Gulf of Mexico Science Volume 25 Article 5 Number 1 Number 1
2007 The nI vasive Cyanobacterium Cylindrospermopsis raciborskii in Southern Louisiana Hans J. Rick
Silke Rick
Soledad Fuentes University of Louisiana-Lafayette
Jodie L. Noel University of Louisiana-Lafayette
DOI: 10.18785/goms.2501.05 Follow this and additional works at: https://aquila.usm.edu/goms
Recommended Citation Rick, H. J., S. Rick, S. Fuentes and J. L. Noel. 2007. The nI vasive Cyanobacterium Cylindrospermopsis raciborskii in Southern Louisiana. Gulf of Mexico Science 25 (1). Retrieved from https://aquila.usm.edu/goms/vol25/iss1/5
This Article is brought to you for free and open access by The Aquila Digital Community. It has been accepted for inclusion in Gulf of Mexico Science by an authorized editor of The Aquila Digital Community. For more information, please contact [email protected]. Rick et al.: The Invasive Cyanobacterium Cylindrospermopsis raciborskii in Sou
Gulfof.Mexim Science, 2007(1), pp. 6l....Sl
The Invasive Cyanobacterium Cylindrospennopsis mciborskii in Southern Louisiana
HANs]. RicK, SILKE RicK, SoLEDAD FuENTES, AND JoDIE L. NoEL
Since 2002 two areas in southern Louisiana (Caernarvon Breton Sound estuary and Atchafalaya basin region) were studied regarding the occuiTence of the invasive and potentially harmful cyanobacterium Cylind1·ospemzopsis raciborskii. In the Caernarvon Breton Sound estuary, the species was detected for the first time in Louisiana in July 2002 in Grand Lake during monthly phytoplankton monitoring surveys. The species occulTed again in the estuary in summer and fall 2003 and 2004. Three distinct morphotypes (straight, curved, curled) were present, with the curved or curled varieties usually most abundant (> 80% ). During summer 2003 the cell numbers in 6 1 Grand Lal
INTRODUCTION but also affects the heart, lung, and spleen (Hawkins et al., 1985; Falconer et al., 1999). ylindrosjJermopsis raciborskii (Woloszy!'iska) The toxin can accumulate in tissues of crayfish, C Seenaya et Subba Raju (Nostocales, Seenaya shellfish, snails, and daphnids (Saker and Eagel and Subba Raju, 1972) is rated one of the most sham, 1999; Nogueira et al., 2004; Saker et al., notorious cyanobacterial species (Padisak, 1997; 2004; White et al., 2006). Briand et al., 2004) because of its potential Additionally there is growing apprehension toxicity (Hawkins et al., 1985; Lagos et al. 1999; about the role of cylindrospermopsin in gastro Humpage et al. 2000), ability to form dense intestinal and liver cancer with longtime low water blooms interfering with several kinds of level exposure (Humpage et al., 2000; Shen et water use, and invasive behavior at midlatitudes. al., 2002, Falconer, 2005). The "Palm Island The species is especially dangerous because in Mystery Disease," which occurred in 1979 in contrast to other harmful cyanobacteria it does Australia, is an example of a serious human not form surface blooms (scum) and cannot be detected by smell, taste, or color of the water poisoning caused by cylindrospermopsin. In ( Chiswell et al., 1997; Saker and Griffiths, 2001). Palm Island, 149 people were hospitalized with Because animals are often not deterred by foul symptoms of hepato-enteritis after consuming tastes, odors, or surface scums (Saker et al., contaminated drinking water (Byth, 1980; Grif 1999) they are more prone to cyanobacterial fiths and Saker, 2003). Cylindrospermopsin is poisonings than humans. Human exposure also believed to be the cause of the gastric usually occurs through direct contact, accidental ailment known as "Barcoo spews" once preva uptake via swallowing or inhaling cells, and lent in outback northern and central Australia uptake of the dissolved toxin via drinking water. (Hayman 1992; Chiswell et al., 1997). Hence, there is a major concern about contam At the beginnings of the last century, Wolos ination of drinking and recreational water zy!'iska (1912) described C. raciborskii as Anabaena supplies (Chapman and Schelske, 1997). The raciborskii. Because heterocyst location and de major toxin, cylindrospermopsin, a tricyclic gua velopment proved to be different to Anabaena, it nidine alkaloid, is a potent inhibitor of protein was then moved to the genus Anabaenopsis (Miller) synthesis (Ohtani et al., 1992). It damages and finally to Cylindrospemwpsis (Seenaya and a range of organs, especially the liver and kidney, Subba Raju). Cylindrospemwpsis raciborskii was
© 2007 by the Marine Environmental Sciences Consortium of Alabama Published by The Aquila Digital Community, 2007 1 Gulf of Mexico Science, Vol. 25 [2007], No. 1, Art. 5 62 GULF OF MEXICO SCIENCE, 2007, VOL. 25(1)
considered as typical for the Indo-Malayan flora Here we document the recent records of C. (Geitler and Ruttner, 1936) but was later classified racibonhii from coastal Louisiana. Occurrence as pantropical. The compilation of floristic data by locations and cell densities are given, and Padisak (1997) implies that C. raciborskii is not an relationships to meteorological, physico-chemi exclusively tropical or subtropical species, as it cal, and planktonic parameters are discussed. shows a small overlap in occurrence witl1 nortllern
circumpolar species. Currently the species is MATERIAL AND METHODS spreading worldwide to midlatitudes (Padisak, 1997; Briand et al., 2004). It was reported from The Caernarvon Breton Sound estuary was several temperate areas in Europe, such as Hun surveyed monthly from Feb. 2002 to Sep. 2004 by gary (Horecka and Komarek, 1979; T6tl1 and sampling a 20-station grid (Fig. 1a, upper left Padisak 1986, Borics et al., 2000), Austria (Dokulil panel). In Oct. 2004, 39 stations were sampled in and Mayer, 1996), France (Coute et al., 1997; the Atchafalaya basin region (Fig. 2) along with Briand et al., 2002), and Germany (Krienitz and some additional water bodies to the west (Fig. 3). Hegewald, 1996; Weidner and Nixdmf, 1997; In 2005 the Caernarvon Breton Sound estuary Fastner et al., 2003). In these areas the phytoplank was surveyed during late Aug. and early Nov.; ton in lakes has been studied for a considerable sampling of the Atchafalaya basin took place in time already; hence it appears that C. raciborskii is June, Sep., and Oct. a new invasive species rather than simply a species Water samples for total nutrient analysis were that has before been unrecorded. For the Amer collected using a stainless steel bucket poured into icas, most identifications of C. racibarshii occurred acid-washed Hish Density Polyeiliylene (HDPE) in Brazil, which has cyanobacterial monitoring in bottles and stored on ice until being returned to drinking water reservoirs (Trogan and Garcia, tlle laboratory. Inorganic nutrients [soluble re 1989; Falconer, 2005). It was also reported from active phosphoms (SRP), ammonium (NH/), reservoirs in Venezuela, Nicaragua, Cuba, and silicate (Si), and the sum of nitrate and nitrite Mexico (Komarek, 1984; Padisak, 1997). (NOX)], total phosphorus (TP), and total nitrogen The earliest record for North America is (TN) samples were analyzed using an automated probably from Kansas (Wooster Lake), where Lachat Quickchem Autoanalyzer and by manual Prescott and Andrews (1955) recorded the colorimeu·ic assays (Clesceri et al., 1998). Samples species as Anabaenopsis se1iata. In 1966, C. were kept fi·ozen ( < - 18 C) until final analysis. mciborskii occurred in several small lakes in Live plankton samples were stored in acid Minnesota (Hill, 1970). It was reported in Lake cleaned polyethylene (PE) bottles and trans Erie in the 1970s (Taft and Taft, 1971). ported to the lab in coolers under ambient water Additionally it was found in Ohio, Michigan, temperature conditions. For subsequent quantifi Illinois, Indiana, and Texas, U.S.A. (Padisak cation of C. raciborshii using the inverted micro 1997; Jones and Sauter, 2005; St. Amand, 2002; scope method (Lund et al. 1958; Utermohl1958) Falconer 2005), and recently in Canada (Kling, an aliquot was fixed with neuu·al formaldehyde to 2004; Hamilton et al., 2005). Florida's sub reach a final concentration of 0.4% (Throndsen, tropical eutrophic lakes and rivers, which fre 1978). Because cell walls between individual cells quently are used as drinking water supplies, witllin a trichome are barely visible and there is often support very large populations of C. almost no constriction between the cells (e.g., raciborskii (Chapman and Schelske 1997; Wil Hill, 1969; Padisak, 2003), samples were stained liams et al. 2001; Falconer, 2005). As far as witll DAPI to visualize cell walls. published information can indicate, adjacent Analysis of the phytoplankton community states have not been screened for this species was primarily performed using a pulse ampli yet. Because it is abundant in Cuba; Florida, tude modulation setup (WALZ Pffi'TOPAM). U.S.A.; Mexico; and subtropical regions else The four-wavelength excitation method (Schrei where in the world, it might exist throughout the ber et al., 1995, 1998; Schreiber, 1998) was higher rainh1ll areas of the southern United applied for a quantitative differentiation be States (Falconer, 2005). It is very likely that C. tween three major groups of phytoplankton [1, raciborskii has been abundant in southcentral Cyanobacteria; 2, Chlorophyceae, and 3, hetero temperate water bodies with suitable environ kontophytes (Chrysophyceae, Xanthophyceae, mental conditions in central North America Eustigmatophyceae, Bacillariophyceae, Raphi longer than the numerous recent records imply dophyceae, and Dictyochophyceae), dinoflagel (Kling, 2004). More in-depth information about lates, and prymnesiophytes]. The method en the genus Cylindrospennopsis can be found in the ables quantifYing chlorophyll levels within these compilation by Komarek and Hauer (2004). three groups. In the following, the chlorophyll of https://aquila.usm.edu/goms/vol25/iss1/5 2 DOI: 10.18785/goms.2501.05 Rick et al.: The Invasive Cyanobacterium Cylindrospermopsis raciborskii in Sou RICK ET AL.-CYLINDROSPERMOPSIS RACIBORSKII IN SOUTHERN LOUISIANA 63
the third group is referred to as "other" in the Caernarvon Breton Sound estuary (Fig. 1a, chlorophyll. midleft panel). The survey grid witll station The quality control program for the PHYTO numbers is shown in the upper left panel of PAM measurements included frequent calibra Figure 1a. Several morphotypes of C. mciborsllii tion using mono and mixed cultures of diatoms, were found; it always occurred in straight and green algae, and cyanobacteria isolated from curved formations, and, additionally, heavily the study areas. Chlorophyll values were as coiled chains were detected (Fig. 4). Curved and sessed by the PHYTOPAM method and for coiled morphotypes were more abundant (> additional cross checking by a U.S. Environ 80%) than straight forms. Cell diameter and cell mental Protection Agency (EPA)-approved length were 2-3 J.Lm and 5-8 J.Lm, respectively. chlorophyll extraction method (Arar and Col Cell density for the first record in Grand Lake was 6 lins, 1997). 3 X 10 cells liter -I. Since its first occurrence, the In situ measurements of water tempera species was a frequent encounter in the Caernar ture and conductivity were performed on each von Breton Sound estuary during summer and fall visit directly in the surface layer at each sam at elevated temperatures of the surface water (> pling station using a 340i WTW multimeter. 27 C) (Fig. 1a,b; Table 1). Highest densities 6 1 Water column light parameters were measured (max. 24.5 X 10 cells liter- ) were detected in occasionally using a LI-COR LI-185B quantum Grand Lake on 10 July 2003. From the spatial meter with a spherical quantum sensor SPQ distribution maps it is obvious that the species 0602 and a Secchi disc. Meteorological data for occurred always in the midsouthern part of the Caernarvon Breton Sound estuary were taken estuary (Fig. 1a,b, St. 7, 8, 9, 16, 17, 22, 23). In from the Louisiana State University (LSU) Agri 2004 C. mciborskii was a more rare sight in this cultural Center's website (LSU AgCenter Citrus estuary. It was only detected in low abundances 1 Station: http:/ /www.lsuagcenter.com/weather/). (10,000 to 50,000 cells liter- ) in two of nine The data were used to establish time charts monthly sunreys (Fig. 1b; Table 1). (2002-05) of daily average wind speeds, minimal During fall 2004 the species occurred wide daily air temperatures (5-d floating mean), and spread in coastal Louisiana (Fig. 3). Cylindrospe~~ cumulative rainfall for the estuary. Additionally mopsis raciborskii was relatively abundant in the wind, rain, and temperature data from the Atchafalaya basin (Fig. 2; Table 1). Elevated cell months before the potential development of densities were detected in the northern part of 6 1 Cylindrospemwpsis (April/May) were compared the basin (up to 5 X 10 cells liter - ) but also in for the 4 yr of the Caernarvon time series. the area of Lake Fausse Pointe (up to 30 X 106 1 Daily discharge volumes of the Caernanron cells liter- ). The species additionally occurred 6 1 diversion structure from 2002-05 were obtained in lower densities (0.01-0.16 X 10 cells liter- ) through the U.S.G.S. National Water Information in the vicinity of Lafayette (Lake Martin), Ville System (http:/ /waterdata.usgs.gov/la/nwis). The Plate (Lake Chicot), and Intracoastal City raw data [cubic feet per second ( CFS)] were used (Fig. 3). The square marked "LS" in this figure 3 1 to calculate monthly averages (m s- ) for the displays a dense Cylindrospennoj;sis bloom, which survey months and at the same time to compare occurred in the upper Barataria estuary in the amount of monthly discharged water to the summer 2003 (Rabalais, 2005). In 2004 the amount of monthly rainfall for the period April species was detected again in Lake Cataouatche, June in 2002-05. For this purpose the discharge Salvador, and Allemands (Ren eta!., 2005). 3 1 flow (m month - ) was converted to water height Chemical and planktonic parameters from 1 (em month - ) based on an overall size of the +CLY (containing Cylindrospermopsis) and -CYL 2 estuary of 656 km . (without Cylindrospemwpsis) samples were com Statistical analyses [ t-tests, analyses of variance pared using t-tests. Only data from surveys in (ANOVAs)] were pelformed usingJMP IN 5.1.2 which Cylindrospermopsis was detected were in software (SAS Institute). The global positioning cluded in the testing. system was used to survey all sampling locations. A comparison for conductivity based on data from the Atchafalaya (fall 2004) and the Caer REsuLTS narvon Breton Sound estuary (2002-05) is shown in Figure 5a. As expected, no pattern is obvious On 16 July 2002 the potentially harmful for the mainly freshwater Atchafalya samples, cyanobacterium, C. mciborskii (Woloszyiiska) See whereas for the Caernarvon Breton Sound naya et Subba Raju, was detected for the first time estuary average conductivities of +CYL samples in Louisiana. It was identified in a phytoplankton were lower compared to -CYL samples although sample from the Grand Lake area that was this proved not significantly different (Table 2). collected witllin monthly phytoplankton surveys Cylindrospermopsis raciborskii did not use the full
Published by The Aquila Digital Community, 2007 3 Gulf of Mexico Science, Vol. 25 [2007], No. 1, Art. 5 64 GULF OF l'vlEXICO SCIENCE, 2007, VOL. 25(1)
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Fig. Ia, b. Temporal-spatial distribution of CylindrospermojJsis mriborshii in the Caernarvon Breton Sound estuary: A grid of 20 to 23 stations (Upper left panel, Fig. 1a) was surveyed monthly from February 2002 to September 2004. Numbers are station numbers, described in Table L The species was detected within 11 out of 38 surveys. Black squares with white numbers or markings indicate stations where Cylindrospermopsis was present while black numbers show stations where the species was not present during the respective survey. In three surveys are additional stations were sampled. These are marked with crosses for 6/1/2003 and 7/10/2003 or letters for 7/13/2004 survey.
https://aquila.usm.edu/goms/vol25/iss1/5 4 DOI: 10.18785/goms.2501.05 Rick et al.: The Invasive Cyanobacterium Cylindrospermopsis raciborskii in Sou RICK ET AL.-CYLINDROSPERMOPSIS RACIBORSKIIIN SOUTHERN LOUISIANA 63
the third group is referred to as "other" in the Caernarvon Breton Sound estuary (Fig. 1a, chlorophyll. midleft panel). The survey grid with station The quality control program for the PHYTO numbers is shown in the upper left panel of PAM measurements included frequent calibra Figure 1a. Several morphotypes of C. raciborskii tion using mono and mixed cultures of diatoms, were found; it always occurred in straight and green algae, and cyanobacteria isolated from curved formations, and, additionally, heavily the study areas. Chlorophyll values were as coiled chains were detected (Fig. 4). Curved and sessed by the PHYTOPAM method and for coiled morphotypes were more abundant (> additional cross checking by a U.S. Environ 80%) than straight forms. Cell diameter and cell mental Protection Agency (EPA)-approved length were 2-3 11m and 5-8 11m, respectively. chlorophyll extraction method (Arar and Col Cell density for the first record in Grand Lake was 6 1 lins, 1997). 3 X 10 cells liter- . Since its first occurrence, the In situ measurements of water tempera species was a frequent encounter in the Caernar ture and conductivity were performed on each von Breton Sound estuary during summer and fall visit directly in the surface layer at each sam at elevated temperatures of the surface water (> pling station using a 340i WTW multimeter. 27 C) (Fig. 1a,b; Table 1). Highest densities 6 1 Water column light parameters were measured (max. 24.5 X 10 cells liter- ) were detected in occasionally using a LI-COR LI-185B quantum Grand Lake on 10 July 2003. From the spatial meter with a spherical quantum sensor SPQ distribution maps it is obvious that the species 0602 and a Secchi disc. Meteorological data for occurred always in the midsouthern part of the Caernarvon Breton Sound estuary were taken estuary (Fig. 1a,b, St. 7, 8, 9, 16, 17, 22, 23). In from the Louisiana State University (LSU) Agri 2004 C. raciborskii was a more rare sight in this cultural Center's website (LSU AgCenter Citrus estuary. It was only detected in low abundances 1 Station: http:/ /W\VW'.lsuagcenter.com/weather /). (10,000 to 50,000 cells liter- ) in two of nine The data were used to establish time charts monthly surveys (Fig. 1 b; Table 1). (2002-05) of daily average wind speeds, minimal During fall 2004 the species occurred wide daily air temperatures (5-d floating mean), and spread in coastal Louisiana (Fig. 3). Cylindrospe1~ cumulative rainfall for the estuary. Additionally nwpsis raciborskii was relatively abundant in the wind, rain, and temperature data from the Atchafalaya basin (Fig. 2; Table 1). Elevated cell months before the potential development of densities were detected in the northern part of 6 1 Cylindrospermopsis (April/May) were compared the basin (up to 5 X 10 cells liter - ) but also in for the 4 yr of the Caernarvon time series. the area of Lake Fausse Pointe (up to 30 X 106 1 Daily discharge volumes of the Caernarvon cells liter- ). The species additionally occurred 6 1 diversion structure from 2002-05 were obtained in lower densities (0.01-0.16 X 10 cells liter- ) through the U.S.G.S. National Water Information in the vicinity of Lafayette (Lake Martin), Ville System (http:/ /waterdata.usgs.gov/la/nwis). The Plate (Lake Chicot), and Intracoastal City raw data [cubic feet per second ( CFS)] were used (Fig. 3). The square marked "LS" in this figure 3 1 to calculate monthly averages (m s- ) for the displays a dense Cylindmspennopsis bloom, which survey months and at the same time to compare occurred in the upper Barataria estuary in the amount of monthly discharged water to the summer 2003 (Rabalais, 2005). In 2004 the amount of monthly rainfall for the period April species was detected again in Lake Cataouatche, June in 2002-05. For this purpose the discharge Salvador, and Allemands (Ren eta!., 2005). 3 1 flow (m month - ) was converted to water height Chemical and planktonic parameters from 1 (em month- ) based on an overall size of the +CLY (containing Cylindrospemwpsis) and -CYL 2 estuary of 656 km • (without Cylindrospemwpsis) samples were com Statistical analyses [ t-tests, analyses of variance pared using t-tests. Only data from surveys in (ANOVAs)] were performed usingJMP IN 5.1.2 which CylindrospermojJsis was detected were in software (SAS Institute). The global positioning cluded in the testing. systern was used to survey all sampling locations. A comparison for conductivity based on data from the Atchafalaya (fall 2004) and the Caer
RESULTS narvon Breton Sound estuary (2002-05) is shown in Figure Sa. As expected, no pattern is obvious On 16 July 2002 the potentially harmful for the mainly freshwater Atchafalya samples, cyanobacterium, C. mciborskii (Woloszynska) See whereas for the Caernarvon Breton Sound naya et Subba Raju, was detected for the first time estuary average conductivities of +CYL samples in Louisiana. It was identified in a phytoplankton were lower compared to -CYL samples although sample from the Grand Lake area that was this proved not significantly different (Table 2). collected within monthly phytoplankton surveys CylindrospermojJsis raciborskii did not use the full
Published by The Aquila Digital Community, 2007 5 Gulf of Mexico Science, Vol. 25 [2007], No. 1, Art. 5
64 GULF OF MEXICO SCIENCE, 2007, VOL. 25(1) a
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Fig. la, b. Temporal-spatial distribution of CylindrosjHmnopsis raciborshii in the Caernarvon Breton Sound estuary: A grid of 20 to 23 stations (Upper left panel, Fig. la) was surveyed monthly from February 2002 to September 2004. Numbers are station numbers, described in Table l. The species was detected within 11 out of 38 surveys. Black squares with white numbers or markings indicate stations where Cylindrospermopsis was present while black numbers show stations where the species was not present during the respective survey. In three surveys are additional stations were sampled. These are marked with crosses for 6/1/2003 and 7/10/2003 or letters for 7/13/2004 survey.
https://aquila.usm.edu/goms/vol25/iss1/5 6 DOI: 10.18785/goms.2501.05 Rick et al.: The Invasive Cyanobacterium Cylindrospermopsis raciborskii in Sou RICK ET AL.-CYLINDROSPERJviOPSIS RACIBORSKII IN SOUTHERN LOUISIANA 65
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Published by The Aquila Digital Community, 2007 7 Gulf of Mexico Science, Vol. 25 [2007], No. 1, Art. 5
66 GULF OF MEXICO SCIENCE, 2007, VOL. 25(1)
-CYL samples were lower compared to +CYL samples but the finding proved significantly different for TN only. Average TN/TP did not differ between the datasets (Table 3). Planktonic parameters were analyzed for both the Caernarvon and Atchafalaya datasets (Fig. 7; Tables 2 and 4). In both sets total chlorophyll concentration and cyanobacterial chlorophyll (expressed as percentage of total chlorophyll) were significantly higher in +CYL compared to -CYL samples. Green algal chlorophyll (% of total) was significantly elevated in the Atchafa laya -CYL samples. The Caernarvon data showed the same trend although both sample sets were not significantly different. Conversely, chlorophyll from heterokontophytes, dinoflagel lates, and prymnesiophytes was significantly lower in the Caernarvon +CYL samples, a trend that was visible for the Atchafalaya, too. It is known from other studies that water temperature and water column stability have an important impact on akinete germination and the subsequent development of Cylindrospemwp sis. For the Caernanron time series, some proxies (minimal air temperature, cumulative rainfall, average wind speed) describing these parameters are shown in Figure 8. In the shallow lake-like 91.75 91.55 w 91.35 areas of the estuary, the water column stability is Fig. 2. Spatial distribution of CylindrospemzojJsis raci strongly influenced by wind and rainfall, whereas borskii in the region of the Atchafalaya basin in fall 2004. the temperature at the water-sediment interface Stations south of Interstate 10 (I 10) were surveyed on triggers akinete germination. Because water 10/01/2004, stations north of I 10 on 10/15/2004. temperature data were not available in high vVhite squares indicate stations where Cylindrospemwpsis resolution for the time series, the development was present while black spares show stations with no of the minimal air temperature was used as occurrence of the species. Cylindrospennopsiswas present a proxy. It is assumed that at minimal air in 20 of 38 samples. temperatures of 18.5 C (Fig. 8, hatched lines) the shallow lakes reach temperatures of > 22 C, range of conductivity in the estuary. It occurred allowing Cylindrospermopsis akinetes to germinate. only at conductivities between 700 JlS em -I and Early warming and extensive droughts during 1 10,000 JlS cm- (Figure 5b). spring characterized the years 2002 and 2003, Nutrient measurements (NOX, SRP, NH/, Si, which is in contrast to 2004 and 2005 (Fig. 8). TN, and TP) were conducted only for samples Since the input of diverted Mississippi River from the Caernarvon Breton Sound time series. water has an additional influence on the water Average values of inorganic dissolved nutrients column stability within the Caernarvon Breton with two of their molar ratios [dissolved in Sound estuary, diversion discharge and rainfall organic nitrogen (DIN)/SRP, and Si/DIN] are for the months before the potential occurrence shown in the Figure 6a,b with standard errors of of CylindrospermojJsis are compared in Figure 9. means (SEM). Whereas no difference between Rainfall and discharge are displayed in the same +CYL and -GYL samples was detected for NH4+, dimension to enable a quantitative comparison SRP, and Si, the average concentration of NOX between both parameters. The amount of water was significantly lower in the -GYL samples. In delivered by rain to the estuary is in the same turn, DIN/SRP and Si/DIN ratios were influ range as the amount discharged by the diversion. enced in the way that averages for +CYL samples
were lower compared to -CYL samples. The DISCUSSION datasets, however, proved not significantly dif ferent from each other. The situation for total Trichome morphology, cell sizes, and cell counts.-It nutrients and their molar ratios is given in is common to find that C. raciborskii exists in Figure 6c. For both TN and TP, averages of different morphotypes (Baker and Fabbro, 1999; https://aquila.usm.edu/goms/vol25/iss1/5 8 DOI: 10.18785/goms.2501.05 Rick et al.: The Invasive Cyanobacterium Cylindrospermopsis raciborskii in Sou RICK ET AL.-CYLINDROSPERJviOPSIS RACIBORSKIIIN SOUTHERN LOUISIANA 67
Fig. 3. CylindrosjJennojJsis mciborskii occurrence in southern Louisiana. Triangles show the occurrence in fall 2004 (LC: Lake Chicot, LIVI: Lake Martin, LFP: Lake Fausse Pointe, AB: Atchafalaya Basin, IC: Intracoastal City). The Caernarvon Breton Sound estuary (CB: circle) was surveyed monthly starting in February 2002. The square (LS) shows the occurrence of the species in the upper Barataria estuary (Rabalais, 2005).
Fig. 4. Different morphotypes (straight, curved, curled) of Cylindrospemwpsis mciborskii collected in southern Louisiana (Grand Lake, Caernarvon-Breton Sound estuary, 7/10/2003).
Published by The Aquila Digital Community, 2007 9 Gulf of Mexico Science, Vol. 25 [2007], No. 1, Art. 5 68 GULF OF MEXICO SCIENCE, 2007, VOL. 25(1)
TABLE 1. Occurrence of Cylindrospermopsis mciborskii in southern Louisiana 2002-04. Sampling dates, locations, positions, and cell numbers per liter. C: Caernarvon Breton Sound estuary; A: Atchafalaya basin area.
Date Station N w Cell number I6 July 2002 C-I6 89.849 29.7I2 3,350,000 28 Aug. 2002 C-9 89.703 29.696 I20,000 28 Aug. 2002 C-I8 89.685 29.62I 930,000 II June 2003 C-7 89.789 29.7ll IO,OOO II June 2003 C-I6 89.849 29.712 IO,OOO 23June 2003 C-I6 89.849 29.7I2 530,000 23June 2003 C-I7 89.772 29.64I 50,000 23June 2003 C-22 89.749 29.67I 90,000 23June 2003 C-23 89.708 29.655 IO,OOO IO July 2003 C-7 89.789 29.7ll I,560,000 IO July 2003 C-I5 89.862 29.682 25,000 IO July 2003 C-I6 89.849 29.7I2 24,530,000 IO July 2003 C-I7 89.772 29.64I 4,720,000 IO July 2003 C-Grancl Lake Northwest 89.83I 29.722 50,000 10July 2003 C'rGrand Lake South 89.84I 29.703 I,070,000 10July 2003 C-Bay Lori 89.839 29.683 10,000 IO July 2003 C-Oak River 89.8I7 29.659 40,000 IO July 2003 C-Pointe Fienne Bay 89.77 29.646 IO,OOO 10 July 2003 C-Bay Jack Nevette 89.758 29.636 10,000 10July 2003 C-Spyder 89.747 29.66 IO,OOO 10July 2003 C-Lake Faussan North 89.753 29.682 IO,OOO IO July 2003 C-Alligator Pass 89.8I7 29.7I8 IO,OOO IO July 2003 C-Little Lake South 89.778 29.694 IO,OOO 24July 2003 C-8 89.708 29.754 30,000 24July 2003 C-9 89.703 29.696 100,000 24July 2003 C-ll 89.565 29.658 90,000 24July 2003 C-I4 89.9I 29.7 I,530,000 24July 2003 C-I5 89.862 29.682 I,060,000 24July 2003 C-I6 89.849 29.712 I,490,000 24July 2003 C-I7 89.772 29.64I 650,000 24July 2003 C-I8 89.685 29.62I 347,000 24July 2003 C-22 89.749 29.671 240,000 24July 2003 C-23 89.708 29.655 580,000 20 Aug. 2003 C-I4 89.9I 29.7 230,000 20 Aug. 2003 C-I5 89.862 29.682 IO,OOO 20 Aug. 2003 C-I7 89.772 29.64I II6,000 20 Aug. 2003 C-22 89.749 29.671 ll6,000 24 Sep. 2003 C-5 89.804 29.793 40,000 24 Sep. 2003 C-I4 89.9I 29.7 7,510,000 24 Sep. 2003 C-I5 89.862 29.682 7,360,000 24 Sep. 2003 C-I6 89.849 29.7I2 780,000 22 Oct. 2003 C-7 89.789 29.7II ll6,000 22 Oct. 2003 C-I4 89.9I 29.7 10,000 22 Oct. 2003 C-I5 89.862 29.682 2,500,000 22 Oct. 2003 C-I6 89.849 29.712 30,000 13July04 C-Lake Amaclee 89.693 29.76I 25,000 13July0'1 C-Tanasia Lagoon 89.68 29.773 50,000 03 Aug. 2004 C-8 89.708 29.754 10,000 03 Aug. 2004 C-9 89.703 29.696 40,000 03 Aug. 2004 C-Lake Amadee 89.693 29.76I IO,OOO 04 Sep. 2004 Lake Martin 91.908 30.22I I60,000 10 Sep. 2004 Intracoastal City 92.I56 29.783 4,000 10 Sep. 2004 Lake Fausse Pointe 91.552 29.936 200,000 29 Sep. 2004 Lake Chicot North Landing 92.286 30.838 10,000 01 Oct. 2004 A-Butte La Rose 91.692 30.281 410,000 01 Oct. 2004 A-Butte La Rose Bay 91.707 30.269 80,000 https://aquila.usm.edu/goms/vol25/iss1/5 10 DOI: 10.18785/goms.2501.05 Rick et al.: The Invasive Cyanobacterium Cylindrospermopsis raciborskii in Sou RICK ET AL.-CYLINDROSPERJviOPSIS RACIBORSKII IN SOUTHERN LOUISIANA 69
TABLE l. continued.
1 Date Station N w Cell number (L } 01 Oct. 2004 A-Lake Dauterive 91.622 30.075 10,000 01 Oct. 2004 A-Lake Fausse Park 91.61 30.062 10,000 01 Oct. 2004 A-Lake Fausse Pointe 91.551 29.948 29,840,000 01 Oct. 2004 A-Lake Fausse Pointe 91.552 29.936 24,750,000 01 Oct. 2004 A-Grand Ayoille Cove 91.545 29.923 20,110,000 01 Oct. 2004 A-Chareton 91.513 29.902 30,000 01 Oct. 2004 A-Wilson Landing 91.294 29.722 10,000 15 Oct. 2004 A-Pelba 91.73 30.341 10,000 15 Oct. 2004 A-Atchafalaya near Pelba 91.715 30.36 25,000 15 Oct. 2004 A-vVhiskey Bay Boat Launch 91.626 30.369 10,000 15 Oct. 2004 A -vVhiskey Bay Pilot Channel 91.636 30.366 30,000 15 Oct. 2004 A-Rama inside Basin 91.512 30.4 25,000 15 Oct. 2004 A-Alabama Bayou 1 91.674 30.41 4,870,000 15 Oct. 2004 A-Alabama Bayou 2 91.672 30.424 1,640,000 15 Oct. 2004 A-Port of Krotz Springs 91.744 30.53 10,000 15 Oct. 2004 A-Dixie Ramp 91.758 30.458 30,000 15 Oct. 2004 A-Atchafalaya Ferry 91.689 30.386 10,000 15 Oct. 2004 A-Lake inside Basin near I 10 91.786 30.344 10,000
Komarkova et a!., 1999; Komarek and Komar a kova, 2003; Shafik, 2003). To date heavily coiled forms of C. raciborskii (Fig. 4, right panel) have ,~ not been described for North America. Coiled E (.) ::::II~ morphotypes of the species are only occasionally (/) common in Australian populations (Baker and ..=!. 3000 ] 1Fabbro, 1999; Komarek and Komarkova, 2003). .n Other species of the genus CylindrospermojJis t) :::! species like CylindrosjJemwpis acwninato-crisjm 't:J 300 c (Coute and Bouvy, 2004, Brasil), Cylindrospermo 0 200 (.) pis jJhilippinensis (Komarek and Komarkova, 100 172 2003, Indonesia, Philippines), Cylindrospermopis Atchafalaya Caernarvon catemaco (Komarkova-Legnerova and Tavera, 1996, Komarek and Komarkova, 2003, southern b California, Mexico, Belize), Cylindrospemwj;is helicodea (Cronberg and Komarek, 2004, central Africa), or Cylindrospermopis cumispora (Cronberg E: (.) and Komarek, 2004; Komarek and Komarkova, (/) 2, 2003, Watanabe, 1995, South Africa, Sri Lanka, ~ Japan) have heavily coiled trichomes only. At the ·:;: moment it is unclear whether the heavily coiled ~ :::! form is a morpho type of C. raciborskii or whether '0c it belongs to another species of the genus. "\,Ye 0 1000 (.) are in the process of culturing different mor 500 photypes for further evaluation. 300 Cell widths (2-3 J.lm) and lengths (5-7 ~tm) match closely with information from the litera 0 m detect non·detect ture (Hill, 1969; McGregor and Fabbro, 2000; Chonudomkul et a!., 2004; Jones and Sauter, Fig. 5. (a) Comparison of conductivity in +GYL 2005). Recorded maximum cell numbers for (black) and -CYL (white) samples from the Atchafa Grand Lake in the Caernarvon Breton Sound laya survey in fall 2004 and the Caemarvon Breton estuary and for the Lake Fausse Pointe area were Sound time series (2002-2004). Average values are 6 1 given with standard errors of means (SEM). Numbers above the threshold level (20 X 10 cells liter- ) at the base of the bars indicate sample sizes. (b) for potential toxicity (McGregor and Fabbro, Conductivity scatter plot of +CYL and -CYL samples 2000). Ren Ling even recorded higher maximum 6 1 from the Caernarvon time series. cell numbers (up to 34.8 X 10 liter- ) during
Published by The Aquila Digital Community, 2007 11 Gulf of Mexico Science, Vol. 25 [2007], No. 1, Art. 5 70 GULF OF MEXICO SCIENCE, 2007, VOL. 25(1)
TABLE 2. Statistical comparison (t-test) of abiotic and planktonic parameters on samples contammg Cylindrospermopsis raciborshii (+CYL) and samples without C. raciborskii (-CYL) fi·om the Caemarvon Breton Sound estuary (summer-fall 2002-04). a-Levels were generally set at 0.05, and levels for total chlorophyll (Total Chi.) at 0.1. Sample size was 50 for +CYL and 178 for -CYL. "Other" Chi.: chlorophyll from heterokontophytes, dinophytes, and6 prymnesiophytes.
% Cyanobact. Green algal ''Other'' Total Cyanobacteria %Greens %"Other" Conductivity Chi. Chi. Chi. Chi. of total of total of total
Significant No Yes No No Yes Yes No Yes difference t-ratio -1.935 2.727 -0.313 0.022 2.151 2.481 -0.668 -3.672 +CYL samples mean 3,196 18.6 7.1 8.5 34.1 49.9 25.1 25.0 SD 2,189 16.9 7.4 7.6 18.2 27.9 25.0 13 -CYL samples mean 4,254 11.5 7.6 8.5 27.6 38.8 27.8 33.4 SD 5,907 13.3 15.1 7.1 21.6 28.1 25.7 18.1
a bloom in Lake Cataouatche, Barataria estuary, It is well know that C. raciborskii has a high LA, in summer 2003 (Rabalais, 2005). tolerance for low light levels (Padisak and Reynolds, 1998; Briand et al. 2002). Shafik et Temperature.-Both in the Caernarvon Breton al. (2001) calculated a light tolerance for the 2 Sound estuary as well in the Atchafalaya basin area species as low as 26 !-lmol m - sec -I in Lake C. raciborskii was only detected in summer and fall Balaton (Hungary). In shallow turbid Brazilian 2 at surface temperatures ranging from 25 C to 33 lakes the species even survived at 0.5 1-lmol m - - C. It is already well known that the occurrence of sec-1 (Bouvy et al., 2000). On the other hand, C. C. raciborskii is heavily affected by water tempera racibm:5hii is able to tolerate relatively high light 2 ture (Branco and Senna, 1994; Souza et al., 1998; levels up to 500 !-lmol m - sec -I (Briand et al., McGregor and Fabbro, 2000). In the tropics the 2004). Secchi disc readings of 30 em are com species is often found year round in the plankton mon in C. raciborskii blooms (Mayer et al., 1997; (Bouvy et al., 1999; Briand et al., 2004), but in Padisak, 1997). For Florida blooms, Chapman temperate and subtropical regions its occurrence and Schelske (1997) reported mean Secchi is restricted to warm summer months (Briand et depths less than 1.0 m, and for blooms in al. 2002; Saker et al., 2003). In the field, the Europe, Secchi depths sometimes decreased to species seems to prefer surface water tempera 0.07 m (Briand et al., 2002). tures exceeding 23 C (Padisak, 1997; McGregor and Fabbro, 2000), whereas temperatures around Conductivity.-In the Caernarvon Breton Sound 30 C were found to be optimal for the growth of estuary, C. raciborskii was detected within conduc the species in cultures (Shafik et al., 2001; Briand tivities ranging from 700 to 9,000 !-lS em -I (up to et al., 2004). 4.8 PSU, Fig. 5b). Tolerance to elevated conduc tivities was already compiled by Padisak ( 1997) as Light.-Because of their low latitude location, the species occurred twice at salinity levels of 1.5- the Caernoravon Breton Sound estuary as well as 2 PSU in the North Caspian Sea, at conductivities the Atchafalaya basin experience relatively high above 4,000 !-lS em -I in Lake Alexandria, and solar radiation. Water smface light measure above 2,000 !-lS cm-1 in Venezuela. Laboratory ments during summer and fall at no cloud experiments by l'vloisander et al. (2002) showed cover-midday ranged from 2,500 to 2,800 !-lmol that 2 g liter- 1 NaCl at least slowed growth of the 2 m - sec -I. Due to high plankton densities, species, whereas the upper limit for salinity vertical light profiles revealed often relatively tolerance was reached at 4 g liter-1 NaCl, which high turbidities in the areas of C. racibor.skii is in good accordance with the highest salinities occurrence. Vertical attenuation coefficients ( 4.8 PSU) where the species could be detected in (kc~) were in the range of 3.8-2.3 accompanied the Caernarvon Breton Sound estuary. with relatively low Secchi disc transparencies (0.2-0.6 m). These numbers show that almost Water column stability.-In the shallow (max. 90% of the smface light is already attenuated at 2.5-3 m) lake-like water bodies of the Caernar depths of 0.6 to 1.0 m, respectively. von Breton Sound estuary, the stability of the https://aquila.usm.edu/goms/vol25/iss1/5 12 DOI: 10.18785/goms.2501.05 Rick et al.: The Invasive Cyanobacterium Cylindrospermopsis raciborskii in Sou RICK ET AL.-CYLINDROSPERMOPSJS RACJBORSKII IN SOUTHERN LOUISIANA 71
a dominance (Branco and Senna, 1994; Bouvy et 14 at., 1999, 2003a; Bormans et at., 2004). :E .=. 10 12 The flow of the diverted water has quadruple 0.. negative effects on the success of C. raciborshii. o"' 8 10 a: z !Q First, water column stability, which often is + 8 z 6 c regarded as a necessary prerequisite for its o"' 6 ... Cll occurrence (e.g., Saker and Griffiths, 2001), is ~ 4 0 disturbed and the water residence time reduced. 0 4 E 0.. Second, dming times of high flow, the species' a: 2 2 (/) akinetes resting in the upper layers of the 0 sediment might be flushed out of the estuary. DIN/SRP SRP Third, the diverted water dilutes and flushes the entire planktonic community, and fourth, it 80 introduces high nutrient concentrations into z the estuary, depriving C. raciborskii of its compet e itive advantage of using low nutrient levels most 60 en ... efficiently (Bouvy et at., 2000; Istv{movics et at., Ill 0 2000; Shafik et at. 2001; Briand et at. 2002). 40 E ... Rainfall and wind speed are additional factors 0 influencing water column stability in these shallow lakes. In contrast to the regional effects 20 ~ ..:!. of diverted water, rainfall and wind affect the en estuary more evenly. The amount of water 0 2 delivered by rain to the estuary (656 km ) is at least in the same range as the amount discharged c by the diversion (Fig. 9). 5 Overall the Caernarvon Breton Sound data 0.. support the view that C. Taciborskii favors relative t: z 80 l 4 ly stable water column conditions (Komarek and 1-... ~ Kling, 1991: Lake Victoria, Uganda; Harris and 0"' 3 !§' Baxter, 1996: North Pine Dam, Australia; Saker E 60 ..:!; and Griffiths, 2001: Lake Julius, Australia; Berger ... 0.. 0 2 1- et at., 2006: Lake Guiers, Senegal). Several !§'.=. 20 CylindTospemwjJsis blooms in Australia and South America occurred in years of low rainfall and ~ increased drawdown of the water column (Bouvy 0 et at., 1999, 2003a; Saker and Griffiths, 2001). In fact, we have experienced a similar situation in Fig. 6. Comparison of nutrient parameters of +CYL (black) and -CYL (white) mixed layer water samples early summer 2006 in the Lake Fausse Pointe from the Caemarvon Breton Sound time series (2002- area (Louisiana), when C. raciborskii bloomed 6 1 2004). Average values are given with standard errors of (up to 88 X 10 cells liter- ) after an extremely means (SEM). Numbers at the base of the bars indicate dry and warm spring with low water levels. the sample sizes. (*) indicates significant differences The literature gives also reports contradicting between datasets. (a) NOX, SRP, and DIN/SRP. (b) the species' dependence on water column NH4+, Si, and Si/DIN. (c) TN, TP, and TN/TP. stability, especially regarding the rain effect. In Mir Alam Lake, India, the species "multiplied water column is mainly affected by the activity of profusely in late summer and throughout the the diversion structure, wind, and rainfall. rainy season" (Seenayya and Zafar, 1979). During the time series C. raciborshii only occurred Similar findings are reported from Lake Kariba, in areas that were not directly influenced by the Zimbabwe (Ramberg, 1987). Branco and Senna diverted waters and hence had high water (1994) found C. raciborskii dominant in Paranoa residence times (Fig. 10). The species could only Reservoir, Brazil, after rainy periods diluting be detected once within the major eastern nutrient levels. pathway of the diverted water in Sep. 2003 In Lake Griffin (FL) it dominated shallow, well (Fig. 10, squared dot), when the diversion mixed waters (Dobberfuhl, 2003). Antenucci et discharge was relatively low (17.3% of maximal at. (2005), who found C. raciborskii dominant capacity). A prolonged water residence time is before and after artificial destratification of the often a necessary prerequisite for C. raciborskii North Pine Dam reservoir (Australia), suggested
Published by The Aquila Digital Community, 2007 13 Gulf of Mexico Science, Vol. 25 [2007], No. 1, Art. 5 72 GULF OF MEXICO SCIENCE, 2007, VOL. 25(1)
TABLE 3. Statistical comparison (t-test) of nutrient parameters on samples containing CylindrosjJermojJsis mciborskii (+GYL) and samples without C. mciborskii ( -GYL) from the Caernarvon Breton Sound estuary (summer-fall2002- 04). Ct.-Levels were generally set at 0.05, and levels for NOX, DIN/SRP, and TN at 0.1. Sample size was generally 29 for +CYL and in most cases 178 for -CYL. Exceptions: sample size was 107 for ( -CYL) TN and ( -CYL) TN/TP, it was 110 for (-CYL) TP.
SRP N02 +NO:~ NH4+ Si DIN/SRP Si/DIN TN Tl' TN/TP
Significant No Yes No No No No Yes No No difference t-ratio -1.202 -4.37 0.071 -0.685 -2.732 -1.753 2.077 1.436 0.078 +GYL samples mean 1.5 1.1 4.6 47.2 3.5 29.5 87.1 4.3 21.9 SD 0.9 1.0 14.1 22.9 7.4 29.3 23.2 1.5 7.8 -CYL samples mean 1.8 8.5 4.4 50.6 9.9 53.5 76.5 3.9 21.7 SD 0.9 20.1 10.2 30.3 23.0 151.0 27.9 1.4 12.7
the ability of the species to compete for phospho occurrence (average 6.6% of maximum capacity) rus triggered the dominance during stratification, dissolved concentrations of Si, NH4+, SRP, and whereas after destratification its superior light overall TP and TN levels were still elevated utilization capability was the determining factor. (Table 3). In contrast, NOX concentrations were relatively low forcing the molar ratio of DIN/SRP Nutrients.-Because of the influence of the to levels way below the Redfield ratio of 16 and diverted, nutrient-rich Mississippi water, the implementing a possible nitrogen limitation to Caernarvon Breton Sound estuary is classified the phytoplankton community. as eutrophic (Lane eta!., 1999, 2004). Despite A statistical comparison of nine nutrient low diversion discharge at times of C. racibonkii parameters for +CYL and -CYL samples re-
70 60 >. ~:; 60 a ..c 1-l+il 50 c. en 0 .=!. 50 l=JiJ ... 40 .Q!::' ..era >. (.) ..c 40 ..... c. 30 iii.s e ·~o 0 30 :2 20 t)~ () 20 ..0 "'0 ~ c: 10 10 . (.) 0 0
>. 50 50 ..c c. ..c>. e~ 40 40 c.~ ..2-S ..c 0 e:s0 0 (.) ..... _...., 30 30 ..c- iii'O (.) 0 .Bl~ i<~~ ra~ 20 20 Q) c: ..c Q) ...... Q) 10 10 0 OJ 0 0 Atchafalaya Caernarvon Atchafalaya Caernarvon Fig. 7. Comparison of chlorophyll parameters of +CYL (black) and -CYL (white) mixed layer water samples from the Atchafalaya surveys in fall 2004 and the Caernarvon Breton Sound time series (2002-2004). Average values are given with standard errors of means (SEM). Numbers at the base of the bars indicate the sample sizes. Sample sizes in (b), (c), and (d) are identical to (a). (*)indicates a significant difference between datasets. (a) total chlorophyll, (b) cyanobacterial chlorophyll, (c) green algal (chlorophyceae) chlorophyll, and (d) heterokontophyte, dinophyte, and prymnesiophyte chlorophyll. https://aquila.usm.edu/goms/vol25/iss1/5 14 DOI: 10.18785/goms.2501.05 Rick et al.: The Invasive Cyanobacterium Cylindrospermopsis raciborskii in Sou RICK ET AL.-CYLINDROSPERJIWPSIS RACIBORSKII IN SOUTHERN LOUISIANA 73
TABLE 4. Statistical comparison (t-test) of abiotic and planktonic parameters of samples containing CylindrosjJermopsis raciborshii (+CYL) and samples without C. raciborshii ( -Cl'L) from the Atchafalaya basin area (Oct. 2004). a-Levels were generally set at 0.05, levels for total chlorophyll (Total Chl.) at 0.1. Sample size was 20 for (+CYL) and 18 for (-CYL). "Other" Chl.: chlorophyll from heterokontophytes, dinophytes, and prymnesiophytes.
Cyanobacterial Green ''Other'' Total % Cyanobarte!ia %Green %"Other" Conductivity Chi. algal Chi. Chi. Chi. of total of total of total
significant No Yes No No Yes Yes Yes No difference t-ratio 0.353 2.701 -1.447 1.699 2.086 3.459 -2.199 -0.483 +CYL samples mean 272 25.4 1.534 21.132 47.98 48.033 5.424 46.967 SD 57 30.1 3.34 28.376 56.173 16.516 12.036 16.017 -CYL samples mean 265 7.0 4.4 10.2 21.4 29.7 21.0 49.6 SD 62 5.2 7.6 4.6 8.6 16.1 29.0 17.4
vealed significant differences only for dissolved than other cyanobacteria and is often found at NOX and TN levels (Fig. 6; Table 3). Samples low DIN/SRP ratios. In subtropical and temper containing OylindrosjJennopsis displayed higher ate regions the species is known to bloom TN and lower NOX levels compared to -CYL relatively late in season when the water is warm samples. SRP and TP concentrations showed the and most of the nutrients have already been used same pattern, but differences were not signifi by other phytoplankton species. Its capability to cant. Consequently, the average DIN/SRP ratio use even extremely low nutrient concentrations of +CYL samples was lower compared to -CYL most efficiently (Branco and Senna, 1994; samples. Istv<'movics et al., 2000; Shafik et al., 2001; Briand On the first glance these findings seem et al., 2002), coupled with the tolerance for low contradictory but they can be explained by the light, enables the species to thrive in systems species' ecology. Bouvy et al. (1999) state that C. characterized by high plankton densities and low raciborskii is possibly less dependent on nutrients dissolved nutrient concentrations. This exactly
35 2004 25 30 25 20 20 15 15 G' 10 e... 10 ci. 5 5 E "C Cl) ~ 0~--~---~~~---~~-~--~ 0 Cl) ... c.. '(ij Ill 30 25 2003 "C c c 'i§ 25 20 ·~ 20 15 15 10 10
5 5
0 0 60 120 180 240 300 360 0 60 120 180 240 300 360 time [days] Fig. 8. Meteorological data (daily average wind speed, minimal air temperature, cumulative rainfall) for the Caernarvon Breton sound estuary (LSU-AG Center, Citrus station 2002-2004). Minimal air temperature are given as 5-day floating average.
Published by The Aquila Digital Community, 2007 15 Gulf of Mexico Science, Vol. 25 [2007], No. 1, Art. 5 74 GULF OF MEXICO SCIENCE, 2007, VOL. 25(1)
(Presing et a!., 1996; Ryan et a!., 2003). Laboratory data showed that at a fixed SRP supply, the biomass in cultures developed similarly, irrespective of the amount and por tioning of available nitrogen forms. Added ammonium and nitrate was fully taken up by C. raciborskii, and the remaining nitrogen demand was met by N 2-fixation. It was suggested that the nitrogen fixation system stopped and was then activated again depending on the nitrogen content of the cells (Strober eta!., 2003). The fact that in Brazilian reservoirs, even at April May June low nitrate and nitrite concentrations, C. raci month borskii trichomes often do not develop hetero cysts and hence do not fix N was attributed to its Fig. 9. Comparison on monthly diversion discharge 2 (gray scale bars with SD) and rain (hatched bars) for preferential uptake of ammonium (Presing eta!., the Caernarvon Breton Sound estuaty. Height of the 1996; Bouvy et a!., 1999; Briand et a!., 2002). In diversion discharge was calculated from USGG dis any case the individuals from the Caernarvon charge data and a total area of the estuary of population regularly displayed heterocysts de 2 656.4 km . spite the often relatively high ammonia levels (Table 3). describes the situation in the lake-like structures CylindrospennojJsis raciborskii has the important within the Caernarvon Breton Sound estuary in competitive advantage of being extremely effi summer. Dense, often nitrogen-limited phyto cient at taking up and storing phosphorus plankton communities dominated in areas where (Shafik et a!., 2001). Compared to other cyano C. raciborskii was most abundant. Because the bacteria, its SRP uptake is four times and SRP species is diazotrophic, it compensates for low affinity is even an order of magnitude higher. DIN concentrations by fixing molecular nitrogen Blooms are sustained at SRP levels as low as 1-
29.8
29.7 N
29.6- 89.85 w 89.75 89.65 Fig. 10. Map of the Caernarvon Breton Sound estuaty with stations sampled in the 2002-2004 time series (x). Hatched arrows show major paths of diverted Mississippi water. The diverted water does not affect the dash dotted area to the Northeast. Cylindrospermopsis raciborsllii was detected in 2002 or 2003 in the area surrounded by the solid line and at one station in Lake Leaty (black dot). In 2004 the species occurred only in low numbers in the areas marked by dotted lines. https://aquila.usm.edu/goms/vol25/iss1/5 16 DOI: 10.18785/goms.2501.05 Rick et al.: The Invasive Cyanobacterium Cylindrospermopsis raciborskii in Sou RICK ET AL.-CYLINDROSPERMOPSIS RACIBORSKII IN SOUTHERN LOUISIANA 75
2 !lg-P liter -I (Istv;inovics et al., 2000). Average Anabaena circinalis (Baker and Humpage, 1994; SRP concentrations during surveys when C. Bowling, 1994). racibm:~hii was detected in the Caernarvon Breton Souza et al. (1998) describe shifts from C. Sound estuary were 25 to 50 times higher. No racibm:shii-dominated to green algal ( Scenedesmus difference was detected between stations featur sp.) dominated communities in Billings reser ing high abundances of C. raciborshii (average 51 voir, Brazil. In African lakes, Ramberg (1987) ± 5) and stations that did not (average 53 ± and Berger et al. (2006) monitored seasonal 28 !lg SRP liter -I). Hence, in this estuary C. dominance shifts from C. mciborshii toward raciborshii could not take advantage of its diatoms. High abundance of C. racibonhii is competitiveness regarding phosphorus utiliza frequently associated with reduced species rich tion. In Florida lakes, Dobberfuhl (2003) saw ness of the phytoplankton community (Branco negative correlations between C. racibm:~hii abun and Senna, 1996; Borics et al., 2000; Dobberfuhl, dance and dissolved total phosphorus (DTP: SRP 2003). The later findings are in line with our + DOP, dissolved organic phosphorus): C. results of lower percentages of both green algal raciborshii declined at DTP > 20 !lg liter- 1 and other chlorophyll (from heterokontophytes, whereas Microc)'stis gained maximum densities dinoflagellates, and prymnesiophytes) in sam at 80 !lg liter -I. The Chl a/DTP ratio (by weight) ples where C. racibm:~hii was detected. is considered a valuable parameter assessing plankton blooms with respect to the occurrence Interannual variability.-The spatial and annual of C. mciborshii (Dobberfuhl, 2003). In Florida temporal distribution of C. mciborshii in the lakes, blooms without C. raciborshii had low ratios Caernarvon Breton Sound estuary could be (> 0.5), whereas Chi a/DTP increased to almost attributed to an interplay of temperature, water two as the species got more abundant. column stability, and nutrient availability within For the Caernarvon Breton Sound the findings the estuary. Differences in the species' abun dance during the years 2002-05 (Fig. 1a,b; were comparable. Because DOP data were not Table I) remain to be explained. In 2002 and available we used the Chi a/SRP instead of the 2003 C. mcibm:shii was very abundant in parts of Chi a/DTP ratio. The Chi a/SRP ratios (by the estuary, which were not primarily affected by weight) were elevated in samples with high C. the diverted water (Fig. 10). In 2003, the year of raciborshii abundance (average: 0.98 ± 0.55) highest abundance, the species occurred already compared to samples with low or no abundance in June, whereas it appeared in 2002 and 2004 1 of the species (average: 0.68 ± 0.81) although mo later. Rabalais (2005) and Ren et al. (2005) the difference was not statistically significant. also reported high abundances of the species from the upper Barataria estuary (Lake Cat Planktonic parameters.-For both of the survey aouatche, Salvador, and des Allemands) in June areas (Atchafalaya, Caernarvon), +GYL samples 2003. showed significantly higher total chlorophyll and Compared to 2003, in 2004 and 2005 exten cyanobacterial chlorophyll levels compared to sively more water was diverted thru the estuary -GYL samples. Considering the ability of the before the potential biomass development of C. species to cope with low light and low nutrient raciborshii, exposing the species to less favorable situations (Branco and Senna, 1994; Shafik et al., conditions. Thirteen times the amount of 2003 2001), these results are in line with expectations. was discharged in the period from April to May Despite its relatively low chlorophyll content per in 2004 and even 30 times the amount of 2003 biomass unit (Dokulil and Mayer, 1996; McGre was discharged in the period from April to May gor and Fabbro, 2000), C. raciborshii is known to in 2005. In 2004 the species was detected first in 3 1 occur frequently or even dominate in high low abundances (25-50 X 10 cells liter- ) in an chlorophyll environments (Mayer et al., 1997; area not affected by the diverted waters (13 July, Bouvy et al., 1999, 2003a, b; Borics et al., 2000; Lake Amadee, Tanasia Lagoon; Fig. lb, mid Jones and Sauter, 2005). Often the species right panel). Then later in Aug., during a period occurs together with other bloom-forming cya of reduced diversion discharge (3.6% of maxi nobacterial genera, such as Oscillatoria, JVIicro mum capacity) it appeared in relatively low 3 1 cystis, Anabaena, AnabaenojJsis, Aphanizomenon, numbers (10 - 40 X 10 cells liter- ) in the and Raphidiopsis (Seenayya and Zafar, 1979; southeastern part of the estuary. Finally, during Ramberg, 1987; Hawkins and Griffiths, 1993; hvo surveys in summer and fall 2005 and monthly Domitrovic et al., 1998; Chellappa and Costa, campaigns in 2006 (April-Aug.) C. mciboshii 2003). In 2003 in the Grand Lake area it wa~ could no longer be recorded in the estuary. mainly associated with high densities of the Ephemeral occurrence of the species in sub potentially saxitoxin-producing cyanobacterium tropical and temperate regions is documented in
Published by The Aquila Digital Community, 2007 17 Gulf of Mexico Science, Vol. 25 [2007], No. 1, Art. 5
76 GULF OF MEXICO SCIENCE, 2007, VOL. 25(1)
the literature (Bouvy eta!., 1999; Hamilton eta!., 65 days of drought beginning on 17 March, 2005; Jones and Sauter, 2005) and in most cases yielding 4.3 em of rain. In 2004 the dry period is explained by climatic variability. Since the started very early (25 Feb.) and lasted for only species is not able to survive the lowered water 42 days, yielding 1.6 em, whereas in 2005 we temperature during winters suspended in the recorded an exceptionally late 53-d drought (7 water column, it relies on resting stages, so called April-29 May) with 6.5 em rainfall. akinetes, which are able to survive harsh envi The average minimal air temperature for April ronmental conditions in the upper sediment. was significantly higher in 2002, and for May was The existence of akinetes in the sediment is significantly higher in 2003 compared to the a prerequisite for the following thoughts. respective months of the other years within the CylindrosjJennojJsis raciborskii akinetes are only time series (Fig. llb; Table 5). In 2002 and able to germinate in a relatively narrow, but high 2003, the critical temperature for C. raciborskii temperature range (22-25 C). Favorable envi akinete germination was probably reached in the ronmental conditions following akinete germi first half of the dry season, enabling the akinetes nation, such as a relatively undisturbed water to germinate and giving the species a favorable column, low winds, and low rainfall, can foster environment for subsequent biomass build-up. mass development of the species (Padisak, 1997, In the low abundance year 2004 this critical 2003; Moore et a!., 2003, 2004, 2005). temperature probably did not occur in dry Comparing C. raciborsllii high-abundance season at all, and it was only reached late in (2002, 2003) and the low- or nonabundance the dry period 2005, exposing the species to less years (2004, 2005), temperature development favorable conditions for akinete germination. and weather factors influencing water column In 2003, the year of highest C. raciborskii stability seem worthy of consideration. The abundance, average winds during the time of development of important influencing parame possible akinete germination were significantly ters (cumulative rainfall, average daily wind lower compared to years of low or nonoccur speed, minimal daily air temperature) for these rence of the species (Fig. lla; Table 5). The fact years is shown in Figure 8. We choose the that April and May 2003 were much calmer development of the minimal daily air tempera compared to 2002, 2004, and 2005 is pro ture (5-d floating mean) as a proxy because time nounced by the frequency of low wind days ( < series data of water temperature at the sediment 6.5 km h-I). Almost half of the time showed low water intelface (important for akinete germina winds in 2003 whereas this percentage ranged tion) were not available. It is assumed that at from below 10% to 30% in the other years a minimal daily air temperature of 18.5 C (shown (Fig. lla). as a hatched line parallel to the time axis) the The fact that the species did not occur in the heating of the water column is sufficient to reach estuary in 2006 might be a side effect of the critical temperature for akinete germination Hurricane Katrina hitting the area directly at (22-25 C). the end of Aug. 2005. The estuary was complete The cumulative rainfall for the first 5 mo in ly flushed with salt water, and lake sediments the years of high C. raciborskii occurrence was were eroded to a huge extent. Akinetes resting 50% or even less compared to years of low and in the upper sediment layers were mixed into no occurrence (2002: 29.7, 2003: 24.9, 2004: the water column and flushed out or at least 61.9, 2005: 69.8 em). Average daily rain during exposed to elevated salinities that presumably periods of potential akinete germination (April killed them. Since the diversion structure was June) was also significantly lower in 2002 and closed completely after Katrina until mid:Jan. 2003 compared to 2004. In 2005 the average was 2006 (Chuck Villarrubia, pers. comm.), remain higher again, but because of a pronounced ing akinetes were exposed to high salinity variability it did not differ significantly from the conditions at least for 4.5 mo. From mid:Jan. to 2002 and 2003 values (Fig. lla; Table 5). mid:June 2006 the diversion structure was run at This underlines the hypothesis that rainfall relatively high discharge (50% more compared (rain deficit, lack of water renewal) is an to the period 2001-05), which also might not important parameter influencing the occurrence have been beneficial for potentially surviving of the species (Harris and Baxter, 1996; Domi akinetes. trovic eta!., 1998; Bouvy eta!., 1999, 2003a; Saker and Griffiths, 2001). Additionally differences in CoNCLUSIONS timing and duration of spring droughts over the years became obvious. The severe 2002 drought The occurrence of C. raciborskii in the Caer started 3 March and lasted for 76 days, with narvon Breton Sound estuary is influenced by an a total rainfall of 5.4 em. In 2003 there were interplay of water temperatures and timing of https://aquila.usm.edu/goms/vol25/iss1/5 18 DOI: 10.18785/goms.2501.05 Rick et al.: The Invasive Cyanobacterium Cylindrospermopsis raciborskii in Sou RICK ET AL.-CYLINDROSPERMOPSIS RACIBORSKII IN SOUTHERN LOUISIANA 77
a 12 7 70
10 6 60 ...... 5 50 ...... 8 'E ~J:: ~ e...~ c: E 4 40 ~ ·e c: ~ 6 Q) "C 3 >. 30 ::I c: 32 C" Q) Q) '3: 4 Q) ... 2 ;:: 20 ....
2 10
0 0 0 2002 2003 2004 2005 ''"""?"'<' wind 4-5 year c=1 rain 4-5 .. 0.. % < 6.5 km/h
b 25 ,r- 20 I r+ 0 +r+ 'L.. -+- c.. 15 E r+r++ ...... Q) 'iij c D D D B A B CB 10 -- .Es::: 5
0 4n 40 4M 4M sn 50 5M 5M month year Fig. 11. Oneway AN OVA based on meteorological data from the Caernarvon Breton Sound time series (2002- 2005). (a) Average daily "~nd speed and weekly cumulative rain for April-May is displayed along with SEM error 1 bars. White squares show the percentage of low-wind days (< 6.5 km h- ) in April and May. (b) Average daily minimal air temperatures with SEM error bars for April and May 2002-2005. Bars not connected by the same letter are significantly different.
water column disturbances, indicated by diver recorded highest biomasses and widespread sion discharge, rainfall, and wind speed. If the spatial abundance of CylindrospemwjJsis. In 2005 critical temperature for enabling akinetes to when the species was no longer observed, germinate is reached during times of low flushing during April to May was almost 30 times disturbance and this calm situation continues higher compared to 2003. for two or three additional weeks, these concli These results give some implications ti:Jr tions favor a rapid development of C. raciborskii. managing the water quality in the Caernarvon In addition to the meteorological conditions, Breton Sound estuary. If the water level of the the flushing effect by diverted waters seems to be Mississippi River permits it, the estuary should be of crucial importance. During the 2-mo time flushed thoroughly during April and May. period before the mass development of the Additionally, it would be beneficial to change species, only a small amount of Mississippi water the hydrology in the estuary in such a way that (ca. 6-8% compared to 2002 and 2004) was the Spanish Lake-Grand Lake area receives diverted through the estuary in 2003, the year we more of the diverted water. This would enhance
Published by The Aquila Digital Community, 2007 19 Gulf of Mexico Science, Vol. 25 [2007], No. 1, Art. 5 78 GULF OF MEXICO SCIENCE, 2007, VOL. 25(1)
TABLE 5. One-way ANOVA of abiotic parameters (average daily wind, weekly cumulative rain, min. daily temperature) for April-May 2002-05, Caernarvon Breton Sound estuary. Years/months not connected by the same letter are significant different (ex = 0.05). Wind (n = 244) and rain data (n 35) were pooled for both months [df (degrees of freedom)= 3]; temperature data (n = 244) were analyzed for each month (df 7).
Daily wind Weekly cumulative rain Daily minimum temperature
F-ratio 3.5346 2.2194 17.7836 Prob. > F 0.0155 0.1056 0.0001 1 Dimension [km h- ] [em] [C] Year/month 2002 (A) 2002 (B) April 2002 (C) May 2002 (B) Mean 10.67 0.47 17.96 20.3 SD 3.62 1.08 3.6 3.93 Year 2003 (B) 2003 (B) April 2003 (D) May 2003 (A) Mean 8.29 1.0 15.89 22.62 SD 5.73 1.68 4.62 2.55 Year 2004 (A) 2004 (A) April 2004 (D) May 2004 (B) Mean 10.16 4.48 15.33 20.22 SD 3.35 4.85 3.64 3.49 Year 2005 (A, B) 2005 (A, B) April 2005 (B) May 2005 (B, C) Mean 9.54 2.26 20.22 19.19 SD 3.92 4.69 3.49 3.04
the flushing of akinetes in these "seeding" areas BAKER, P. D., AND L. D. FABBRO. 1999. A Guide to the for Cylindrospermopsis and could also be used as Identification of Common Blue-Green Algae (Cya an active management tool to control potentially noprokaryotes) in Australian Freshwaters. In: Identi developing blooms of the species. fication Guide. J. Sonnerman and J. H. Hawking (eds.). Cooperative Research Centre for Freshwater Ecology, Thurgoona, NSW. AcKNOWLEDGMENTS ---, AND A. R. HuMPAGE. 1994. Toxicity associated with commonly occurring cyanobacteria in surface Funding for this study was provided by the waters of the l'vfurray-Darling Basin, Australia. Aust.J. Governor's Office of Coastal Activities-Gover l'l'far. Freshw. Res. 45:773-786. nor's Applied Coastal Research and Develop BERGER, C., N. BA, M. GuGGER, M. Bouvv, F. RuscoNI, A. ment Program (GOCA-GACRDP: Cl90364) and CoUT, M. TROUSSELLIER, AND C. BERNARD. 2006. the Water and Watershed Research Program of Seasonal dynamics and toxicity of CylindrospennojJsis the EPA/USDA/NSF (EPA Grant Number: raciborskii in Lake Guiers (Senegal, West Africa). R828009). Additional support came from the FEMS Microbial. Ecol. 57:355-366. Delacroix Corporation, the LSU Agricultural Bomcs, G., I. GRJGORSZKY, S. SzAn6, AND J. PAmsAK. 2000. Center, the Louisiana Department of Natural Phytoplankton associations in a small hypertrophic Resources, the U.S. Geological Survey, and the fishpond in east Hungary during a change from bottom-up to top-down control. Hydrobiologia. 424: Caernarvon Interagency Advisory Committee. 79-90. We would like to thank John Day, Robert Lane, BoiU.IANS, M., P. W. Form, L. FABBRO, AND G. HANcocK. and Robert Twilley for providing nutrient data 2004. Onset and persistence of cyanobacterial and fieldwork logistics. Special thanks to all the blooms in a large impounded tropical river, Aus colleagues who helped with the fieldwork: Roger tralia. Mar. Freshw. Res. 55:1-15. Holland, Justin Baker, Daniel Bond, Dane Bouvv, M., D. FALcAo, l'vf. MARINHO, M. PAGANO, AND A. Dartez, Jason Day, and Emily Hyfield. MouRA. 2000. Occurrence of Cylin ---,---, ---, ---, AND --- 2003b. controls, and management implications. Lake Re Ecological approach of the water quality in reservoirs serv. Manage. 19:341-348. located in the semiarid region of the State of DoKULIL, M. T., AND ]. .tvlAYER. 1996. Population Pernambuco (Northeast Brazil). Secheresse (Mon dynamics and photosynthetic rates of a CylindrosjJeJc trouge). 14:85-93. mopsis-Limnothrix association in a highly eutrophic BowLING, L. 1994. Occurrence and possible causes of urban lake, Alte Donau, Vienna. Algol. Stud. 83:179- a severe cyanobacterial bloom in Lake Cargelligo, 195. New South Wales. Aust. ]. Marine Freshw. Res. DOMITROVIC, Y. Z. DE, V. M. 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