JOURNAL OF PLANKTON RESEARCH j VOLUME 27 j NUMBER 6 j PAGES 519–529 j 2005 Ontogenetic vertical distribution and diel migration of the copepod Eucalanus inermis in the oxygen minimum zone off northern Chile (20–21
S) PAMELA HIDALGO1,2*, RUBEN ESCRIBANO2 AND CARMEN E. MORALES2 1 2 PROGRAMA DE POSTGRADO EN OCEANOGRAFIA, UNIVERSIDAD DE CONCEPCION, CONCEPCIÓN, CHILE AND CENTER FOR OCEANOGRAPHIC RESEARCH IN THE EASTERN SOUTH PACIFIC (FONDAP-COPAS), ESTACIÓN DE BIOLOGÍA MARINA-DICHATO, DEPARTAMENTO DE OCEANOGRAFÍA, UNIVERSIDAD DE CONCEPCIÓN, CONCEPCIÓN, CHILE *CORRESPONDING AUTHOR: pahidalg@udec.cl Received February 2, 2005; accepted in principle March 24, 2005; accepted for publication April 19, 2005; published online May 11, 2005 Communicating editor: K.J. Flynn The vertical and ontogenetic distribution, and diel vertical migration (DVM), of Eucalanus inermis in relation to the strong vertical gradient in oxygen concentration associated with an intense oxygen minimum zone (OMZ ) were studied at a coastal area off northern Chile (20–21
S). A close relationship between the abundance of the whole copepod population and low oxygen waters was found, with most developmental stages remaining near the base of the oxycline (30–80 m) and within the upper zone of the OMZ (30–200 m). All stages performed DVM but not at all the stations, mainly between the 30–60 and 60– 200 m strata; a small fraction (<20%) appeared in the surface layer (0–30 m) mostly at night. This strategy of movement would result in a better utilization of food resources since the strong physical and chemical gradients at the base of the oxycline and upper OMZ boundary might serve as a site of particle accumulation. A secondary fluorescence peak was, in fact, found at all the stations, coinciding with minimal dissolved oxygen (DO, <1 mL O2 L1) at the base of the oxycline or in the upper OMZ boundary. The relevance of the biogeochemical flux involved in this diel migration pattern was assessed by calculating the potential active input of carbon and nitrogen from the upper layers into deeper the OMZ. INTRODUCTION The Humboldt Current system (HCS) is well known for its high biological productivity driven by coastal upwelling (Sherman, 1990; Mann and Lazier, 1991). Off northern Chile (18–24
S), the high levels of primary production (Marı́n et al., 1993; Daneri et al., 2000) help to sustain the biomass of the zooplankton community (Heinrich, 1973; Escribano and Hidalgo, 2000a; Hidalgo and Escribano, 2001), which in turn supports the strong fisheries of Chile and Peru. This region is also subject to the presence of an intense oxygen minimum zone (OMZ, <1 mL L1) which influences the vertical distribution of most planktonic forms (Morales et al., 1999). However, little is known about the adaptations or strategies that the zooplankton may have adopted to cope with a persistently low-oxygen layer in this upwelling region. Off northern Chile pelagic copepods are the dominant components of the mesozooplankton (Heinrich, 1973; Escribano and Hidalgo, 2000a). Among them, the large copepod Eucalanus inermis is abundant in shallow waters during most of the year in a coastal area off Antofagasta (23
S) associated with an upwelling center (Hidalgo et al., 2004; Escribano and Hidalgo, 2000b; Hidalgo and Escribano, 2001). Previous studies of this species in the eastern South Pacific indicate that its adult populations are mostly distributed at mid-depth (>50 m) in both oceanic (Longhurst, 1967; Saltzman and Wishner, 1997) and coastal waters (Boyd and Smith, 1982; Flint et al., 1991). However, the vertical distribution of the different developmental stages is unknown. This has limited our understanding of how the population interacts with the OMZ. It is known that the strong vertical gradient in dissolved oxygen (DO) concentration in the water column doi:10.1093/plankt/fbi025, available online at www.plankt.oxfordjournals.org Ó The Author 2005. Published by Oxford University Press. All rights reserved. For Permissions, please email: journals.permissions@oupjournals.org. JOURNAL OF PLANKTON RESEARCH j VOLUME imposes an important constraint for the diel vertical migration (DVM) of zooplankton, such that most species tend to remain in the upper layer (<50 m depth), avoiding the OMZ in the region off Peru (Judkins, 1980; Boyd and Smith, 1982) and northern Chile (Escribano, 1998; Antezana, 2002). Late developmental stages of E. inermis have been found within the OMZ in the HCS (Boyd et al., 1980), but how long they remain in this layer, whether they perform DVM and whether their vertical distribution and DVM depend on their ontogeny, are all questions which need answering in order to define the habitat of this species (in the vertical plane). Furthermore, a better knowledge on the vertical movement and distribution of the whole population is required to evaluate their role in the active vertical transport and cycling of carbon (C) and nitrogen (N) in the region; considering that, due to their large body size, apparent large range of migration and high abundance/biomass, they may influence the biogeochemical fluxes. In order to provide answers to these questions, we analyzed the vertical ontogenetic distribution and DVM of E. inermis in a coastal area off northern Chile (20–21
S) 27 j NUMBER 6 j PAGES 519–529 j 2005 during late summer, when the OMZ is shallower and the oxycline is stronger. The study focused on the association between stage-specific vertical distribution and the vertical gradient of oxygen concentration. In addition, a morphological description of the copepodid developmental stages was summarized to allow their identification and quantification from field samples. The extent to which E. inermis DVM may influence the vertical fluxes of C and N in the HCS region is also explored. METHOD The study was carried out off Iquique (20–21
S) in the coastal zone of the northern region of Chile (Fig. 1) which is subjected to moderate, coastal upwelling throughout the year. The oceanographic information and zooplankton samples were available from the minimum oxygen (MinOx) cruise performed in March 2000 onboard the R/V Vidal Gormáz. This cruise was oriented toward an integrated study of the biogeochemistry of the OMZ, so that the main efforts were focused on the vertical gradient of DO in the upper oxycline. Fig. 1. SeaWiFS image of surface chlorophyll a distribution on March 21, 2000, in the coastal upwelling area off northern Chile, illustrating the position of the stations for the MinOx cruise carried out on the 22–28 March, 2000. 520 P. HIDALGO ETAL. j VERTICAL DISTRIBUTION OF EUCALANUS INERMIS In order to describe the oceanographic conditions at each station, several profiles of temperature, salinity, DO and fluorescence were obtained at different times of the day. For this, a CTD-rosette SeaBird SBE-25, equipped with a SeaBird SBE-43 oxygen sensor and a Wetstar fluorometer, was deployed. The DO concentrations estimated from the calibrated CTD sensor were compared with Winkler measurements, following the procedures described by Knap et al. (Knap et al., 1993). Both measurements yielded similar results and continuous data from the CTD sensor were preferred for generation of the vertical profiles. Zooplankton samples were collected at four stations, MO-3, MO-8, M10 and MO-8b, as indicated in Fig. 1. At each station, the zooplankton was captured by oblique tows with a 1 m2 Tucker Trawl net, within 4 depth strata: 0–30, 30–60, 60–200 and 200–400 m. An additional stratum, 400–600 m, was sampled at station MO8 only. These strata were chosen on the basis of the vertical profiles of DO and temperature, such that the upper 0–30-m layer represented the well-mixed oxic layer (>5 mL O2 L1), the 30–60-m layer included the oxycline in most cases, the 60–200-m layer contained the OMZ, the 200–400 m represented the core of the OMZ and of the associated equatorial subsurface waters (ESSW) (Blanco et al., 2001) and the 400–600-m layer represented the upper portion of the Antarctic intermediate waters (AAIW) which are known to exhibit an increase in DO (Blanco et al., 2001). The zooplankton net (mesh size = 300 mm) was equipped with a calibrated flowmeter to estimate the volume of water sampled. It was assumed that all copepodid stages would be equally sampled with this mesh size given their relatively large size, >1.5 mm in prosome length for stage C1, according to our previous observations. The ontogenetic aspects were analyzed only for copepodid and adult stages. The depth strata were sampled in the day and at night. Station MO-3 was sampled on 22 March (00:00, 11:00), station MO-8b on 25 March (10:45) and 26 March (00:00), station MO-8 on 26 March (14:45) and on 27 March (00:00) and station M10 on 27 March (18:30) and 28 March (00:15). All samples were preserved in 4% neutralized formalin. As relatively little is known about the diagnostic features of the various stages of E. inermis, initial work focused on identifying the features which distinguished each stage. The identification of the different copepodid stages was based on a morphological description of each stage, according to external characters such as body shape and size, setae development, body segmentation, the number and development of appendages, the number and development of swimming legs and the segmentation of appendages, following characters described for Johnson (Johnson, 1937). All observations were made under a dissecting microscope with calibrated micrometry. Copepodids were characterized by having a very elongated and transparent body, a triangular rostrum and two rostral filaments. They were also distinguished by being the largest copepodids found in all the samples. The key characteristics to distinguish the stages C1 through adults are the number of abdominal segments and the number of swimming legs. Adults and stages C4 and C5 have four free-thoracic segments and a fifth one fused to the fourth segment. Sexual dimorphism became evident from stage C4. Males exhibit a rudimentary development of the fifth swimming leg whereas the females show only four pairs of swimming legs and an incipient development of the genital segment. Stages C4, C5 and adults are also distinguished by the number of segments in the urosome. Segmentation of the antennules also increases with development stage. All these characteristics are summarized in Table I. In order to analyze the vertical distribution of copepodids, stage-specific abundances were first estimated as individuals per cubic meter (individuals m3). With these data, depth-weighted averages P (DWA) P per stratum were calculated from DWA = ðxi  zi Þ xi where xi is the abundance of the i stage (individuals m3) and zi is the corresponding mid-depth of the stratum. These DWA values were then related to concentrations of DO and other environmental variables. Also, abundances were integrated for each depth stratum (individuals m2) so as to evaluate the vertical movements of E. inermis. Stratumintegrated abundances were converted to copepod biomasses. Since direct estimates of stage-specific body weights of E. inermis were not available, prosome lengths were used, employing the weight–length regression for a related species, Eucalanus californicus, whose stages have the same size (lengths), morphology and body consistency as E. inermis (Hopcroft et al. 2002). Carbon was assumed to be 40% of dry weight (Harris et al., 2000). RESULTS Oceanographic conditions A high resolution (1  1 km) SeaWiFS image of surface chlorophyll a (Chl a) obtained when the MinOx cruise was in progress outlines the general conditions associated with the sampling stations, in terms of surface phytoplankton biomass as potential food source (Fig. 1). Station MO-3 was located at the southern edge of the surface phytoplankton patch and had a concentration <1 mg Chl a m3. At this station (Fig. 2a), the water 521 JOURNAL OF PLANKTON RESEARCH j VOLUME 27 j NUMBER 6 j PAGES 519–529 j 2005 Table I: Morphological and morphometric characters for the copepodids of Eucalanus inermis occurring off northern Chile Stage of development Antennule segments Segmentation Body length (mm) Number of pairs of swimming legs Thoracic Abdominal C1 8 4 1 1.5–1.7 2 C2 13 5 2 2.0–2.2 3 C3 18 6 3 2.6–3.3 4 C4 female 20 6 3 3.6–4.2 4 C5 male 20 6 3 3.1–3.6 5 C5 female 22 6 3 4.4–4.7 4 C5 male 25 6 4 4.2–4.5 5 Female adult 24 6 3 5.3–6.2 4 Male adult 25 6 5 4.5–5.4 5 Abdominal segmentation excludes the anal segment bearing the caudal rami. Measurements and characters were determined from formalin preserved specimens obtained in this study and following the descriptions of Johnson (Johnson, 1937). DO (mL L–1) Depth (m) 0 0 10 20 30 40 50 60 70 80 90 100 110 120 130 140 150 160 170 180 190 200 210 220 230 240 250 1 2 3 4 5 6 7 Station MO-3 a 10 12 14 16 18 20 22 24 0 0 10 20 30 40 50 60 70 80 90 100 110 120 130 140 150 160 170 180 190 200 210 220 230 240 250 1 2 3 4 5 6 0 7 Station MO-8 Temperature Oxygen Fluorescence b 10 12 14 16 18 20 22 24 0 10 20 30 40 50 60 70 80 90 100 110 120 130 140 150 160 170 180 190 200 210 220 230 240 250 1 2 3 4 5 6 0 7 Station M10 c 10 12 14 16 18 20 22 24 0 10 20 30 40 50 60 70 80 90 100 110 120 130 140 150 160 170 180 190 200 210 220 230 240 250 1 2 3 4 5 6 7 Station MO-8b d 10 12 14 16 18 20 22 24 Temperature (°C) 0.0 0.2 0.4 0.6 0.8 1.0 1.2 0.0 0.2 0.4 0.6 0.8 1.0 1.2 0.0 0.2 0.4 0.6 0.8 1.0 1.2 0.0 0.2 0.4 0.6 0.8 1.0 1.2 Fluorescence (volts) Fig. 2. Vertical profiles of dissolved oxygen (DO), temperature and fluorescence at four stations off northern Chile, during March 2000. a = station MO-3, b = station MO-8, c = station M10 and d = station MO-86. The shaded area illustrates the location of the oxycline and defines the upper boundary (1 mL L1) of the oxygen minimum zone (at the base of the shaded area). 522 P. HIDALGO ETAL. j VERTICAL DISTRIBUTION OF EUCALANUS INERMIS column was stratified, with a difference of >4
C between the surface and 30 m depth, the mixed layer being about 20 m. The well oxygenated layer (>4 mL O2 L1) was present down to 60 m, the oxycline being much deeper (50–80 m) than at the other three stations with the 1 mL L1 oxyisoline located at 70 m. The fluorescence profile revealed a weak primary chlorophyll peak in the upper layer (25–45 m) and a secondary peak below (85 m). This interesting vertical structure of the phytoplankton biomass could not certainly be resolved by the SeaWifs image. Stations MO-8 and MO-8b were located within the area of the surface phytoplankton patch and, though they were very close to each other (Fig. 1), they were sampled at different dates and examined separately. At station MO-8 (Fig. 2b), stratification was stronger than at station MO-3 and the thermocline was shallower (10 m); the mixed layer was <5 m deep. The oxycline was much shallower (10–40 m), with the oxygenated layer at 20 m and the 1 mL L1 oxy-isoline located at 35 m. The chlorophyll fluorescence profiles showed well-defined (20 m) and secondary peaks (60 m). Station M10 was the nearest to shore (Fig. 1) and exhibited similar characteristics to station MO-8 but the oxycline was steeper (15–35 m) and the fluorescence peaks were shallower (primary at 15 m, secondary at 35–45 m; Fig. 2c). Station MO-8b (Fig. 2d) shared similar characteristics with these two stations and a bimodal distribution of the fluorescence peaks (primary between 25 and 35 m, secondary peak at 50 m; the 1 mL L1 oxy-isoline was located at 35 m). At all the sampled stations, the secondary fluorescence peak coincided with minimal DO concentrations (<1 mL L1), either at the base of the oxycline or in the upper zone of the OMZ. Vertical distribution and diel vertical migration The total integrated abundance (copepodids and adults) of E. inermis was highly variable with regard to stations and strata (Table II). In both day and night samples, station MO-3 presented the lowest values (<450 individuals m2) and MO-8 the highest (>1000 individuals m2). Log-transformed day and night abundances of copepodids, separated by stages (n = 7) and stations (n = 4) and integrated over the water column (0–600 m), showed nonsignificant differences (one-way ANOVA F1,54 = 1.75, P > .05) suggesting that the same population was sampled during day and night. With respect to the vertical distribution, most of the peaks in total abundance at each station were observed in the 30–60 (night) and the 60–200 m strata (day). Station MO-8 exhibited a substantial increase in the abundance at nighttime compared with that during the day but this was not so for the other stations. A diel vertical displacement between strata of the copepodids and adults seemed evident from the changes in the maximum abundance values between day and night samples, except at MO-3. In fact, there were significant effects of strata and daytime/nighttime conditions on the vertical distribution of the different stages (two-way ANOVA, F4,168 = 4.0, P < .01). The vertical distribution of E. inermis biomass (Table II) showed a similar pattern to that of the numerical abundance, though the diel changes of the two may not necessarily be similar because of stage-dependent DVM. To illustrate the stage-specific vertical distributions and the DVM behavior, the relative abundance in each stratum (%) with respect to the total integrated abundance in the water column was estimated; results are shown in Fig. 3. In the time, all of the stages were found to be concentrated in the 60–200 m stratum, though the males also appeared in a similarly high percentage in the 30–60 m stratum. All of the stages showed a clear trend of ascent to the stratum above 30–60 m during the night (>50%), remaining within the oxycline and the upper most part of the OMZ. To a lesser degree (15–20%) some reached the shallower waters (0–30 m). Only the adult females (60%) showed a significant upward migration to this surface stratum during the night. To relate the ontogeny of E. inermis to the distribution of the OMZ, the DWA of the abundance for each stage was plotted for day and night samplings (Fig. 4). In this illustration, not only the differences in the depth of day and night populations became more evident, but also the differences between sampling stations. At station MO-3, most of the organisms were concentrated in the 60–200-m layer, both during the day and the night, only stages C1 and C2 becoming deeper at night. At the other stations, however, the organisms were deeper during the day and performed a vertical ascent at night, all of the stages behaving in a similar fashion (i.e. the whole population performed DVM), with only a few exceptions (e.g. at M10, no C1 appeared at night and C5 were found deeper in the water column than during the daylight hours). The diel vertical distribution of DWA of the abundance for all stages showed a pattern associated with the DO concentration in the water column (Fig. 5). At all stations, the different stages were mostly concentrated in low oxygen water. This implies that the whole copepodid population tends to remain under low-oxygen conditions, the DVM being mostly restricted to the layers below the oxycline. DISCUSSION Marine copepods have been studied extensively worldwide. However, investigations of their developmental 523 JOURNAL OF PLANKTON RESEARCH j VOLUME 27 j NUMBER 6 j PAGES j 519–529 2005 Table II: Total integrated abundance and biomass of copepodids and adults of Eucalanus inermis at the different depth strata, from daylight (D) and nighttime (N) samples, obtained at four stations off northern Chile during March 2000 Depth stratum (m) Stations M0-3 D M0-8 N D M10 N D MO-8b N D N Abundance (individuals m2) 0–30 0.0 3.7 5.4 910.5 8.4 54.7 56.5 87.5 30–60 0.0 0.0 194.3 4796.2 157.5 59.4 96.9 266.2 60–200 397.1 44.7 1067.1 375.1 841.1 4.0 678.4 61.1 200–400 47.5 69.1 132.4 411.1 38.9 28.5 62.6 0.7 97.9 82.9 400–600 Biomass (mg C m2) 0–30 0.00 0.03 0.01 8.07 0.25 2.10 0.28 2.15 30–60 0.00 0.00 5.16 38.82 2.32 0.73 0.97 5.54 60–200 4.08 0.75 20.04 3.58 10.46 0.18 14.12 1.03 200–400 1.78 0.23 1.54 3.59 2.72 0.64 0.91 0.00 1.1 2.1 400–600 Biomass was estimated from prosome length measurements and using a weight–length regression described for a related, same-size, species (Eucalanus californicus). stages are scarce even though they represent the growth pattern of the population. In fact, on most occasions, the earlier stages are much more abundant than the later (adult) stages but the younger ones are often overlooked because of the difficulties of identifying them or due to the sampling gear not retaining the smaller sizes. Therefore, morphological descriptions of all the developmental stages are needed and could become a crucial tool for the description of copepod population dynamics. This issue may be even more critical for species like E. inermis, which appears to exhibit sexual dimorphism from the early stages. This observation has been reported in previous work dealing with ontogenetic description of other Eucalanidae species (Johnson, 1937; Bjönberg, 1981; BradfordGrieve et al., 1999) and probably causes difficulties for distinguishing the developmental stages in field samples. Several dominant species of zooplankton and fish larvae in the coastal upwelling area of the HCS have been studied in connection with the OMZ and a close association of some species with low-oxygen waters has been described (Boyd and Smith, 1982; Antezana, 2002; Escribano et al., 2002). E. inermis inhabits the low-oxygen waters of the Peruvian upwelling zone (Boyd and Smith, 1982; Flint et al., 1991) and off northern Chile (this study), in close association with the OMZ. During the present study, the population of E. inermis was generally located in a depth range that would allow rapid migration between the low-oxygen waters below the oxycline and the zone of the oxycline, and, in some cases, up to the high-oxygen surface waters. This behavior could allow them to better utilize the available food resources, which may aggregate at the oxycline (usually coinciding with the thermocline, halocline, and nutricline in this region), or in the upper OMZ boundary; a secondary fluorescence peak was found at all the sampling stations, coinciding with minimal DO concentrations (<1 mL L1), at the base of the oxycline or in the upper OMZ boundary (Fig. 2). Many dominant species of zooplankton in the HCS actively avoid the OMZ and remain in the upper highly oxygenated layer (Morales et al., 1996; Escribano, 1998; Escribano and Hidalgo, 2000a). Others, however, have evolved the capacity to withstand low oxygen waters, either temporarily (through active DVM) or for extended periods, and may use it for their benefit. Entering or remaining in the OMZ could be metabolically advantageous by saving energetic demands, because of a greatly diminished metabolism under low oxygen coinciding with a lower temperature (Svetlichny et al., 2000), and also the OMZ might provide a refuge to avoid predation in the near surface waters (Escribano et al., 2000). Off northern Chile, gelatinous zooplankton may predate copepods (González et al., 2004) and species which perform DVM into the OMZ, such as E. inermis, may be protected from this. The DVM of E. inermis during this study involved interzonal (across clines) or interlayer (between upper 524 P. HIDALGO ETAL. j VERTICAL DISTRIBUTION OF EUCALANUS INERMIS 0 15 C1 45 80 130 160 300 240 500 320 15 MO-3 C2 45 400 0 C2 130 300 80 500 160 C3 45 240 130 Depth (m) Mid-depth of the strata (m) 15 300 500 15 320 MO-8 400 0 C4 45 80 130 160 300 500 240 15 320 C5 45 M1O 400 0 130 300 80 500 15 160 M 45 240 130 300 Daytime Nighttime 320 500 400 15 F 45 C1 C2 MO-8b C3 C4 C5 M F Development stages 130 Daytime Nighttime 300 500 0 20 40 60 80 100 Fig. 4. Mean depth-weighted averages (DWA) of day and night abundances of Eucalanus inermis copepodid stages (C1–C5) and adults (M, males and F, females) in northern Chile during March 2000. Data from the four stations were pooled. Relative abundance (%) Fig. 3. Day and night vertical distribution of Eucalanus inermis copepodids (C1–C5) and adults (M, males and F, females) in northern Chile during March 2000. Data from the four stations were pooled. and lower depth strata) migration between the productive photic layer (including the oxycline and upper boundary of the OMZ in this region) and the deeper parts of the OMZ (>60 m). This downward active transport of matter from the upper layers, if maintained in time through the year, should have an impact on C and N cycling in the region, as found for other migrating copepods and zooplanktonic assemblages in oligotrophic regions (Morales, 1999; Steinberg et al., 2000, 2002). For the purpose of exploring its contribution to C and N fluxes in the water column, the integrated migrant abundances of E. inermis (day and night differences in a given strata), together with estimates of feeding and metabolic rates derived from published allometric data (e.g. Ikeda et al., 2000) were calculated. The data for station MO-8 (Table III), where the highest abundances were observed, were used to estimate a maximum value for the potential transport. Two depth strata were considered in the calculations of migrant biomass, 0–30 and 0–60 m, the first representing the movement between the surface layer and oxycline into the OMZ (active export), and the second representing migration to and from the surface layer and upper OMZ boundary into the deeper parts of the OMZ (>60 m). The calculations show that, at MO-8, the night ascent of E. inermis from depth (>60 m) toward the surface 525 JOURNAL OF PLANKTON RESEARCH j VOLUME 27 j NUMBER Day 0 6 j PAGES 519–529 j 2005 Night 80 160 240 320 400 Depth of accumulation of copepodid and adult stages (m) 480 Station MO-3 Station MO-3 Station MO-8 Station MO-8 0 80 160 240 320 400 480 0 80 160 240 320 400 480 Station M10 Station M10 0 C1 80 C2 C3 C4 C5 M F 160 240 320 400 480 Station MO-8b 0 1 2 3 4 5 Station MO-8b 0 6 1 2 3 4 5 6 Dissolved Oxygen (mL L–1) Fig. 5. Mean depth-weighed averages (DWA) of day and night abundances (depth of accumulation of copepodid and adult stages) of Eucalanus inermis in relation to oxygen concentration of the corresponding DWA at four sampling stations in northern Chile during March 2000. (0–30 m) and subsurface layers (30–60 m) would result in daily biomass transports of 8 and 34 mg C m2, respectively (Table II). The former is mainly due to adult females while all stages contributed to the latter (Figs 3 and 4). This would increase the grazing pressure of the zooplankton on the planktonic communities in the foodrich layers (primary and secondary fluorescence peaks) and, at the same time, contribute to the recycling of 526 P. HIDALGO ETAL. j VERTICAL DISTRIBUTION OF EUCALANUS INERMIS Table III: Estimation of the transport of carbon and nitrogen by Eucalanus inermis into the oxygen minimum zone (OMZ) at station MO-8 in the upwelling zone off northern Chile and comparison with literature data Composition Migrants O2 NH4 C defecation N defecation Total C flux Total N flux (source) (individuals respiration excretion (mg C m2 (mg N m2 (mg C m2 (mg N m2 d1) 1 d 1 f 2 a m ) (mg C m 2 (mg N m day1)b day1)c 2 day ) day ) 1 day ) Eucalanus inermis (this study) 0–30 m 905.1 0.32 0.04 2.29 0.29 2.6 0–60 m 5,555.8 1.83 0.18 12.22 1.53 14.1 1.7 2.0–14.5f 0.6–3.6g Zooplankton 0.3 (various sources) a Calculated as the difference between day and night biomasses in the 0–30- and 0–60-m layers, respectively. Calculated from allometric equations for copepods (Ikeda et al., 2000), using dry weight (DW) and mean temperature in the 60–600-m layer (12
C); carbon conversion using respiratory quotient = 0.8, assuming a largely protein-based diet (Zhang and Dam, 1997; Al-Mutairi and Landry, 2002). c Calculated from allometric equations for copepods (Ikeda et al., 2000), using DW and mean temperature, as in footnote b. d Calculated from ingestion rates (I) based on the fluorescence method, using an allometric equation for gut fluorescence in copepods (Morales et al., 1990) and an evacuation rate value for Eucalanus inermis females (Flint et al., 1991), the latter considering that it does not vary with size (Morales et al., 1990); pigment concentration converted to carbon with a C : Chl a ratio of 60 and a 70% assimilation efficiency was assumed. e Calculated from footnote d, using a C : N ratio of 8 for faecal pellets (Morales, 1986). f From Table II in Steinberg et al. (Steinberg et al., 2000). g From Table IV in Steinberg et al. (Steinberg et al., 2002). b nutrients/substrates in these layers as a result of the metabolic activities of the zooplankton [CO2, NH4, dissolved organic carbon (DOC) and dissolved organic nitrogen (DON) production]. Dagg et al. (Dagg et al., 1980) found that most abundant copepods in the nearby upwelling area off Peru (mostly females of Calanus chilensis, E. inermis and Centropages brachiatus) ingested <5% of the daily primary production. This implies a minimal effect upon the autotrophic carbon flux by these large copepods but since the maximum primary production values in the upwelling area of the HCS are quite high (>1 g C m2 day1) (Daneri et al., 2000), the C channelled by copepods might still be high in absolute terms. Furthermore, at the secondary fluorescence peak, E. inermis could be exerting a greater control on primary production if it is able to consume the smaller particles (i.e. cyanobacteria) associated with this peak (Molina et al., 2005) but this needs to be investigated. Dagg et al. (Dagg et al., 1980) estimated the consumption rates on autotrophs, specifically for E. inermis females, in the range of 0–11 mg C m2 day1 (mean: 4.3 mg C m2 day1, n = 17), comparable with our value (10 mg C m2 day1) indirectly obtained for the same stage, using literature data on the copepod gut fluorescence–size relationship (Morales et al., 1990), E. inermis evacuation rate (Flint et al., 1991) and assuming a 12-h feeding period in the surface layer. The evacuation rate of E. inermis (0.3 h1) is typical of a diel vertical migrant (Morales, 1999; Schnetzer and Steinberg, 2002), i.e much slower than that of a nonmigrant (1–2 h1). Food in the gut could therefore be transported out of the surface and subsurface layers (time residence of 3 h) by the copepods, suggesting that a considerable amount of fresh organic and inorganic matter can be carried into the deeper parts of the OMZ. Estimates of carbon flux to depth by E. inermis at station MO-8 (Table III) were derived from total respiration rate (O2 consumption–respiratory quotient) and defecation rate (C-ingestion–assimilation–C : Chl a ratio). It should be noted that total C-transport by this population might have been underestimated because other C-sources, such as DOC excretion (Steinberg et al., 2000) and mortality at depth (Zhang and Dam, 1997) were not considered. Downward nitrogen flux through E. inermis (Table III) was estimated from total ammonium production and fecal N-production rate. Total N-transport by this species might similarly have been underestimated by not considering other N-sources, e.g. DON, urea and primary amines (Steinberg et al., 2002) as well as mortality at depth (Zhang and Dam, 1997). In both types of flux calculations, stagespecific, individual rates of feeding and metabolism were obtained and added to obtain a total. The total rates were combined with the migrant abundance estimates and, assuming that E. inermis spends half a day in the upper 527 JOURNAL OF PLANKTON RESEARCH j VOLUME layer and the other half at depth, total downward C and N fluxes were obtained. The maximum potential contribution of E. inermis to the fluxes of C and N into the OMZ at station MO-8 would be mainly attributable to defecation at depth (Table III). The total C and N fluxes appear to be significant in comparison with the active flux estimates for other, mostly oligotrophic, open ocean areas (Table III), and for bulk zooplankton, including sometimes micronekton or nekton (Steinberg et al., 2000, 2002). This is the first time that an estimate for a single species, including all its copepodid developmental stages, has been obtained, so that the total flux in this region will certainly be higher. There are other species capable of entering or residing in the OMZ for an extended period among them, other species of Eucalanus and euphausiids, including the very abundant Euphausia mucronata (Judkins, 1980; Escribano et al., 2000). The contribution of E. inermis and other species inhabiting the OMZ to the export of organic and inorganic matter from the upper mixed layer needs further investigation, using finer vertical sampling and direct measurements of biomass, feeding and metabolic rates. An important export of carbon to the OMZ off northern Chile is through the sinking of particulate C from the surface food-rich layer. A few estimates available for the coastal zone and during a similar period to that of the present study range between 125 and 176 mg C m2 day1 at 65 m depth and 20–119 mg C m2 day1 at 300 m depth (González et al., 1998). Thus, the potential transport by E. inermis alone (2.6–14.1 mg C m2 day1) can represent between 1.5 and 11.3% of the sedimentation at 65 m depth and between 2.2 and 70.5% of the sedimentation at 300 m depth. The sedimentation and decomposition of organic matter may greatly contribute to the formation and maintenance of the OMZ in this region (Wyrtki, 1962; Helly and Levin, 2004). The question is whether active transport by E. inermis may provide a more readily available source of nutrients or substrate, and perhaps of a different quality, to the different layers through which they move. On the one hand, by moving into the top 60-m layer, it can provide inorganic N and phosphorus (P) compounds (by excretion), which can be readily used by primary producers (Frangoulis et al., 2004), especially by those in the area of the oxycline and upper OMZ boundary (30–60 m), where the secondary fluorescence peak contains a unique community, mainly of prokaryotes, which contributes to high rates of N cycling (Molina et al., 2005). On the other hand, by moving to the deeper parts of the OMZ, E. inermis may carry organic and inorganic C and N to the deeper OMZ communities, the structure and functioning of which very little is presently known. 27 j NUMBER 6 j PAGES 519–529 j 2005 ACKNOWLEDGEMENTS This work has been supported by the FONDAPCOPAS Center for Oceanographic Research in the eastern South Pacific (CONICYT Project N 150100007). The MinOx cruise was supported by the FONDAPHumboldt Program. We thank C. Krautz for assisting with sampling and the crew of the R/V Vidal Gormáz. 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