Mechanisms involved in the proliferation and distribution of phytoplankton in the Patagonian Sea, Argentina, as revealed by remote sensing studies

Studies about the mechanisms that control the dynamics of phytoplankton in terms of surface chlorophyll patches by means of remote sensing information were encouraged in the Patagonian Sea (South Atlantic Ocean). Over this sea, circulation of the Patagonian Current and Malvinas Current, originated in the Circumpolar Antarctic Current, has much to do in the distribution of algal biomass. The study confirms the existence of three ecosystems: Coastal system, Shelf waters system and Shelf break. In the former, algal blooms are detected mostly between March and August. Later, the patches move inside the shelf area, the second ecosystem, towards NNE direction from approximately August to December under the influence of the Patagonian Current to reach the Malvinas Current, which circulates along the shelf break. The third ecosystem, Malvinas system, may be divided into the Malvinas Islands, where an intense algal bloom from December to January could be verified, and the Malvinas Current that shows a high concentration of algal pigment in the same period, although evidences support the hypothesis that the latter has mainly an allochthonous character. At about 37°S–39°S and 53°W–56°W, variable position, the confluence between Malvinas Current and Brazil Current takes place. As a result, the chlorophyll that functions as a tracer indicates that the impact has the characteristics of being an elastic collision, since the Malvinas Current identity was preserved afterwards. Special events, such as the climatic conditions that prompt changes in the annual behavior of the phytoplankton distribution, are discussed.


Introduction
The purpose of this report about the phytoplankton biomass found in the Continental Patagonian Shelf in the South Atlantic Ocean (Fig. 1a) is to consider the chlorophyll photosynthetic pigment observed by satellite image.Studies on the mobility of sediments and materials in suspension on the Patagonian coastal area were made by Ulibarrena (1974).Studies on phytoplankton acquired the importance in this environment with the pioneer work of Carreto et al. (1985) that took advantage of satellite image in combination with in situ samples to investigate the death of two fishermen in 1980, due to intoxication by mussel ingestion containing toxic species identified as Gonyaulax excavate.Posteriorly, taking into account the importance of the phytoplankton for the rest of the members of the food chain, many other works referring to physical, chemical and biological variables associated with it have appeared (Carreto et al. 1985;Forbes and Garraffo 1988;Podesta ´1989; Research and Fishing Development (Instituto Nacional de Investigacio ´n y Desarrollo Pesquero, Argentina).
The advantage of using a spectrometer, mounted on a space platform for observing the sea surface, gives the possibility of instantly focusing on an overall area-synoptic view-for the perception of several simultaneous events in different parts of the area of interest.Moreover, the information so obtained can be available in a computer to be revised as often as desired.This exceeds by far the study which takes into account transects in aquatic environments that only record partial information ignoring what happens in very near areas.The instruments used to measure the sea color register the electromagnetic radiation that emerges from the water mass, especially in the visible range.The presence of photosynthetic pigments and coccolithes, inorganic and organic matter alters the optical properties of the sea water.Such alteration could be usually used to measure the concentration of the suspended matter.These images are presented in a combination of real color, for example biomass appears as patches in different shades of green and blue according to its concentration in the aquatic ecosystem.Therefore, the observation of the pigment detected by remote sensing has proved to be a useful tool in ecological research.Several satellites obtain information about oceanic environments.In our case, the satellite used was OrbView-2 provided by the SeaWIFS sensor which was used to show in a qualitative way the spatial and temporal variation of the patches of phytoplankton (chlorophyll and coccolithes) present in the Patagonian Sea to visualize the formation and disposition in the coast and their movement after the separation from it towards NNE to meet the Malvinas current.Previous studies did not consider the mechanisms that govern the distribution of phytoplankton at all, although they provide valuable data obtained by in situ samples through transects and by remote sensing.Those studies make clear the existence of three aquatic ecosystems (Roux et al. 1988;Lutz and Carreto 1991;Carreto et al. 1995): the Coastal system; the Shelf waters system and the Malvinas system.These systems, though connected, behave as independent compartments.
In the present paper, results of the observation of the patches belonging to phytoplankton biomass of 2,000 satellite images taken between 1997 and 2006, provided by SeaWIFS, are reported.This long-term temporal and spatial study allows a thorough analysis of the behavior of chlorophyll.Apart from the confirmation of the three ecosystems mentioned, the images demonstrate the appearance of special events like the high abundance of chlorophyll in the Strait of Magellan, the influence of strong winds in the sea and in the coastal continent, as well as the phenomena around, before and after the confluence of the Malvinas Current with the Brazil Current.Therefore, the aim of the present paper is to afford hypothesis in a qualitative way about the mechanisms that condition the proliferation, transport and distribution of phytoplankton as revealed by remote sensing information in the Patagonian Sea.

Materials and methods
The instruments used to measure the sea color are multispectral radiometers that register the electromagnetic radiation that emerges from the water mass, especially in the visible range of underwater light.
The presence of photosynthetic pigments and inorganic/ organic matter alters the optical properties of the sea water.Such alteration could be used to measure the concentration of this suspended matter.In the case of chlorophyll, the reflectance becomes higher in the green region (0.515-0.565 nm) while absorbing blue and red light.Then, the presence of chlorophyll imparts a green color to the water, which is more intense with the increase of concentration.The presence of coccolithes produces another change of color in the water, usually moving from deep to light blue.This fact finally constitutes a useful tool to obtain information about proliferation, transport and distribution of fish that may be important, for example, for fishing activities.
This study was performed with information provided daily and preferentially by the SeaWifs sensor of the satellite ORBVIEW 2, from 1997 to 2006.The Comisio ´n Nacional de Actividades Espaciales (CONAE) (National Commission for Spatial Activities) of Argentina received this information from November 18, 1997 to December 22, 2006, with approximately 1 year interruption during 1998 (available data only for January 1998).
The source of information used agrees with the catalog of CONAE, where the satellite images are presented in true color and thumbnail format.About 2,000 images from this catalog were examined and 870 preselected.In a second step, 111 images were selected and 21 were chosen to make the nine figures included in this paper.This instrument that is operated by ORBIMAGE company has the following characteristics: daily temporal resolution, instantaneous field of view (IFOV) 1,600 m and field of view (FOV) 2,800 km, radiometric resolution ten bits with eight channels to register, from which six of them belong to the visible range of the electromagnetic spectrum and 20 nm to the band width.
Given the huge amount of existing information recorded by the satellite OrbView with SeaWifs instrument, that had to be revised, it was decided to use the thumbnail image format from the CONAE catalog.These images are presented in a combination of real color, using red, blue and green bands so that chlorophyll appears in different green levels and coccolithes in blue in accordance with its concentration in the aquatic ecosystem.
These thumbnail format images are displayed with gamma value 1, exactly as recorded on the sensor.The images registered in the marine environment generally are low contrast, especially in the polar and sub Polar Regions.Some features and marine phenomena, as in this case, tend to have a low-key histogram-low dynamic range-generating a dark output image or without tonal contrast suitable for later analysis.
In these histograms, the sector that belongs to the ocean area is recorded in the center towards the left of the x axis; as a consequence, a dark gray image is obtained.Therefore, this requires an improvement of information, and for that purpose PhotoFiltre Studio X programme based on digital processing techniques was applied.All the images were enhanced by applying a linear stretch, especially the sector of marine waters.Thus, the minimal tonal variations observed in marine waters can be strongly enhanced, while the brightness of the continental areas are very washed or burned, because they are displayed to the minimum level of the remaining pixels.
In some special cases like the high cloud cover, the images of SeaWifs were replaced by images of satellite Aqua Modis, obtained also from the CONAE catalogs.These latest images are presented with an excellent size and better resolution (12 bits) than SeaWifs images.Unfortunately, on account of their orbital characteristics not always do they fully cover the Patagonian coast.
The main objective of this paper was to show in a qualitative way the spatial and temporal variation of the phytoplankton (biomass) patches present in the Patagonian Sea to visualize their formation and disposition in the coast, and their movement after the separation towards NNE to meet the Malvinas Current.The presence of clouds was not corrected to show the natural climatic and oceanographic conditions taking into account the strong relation between clouds, winds, waves and movement of the phytoplankton biomass at the moment of registration.

Results and discussion
Annual behavior of the distribution of Phytoplankton (chlorophyll coccolithes) The coastal system, shelf waters system and Malvinas system mentioned are the three ecosystems to be considered for the study of the annual distribution of chlorophyll in the Patagonian Sea, as follows: Coastal system Some of the rivers that discharge their freshwaters in the coastal area of Argentina carry urban wastes from the cities of Viedma, Rawson, Puerto Deseado, Rı ´o Gallegos and Rı ´o Grande.In the case of Comodoro Rivadavia, an important city of Patagonia, the wastes move directly to the San Jorge Gulf (Fig. 1, left b; Table 1).The mentioned rivers contribute to the diminution of the salinity, the supply of chlorophyll and nutrients that stimulate the algal growth in the frontal systems, and the presence of sediments.Another important source of sediments comes from the continent from the strong winds that blow from the west to the east as illustrated in Fig. 1, right b. Referring to chlorophyll, the images corresponding to 17 X 2006 (Fig. 2a) and 08 XII 2009 (Fig. 2b) are examples of the transportation of pigments to this system by the rivers located south of Tres Puntas Cape (Fig. 1, right b; Table 1, number 13).
In the Patagonian coast, chlorophyll appears between March and October in a progressive way in the frontal systems (Fig. 1, right b).The observation of the selected images, like the one obtained in 07 VI 2003 (Fig. 3a), demonstrates that the proliferation takes part even in winter indicating that nutrients, hydrological factors and also the temperature prevail over the limitation of light.
Image 29 III 2006 (Fig. 3b) makes it evident that the proliferation starts associated with the renewal of nutrients after the consumption during summer and with the beginning of the autumn vertical mixing.Table 2 shows this relatively constant behavior between 1997 and 2007.After September-October, chlorophyll patches separate from the coast and move to the NNE to meet the Malvinas Current.

Shelf waters system
After the proliferation of in the coast during autumn and winter already mentioned, a displacement occurs at the beginning of the spring.The images of 24 XII 2007 (Fig. 3c) and 01 XI 2007 (Fig. 3d) show that chlorophyll develops patches that modify its shape, lengthening in an NNE direction under the influence of the Patagonian Current (Fig. 1, left b).The displacement of chlorophyll behaves as a tracer to visualize the movement of this stream.Also the image of 30 XI 2001 (Fig. 4c) shows that in spring and summer, the patches of the coastal areas, after circulating several 100s of kilometers in an NNE direction, together with the chlorophyll originating in the shelf area itself, stick to the occidental border of Malvinas Current and continue their journey to reach the collision zone between Brazil and Malvinas currents.Notice that this chlorophyll does not mix fast with the one that comes from the Malvinas Current.
The information provided by SeaWIFS images does not assure that the chlorophyll present in the shelf area comes from Chilean Coast as some authors assert because this shelf area is very narrow and the Humboldt Current circulates from south to north in the Pacific Ocean (Fig. 1, right a) and besides, no patches of chlorophyll are seen in the south of the Chilean Coast (image not included).The images recorded provide no evidence of the supply of chlorophyll from the Pacific Ocean to the Atlantic Ocean.Thus, it could be stated that the present in the Continental Patagonian Shelf originates in the coastal and shelf areas of Argentina.

Malvinas system
This system is divided in the region all around the Malvinas Islands and in the shelf break, where the Malvinas current circulates following the outer edge of the continental shelf of Argentina, until it reaches the Brazil Current.

Malvinas Islands
After its origin in the Circumpolar Antarctic Current, the Malvinas Current moves around the Burdwood Bank (Fig. 1, right b; Table 1, number 20) and also to the Malvinas Islands.This circulation promotes the resuspension of nutrients with the consequence of high productivity in the region of the islands comparable to what is found in the frontal systems of the coastal areas (Campagna et al. 2005).From the observation of different images, it is important to note that this high productivity occurs between December and January with definite periods of time.That is to say, the number of days is nearly constant although the beginning and the ending vary from year to year (Table 3).This curious behavior may be associated with the increase of the photoperiod and with hydrological factors that trigger the upwelling of nutrients stimulating the algal growth, while the ending may be related to the limitation of nutrients by consumption and/or to the zooplankton grazing.This fact is reflected in the development of patches observed in the image of 02 XII 2001 (Fig. 4a).The image of 10 X 2001 (Fig. 4b), previous to the beginning of such periods, indicates the absence of patches.

Shelf break
The image of 30 XI 2001 (Fig. 4c) indicates the presence of a significant concentration of chlorophyll (biomass) along the shelf break that begins at the end of spring and lasts during the summer, while in image of 09 III 2009 (Fig. 4d), low volume of biomass is observed.Although these waters are rich in nutrients transported by the Malvinas Current (Fig. 1, left b, right b), they are too turbulent due to the strong and permanent winds of approximately 400 m/h (Piola and Rivas 1997) that makes difficult the carbon fixation which finally limits the phytoplankton production (Campagna et al. 2005).So, apart from the chlorophyll that could be generated on the stream, the high algal biomass observed has its origin in the Circumpolar Antarctic current (Fig. 9a) as suggested by the satellite image, together with the pigment coming from the region of the Malvinas Islands as previously mentioned.Then, the chlorophyll (biomass) present in the stream may have an autochthonous and mostly an allochthonous character.
About the Malvinas Current, there are some aspects that must be taken into consideration.To begin with, the Malvinas Current behaves as if it is a river inside the water masses.That makes it function as a mechanical barrier by which the phytoplankton coming from the shelf area does not enter inside the current as mentioned before.Apart from that, the mechanical barrier has two consequences,  the first is to prevent the phytoplankton coming from shelf area from moving to the east and the second is to improve the hydraulic retention time of the whole shelf area.This improvement has an influence in favoring the growth of algae in the shelf area.

Movement of patches
To appreciate the displacement of the phytoplankton biomass, Fig. 5 shows the movement of a patch along a period of time.During 2006, on August 1st it was placed at 40°30 0 S/ 56°30 0 W (Fig. 5a) and on January 18th it was at 38°30 0 S/ 52°00 0 W (Fig. 5b).Thus, the patch has displaced about 550 km in 10 days, which implies an approximate velocity of 2.3 km/h.

Strait of Magellan
The high concentration of chlorophyll (phytoplankton) encountered in the strait (Fig. 1, left b; Table 1, number 16) contributes a lot to benefit the coastal area, 09 X 2004 image (Fig. 6a), and may be connected to hydrological factors, long retention time, and the influence of nutrients related to the presence of birds and guano coming mainly from the west of the strait, but specially from the Chilean San Felipe Bay (52°45 0 S/69°57 0 W), where an abundant concentration of chlorophyll is generated which is later displaced to the oriental mouth of the strait and then moves to the Atlantic Ocean, 18-12-2003 (Fig. 6b). of around 50-100 km/h blow in some regions (Fig. 7, promoting a modification in the common annual pattern of the displacement of patches.This can be observed in 07-3-2003 (Fig. 7a) image, especially in the former, where the magnitude of this phenomenon was the greatest detected during the whole studied period.
• Over the coastal continent.
A sporadic phenomenon related to strong winds, such as dust storms, takes place in different areas of the Patagonian coast.This is shown in 21-12-2006 (Fig. 7b) images, with the wind blowing from the west at 95-105 km/h.Another example is 16-1-2005 (Fig. 7c) image, in spite of the absence of data, supposing the wind was blowing on an SW direction at about 60 km/h.This dust, that blows over the Patagonian Sea and creates feathers, contributes

Malvinas and Brazil confluence Currents
The confluence of the two currents place at about 37°-39°S/53°W-56°W, variable position.Figure 8 indicates that this confluence is really an impact after which the Malvinas Current turns to the SE.In this case, Phytoplankton (chlorophyll/coccolithes) behaves as a tracer to make clear that the impact is an elastic collision.
After that, the Malvinas Current preserves its identity in curious and eccentric forms, for example it does not mix with the Brazil Current.Examples of this are the images of    16-12-2004 (Fig. 8a), 23-12-2004 (Fig. 8b).Another fact that becomes evident is the lack of Phytoplankton (chlorophyll/coccolithes) in Brazil Current.
After the confluence and moving to the south, the origin of the Malvinas Return Current takes place (Falabella et al. 2009).The Phytoplankton (chlorophyll/coccolithes) concentration diminishes and begins to dissipate and disperse, covering extensive areas of the sea, due to the presence of many thread-like eddies that mix these waters.
Georgias del Sur Islands (36817 0 S/54831 0 W) In spite of the fact that these islands (g in the Fig. 1, right a) do not belong to the Patagonian Sea and in consequence they are out of consideration in the present report; it is interesting to point out an event that occurs during the months of November to January (austral summer).This event is characterized by an anomalous high concentration of phytoplankton chlorophyll, attending/in relation to the scarcity of nutrients of the region and the circulation of currents that prevent stability for the algal proliferation.The reason could not be elucidated with the available information.Probably, the chlorophyll has origin in the Malvinas Return Stream as mentioned before and arrives to the southern region.Then, it is influenced by the Circumpolar Antarctic current that finally disperses it to reach these islands as it is suggested by 09-12-2004 (Fig. 9a) image and also the incidence of eddies rotating between Malvinas Islands and Georgias del Sur Islands according to 26-12-2000 image (Fig. 9b).

Conclusions
From the information obtained and the superimposition of Tables 2 and 3, it can be stated that the Patagonian Sea, as a whole, shows algal blooms almost all year-round.This reveals the abundance of phytoplankton, estimated as three times the values registered in the rest of the oceans that conditions the abundance of the other members of the food chain, like plankton, fish, mammals and birds.The case of the fish is particular due to the commercial fishing of several international companies.Because of this circumstance, the government controls this fishing activity, although with relatively little success due to the extensive area to cover.Future research must involve the determination of in situ samples of phytoplankton to complete and to corroborate the results obtained by the remote sensing information presented here.

Fig. 2
Fig. 2 The rivers provide chlorophyll to the coastal area (indicated by orange arrows).a Coastal systems 08-XII-2009.The rivers located south of Cape Tres Puntas which provide chlorophyll to coastal waters are: Deseado, 11 de Septiembre (can ˜adon), Santa Cruz, Coyle, Gallegos and Chico, eastern mouth of the Strait of Magellan and Grande (Tierra del Fuego).No chlorophyll seen in the western mouth

Fig. 4
Fig.4Changes produced throughout the year.a Malvinas System.The higher productivity of chlorophyll/biomass observed around the Malvinas Islands occurs between the months of December and January.The number of days remains approximately constant every year.b In the previous image at the beginning of period with greater biomass productivity, no spots are observed.c High concentration of chlorophyll/biomass is observed close to the edge of outer shelf.d After the austral summer, a low concentration of chlorophyll/biomass is observed

Fig. 5
Fig. 5 Movement of patches in the shelf area (indicated by orange arrow).a The northern end of the chlorophyll/biomass spot is placed approximately at position 40°30 0 S/56°30 0 W. b The north end of the same spot is approximately at position 38°30 0 S/52°00 0 W.During 10 days, the spots moved approximately 550 km towards the NE

Fig. 6
Fig. 6 The special events.Chlorophyll in the Strait of Magellan (indicated by orange arrows).a The high concentration of chlorophyll/ biomass out of the mouth of the Strait of Magellan (Fig. 1, left b,Table 1, number 16) is traveling towards the NE.b Stainschlorophyll/biomass out of the Strait of Magellan and Cape Tres Puntas, clearly traveling to meet the Malvinas Current

Fig. 7
Fig. 7 Special events (indicated by orange arrows), influence of strong winds.a High winds NW quadrant generates a strong/violent modification in the movement pattern of chlorophyll/biomass spots in suspension.b Another phenomenon associated with strong winds crossing Patagonia is dust storms, as seen in the coastal area near the

Fig. 8
Fig. 8 Special events.Eccentric figure in the area of impact of Malvinas and Brazil currents (indicated by orange arrows).a Strange figure tapes biomass observed in the vicinity of position 56°W/40°S, after impact of Malvinas and Brazil currents.b Figure developed by chlorophyll becomes more complicated Fig. 1 Left a South America, Republic of Argentina.Shaded area shows the Patagonian Sea.b Gross arrow lines indicate the direction and movement of the Malvinas Current, dotted gross arrow lines the Brazil Current and the thin arrow lines the

Table 1
References indicated in Fig. 1, left b

Table 2
Seasonal productivity in the coastal area

Table 3
Seasonal productivity in the Islas Malvinas

Table 1
, number III), it is caused by winds SW quadrant.cAsmall plume of dust is observed in the vicinity of Cape Three Points, caused by strong winds SW quadrant (Fig.1b, left; Table 1, number 13)