cultures of the dinoflagellates P. mimimum and K. veneficum were labeled with the fluorescent stain CellTrackerTM Green CMFDA. Live, labeled P. minimum and K. veneficum cells were used as potential prey for the natural microzooplankton assemblages at target concentrations of approximately 500 cells mL-1 to determine the strength of top-down control by microzooplankton grazing. Grazing experiments with copepods were conducted with natural microplankton assemblages from the biological stations to determine the clearance rates for 10 μm or greater phytoplankton (size category that includes small dinoflagellates) and microzooplankton. The individual copepod clearance rates were combined with the copepod abundance to estimate copepod community grazing impact on both dinoflagellates and microzooplankton.
During our project, freshwater flow in the Choptank and Patuxent Rivers was unusually low in spring 2002, a record drought year (below average flow), and 2003, an extreme wet year (above average flow) (Figure 2). In 2004, spring flow was similar to long-term mean flow. These differences in flow were reflected in the relatively high salinity, low inorganic nutrients, low turbidity, and low chlorophyll levels in 2002 and low salinity, high inorganic nutrients, high turbidity, and high chlorophyll in 2003. Spring 2004 was a more “normal” year in terms of freshwater flow, nutrients, and chlorophyll. Both tributaries exhibited a rapid return to better water quality, compared to the recent past, during the record dry year. This is because nutrient delivery from the watershed to the estuary is linked to freshwater flow. During our study there were large differences from year to year in water structure, residence time, nutrient availability, light availability, and trophic structure in the two estuaries.
Although large, extensive blooms of small dinoflagellates (primarily P. mimimum and K. veneficum) have occurred historically in both tributaries in late spring, we did not observe a large bloom during our investigation. In the dry year (2002), the abundance of small dinoflagellates was low (Table 1). In the wet year (2003), P. minimum and K. veneficum formed small blooms that were observed at some of the stations (Table 1). Surprisingly, in 2004, the more “average” year, dinoflagellates abundances remained low. We did not get the blooms we expected.
We evaluated the factors that regulated dinoflagellate net population growth during the three very different years. The maximum growth coefficients (μ) reported for P. mimimum and K. veneficum are 1.4 and 0.9/day. In situ growth conditions, however, are seldom ideal, and growth rates in nature are thought to be lower most of the time than the maximum obtained in culture because of light, nutrient, and temperature limitations in nature. During the dry year, availability of inorganic nutrients limited phytoplankton biomass. Potential microzooplankton community grazing on P. mimimum and K. veneficum was high, with average rates between 0.3 and 7.6/day (Table 2). In the “nutrient-limited” year, top-down regulation by microzooplankton grazing was strong.
Figure 2. Mean Stream Flow as Recorded at U.S. Geological Survey (USGS) Stream Gages (Data From USGS). The long-term mean for the Patuxent encompasses 25 years of data and 55 years of data for the Choptank. Stream flow in 2004 is not shown, as the mean 3-month flow is indistinguishable from the long-term mean when graphed.
Tributary | Year | P. minimum | K. veneficum | ||
| Mean (SD) | Max | Mean (SD) | Max | |
Choptank | 2002 | 22(30) | 127 | 22(59) | 253 |
2003 | 9,021(37,100) | 178,879 | 128(172) | 575 | |
2004 | 69(144) | 633 | 116(288) | 1,152 | |
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Patuxent | 2002 | 42(61) | 160 | 8(7) | 18 |
2003 | 7,210(13,159) | 35,515 | 1,086(1,394) | 5,221 | |
2004 | 118(190) | 551 | 112(444) | 1,836 |
Tributary | Year | Month | Grazing Coef. , g/d (SD) | |
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| P. min | K. ven | |
Choptank | 2002 | Mar | 0.3(0.34) | 0.5(0.36) |
| Apr | 0.4(0.53) | 0.3(0.38) | |
| May | 0.6(1.01) | 0.4(0.65) | |
2003 | Mar | 0.2(0.90) | 0.1(0.04) | |
| Apr | 0.5(0.74) | 0.6(0.93) | |
| May | 1.2(1.57) | 1.0(1.08) | |
2004 | Mar | nd | nd | |
| Apr | <0.0 | <0.0 | |
| May | 0.2(0.31) | 0.3(0.25) | |
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Patuxent | 2002 | Mar | 1.5(0.06) | 1.6(0.33) |
| Apr | 0.4(0.54) | 0.7(1.10) | |
| May | 7.6(1.21) | 0.7(0.68) | |
2003 | Mar | 0.5(0.29) | 0.2(0.25) | |
| Apr | 2.4(2.28) | 0.3(0.47) | |
| May | 0.14(0.22) | 0.08(0.11) | |
2004 | Mar | nd | nd | |
| Apr | <0.00 | 0.1(0.03) | |
| May | na | na |
During 2003, the wet year, inorganic nitrogen was abundant, but we did not observe large, extensive dinoflagellate blooms, only mini-blooms. Light limitation, caused by cloudy weather and turbidity, and low residence times helped limit net growth of dinoflagellate populations. Top-down control by grazing was again an important loss factor. A bloom of the small dinoflagellates, Heterocapsa spp., was in progress when we started sampling in March 2003, but the bloom declined rapidly. Calculation of the copepod community grazing impact indicated that copepod grazing was an important source of mortality to Heterocapsa populations (Figure 3). Copepod grazing appeared to be a relatively insignificant source of mortality to dinoflagellates during late spring (Figure 3).
Figure 3. Calculated Grazing Pressure of Adult Copepods on Phytoplankton (Top Panel) and Heterocapsa Abundance (Lower Panel), Choptank River, 2003. Mean (SD).
During late April and early May 2003, microzooplankton grazing pressure on small dinoflagellates was high but spatially variable. Microzooplankton grazing appeared to inhibit the development of a K. veneficum bloom in the Choptank in May (Figure 4). Although average microzooplankton grazing on P. minimum also was high in late April and early May, a short duration, low-density bloom of this dinoflagellate did occur in mid-May in the Choptank River (Figure 5). Spatial variability in dinoflagellate populations, grazing pressure and residence time may allow mini-blooms to develop even when average microzooplankton grazing pressure in high. Once high prey densities are present, grazers become food saturated and community grazing coefficients decline (Figure 5, mid-May data). Although microzooplankton grazing may slow or prevent net growth of dinoflagellate populations in the early stages of bloom formation, at the peak of blooms, grazing probably has little impact. Once dinoflagellate densities decline, microzooplankton grazing is again an important loss factor (Figure 5, end of May).
Figure 4. Microzooplankton Potential Grazing Pressure on K. veneficum (Top Panel) and K. veneficum Abundance (Lower Panel), Choptank River, 2003. Mean (SD).
Figure 5. Microzooplankton Potential Grazing Pressure on P. minimum (Top Panel) and P. minimum Abundance (Lower Panel), Choptank River, 2003
In 2004, although flow conditions were “intermediate” and should have been suitable for dinoflagellate population growth, dinoflagellate populations remained low (Table 1). We cannot ascribe this to grazing control, because potential grazing coefficients were lower than in the previous two years (Table 2). We do not know why there was a lack of numerical response in dinoflagellate populations.
One of our goals was to test the hypothesis that high copepod abundance can result in top-down control of microzooplankton and hence release of small dinoflagellates from microzooplankton grazing pressure (i.e., a trophic cascade). In the dry year (2002), copepod populations were very low (Figure 6) and removed a calculated maximum of 3 percent of the microzooplankton standing stock daily (Figure 7). Although chlorophyll levels were relatively low for the tributaries, microzooplankton standing stocks still were high (Figure 6) and, in particular, large algivorous ciliates were adundant. During the wet year, copepod standing stocks were about 40 times higher than in the previous dry year, and copepods were estimated to consume a large proportion of the microzooplankton standing stock daily (Figure 7). Large algivorous ciliates were rare in 2003. It is likely that the lack of a strong numerical response of microzooplankton populations to the increased phytoplankton resources in the wet year (2003) was at least partially caused by top-down control of microzooplankton by copepod predation during the spring. The relationship of biomass components (phytoplankton, microzooplankton, copepods) differed greatly among the three years (Figure 6) and suggest relatively tight coupling of microzooplankton to phytoplankton in the dry year and less control in the wetter (more eutrophic) years.
Figure 6. Estimated Biomass Of Phytoplankton (Grey-Filled Squares), Microzooplankton (Black -Filled Squares) and Copepods (Open Squares) Spring 2002 (Dry Year), 2003 (Wet Year), and 2004 (Normal Year). Data from Choptank and Patuxent combined. Percent change in populations from dry to wet year is shown in the left bottom corner and from wet to normal year in the right bottom corner.
Figure 7. Calculated Average Percentage of Microzooplankton and Large Phytoplankton (> 10 μm) Phytoplankton Standing Stock Removed d-1 by Adult Copepod Grazing. Statistical differences between 2002 (dry) and 2003 (wet) year are denoted by * (p < 0.05) and **(p < 0.005).
The patterns of relative biomass among years suggests that high freshwater flow and the linked nutrient delivery from the watershed favor high phytoplankton biomass, including blooms of small cell-size dinoflagellates, not only because it increases the amount of biomass that can be supported but also because top-down control by microzooplankton during the spring is weakened because of predation on microzooplankton by copepods. This pattern may be reversed in the summer. Phytoplankton blooms and high copepod biomass during spring can lead to high biomass of ctenophores and other gelatinous zooplankters that prey on copepods during the summer. This change in the number of trophic levels could lead to a relative relaxation of copepod grazing pressure on microzooplankton and hence increased microzooplankton grazing on small dinoflagellates during the summer. These scenarios do not apply to top-down control of large cell-size, summer–blooming dinoflagellates (such as Akashiwo sanguinea and Ceratium furca) as they should be less susceptible to microzooplankton grazing.
Figure 8. Electron Micrographs of Toxic Pseudo-nitzschia spp. From the Choptank River. A, B, E = P. fraudulenta; C,D, F = P. multiseries. P. callinantha also was observed in samples from the Choptank. Scale bar = 1 micron in A,B,C, and D; scale bar = 5 microns in E and F.
One unexpected finding was that in 2002, the dry year, there was an increased abundance of the diatoms in the genus Pseudo-nitzschia. Some Pseudo-nitzschia spp. produce the neurotoxin domoic acid. Several toxic species were observed in samples from the “windows” cruises (Figure 8) and toxic strains were isolated. The production of domoic acid was confirmed by amnesic shellfish poisoning competitive enzyme-linked immunosorbent assay, high performance liquid chromatography, and mass spectrometry. In 2003 and 2004, toxic strains were once again isolated. These are the first reports of toxic Pseudo-nitzschia inthe Chesapeake Bay region.
Journal Articles:
No journal articles submitted with this report: View all 22 publications for this projectSupplemental Keywords:
marine, estuary, ecosystem, aquatic, marine science, ecology, Chesapeake Bay, East Coast, ecological risk assessment, oceanography, algal blooms, Choptank River, HAB ecology, Patuxent River, dinoflagellate blooms, dinoflagellates, ecology, estuaries, grazing and window opportunities,, RFA, Scientific Discipline, Geographic Area, Water, Ecosystem Protection/Environmental Exposure & Risk, State, Oceanography, algal blooms, Ecological Risk Assessment, Ecology and Ecosystems, Biology, Chesapeake Bay, East Coast, microbiology, dinoflagellates, estuaries, ecology, Patuxent River, HAB ecology, Choptank River, Maryland (MD), water quality, grazing and window opportunitiesProgress and Final Reports:
Original AbstractThe perspectives, information and conclusions conveyed in research project abstracts, progress reports, final reports, journal abstracts and journal publications convey the viewpoints of the principal investigator and may not represent the views and policies of ORD and EPA. Conclusions drawn by the principal investigators have not been reviewed by the Agency.