An Unusual and Massive Bloom of Tetraselmis Sp.
in the Valparaiso Bay, Chile
Marlene Pizarro1*, Rodolfo Iturriaga2, Alejandro Silva3 and Sonia Gallegos4
1Centro de Investigación y Gestión de Recursos Naturales (CIGREN), Universidad de Valparaíso, Chile
2Department of Biological Sciences, University of Southern California, USA
3Department of Oceanografia Física, Universidad Católica de Valparaíso, Chile
4Naval Research Laboratory, Ocean Sciences, USA
Submission: March 26, 2018; Published: May 24, 2018
*Correspondence author: Marlene Pizarro, Centro de Investigación y Gestión de Recursos Naturales (CIGREN), Universidad de Valparaíso, Chile.
How to cite this article: Marlene P, Rodolfo I, Alejandro S, Sonia G. An Unusual and Massive Bloom of Tetraselmis Sp. in the Valparaiso Bay, Chile. Oceanogr Fish Open Access J. 2018; 7(4): 555717. DOI:10.19080/OFOAJ.2018.07.555717
An intense bloom of Tetraselmis sp., producing strong water discoloration was observed from December 28th of 2005 through January 10th of 2006 in the Valparaiso Bay (32º 57’S; 71º 33’W). Blooms of Tetraselmis sp. have never been reported in this bay, or along the coast of Chile. The confluence of a series of environmental conditions observed before and during the bloom such as: high solar radiation, anomalous UV radiation levels, high sea surface temperatures, water stratification and high nutrient concentrations may have contributed to the development of this unique event.
Keywords:Bloom tetraselmis sp; High solar irradianc; Positive UV anomaly; Valparaiso bay; Chile
Algal blooms are recurring events in coastal regions frequently associated with high nutrients concentrations, particularly of phosphorus and nitrogen. In the Valparaiso Bay, southwesterly winds prevail during the spring and early summer producing upwelling conditions and sporadic phytoplankton blooms, often composed by small diatoms . Blooms of Tetraselmis sp., a microflagellate of the group Prasinophyceae, have never been observed in the Valparaiso Bay waters, or along the coast of Chile. In the Southern Hemisphere only two massive Tetraselmis sp. blooms, producing intense water discoloration have been reported; the first at the Frank Kitts Lagoon, Wellington Harbor, New Zealand on December 10th of 1993, the second at the Saldanha Bay, South Africa on January 15th of 2003 [2,3]. During the bloom at Frank Kitts Lagoon, Tetraselmis sp., reached concentrations from 7.7 x 102 to 1.9 x 103 cells mL-1, other small flagellates such as, Cryptomonas spp. and Pyramimonas spp. were observed at lower concentrations (3.2 x 102 to 5.5 x 102 cells mL-). Water surface temperatures were between 15 °C-15.8 °C, and this was the only environmental parameters measured. During the Saldanha bay bloom, only visual observations were reported. In the Northern Hemisphere, small blooms of Tetraselmis sp.
have been frequently observed during the summer at the site of
the Harmful Algal Bloom Monitoring Program of the Southern California Coastal Ocean Observing System, San Diego, California (SCCOOS).
The Valparaiso Bay Tetraselmis sp. bloom developed on December 28th of 2005, after a period of calm winds, high solar irradiance, and nutrient concentrations (Nitrates over 30μmL-1 and Phosphates 20μmL-1), cell densities were up to 300 x 103 cellmL-1. The bloom reached a large spatial distribution until January 6th, when nutrient concentrations were near depletion (Phosphates dropped between 0.8-0.3 30μmL-1 and Nitrates below detection). The bloom ended by January 10th of 2006.
The spectral absorption of suspended particulate matter Ap(λ) was determined according to Mitchell . Water samples (25ml, due to the high cell concentrations) were filtered onto
Whatman GF/F filters at low vacuum pressure (<2mmHg>). The
spectral absorption was determined with a double beam UV-VIS
Shimadzu-2500 spectrophotometer. A filter saturated with 0.2μm
filtered seawater was used as a blank reference. The contribution
of detrital particulates to the total Ap(λ) was determined according
to Kishino . The absorption coefficients were calculated using
the path-length amplification factor β(λ) described by Mitchell .
For data comparison, in situ chlorophyll a, was determined
using the relationship between the chlorophyll a specific
absorption coefficient (a*pchl a (λ)) and Ap(λ) at 675nm, as
follows: (a*pchl a (λ) = Ap(λ)/chl a). A specific absorption
coefficient of 0.02 for chlorophyll a was used, thereby making chl
a = Ap (λ)/0.02) [6,7]. Concentrations were expressed in mg chl
Ultra violet radiation (UVR) data were provided by the UV
monitoring Station Campbell CR 10X, located 60m above sea
level at the Universidad Federico Santa María (33°02’05’’S;
71°35’44’’W). This station is equipped with NR-LITE-CNR1
sensors. UVA and UVB levels are registered every 10 minutes
year-round. Sea surface water temperatures and wind data were
provided by the Servicio Hidrográfico y Oceanográfico (SHOA),
Armada de Chile, and the Gobernación Marítima de Valparaíso,
respectively. The first station is located at 33º 01’ 38” S, 71º
37’ 33” W, the second at 33º 01’ 22’’ S, 71º38’50’’ W (Figure 1).
Nutrient concentrations were reported by Collantes & Prado
. Data for water column temperatures and light attenuation
coefficients (Kd) determined with a Secchi disc, were provided by
the Universidad de Valparaíso.
An image acquired by the Moderate Resolution Imaging
Spectroradiometer (MODIS/AQUA), during a pass on January
9th of 2006 over the Valparaiso Bay, was utilized to estimate
Chlorophyll concentrations and geographical distribution. MODIS
level 1b products from this image were obtained from the NASA
archives and converted into Chlorophyll a, using the Automated
Processing System (APS) at the Naval Research Laboratory, Stennis
Space Center, Mississippi (NRL-SSC). This is a fully automated
software package able of processing data for most of the ocean
color sensors, delivering accurate Level III and IV products [8,9].
The bloom was unique for its magnitude and monoculture
type resemblance as shown by the Ap(λ) and shape of the spectra.
The Ap(λ) values reflect the cell concentrations and the shape of
the spectra, which highlights the absorption peaks of chlorophyll
a, at 440nm and 675nm, and chlorophyll b at 470nm and 650nm.
Chlorophyll b is distinctive of the Prasinophyceae taxonomic
group. These spectral markers were observed in all samples
during the bloom (Figure 2).
The contribution of detrital matter to the total Ap (λ) was low
(0.2 to 0.8m-1 at 350nm and less than half at 450nm), indicating
that cellular material was one of the main components within the
suspended particulate matter.
The maximum Ap (λ) values were observed at station
4 on January 4th. This site is located in the proximity of the
Marga Marga river small outfall, where conditions for a higher
proliferation of Tetraselmis sp. appeared to be optimal that day.
The lowest Ap (λ) values were observed at Station 1. Chlorophyll
a in vivo concentrations estimates ranged between 11 to 18mg m-3
at Station 1, between 78 to 142mg m-3 at Station 2, between 82
to 292mg m-3 at Station 3 and from 237mg m-3 to a maximum of
678mg m-3 at Station 4 (Figure 2).
During the pre-bloom period (December 14th through the
27th of 2005), UVA levels increased from 3.11 to 5.8mW cm-2 and
UVB from 15.49 to 30.31μW cm-2 (Figures 3 & 4). During the
bloom period (December 28th to approximately January 10th),
UVB radiation continued to rise up to 36.94μW cm-2 on January
6th of 2006, while UVA levels remained steady. During the pre-and
bloom periods, UVA and UVB reached their highest intensities at
Data collected from 2001 through 2006 during the months
of January and July were used to determine the patterns of UVR
levels at different times scales (daily, monthly, annually) and to
select the periods when the maximum and minimum UVA and
UVB intensities were above the average. At mid latitudes, the
months of January and July represent the highest and the lowest
solar radiation levels registered during all seasons. An anomaly
refers to values that are above average (positive anomaly), or
below (negative anomaly) within a period. The daily anomaly for
the Valparaiso bay was calculated using an average of the daily
UVA and UVB radiation levels.
During the pre-bloom period, short-term anomalies for UVA
and UVB were registered. However, during the bloom period the
magnitude of the positive anomaly for UVB remained in the order
of ~ 2.5 - 5μW cm-2, the UVA anomaly remained without major
changes at 0.5mW cm-2 (Figure 5).
The high Kd values observed in the coastal areas indicated that
Tetraselmis sp. cells reached their maximal growth at the surface
and remained in the upper surface during the bloom, restricting
the euphotic zone to the upper 3.5 meters. Photosynthetic activity
of non-motile phytoplankton (e.g., diatoms) unable to migrate
to the surface, may have been affected by the low light levels
prevailing below that depth (Figure 6). Previous Kd values for the
Valparaiso Bay fluctuated between 0.68m-1 and 0.1m-1.
During the pre-bloom period, sea surface temperatures
oscillated between 16 °C and 18.6 °C. During the bloom period,
they reached a maximum of 19 °C on January 6th (Figure 7).
A water temperature profile performed near the coast on
December 27th indicated that a distinctive thermocline had started
to develop at 16m depth. Taking into account that sea surface
temperatures continued to increase until January 6th, a shallower
thermocline and mixed layer are expected to have developed in
the coastal waters of the bay (Figure 8).
During the pre-bloom period, weak southwesterly (SW) and
northerly (N) winds predominated. Daily wind speed averaged
from 1.85ms-1 to 5ms-1, remaining calm during the bloom period.
By January 10th the wind direction (SW) increased over 13m s-1,
coinciding with the end of the bloom (Figure 9). Wind speeds
within the range of 15-10m s-1 generate upwelling conditions in
the Valparaiso Bay [10-14].
The MODIS/AQUA image illustrates the extent and
distribution of the bloom spreading latitudinally along the coast
of the Valparaiso Bay from 32° to 34° N, and longitudinally
from the coast line to 72° W. As a result of the high chlorophyll
concentrations in the coastal waters (above 4.0mg m-3), the color
gradient fell out of scale. In offshore waters, chlorophyll estimates
were in the range of 0.2mg m-3, with fringes extending to the north
and south. However, no in situ chlorophyll determinations were
performed to cross-validate these estimates (Figure 10).
There was an indication of a clockwise circulation delineated
by the chlorophyll concentrations between 1 and 2mg m-3. The
presence of such cold eddies may have had some role in the
encroachment of coastal waters during the pre- and bloom periods.
Outside of the eddy-like circulation, chlorophyll concentrations
were below 0.5mg m-3, values commonly observed in offshore
waters of this region. However, due to the extensive cloud cover,
common along the coast of Chile, it was not possible to follow the
development of eddies from satellite imagery.
The Valparaiso Bay Tetraselmis sp. bloom occurred in the
middle of the summer season of the southern hemisphere. The
bloom developed rapidly after a period of wind relaxation, high
solar irradiance, higher water temperatures, stratification of the
upper water column, as well as high nutrient concentrations.
The confluence of all these factors, in addition to a positive UVR
anomaly may have provided a unique scenario for the development
of this massive bloom.
A comparison of previous records of sea surface temperatures
in the Valparaiso Bay during December and January indicated an
average within 15-17 °C [11,14]. During the pre-bloom period
of Tetraselmis sp., sea surface temperatures registered 18 °C,
reaching 19 °C during the bloom. Nutrient concentrations during
the pre-bloom period was in the order of 30μm L-1 and 46μm L-1
for nitrate and phosphate respectively. Such high concentrations
facilitated the high cell density observed along the coast of the
bay during the bloom. At Station 4, cell concentrations reached
300 x 103 cell mL-1, with chlorophyll a values of 642mg m-3. These values superseded an intense red tide bloom of Lingulodinium
polyedra observed in La Jolla, California, in 1995, where cell
concentrations reached 20 x 103 cell mL-1 and surface chlorophyll
a exceeded 100mg m-3, with one observation reaching 500mg m-3
. Several dinoflagellate blooms with cell concentrations in
the order of 2 x 103 cell mL-1 and chlorophyll a values of 500mg
m-3, were reported for this same area during 1964, 1965 and
1966 . In the Valparaiso Bay, during a typical spring season
upwelling, previous data for nutrient concentrations indicated
values between 3 and 9μmL-1 for nitrate and between 2 and
3μmL-1 for phosphates. However, chlorophyll a concentrations
fluctuated between 0.9 to 31mg m-3 . During the Valparaiso
Bay pre-bloom period nitrates and phosphates reached values
over 30μmL-1 and 20μmL-1. Wind speed measured during the preand
bloom periods remained calmed facilitating water column
stratification, only near the end of the bloom wind speed reached
values over 13m s-1, typical upwelling conditions for the Valparaiso
Bay develop when wind speeds reach between 15 - 20m s-1 .
The high attenuation coefficient, Kd (m-1), observed during
the Valparaiso Bay bloom indicated that Tetraselmis sp. cells
proliferated and remained approximately in the upper 3 meters.
Photosynthetic activity of non-motile species (e.g. diatoms)
unable to migrate to the surface may have been affected by the
low light levels prevailing below that depth (Kd values at Station 1
and station 4, between 1.5m-1 to 3.5m-1, respectively). The values
were much higher when compared to previous Kd measurements
for the bay that fluctuating between 0.68m-1 and 0.1m-1 .
Another factor to be considered was the high UVR levels
and positive UV anomaly observed before and during the bloom.
Photosynthesis is affected by the levels of photosynthetically active
radiation (PAR: 400–700nm) and ultraviolet radiation (UVR: 290–
400nm) penetration in the upper water column. Excessive PAR
and UVR inhibit photosynthesis and damage cellular components
[17-22]. UVB (290nm-320nm) radiation has raised concerns
for its effects on marine ecosystems [23,24]. An increase in UVB
can alter species composition and standing crop of microalgae
[25-27]. Though, species with micosporin-like-aminoacids
(MAA) cellular content are more tolerant to higher UVB levels
[24,28-30]. Previous studies have indicated that Tetraselmis sp.
is able to sustain and grow under higher UVR levels than other
phytoplankton. Experimental data showed no evidence of delay in
cellular division of Tetraselmis sp. under solar radiation dosages
of 416cal cm-2 d-1 for five days, showing a high tolerance to UVR
. Furthermore, a study about the relative sensitivity to UVB by
Tetraselmis suecica, showed no inhibition to dosages of 0.4 Wm-2
. These studies suggest that under experimental conditions
this specie is tolerant to higher UVR levels [32,33]. However, the
extent of UVR damage to the phytoplankton community, has not
yet been resolved .
Information about Tetraselmis sp. massive blooms are
restricted to the few previous observations, they are also limited
by the lack of long-term oceanographic data available, including
the one observed at the Valparaiso Bay. Therefore, it is difficult
to formulate unambiguous conclusions without falling into
speculations. Although, we can assume that the simultaneous
confluence of high solar irradiances, sea surface temperatures,
water column stratification, high nutrient concentrations, and a
positive UV anomaly after a period of wind relaxation, facilitated
the rapid growth Tetraselmis sp., outpacing other species. A
relevant feature about this bloom, was provided by the MODIS/
Aqua image revealing the magnitude and distribution of this
bloom. What remains unknown is the phytoplankton composition
beyond the Valparaiso Bay coastal waters.
We thank Drs. Mario Caceres, Roberto Prado and Gloria
Collantes, Facultad de Ciencias del Mar y Recursos Naturales,
Universidad de Valparaíso, Drs. Roberto Sota and Luis Da Silva,
Universidad Santa Maria. We also thank the Servicio Hidrográfico
y Oceanográfico de la Armada de Chile and the Gobernación
Marítima de Valparaíso for their collaboration. We extend our
gratitude to the NRL’s Slope to Shelf Energetics and Exchange
Dynamics project and Mr. S. Ladner for MODIS data processing.
This work was supported by the MECESUP-Chile Program.