ARTICLE IN PRESS Deep-Sea Research II 51 (2004) 2389–2411 www.elsevier.com/locate/dsr2 Biological and chemical consequences of the 1997–1998 El Niño in the Chilean coastal upwelling system: a synthesis Rubén Escribanoa,b,, Giovani Daneria,c, Laura Farı́asa,d,e, Vı́ctor A. Gallardoa,c, Humberto E. Gonzáleza,f, Dimitri Gutiérrezg, Carina B. Langea,c, Carmen E. Moralesa,b, Oscar Pizarroa,e,h, Osvaldo Ulloaa,c,e, Mauricio Brauni a Centro de Investigación Oceanográfica en el Pacı´fico Sur-Oriental (FONDAP-COPAS), Universidad de Concepción, Casilla 160-C, Concepción, Chile b Departmento de Oceanografı´a, Estación de Biologı´a Marina, Universidad de Concepción, Casilla 42, Dichato, Concepción, Chile c Centro de Ciencias y Ecologı´a Aplicada (CEA), Universidad del Mar, Campus Valparaı´so, Carmen 446, Placeres, Valparaı´so, Chile d Departamento de Oceanografı´a, Universidad de Concepción, Casilla 160-C, Concepción, Chile e Programa Regional de Oceanografı´a Fı´sica y Clima (PROFC), Casilla 160-C, Concepción, Chile f Instituto de Biologı´a Marina, Universidad Austral de Chile, Casilla 567, Valdivia, Chile g Instituto del Mar del Peru (IMARPE), Apartado 22, Callao, Lima, Peru h Departamento de Fı´sica de la Atmósfera y del Océano, Universidad de Concepción, Casilla 160-C, Concepción, Chile i Instituto de Fomento Pesquero (IFOP), Casilla 8-V, Valparaı´so, Chile Accepted 27 July 2004 Abstract The coastal upwelling ecosystem of the Humboldt Current System off Peru and Chile exhibits strong interannual variability due to changes in the oceanographic conditions related to the El Niño (EN) Southern Oscillation. It is generally believed that major changes occur in the community structure and biological production of this system as a consequence of El Niño-La Niña periods. This paper presents a summary of the information available on the physical, chemical, and biological responses of the Chilean upwelling zone resulting from the strong 1997–1998 EN event. Oceanographic changes for the whole region included the intrusion of oceanic, low-nutrient, warmer, and more oxygenated waters into the coastal areas, with positive sea-surface temperature anomalies lasting until the winter of 1998. Off northern Chile, small-sized phytoplankton prevailed and chlorophyll-a fluctuated widely during most of the EN event, although inshore levels were consistently high. Zooplankton assemblages shifted to smaller species during the warm phase; the total biomass, however, did not change. Primary production rates and the vertical flux of carbon were Corresponding author. Departmento de Oceanografı́a, Center for Oceanographic Research in the eastern South Pacific (FONDAP-COPAS), PO Box 42, Dichato, Concepcion, Chile. Tel.: +56 451 683247; fax: +56 41 683902. E-mail address: rescribano@udec.cl (R. Escribano). 0967-0645/$ - see front matter r 2004 Published by Elsevier Ltd. doi:10.1016/j.dsr2.2004.08.011 ARTICLE IN PRESS 2390 R. Escribano et al. / Deep-Sea Research II 51 (2004) 2389–2411 not greatly affected. The total anchovy catch for 1997 held stable, reaching up to 1 million tons. In 1998, the catch decreased to 400,000 tons before recovering to 1.2 million tons in 1999 and 2000. Off central/southern Chile, the ‘normal’ seasonal regime (spring/summer benthic hypoxia) was replaced by oxygenation near the bottom and lower carbon input as a result of the EN event. Macrofaunal biomass increased significantly in the inshore sediments during the warm phase, then diminished in the following spring/summer period. The decreased macrofaunal biomass was associated with the disappearance of filamentous bacterial mats and increased benthic bioturbation. The overall productive capacity of the Chilean upwelling systems seems to have recovered rapidly after the EN decline, suggesting weaker ecological impacts than those observed in the seasons after the 1972–1973 and 1982–1983 events. r 2004 Published by Elsevier Ltd. 1. Introduction The coastal upwelling zone of the Humboldt Current System (HCS) in the eastern South Pacific (ESP) is well known for its rich biological productivity, as reflected in the large anchovy, sardine (Ryther, 1969; Cushing, 1990), and jack mackerel (Alheit and Bernal, 1993) fisheries in the area. This high production is mostly sustained by the fertilizing effect of wind-driven coastal upwelling, which pumps nutrients into the euphotic zone over the continental shelf (Barber and Smith, 1981). The HCS is, however, subject to strong interannual variability due to the El Niño Southern Oscillation (ENSO). Perhaps because of the catastrophic collapses of the Peruvian fishery after the 1972–1973 El Niño (EN) event, much of the knowledge regarding EN effects in the region comes from the Peruvian ecosystem. Several studies have dealt with the physical variability (Enfield and Allen, 1980; Smith, 1983; Huyer et al., 1987; Enfield, 1989; Fahrbach et al., 1991) and the biological consequences of EN events on the pelagic system (Barber and Chavez, 1983, 1986; Thomas et al., 2001), benthic communities (Arntz et al., 1987; Tarazona et al., 1988; Arntz and Tarazona, 1990), and fisheries (Alamo and Bouchon, 1987; Arntz and Tarazona, 1990). In general terms, this research suggests that upwelling is greatly reduced during warm ENSO phases, causing, in turn, a significant reduction in primary production and a dramatic impoverishment of the entire marine ecosystem (see Artnz and Farhbach, 1996 for a review). In terms of ENSO effects, the upwelling systems off the Chilean coast remain the least-studied parts of the HCS. Studies of the upwelling system off northern Chile (18–301S) show interannual fluctuations in anchovy catches (Blanco et al., 2001) and changes in surface chlorophyll-a (Chl-a) levels associated with the 1996–1998 transition from La Niña to EN conditions (Thomas et al., 2001; Blanco et al., 2002; Carr et al., 2002). Data from regular monitoring of the biological and chemical conditions off Chile’s coast is limited, as is the background information necessary to assess the ecosystem’s response to ENs. Little attention has been paid to ENSO-related biogeochemical changes in the HCS (Guillen, 1987; Wilkerson et al., 1987). Nevertheless, carbon (C) and nitrogen (N) fluxes play a key role in the regulation of oceanic production (Walsh, 1991), as greenhouse gases are actively exchanged with the atmosphere (CO2, N2O) during upwelling and a shallow, intense oxygen minimum zone (OMZ) is found in the water column (Codispoti et al., 1986; Morales et al., 1999) and over the continental shelf (Gallardo et al., 1995). The concurrence of the recent 1997–1998 EN with a number of multidisciplinary studies in different regions along the Chilean coast provided important information on the physical, chemical, and biological responses of the HCS to the EN. This paper consolidates the information available on the main biological and chemical consequences of the 1997–1998 EN in the coastal upwelling systems off Chile. 1.1. Environmental setting and study areas The two main upwelling regions of the Chilean HCS are identified by previous and current research, large-scale fishery zones, and oceanographic and biogeochemical conditions (Fig. 1). The northern region (18–301S) experiences year-round coastal ARTICLE IN PRESS R. Escribano et al. / Deep-Sea Research II 51 (2004) 2389–2411 2391 Fig. 1. The study area in the HCS off Chile, including the two major coastal upwelling regions, northern and central/southern Chile, limited by the subtropical convergence (301S) in the eastern South Pacific. The sources of data used in this synthesis, location of the sampling stations, and type of observations along the Chilean coast are also illustrated. upwelling and moderate winds (5–10 m s
1), with maximum winds coming from the S-SW during spring–summer (Pizarro et al., 1994). Water mass distribution (Robles et al., 1976; Silva and Sievers, 1981) and large-scale circulation patterns have been reviewed by Strub et al. (1998), whereas the seasonal climatology of the oceanographic conditions has been reported by Blanco et al. (2001). Wind-driven coastal upwelling usually promotes the ascent of equatorial subsurface waters so that a persistent OMZ (o 0.5 mL O2 L
1) penetrates the euphotic layer (o50 m depth) close to the coast (Morales et al., 1999). The continental shelf is very narrow or almost non-existent (o20 km wide) and high levels of biomass/productivity are mostly restricted to a very narrow coastal band (Morales et al., 1996a; Daneri et al., 2000). The northern upwelling system sustains a strong pelagic fishery, at times attaining ARTICLE IN PRESS The stations off Arica and Antofagasta (1) are routinely sampled by the IFOP. The Antofagasta (2) station was part of a local study (Ulloa et al., 2001) and the Concepción sampling consisted of an inshore–offshore transect, also as part of a local study by the University of Concepción (Gutiérrez et al., 2000; Sellanes, 2002; Farı́as et al., 2004). Discrete depths: temperature, salinity, Chl-a Discrete depths: temperature, salinity, Chl-a CTDO, fluorescence, zooplankton CTDO, Chl-a, benthic fauna, C and N in sediments 1996–2002 1996–2002 Jun. 1996 –Jan. 1998 Mar. 1997 –Dec. 1998 Monthly Monthly Every 15 days Every 2 months Period Arica (181S) one fixed coastal station Antofagasta (231S) (1) one fixed coastal station Antofagasta (231S) (2) one fixed coastal station Concepcion (361S) 5 stations in a transect This synthesis uses data collected in various locations, manners, and times; Fig. 1 presents a summary of the sampling sites and observations. Time-series data are from serial observations maintained by the Chilean Institute for Fishery Research (IFOP) during the last 5 years at four coastal stations off northern Chile (unpublished data); the information used here comes from two such stations: Arica (181S) and Antofagasta (231S). Monthly observations began in May 1997, and comprise discrete water samples for temperature, salinity, and Chl-a (Table 1) down to 50 m water depth. Temperature was measured with reversed-calibrated thermometers, salinity with an Autolab salinometer, and Chl-a by filtration onto GF/F filters and by fluorometric determination (Parsons et al., 1984). No information on the depth of the photic layer is available to estimate the depth-integrated values, so Chl-a maximum Frequency 2. Observations and measurements Station locations 5–6 million tons per year and accounting for 40% of total annual Chilean fish landings. The central/southern upwelling region (30–401S) is highly seasonal, with intense events during the spring and summer (Cáceres and Arcos, 1991; Strub et al., 1998; Figueroa and Moffat, 2000). The continental shelf (20–60 km), some 30 km wider than in the north, is interrupted by submarine canyons (Fig. 1). Rainfall and river runoff are important in this area and low salinity waters (o33.8) may extend far offshore (430 km) during winter and early spring (Strub et al., 1998; Faúndez et al., 2001). The central/southern OMZ, deeper (450 m) and less intense (40.5 mL O2 L
1) than the northern one, has produced some of the highest primary production rates (10 g C m
2 d
1) ever recorded (Fossing et al., 1995; Daneri et al., 2000). This high primary production is thought to sustain the region’s large fisheries, including jack mackerel landings of 3 million tons between 1990 and 1996 (Arcos et al., 2001). In the shelf sediments, extended periods of suboxia affect the benthic environment, favoring high biomass development in the form of giant bacterium Thioploca mats (Gallardo, 1977; Gallardo et al., 1995). Measurements R. Escribano et al. / Deep-Sea Research II 51 (2004) 2389–2411 Table 1 Summary of time-series measurements at coastal stations off Chile during 1996–2000 2392 ARTICLE IN PRESS R. Escribano et al. / Deep-Sea Research II 51 (2004) 2389–2411 values from each profile were used to estimate monthly anomalies by subtracting the 4-year monthly means. This information was used to analyze the temporal variation of the phytoplankton biomass. In addition, a coastal station near Antofagasta was sampled every 15 days, from July 1996 to January 1998, to obtain CTDO data, fluorescence profiles, and zooplankton samples (details in Escribano and McLaren, 1999) (Table 1). Routine measurements of sea-surface temperature (SST) and sea level were taken from the database of the Hydrographic Service of the Chilean Navy (SHOA), which is made up of data collected over the last 10–20 years from tide gauges in several ports along the Chilean coast. SST is routinely measured with nearshore temperature sensors and loggers (1 m depth) at each port. SST anomalies were calculated by subtracting the mean annual signal from the time series; the mean annual signal was estimated at each site by adjusting four harmonics with periods of 1, 12; 13; and 14 year to a monthly SST time-series stretching from January 1980 to December 2000. Wind-stress anomalies were calculated from satellite data using the same methodology, although, in the case of wind stress, the basal period for estimating the annual signal was January 1992 to December 2002. Information on currents was taken from a mooring station on the continental slope (water depth, 875 m) off Coquimbo (301190 S–711470 W). This is a long-term deployment initiated as part of the Chilean JGOFS program (Shaffer et al., 1999; Hormazabal et al., 2002). The present analysis uses data collected by a current meter at 220 m depth between October 1997 and October 1999. Several CTD (calibrated SeaBird-25 and EG&G MarkIII) casts were made near this mooring station (301210 S–711550 W) in November 1997 (EN condition) and July 1998 (non-EN condition). A second mooring station in the oceanic area off Coquimbo (301S–731W; water depth of 4300 m), provided the time series of the vertical flux of fecal C and its relative contribution to total particulate carbon. The data were obtained from a sediment trap located at 2300 m depth between 1993 and 1998 (see details in González et al., 2004). 2393 Additional information on the water column was taken from two process-oriented cruises conducted off Antofagasta during July 1997 and January 1998 (González et al., 1998, 2000; Daneri et al., 2000; Iriarte et al., 2000). These data include CTDO profiles, primary production rates, zooplankton and phytoplankton biomass and composition, and vertical fluxes of organic carbon (methods described in González et al., 1998). The data for the area off Concepcion (361S) come mainly from benthic studies and bimonthly cruises (1997–1998) carried out along a cross-shelf transect (five stations) from the middle of Concepción Bay to the outer shelf (50 km offshore). These cruises included CTDO (Sea Bird-25) and nutrient profiles, nutrient concentrations, benthic fauna abundance, and the vertical flux of organic matter to the sediments. Methodological details are provided in Gutiérrez et al. (2000) and Farı́as et al. (2002). 3. Results 3.1. SST evolution during the 1997–1998 EN in the HCS The 1997–1998 EN event began developing late in 1996 in the western equatorial region in response to the weakening and reversal of the trade winds (Chavez et al., 2002). NOAA satellite data for the ESP (Fig. 2) showed a positive SST anomaly, or pre-EN conditions, during January 1997. Although the region had almost returned to normal in March 1997, the first Kelvin wave was observed off the Chilean coast in April–May 1997 (Ulloa et al., 2001). After May 1997, warm conditions prevailed and positive SST anomalies (1–3 1C) lasted for up to 14 months, reaching maximum intensity in late 1997 and early 1998. The subtropical area of the ESP had started to cool by March 1998, although positive SST anomalies were observed until the end of 1998. Positive SST anomalies were observed along the Chilean coast during 1997–1998 (Fig. 3). Fiveday average anomalies, taken from the daily SST data collected at different ports (Arica, Antofagasta, Coquimbo, Valparaı́so, and Talcahuano), ARTICLE IN PRESS 2394 R. Escribano et al. / Deep-Sea Research II 51 (2004) 2389–2411 Fig. 2. Monthly means of SST anomalies from satellite information (NOAA satellite data) for the eastern South Pacific region during 1997 and 1998. exhibited fairly synchronous warm and cold periods, revealing the effects of remotely forced ENSO variability acting on local conditions. Off northern Chile (Arica to Coquimbo), there were two positive peaks in SST anomalies (Fig. 3) associated with the passage of two Kelvin waves of equatorial origin (Ulloa et al., 2001). Further south (Valparaiso to Talcahuano), the two-peak pattern of the north was less clear. An abrupt cooling of the nearshore waters occurred all along the coast off Chile between August and September 1998. Upwelling driven by local wind forcing also could cause the fluctuations in the SST measured at each of these ports. Ekman transport data estimated for the region from the ERS 1 and ERS 2 satellites (Fig. 4) show strong seasonal variation between 51 and 401S, moderate intra-seasonal variability south of 251S, and latitudinal variability from the coast off northern Peru to central/ southern Chile. Negative Ekman transport values indicate favorable conditions for offshore advec- tion and coastal upwelling. When superimposed over the seasonal variation, the offshore Ekman transport appears to be greater during 1997. This increase, however, actually took place off Peru. In the Chilean upwelling area (18–401S), the seasonal pattern remained similar to that of both previous and subsequent years. Upwelling favorable winds, therefore, were present even during the EN conditions of the spring and summer season. These observations are consistent with the negative Ekman transport anomalies measured off Peru and Chile (less pronounced) in austral winter 1997. Seasonal and intra-seasonal scale anomalies in the wind field may have resulted from the influence of ENSO-related atmospheric disturbances of equatorial origin (e.g., Hormazabal et al., 2002). In any case, such variation seems to interact strongly with equatorial Kelvin waves, thus greatly moderating the EN’s expression in the ESP, causing variability in upwelling frequency and intensity, in both time and space. ARTICLE IN PRESS R. Escribano et al. / Deep-Sea Research II 51 (2004) 2389–2411 2395 Fig. 3. SST anomalies along the Chilean coast from January 1997 to December 1998. Values are 5 day averages estimated from daily observations provided by the Hydrographic and Oceanographic Service of the Chilean Navy (SHOA). The thicker horizontal lines illustrate the two positive peaks observed off northern Chile. ARTICLE IN PRESS 2396 R. Escribano et al. / Deep-Sea Research II 51 (2004) 2389–2411 Fig. 4. Offshore Ekman transport (left) and its anomaly (right) along the western coast of South America between 5.51 and 41.51S, during 1996–1998. Negative (offshore) values are in blue, contours are every 0.5 m2 s
1 in the left panel and 0.2 m2 s
1 in the right one; the thick line shows the zero contour. Ekman transport was estimated using weekly wind-stress data derived from ERS 1 and 2 satellite observations. Weekly data were low-passed using a five-point triangular filter. 3.2. Physical–chemical consequences The onset of the 1997–1998 EN event was marked by a significant deepening of the thermo- cline at the coastal stations off Arica and Antofagasta (Fig. 5). The 15 1C isotherm descended to below 50 m and two Kelvin waves were observed (May and December 1997). These ARTICLE IN PRESS R. Escribano et al. / Deep-Sea Research II 51 (2004) 2389–2411 2397 Fig. 5. Time series of temperature (1C) at two coastal stations off northern Chile from May 1997 to March 2002, illustrating the warming of the entire water column upon the arrival of two Kelvin waves by May and December 1997. alterations in the vertical thermal structure were the same as those reported in the time series off Antofagasta (Ulloa et al., 2001). A sharp increase in salinity in the upper 50 m was also associated with the Kelvin waves; values which are usually o34.8 in this layer passed 35.0 during this period (Fig. 6). CTD profiles from November 1997 (EN) and October 1998, taken off Coquimbo, indicate that the whole water column (down to 600 m) became warmer (Fig. 7a) and more saline (Fig. 7b) during the EN event. The structure of the water mass changed and the shallow salinity minimum disappeared during the warm period (Fig. 7c). Although seasonal variations in this coastal mooring’s alongshore component of currents at 220 m depth (Fig. 8) are large, alterations in the Peru–Chile Undercurrent flow are not evident. Two maxima in the southward flow do coincide with the May and December 1997 Kelvin waves; however, poleward flow also occurs during these months in other years. The normally shallow nearshore OMZ (o1 mL O2 L
1) deepened with the arrival of the Kelvin waves. The oxygenation of the water column increased at the two coastal stations off northern Chile (Arica and Antofagasta) during the EN event. The O2 concentrations of 44 mL L
1 in the upper 40 m are noteworthy, as under normal conditions, the OMZ is a prominent feature of the 0–50 m layer ARTICLE IN PRESS 2398 R. Escribano et al. / Deep-Sea Research II 51 (2004) 2389–2411 Fig. 6. Time series of salinity at two coastal stations off northern Chile from May 1997 to March 2002, illustrating the increase in salinity in the water column upon the arrival of two Kelvin waves by May and December 1997. (Fig. 9). In the central/southern region (Concepción), the OMZ is usually shallow in coastal waters (50–100 m depth) during normal upwelling conditions. The OMZ deepened during the EN event (May, August, and November 1997) and returned to typical conditions in March and November 1998, with low oxygen (o2 mL L
1) at depths as shallow as 30 m (Fig. 10). The deepening of the OMZ in May 1998 apparently resulted from suppressed upwelling under non-EN conditions. Nutrient information from the 1997–1998 EN is scarce. Nitrate concentrations were measured at three coastal stations off Antofagasta in January 1998. In the nearshore zone (2 km from the coast), nitrate levels were variable but still 45 mM in the upper 50 m layer. However, at the coastal front (18 km from the coast) and the offshore (36 km from the coast) stations, there was very little nitrate in the same layer (Fig. 11). Changes in the nitrate concentrations of the same top layer in the central/southern region (off Concepción) were not obvious in the May 1997 and 1998 data, although the maximum levels at depths below 50 m decreased during the latter period (Fig. 12). The vertical flux of organic C was investigated off Antofagasta, Coquimbo, and Concepción. The vertical flux of particulate organic carbon (POC) off Antofagasta, based on short-term deployments, was lower in July 1997 (EN condition) than in January 1997 (pre-EN condition) ARTICLE IN PRESS R. Escribano et al. / Deep-Sea Research II 51 (2004) 2389–2411 2399 Fig. 7. Vertical profiles of temperature (A) and salinity (B) and the corresponding T-S diagram (C) from CTD data obtained off Coquimbo, near the mooring station (30121.30 S–711550 W), during November 1997 (EN condition; fine line) and July 1998 (thick line). Plots are mean data from seven CTD casts for November 1997 and three casts for July 1998. Fig. 8. Alongshore velocity (cm s
1) at 220 m depth over the slope, at about 15 km from the coast off Coquimbo (301S). Positive values are approximately equatorward. Daily means were estimated from hourly data and then low-passed using a seven-point triangular filter. The long-term mean of the alongshore velocity at this location is about
13 cm s
1. (Table 2), although the possibility that this may have been an expression of the different seasonal conditions of summer (January) and winter (July) cannot be discarded. The time series for the flux of fecal C and its contribution to total particulate carbon from the long-standing sediment trap off Coquimbo (2300 m depth) did not show a notable difference between 1997 and previous years (Fig. 13). Fecal C contributed 30% on average to total C sedimentation, and the seasonal pattern of variability observed during 1993–1996 seemed not to be remarkably different from that of 1997–1998, suggesting that vertical fluxes of organic matter, in terms of fecal C, did not alter during the EN event. However, in the same area, the annual flux of siliceous plankton was markedly lower during EN (1997–1998) compared to non-EN (1993–1994) years (Romero et al., 2001). Meantime, in the coastal zone off Concepción, the vertical fluxes of C and N were found to be significantly reduced in the summer 1998 (EN condition) in comparison with the summer 1999 and 2000, as estimated from the amount of Chl-a and total C and N in the sediments over the continental shelf (Farı́as et al., 2004). ARTICLE IN PRESS 2400 R. Escribano et al. / Deep-Sea Research II 51 (2004) 2389–2411 Fig. 9. Time series of dissolved oxygen (mL L
1) at the coastal stations off Arica and Antofagasta (northern Chile) from May 1997 to March 2002, illustrating the abrupt deepening of the oxycline and retrieval of the OMZ from nearshore waters upon the arrival of two Kelvin waves in May and in December 1997. 3.3. Biological consequences Information on primary production rates is still too limited (Daneri et al., 2000) to allow a precise comparison of EN and non-EN levels in the coastal upwelling regions off Chile (Table 3). The estimates of pre-EN (January 1997) and EN (July 1997) primary production made off Antofagasta do not differ, either for coastal or offshore waters, from estimates made during subsequent years in coastal and oceanic areas off northern and central/ southern Chile (González et al., 1998; Daneri et al., 2000, unpublished data). More information is available on changes in phytoplankton biomass, measured as Chl-a concentration, derived from the time-series studies at the nearshore stations off Arica and Antofagasta during the 1997–2000 period (Fig. 14). Chl-a levels appeared to be reduced in the upper 50 m during 1997 compared to subsequent years. Even though monthly anomalies of Chl-a maximum in the water column remained negative during 1997, variation both in time and between stations was very high. In fact, Ulloa et al. (2001) found no significant differences in Chl-a concentrations between EN and non-EN months in the time series off Antofagasta between June 1996 and January 1998. The analysis of planktonic communities off Antofagasta during cruises undertaken in January and July 1997 revealed that small-sized species, ARTICLE IN PRESS R. Escribano et al. / Deep-Sea Research II 51 (2004) 2389–2411 2401 Fig. 10. Dissolved oxygen (mL L
1) distribution in the water column off central/southern Chile, near Concepción (361S), during 1997 and 1998. Contours are from CTDO profiles at five stations over a cross-shelf transect. The broken line shows the 1 mL L
1 oxyline, representing the behavior of the OMZ (data from Sellanes, 2002). including small diatoms and autotrophic flagellates, dominated the phytoplankton during EN conditions, whereas large diatoms prevailed under normal upwelling conditions (Iriarte et al., 2000). Zooplankton time-series data off Antofagasta also displayed a shift towards small-sized species during EN, although total biomass in the nearshore did not suffer abrupt collapses when compared with the previous year (Ulloa et al., 2001). During normal upwelling, the coastal zooplankton community was commonly dominated by large copepods, such as Eucalanus spp., and euphausiids, mainly the endemic HCS species, Euphausia mucronata (Hidalgo and Escribano, 2001; Fernández et al., 2002). During the warm event, the abundance of small-sized copepods, such as Oithona spp. and Paracalanus parvus, increased and the occurrence of euphausiids and the large Eucalanus spp. decreased (González et al., 2002). Larval stages of euphausiids, however, seemed to increase in abundance during EN months (Fernández et al., 2002). The abundant, medium-sized copepod Calanus chilensis also increased in number in the nearshore during EN conditions, although the female adults were reduced in body size in the warmer waters (Ulloa et al., 2001). Information on the responses of the benthic community to the 1997–1998 EN was obtained from the shelf off Concepción and is described in detail in Gutiérrez et al. (2000). An important consequence of the deepening of the OMZ during EN events is the contact of oxygenated waters with the normally suboxic or anoxic sediments on the shelf, causing changes in bottom communities. Under normal upwelling conditions (and cold La ARTICLE IN PRESS 2402 R. Escribano et al. / Deep-Sea Research II 51 (2004) 2389–2411 Fig. 11. Vertical profiles of nitrate concentration (mM) obtained in the coastal zone off northern Chile, near Mejillones (231S), during January 1998 at three stations located in the nearshore, the coastal front, and offshore (36 km from the coast). Fig. 12. Nitrate concentration (mM) in the water column off central/southern Chile, near Concepción (361S), in May 1997 and May 1998 (data from Sellanes, 2002). Niña phases), a reduced environment dominates the shelf bottom, promoting the growth of large mats of the giant filamentous bacteria Thioploca. During the EN months, the greater oxygenation of the bottom sediments was associated with a sharp decrease in Thioploca biomass. The response of the ARTICLE IN PRESS R. Escribano et al. / Deep-Sea Research II 51 (2004) 2389–2411 macro-benthic assemblages varied according to distance from the shore. Macrofaunal biomass increased in mid-bay sediments and decreased in Table 2 Ranges of vertical flux of POC as estimated from floating sediment traps off Antofagasta (231S) under pre-El Niño conditions (January 1997) and during El Niño (July 1997) Depth (m) Location 2403 shelf sediments during EN. The bioturbation of sediments, however, intensified at all sampling sites during EN, possibly as a consequence of changes in community structure as the relative contribution of different functional groups was altered. Also, the organic matter deposited on the shelf became oxidized and was released from the sediments during the warm event. POC (mg C m
2 d
1) January 1997 July 1997 65 Coastal Offshore 166.8–176.4 125.1–141.6 71.4–164.3 32.3–103.6 300 Coastal Offshore 117.9–119.0 19.8–No data 35.0–40.9 18.3–47.3 Data from González et al. (1998). 4. Discussion A conceptual model of the response of the HCS ecosystem off Chile to the 1997–1998 EN was designed in an attempt to integrate the above information. This particular event was considered to be one of the most intense recorded (McPhaden, Fig. 13. Time series of the vertical flux of fecal carbon (mg C m
2 d
1) and the proportion of fecal carbon over total organic carbon (%), estimated from sediment traps located at 2300 m at the deep-mooring station off Coquimbo (301S), from 1993 to 1998. The shaded area denotes the 1997–1998 EN event. ARTICLE IN PRESS 2404 R. Escribano et al. / Deep-Sea Research II 51 (2004) 2389–2411 Table 3 Water-column integrated estimates (mean7SD) of primary production rates in the Chilean coastal upwelling system during 1997–2000 Period January 1997 pre-El Niño cruise July 1997 El Niño cruise October 1998 spring cruise 2000 summer cruise Location Antofagasta (231S) Antofagasta (231S) Concepción (361S) Iquique (201S) Primary production (g C m
2 d
1) Coastal Offshore 3.1771.81 2.0371.40 4.1372.56 3.3 0.8270.29 1.5671.18 0.32 0.3 Source González et al. (1998) González et al. (1998) Daneri et al. (2000) Single estimate (Unpublished data) Values were all obtained by in situ incubations and integrated over the photic layer (1% of light level). A single measurement was available for Iquique. 1999). The model summarizes the main alterations in the physical and chemical environment and the biological consequences for the pelagic and benthic systems by comparing a cold phase (normal upwelling) with a warm ENSO phase (Fig. 15). The model is largely based on the northern upwelling region. Since satellite data showed positive SST and sea-level anomalies during the 1997–1998 EN event to be greatest between 51 and 151S but extending beyond 401S (Carr et al., 2002), similar, less intense changes are expected for the central/southern region. During a ‘‘normal’’ cold condition (Fig. 15, upper panel), the SSTs in the coastal upwelling area vary between 15 and 18 1C, coastal fronts are well developed (Sobarzo and Figueroa, 2001; Marı́n et al., 2001), and the cold (12 1C), nutrient-rich, equatorial subsurface waters ascend in the nearshore, shoaling the OMZ and creating a low-oxygen environment near the surface waters (Blanco et al., 2001, 2002). These conditions favor higher NO3 inputs into the photic zone. Primary production is expected to be higher and mostly sustained by NO3 (new production). The resulting high biomass values that are associated with reducing conditions in subsurface waters will, in turn, favor higher sedimentation and accumulation rates of organic matter on the shelf (Carr, 2003). Phytoplankton is distributed mainly in the upper 50-m layer, within a shallow photic zone (60 m) (González et al., 1998) and restricted to the nearshore band (Escribano, 1998; Escribano and Hidalgo, 2000; Morales et al., 2001). Similar observations have been made for the zooplankton and small pelagic fish, whose vertical distributions and diel migrations seem restricted by a shallow OMZ (Judkins, 1980; Jarre et al., 1991; Morales et al., 1996b; Escribano and Hidalgo, 2000; Escribano et al., 2000; Rojas et al., 2002). The structure of this highly concentrated pelagic ecosystem is dominated by large species of diatoms, euphausiids, and large-sized copepods (Iriarte et al., 2000; Hidalgo and Escribano, 2001; Ulloa et al., 2001). During the warm ENSO phase (Fig. 15, lower panel), surface waters become warmer (420 1C), coastal fronts weaken or disappear (Blanco et al., 2002), and the photic layer deepens to below 100 m (González et al., 1998). In conjunction with changes in the coastal zone’s water mass composition, the thermocline, oxycline, and OMZ deepen, oxygenating the subsurface waters overlying the shelf and shelf break (Blanco et al., 2002). Upwelling may continue during this phase (Carr et al., 2002), but a deeper nutricline limits the input of new nutrients into the photic zone, favoring regenerated production (Carr, 2003). The limited data available on nutrients off Chile suggest that NO3 is reduced except close inshore. The deepening of the thermocline may occur under conditions of sustained upwelling and may even be increased by Ekman pumping (Halpern, 2002). This deepening may allow a vertical expansion of the photicoxygenated layer and, along with the disappearance of coastal fronts, would result in a higher dispersion—both vertical and horizontal—of plankton and fish (clupeids) (Escribano, 1998; Escribano et al., 2000; Ulloa et al., 2001). The ARTICLE IN PRESS R. Escribano et al. / Deep-Sea Research II 51 (2004) 2389–2411 2405 Fig. 14. Time series of Chl-a concentration (upper panels) and corresponding anomalies (lower panels) in Arica and Antofagasta (northern Chile) from May 1997 to March 2002. Units are in mg Chl-a m
3. Between May 1997 and February 1998, a decrease in Chl-a occurred at both stations, being less pronounced off Antofagasta. Negative monthly anomalies in maximum values of Chl-a prevailed during 1997 at both stations. ARTICLE IN PRESS 2406 R. Escribano et al. / Deep-Sea Research II 51 (2004) 2389–2411 Fig. 15. Conceptual model summarizing the main oceanographic changes and their chemical and biological consequences during the two phases of the ENSO in the Chilean coastal upwelling ecosystem: ‘‘normal’’ upwelling condition (upper panel) and the EN condition (lower panel). The model is mostly based on information derived from the northern region (18–301S), but similar—though less intense—responses are expected for the central/south (30–401S) upwelling region. The 12 1C isotherm represents the average temperature of the ESSW (Equatorial subsurface water) within 100–200 m and thus illustrates the retrieval of the OMZ from the coastal zone under EN conditions. ARTICLE IN PRESS R. Escribano et al. / Deep-Sea Research II 51 (2004) 2389–2411 pelagic ecosystem appears to be dominated by lower trophic levels, including flagellates, small diatoms and copepods, larval stages of euphausiids, and gelatinous species (Fernández et al., 2002; González et al., 2002). During normal or cold events, the denitrification rates within the OMZ and the accumulation of N2O close to the surface waters are expected to intensify (Codispoti et al., 1986; Morales et al., 1999). During active upwelling, a strong initial outgassing of CO2 and N2O, both greenhouse gases, is expected in the areas of an intense and shallow OMZ, probably with a net outsourcing from the ocean albeit the potential increase in new production by the phytoplankton community. During EN, the oxygenation of the water column would result in lower denitrification rates (Morales et al., 1999) and in a reduced supply of organic matter to deeper waters, and also in the release of organic matter from the shelf sediments (Gutiérrez et al., 2000). EN events may favor higher nitrification, potentially contributing NO3 to the photic layer. The expansion of the habitable volume for planktonic communities may allow an increase in the total community aerobic respiration by small organisms (microplankton), thus affecting the production/respiration ratio (Eissler and Quiñones, 1999). The sea to atmosphere exchange of CO2 is likely to be reduced unless upwelling favorable winds remain during the EN event, as was the case off Coquimbo in July 1997 (Torres et al., 2003). Altogether, these changes alter the region’s biogeochemical cycling and the gas exchange between the sea and the atmosphere, a key issue considering the potential loss of biologically available N from the ocean. The nature and magnitude of the alterations however, remain, to be assessed. The oceanographic alterations during the 1997–1998 EN caused a reduction in surface Chla in the ESP region, especially off northern Chile, according to satellite data (Thomas et al., 2001; Blanco et al., 2002; Carr et al., 2002). However, the Chl-a levels, which appear relatively high in the coastal waters, seem reduced offshore (Carr et al., 2002), suggesting that the satellite data resolution (9 km) used in these studies does not provide accurate information for the nearshore band. 2407 Also, surface Chl-a does not adequately reflect the phytoplankton biomass vertically integrated over the euphotic zone, which deepens during EN. The in situ data from the two coastal stations off northern Chile showed lower Chl-a during 1997, although negative maximum Chl-a anomalies also occurred through 2002. Although the maximum Chl-a in the water column was very low (0.1–0.2 mg L
1) at both stations in August 1997, the highest values (2.4 mg L
1) did not coincide in time: Arica peaked in May 1997 and Antofagasta in October 1997. Thus, in addition to cross-shelf variation, timing and latitudinal variability also need to be considered when evaluating EN effects on phytoplankton biomass. Moreover, if the integrated phytoplankton biomass remains unchanged in the water column upon an increase in the depth of the euphotic zone, for example, due to nutrient limitation, lower biomass per unit volume will be found; this could explain the lower surface Chl-a values described by Thomas et al. (2001) during the warm 1997–1998 event. Changes in Chl-a also may be related to the shift to small-sized species in the phytoplankton community structure during EN (Iriarte et al., 2000), a relationship that warrants further study. The observed changes in the species composition of planktonic assemblages during EN may have important consequences for the trophic structure and biogenic fluxes in the coastal waters of the HCS. The shift towards small-sized classes during EN would favor regenerated production and the microbial food web as the dominant pathways of C and N, sustaining the productivity of the coastal areas (Carr, 2003). When small copepods dominate the zooplankton, a smaller contribution to the vertical flux of POC and fecal pellets is expected (González et al., 2000). Abundant small-sized species, like cyclopoid copepods, may substantially reduce the vertical flux of particulates by feeding on phytodetritus and fecal pellets. In contrast, when large copepods and euphausiids are abundant, an intense vertical flux of their fecal material is expected, allowing greater amounts of organic matter to sink faster. Such changes in phytoplankton and zooplankton community structures also can affect the food spectrum available for higher trophic levels. ARTICLE IN PRESS 2408 R. Escribano et al. / Deep-Sea Research II 51 (2004) 2389–2411 The full impact of the 1997–1998 EN on HCS fishery resources is far from clear. The strong fishery of small pelagic anchovy and sardines in northern Chile was not noticeably affected in 1997, as was the Peruvian anchovy industry as a result of the 1982–1983 EN (see Arntz and Fahrbach, 1996 for a review). Our data indicate that food levels, at least in nearshore waters where anchovy normally spawn (Castro et al., 2000), might have been sufficient for larval survival. In fact, winter spawning took place as usual during the 1997–1998 EN and high concentrations of anchovy eggs were collected in the annual IFOP survey (Oliva et al., 1998). This year’s class, however, produced lower landings in 1998 (Oliva et al., 2000). Abnormally high surface temperatures and changes in the larval food spectrum (shift to smaller size classes) probably caused greater egg and larvae mortalities, but insufficient knowledge of the food requirements for clupeid larvae off northern Chile hinders any assessment of the food effect. Acoustic anchovy surveys during EN and normal conditions indicated that the adult population deepened and even tended to remain near the bottom, at depths around 60 m, in coastal waters during the warm event (IFOP, unpublished information). This particular change in behavior during EN also was observed in Peruvian waters (Gutiérrez, 2001). Arcos et al. (2001) analyzed the effects of the 1997–1998 EN on the jack mackerel fishery off central/southern Chile. The oceanographic conditions altered by EN triggered changes in migratory routes and nursery distributions of this species, in turn reducing availability of the resource for the local fishery industry. Anchovy and the common sardine, Strangomera bentincki, are also important resources in this region, and, as suggested for the northern area, a reduction in recruitment was reported for both species, affecting the stock during subsequent years (1998–1999) (Cubillos and Arcos, 2002). In the conceptual scheme presented here (Fig. 15), the strong alterations in the physical–chemical environment and the biological responses during the 1997–1998 EN have been emphasized. However, the apparent weak level of ecological impact, compared to previous events, seems to be an important feature of this EN in the HCS off Chile. Despite the strong variability of the in situ Chl-a presented here, it is likely that primary production in the nearshore was sustained at similar levels during this warm event supporting the production of zooplankton since the total biomass did not suffer major changes (Ulloa et al., 2001). In the California Current System, ecological impacts of this event also were considered to be less extensive. Chavez et al. (2002) suggested that the onset of the event occurred at the time when the Pacific decadal oscillation was shifting from a warm to a cold phase, resulting in weaker ecological effects as compared to the 1982–1983 and 1991–1992 events that took place during a warm phase and produced drastic ecological impacts. It is likely that long-term climate regimes of the Pacific Ocean play an important role in regulating the ecosystem responses to alternating EN–La Niña events. Acknowledgments We are grateful to Drs. A. Thomas, S. Hormazabal, and J.T. Pennington for valuable comments that improved the manuscript. We thank SHOA (Hydrographic Service of the Chilean Navy) for providing SST and sea-level data. 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