Population fluctuations of Pyrodinium bahamense and Ceratium furca Dinophyceae) in Laguna Grande, Puerto Rico, and environmental variables associated during a three-year period
Miguel P. Sastre1*, Efraín Sánchez1,2*, Marineé Flores1,3*, Samuel Astacio1,4*, Julianna Rodríguez1, Melissa Santiago1, Karina Olivieri1, Veronica Francis1 & Juan Núñez1
*Dirección para correspondencia: Abstract ]]>
Fluctuaciones poblacionales de Pyrodinium bahamense y Ceratium furca (Dinophyceae) en Laguna Grande, Puerto Rico, y variables ambientales asociadas durante un periodo de tres años. Bioluminescent bays and lagoons are unique natural environments and popular tourist attractions. However, the bioluminescence in many of these water bodies has declined, principally due to anthropogenic activities. In the Caribbean, the bioluminescence in these bays and lagoons is mostly produced by the dinoflagellate ]]>
Resumen ]]>
Este estudio describe parámetros de calidad de agua y fluctuaciones en la densidad poblacional de Pyrodinium bahamense Plate 1906 y Ceratium furca (Ehrenberg) Claparède & Lachmann 1859, los dos dinoflagelados más abundantes en las bahías y lagunas bioluminiscentes de Puerto Rico, durante un periodo de tres años, en Laguna Grande, Puerto Rico. En P. bahamense se observó un patrón de densidad poblacional, donde se ]]>
las densidades más altas mayormente desde abril hasta septiembre y las más bajas desde octubre hasta febrero. En C. furca las fluctuaciones en densidad fueron más erráticas y no se observó un patrón repetitivo. La densidad poblacional promedio de P. bahamense (media=18 958.5 células/L) fue significantemente mayor que la de C. furca (media=2 601.9 células/L). No se encontraron diferencias significantes entre las muestras de superficie y las de 2m de profundidad para temperatura, fosfatos, nitratos, salinidad, ]]>
La densidad poblacional media de P. bahamense y C. furca en Laguna Grande está dentro del rango de las densidades que han sido reportadas para otras lagunas bioluminiscentes en Puerto Rico y Florida, EE.UU.
Palabras clave: Pyrodinium bahamense, Ceratium furca, Laguna Grande, Puerto Rico, bioluminiscencia, lagunas bioluminiscentes. Bioluminescent bays and lagoons are economically important as tourist attractions (González-Sánchez, Muñoz-Salinas & Roset, 2012). The bioluminescence in many of these water bodies have declined ]]>
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Caribbean bioluminescent bays and lagoons are usually bordered by highly productive mangrove communities (Seliger, Carpenter, Loftus, Biggley & McElroy, 1971), which release large quantities of nutrients into adjacent waters (Odum, McIvor & Smith, 1982; Lee, 1995). Nitrates, phosphates, B vitamins (Burkholder & Burkholder, 1958), humic substances (Prakash & Rashid, 1968; Carlsson & Granéli, 1993) and other nutrients, help to sustain the highly productive (Burkholder, Burkholder, ]]>
Dinoflagellate bioluminescence is a defensive behavior that reduces grazing (Esaias & Curl, 1972; White, 1979) by affecting the behavior of animals that feed on them (Buskey & Swift, 1983; Buskey et al., 1983). In addition, it may serve as a “burglar alarm” to attract a secondary predator that threatens to eat the primary predator (Morin, 1983; Young, 1983). ]]>
Margalef (1961) proposed a general water circulation mechanism for Bahía Fosforescente (Puerto Rico), in order to explain the retention of P. bahamense var. bahamense, as well as other phytoplankton. Inshore winds, aimed towards the inside of bioluminescent bays, can also create hydrological conditions leading to high water retention times in the shallower innermost portions of these water bodies (Seliger et al., 1971). This could also contribute to the retention of nutrients and phytoplankton.
P. bahamense var. bahamense has been reported and/or studied in several bays and lagoons in tropical and subtropical Atlantic waters, including Fire Lake (near Nassau), Bahamas (Harvey, 1952); Oyster Bay, Jamaica (Seliger & McElroy, 1968; Seliger et al., 1970); and Tampa Bay (Steidinger, Tester & Taylor, 1980; Phlips et al., 2006; Badylak, Phlips, Baker, Fajans & Boler, 2007), Florida Bay (Phlips & Badylak, 1996; Phlips et al., ]]>
The dinoflagellate, Ceratium furca (Ehrenberg) Claparède & Lachmann 1859 var. hircus (Steidinger & Tangen, 1997), can also reach very high densities in bioluminescent bays and lagoons in Puerto Rico, but is not bioluminescent. C. furca is cosmopolitan and found from cold temperate ]]>
In Puerto Rico, population dynamics of P. bahamense var. bahamense and C. furca have been described in Bahía Fosforescente (also known as Bahía Bioluminiscente; Margalef, 1961; Seixas, 1983, 1988; Walker, 1997; Soler-Figueroa, ]]>
Even though the presence of P. bahamense var. bahamense has been reported for Laguna Grande (Candelas, ]]>
The goal of this study was to describe water quality parameters on density fluctuations of P. bahamense var. bahamense and C. furca, the two most abundant ]]>
Materials and Methods
Study site: Laguna Grande is a coastal lagoon located on the North-East coast of Puerto Rico. It is situated within a basin-type mangrove forest (sensu Lugo & Snedaker, 1974) and bordered by Rhizophora mangle (Linnaeus, 1753). The Lagoon is surrounded by the Cabezas de San Juan Natural Reserve, managed by the Conservation Trust of Puerto Rico (
Fig. 1).
The average depth of Laguna Grande is 3m and its maximum depth is 5m. It occupies an area of about 50ha and contains about 662 000m3 of water (Soler-López & Santos, 2010). The South-Eastern portion of Laguna Grande is connected to Las Croabas Bay by the Laguna Grande Channel, a 1.5km long channel (or tidal inlet) that averages about 5m across and 1m deep (Zayas, 1979; ]]>
Zayas (1979) reported salinity concentrations ranging from 20.5 to 36.2psu (mean=33.6psu), oxygen concentrations ranging from 2.0 to 7.2mg/L (mean=5.3mg/L), and phosphate concentrations ranging from 0.01 to 0.10μg-at /L (mean=0.03μg-at /L), for stations located in the center of the lagoon. The average flushing rate of Laguna Grande is 7.7d (Soler-López ]]>
Field methods: Three sampling stations were established in the central portion of Laguna Grande, using a Garmin® GPS model 73 (Station 1: 18°22’31.69” N - 65°37’28.98” W; Station 2: 18°22’34.93” N - 65°37’22.24” W; Station 3: 18°22’40.32” N - 65°37’26.31” W; Fig. 1). At each station, water samples were collected in triplicate using 500mL ]]>
The water temperature in each sample was determined immediately after collection using an alcohol laboratory thermometer. Water transparency was determined at each station using a 20cm diameter black/white quadrant limnological Secchi disk. All samples were collected during the daytime. The field sampling procedures lasted approximately two hours. ]]>
Laboratory methods: Water samples were taken to the laboratory within one hour after performing the field sampling procedures. Sample bottles were mixed by inversion in order to distribute the sample homogeneously. One 250mL sub-sample was taken from each sampling bottle for each physico-chemical parameter to be analyzed.
Chlorophyll-a was ]]>
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Nitrates and phosphates were analyzed using a calibrated and certified (Calitek, Inc., Bayamón, Puerto Rico) Hach spectrophotometer model DR-2000 (Hach Company, 1996a). Nitrates were analyzed according to Method 8192 (cadmium reduction method), and orthophosphates according to Method 8048 (ascorbic acid method; Hach Company, 1996b).
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Salinity was determined using a Fisher model 13-946-27 refractometer, calibrated with distilled water prior to analysis. Daily rainfall data was obtained from NOAA’s Paraíso station, located approximately 13km Southwest of the study area. Rainfall data was recorded using a Fischer Porter Rain Gauge. Cumulative precipitation was calculated for 3, 6, 9, 12, 15 and 18 day intervals before each sampling date.
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In order to preserve samples, each sampling bottle was mixed several times by gentle inversion. Immediately afterwards, a 248.5mL sub-sample was poured into a modified sedimentation chamber and preserved in 1% Lugol’s solution, making a final volume of 250mL. The preserved subsamples were allowed to settle by gravity for three days (Wetzel & Likens, 2000). Each subsample was concentrated to 100mL by carefully removing the supernatant with a pipette. The supernatant was gravity filtered through a 20µ Nitex® Nylon Bolt Cloth, and the cloth inspected for the presence ]]>
After mixing each 100mL concentrated plankton sample, one mL subsample was obtained, with an automatic volumetric pipet, and transferred to a Sedwick-Rafter (S-R) counting cell (Wetzel & Likens, 2000). The S-R cell was covered with a coverglass and all P. bahamense var. bahamense and C. furca were ]]>
A main effects three-way ANOVA was used to evaluate differences between months, sites and depths, for population densities of P. bahamense var. bahamense and C. furca, and for all physical-chemical parameters; except Secchi depth, which was evaluated using a two-way ANOVA (Secchi depth was measured vertically ]]>
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A multiple correlation was used to determine possible relationships among all variables (Sokal & Rohlf, 1994). Statistical analyses were performed using IBM® SPSS® Statistics 19 software (http://www.spss.com). Any correlation equal to, or less than 0.5 was considered significant.
Results
Temperature: The average water temperature during the sampling period was 29.1°C (SD=1.8, n=40; Table 1). The highest temperature (34.0°C) was recorded during August 16, 2003, and the lowest one, 24.3°C, during January 31, 2006. Kruskal-Wallis non-parametric tests did not detect significant differences between depths nor between sites (p>0.05). However, ]]>
Salinity: Salinity ranged from 18 to 42 practical salinity units (psu, Fig. 2). During strong rainfall events decreases in salinity were observed both in surface and 2m depth waters. During less severe events, decreases in salinity were observed ]]>
Table 2).
Water transparency: Average Secchi depth was 1.68m (SD=0.43, n=35; Table 1). It was positively correlated with salinity (r=0.385, df=33, 0.02<p<0.05) and negatively correlated with fluorescence (r=-0.634, df=34, p<0.001). The lowest ]]>
Table 2).
Rainfall: Daily rainfall at Paraíso Station ranged from 0 to 10.4cm (
Table 1). Cumulative 9-d, 12-d, 15-d and 18-d rainfall data (cumulative amount of rain recorded prior to each sampling occasion) was negatively correlated with salinity. Also, cumulative 6-d, 9-d, 12-d, 15-d and 18-d rainfall data was negatively correlated with fluorescence. Cumulative 9-d rainfall was negatively correlated with Secchi depth; and cumulative 3-d rainfall was correlated with phosphates (Table 3).
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The lowest salinity concentrations (18psu, Table 1), recorded during September 21, 2004, corresponded to the passage of Hurricane Jeanne on September 14 (22.9cm of rain in 24hr at the Paraíso station). The second lowest salinities, recorded during November 21, 2003, were caused by the heavy rains received during the occurrence of a tropical wave in November 13, 2003 (20.8cm of rain in 24hr at the Paraíso station). The highest salinity (42psu), recorded during April 1, 2005, corresponded with a period of ]]>
Figure 2). Even though periods of 7 and 8d had passed between the passage of Hurricane Jeanne, the tropical wave; and the sampling dates after those events, low salinity readings were still recorded at Laguna Grande.
Phosphates: Soluble ]]>
Fig. 3). Average SRP concentration was 0.08 mg/L (SD=0.10, n=41; Table 1). Kruskal-Wallis non-parametric tests detected significant differences between months (p<0.001) but not between depths or sites (p>0.05).
Nitrates: Nitrate ]]>
Table 1). ANOVA detected significant differences between months (p<0.001) but not between depths or sites (p>0.05, Table 2).
Fluorescence: The ]]>
Table 1) were observed during the low salinity dates of November 21, 2003; September 21, 2004; and May 26, 2005 (Fig. 4). During the first two peaks fluorescence was higher in the surface; however, during the third peak, higher readings were observed in the 2m depth samples. Fluorescence was negatively correlated with salinity (r=-0.802, df=40, p<.0001). ANOVA detected significant differences between months (p<0.001) but not between depths or sites (p>0.05, ]]>
Table 2).
Densities of P. bahamense var. bahamense and C. furca: ANOVA detected significant differences between months but not between stations or depths, for densities of P. bahamense var. bahamense and C. furca (Table 2). ]]>
Densities of P. bahamense var. bahamense ranged from 0.48 to 90 978 cells/L (Figs. 5and 6). Even though no seasonality was observed for P. bahamense var. bahamense density fluctuations, higher densities were observed from April to September and lower densities from October to February. ]]>
C. furca densities ranged from 0 to 11 200 cells/L (Figs. 5and 6). Population densities of P. bahamense var. bahamense were negatively correlated with C. furca densities during the first year of sampling (r=-0.576, df=13, .01<p<.05). During the third year of sampling they were positively correlated to each other (r=0.759, df=13, .001<p<.005). No significant ]]>
Discussion
Laguna Grande has ]]>
Fig. 1). The restricted water flow into the lagoon causes a 3.5hr delay between the tidal peaks in the ocean and the corresponding tidal peaks inside the lagoon (Soler-López & Santos, 2010). It is ]]>
In this study P. bahamense var. bahamense was observed at temperatures up to 34°C (range: 24-34°C), higher than what has been reported for other populations ]]>
A broader salinity range was observed in Laguna Grande (18-42psu) than in other bioluminescent water bodies in Puerto Rico (combined range: 32-39psu; Seixas, 1983 1988; ]]>
Since the geomorphological and hydrological characteristics of Laguna Grande can lead to water accumulation in the lagoon, we calculated cumulative rainfall (3, 6, 9, 12, 15 and 18 day intervals before each sampling date, using NOAA Paraíso station data) and correlated it with the ]]>
The non-significant correlations between the fluorescence values; and the densities of P. bahamense var. bahamense, and C. furca were possibly due to the fact that all the other photosynthetic planktonic microalgae in the lagoon were not considered in these analyses. The densities of P. bahamense var. bahamense and C. furca are only a portion of the total density of all ]]>
The non-significant differences detected in Laguna Grande, between surface and 2m depth samples, for temperature, salinity, phosphates, nitrates, fluorescence, and densities of P. bahamense var. bahamense and C. furca, suggest a vertically mixed water column. Relatively strong trade winds, combined ]]>
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The correlations between the density of P. bahamense var. bahamense and C. furca were performed to show numerical relationships between these species but not to infer predator-prey or competition relationships. However, significant negative correlations might indicate potentially competing species. The correlation was significantly positive during the first year of our study, significantly negative during the third year, but not significant over the entire three-year period. Similarly, Seixas (1983, 1988), Walker (1997) and Soler-Figueroa (2006) did not observe ]]>
Heterotrophic dinoflagellates of the genus Protoperidinium (Hansen & Calado, 1999), observed at low densities in Laguna Grande, might prey on C. furca and/or P. bahamense and may affect their densities. However, we have not detected this interaction in live phytoplankton samples from Laguna Grande.
During this study, the highest monthly mean density of P. bahamense var. bahamense was 90 978 cells/L (SD=39 431, n=6); and for C. furca was 11 200 cells/L (SD=6 601, n=6). Monthly mean densities of P. bahamense var. bahamense, up to 511 882 cells/L, and of C. furca, up to 25 613 cells/L, have been reported for Puerto Mosquito; and monthly mean densities of P. bahamense var. bahamense, up to 303 053 cells/L, and of C. furca, up to 830 199 ]]>
An attempt was made to compare the ]]>
Table 1), with those reported by Seixas (1983, 1988), Walker (1997), Soler-Figueroa (2006) and Phlips, Badylak, Youn & Kelley (2004, no data for C. furca). The mean population density of P. bahamense var. bahamense and C. furca in Laguna Grande is within the range of these other studies. The density of P. bahamense var. bahamense is higher than that of C. furca in Laguna Grande and Puerto Mosquito, but mostly lower in Bahía ]]>
In order to conserve the continuous P. bahamense var. bahamense populations in Laguna Grande, as well as most of its bioluminescence, it is important to maintain the existing ]]>
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In order to have more accurate measurements of density variations through time in Laguna Grande it is important to sample at more frequent intervals since the replication rate of P. bahamense var. bahamense and C. furca is much faster than the sampling interval used in this study.
Acknowledgments
We want to acknowledge the effort given by the following people who have helped during the field sampling, water analyses and/or other aspects of this study: Elizabeth Padilla, Arlyn Fuentes and Sandra Maldonado (Conservation Trust of Puerto Rico); Rufo Vega, Sylvia Vélez, Cedar García, Raymond Tremblay, Juan Morales, Jackie Vega, Jackeline Maldonado, ]]>
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*Correspondencia a: 1Miguel P. Sastre: Department of Biology, University of Puerto Rico at Humacao, Road 908 km 1.2, Humacao, Puerto Rico 00791; miguel.sastre@upr.edu 1Efraín Sánchez: Department of Biology, University of Puerto Rico at Humacao, Road 908 km 1.2, Humacao, Puerto Rico 00791. 2Department of Biochemistry, Purdue University, West Lafayette, Indiana 47907 USA; sanchee@purdue.edu 1Marineé Flores: Department of Biology, University of Puerto Rico at Humacao, Road 908 km 1.2, Humacao, Puerto Rico 00791. 3US Customs and Borders Protection, Homeland Security, Miami, Florida 33101 USA; marineeflores@gmail.com 1Samuel Astacio: Department of Biology, University of Puerto Rico at Humacao, Road 908 km 1.2, Humacao, Puerto Rico 00791. 4Amgen, Road 189, PO Box 4060, Juncos, Puerto Rico 00777; sastacio20@gmail.com ]]>
1Julianna Rodríguez: Department of Biology, University of Puerto Rico at Humacao, Road 908 km 1.2, Humacao, Puerto Rico 00791; canavalia.maritima@gmail.com 1Melissa Santiago: Department of Biology, University of Puerto Rico at Humacao, Road 908 km 1.2, Humacao, Puerto Rico 00791; seamelfly@gmail.com 1Karina Olivieri: Department of Biology, University of Puerto Rico at Humacao, Road 908 km 1.2, Humacao, Puerto Rico 00791; karinam75@hotmail.com 1Veronica Francis: Department of Biology, University of Puerto Rico at Humacao, Road 908 km 1.2, Humacao, Puerto Rico 00791; veronica_francis@live.com 1Juan Núñez: Department of Biology, University of Puerto Rico at Humacao, Road 908 km 1.2, Humacao, Puerto Rico 00791; ceratiumjuan@gmail.com
Received 14-IX-2012. Corrected 20-II-2013. Accepted 21-III-2013.
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