Proliferaciones masivas de salpas en el mar interior de la isla de Chiloe (sur de Chile): posibles causas y consecuencias ecologicas.
The sudden increase of massive gelatinous zooplankton outbreaks in several coastal areas around the world has become more frequent, especially during the last few decades. The most documented case is the intrusion of the non-indigenous ctenophore species Mnemiopsis leidyi in the Black Sea during the 80's, which latter spread into the Caspian, Baltic, and North Seas (Shiganova et al., 2001; Faasse & Bayha, 2006; Javidpour et al., 2006), considerably affecting the food web structure and possibly helping to promote the collapse of fisheries in the Black Sea (Kideys, 1994, 2002). Major gelatinous outbreaks were also reported in 2011 and serious problems in nuclear plants in Israel, Japan and USA were reported where the seawater cooling systems became clogged with jellyfish (Purcell, 2012). In addition, the bursting of fishing nets caused by the giant Nemopilema nomurai in the coasts of Japan have forced fishermen to adapt fishing equipment in order to keep out jelly swarms (Uye, 2008).
The impacts of these gelatinous zooplankton outbreaks on tourism have also increased considerably and include the temporary closing of beaches, as well as cases of bathers being injured and even killed. It seems that human alterations to major ecosystems, which in turn have caused jelly outbreaks, are behind planktonic ecosystem shifts, and some anticipate that this will worsen in the future (Richardson et al., 2009). Meanwhile, a recent review (Condon et al., 2012) brings some caution to these findings based on the little knowledge of the historical ecosystem baseline for almost all jelly plankton species. The lack of historical background, the inaccuracy of the plankton nets used and sporadic sampling efforts is the main drawback to solve the paradigm of the abundance of these groups.
In most cases, harmful gelatinous outbreaks are referred to as carnivorous zooplankton, mainly cnidarians and occasionally ctenophores. Records of filter feeding zooplankton (salps, doliolids and pyrosomes) are less frequent and in most cases not even properly recorded. The latter group of zooplankton, due to its nature, is harmless to humans and therefore not of general concern. Salps have the ability to increase in number in short periods of time by the use of a complex life cycle with an obligatory alternation of sexual and asexual generations, allowing them to make rapid use of resources when environmental conditions are favorable (Goy et al., 1989; CIESM, 2001; Molinero et al., 2005). Salps are capable of filtering particles even in the 0.1 to 1 qm range, making them able to feed upon small bacteria, Prochlorococcus and colloids (Sutherland et al., 2010), thereafter inducing an exceptional food web shortcut between small particles and higher trophic levels, bypassing the microbial loop. The wide size range of potential food sources, high clearance rates (250-801 mL [mg.sup.-1] [h.sup.-1]) (Deibel, 1982a; Mullin, 1983), and reproductive cycle strategy allows them to achieve exceptional growth rates, ranging between 0.3% and 28% body length per hour (Deibel, 1982b; Le Borgne & Moll, 1986). Each solitary individual (oozooid) produces, by budding, a stolon which strobilates into chains, between 25 and 75 aggregated individuals (blastozooids), depending on the oozooid size (Heron & Benham, 1985), for Thalia democratica. These chains are fertilized shortly after they detach from the stolon to form a free living, pseudo-colonial group. The latter process allows salps to achieve high densities in short periods of time, while mortality is likely minimal as a result of viviparity (Heron, 1972), and causes the overgrazing of food resources during these short burst increases. This can come from rapid reproduction and growth during highly favorable environmental conditions where asexual propagation exceeds physical dilution.
In situ evidence and anecdotic information on the salp outbreak formation
During the 2010 austral summer, several warnings of salp outbreaks of the species Ihlea magalhanica were recorded, mainly by salmon farmers, in the ISCh, southern Chile. The first report occurred on 25 February, and lasted until 3 March 2010, when a massive outbreak was recorded close to Quemchi (Fig. 1a). This bloom was the onset of the first alert which was followed by several observations in diverse areas of the ISCh. During this outbreak, pictures were taken by local salmon farmers and dissections of dead salmon were performed in order to determine causes of ca. 25,000 salmon mortalities (Fig. 2a). Local salp abundances were not recorded, however farmer s estimate, indicate abundances of a couple of thousand per cubic meter. Massive concentrations clogged fish gills, probably the primary cause of fish deaths. Dissections of fish revealed the magnitude of this outbreak as depicted by gut content analyses that sho wed guts almost entirely filled with salps (Fig. 2b), which ultimately could cause fish starvation due to the low energy content of salps compared to food pellets. SeaWiFS true color images taken on 26 February unveiled a whitish structure, 5 km in length by ca. 1 km in width, crossing the Cacahue Channel, which was most likely a result of this unusual outbreak (Fig. 1b). One week later, a second event was registered on March 10, close to Chaiten, 90 km away from the first report (Fig. 1a). After this, several warnings were received during March across the ISCh: March 20 at Maillen Island (600 thousand oozooids and 54 thousand blastozooids per [m.sup.-3]), March 24 at Cholgo Channel and March 29 at Caleta Arena (Fig. 2c). No more warnings of salp outbreaks were recorded until September in the north of Chiloe Island (Huelden Bay) and Ancud Sound (September to October 2010).
Ihlea magalhanica is a subantarctic species with an oceanic distribution centered between the subtropical convergence and the Antarctic convergence (Esnal & Daponte, 1999). It is usually described as a stenothermal cold water species (Ihle, 1958; Foxton, 1971), adapted to a temperature range between 4-16.8[degrees]C (Foxton, 1971; Daponte et al., 1993) while highest abundances are usually recoded in association to cold water masses (5-7[degrees]C, Daponte et al., 1993). Few organisms were collected at the Magellan region (Michaelsen, 1907), south of 43.5[degrees]S (F. Cabello, pers. comm.) and off Valparaiso (Chile) (~33[degrees]S, Fagetti, 1959), the later being the most northerly location ever recorded.
Ihlea magalhanica, as most salp species, is usually found in large numbers in open ocean waters and exceptionally in neritic regions. Thus, the presence of this species in coastal waters is usually linked to the horizontal advection of oceanic water masses into coastal areas. The area of the east Pacific where salp outbreaks were observed during 2010 coincides with the region in which the South Pacific Current (SPC) reaches the eastern margin of the Pacific Ocean. Here, the SPC splits into two branches; to the north, the Humboldt Current or Chile-Peru Current and to the south the Cape Horn Current. Forced by the SPC, Subantarctic Water (SAAW) mass penetrates the inlets of the ISCh through the Guafo Passage, where it mixes with the Estuarine Water (EW), forming the Subantarctic modal water (Silva et al., 1998; Sievers & Silva, 2006). We hypothesize that temporal anomalies in the currents (i.e., displacement of the SPC, intrusion of anomalous cold water masses into the ISCh), may favor the entrance and establishment of salp populations, while local food availability conditions could have allowed the massive increase in population abundance which were observed during 2010.
The aim of this study was to explore the scenarios which have lead to the intrusion of I. magalhanica into the ISCh, as well as the environmental conditions which allowed the persistency and development of a several massive outbreaks in this region during 2010.
MATERIALS AND METHODS
Sea surface temperature and surface current along the outer coast off Chiloe Island and the Patagonian fjord region
Field data with a spatial resolution of 1/12[degrees] x 1/12[degrees] were obtained from the model outputs of Hybrid coordinate Ocean Model [HYCOM; Chassignet et al. (2009)] with a Navy Coupled Ocean Data Assimilation (NCOdA) System (Cummings, 2005) for data assimilation. The hybrid coordinate in HYCOM is isopycnal in the open, stratified ocean, but smoothly reverts to a terrainfollowing coordinate in shallow coastal regions, NCODA uses the model forecast as a first guess in a multivariate Optimal Interpolation scheme and assimilates available satellite altimeter observations satellite and in situ SST as well as available in situ vertical temperature and salinity profiles from XBTs, ARGO floats and moored buoys. Monthly means and their anomalies from January to March were calculated from daily sea surface temperature and the ocean surface velocity field (42[degrees]-46[degrees]S, 74[degrees]-76[degrees]W) from 2004 to 2011.
Chlorophyll-A and sea surface temperature in the ISCh
In order to explore the general scenario in which I. magalhanica outbreaks were established and developed, we analyzed monthly means of historical satellitederived chlorophyll-a (Chl-a) and sea surface temperatures (4 x 4 km pixels, 11 [micro]m night product) and compared them with the monthly mean values for the year 2010. SST and Chl-a values were estimated from the Moderate Resolution Imaging Spectro-radiometer Aqua sensor (MODIS Aqua) from July 2002 to July 2010. Data were averaged over an area which included all the locations where salps were seen (ca. 4000 [km.sup.2]) (Fig. 1a). Analysis used in this study was produced with the Giovanni online data system, developed and maintained by the NASA GeS DISC (Acker & Leptoukh, 2007).
Sampling and analysis
On 5 September, during the first outbreak recorded in Huelden Bay (northern Chiloe Island), vertical zooplankton samples (20-0 m) were collected on the third (and last) day of the outbreak with a WP-2 net (200 [micro]m mesh size) equipped with a calibrated flowmeter. Zooplankton samples were collected along a transect consisting of five stations, 500 m apart, starting from close to the coast (ca. 100 m) into the ISCh. After collection, the samples were fixed in 5% buffered formaldehyde in sea water and stored for further analysis. Abundance and identification of salp species and life history phases were determined under a stereo microscope at 20x, by observing the entire sample. Salps were identified using the taxonomic literature (Fagetti, 1959; Foxton, 1971; Esnal & Daponte, 1999).
In order to explore the in situ potential effect of salps on the autotrophic community, water samples for determining phytoplankton and chlorophyll-a were collected using 5-L PVC Go-Flo bottles at three depths (0, 5 and 10 m). Subsamples (300 mL) were filtered through 0.7 [micro]m GFF filters, immediately frozen (-20[degrees]C) for later pigment extraction and fluorometric analysis (Turner Design TD-700), according to Parsons et al. (1984). To quantify phytoplankton abundance, 250 mL subsamples were fixed in acid Lugol's solution (1% final concentration) for phytoplankton cell counts. A 50 mL aliquot was taken from each subsample and placed in a settling chamber for 30 h prior to analysis under an inverted microscope (Zeiss Axiovert 200, 400x magnification) and counted using standard counting methods (Utermohl, 1958).
During the second salp outbreak at Huelden Bay which occurred between 25 and 28 September, salmon farm workers collected water samples using a 15 L bucket at irregular intervals (0.5 to 10.5 h) at a fixed point within a salmon cage. The sampling point was located on the edge of the salmon cage facing the inner sea. Salps were sieved and directly counted (no distinction between oozooids and blastozooids were made). Salp samples were fixed and sent to the laboratory for later taxonomic identification.
Time series of salp abundance at the Reloncavi Sound
Zooplankton samples were collected monthly by oblique tows using a Tucker trawl net (0.5 [m.sup.-2] mouth area, 300 [micro]m mesh size) equipped with a digital flowmeter for water volume quantification, during daytime from July to November 2010 at a fixed station (41[degrees]32.6'S, 72[degrees]52'W). Samples were collected at 9 depth intervals, from 5 to 100 m (0-5-10, 10-15, 15-20, 20-30, 30-40, 40-50, 50-75 and 75-100 m) and preserved in borax buffered formalin (10%) for later analysis. Salps were identified up to species level and measured from the oral to the cloacal opening (excluding posterior projections). Along with the zooplankton samples, vertical CTD casts (Seabird 19 plus) were obtained during each sampling date from the surface down to 91 m.
Time series of phytoplankton functional group abundances prior to and after salp outbreaks
Phytoplankton abundance from January 2009 to December 2011 was obtained for the three major basins along the ISCh: Reloncavi Sound, Ancud Sound, and Corcovado Gulf, and the region of the Desertores Islands. The amount of stations per basin varied from between 2 (Reloncavi Sound) up to 52 (Desertores Islands), while each basin was sampled between 1 and 24 times per month. Integrated samples (0-20 m) were collected using a 2.5 cm diameter hose raised vertically and preserved in an acid Lugol's solution. From these samples, a 12 mL subsample was analyzed for diatom and flagellate counting using standard methods (Utermohl, 1958).
Large scale offshore temperature and sea surface current climatology during austral summer
HYCOM model output derived SST climatology revealed the presence of cold SAAW water surrounding the outer coast from southern Chile during January (Fig. 3 a), this cold water approached the coast from the south-west around 45[degrees]30'S (Fig. 3d). Close to the coast, the northward current deflected into two branches south of the Guafo Island (~44[degrees]S), one continued equatorward around Guafo Island, while the second entered the ISCh through the Guafo Passage at a speed of 0.06 m [s.sup.-1] (Fig. 3d). Equatorward currents flowed relatively slow close to the coast (0.05 m [s.sup.-1]) and tended to increase along a narrow band between 75[degrees]20'-75[degrees]40'W which expanded north of the Guafo Island where it reached the coast of Chiloe Island up to 75[degrees]4'W.
During February, the currents ran in a predominately meridional direction to the north with an increase in velocity over a wider zonal range, while eastward currents along the western margin were less intense and only apparent south of 45[degrees]S (Fig. 3e). There was also an increase in SST of ca. 1[degrees]C associated with modifications in meridional currents over the entire study area (Fig. 3b). The northern warm core tended to show a displacement to the south-east and low SST was only seen in a restricted area close to the outer coast of the Patagonian fjord region and the Guafo Passage.
During March, SST conditions were more similar to those in January (Figs. 3a, 3c), with a cold SST in the outer fjord region, coupled with a change in the meridional currents to a more oblique zonal current plane (eastward) during March (Fig. 3f). The oceanic meridional currents were weaker and more homogeneous (0.05-0.15 m [s.sup.-1]) with a slight increase in speed close to the continent (Fig. 3f). As in January, a branch of cold water was projected to the ISCh, through the Guafo Passage.
Large scale offshore SST anomalies and currents prior to and during outbreaks in austral summer 2010
During January 2010 the oceanic region off Chiloe Island and the fjord region experienced a cooling in relation to its climatology (Figs. 4a, 5a). South of the Guafo Passage a decrease of ca. 0.5[degrees]C was observed, while positive anomalies were mainly located in the northern region close to the coastal environment. Sea surface currents during this month displayed a wider predominance of shoreward zonal currents (Fig. 4d), which deflected to the north as they approached the continent. Meridional currents along outer Patagonia displayed a similar spatial trend, while slowing down in relation to its climatology. During February, the entire area exhibited a decrease in SST (Fig. 4b) and sea surface currents (Fig. 4e). Offshore negative SST anomalies reached as low as -1.5[degrees]C, covering almost the entire south western area. The rest of the area experienced an SST drop of 0.5 and 1[degrees]C. Concomitant to the decrease in SST a significant decrease in offshore current was observed. Meridional surface currents decreased to less than 0.05 m [s.sup.-1] in the oceanic region, while currents close to the coast and interior of the Guafo Passage did not change significantly with respect to the climatology (Figs. 4b, 4e). Zonal currents were weak, always heading north, similar to climatologically conditions. During March, conditions tended to stabilize; SST showed a slight decrease of 0.5[degrees]C over the entire area, while currents remained close to that which can be expected for this month (Figs. 4c, 4f).
General scenario in the ISCh (Ancud Sound) prior to and during salp outbreaks in summer 2010
On an annual time scale, temperatures displayed a typical seasonality with maximum values during austral summer (14-13[degrees]C, January to March) and a continuous decline from autumn to winter, with minimum SST during July and August (9.8[degrees]C) (Fig. 5a). Subsequently, temperatures started to rise during spring through to summer. Surface Chl-a however presented a more variable cycle during the year and is partially decoupled with temperature (Fig. 5b). High concentrations of Chla were typically observed in austral autumn rather than in summer. During January and February (austral summer), Chl-a concentrations fluctuated around 10 mg Chl-a [m.sup.-3], March and April being the months with the highest satellite Chl-a concentrations (~13.5 mg Chl-a [m.sup.-3]). Usually after May there is a substantial drop of one order in magnitude in Chl-a (10.5 to 0.9 mg Chla [m.sup.-3]) when it reaches its lowest value along the annual cycle (Fig. 5b).
During 2010, SST in the Ancud Sound experienced the similar annual drop as that seen offshore, although in a more restricted range. During January, SST and satellite derived Chl-a were close to their historical mean (14.1[degrees]C and 10 mg [m.sup.-3], respectively). However, during February the basin experienced a significant cooling of 1[degrees]C in relation to its historical mean and 0.7[degrees]C below standard error (Fig. 5a). This drop was not followed by any significant change in Chl-a concentration, which increased slightly during this month. After this event, temperatures rose again to "normal" conditions while chlorophyll experienced a substantial drop from normal values of 13.5 to 4 mg Chl-a [m.sup.-3] (Fig. 5b). After this drop, Chl-a did not recover and remained low throughout the entire year. Unfortunately during June, satellite images could not be obtained due to cloud cover (Fig. 5b).
Time series of phytoplankton functional groups in the four major regions in the ISCh
Throughout the annual cycle, the three basins and Desertores Islands were dominated by chain forming diatoms such as Chaetoceros spp., Skeletonema spp. and Thalassiosira spp. In the austral spring and summer (September to May), these species tend to form blooms, especially in the three largest regions (Ancud Sound, Desertores Islands and Corcovado Gulf) while the Reloncavi Sound has a less marked seasonality with sporadic autumn and winter blooms (Fig. 6). Phytoplankton cell concentrations show a north to south gradient with higher concentrations in the Reloncavi and Ancud sounds, declining in the Desertores Islands. This region functions as a barrier between the highly productive northern Ancud Sound and the southern Corcovado Gulf, where the lowest phytoplankton abundances were measured.
A marked reduction in phytoplankton spring bloom in 2010 was evident in the Ancud Sound, Desertores Islands and Corcovado Gulf, in which phytoplankton abundance decreased down to half of what was later recorded in 2011, with no evident change in species composition between years. From May through September 2010, there was a marked reduction in abundance of large phytoplankton cells at Reloncavi Sound, during which small cell numbers of the genus Chaetoceros and other less representative algae's dominated. During 2009 the Ancud Sound experienced an unusual extension for ca. two months of this less productive phase due to the early decline of the summer bloom and coincided with a drop in cell abundance which lasted until the end of 2010. The Ancud Sound experienced a massive bloom of small flagellates Tetraselmis spp., during the end of spring 2009 and beginning of summer 2010, just after the last recorded outbreak of I. magalhanica in 2010.
Ihlea magalhanica sampling and analysis Huelden (Ancud Sound)
Zooplankton samples taken during the first outbreaks in Huelden (5 September 2010), were low in salp abundance compared to the outbreaks reported during the austral summer by local salmon farmers at the same location almost three weeks later. The total abundance of aggregate and solitary forms reached up to 1.13 ind [m.sup.-3] (Fig. 7a) and were dominated by aggregate individuals (93% of the total population) as expected. The size of the aggregate phase was of 7.7 [+ or -] 5.3 mm in length (mean [+ or -]; n = 79) while small buds (~1 mm length) which were not considered for the abundance counts, represented 31% of total measured individuals. Solitary forms were only collected at stations 1 and 2, with a mean size of 22 [+ or -] 4 mm (mean [+ or -] SD; n = 6). The total abundance was higher at the two stations located close to the coast with 0.9-1.13 ind [m.sup.-3]. These stations experienced a sharp decline of Chl-a (Fig. 7a) associated with the decline of flagellates, which were the dominant microplankton group in all stations with over 58% of the total abundance (mean 64%) (Fig. 7b). The main contributors (over 98.7%) to flagellate abundance were small sized (<20 [micro]m) loricated flagellates, followed by small (<20 [micro]m) naked dinoflagellates (0.5%), Gonyaulax spp. (0.4%), Diplopsalis spp. (0.3%) and others (0.1%). Diatoms, coccolitophores and ciliates did not show any apparent change in their relative abundances that could be associated with changes in salp abundance (Fig. 7b).
Twenty days after this event and in this same location, a massive outbreak of I. magalhanica took place (Fig. 7b). Abundance on this occasion was around 10,000 ind [m.sup.-3] in the first 3 h after the first measure ments were taken. Afterwards, their abundance increased steadily over the next 21 h, reaching a maximum of 33,330 and 32,000 ind [m.sup.-3] at 21:30 and 24:00 on 25 September 2010, respectively. This drastic increase is most likely a result of aggregation rather than reproduction taking into account the rapid increase in just a couple of hours. Consecutive changes in abundance were of great magnitude, increasing/ decreasing approximately 4-fold in a range of just 3 h. These temporal oscillations in abundance were coupled with the tidal phase. The highest abundances usually recorded in periods of tidal rise, while decreases were observed during the ebbing tide (Fig. 7c). The zooplankton samples were taken from a salmon cage facing towards the inner sea, and therefore, observed increases are mainly a result of the aggregation and clo gging of salps in salmon farm nets during the rising tide. While during the ebbing tide, salps were transported towards to the inner sea, reducing abundance significantly close to the farm. This outbreak lasted for almost three days after the first observations, reducing gradually on the afternoon of the third day. By the fourth day no noticeable abundances were recorded by the salmon farmers, therefore sampling was terminated. Potential relationships between the abundance of organisms and the diel cycle were not observed which lead us to discard changes in abundance due to vertical migrations.
The I. magalhanica abundances recorded between July and November 2010 show a clear outbreak event in the Reloncavi Sound. While from July to August no individuals were collected. During September the first appearance of salps were observed with a large predominance of adult and young solitary forms, which are both close to the abundance of aggregate individuals (aggregate/solitary mean ratio of 2.1) (Fig. 8a). Salps showed low abundance at surface (<0.23 ind [m.sup.-3] in the 0-10 m depth stratum), and increased sharply up to 18.5 ind [m.sup.-3] below a depth of 10 m where salps were distributed almost evenly down to a depth of 50 m (Fig. 8a). Their abundance declined again sharply to less than 0.4 ind [m.sup.-3] below 50 m. One and a half months later (mid November), a new massive outbreak took place (up to 628 ind [m.sup.-3], Fig. 8b), in which a change to their relative reproductive life cycle phase contribution occurred as depicted by the decrease in the relative abundance of solitary forms to levels similar to those previously recorded in Huelden, and the aggregate phase dominated overall (aggregate/solitary mean ratio of 18.8).
Vertical distribution was uneven with low abundance on the surface and a steady increase from 200 ind [m.sup.-3] at the 5-10 m stratum up to 422 ind [m.sup.-3] at the 15-20 m depth stratum (Fig. 8b). Under this depth range, there was a region (20-40 m depth) that showed a decline in abundance and then an abrupt increase in the 40-50 m stratum, coinciding with the higher abundance recorded at this station (628 ind [m.sup.-3]). Finally, below this stratum abundances decreased down to 0.2 ind [m.sup.-3] from 50 to 100 m depth; following the same pattern observed in September. In parallel with the observed changes in salp abundance, the hydrographic characteristics at the Reloncavi Sound also changed significantly from September to October 2010 (Figs. 8c, 8d). During September, a vertical quasi-homogeneous thermal distribution (10.4[degrees]C) was found (Fig. 8c) with a weak saline gradient, forming a fragile halocline at a depth of 25 m (Fig. 8c). In October, a strong vertical thermal and haline gradient was formed with low salinity (30.6) and a high temperature (12.7[degrees]C) at surface, decreasing sharply at 20 m where the base of the mixed layer is formed (Figs. 8c, 8d).
The Patagonian fjord offshore region is influenced by the eastward flow of the SPC, which reaches the coast of South America at ~45[degrees]S were it deflects, forming the Cape Horn Current to the south, and the Humboldt Current to the north. Part of the SAAW near the coast enters at subsurface depths (see below) to the ISCh through a narrow 2 km, 150 m deep channel (Chacao Channel, 42[degrees]S) to the north of Chiloe Island, and the Guafo Passage (43.5[degrees]S), a 37 km wide channel with an entrance at sill ca. 150 m depth (Silva et al., 1995). SAAW which enters through the Guafo Passage has a low salinity signature (~33, Palma & Silva, 2004), derived from the northward costal transport of fresh water discharges along the fractured coast line from 47 to 43[degrees]S (Davila et al., 2002). This low salinity water mass, results from the mix of SAAW and Estuarine Water (EW), which forms the Modified Subantarctic Water (MSAAW). The general circulation pattern through the Guafo Passage is an offshore outflow of MSAAW at the surface (upper 25 m) and an inflow of SAAW at depth (25-110 m) (Palma & Silva, 2004). Thus the entrance of subantarctic species into the ISCh under normal conditions should occur at the subsurface. However, during some episodic events such as those observed during January 2010, a change in the circulation pattern associated with the intensification of zonal currents can cause a massive entrance of SAAW into the ISCh, as revealed by a temperature drop in the Guafo Passage and around the ISCh from January to February 2010 (Fig. 4e). This intrusion was most probably responsible for the transport of oceanic subantarctic species, such as I. magalhanica into this coastal semi enclosed habitat.
The ISCh is geographically divided into three clearly defined sub-basins (Tello & Rodriguez-Benito, 2009): (1) the northern one being the Reloncavi Sound, a semi enclosed system influenced by a strong silicicacid-rich freshwater input and strong stratification in the upper 4-7 m. Beneath this layer, a strong nutricline develops isolating the lower SAAW, nutrient-rich (nitrate and orthophosphate) water (Silva et al., 1998; Gonzalez et al., 2010). The particular geographical structure of the ISCh, i.e., being split into three subbasins, allows for the development of high numbers of large chain-forming diatom blooms which (see Fig. 6), are not only limited to the austral spring and summer seasons but are also frequent in winter and autumn. (2) The central sub-region (Ancud Sound) is a larger basin with less intense haline stratification and a seasonal production coupled with the light regime, supporting a rich phytoplankton biomass, largely dominated by large chain-forming diatoms (Fig. 6, Gonzalez et al., 2010). (3) The southernmost basin (Corcovado Gulf) is separated from the middle basin (Ancud Sound) through a string of islands (Desertores Islands). The Corcovado Gulf connects with the Pacific Ocean through the Guafo Passage, where the SAAW mixes with fresh waters coming from rivers, generating a lower salinity water mass (31 to 33, Silva et al., 1998). The entire area between Desertores Islands and up to the Corcovado Channel is less productive than the enclosed northern and central basins, while a clear seasonality is still observed (Fig. 6, Lara et al., 2010).
Proliferation of salps were only recorded in the Reloncavi and Ancud sounds, north of Desertores Islands, while no records were registered in the Corcovado Gulf, despite several salmon farms existing in this region that might have documented the event (ca. 170 fish farms, Fig. 9). Why the salp outbreaks developed exclusively in the northern innermost basins is not yet clear. One possible hypothesis is that the Desertores Islands may function as a natural barrier, creating a retention area for planktonic organisms, by limiting the circulation and dispersal of organisms across the central and southern basins while providing a suitable area for aggregation and development, as sugested by Tello & Rodriguez-Benito (2009). Salp outbreaks, such as those observed in this study, occur explosively, facilitated by their direct development and release of progeny at relatively large sizes, high growth rates and short generation times as the reported for other salp species such as Thalia democratica (Madin & Purcell, 1992; CIESM, 2001). A drastic increase in abundance was observed in September 2010 at the station located at the Ancud Sound, where tens of solitary forms were collected initially, while at the end of October, six weeks later, abundances reached up to 600 ind [m.sup.-3], mainly dominated by aggregates, indicating that this species is most likely capable to complete its life cycle in the ISCh. The absence of salps, during the months before or after the outbreaks, are not necessarily a result of a lack of reproduction over the entire area but most likely related to the patchy distribution of this event. The fast increase and in most cases short persistency of the outbreaks in a particular area makes it extremely difficult to follow and almost impossible to predict. Thus, most of the warnings we received could not be properly investigated and upon our arrival (one to two days after warnings) the salps had already gone.
Reports of salps in Patagonia are scarce and usually include numbers less than 0.052 ind. [m.sup.-3] (Fig. 10). These have only been recorded during winter time and have been absent during spring and summer. Thus, the outbreaks during 2010 are the highest recorded for this group of species to date and occurred in summer and spring. The first large-scale outbreaks were recorded in late February 2010, a situation in which the ISCh offshore and inshore temperature showed strong negative anomalies (-1.5[degrees]C) and a month later accompanied by Chl-a concentrations well below the historical averages expected for this region (Fig. 5b).
The reason why outbreaks did not developed in the past is unknown, despite of the presence of salps in this region in previous years and that intensive aquaculture established since the 1990's. Prior recorded abundances of salps in the ISCh were usually low, probably limiting a successful reproduction, which leads to assume that the intrusion of SAAW might have transported an already developed outbreak into the ISCh.
The potential effect on the phytoplankton community in the ISCh might be considerable when taking into account that they filter continuously throughout the day and also that each salp may display very high filtering rates as in the case of Pegea confoederata that can exert grazing pressure equivalent to that of several hundreds of large calanoid copepods (Harbison & Gilmer, 1976) considering that the filtration rate is not known for I. magalhanica. This is especially relevant given the high concentrations recorded of up to 654,000 salps [m.sup.-3] close to coastal net pens and 600 ind [m.sup.-3] in the more open systems in the Reloncavi Sound.
Accordingly, the effect of the salp outbreaks on the ISCh pelagic food web might be considerable taking into account the drastic decrease in phytoplankton cell abundance and Chl-a biomass. If this decrease was mainly result of grazing we also might expect a substantial export of organic carbon out of the photic zone via fecal pellets. Salps are able to filter on a wide size range of particles above 0.1 [micro]m, which results in an aggregation of small particles into large and fast sinking fecal pellets. Sinking rates of salp fecal pellets range from between 59 up to 2238 m [d.sup.-1] (Bruland & Silver, 1981; Madin, 1982), which implies an extremely efficient export of organic matter and nutrients from the upper water column down to the benthos.
Massive sinking events of fecal pellets and senescent bodies during salp outbreaks have been previously reported in other regions (Bathmann, 1988). On that occasion, salps with an abundance more than 700 ind [m.sup.-3] were able to deplete surface nutrients by exporting organic matter and nutrients out of the photic zone off the coast of Ireland. This process could explain why phytoplankton was not able to recover its biomass over several months after the first outbreaks in the ISCh. The only phytoplankton species which showed an unusual increase were small flagellates, which are capable of migrating through the water column to the nutricline and have lower nutrient requirements than diatoms because of their larger surface to volume ratio. On the other hand, the decrease in cell abundances of large, chain-forming diatoms (especially those equipped with long setae and protuberances) throughout 2010 would also favor the development of I. magalhanica growth, since large phytoplankton have shown to be deleterious to filtering activity, causing clogging of feeding structures (Harbison et al., 1986).
Gelatinous species with short generation times such as ctenophores (Sullivan et al., 2001) siphonophores (Pages et al., 2001) and pelagic tunicates (Purcell & Madin, 1991), have the ability to make use of aggregation for reproductive purposes to maintain and/or increase their population density. In this study, field observations indicated that salmon net pens can effectively act as a physical barrier to salp movement, promoting the clogging, increasing local salp aggregations. Thanks to short generation times, these massive aggregations along salmon net pens have the potential to increase reproductive encounter rates, which can result in a highly effective instrument to maximize reproductive success and promote outbreak formation (Heron & Benham, 1985).
Aggregations have generally been described by the presence of geological barriers (i.e., shoreline and seafloor) and hydrographic (i.e., horizontal fronts and vertical discontinuities) (reviewed by Graham et al., 2001) or mesoscale eddies (Everett et al., 2011). However, the effect of man-made barriers is less well documented (Purcell et al., 2007; Doyle et al., 2008; Baxter et al., 2011; Mianzan et al., 2014). The ISCh possess the majority of the country's salmon farms with over 500 fish farms along the ISCh coast (excluding fjords) (Fig. 10), thus the potential use of these structures as aggregation barriers to achieve a high reproductive success is enormous.
Effect on aquaculture
Warnings of high densities of salps close to salmon farms occurred seven times in 2010, while adverse effects were only recorded on one occasion. High salp density inside fish cages hamper normal fish feeding on food pellets, as observed in the guts of dead salmon collected from cages. The stomachs of these fish were entirely filled with salps, while gills were clogged by salp remains. Several salmon biopsies could not reveal the exact cause of death; however, veterinarians suggested that gill damage and the reduction of the oxygen diffusion due to clogging might be the primary cause of death.
Overall, Chl-a levels and cell density remained low throughout the entire year, which not only favored the persistence of salps (until the end of October) but also showed serious negative consequences for blue mussel farmers, who experienced decreased growth of adults and little settlement of juveniles in the following season (http://www.mundoacuicola.cl/comun/?modulo-=3& view=1&cat=1&idnews=341). Deleterious effect of gelatinous zooplankton on aquaculture has becoming increased attention in the last decades; which on one hand has being linked to climate-driven variability (Condon et al., 2012) and to the proliferation of settlements and increased human activities in coastal areas (Purcell, 2012). The inner sea of Chiloe is not an exception, where proliferations of the scyphomedusa Chrysaora plocamia and Phacellophora catschatica have affected salmon farming installations (Palma et al., 2007; Bravo et al., 2011). Unfortunately, and as same as most cases, reports as same as impacts are mainly based on anecdotic information given by local farmers (see Mianzan et al., 2014), and more reliable information based on scientific orientated approaches are extremely scarce. The random nature of the occurrence (spatial and temporal) basically associated to a complex life cycle and "r" strategy (Boero et al., 2008), makes gelatinous zooplankton outbreaks very hard to follow.
There is no clear evidence of which kind of remote forcing might have been involved during the intrusion of oceanic water into the ISCh, and whether it might increase/decrease in frequency in the future. There is however some hints from remote atmospheric anomalies that occurred during the end of 2009 and the beginning of 2010 which might have been partially responsible for the build-up of this scenario which favors the intrusion of SAAW into the northern ISCh.
In the last few decades it has become evident that climate variability in the southern hemisphere is mainly forced by the variability on timescales from intraseasonal to interannual by the Southern Annular Mode (SAM), which is characterized by a large scale alteration of atmospheric mass between mid and highlatitudes; modifying the latitudinal distribution of the westerly winds. Positive SAM is associated with a significant increase in SST in the Subtropical Zone (STZ) (Lovenduski & Gruber, 2005), while inverse patterns occur during negative anomalies (Hall & Visbeck, 2002).
Positive anomalies usually persist throughout all seasons, but are strongest during the austral summer (Marshall, 2003). During the austral summer 2010, an unusual negative SAM was documented (Fig. 11) coinciding with strong negative SST anomalies at the outer Patagonian region. If this anomaly triggered the entrance of I. magalhanica to the ISCh, two processes must have occurred simultaneously to achieve these outbreaks. First we would need a substantial transport of SAAW towards to the coast, which ultimately must carry enough organisms to facilitate a successful reproduction to generate an abundant offspring. The achievement of these two conditions makes these scenario relatively improbable phenomena to occur on a regular basis. The exact mechanism controlling the coupling between climate forcing and zooplankton outbreaks needs further study and many questions remain unanswered. Examining the role of the meridional circulation across the Southern Pacific and the advection of oceanic water masses into the ISCh and its relation to remote forcing such as the SAM variability might help to unveil some of these answers. Additional modeling work, both regionally and globally, can help to demonstrate biological and physical coupling and allow potential predictions on changes in productivity and help to anticipate potential invasions.
Received: 15 October 2013; Accepted: 20 June 2014
This research was supported by the COPAS-Sur Austral project and a FONDECYT 1100534 grant to Leonardo Castro. We are grateful to Rodrigo Cristi and Dr. Dirk Schories for providing information and photographs of outbreaks. We also thank Marine Harvest for providing technical assistance during sampling campaigns and L. Cisternas and M.J. Cuevas for sap sorting from zooplankton samples. To Dr. Hector Paves and Program CIMAR-Fiordos 9, 12 and 13 (CONA-SHOA) to provide data on abundance of salps collected on several oceanographic expeditions along the fjord region of the southern Chilean Patagonia.
Acker, J.G. & G. Leptoukh. 2007. Online analysis enhances use of NASA Earth science data. EOS. Trans. Am. Geophys. Union, 88(2): 14-17.
Bathmann, U.V. 1988. Mass occurrence of Salpa fusiformis in the spring of 1984 off Ireland: implications for sedimentation processes. Mar. Biol., 97(1): 127-135.
Baxter, E.J., M.M. Sturt, N.M. Ruane, T.K. Doyle, R. McAllen, L. Harman & H.D. Rodger. 2011. Gill damage to Atlantic salmon (Salmo salar) caused by the common jellyfish (Aurelia aurita) under experimental challenge. PloS ONE, 6: 1-6.
Boero, F., J. Bouillon, C. Gravili, M.P. Miglietta, T. Parsons & S. Piraino. 2008. Gelatinous plankton: irregularities rule the world (sometimes). Mar. Ecol. Prog. Ser., 356: 299-310.
Bravo, V., S. Palma & N. Silva. 2011. Seasonal and vertical distributional patterns of medusae in Aysen region, southern Chile. Lat. Am. J. Aquat. Res., 39(2): 359-377.
Bruland, K.W. & M.W. Silver. 1981. Sinking rates of fecal pellets from gelatinous zooplankton (Salps, Pteropods, Doliolids). Mar. Biol., 63(3): 295-300.
Chassignet, E.P., H.E. Hurlburt, E.J. Metzger, O.M. Smedstad, J.A. Cummings, G.R. Halliwell, R. Bleck, R. Baraille, A.J. Wallcraft, C. Lozano, H.L. Tolman, A.Srinivasan, S. Hankin, P. Cornillon, R. Weisberg, A. Barth, R. He, F. Werner & J. Wilkin. 2009. US GODAE Global Ocean Prediction with the HYbrid Coordinate Ocean Model (HYCOM). Oceanography, 22(2): 64-75.
Condon, R.H., W.M. Graham, C.M. Duarte, K.A. Pitt, C.H. Lucas, S.H.D. Haddock, K.R. Sutherland, K.L. Robinson, M.N. Dawson, M.B. Decker, C.E. Mills, J.E. Purcell, A. Malej, H. Mianzan, S.I. Uye, S. Gelcich & L.P. Madin. 2012. Questioning the rise of gelatinous zooplankton in the World's Oceans. BioScience, 62(2): 160-169.
Cummings, J.A. 2005. Operational multivariate ocean data assimilation. Q.J.R. Meteorol Soc., 131(613): 3583-3604.
Daponte, M.C., F.L. Capitanio, L. Machinandiarena & G.B. Esnal. 1993. Planktonic tunicates (Chordata, Tunicata) of the RTMA "Evrika" in the southwestern Atlantic Ocean. Iheringia, 74: 71-80.
Davila, P.M., D. Figueroa & E. Muller. 2002. Freshwater input into the coastal ocean and its relation with the salinity distribution off austral Chile (35-55[degrees]S). Cont. Shelf Res., 22: 521-534.
Deibel, D. 1982a. Laboratory-measured grazing and ingestion rates of the salp, Thalia democratica Forskal, and the doliolid, Dolioletta gegenbauri Uljanin (Tunicata, Thaliacea). J. Plankton Res., 4(2): 189-201.
Deibel, D. 1982b. Laboratory determined mortality, fecundity and growth rates of Thalia democratica Forskal and Dolioletta gegenbauri Uljanin (Tunicata, Thaliacea). J. Plankton Res., 4(1): 143-153.
Doyle, T.K., H. De Haas, D. Cotton, B. Dorschel, V. Cummins, J.D. Houghton, J. Davenport & G.C. Hays. 2008. Widespread occurrence of the jellyfish Pelagia noctiluca in Irish coastal and shelf waters. J. Plankton Res., 30(8): 963-968.
Esnal, G. & M.C. Daponte. 1999. Salpida. In: D. Boltovskoy (ed.). South Atlantic zooplankton. Backhuys, Leiden, pp. 1423-1444.
Everett, J.D., M.E. Baird & I.M. Suthers. 2011. Three-dimensional structure of a swarm of the salp Thalia democratica within a cold-core eddy off southeast Australia. J. Geophys. Res., 116: C12046.
Faasse, M.A. & K.M. Bayha. 2006. The ctenophore Mnemiopsis leidyi (Agassiz, 1865) in coastal waters of the Netherlands: an unrecognized invasion? Aquat. Invasions, 1(4): 270- 277.
Fagetti, E. 1959. Salpas colectadas frente a las costas central y norte de Chile. Rev. Biol. Mar. Valparaiso, 9(1-3): 201-228.
Foxton, P. 1971. On Ihlea magalhanica (Apstein, 1894) (Tunicata, Salpidae) and lhlea racovitzai (Van Beneden). Discovery Rep., 35: 179-198.
Gonzalez, H.E., M.J. Calderon, L. Castro, A. Clement, L.A. Cuevas, G. Daneri, J.L. Iriarte, L. Lizarraga, R. Martinnez, E. Menschel, N. Silva, C. Carrasco, C. Valenzuela, C.A. Vargas, & C.Molinet. 2010. Primary production and plankton dynamics in the Reloncavi Fjord and the Interior Sea of Chiloe, Northern Patagonia, Chile. Mar. Ecol. Prog. Ser., 402: 13-30.
Goy, J., P. Morand & M. Etienne. 1989. Long-term fluctuations of Pelagia noctiluca (Cnidaria, Scyphomedusa) in the western Mediterranean Sea. Prediction by climatic variables. Deep Sea Res. (I Oceanogr. Res. Pap.), 36(2): 269-279.
Graham, W.M., F. Pages & W.M. Hamner. 2001. A physical context for gelatinous zooplankton aggregations: a review. Hydrobiologia, 451(1): 199212.
Hall, A. & M. Visbeck. 2002. Synchronous variability in the southern hemisphere atmosphere, sea ice, and ocean resulting from the annular mode. J. Climate, 15(21): 3043-3057.
Harbison, G.R. & R.W. Gilmer. 1976. The feeding rates of the pelagic tunicate Pegea confoederata and two other salps. Limnol. Oceanogr., 21(4): 517-528.
Harbison, G.R., V.L. McAlister & R.W. Gilmer. 1986. The response of the salp, Pegea confoederata, to high levels of particulate material: starvation in the midst of plenty. Limnol. Oceanogr., 31(2): 371-382.
Heron, A.C. 1972. Population ecology of a colonizing species: the pelagic tunicate Thalia democratica. Oecologia, 10(4): 269-293.
Heron, A.C. & E.E. Benham. 1985. Life history parameters as indicators of growth rate in three salp populations. J. Plankton Res., 7(3): 365-379.
Ihle, J.E.W. 1958. Salpidae. In: H.G. Bronns (ed.). Klassen und Ordnungen des Tierreichs Akademische Verlagsgesellschaft Geest und Portig K.G., Leipzig, pp. 241-401.
Javidpour, J., U. Sommer & T. Shiganova. 2006. First record of Mnemiopsis leidyi A. Agassiz 1865 in the Baltic Sea. Aquat Invasions, 1(4): 299-302.
Kideys, A.E. 1994. Recent dramatic changes in the Black Sea ecosystem: the reason for the sharp decline in Turkish anchovy fisheries. J. Mar. Syst., 5(2): 171181.
Kideys, A.E. 2002. Fall and rise of the Black Sea ecosystem. Science, 297(5586): 1482-1484.
Lara, C., M. Miranda, V. Montecino & J.L. Iriarte. 2010. Chlorophyll-a MODIS mesoscale variability in the Inner Sea of Chiloe, Patagonia, Chile (41-43[degrees]S): Patches and gradients? Rev. Biol. Mar. Oceanogr., 45(2): 217-225.
Le Borgne, R. & P. Moll. 1986. Growth rates of the salp Thalia democratica in Tikehau atoll (Tuamotuis.). Oceanogr. Trop., 21(1): 23-29.
Lovenduski, N.S. & N. Gruber. 2005. Impact of the southern annular mode on southern ocean circulation and biology. Geophys. Res. Lett., 32: L11603.
Madin, L.P. 1982. Production, composition and sedimentation of salp fecal pellets in oceanic waters. Mar. Biol., 67(1): 39-45.
Madin, L.P. & J.E. Purcell. 1992. Feeding, metabolism, and growth of Cyclosalpa bakeri in the subarctic Pacific. Limnol. Oceanogr., 37(6): 1236-1251.
Marshall, G.J. 2003. Trends in the Southern Annular Mode from observations and reanalyses. J. Climate, 16(24): 4134-4143.
Mianzan, H., J. Quinones, S. Palma, A. Schiariti, E.M. Acha, K.L. Robinson & W.M. Graham. 2014. Chrysaora plocamia: a poorly understood jellyfish from South American waters. In: K.A. Pitt & C.H. Lucas (eds.). Jellyfish Blooms. Springer Netherlands, pp. 219-236.
Michaelsen, W. 1907. Tunikaten. Friedrichsen & Co, Hamburg, 1:1-84.
Molinero, J.C., F. Ibanez, P. Nival, E. Buecher & S. Souissi. 2005. North Atlantic climate and northwestern Mediterranean plankton variability. Limnol. Oceanogr., 50(4): 1213-1220.
Mullin, M.M. 1983. In situ measurement of filtering rates of the salp, Thalia democratica, on phytoplankton and bacteria. J. Plankton Res., 5(2): 279-288.
Pages, F., H.E. Gonzalez, M. Ramon, M. Sobarzo & J.-M. Gili. 2001. Gelatinous zooplankton assemblages associated with water masses in the Humboldt Current System, and potential predatory impact by Bassia bassensis (Siphonophora: Calycophorae). Mar. Ecol. Prog. Ser., 210: 13-24.
Palma, S. & N. Silva. 2004. Distribution of siphonophores, chaetognaths, euphausiids and oceanographic conditions in the fjords and channels of southern Chile. Deep-Sea Res. Part II, 51(6-9): 513-535.
Palma, S., P. Apablaza & N. Silva. 2007. Hydromedusae (Cnidaria) of the Chilean Southern channels (from the Corcovado Gulf to the Pulluche-Chacabuco channels). Sci. Mar., 71(1), 65-74.
Parsons, T.R, R. Maita & C.M. Lalli. 1984. Counting, media and preservatives. A manual of chemical and biological methods for seawater analysis. Pergamon Press, Oxford, UK, 157-164.
Purcell, J.E. 2012. Jellyfish and ctenophore blooms coincide with human proliferations and environmental perturbations. Annu Rev. Mar. Sci., 4(1): 209-235.
Purcell, J.E. & L.P. Madin. 1991. Diel patterns of migration, feeding, and spawning by salps in the subarctic Pacific. Mar. Ecol. Prog. Ser., 73: 211-217.
Purcell, J.E., S.I. Uye & W.T. Lo. 2007. Anthropogenic causes of jellyfish blooms and their direct consequences for humans: a review. Mar. Ecol. Prog. Ser., 350: 153-174.
Richardson, A., A. Bakun, G. Hays & M. Gibbons 2009. The jellyfish joyride: causes, consequences and management responses to a more gelatinous future. Trends Ecol. Evol., 24: 312-334.
Shiganova, T.A., Z.A. Mirzoyan, E.A Studenikina, S.P. Volovik, I. Siokou-Frangou, S. Zervoudaki, E.D. Christou, A.Y. Skirta & H.J. Dumont. 2001. Population development of the invader ctenophore Mnemiopsis leidyi, in the Black Sea and in other seas of the Mediterranean basin. Mar. Biol., 139(3): 431445.
Sievers, H. & N. Silva 2006. Masas de agua y circulacion en los canales y fiordos australes. In: N. Silva & S. Palma (eds.). Avances en el conocimiento oceanografico de las aguas interiores chilenas, Puerto Montt a Cabo de Hornos. Comite Oceanografico NacionalPontificia Universidad Catolica de Valparaiso, Valparaiso, pp. 53-58.
Silva, N., H.A. Sievers & R. Prado. 1995. Caracteristicas oceanograficas y una proposicion de circulacion para algunos canales australes de Chile entre 41[degrees]20'S y 46[degrees]40'S. Rev. Biol. Mar., Valparaiso, 30(2): 207-254.
Silva, N., C. Calvete & H.A. Sievers. 1998. Masas de agua y circulacion general para algunos canales australes entre Puerto Montt y Laguna San Rafael, Chile (Crucero Cimar-Fiordo 1). Cienc. Tecnol. Mar., 21: 17-48.
Sullivan, B.K., D.V. Keuren & M. Clancy 2001. Timing and size of blooms of the ctenophore Mnemiopsis leidyi in relation to temperature in Narragansett Bay, RI. Hydrobiologia, 451(1): 113-120.
Sutherland, K.R., L.P. Madin & R. Stocker. 2010. Filtration of submicrometer particles by pelagic tunicates. Proc. Nat. Acad. Sci., 107(34): 1512915134.
Tello, G.A. & C. Rodriguez-Benito. 2009. Characterization of mesoscale spatio-temporal patterns and variability of remotely sensed Chl-a and SST in the Interior Sea of Chiloe (41.4-43.5[degrees]S). Int. J. Remote Sens., 30(6): 1521-1536.
The Mediterranean Science Commission (CIESM). 2001. Gelatinous zooplankton outbreaks: theory and practice, Naples, 29 August -1st September 2001. CIESM, Monaco, 110 pp.
Utermohl, H. 1958. Zur Vervollkommnung der quantitativen Phytoplankton-Methodik. Mitt. Int. Ver. Theor. Angew. Limnol., 9: 1-39.
Uye, S.I. 2008. Blooms of the giant jellyfish Nemopilema nomurai: a threat to the fisheries sustainability of the East Asian Marginal Seas. Plank. Benth. Res., 3(Suppl.): 125-131.
Ricardo Giesecke (1,2), Alejandro Clement (3), Jose Garces-Vargas (1), Jorge I. Mardones (4) Humberto E. Gonzalez (1,6), Luciano Caputo (1,2) & Leonardo Castro (5,6)
(1) Instituto de Ciencias Marinas y Limnologicas, Facultad de Ciencias, Universidad Austral de Chile P.O. Box 567, Valdivia, Chile
(2) Centro de Estudios en Ecologia y Limnologia Chile, Geolimnos, Carelmapu 1 No 540, Valdivia, Chile
(3) Plancton Andino, P.O. Box 823, Puerto Montt, Chile
(4) Institute for Marine and Antarctic Studies, University of Tasmania Private Bag 55, Hobart, Tasmania 7001, Australia
(5) Departamento de Oceanografia, Universidad de Concepcion, P.O. Box 160-C, Concepcion, Chile
(6) Programa de Financiamiento Basal, COPAS Sur-Austral y Centro COPAS de Oceanografia Universidad de Concepcion, P.O. Box 160-C, Concepcion, Chile
Corresponding author: Ricardo Giesecke (firstname.lastname@example.org)
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|Title Annotation:||articulo en ingles|
|Author:||Giesecke, Ricardo; Clement, Alejandro; Garces-Vargas, Jose; Mardones, Jorge I.; Gonzalez, Humberto E|
|Publication:||Latin American Journal of Aquatic Research|
|Date:||Jul 1, 2014|
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