4.1. Overall changes and potential effects
In general, K. brevis was more abundant nearshore than offshore and became more abundant from 1954-1963 to 1994-2002. Overall, concentrations increased approximately 13-18-fold and the blooms extended farther offshore. K. brevis occurred at relatively high concentrations for more months of the year in 1994-2002 relative to 1954-1963, occurring earlier in the fall and extending on through the winter and into the spring.
This extension of the K. brevis
blooms into the spring months causes two problems today that were much less of a problem in the past. Late winter and early spring is the prime time for tourists from more northern latitudes to visit Florida. The higher incidence and abundance of K. brevis
, with the associated irritating aerosols and fish kills, during this time period can cause problems to the local tourist industry and economy. Springtime is also when West Indian manatees (Trichechus manatus latirostris
) migrate from the estuaries back into the coastal waters (Landsberg and Steidinger, 1998
; Landsberg, 2002
). Half a century ago, K. brevis
was usually not very abundant at this time (Figs. and ). As a result of K. brevis
occurrence now extending more into the spring in recent years, many manatees are now being exposed to brevetoxin and dying (Landsberg and Steidinger, 1998
; Florida Fish and Wildlife Research Institute, 2006
The concentration frequency spectra () indicated that all concentration categories above the 103
background level, not just the lethal bloom concentrations, have increased over time. The significant increase in these sublethal concentrations of K. brevis
could have serious implications. These concentrations are not high enough to kill organisms directly, but perhaps allow for the accumulation of the brevetoxin in their tissues. Biomagnification of this lipid-soluble toxin through the food web could lead to rather high concentrations at higher trophic levels. Flewelling et al. (2005)
have argued that this scenario may explain the mortality of many bottlenose dolphins (Tursiops truncatus
) and West Indian manatees (Trichechus manatus latirostris
) along the west Florida coast in recent years in areas where no large blooms of K. brevis
could be found at the time. The high concentrations of brevetoxins observed in the tissues and stomach contents of the marine mammals suggested trophic transfer and biomagnification of brevetoxin (Flewelling et al., 2005
). This evidence, along with the observed increase in frequency of sublethal concentrations of K. brevis
from 1954-1963 to 1994-2002 () suggests a possible increasing threat to seafood safety in west Florida coastal waters.
4.3. Sampling bias
While the data available (Florida Fish and Wildlife Research Institute, 2002
) do not indicate the sampling strategies employed, it is almost certain that at least some of the sampling was not unbiased, but rather the result of searches for K. brevis
blooms to sample and study, leading to an overestimate of its true average abundance. There was no evidence that sampling bias was so much more severe in 1994-2002 than 1954-1963 that it could result in a 13-18-fold increase in estimated biomass. Indeed, it is more likely that there was more bias intheearly days of K. brevis
research to collect samples for examination of the newly discovered toxic dinoflagellate as a source of fish kills, and less bias in more recent times with more emphasis on objective oceanographic sampling. The data on seasonal sampling bias indicated relatively little bias during the 1954-1963 and 1994-2002 periods and no significant difference between the two in monthly sampling variability (both had a coefficient of variation of 28%).
Another potential bias that must be considered is often called “the observer effect”. As there were many more people along the coast and out on the water in 1994-2002 than 1954-1963, more K. brevis blooms could have been reported in the later years that might have gone unnoticed a half-century earlier. A comparison of the number of samples taken indicated no major differences between the 1954-1963 and 1994-2002 periods (2158 and 3312 samples, respectively). Furthermore, all data were normalized to number of samples, so it does not affect the estimated concentration of K. brevis.
To avoid the potential problem of more samples being taken during obvious blooms than when no blooms occur, the data were also binned by month and monthly averages used to compare 1954-1963 to 1994-2002 average concentrations. This analysis showed an 18-fold increase that was highly significant.
One possible bias is the use of remote sensing for the detection of K. brevis blooms, a technology not available in 1954-1963. This is definitely a possibility farther offshore where K. brevis is sparse and not noticed by many people. This is less probable along the shoreline where there is routine sampling whether remote sensing shows the presence of K. brevis or not. Furthermore, people in the 1950s did not need remote sensing to detect red tide along the shoreline because of the observations of dead fish and noxious aerosols. As a result, one would expect remote sensing capabilities to lead to a bias offshore but not along the shoreline. Examination of only data below the remote sensing detection limit of 105 cells L-1 (, ) indicated that any potential remote sensing bias alone cannot explain the large increase in average K. brevis concentration.
The increase in the frequency of K. brevis occurrence at concentrations that are elevated but not noticeable to remote sensing or the human eye (103 to 105 cells L-1), as seen in the concentration frequency spectra () also indicated that sampling bias, the observer effect, and remote sensing bias alone cannot explain the large increase in K. brevis concentrations. It also cannot explain the change in the seasonal pattern in K. brevis occurrence. It is concluded that the apparent increase in K. brevis abundance is real.
4.4. Long term changes or oscillations in the ecosystem
While using the average of a decade of data helps average out the year to year variability in K. brevis
occurrence and concentration, one cannot rule out some long term natural change or oscillation in factors that influence the ecology of K. brevis
. For example, one possibility is that the North Atlantic Oscillation, Atlantic Multidecadal Oscillation, or periodicity in hurricane activity could ultimately influence the population dynamics of K. brevis
. An examination of the timing of those oscillations (Enfield et al., 2001
; Stenseth et al., 2002
; Chavez, 2004
; Trenberth, 2005
) however indicates that the 1954-1963 and 1994-2002 periods are approximately in phase, not out of phase with each other. This does not preclude some other oscillatory phenomenon from causing K. brevis
to be less prevalent in 1954-1963 than 1994-2002, but we know of none at the present time.
Another possible hypothesis is that the increase in water temperature and change in water mass structure over the past half-century (Houghton et al., 2001
; Rayner et al., 2003
; Sheppard and Rioja-Nieto, 2005
) caused a shift in community structure, but our understanding of it is too poor to document such a change and demonstrate a mechanism by which it could lead to an increase in K. brevis
. Any change in the ecosystem is just as likely to cause a decrease in K. brevis
as an increase.
The decline of nekton on the west Florida shelf as a result of fishing pressure has probably affected community structure as a result of “top down controls”, but again, no specific mechanism can be identified that would predict an increase in K. brevis
as a result. One can envision ways in which changes in temperature and community structure could lead to reduced grazing or competition from other phytoplankton species, but one can just as easily envision exactly the opposite. Furthermore, peak blooms of K. brevis
tend to become almost monospecific (Steidinger and Vargo, 1988
), so the observed increase over a half-century is not just a shift toward K. brevis
being a larger proportion of the phytoplankton community. Overall K. brevis
biomass is higher and that implies higher nutrient availability.
Because most of the nutrients available end up in the biomass of K. brevis
as the bloom matures and becomes almost monospecific (Steidinger and Vargo, 1988
), the amount of available nutrients determines the maximum biomass of K. brevis
that can develop. The 13-18-fold increase in K. brevis
abundance from 1954-1963 to 1994-2002 () and the increase in the highest achieved concentrations imply an increase in nutrient availability.
Lenes et al. (2001)
and Walsh and Steidinger (2001)
have hypothesized that iron-rich dust from North Africa stimulates the growth of Trichodesmium
, which in turn enriches the ecosystem with nitrogen by way of nitrogen fixation. This hypothesis appears quite plausible. It is less clear that it can explain a 13-18-fold increase in K. brevis
over a half-century or the much higher concentrations within 5 km of the coastline. Prospero and Lamb (2003)
estimate that there may have been as much as a 4-fold increase in dust from Africa from 1950s to 1980s and no significant changes throughout the 1980s and 1990s. This increase could be a contributor to the increase in K. brevis
abundance. As African dust is spread throughout the West Florida Shelf, however, this hypothesis does not explain why concentrations of K. brevis
are much higher a long the shoreline than farther offshore (). While iron could be a limiting nutrient offshore, it is unlikely to be a limiting nutrient in the shallow waters along the coastline. Because of large amounts of iron supplied by land runoff and sediments, additional iron from African dust is probably insignificant inshore.
We know of no natural sources of nutrients that have increased 13-18-fold. The most plausible hypothesis for a large increase in nutrient availability is that the large increase in human activities in South Florida is involved. The large increase in the human population along the southwest coast of Florida () would be expected to produce more sewage, more disturbance of terrestrial and wetlands ecosystems and their ability to sequester nutrients, and more land surface runoff. There has also been a large increase in agriculture, fertilizer use, mining of phosphate deposits, and oxidation of nitrogen-rich organic peat (McPherson and Halley, 1996
). While we do not have historical data on fertilizer use in the watershed of the southwest Florida coast, nationwide trends probably reflect the changes in Florida reasonably well. Heimlich (2003)
found that 2.7 million tonnes of nitrogen fertilizer was used in 1960 and 11.4 million tonnes were used in 1980 in the United States. The amount of fertilizer used after 1980 remained about the same through to 1998.
The 4-fold enlargement of the Caloosahatchee River watershed () alone would have also greatly increased the nutrient load to the coastal waters. The release of buried nutrients as a result of draining the northern Everglades, which led to oxidation of the organic peat and release of the associated nutrients, has been a major factor in the eutrophication of many areas of South Florida, including Lake Okeechobee (Brand, 2002
; Steinman et al., 2002
), and thus the Caloosahatchee River and coastal waters downstream.
The similar seasonal pattern of flow down the rivers () and K. brevis (), with the peak in K. brevis prevalence a couple of months after the peak river flow, is suggestive. It is important to recognize that these are just averages over many years, and river runoff does not necessarily result in a K. brevis bloom each year. The timing of individual blooms is actually quite sporadic from year to year. The sporadic timing suggests local physical circulation, species competition, and ecosystem processes determine whether or not a bloom of K. brevis develops. River flow and nutrient availability may determine how large a K. brevis bloom can become once other environmental circumstances allow it to outcompete other phytoplankton species and develop.
Interestingly, a comparison of seasonal flow in the 1994-2002 period with the 1964-1973 period (1954-1963 data are not available) for the Caloosahatchee River () indicated the same increase and extension into late winter and spring as seen in K. brevis
seasonality (Figs. and ). The data suggest that increased flow down the Caloosahatchee River in the winter and spring may be related to increased K. brevis
downstream in the winter and spring. Interestingly, Gunter and Hall (1962)
recognized the potential problem, but argued that increasing the flow of water from Lake Okeechobee down the Caloosahatchee River in spring would not increase K. brevis
abundance because it occurs in the fall. The long-term data suggest that increasing flow in the spring has changed the timing of K. brevis
occurrence, so that it now often occurs in both the fall and spring.
Comparison of the average monthly flow through S79 on the Caloosahatchee River between the 1964-1973 and 1994-2002 time periods. Data before 1964 are not available. Data from South Florida Water Management District.
Few long term records are available, but Turner et al. (2006)
found over a 10-fold increase in both nitrate in the Peace River and sediment chlorophyll in Charlotte Harbor at the mouth of the Peace River from 1960 to 1980. In sediment cores dated back 200 years, sharp increases in organic carbon, nitrogen, phosphorus, and biogenic silica were observed after 1950 (Turner et al., 2006
). The data indicate that nutrient enrichment has occurred in these coastal waters.
Hu et al. (2006)
have argued that nutrients from rivers along the west coast of Florida alone are insufficient to generate the recent large blooms of K. brevis
and that groundwater flow is a likely major source of nutrients. While estimating the actual flux of nutrients into coastal waters by groundwater is much more difficult than the flux of river input, it is well established that the flux of nutrients through groundwater is a significant source of nutrients to coastal waters (D’Elia et al., 1981
; Simmons, 1992
; Moore, 1999
; Paytan et al., 2006
) and should not be ignored. Miller et al. (1990)
demonstrated the importance of groundwater flow in Charlotte Harbor near the mouth of the Peace River. Scott et al. (2006)
found approximately a 20-fold increase in nitrate concentrations in 13 of Florida’s largest springs from 1992 to 2001, indicating a large increase in groundwater nutrients.
Hu et al. (2006)
argued that river flow could only provide 20-30% of the nitrogen needed to generate the K. brevis
bloom observed in 2004-2005, but acknowledged the calculation was based only upon inorganic nitrogen, and that organic nitrogen could provide some unknown additional amount of nitrogen to K. brevis
blooms. Using the nutrient bioassay methods of Brand (2002)
, we have estimated the total amount of nitrogen available to phytoplankton in the Caloosahatchee and Peace Rivers is approximately two to three times larger than just the inorganic nitrogen (Brand and Compton, unpublished data). These are the two large strivers along the south west coast of Florida (). Furthermore, in addition to river flows, non-point source flows along the coastline, which is now highly developed in southwest Florida, must also be considered. This does not diminish the potential importance of groundwater fluxes, but does indicate that surface runoff is not necessarily minor. We suspect a combination of river flow, non-point source inputs, and groundwater provide sufficient nutrients to generate the K. brevis
blooms observed inshore.
A factor that may be enhancing the effects of land runoff of nutrients is reduced advection due to a persistent transport barrier (Yang et al., 1999
; Olascoaga et al., in press
) in the nearshore waters where K. brevis
is most prevalent (). The long residence time inshore could allow for the buildup of both nutrients and K. brevis
We hypothesize that the many decades of increased nutrient flux to the coastal ecosystem from land have increased the nutrient pool in this ecosystem. These nutrients can be stored in sediments, detritus, and long-lived macroalgae and seagrasses. The data of Turner et al. (2006)
on increasing sediment nutrients, and Lapointe and Bedford (in press)
on increasing amounts of macroalgae in these coastal waters support this hypothesis. We hypothesize that this large reservoir of nutrients on the West Florida Shelf ultimately allows for the development of blooms with nutrient requirements that exceed the actual input of nutrients at any given time. This could explain why estimates of nutrients from river flow alone (Vargo et al., 2004
; Hu et al., 2006
) appear to sometimes be insufficient to support some of the largest blooms. It is hypothesized that processes currently not understood allow for the eventual transfer of nutrients from these benthic pools to K. brevis
under certain circumstances, promoting its increase in biomass. Walsh et al. (2001)
and Walsh and Steidinger (2001)
have also suggested that benthic nutrient sources play an important role in the development of K. brevis
blooms. A long-term increase in the benthic nutrient pool could then lead to an overall increase in planktonic K. brevis
Another factor to consider is the life cycle of K. brevis
. The entire life cycle of K. brevis
is not known, but a benthic stage is suspected (Steidinger et al., 1998
). If this is the case, elevated benthic nutrients could also be enhancing benthic populations of K. brevis
, ultimately leading to the larger planktonic populations observed.
For blooms that start offshore (Tester and Steidinger, 1997
; Steidinger et al., 1998
; Walsh and Steidinger, 2001
), the initial bloom may not be supported by nutrients from land runoff, but we hypothesize that land-based nutrients contribute to the much higher K. brevis
concentrations found inshore (Figs. and ) once the blooms have been transported inshore. The association of high K. brevis
abundance with high silicate concentrations in all four blooms they examined led Vargo et al. (2004)
to conclude that local estuaries were a significant source of nutrients to the blooms.
The complete life cycle of K. brevis, the exact pathways of nutrients leading to K. brevis populations, and how K. brevis can outcompete other faster growing phytoplankton species under certain circumstances are not known. Nevertheless, the large increase in K. brevis abundance over the past 50 years requires a large increase in nutrient availability. We hypothesize that the large increase in human activities in South Florida in the past 50 years is ultimately the major source of these additional nutrients. The much higher concentrations of K. brevis inshore than off shore also support the hypothesis that nutrient inputs from land are a major factor.