Tetraselmis sp. algal bloom and bio-oceanographic variables off Puntilla de Santa Elena-Ecuador during May 2018.

Bloom algal de Tetraselmis sp. y variables bio-oceanográficas frente a la Puntilla de Santa Elena-Ecuador durante mayo de 2018

Torres, Gladys; Recalde, Sonia; Salazar, Elsa; Narea, Richard; Lopez, Freddy

Gladys Torres

gladys.torres@inocar.mil.ec

Oceanographic and Antarctic Institute of the Navy Ecuador

Sonia Recalde

sonia.recalde@inocar.mil.ec

Oceanographic and Antarctic Institute of the Navy Ecuador

Elsa Salazar

elsa.salazar@inocar.mil.ec

Oceanographic and Antarctic Institute of the Navy Ecuador

Richard Narea

richard.narea@inocar.mil.ec

Oceanographic and Antarctic Institute of the Navy Ecuador

Freddy Lopez

freddy.lopez@inocar.mil.ec

Oceanographic and Antarctic Institute of the Navy Ecuador

ACTA OCEANOGRAFICA DEL PACÍFICO

Instituto Oceanográfico y Antártico de la Armada, Ecuador

ISSN: 1390-129X

ISSN-e: 2806-5522

Periodicity: Semestral

vol. 4, no. 2, 2022

acta.oceanografica@inocar.mil

Received: 05 April 2022

Accepted: 08 June 2022

URL: http://portal.amelica.org/ameli/journal/648/64835846483584006/

Non-profit publishing model to preserve the academic and open nature of scientific communication

ePub generated from XML JATS4R

Abstract: On May 5, 2018, an intense green bloom caused by Tetraselmis sp. was evidenced 10 miles off the coast off the Santa Elena peninsula, the same bloom that has been recorded along the coastal edge of the provinces of Santa Elena and Manabi since April 23, 2018. Samples were collected for the determination of phytoplankton components, and simultaneously multidisciplinary data between 0 and 50m depth, characterizing the physical, chemical and biological variables during the algal bloom, being a first report 10 miles offshore. During the bloom, the abundance of Tetraselmis sp. was observed, with a decrease in diatoms and an increase in dinoflagellates, which favored the proliferation of euphausiids (calyptopis stage) with the presence of other zooplanktonic groups. Monitoring of satellite chlorophyll concentrations off the coast of Ecuador showed that the algal bloom began in mid-March and ended in mid-May, which coincided with local reports of the intense green color of the sea. The limits of the thermal variables corresponding to tropical waters with ranges between 19.79 to 25.05 °C with a thermocline at 15 m, with a nitrate and silicate nutricline located near 25 m that favored the slight increase of Tetraselmis sp. at 20 m, a species that has been used massively in culture for food in the larval laboratories recorded in the coastal area off both provinces.

Keywords: Algal bloom, Tetraselmis sp., biooceanographic variables, Santa Elena..

Resumen: El 5 de mayo de 2018 se evidenció una intensa floración de color verde causada por Tetraselmis sp. a 10 millas de la costa frente a la península de Santa Elena, la misma que se ha venido registrando en el borde costero de las provincias de Santa Elena y Manabí desde el 23 de abril del 2018. Se recolectaron muestras para la determinación de los componentes del fitoplancton, y simultáneamente los datos multidisciplinarios entre 0 y 50m de profundidad, que caractericen las variables físicas, químicas y biológicas durante el bloom algal, siendo un primer reporte a 10 millas de la costa. Durante el bloom se observó la abundancia de Tetraselmis sp., con disminución de diatomeas e incremento de dinoflagelados, lo cual favoreció la proliferación de eufáusidos (estado de calyptopis) con presencia de otros grupos zooplanctónicos. En el seguimiento de las concentraciones de clorofila satelital frente a las costas de Ecuador se observó que la floración algal se inició a mediados de marzo y terminó a mediados de mayo, lo cual fue coincidente con los reportes locales de la tonalidad verde intensa del mar. Los límites de las variables térmicas correspondientes a aguas tropicales con rangos entre 19.79 a 25.05 °C con una termoclina a los 15m, con una nutriclina de nitrato y silicato ubicada cerca de los 25m que favoreció el ligero incremento de Tetraselmis sp. a 20 m, especie que ha sido utilizada masivamente en cultivo para alimento en los laboratorios de larvas registrados en el área costera frente a ambas provincias.

Palabras clave: Bloom de Algas, Tetraselmis sp., variables biooceanográficas, Santa Elena.

Introduction

In the oceans, plankton ecological indicators can be measured using a variety of observing systems including remote sensing of ocean color in chlorophyll overestimation in support of coastal marine ecosystem condition assessment (Racault et al., 2014). Temporal and spatial monitoring by bio-optical techniques of harmful algal blooms in aquaculture areas is a crucial component because of the accumulation of large algal cell biomass (Busch, 2013).

The use of microalgae in aquaculture is a fundamental component for feeding mollusk, crustacean and fish larvae. In this regard, the alga Tetraselmis chuii has been widely used due to its nutritional and commercial importance (Ha-Le, 2000; Acosta and Moreira, 2013). During the protozoan stage they are basically fed by phytoflagellates and diatoms (Mallo & Fenucci, 2004). Among the main genera of microalgae used in aquaculture are: Skeletonema, Chaetoceros, Isochrysis, Pavlova, Tetraselmis, Chlorella, Dunaliella, among others (Helm & Bourne, 2004; Alvarado & Romero, 2008; Osuna, 2015). The most commonly used monospecific algae are Chaetoceros gracilis and Tetraselmis spp. (Calderón, 1993).

Shrimp larval production laboratories basically have sections for maturation, larviculture, algae culture (strains and massive) and Artemia (Calderón, 1993); they are located mainly in Santa Elena and Manabí with 61% and 25%, respectively (Alvarado and Romero, 2008). The high demand for larvae generated pressure on laboratories, and in some cases, biosecurity failures have been detected that caused mortality of 20% to 70% in rearing tanks generated by bacterial presence (Mendoza, 2018).

The local press and the newspapers El Mercurio/El Telégrafo reported that on the coasts of Santa Elena and southern Manabí an excessive proliferation of microscopic algae has been observed, causing an intense green coloration of the sea (Photo 1), possibly due to the unusual abundance of nutrients. The algal bloom is not toxic, so there is no reason not to swim in the sea or eat seafood from the area.

Figure 1
Figure 1.

Intense green color of the sea at Playa Rosada.

Therefore, the objective of this research was to disseminate the description of bio-oceanographic variables during the first algal bloom of Tetraselmis sp. that caused an intense green discoloration on May 5/2018, during the monthly monitoring 10 nautical miles off Santa Elena puntilla conducted by the Oceanographic and Antarctic Institute of the Navy (INOCAR).

Materials and methods

The study area was the fixed station located 10 nautical miles off Santa Elena (Figure 1), with an approximate depth of 100 m, is the most salient coastal edge of the southeastern Pacific Ocean of the Ecuadorian coast called Puntilla de Santa Elena, which corresponds to one of the monthly monitoring sites that INOCAR executes.

Figure 2
Figure 2.

Location of the fixed station La Libertad, in front of the Santa Elena Peninsula.

Sampling was carried out on May 5, 2018, on board a Coast Guard boat, collecting samples in the water column with Niskin bottle (5 L) at 7 depth levels (0, 10, 20, 20, 30, 40, 50 and 75m) in the morning hours between 08:00 and 10:00. To determine the different parameters (nutrients, phytoplankton and zooplankton) were carried out following standardized norms by the Chemistry, Physics and Biology Divisions of the Oceanography and Marine Meteorology Directorate of INOCAR.

Figure 3
Figure 3

Quali-quantitative phytoplankton sampling, where green seawater and zooplankton abundance were observed on May 5/2018.

Temperature and salinity were obtained with casts from a CTD-SBE19. Samples were collected at surface level with plankton nets (55 and 335 µm) for 10 minutes at 2 knots of speed and fixed with 4% formalin previously neutralized with borax. In the laboratory, phytoplankton taxonomy and environmental/oceanographic variables (Figure 3), proceeded according to Torres et al., (2017), INOCAR-ERFEN (2018), Guiry & Guiry, 2020. Zooplankton samples were separated into equal aliquots, using the Folsom separator (Mc Ewen et al. , 1954). Additionally, the obtained aliquot was poured into the Bogorov chamber for quali-quantitative analysis and with the help of a stereo-microscope the zooplankton analysis was performed. For the analysis of zooplankton communities, the keys of Trégouboff & Rose (1957), Boltovskoy (1981); Gasca & Suárez (1996), Palma & Kaiser (1993) were used, For a better interpretation of this event, in case of phytoplankton it was related to the abundance of functional groups and main genera recorded in May (2014, 2015, 2015, 2016, 2017); with zooplankton collected in April and June.

Figure 4.
Figure 4

Schematic of sampling methods and equipment.

Chlorophyll-a surface maps were analyzed from data available from the Copernicus-GlobColor satellite observation, which were downloaded and processed by reanalysis at 4km resolution, combining imagery from remote sensors (SeaWiFS, MODIS Aqua, VIIRS NPP, VIIR-JPSS1 OLCI-S3A and OLCI-S3B), in situ data (Argo, AERONET-OC) and cruise data from the British Oceanographic Data Centre, NASA SeaBASS repository, among others (Garnesson et al. 2021). Data dates corresponded to reports of the sea green algal bloom from local fishermen, technicians from the Instituto Nacional de Pesca (INP), local press and this research, in order to evidence the dynamics of the highest chlorophyll-a concentration off the coast of Ecuador and northern Peru up to 85°W latitude.

Results

Phytoplankton Structure and Distribution

The intense green color in the sea was caused by the bloom of Tetraselmis sp. with a density between 2021620 Cél.L-1 (08h00) at the beginning of the sampling without coloration and 14207886 Cél.L-1 (09h00) with coloration, with a green layer a few centimeters thick observed in the submerged net (Figure 2) coinciding when solar radiation was more intense; at 3m the algal density decreased with 42412 Cél.L-1 , then increased slightly at 10 and 20m (Table 1). Unlike the phytoplankton collected in the surface trawl (50 µm) also evidenced the dominance of Tetraselmis sp. 567000 Cél.m-3 near 9h40 (Figure 4-B).

Table 1

Table 1

Tetraselmis sp. density and environmental variables on May 5/2018.

The structure of the main functional groups of phytoplankton collected with Niskin bottle in May 2018, at the beginning (08h00) and after one hour evidenced a drastic algal increase composed of the "others" group, compared to May of other years (2014-2017) which dominated diatoms (centric and pennate) and with scarce dinoflagellates (Figure 4-A). Similar behavior was recorded in the surface net samples (Figure 4-B). In both samplings the "others" group was composed by the phytoflagellate Tetraselmis sp., it is a Chlorophyta with rapid growth intensifying a bright green color in almost 1 hour. In the other years from 2014 to 2017 diatoms have always prevailed over the other functional groups (Torres et al., 2017).

Figure 5
Figure 5.

Main functional groups of phytoplankton at surface level with Niskin bottle (A) and with 50 µm net (B), in May 2018.

In surface water samples, 23 species of phytoplankton were recorded (6 diatoms, 12 dinoflagellates and 2 as "others"); at the time of the event (9h00) only 9 species were recorded (7 dinoflagellates and 2 as "others"). Meanwhile, in net samples 33 species were recorded (9 diatoms, 24 dinoflagellates and 4 as "others"). This shows that during this event a total of 49 species were recorded with both methods. Diatom species were scarce with an increase in dinoflagellate species. On the other hand, it is worth mentioning that the Shannon diversity index during the bloom was very low with 0.10 bits/cel in water, and 0.225 bits/cel in net; while in the water column (0-50m) it registered variability with ranges between 3.99 to 0.45 bits/cel (Table 1).

During the bloom, the main diatom genera with both methods showed low algal density compared to the totals recorded in previous years (Figure 5-A). In contrast, the dinoflagellate group at the beginning (08h00) was more abundant than at (09h00), with slight abundance of Scripssiella sp. was more representative at the surface level (Figure 6-A); in the genera recorded in net some increased in 2018 compared to previous years (Figure 6-B). Tripos recorded 9 species with T. furca (= Ceratium furca) and T. muelleri (=Ceratium tripos) being more representative; Protoperidinium recorded 5 species with P. quarnerense being outstanding; other species such as Pyrophacus steinii, Choclodinium catenatum, Dinophysis caudata and D. doryphorum increased, species that in previous years were less representative.

Figure 6.
Figure 6

Main diatom genera at surface level with Niskin bottle (A) and with 50µm net (B), May 2018.

Figure 7
Figure 7.

Main dinoflagellate genera and Mesodinium ciliate at surface level with Niskin bottle (A) and with 50µm net (B), May 2018.

The distribution maps of the highest concentration of chlorophyll-a spectral absorption, showed in March 22 slight patches off the coast, on April 23 and May 5 high concentrations intensified both off the coast at 84°W and the coastal edge, including the remarkable change in the color of the sea in some tourist beaches (Photo 1); subsequently on May 25 it was decreasing (Figure 7). The chlorophyll maximums possibly correspond to the algal bloom caused by Tetraselmis sp.

Figure 8
Figure 8.

Evolution of surface chlorophyll from March 6 to May 25, 2018: in March 6 was without reports of the event, in March 22 already evidenced reports of the event by fishermen, in April 23 the event was reported by the INP, fishermen and local press reported the event, in May 1 corresponds to this research, in May 25 the event decreased.

Zooplankton Structure and Distribution

Zooplankton abundance was higher at the surface level with 180392796 Org/100m3 (Figure 8), composed of 19 taxa, represented with 99.9% by the Malacostraca group represented by Euphausiids in calyptopsis state (Guglielmo et al., 2015), while among "other groups" they represented 0. 1%. At the subsurface level (0-50 m) zooplankton abundance decreased to 115621 Org/100m3 with 22 taxa, with dominance of copepods (61%), followed by Euphausiids (29%), doliolum and quetognathids (3%), radiolarians (2%), among other groups (Figure 9). This zooplanktonic abundance was higher relative to April and June 2018 (Figures 8).

Figure 9.
Figure 9

Distribution of above and below ground zooplankton biomass in La Libertad May/2018.

Figure 10
Figure 10.

Relative abundance of the main zooplankton groups in La Libertad: surface (A) and vertical (B), May/2018.

Euphausiids constituted the dominant group of zooplankton, they are considered indicators of cold waters and are a food source for numerous marine resources, being a link between phytoplankton production and higher levels (Antezana, 1978).

Oceanographic Physical-Chemical Conditions

Regional oceanographic thermal conditions during the first week of May showed a strengthened Equatorial Front in front of Puntilla Santa Elena and Manta. At the subsurface level, there was an increase in temperature in May compared to April, with a thermocline between 10 and 20m corresponding to tropical waters, with temperature ranges between 25.05 to 19.79 °C above 20m; and salinity showed a slight increase in May (Figure 10).

Figure 11
Figure 11

Regional distribution of surface temperature from 3 to 7 May (data obtained from UK Met Office data, GHRSST/OSTIA L4, UKMO/NASA/JPL/PO-DAAC); subsurface distribution of temperature and salinity at the fixed station off St. Helena Peninsula and its variability from January to May 2018.

At the surface level, nitrate and phosphate showed minimal concentrations, possibly due to algal bloom consumption, while silicate showed high concentrations; at the subsurface level, nutrients increased without registering a well-defined thermocline (Figure 11). When related to previous months, in February high concentrations of nitrate and phosphate were observed with a nutricline (20 to 40m) coinciding with the lower edge of the thermocline. These nutrients must have possibly surfaced between February and March, which must have strengthened and maintained the algal bloom during this period until May.

Figure 12.
Figure 12

Surface and subsurface distribution of nitrate (A), phosphate (B) and silicate (C) ug/at/l, from January to May 2018.

Discussion

Scarce evidence of blooms formed by this genus of Tetraselmis has been recorded. Arora et al., (2013) indicates that many Tetraselmis species have been described as endosymbionts and are economically important for mass culture because they are euryhaline and eurythermal in nature, sometimes causing blooms in some bays, research is lacking in tropical areas and atypical or extreme environments. Currently 36 species of Tetraselmis are known (Guiry & Guiry, 2020). In Chile, from December 28, 2005 to January 10, 2006 they reported the bloom of Tetraselmis sp. , coinciding with the onset of upwelling (Pizarro et al., 2018). Tetraselmis striata has been targeted for bio-diesel production near Korea, but the environmental impacts are not yet studied (Sae-Hee et. al., 2020). Daoudi et al., (2012) mentioned that when there is higher pollution (excess of N, P, Si) evidenced the disappearance of local phytoplankton and favor the proliferation of Tetraselmis sp.

Since mid-March and May/2018 off the coasts the provinces of Santa Elena and southern Manabi, local fishermen reported the sea of intense green color, the results of the technicians reported that these events were caused by Tetraselmis sp. (Macias et al, 2018; Prado et al; 2020). In this research of May 5/2018 during the intense bloom (09h30) no diatoms were found and dinoflagellates decreased at the surface level; in net sample an increase of some dinoflagellates was recorded. The high density of Tetraselmis sp. recorded with both collection methods (Niskin and net) mainly in the surface layer, contributed with food availability that favored the abundance of euphausiids, while other groups such as copepods, cladocerans, decapod larvae, and quetognathans, among others, recorded minimum percentages. The abundance of euphausiids during and after flowering of Tetraselmis" reported by Prado et al., 2020, was also coincident with this study. The distribution of euphausiids is often associated with thermal characteristics, upwelling or fronts characterized by high productivity. The abundance of phytophagous fish egg stages and larvae recorded at Punta Carnero was a response to food availability by Tetraselmis sp. (Prado et al., 2020). In May/2018 off Salinas, an abundance of small pelagic fish was observed and coincided with the reproductive activity of adult individuals with hydrated gonads evidencing spawning process (INOCAR-ERFEN, 2018). Ormaza (2018), mentions that fish populations should benefit from nutrients derived from the Humboldt and Cromwell Currents, when the various phytoplankton species bloom.

Additionally, on March 25/18 in Santa Elena Bay (Salinas and La Libertad) red tide patches caused by Gymnodinium catenatum were reported; the other red tide event on April 16/18 occurred off San Pedro in CENAIM-ESPOL was caused by Chlocodinium catenatum, both events were of short duration (Torres et al, 2018).

Regarding environmental variables, Martín & Rivera (2010) mentioned the use of algae cultures including Tetraselmis sp. between 1985 and 1999, with salinity between 33 to 35 ups and temperature between 28 to 32 °C. Arora et al. , (2013) also report that Tetraselmis tolerates wide temperature ranges 28 to 48°C and hypersaline conditions between 35 to 350 ups. Ha-Le (2000) mentions at laboratory level Tetraselmis sp. tolerates a wide range of salinity and prefers high salinity between 35-45 ppt; the optimum temperature was 28°C, N concentration for growth was 7.36 to 22.36 mg/l, and phosphate was 0.77 to 3.27 mg/l.

In May 2018, the bloom of Tetraselmis sp. recorded eurythermal characteristics with low nutrient content due to possible nutrient consumption. Marín (2016) calculated the climatology of sea surface temperature (SST) with 22 years of monthly sampling at the station off La Libertad, showing that SST have their maximum values in February and March, declining to their minimums in August. Recalde (2014) presented that the climatology of salinity has a somewhat different behavior, its maximums are in May - June to decay with the minimum in November, showing that the annual variation of salinity does not respond to the contribution of the rainy season in the area of the peninsula of Santa Elena.

Ormaza (2018), mentions that elevated nutrient conditions caused the bloom of Tetraselmis sp. which due to their high concentrations of lipids and proteins are used in mega-cultures in aquaculture laboratories, as occurs in shrimp larvae laboratories along the coast of the Santa Elena Peninsula. In Ecuador, there are approx 200 laboratories that produce shrimp larvae that have been operating since the late 1990s such as Texcumar, Aquatropical among others; which use intensive microalgae cultures (Calderón, 1993; Alvarado & Romero, 2008) and that due to possible poor biosecurity procedures has caused larval mortality (Mendoza, 2018).

Conclusions

The algal bloom of Tetraselmis sp., was the first algal event on the coasts of Manabi and Santa Elena produced on May 5, 2018 10 miles offshore corresponded to in the surface layer (< 1m), with reduction of diatoms and slight frequency of dinoflagellates. Previously local fishermen observed green patches on April 23 and reports from the National Fisheries Institute, which was reflected in the satellite chlorophyll high patch tracking that presented a shift coincident with the position of the Equatorial Front in a meridional manner between 85°W and 82°W, evidencing that the event started in mid-March and ended in mid-May 2018.

The bloom conditions favored the abundance of euphausiids in the 99.99% calyptopis stage, with the presence of copepods, cladocerans, decapod larvae, quetognathans and other zooplanktonic groups.

Tolerance limits to thermal variables were wide between 19.79 to 25.05 °C with a thermocline at 15m, while in the vicinity of the nitrate and silicate nutricline located near 25m favored the slight increase of Tetraselmis sp. at 20m.

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